SERIES PUBLICATIONS OF THE SMITHSONIAN INSTITUTION

Emphasis upon publication as a means of “diffusing knowledge” was expressed by the first Secretary of the Smithsonian. In his formal plan for the institution, Joseph Henry outlined a program that included the following statement: “It is proposed to publish a series of reports, giving an account of the new discoveries in science, and of the changes made from year to year in all branches of knowledge.” This theme of basic research has been adhered to through the years by thousands of titles issued in series publications under the Smithsonian imprint, commencing with Smithsonian Contributions to Knowledge in 1848 and continuing with the following active series:

Smithsonian Contributions to Anthropology

Smithsonian Contributions to Botany

Smithsonian Contributions to the Earth Sciences

Smithsonian Contributions to the Marine Sciences

Smithsonian Contributions to Paleobiology

Smithsonian Contributions to Zoology

Smithsonian Folklife Studies

Smithsonian Studies in Air and Space

Smithsonian Studies in History and Technology

In these series, the Institution publishes small papers and full-scale monographs that report the research and collections of its various museums and bureaux or of professional colleagues in the world of science and scholarship. The publications are distributed by mailing lists to libraries, universities, and similar institutions throughout the world.

Papers or monographs submitted for series publication are received by the Smithsonian Institution Press, subject to its own review for format and style, only through departments of the various Smithsonian museums or bureaux, where the manuscripts are given substantive review. Press requirements for manuscript and art preparation are outlined on the inside back cover.

I. Michael Heyman

Secretary

Smithsonian Institution

SMITHSONIAN CONTRIBUTIONS TO ZOOLOGY • NUMBER 586

Systematics and Biogeography of Cephalopods

VOLUME I

Nancy A. Voss, Michael Vecchione, Ronald B. Toll, and Michael J. Sweeney

EDITORS

SMITHSONIAN INSTITUTION PRESS

Washington, D.C.

1998

ABSTRACT

Voss, Nancy A., Michael Vecchione, Ronald B. Toll, and Michael J. Sweeney, editors. Systematics and Biogeography of Cephalopods. Smithsonian Contributions to Zoology, number 586, 2 volumes, 599 pages, 257 figures, 69 tables, 1998.—This multiauthored publication is a compendium of the results of the International Workshop on Systematics and Biogeography of Cephalopods. The contributions cover the general systematics and biogeography of the majority of the ecologically, economically, and biomedically important families of cephalopods. The work begins with a series of contributions on the analysis of systematic characters, a necessary activity in the study of the systematics of any group. This is followed by the largest section, consisting of the systematic and biogeographic treatments of seven cephalopod families: Sepiidae, Loliginidae, Enoploteuthidae, Onychoteuthidae, Histioteuthidae, Ommastrephidae, and Octopodidae. These families were chosen for study based on a combination of their relative importance and the need for improved systematic knowledge. The work concludes with a summary of the current classification, type localities, and type repositories of the Recent Cephalopoda. The workshop organizers intend these volumes to serve as a companion to Smithsonian Contributions to Zoology, number 513, 1992.

OFFICIAL PUBLICATION DATE is handstamped in a limited number of initial copies and is recorded in the Institution's annual report, Annals of the Smithsonian Institution. SERIES COVER DESIGN: The coral Montastrea cavernosa (Linnaeus).

Library of Congress Cataloging-in-Publication Data
Systematics and biogeography of cephalopods / Nancy A. Voss…[et al.], editors.
          p. cm.—(Smithsonian contributions to zoology ; no. 586)
   Companion to: Smithsonian contributions to zoology, no. 513, 1992. “This multiauthored publication is a compendium of the results of the International Workshop on Systematics and Biogeography of Cephalopods”—Abstract.
    Includes bibliographical references.

1. Cephalopoda—Classification—Congresses. 2. Cephalopoda—Geographical distribution—Congresses. I. Voss, Nancy A. II. International Workshop on Systematics and Biogeography of Cephalopods. III. Series.

QL1.S54 no. 586
[QL430.2]
590 s—dc21
[594′.5′015] 97-28670

art The paper used in this publication meets the minimum requirements of the American National Standard for Permanence of Paper for Printed Library Materials Z39.48—1984.

Dedication

            These volumes are warmly dedicated to Gilbert L. Voss (1918–1989) and William Adam (1909–1988). The dedication both honors and acknowledges the significant, lasting contributions they made, through research and teaching, to the field of cephalopod systematics and zoogeography. The importance of their work may, in small part, be recognized by the number and quality of references to their publications listed in the contributions to these volumes. Where they have led, we shall follow.

Volume I

Foreword

This publication is a compendium of the results of the International Workshop on Systematics and Biogeography of Cephalopods held in Washington, D.C., on 10–26 July 1988 and conducted under the auspices of the Cephalopod International Advisory Council (CIAC). The statutory goals of CIAC from its inception in 1983 are to (1) stimulate and influence scholarly research on cephalopods from an international perspective, (2) provide information, advice, and assistance on all aspects of cephalopod biology, including those associated with the development and management of cephalopod fisheries resources, and (3) disseminate information on past and current cephalopod research. One major method to achieve the objectives of CIAC is to sponsor international workshops, symposia, and training courses.

Experience from the workshop on “Larval” and Juvenile Cephalopods held in Banyuls-sur-Mer, France, in 1985, where innumerable problems of a systematic nature arose, led the CIAC members to conclude that the next workshop should be on the systematics and biogeography of cephalopods. The paucity of modern, comprehensive familial and generic diagnoses and descriptions, as well as of information on phylogenetic relationships and biogeography, was considered to be a major impediment to progress in many areas of cephalopod research. CIAC designated the families Sepiidae, Loliginidae, Enoploteuthidae, Onychoteuthidae, Histioteuthidae, Ommastrephidae, and Octopodidae as critical families, those most in need of systematic and biogeographic clarification. These families are vitally important in their respective ecosystems, as subjects for biomedical and neurophysiological research, and, some, as target species in world fisheries.

The objectives of the workshop were to (1) summarize, evaluate, and improve our present knowledge of the systematics and biogeography of the selected families of cephalopods; (2) identify problems and gaps in information; (3) determine which of these problems could be solved within the context, opportunities, and constraints of the workshop; (4) summarize the systematic problems that cannot be resolved at the present stage of our knowledge and research; (5) determine the biogeography of taxa in topic families as it relates to present distribution and systematics, rather than as it relates to evolution or theoretical biogeography; and (6) provide direction and stimulation for future systematic work through a published volume of results.

The participants were encouraged to attain the objectives by compiling as much of the following information as possible (but not necessarily limited to these). (1) Unequivocal diagnoses of the family and all its genera, indicating the type genus and type species and designating the best (primary) systematic characters for each taxon. (2) For species-level problems, reviews of all currently recognized species with author, date, reference to original description, precise type locality, deposition and status of the type; annotated information on paratypes, revisions, confirmed geographical distribution and habitat, and species complexes. (3) Discussions of primary systematic characters in all taxa; evaluation of systematic characters within taxa, including evaluation of the systematic potential of nontraditional characters. (4) Comparative analyses of original descriptions, holotypes, paratypes, and other materials to determine valid species and genera; lists of synonyms.

The workshop, under the sponsorship of the Smithsonian Institution, was conducted at The George Washington University Department of Biological Sciences, where laboratories and support space were available. C.F.E. Roper of the Smithsonian Institution was Convener and M.J. Sweeney, Smithsonian Institution, and M. Vecchione, National Marine Fisheries Service, served on the organizing committee. In order to address the systematic objectives of the workshop, approximately 300 types were borrowed from over 30 museums and institutes, and over 3000 additional specimens (either borrowed, brought by participants, or from the Smithsonian Institution's collection at the National Museum of Natural History (NMNH)) were available for study. Resources to support work on these specimens by the leading specialists in the field were provided; these included the complete NMNH specialty library of cephalopod literature, access to computers and copy machines, and the assistance of a collections manager and three student intern/assistants.

The 35 participants in the workshop represented 12 countries: Australia, Brazil, Canada, China, France, Germany, Great Britain, Japan, New Zealand, Spain, the United States, and the former USSR. Additional topics were addressed by seven other scientists from Canada, England, Scotland, and the United States (see “Workshop Participants and Their Current Addresses”).

The workshop schedule was designed to make most efficient use of the participants' expertise in various aspects of cephalopod systematics. The routine consisted of early morning discussions and informal presentations on the systematic status of the seven target families, evaluation of systematic characters, geographic variation, biogeographic principles and practices, and use of phylogenetic and molecular methods in systematic studies of cephalopods. Late mornings and afternoons were devoted to examination and analysis of specimens. Studies concentrated on species identification, character analysis and variation, geographic distribution, and distinguishing species complexes. Evenings were devoted to discussions of special topics and guest lectures about modern trends and techniques in systematics.

Two of the working groups were able to accomplish the major portion of their work at the workshop, but the majority required considerable additional research time, which extended long after the formal conclusion of the workshop.

The results of the workshop studies were to be published in a work that was to be edited by G.L. Voss and N.A. Voss, Rosenstiel School of Marine and Atmospheric Science, University of Miami. Following the untimely death of Professor G.L. Voss in January 1989, N. Voss invited M. Vecchione and R. Toll to join her as coeditors and later invited M. Sweeney to join in recognition of his substantial work in the production of these volumes.

In summary, the CIAC-88 Workshop has resulted in the attainment of significant advances in the systematics and biogeography of cephalopods. This publication will be a beginning point for future studies in these critical families.

Clyde F.E. Roper, Convener

Workshop Participants and Their Current Addresses

(The list is arranged by taxonomic working groups. Within each group, the group leader's name is followed by group participants, who are listed alphabetically.)

FAMILY SEPIIDAE

S.v. Boletzky, Group Leader. Laboratoire Arago, Banyuls-sur-Mer, France

Zh. Dong, Institute of Oceanology, Academia Sinica, Qingdao, People's Republic of China

A. Guerra, Instituto de Investigaciones Marinas, CSIC, Vigo, Spain

D. Khromov, All-Union Research Institute of Marine Fisheries and Oceanography (VNIRO), Moscow, Russia

C.C. Lu, Department of Zoology, National Chung Hsing University, Taichung, Taiwan

FAMILY LOLIGINIDAE

M. Vecchione, Group Leader. Systematics Laboratory, National Marine Fisheries Service, National Oceanographic and Atmospheric Administration (NOAA), Washington, D.C., United States

T. Brakoniecki, Miami, Florida, United States

R. Hanlon, Marine Resources Center, Marine Biological Laboratory, Woods Hole, M, United States

Y. Natsukari, Faculty of Fisheries, Nagasaki University, Nagasaki, Japan

FAMILIES ENOPLOTEUTHIDAE, PYROTEUTHIDAE, AND ANCISTROCHEIRIDAE

R. Young, Group Leader. Department of Oceanography, University of Hawaii, Honolulu, H, United States

L. Burgess, Red Bank, New Jersey, United States

C. Roper, Department of Invertebrate Zoology, National Museum of Natural History, S Institution, Washington, D.C., United States

S. Stephen, Inspection Services Branch, Ottawa, Ontario, Canada

FAMILY ONYCHOTEUTHIDAE

T. Okutani, Group Leader. College of Bioresource Sciences, Nihon University, Fujisawa City, Japan

M. Clarke, Southdown, Millbrook, Torpoint, Cornwall, England, United Kingdom

T. Kubodera, National Science Museum, Tokyo, Japan

U. Piatkowski, Institut für Meereskunde an der Universität Kiel, Kiel, Germany

FAMILY HISTIOTEUTHIDAE

N. Voss, Group Leader. Rosenstiel School of Marine and Atmospheric Science, Universityof Miami, Miami, Florida, United States

K. Nesis, Institute of Oceanology, Russian Academy of Sciences, Moscow, Russia

P. Rodhouse, British Antarctic Survey, Cambridge, England, United Kingdom

FAMILY OMMASTREPHIDAE

J. Wormuth, Group Leader. Department of Oceanography, Texas A&M University, College Station, Texas, United States

M. Dunning, Fisheries Division, Queensland Department of Primary Industries, Brisbane, Queensland, Australia

E. Förch, Foundation for Research and Technology, Wellington, New Zealand

H. Haimovici, Departamento de Oceanografia, Fundação Universidade do Rio Grande, Rio Grande, RS, Brazil

Ch. Nigmatullin, Atlantic Scientific Research Institute of Marine Fisheries and Oceanography (AtlantNIRO), Kaliningrad, Russia

FAMILY OCTOPODIDAE

G. Voss, Group Leader. Rosenstiel School of Marine and Atmospheric Science, University of Miami, Miami, Florida, United States (deceased, 1989)

F. Hochberg, Department of Invertebrate Zoology, Santa Barbara Museum of Natural History, Santa Barbara, California, United States

K. Mangold, Laboratoire Arago, Banyuls-sur-Mer, France

T. Stranks, Department of Invertebrate Zoology, Museum of Victoria, Melbourne, Victoria, Australia

R. Toll, Department of Biology, Wesleyan College, Macon, Georgia, United States

J. Voight, Department of Zoology, Field Museum of Natural History, Chicago, Illinois, United States

Workshop Collections Manager

M. Sweeney, Department of Invertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, D.C., United States

Other Participants

M. Nixon, New Barnet, Hertfordshire, England, United Kingdom

S. Candela, Rosenstiel School of Marine and Atmospheric Science, University of Miami, Miami, Florida, United States

S. Hess, Miami, Florida, United States

G. Kuncio, University of Pennsylvania, Philadelphia, Pennsylvania, United States

J. Messenger, The University, Sheffield, England, United Kingdom

R. O'Dor, Department of Biology, Dalhousie University, Halifax, Nova Scotia, Canada

W. Rathjen, Center for Fisheries Engineering Studies, Florida Institute of Technology, Melbourne, Florida, United States (deceased, 1990)

Acknowledgments

The contributions of a number of people and organizations made it possible to conduct this workshop. To all of them are extended acknowledgment and gratitude for their good efforts on behalf of the advancement and diffusion of knowledge about cephalopods (positions and affiliations are listed as at the time of the workshop): the Cephalopod International Advisory Council (CIAC) officers and members; the Smithsonian Institution, R. McC. Adams, Secretary, and the following Smithsonian units: the National Museum of Natural History, R. Fiske and R. Hoffman, consecutive Directors; the Office of the Assistant Secretary for Science (Research), D. Challinor and R. Hoffman, consecutive Assistant Secretaries; the Office of International Activities, G. Ellsworth, Deputy Director, F. Berkowicz, Assistant Director; the Office of Fellowships and Grants, R. Rubinoff, Director; the Women's Committee of the Smithsonian Associates; the Department of Invertebrate Zoology, R. Cressey, C. Hart, consecutive Chairs; the Naturalist Center, R. Efthim, Program Director; the National Zoological Park, M. Robinson, Director, and its Invertebrate Zoo, J. Horsley, Curator; The George Washington University Department of Biological Sciences, R. Nowlton, Professor, R. Packer, Chairman, and the Offices of Housing and Food Services; student assistants, A. Oliver, E. Keane, and L. Jackintell; activities coordinator, I. Roper.

In acknowledging the efforts of others in support of this publication, one contribution in particular deserves to be highlighted. Clyde Roper was one of the initiators and the principle organizer of the CIAC workshop, but his efforts did not cease when the participants went home from Washington, D.C. Clyde maintained a personal interest in furthering the compilation and publication of this work. He participated in many discussions about the best ways to overcome numerous problems faced by the editors. In addition, he provided the time for the editing done by Mike Sweeney. We are most grateful for Clyde's continued assistance.

All participants also are acknowledged for their cooperation and hard work during the two weeks of record-breaking heat in Washington, D.C. This spirit of cooperation continued well after the workshop and is reflected by the many multiauthored contributions. In addition, many individuals were asked to act as reviewers, which required extensive long-distance communications. The editors extend their heartfelt thanks to all of the reviewers (see list below); they served their roles with distinction, and without them the production of these volumes would have been impossible.

MANUSCRIPT REVIEWERS

F. Bayer, National Museum of Natural History, United States

S.v. Boletzky, Laboratoire Arago, France

E. Boucaud-Camou, Universite de Caen, France

D. Donovan, University College London, England

M. Dunning, Queensland Department of Primary Industries, Australia

F. Hochberg, Santa Barbara Museum of Natural History, United States

D. Khromov, Moscow Ecological Center, Russia

T. Kubodera, National Science Museum, Japan

C.C. Lu, National Chung Hsing University, Taiwan

K. Mangold, Laboratoire Arago, France

R. Mattlin, Ministry of Agriculture and Fisheries, New Zealand

Y. Natsukari, Nagasaki University, Japan

K. Nesis, Shirshov Institute of Oceanology, Russia

T. Okutani, Nihon University, Japan

M. Roeleveld, South African Museum, South Africa

C. Roper, National Museum of Natural History, United States

M. Sweeney, National Museum of Natural History, United States

R. Toll, Wesleyan College, United States

M. Vecchione, National Marine Fisheries Service, United States

J. Voight, Field Museum of Natural History, United States

N. Voss, University of Miami, United States

J. Wormuth, Texas A&M University, United States

R. Young, University of Hawaii, United States

Systematics and Biogeography of Cephalopods

Introduction

Nancy A. Voss, Michael Vecchione, Ronald B. Toll, and Michael J. Sweeney

The contributions that constitute the proceedings of the International Workshop on Systematics and Biogeography of Cephalopods represent the most comprehensive compilation on this subject. They cover the general systematics and biogeography of the majority of the ecologically, economically, and biomedically important families of cephalopods. Such detailed systematics reviews and revisions were long overdue for most family-level taxa treated herein. For the other families, updates of earlier revisions were necessary in order to encompass and disseminate new information based on extensive collections of new material. The biogeographic treatments represent significant milestones in this field of study.

The enormity of the task of major, family-level reviews and revisions was, in part, the reason that these studies had not been done before. The workshop, designed specifically to address the need for modern systematic and biogeographic studies and revisions, gathered together cephalopod biologists from around the world. Organizers facilitated the acquisition of an immense number of type specimens as well as comparative material for examination, and they provided support, incentive, and continued encouragement for the completion of the individual contributions.

The publication of these proceedings has a long and complex history, including the planning and execution of the workshop and the production of the final product. Virtually all contributors recognized the need and devoted the requisite time and energies to do additional work and study at their home institutions following the conclusion of the workshop. The contributors have thereby achieved the goal of providing as much information as realistically possible to projected user groups, such as cephalopod systematists, marine biogeographers, fishery scientists, biomedical researchers, marine ecologists, and evolutionary biologists.

Volume I begins with a series of contributions on the analysis of systematic characters, a necessary activity in the study of the systematics of any group. The volume begins with introductory comments and a general overview of cephalopod characters and includes separate treatments on ontogenetic characters, digestive organs, cephalic cartilages, radulae, teuthoid gladii, and statoliths. Contributions on character analysis, the taxonomic use of the sepiid sepion, and a survey of the seminal receptacles in the Enoploteuthidae are included in the systematics sections dealing with those families. Unfortunately, despite all of the published studies to date on cephalopod character analysis, as well as the information contained herein, vast gaps remain in our knowledge of many of the characters we use every day, not to mention potentially valuable characters of which we know little.

The largest part of the work consists of the systematic and biogeographic treatments of seven cephalopod families: Sepiidae, Loliginidae, Enoploteuthidae, Onychoteuthidae, Histioteuthidae, Ommastrephidae, and Octopodidae. These families were chosen for study based on a combination of their relative importance and the need for improved systematic knowledge. Exhaustive efforts were applied to their study both during the workshop and in the period following it. The focus differs among the families because of differences in the questions most in need of attention in each group.

The systematic contributions on the Sepiidae collectively represent the first broad-based revisionary work since the 1966 monograph of Adam and Rees. In addition to these treatments, papers are included on the distributional patterns of sepiids and the taxonomic use of the sepiid sepion. Appendices to one paper provide a key to genera and species complexes and a list of the nominal type specimens housed in the Natural History Museum, London.

The loliginid section comprises two contributions. The first provides a provisional generic classification of the family, and the second presents a list of the multitude of nominal generic- and species-level taxa that have been introduced into the family.

Three papers constitute the section on the Enoploteuthidae, which concludes Volume I. These include a classification of the Enoploteuthidae (and the two closely related families previously included in the family, Pyroteuthidae and Ancistrocheiridae), a contribution on the phylogenetic relationships of this enoploteuthid group of families, and a survey of the seminal receptacles in the family.

Volume II begins with the family Onychoteuthidae. The families Onychoteuthidae and Histioteuthidae each are represented by single papers that include systematic and biogeographic treatments. The latter paper is a thoroughly expanded revision of Voss's 1969 monograph on the family.

The section on Ommastrephidae includes a total of six contributions arranged by genus. The first five address one or more genera each and the final paper is a biogeographic treatment of arrow squids from the Coral and Tasman seas.

The section on Octopodidae, which begins with an introduction, is divided into separate papers on the taxa described from the western Atlantic, eastern Atlantic and Mediterranean Sea, Indian Ocean and Red Sea, West Pacific, and Australia. The final paper is a world-wide overview of the biogeography of the shallow-water octopods. The octopod section, as a whole, represents the most complete treatment of the family since Robson's 1929 monograph.

Volume II concludes with a summary of the current classification, type localities, and type repositories of the Recent Cephalopoda, including a considerable amount of new data incorporated from the accompanying papers.

A question recently has arisen concerning the correct ending to some family names. The systematic contributions herein retain the traditional family ending of “teuthidae.”

We believe that this publication, a reflection of the hard work and dedication of nearly 40 participants and authors, will be a substantial aid to the study of the organisms to which many persons have dedicated their research energies. As such, it is presented as a working document to be used, expanded, and revised as future needs and knowledge dictate.

Literature Cited

Adam, W., and W.J. Rees

1966.   A Review of the Cephalopod Family Sepiidae. Scientific Reports of the John Murray Expedition 1933–1934, 11(1):1–165.

International Commission on Zoological Nomenclature (ICZN)

1985.   International Code of Zoological Nomenclature. 338 pages. Los Angeles: University of California Press.

Robson, G.C.

1929.   A Monograph of the Recent Cephalopoda Based on the Collections of the British Museum (Natural History), Part I: Octopodinae. 236 pages. London: British Museum (Natural History).

Voss, N.A.

1969.   A Monograph of the Cephalopods of the North Atlantic: The Family Histioteuthidae. Bulletin of Marine Science, 19(4):713–867.

Character Analysis: Introductory Comments

Michael Vecchione

____________

Michael Vecchione, National Marine Fisheries Service, Systematics Laboratory, National Museum of Natural History, Washington, D.C. 20560, United States.

ABSTRACT

Character analysis is the hypothesis-testing core of taxonomy and systematics. Whether used for phenetic comparisons, cladistic analyses, or evolutionary studies, character states are summarized based on assumptions about homology. During the workshop upon which this publication reports, a series of in-depth presentations and discussions were conducted to examine the information content of various suites of characters, mostly anatomical. Detailed reports on some of these characters follow as separate chapters of this publication.

Systematic characters may be used for taxonomy or for classification and phylogenetic analysis. For taxonomy, the science of discovering, describing, naming, and identifying species and groups of species (taxa), character analysis may be difficult in practice, but conceptually it is straightforward. Common characteristics of a group of organisms are sought to distinguish the group consistently from other groups. Although controversy exists about the definition of a species (e.g., Coyne et al., 1988; de Queiroz and Donoghue, 1988; Chandler and Gromko, 1989; Masters and Spencer, 1989; Nixon and Wheeler, 1990), once an investigator adopts a species concept, he or she looks for characters from which to infer the defining properties of that concept, such as reproductive isolation. Use of characters to construct systems of classification (systematics), however, is the subject of considerable controversy.

All methods for analysis of systematics are actually inductive in nature, constructing systems of taxonomic organization by assembling and organizing as much information as possible. The deductive, hypothesis-testing procedures in systematics occur during character analysis (Bryant, 1989). Both inductive and deductive procedures are valid components of scientific investigation, but the deductive nature of character analysis is not always recognized for its critical importance in systematic science. Although descriptions of taxa still include essential “types,” the importance of many components of variability is now widely acknowledged. A species is not composed solely of mature adults; eggs, larvae, and other life stages are equally representative of the species. Therefore, character analysis and the resulting classifications should be based on the entire life cycle, not on any particular stage (traditionally the adult).

In any field of science, the assumptions that apply to the research often are not stated explicitly because they are so well known to the specialists in that field that publishing them in every paper would be needlessly redundant. The assumptions, however, and their implications on inferences drawn from the data should occasionally be examined. Thus, the systematic literature should be examined critically for implied assumptions.

The concept of homology is central to all fields of comparative biology, especially systematics. Character analysis is, among other things, a test of the hypothesis that the characters being compared among taxa are homologous. Nevertheless, an exact and rigorous definition of homology remains elusive (see Bock, 1989; Wagner, 1989; Haszprunar, 1992, for recent reviews). In general, homology in systematics refers to historical, rather than iterative, homology. Historical homology is based on evolutionary conservation of structure even though the feature may have changed in position, form, or function. This assumes that the taxa being compared evolved from a common ancestor that had a genetically similar feature, the similarity reflected in its structure (Bock, 1989). This continuity of structure is actually very difficult to prove, because structures do not reproduce themselves directly. All organisms go through intermediate developmental stages (e.g., the zygote) that lack the morphological characters used in systematics. Although comparative embryology can trace the development of a structure to a particular region of the zygote, what is known about the genetic programming of development does not preclude the possibility that alternative genetic coding could produce similar features molded from the same zygotic clay (Wagner, 1989).

Classification systems are constructed by summarizing the results of character analysis. Several fundamentally different methods exist to construct these summaries. One tool that has become very important in systematic studies is cladistic analysis. The goal of this analytical method is to reconstruct phylogenetic relationships objectively by maximizing the importance of shared derived characters (synapomorphies) within groups of presumably related taxa while minimizing the presumed likelihood of convergences or evolutionary reversals (homoplasies; see Wake, 1991, for a discussion). Steps to accomplish this goal include determination of transformation sequences for multistate characters as well as determination of polarity (distinguishing primitive from derived) for character states (Mickevich, 1982). In other words, the researcher must have some idea of historical relationships among alternative phenotypes to determine whether the various configurations of a taxonomic character are ancestral (also termed conservative characters or plesiomorphies) or derived (adaptive characters or apomorphies). Three methods exist for determining polarity: (1) direct examination of ancestral condition in the fossil record (Bandel and Boletzky, 1988; Donoghue et al., 1989); (2) outgroup comparisons with “sister taxa” that are presumed to be closely related to the taxon under investigation (Kluge, 1985); and (3) examination of ontogenetic sequences (Nelson, 1985). Of these methods, the first is generally unsatisfactory for dibranchiate cephalopods because the fossil record of these animals is depauperate (Donovan, 1977). Therefore, to determine character polarity for most Recent cephalopods a researcher must either choose sister taxa for outgroup comparison or examine ontogeny (or both, see Voss and Voss, 1983). Either strategy is subject to its own suite of advantages and disadvantages, and it is not within the scope of this paper to enter the debate between outgroup selection and use of ontogenetic characters (e.g., Kluge and Strauss, 1985; Nelson, 1985; Mabee, 1989). Apomorphies may be shared among taxa being investigated (synapomorphies) or may be found only in a single taxon (autapomorphies). The only characters considered in cladistic analysis to contain information on phylogenetic relationships are synapomorphies.

Character analysis also is crucial in the other two primary methods of constructing systematic classifications, phenetic analysis and evolutionary classifications. The mathematically rigorous form of phenetic analysis, known as numerical taxonomy, uses repetitive numerical methods, such as ordination or numerical classification (cluster analysis), to form groups, or clusters, of whatever is being considered based on overall similarity of measured characteristics (e.g., Wormuth, 1976); the same methods are used in diverse disciplines ranging from community ecology and physical oceanography to economics and psychology. In numerical taxonomy, these clusters generally are formed based on similarity of unweighted phenotypic characters without regard to homology or evolutionary convergence. Numerical taxonomy does not depend on subjective decisions about outgroups, homoplasies, or character-state polarity, or their implicit assumptions. What results is simply a phenogram of similarity that does not attempt to convey evolutionary history or relatedness among taxa.

Evolutionary classification dates back to Darwin's attempts to construct a detailed history of the evolution of a group. This method uses all available information, including ontogeny, ecology and adaptation, historical biogeography, and rates of genetic divergence, to name just a few of the diverse potential sources. Particular attention is directed to homology and convergence, and, unlike cladistic analysis, this method stresses shared ancestral characters (symplesiomorphies) in addition to synapomorphies. The multidimensional branching through time described by this method is supposed to represent the genealogy of the taxa investigated, and from this genealogy an evolutionary classification can be formed (e.g., Donovan, 1977). This method of phylogenetic reconstruction has been widely criticized for subjectivity because it lacks the computational rigor of either numerical taxonomy or cladistic analysis, although computational methods are progressing (e.g., Carpenter et al., 1995). Its emphasis on homology, though, makes ontogenetic analysis an important component of evolutionary classification; observation of development of similar structures from the same germ tissues and by similar developmental pathways in the embryos is the strongest argument for homology.

In recent years, there has been heated debate about the relative virtues of these methods. I think that it would be better to view them as a sequence. Determination of phenetic similarity is a necessary first step prior to detailed analysis of characters to test hypotheses about homology, relative plesiomorphy and apomorphy, and homoplasy for cladistic analysis. When evolutionary rates can be added to a well-supported cladogram, the result is a phylogenetic classification with maximum information content.

Rigorous character analysis involves determination of (1) the characters to be used, (2) the alternative conditions or character states, (3) transformational steps among the character states, and (4) polarity or evolutionary sequence of these transformations. Assumptions are required for each step, and not all of these steps can be performed for all characters.

Selection of characters for analysis is part of the overall problem of character weighting. In other words, how much relative importance should be assigned to various characters (Neff, 1986) in systematic studies? This, in turn, implies questions about evolutionary processes. For example, are changes in reproductive characters more important to the evolution of a species than changes in characters associated with locomotion or feeding? The simple solution of not assigning weights (usually based on the argument that weighting is arbitrary and subjective) is actually a form of character weighting because it requires the assumption (usually not stated explicitly) that all characters have the same evolutionary and systematic importance. As stated above, selection of characters also is a form of weighting because it implies that the characters not selected have no importance.

Vecchione (1994) defined five categories of characters for cephalopods and gave examples of each. These categories form a continuum that is actually circular in nature. (1) Gross-morphological characters are the traditional systematic characters, based on overall, primarily external, appearance. (2) Anatomical characters refer to the structure of internal organs. (3) Histological characters are features of microscopic anatomy. (4) Biochemical characters include analyses of allozymes and nucleic acids (both DNA and various forms of RNA) as well as other biochemical characteristics, such as euryhalinity. (5) Behavioral characters provide information based on live animals. For more information, see the literature reviewed by Vecchione (1994). Many characters, particularly in the morphological and behavioral categories, actually are composed of complex suites of components, each of which could be considered in detailed character analysis to be separate characters.

The Cephalopod International Advisory Council organizers of this International Workshop on Systematics and Zoogeography of Cephalopods recognized the importance of broad comparative analysis of taxonomic and systematic characters by devoting a series of afternoon and evening sessions to character analysis. Participants were asked to make summary presentations and to lead discussions on suites of characters. The emphasis was on anatomical systems and included the following:

Presentor/Moderator | Topic
S.v. Boletzky | eggs
T.F. Brakonecki | hectocotylus
S. Candella | beaks
M.R. Clarke | statoliths
R.T. Hanlon | behavior
S.C. Hess | spermatophores
F.G. Hochberg | skin structures
K. Mangold | digestive system
J.B. Messenger | central nervous system
M. Nixon | introduction to cephalopod characters
M. Nixon | cephalic cartilage
M. Nixon | radulae
T. Okutani | funnel-locking apparatus
R.B. Toll | gladius
R.B. Toll | morphometric analysis
G.L. Voss | optic tract
G.L. Voss | fin supports
N.A. and G.L. Voss | funnel organ
M. Vecchione | paralarval ontogeny

Additional presentations on sucker rings and hooks, photophores/photosensitive vesicles, and cuttlebones had been planned but were not presented. Although a number of the topics that were presented have been published elsewhere in journals or dissertations, I am pleased that seven topics are reviewed in the chapters that follow. I hope this will inspire others to pursue similar comparative studies across a broad range of taxa.

Literature Cited

Bandle, K., and S.v. Boletzky

1988.   Features of Development and Functional Morphology Required in the Reconstruction of Early Coleoid Cephalopods. In T. Wiedmann and T. Kullmann, editors, Cephalopods—Present and Past, pages 229–246. Stuttgart: Schweizerbartische Verlagbuchhandlung.

Bock, W.J.

1989.   The Homology Concept: Its Philosophical Foundation and Practical Methodology. Zoologische Beitraäge, new series, 32:327–353.

Bryant, H.N.

1989.   An Evaluation of Cladistic and Character Analyses as Hypothetico-deductive Procedures, and the Consequences for Character Weighting. Systematic Zoology, 38:214–227.

Carpenter, K.E., B.B. Collette, and J.L. Russo

1995.   Unstable and Stable Classifications of Scombroid Fishes. Bulletin of Marine Science, 56:379–405.

Chandler, C.R., and M.H. Gromko

1989.   On the Relationship Between Species Concepts and Speciation Processes. Systematic Zoology, 38:116–125.

Coyne, J.A., H.A. Orr, and D.J. Futuyma

1988.   Do We Need a New Species Concept? Systematic Zoology, 37:190–200.

de Queiroz, K., and M.J. Donoghue

1988.   Phylogenetic Systematics and the Species Problem. Cladistics, 4:317–338.

Donoghue, M.J., J.A. Doyle, J. Gauthier, A.G. Kluge, and T. Rowe

1989.   The Importance of Fossils in Phylogeny Reconstruction. Annual Review of Ecology and Systematics, 20:431–460.

Donovan, D.T.

1977.   Evolution of the Dibranchiate Cephalopoda. Symposia of the Zoological Society of London, 38:15–48.

Haszprunnar, G.

1992.   The Types of Homology and Their Significance for Evolutionary Biology and Phylogenetics. Journal of Evolutionary Biology, 5:13–24.

Kluge, A.G.

1985.   Ontogeny and Phylogenetic Systematics. Cladistics. 1:13–27.

Kluge, A.G., and R.E. Strauss

1985.   Ontogeny and Systematics. Annual Review of Ecology and Systematics, 16:247–268.

Mabee, P.M.

1989.   An Empirical Rejection of the Ontogenetic Polarity Criterion. Cladistics, 5:409–416.

Masters, J.C., and H.G. Spencer

1989.   Why We Need a New Genetic Species Concept. Systematic Zoology, 38:270–279.

Mickevich, M.F.

1982.   Transformation Series Analysis. Systematic Zoology, 31:461–478.

Neff, N.A.

1986.   A Rational Basis for a priori Character Weighting. Systematic Zoology, 35:110–123.

Nelson, G.

1985.   Outgroups and Ontogeny. Cladistics, 1:29–45.

Nixon, K.C., and Q.D. Wheeler

1990.   An Amplification of the Phylogenetic Species Concept. Cladistics, 6:211–223.

Vecchione, M.

1994.   Systematics and the Lifestyle and Performance of Cephalopods. Marine Behavior and Physiology, 25:179–191.

Voss, N.A., and R.S. Voss

1983.   Phylogenetic Relationships in the Cephalopod Family Cranchiidae (Oegopsida). Malacologia, 23:397–426.

Wagner, G.P.

1989.   The Biological Homology Concept. Annual Review of Ecology and Systematics, 20:51–69.

Wake, D.B.

1991.   Homoplasy: The Result of Natural Selection, or Evidence of Design Limitations? American Naturalist, 138:543–567.

Wormuth, J.

1976.   The Biogeography and Numerical Taxonomy of the Oegopsid Squid Family Ommastrephidae in the Pacific Ocean. Bulletin of the Scripps Institution of Oceanography, 23:1–90.

Overview of Cephalopod Characters

Marion Nixon

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Marion Nixon, Norfolk Road, New Barnet, Herts EN5 5LT, United Kingdom.

ABSTRACT

A brief overview of the types of characters used for cephalopod systematics is presented. In addition to soft tissues there are hard tissues composed of chitin-protein complexes, calcified structures, cartilage-like structures, and other tough tissues for which the chemical composition is not yet known, such as teuthoid hooks. Aside from morphology, other taxonomic characters, such as behavior and biochemistry, have been little explored in cephalopods.

During the nineteenth and early twentieth centuries the number of species of Cephalopoda described increased quite quickly, especially following the return of scientific expeditions (see Voss, 1977). The descriptions were mostly of morphological features, internal and external, and some included measurements. Dimensions of the whole animal and of its anatomical structures often lacked precise definition of the points between which the measurements were taken. Robson (1929) recognized this omission and defined such sites, after which descriptions were more rigorous and detailed (see for example Pickford, 1949; Thore, 1949; Adam, 1952). Standards were again raised with the careful definitions of meristic characters listed by Voss (1963), and twenty years later those were modified and expanded by Roper and Voss (1983), who also provided detailed guidelines for describing, or redescribing, a species.

In the past three decades, a marked change has taken place in the degree of scrutiny to which a morphological feature is subjected. One example is the beak, on which, after finding huge numbers in the stomachs of large predators, studies were initiated to determine whether they possessed features of taxonomic value for identification. Beaks were first utilized in this way by Beteshava and Akimushkin (1955). Shortly afterwards, Clarke (1962a:560) commented that beaks “are notoriously difficult to identify when found isolated,” but he has since elegantly demonstrated the presence of characters that do permit identification to the level of genus, and even to species (Clarke, 1962b, 1980, 1986; Clarke and Maddock, 1988). Another example is the gladius. The careful analyses by Toll (1982, 1988) revealed that the gladius can be used to separate closely related taxa, such as those that may be encountered in a predator's stomach (Hess and Toll, 1981).

These anatomical structures are two of a small number present in these soft-bodied mollusks that are composed wholly, or partly, of tough or hard tissues. The beak and gladius both consist of chitin-protein complexes (Hunt and Nixon, 1981; Hunt and Huckerby, 1987). Other tissues formed of chitin-protein complexes include the radulae and also the sucker discs of octopods (Hunt and Nixon, 1981). Crystallin protein is present in the lens of the eye (Tomarev and Zinovieva, 1988). Cartilage encases the central nervous system of many cephalopods (see Nixon, 1998) and is the supporting tissue in the mantle- and nuchal-locking apparatus. Hard tissues are present in some of the various forms of dermal armature (Lu, 1977; Roper and Lu, 1990), whereas cartilage is present in the tubercles of cranchiid squids (Dilly and Nixon, 1976). The hooks of teuthoids are of tough tissue that, like the beaks, can survive digestive processes and fossilization. The chemical composition is not known, but in one hook, from an Ancistrocheirus, traces of metal elements were found (Engeser and Clarke, 1988). Calcified tissue is found in the shell of Nautilus, Spirula, and Argonauta, the cuttlebone of Sepia (see Gregoire, 1972; Watabe, 1988), and the statoliths (Clarke, 1978) and the rhyncholite and concholite of the beak of Nautilus (Lowenstam et al., 1984). Hard tissue provides support for the gills and this too survives fossilization (Reitner and Mehl, 1989), but its composition has not been analyzed. Structures of complex form with sites for muscle attachment, and/or orifices for the passage of nerves and blood vessels, are most likely to possess structural features and ornamentation of value for descriptive purposes. These hard- or tough-tissue structures are better able to withstand adverse conditions, such as that experienced during capture, and they survive largely without distortion or loss of material, even after immersion in the digestive juices of a predator (see for example Clarke, 1980; Hess and Toll, 1981), postmortem changes, and even fossilization (see Saunders and Richardson, 1979; Lehmann, 1981; Clarke and Trueman, 1988). Several of these anatomical structures are discussed in this volume (statolith, radula, cephalic cartilage), but others remain to be examined.

Other taxonomic characters, besides morphological ones, have been little explored in cephalopods. Many of the coastal species, at least, exhibit a wide range of color, body patterns, and behavior (Packard, 1963; Packard and Hochberg, 1977; Moynihan and Rodaniche, 1982; Hanlon and Messenger, 1988). Hanlon (1988) investigated the behavior and body patterns of shallow water octopods of the Caribbean Sea and gave guidelines for the collection and analysis of data of ecological and ethological importance. Roper and Hochberg (1988) observed the cephalopods living around a small island, both in situ and in aquaria, and found that both ecological and ethological characters were of use for the identification of living animals. The value of such studies was amply demonstrated by the discovery (Roper and Hochberg, 1988) of an entirely unsuspected mode of locomotion that, if unique, could form a taxonomic character. Such a type of movement could not have been predicted from morphological studies of preserved material.

Biochemical characters have received less attention. The application of protein electrophoresis and isoelectric focusing to cephalopod tissues now allows genetic comparison. This has already proved valuable in determining differences, or similarities, between nominal species and apparently geographically separated populations (Ally and Keck, 1978; Christofferson et al., 1978; Smith et al., 1981; Levy et al., 1988). A study of two nominal species of Loligo combined morphological measurements, meristic counts, and genetic evidence to determine their status (Augustyn and Grant, 1988). Genetic variation in the genus Nautilus was examined by Woodruff et al. (1987) and was examined in the family Loliginidae by Kuncio and Hanlon (1991). Protein polymorphisms reflect the structure of the genes and should record molecular phylogeny more clearly than phenotypic characters; thus, such studies should in time be of great value in taxonomy.

In the future, an ideal description of a cephalopod will include morphological, meristic, ecological, ethological, and biochemical characters. Such a detailed description of a single species will inevitably generate a wealth of data. Thus, perhaps this is an appropriate time for consideration of the best methods to describe and measure the various characters and for consideration of the presentation, storage, retrieval, and distribution of this information, as well as developments for handling taxonomic descriptions using computers (see Alkin and Bisby, 1984).

Literature Cited

Adam, W.

1952.   Céphalopodes. Résultats Scientifiques, Expédition Océanographique Belge dans les Eaux Cotiéres Africaines de l'Atlantique Sud (1948–1949), 3:1–142.

Alkin, R., and F.A. Bisby, editors

1984.   Databases in Systematics. The Systematics Association Special Volume, 26: 329 pages.

Ally, J.R.R., and S.A. Keck

1978.   A Biochemical-Genetic Population Structure Study of Market Squid, Loligo opalescens, along the California Coast. Fishery Bulletin, California, 169:113–122.

Augustyn, C.J., and W.S. Grant

1988.   Biochemical and Morphological Systematics of Loligo vulgaris vulgaris Lamarck and Loligo vulgaris reynaudii D'Orbigny nov. comb. (Cephalopoda: Myopsida). Malacologia, 29:215–233.

Beteshava, E.I., and I.I. Akimushkin

1955.   [Food of the Sperm Whale (Physeter catodon) in the Kurile Islands Region.] Trudy Instituta Okeanologii, 18:86–94. [In Russian.]

Christofferson, J.P., A. Foss, W.E. Lambert, and B. Welge

1978.   An Electrophoretic Study of Select Proteins from the Market Squid, Loligo opalescens Berry. Fishery Bulletin, California, 169: 123–134.

Clarke, M.R.

1962a. Significance of Cephalopod Beaks. Nature, 193:560–561.

1962b. The Identification of Cephalopod “Beaks” and the Relationship between Beak Size and Total Body Weight. Bulletin of the British Museum (Natural History), Zoology, 8:449–480.

1978.   The Cephalopod Statolith—An Introduction to Its Form. Journal of the Marine Biological Association of the United Kingdom, 58: 701–712.

1980.   Cephalopoda in the Diet of Sperm Whales of the Southern Hemisphere and Their Bearing on Sperm Whale Biology. Discovery Reports, 37:1–324.

Clarke, M.R., editor

1986.   A Handbook for the Identification of Cephalopod Beaks. 273 pages. Oxford: Clarendon Press.

Clarke, M.R., and L. Maddock

1988.   Beaks of Living Coleoid Cephalopoda. In M.R. Clarke and E.R. Trueman, editors, The Mollusca, 12: Paleontology and Neontology of Cephalopods, pages 123–131. San Diego: Academic Press.

Clarke, M.R., and E.R. Trueman, editors

1988.   The Mollusca, 12: Paleontology and Neontology of Cephalopods. 355 pages. San Diego: Academic Press.

Dilly, P.N., and M. Nixon

1976.   The Dermal Tubercles of Cranchia scabra (Mollusca, Cephalopoda): Surface Structure and Development. Journal of Zoology, London, 179:291–295.

Engeser, T.S., and M.R. Clarke

1988.   Cephalopod Hooks, Both Recent and Fossil. In M.R. Clarke and E.R. Trueman, editors, The Mollusca, 12: Paleontology and Neontology of Cephalopods, pages 133–151. San Diego: Academic Press.

Gregoire, C.

1972.   Structure of the Molluscan Shell. In M. Florkin and B.T. Scheer, editors, Chemical Zoology. 7: Mollusca, pages 45–102. New York: Academic Press.

Hanlon, R.T.

1988.   Behavioral and Body Patterning Characters Useful in Taxonomy and Field Identification of Cephalopods. Malacologia, 29:247–264.

Hanlon, R.T., and J.B. Messenger

1988.   Adaptive Coloration in Young Cuttlefish (Sepia officinalis): The Morphology and Development of Body Patterns and Their Relation to Behavior. Philosophical Transactions of the Royal Society of London, series B, 320:437–487.

Hess, S.C., and R.B. Toll

1981.   Methodology for Specific Diagnosis of Cephalopod Remains in the Stomach Contents of Predators with Reference to the Broadbill Swordfish, Xiphias gladius. Journal of Shellfish Research. 1: 161–170.

Hunt, S., and T.N. Huckberby

1987.   A Comparative Study of Molluscan and Crustacean Chitin Proteoglycans by Carbon-I 3 NRM Spectroscopy, Identification of Carbohydrate and Amino-Acid Contributions and the Determination of Amino-Acid Shifts in Anhydrous Formic Acid. Comparative Biochemistry and Physiology, 88B: 1107–1116.

Hunt, S., and M. Nixon

1981.   A Comparative Study of Protein Composition in the Chitin-Protein Complexes of the Beak, Pen, Sucker Disc, Radula and Oesophageal Cuticle of Cephalopoda. Comparative Biochemistry and Physiology, 68B:535–546.

Kuncio, G.S., and R.T. Hanlon

1991.   Analysis of Cephalopod Evolution and Systematics Using Ribosomal RNA Sequence Data. [Abstract.] Bulletin of Marine Science, 49:665.

Lehmann, U.

1981.   The Ammonites: Their Life and Their World. 246 pages. Cambridge: Cambridge University Press.

Levy, J.A., M. Haimovici, and M. Conceicao

1988.   Genetic Evidence for Two Species to the Genus Eledone (Cephalopoda: Octopodidae) in South Brazil. Comparative Biochemistry and Physiology, 90B:275–277.

Lowenstam, H.A., W. Traub, and S. Weiner

1984.   Nautilus Hard Parts: A Study of the Mineral and Organic Constituents. Paleobiology, 10:268–279.

Lu, C.C.

1977.   A New Species of Squid, Chiroteuthis acanthoderma, from the South West Pacific (Cephalopoda, Chiroteuthidae). Steenstrupia. 4:179–188.

Moynihan and Rodaniche

1982.   The Behavior and Natural History of the Caribbean Reef Squid Sepioteuthis sepioidea, with a Consideration of Social, Signal and Defensive Patterns for Difficult and Dangerous Environments. Advances in Ethology, 25:1–151.

Nixon, M.

1998.   Cephalic Cartilage of Cephalopoda. In N.A. Voss, M. Vecchione, R.B. Toll, and M. Sweeney, editors, Systematics and Biogeography of Cephalopods. Smithsonian Contributions to Zoology, 586(1): 31–38.

Packard, A.

1963.   The Behavior of Octopus vulgaris. Bulletin de l'Institut Océanographique de Monaco, special number, 1D:35–49.

Packard, A., and F.G. Hochberg

1977.   Skin Patterning on Octopus and Other Genera. Symposia of the Zoological Society of London, 38:191–231.

Pickford, G.

1949.   Vampyroteuthis infernalis Chun, an Archaic Dibranchiate Cephalopod, II: External Anatomy. Dana Report, 32:1–132.

Reitner, J., and J. Mehl

1989.   Ein besonders Fossil. Paläontologische Zeitschrift, 63:3–4.

Robson, G.C.

1929.   A Monograph of Recent Cephalopoda, Part I: Octopodinae. 236 pages. London: British Museum (Natural History).

Roper, C.F.E., and F.G. Hochberg

1988.   Behavior and Systematics of Cephalopods from Lizard Island, Australia, Based on Color and Body Patterns. Malacologia, 29:153–193.

Roper, C.F.E., and C.C. Lu

1990.   Comparative Morphology and Function of Dermal Structures in Oceanic Squids (Cephalopoda). Smithsonian Contributions to Zoology, 493: 40 pages.

Roper, C.F.E., and G.L. Voss

1983.   Guidelines for Taxonomic Descriptions of Cephalopod Species. Memoirs of the National Museum of Victoria, 44:49–63.

Saunders, W.B., and E.S. Richardson

1979.   Middle Pennsylvanian (Desmoinesean) Cephalopoda of the Mason Creek Fauna, Northeastern Illinois. In H. Nitecki, editor, Mason Creek Fossils, pages 333–359. New York: Academic Press.

Smith, P.J., P.E. Roberts, and R.J. Hurst

1981.   Evidence for Two Species of Arrow Squid in the New Zealand Fishery. New Zealand Journal of Marine and Freshwater Research, 15:247–253.

Thore, S.

1949.   Investigations of the “Dana” Octopoda, Part I: Bolitaenidae, Amphitretidae, Vitreledonellidae and Alloposidae. Dana Report, 33:1–85.

Toll, R.B.

1982.   The Comparative Morphology of the Gladius in the Order Teuthoidea (Mollusca: Cephalopoda) in Relation to Systematics and Phylogeny. 390 pages. Doctoral dissertation, University of Miami, Coral Gables, Florida.

1988.   Functional Morphology and Adaptive Patterns in the Teuthoid Gladius. In E.R. Trueman and M.R. Clarke, editors, The Mollusca, 11: Form and Function, pages 167–182. San Diego: Academic Press.

Tomarev S.I., and R.D. Zinovieva

1988.   Squid Major Lens Polypeptides are Homologous to Glutathione S-transferases Subunits. Nature, 336:86–88.

Voss, G.L.

1963.   Cephalopods of the Philippine Islands. Bulletin of the United States National Museum, 234:1–180.

1977.   Present Status and New Trends in Cephalopod Systematics. Symposia of the Zoological Society of London, 38:49–60.

Watabe, N.

1988.   Shell Structure. In E.R. Trueman and M.R. Clarke, editors, The Mollusca, 11: Form and Function, pages 69–104. San Diego: Academic Press.

Woodruff, D.S., M.P. Carpenter, W.B. Saunders, and P.D. Ward

1987.   Genetic Variation and Phylogeny in Nautilus. In W.B. Saunders and N.H. Landman, editors, Nautilus: The Biology and Paleobiology of a Living Fossil, pages 65–83. New York: Plenum.

Ontogenetic Characters and Cephalopod Systematics

Michael Vecchione

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Michael Vecchione, National Marine Fisheries Service, Systematics Laboratory, National Museum of Natural History, Washington, D.C. 20560, United States.

ABSTRACT

Ontogenetic characters include any somatic feature for which the relative timing (measured by age) of changes in size and/or shape provides information on the systematic relationships among groups of organisms. These characters can be used for determination or identification of species or for inferring relationships among species, either directly, based on distribution of the characters among taxa, or indirectly, by providing information on relative primativeness of alternative character states. Although the embryology of a few species is well known, morphological development of species in most families is not, especially for the paralarvae. Numerous examples of paralarval characters are provided here to illustrate the potential that comparative studies of ontogeny have for resolving systematic problems.

What Is an Ontogenetic Character?

Anyone who has taken an introductory course in biology has probably been exposed to Haeckel's “Biogenetic Law” about ontogeny recapitulating phylogeny. Somewhat less well known is the controversy that has enveloped the conceptual relationship between ontogeny and phylogeny. Gould (1977) has compiled a very thorough review of the history of this concept, from its classical Greek beginnings, through von Baer, Agassiz, and Haeckel, and the subsequent disrepute of the concept, to its present status within the “modern synthesis” of genetics, historical evolution, and experimental embryology. Gould argued convincingly for renewing the importance of ontogeny in assessing systematic relationships. In particular, he proposed that changes in the timing of developmental events, termed heterochrony, are among the most important driving forces of evolution. Gould's book stimulated a great amount of interest and a revitilization of research into relationships between individual development and the history of life, as demonstrated by recent symposia (e.g., Atkinson, 1992) and controversy (Strathmann, 1993).

Gould (1977) summarized earlier embryological work by de Beer (1930) to show that heterochrony can be categorized as either (1) accelerated or (2) retarded development of either (a) somatic features or (b) reproductive organs, thus forming four independent categories. If one assumes that evolution occurs by addition or deletion of characteristics only at the end of a developmental sequence (see discussion of this assumption below under “Problems with Ontogenetic Characters”), then these four categories can converge on just two types of morphological results. Accelerated development of somatic features results in recapitulation of ancestral characteristics in an ontogenetic sequence, the basis of Haeckel's “law.” Recapitulation, however, also can result from retarded development of reproductive organs, termed hypermorphosis. Conversely, accelerated development of the reproductive organs results in paedomorphosis by truncation, also known as paedogenesis or progenesis. Paedomorphosis by retardation results from retarded development of somatic features; this category is referred to as neoteny.

In a sense, all morphological characters can be considered to be ontogenetic because they have a progression of development from undifferentiated precursors (de Queiroz, 1985). Intermediate steps or phases in developmental sequences can be of use for a variety of goals in systematics. They can be used for identification of early life-history stages or to delineate new species. They also can be used to infer relationships among taxa based on shared developmental characters. An important use of developmental sequences has been to determine homology and polarity (relative apomorphy or plesiomorphy) of character states for cladistic analysis (see Vecchione, 1998, for discussion of these terms).

The Use of Ontogenetic Characters

Most research on the systematic importance of ontogenetic characters involves the development of somatic features. Gould (1977) proposed a model for comparisons of heterochrony among species. This model includes three independent scales for measurement of systematic characters: size, shape, and age. The age at which reproductive maturity is attained forms a standard milestone within the age scale. Within this model, therefore, comparisons of heterochrony involve the allometric changes in size and shape of a character with respect to the age of the organism.

Allometric growth is the general term for change in relative size and shape of various features during overall growth with age (Sweet, 1980). Changes in shape with growth, or differences in shape among taxa, can be decomposed into multiple size components (Kluge and Strauss, 1985). Formal graphic, mathematical, and statistical methods have been proposed for the analysis of allometry (Alberch et al., 1979). Analyses of ontogenetic characters, however, rarely consider the multidimensional aspects of growth (Strauss, 1987) but rather treat character states, including intermediates, as distinct entities, with essentially instantaneous transitions among states during development (e.g., Mabee, 1989a).

In recent years, and particularly since the publication of Gould's book, ontogenetic characters have been prominent in many systematic studies. Many examples could be given of the importance of ontogeny in recent systematic studies, but I will mention only a few representative works to illustrate the variety of problems to which ontogenetic studies are being applied.

The American Society of Ichthyologists and Herpetologists published a massive tome on ontogeny and the systematics of fishes (Moser et al., 1984). This book, the result of a workshop that brought together most of the world's leading fish systematists and students of larval fishes, summarized and, in some cases, synthesized divergent hypotheses that had resulted from independent studies of the larvae and the adults in many families of fishes. For the decapod crustacea, Rice (1980) published a comprehensive review of the morphology of crab zoeae and proposed a new classification of the Brachyura based on larval characters. Van Dover et al. (1982) analyzed 340 published descriptions of anomuran and brachyuran larval development and showed that the maxillary scaphognathites could be grouped into eight “types” and five developmental sequences that they concluded were of systematic importance. At a higher systematic level, Jones and Gardiner (1988) presented developmental evidence of the relationships of the newly established phylum Vestimentifera with other phyla. Nielsen (1985) proposed a new phylogeny of the Metazoa based on the developmental characteristics summarized in his trochaea theory. A controversial new theory on the mechanisms of evolution, based on peculiarities in larval development, was presented by Williamson (1992).

Problems with Ontogenetic Characters

Often, character states are viewed as typological phenomena, without regard to variability. The relative amount of phenotypic variation within a species changes during the life cycle of the animals considered (Atchley, 1984). For many species, phenotypic variance increases rapidly after birth or hatching, attaining maximum variance early in ontogeny, and decreases to minimum variance (aside from sexual variation) in adults. Thus for cephalopods, maximum phenotypic variation theoretically could be expected to occur in paralarvae. When variability is examined for cephalopod paralarvae, it is sometimes inadequately assessed. This is especially true for laboratory studies. Hatching and rearing paralarvae in the laboratory is necessary to be sure of parental taxonomy but results in very limited genetic stock. Although thousands of paralarvae may be obtained for some species this way, assessing variance among many specimens that all came from the same parents, or even from a limited spawning area, is an example of pseudoreplication (Hurlburt, 1984) if the results are extrapolated to the species as a whole. Pseudoreplication will not answer the real questions of variation within and among taxa.

The use of ontogenetic characters to determine character-state polarity implies a very important assumption: that novel configurations of a character develop only at the terminus of the ontogenetic sequence. This assumption of terminal addition or deletion is central to Gould's (1977) model of development; however, it has been questioned by several systematists, and Mabee (1989b) empirically rejected the assumption of terminal addition, and therefore ontogenetic determination of polarity, for centrarchid fishes. Cohen and Massey (1983) have proposed that alternative controls of development exist at different phases in ontogeny, specifically larval compared with adult. This seems intuitively to be reasonable; for example, a crab zoea is subjected to different selection pressures than is a megalopa or an adult, and, optimally, adaptation would occur at any of those phases of the ontogenetic sequence. It remains to be seen whether nonterminal change in character states within ontogenetic sequences is a general phenomenon in evolution, but firm rejection of the assumption in one case weakens its use in other studies.

Simply obtaining developmental series for comparative analyses of ontogenetic characters is quite difficult. The eggs and embryos are unknown for most cephalopod species. Comparatively few species can presently be reared in the laboratory. Almost all of those that can be reared belong to three neritic families: Sepiidae, Loliginidae, and Octopodidae. Therefore, the primary source of ontogenetic information for diverse cephalopod species is paralarvae collected in the field.

In assembling a series of paralarvae from field collections to describe the development of a species, several assumptions must be fulfilled. First, the series must be taken from a relatively limited geographical area. What are currently considered to be widespread species (e.g., Onychoteuthis banksii (Leach), Octopus vulgaris Cuvier) may actually comprise unrecognized complexes of several species with limited distributions; a geographically disjunct collection of paralarvae from such a “species” could confuse developmental changes with interspecific variability or geographical variability within a species. Indeed, collection of paralarvae with variable morphology may offer evidence for unrecognized taxa (e.g., Young and Harman, 1987; Loffler and Vecchione, 1993). Second, the cephalopod fauna of an area must be known well enough so that each species within a genus can be distinguished in that area, even if the species from that area have not yet been described formally or compared with similar species from other geographical areas. If the number of species of a genus in an area is not known with reasonable confidence, then a series may confuse interspecific differences with developmental changes. For example, off the southeast coast of the United States, some authors believe the genus Illex to comprise several species, whereas others consider this to be an example of intraspecific variability. A collection of paralarval Illex from this area may therefore include just one species or may include several species (Vecchione, 1979). Third, the series must progress backward in size from a juvenile stage that can be identified unambiguously to species, again even if the species has not yet been described. In the Illex example above, if the multiple-species hypothesis is correct, only mature adult males can be identified confidently at this time, and a developmental series could still be confused. Fourth, the series must include several sizes of paralarvae, enough so that transitions among different states of appropriate characters can be inferred. Descriptions of one or a few paralarvae may be helpful for identifying future specimens but are not adequate for systematic comparisons of developmental heterochrony.

Because of their size, paralarvae deteriorate more rapidly in preservative than do adult specimens, and it is not always possible to obtain paralarvae of all species throughout the geographic range of whatever taxonomic group is being systematically reviewed. Furthermore, voucher specimens of paralarvae generally are not deposited in archival museums; this problem is discussed by Smith (1989) for fish larvae. Therefore, analysis of characters presented in published descriptions is an option to be considered. Many published descriptions, however, violate one or more of the assumptions presented above. Thus, caution must be exercised in analysis of characters based on literature review. Some examples of descriptions of developmental series that generally fulfill these assumptions are presented in Table 1.

Comparisons among taxa somehow must be standardized by age or size. Determination of size and age, especially the latter, involves some serious problems. The standard measure of cephalopod size is dorsal mantle length (ML), but this may not be an adequate parameter for comparisons among some taxa. In octopods, which lack either gladius or cuttlebone, ML is quite variable. In some cephalopod species ML comprises almost the total length of the animal, whereas in others ML is a relatively small percentage of total length. Comparisons cannot be based on total length because the arms and tentacles can be extended and retracted, and the head can be pulled into the mantle. Weight is sometimes used as a measure of size, but because of water retained in the mantle cavity, weight also is quite variable. For paralarvae and small juveniles, methods of obtaining a reasonably accurate weight are unacceptably destructive. Furthermore, weights and lengths, both of entire animals and of organs used as systematic characters, are known to be affected by preservatives, but quantitative studies of preservative effects are few for adult cephalopods and are nonexistent for paralarvae.

TABLE 1.—Developmental series of cephalopods from field studies that fulfill most of the assumptions discussed in the text.

Species | Study
Spirula spirula | Clarke, 1970
Lolliguncula brevis | Vecchione, 1982
Abraliopsis felis | Okutani and McGowan, 1969
Onychoteuthis borealijaponica | Okutani and McGowan, 1969
Gonatus madokai | Kubodera and Okutani, 1977
Gonatus middendorffi | Kubodera and Okutani, 1981
Illex argentinus | Vidal, 1994
Illex illecebrosus | Vecchione, 1979
Todarodes pacificus | Hamabe, 1961; Okutani, 1966
Thysanoteuthis rhombus | Issel, 1920
Bathyteuthis abyssicola | Roper, 1969
Chtenopteryx sicula | Naef, 1923
Teuthowenia megalops | Dilly and Nixon, 1976; Voss, 1985
Vampyroteuthis infernalis | Pickford, 1949

Age is important for Gould's (1977) model of heterochrony and is a reasonable parameter for developmental comparisons. Methods for age determination in field-collected specimens, however, are only now being developed and have been objectively verified for very few species. Even in laboratory situations, where age can be determined, it is not clear how comparisons should be made between species with large eggs and those with small eggs. Should age be measured from the time the eggs are laid or from hatching? The two procedures would result in different interpretations (for example, see discussion of chromatophores, below). Several systems of assigning embryos to stages have been proposed, and these permit comparisons among taxa. The only clear example of paralarval stages is in the family Ommastrephidae, in which separation of the tentacles is a distinct developmental event. Concise definition of other such events, analagous to preflexion, flexion, and postflexion stages of fish larvae (Kendall et al., 1984), would be very useful for studying paralarval development in cephalopods.

Ontogenetic Characters in Cephalopod Systematics

The history of the use of ontogenetic characters in cephalopod systematics is, to a certain extent, a small-scale mirror of the history of the ontogeny/phylogeny concept presented by Gould (1977). Little was known of cephalopod development prior to the late 19th century. Following Haeckel's lead, cephalopod systematists in the late 19th and early 20th centuries, such as Chun (1910) and Pfeffer (1912), examined the early stages of cephalopods for information relating to the systematics of the class. Indeed, Naef (1923), who used cephalopods as his primary model, was one of the pioneers of ontogenetic systematics. During the period from about the late 1930s through the 1960s, however, the theories of Haeckel and von Baer first were widely criticized and later were largely ignored. This trend was compounded in cephalopod systematics by the increasing realization of the difficulties with the taxonomy of paralarvae collected in plankton studies and by a complete lack of knowledge on the embryology of all but a few species.

During the 1960s and 1970s the study of experimental embryology gained importance. Information again accumulated indicating that embryological development contained clues to evolution and systematics. Most cephalopod species are difficult or impossible to culture with present laboratory methods. Some neritic species, however, especially those with relatively large eggs, can be reared and thus are potential targets for embryological investigations. Throughout the 1970s and 1980s, Arnold, Boletzky, Fioroni, Marthy, and others (see references in Boletzky, 1989) conducted important studies of the embryology of cephalopod species that could be maintained in the laboratory; these studies provided information from which systematic inferences could be drawn.

Paralarval morphology and taxonomy was a barren field from Naef's time, the years around and following World War I, until the late 1960s, when Okutani began his work (see review by Okutani, 1987). This is because of the continuing difficulties of collecting and studying planktonic cephalopods (Vecchione, 1987). In the late 1970s and early 1980s, however, renewed interest developed in paralarval taxonomy (e.g., Nesis, 1979; Roper and Lu, 1979; Vecchione, 1979, 1981, 1982; McConnathy et al., 1980; Voss and Voss, 1983). This interest culminated in a workshop convened in 1985 by the Cephalopod International Advisory Council in Banyuls-sur-Mer, France, to study paralarval cephalopods. The manual produced as a result of this workshop (Sweeney et al., 1992) is a very important tool for anyone interested in cephalopod paralarvae. This manual, together with improved methods for collecting zooplankton (Roe and Shale, 1979; Wiebe et al., 1985) and rearing cephalopods (Boletzky and Hanlon, 1983; Young et al., 1985), should provide the impetus for rapid progress in the study of paralarval morphology and taxonomy. Whereas the focus of the handbook is the identification of young cephalopods, I propose that paralarval characters also should be used to assess relationships among species and higher-level taxa.

I provide below some examples of ontogenetic characters that may be of importance in cephalopod systematics (also see Table 2). Of course, the timing of development of any adult systematic character could be important within the concept of heterochrony. Many other characters undoubtedly will prove to be equally useful, but because of the paucity of studies on paralarval development little information is available. My purpose herein is to highlight the potential of ontogeny as a tool for investigating the problems of cephalopod systematics.

The premier example of congruence between paralarval ontogeny and numerous adult characters is found in the family Ommastrephidae. All ommastrephids, and only ommastrephids, develop through a paralarval form so distinctive that it originally was assigned the generic name Rhynchoteuthis Chun (later emended to Rhynchoteuthion). In rhynchoteuthion paralarvae, the tentacles are fused into a single appendage, with suckers confined to the distal end. Furthermore, the two ventral pairs of arms do not develop until after hatching. Thus, a hatchling ommastrephid, nominally a decapod, has but five circumoral appendages, two pairs of arms and a fused pair of tentacles.

As in some other phyla, the early posthatching stages of some oegopsid cephalopod species differ so markedly from the adults that they were initially described as new genera. In addition to the rhynchoteuthion stage of ommastrephids, other examples include the doratopsis stage of chiroteuthids, the pyrgopsis stage of the cranchiid genus Leachia, the asthenoteuthion stage of Lycoteuthis, and probably other poorly known “genera” such as Cirrobrachium in Thysanoteuthidae.

Heterochrony in the sequence of arm development was noted by Naef (1921, 1923) as an important distinction among teuthoid squids. Paralarvae of the family Loliginidae can easily be distinguished from other planktonic squids because the ventral arms develop more rapidly than the dorsal arms. The opposite pattern holds true among the many oegopsid families, in which development of the ventral arms is retarded compared with the dorsal arms and tentacles. The ventral arms also develop more robustly than the dorsal arms in the sepioids, except for Idiosepius, whereas no clear pattern is apparent in the timing of arm development among most paralarval octopods. One morphotype of octopod paralarva, however, originally described as the genus Macrotritopus, is distinctive in the precocious development of the third pair of arms. The macrotritopus stage is currently thought to belong to a single species of the diverse genus Octopus. It seems likely that the distinctive developmental pattern is representative of generic separation and that more than one species develops through a macrotritopus stage.

Hatchlings of Onychoteuthis appear to have three pairs of arms, but actually the appendages comprise the two dorsal pairs of arms and the tentacles. Later, as arm pairs III and IV develop (in the system of designation used for squids; within the context of embryological development of cephalopods in general these would be arm pairs III and V (Boletzky, 1989)), the tentacles elongate and tentacular suckers are confined to a distal club. Thus, at least in this genus, early development of the tentacles is practically indistinguishable from that of the arms. This situation mimics, in terms of tentacular development, what is thought to be the ancestral coleoid condition, with the tentacles undifferentiated from the arms (Engeser and Bandel, 1988).

The patterns of development of the arms and tentacles, and their attachment structures (i.e., the arm-crown stalk), are among the earliest clues to the identity of paralarval cephalopods. Thus heterochrony in the development of arm and tentacular characters should be examined formally to determine their value in resolving questions of higher-level relationships among species. For example, heterochrony in arm-crown development is obvious among genera of Enoploteuthidae. Paralarval Abraliopsis are readily distinguishable from other enoploteuthids at similar mantle lengths by their precocious development of long arms and tentacles (Young et al., 1992). Similarly, differences in relative arm lengths are used to identify genera of paralarval octopods (Hochberg et al., 1992). Along with other distinctive features, the character that is most easily used to identify paralarval Chtenopteryx is the very unusual shape of the tentacular club, which can be seen in even the smallest specimens.

TABLE 2.—Characters used for identification of cephalopod paralarvae. Asterisks indicate characters that can change substantially during postembryonic development and therefore can be of use in the comparative study of heterochrony.

  1. Arms

*Relative development of arm pairs
*Pattern of webbing
*Special modifications (e.g., development within a pocket)
*Presence of cirri

  2. Arm Suckers

Attachment to arm (i.e., stalked or sessile)
*Number of rows
*Total number
*Development into hooks

  3. Tentacles

*Presence
*Fusion
*Development compared to arms
*Club shape

  4. Tentacle Suckers

*Number of rows in carpus, manus, and dactylus
*Total number
*Relative sizes
*Development into hooks and/or knobs

  5. Velar Filaments

Presence

  6. Head

*Presence of gelatinous regions
*Length of arm-crown pillar
*Buccal-mass size
? Pattern of buccal-membrane to arm connectives

  7. Eyes

*Relative sizes
*Shape
*Stalk length
*Position on head and orientation
Presence of corneal membrane

  8. Neck

*Length
Esophageal position
*Presence of dorsal hump
Nuchal fusion with mantle

  9. Funnel

Cartilage shape
Fusion with mantle

10. Mantle

*General shape
*Tail length
*Muscular consistency
Dorsal musculature
*Surface structures

11. Shell, Gladius, or Fin Supports

Chemical composition
Structure (e.g., chambered, coiled, etc.)
*Shape
Attachment to mantle and fins

12. Fins

Presence
*Position
*Shape
*Relative size
Presence of support rays
*Presence of secondary fins

13. Digestive Gland

*Relative size
*Shape
*Position

14. Light Organs

*Presence
*Locations (e.g., integument, mantle, eyes, viscera, etc.)
*Positions and grouping patterns within locations
*Relative sizes
*Shapes
*Numbers

15. Chromatophores

*Presence
*Locations (e.g., integument, mantle, eyes, viscera, etc.)
*Positions and grouping patterns within locations
*Relative sizes
*Numbers

A number of species in several families of oegopsids (e.g., Cranchiidae, Chiroteuthidae, Mastigoteuthidae) develop through paralarval stages in which the arms and tentacles are separated from the head by a brachial pillar or “arm-crown stalk.” Similarly, paralarvae of several cranchiid species have long stalks separating their eyes from their heads. Some species, such as Ancistrocheirus lesueuri (Orbigny) and Octopoteuthis spp., also appear to have stalks and pillars on which the eyes and arm crowns occur, but these stalks and pillars are embedded in gelatinous tissue of the head. It would be interesting to determine for which of these species the stalks are homologous and for which they are a result of convergence.

Incirrate octopods hatch with a few fully developed suckers on each arm (Young et al., 1989). Eventually, additional suckers develop distally, but these are easily distinguished at first from the proximal group present at hatching. Octopod paralarvae can therefore be placed phenetically into multispecies groups based on the number and pattern of this proximal group of suckers (Hochberg et al., 1992). The family Octopodidae is very speciose and generic relationships have not been resolved satisfactorily. It is possible that the species grouping based on hatchling suckers could be important to generic relationships within the family if the sucker patterns prove to be synapomorphic.

Another paralarval character by which species can be grouped phenetically within families is the relative sizes of the suckers. For example, the suckers on the fused tentacles of paralarval ommastrephids are all approximately equal in size for some species, whereas in other species two of the suckers are slightly enlarged or the same two suckers are greatly enlarged (Roper and Lu, 1979; Vecchione, 1979; Harman and Young, 1985). Similar patterns of species groups with different patterns of relative sucker enlargement also seem to hold for paralarval octopods (Young et al., 1989).

Development of sucker armature also holds promise for inferring systematic relationships, but few detailed studies have been published. The following are some examples of studies that presented aspects of the development of sucker rings or hooks:

Species |  | Publication
Loligo edulis Hoyle |  | Okutani et al., 1975
Loligo japonica Hoyle |  | Okutani et al., 1975
Gonatus spp. |  | Young, 1972
Galiteuthis glacialis (Chun) |  | McSweeny, 1978

Also, scanning electron microscopy (e.g., Harman and Young, 1985) has shown that sucker pegs may be a novel ontogenetic character for studies of cephalopod systematics.

The unusual sucker development in the family Chiroteuthidae is worth noting. Development of suckers along the arms or tentacles of a cephalopod can generally be considered to be an example of iterative homology (Bock, 1989; Wagner, 1989). In other words, each sucker develops along the same plan, and presumably from the same genetic code, as its neighbors along the arm. The tentacular club suckers of adult chiroteuthids, however, develop late in paralarval ontogeny as a distinct group, separate from the tentacular club suckers of hatchlings. The result is suckers that are very different qualitatively from any other cephalopod suckers. Presumably these suckers are a secondary adaptation, not true iterative homologues of their predecessors in ontogeny. This ontogenetic sequence, together with other unusual paralarval characters (Young, 1991; Vecchione et al., 1992), provide confirmation of the distinctiveness of the genus Chiroteuthis.

The chromatophores of paralarval Lolliguncula are distinctive both in color and pattern among the Loliginidae (Vecchione, 1982), another speciose family in which generic relationships have long been confused (see Vecchione et al., 1998). Similarity in chromatophore patterns between Lolliguncula brevis (Blainville) and L. mercatoris Adam paralarvae support their congeneric relationship rather than proposed alternatives (Vecchione and Lipinski, 1995). Other chromatophore patterns, however, especially the reverse countershading of hatchlings (Hanlon et al., 1992), apparently result from convergence with sympatric species of Loligo and confound the use of chromatophore patterns in this family. Furthermore, the great variability in egg size, and therefore size at hatching, among loliginid species creates problems in determining proper developmental stages for comparisons among species. For instance, Sepioteuthis hatchlings are densely covered with chromatophores on all surfaces whereas, as far as we know, all other genera hatch with far fewer chromatophores that are arranged nonrandomly among the regions of the integument. But all species of Sepioteuthis hatch at a much larger size than any other loliginid, and by the time paralarvae of other genera reach the size of a Sepioteuthis hatchling, they have developed a much more complete covering of chromatophores. So, if comparisons are based on the stage at hatching, very clear differences are apparent, whereas if the comparable stage is at equal sizes (and, therefore, perhaps about the same amount of time after fertilization), the differences are much less distinctive. Paralarval chromatophore patterns have been shown to be important at the species level in other families. For instance, only a single species of Onychoteuthis, O. banksii, has generally been recognized in Hawaiian waters. A second species, O. compacta (Berry), was described from a single early juvenile specimen. Young and Harman (1987), however, described the development of four distinct morphotypes of Hawaiian Onychoteuthis paralarvae based on chromatophore patterns. One of these morphotypes can be assigned to O. compacta, and one could belong to a northern species, O. borealijaponicus Okada. The other two morphotypes include at least one undescribed species, and probably neither represents O. banksii sensu stricto. In Hawaiian waters, similar speciesspecific chromatophore patterns have been demonstrated in enoploteuthids (Young and Harman, 1985), ommastrephids (Harman and Young, 1985), and octopodids (Young et al., 1989). As with the onychoteuthids, Hawaiian octopodid paralarvae proved to have more distinct morphotypes than there are recognized species in local waters. Okutani (1987) pointed out that the basic arrangements of major chromatophores on the mantles of paralarvae of myopsid and oegopsid squids may be classified into four types: (1) a single row along the middorsum; (2) transverse rows; (3) polygonal arrangements; and (4) irregular patterns. Arrangements 2 and 3 are found in many diverse families, so probably they are of little use in systematics above the species level. The first category is quite unusual, though, and could be of use in higher-level systematics. The irregular patterns may be where ontogenetic synapomorphies should be sought. The example that Okutani used for this category was Thysanoteuthis rhombus Troschel, which comprises a monospecific family with paralarvae that are quite distinctive because their mantles are very heavily covered with small, dark chromatophores.

Like chromatophores, photophores form distinctive patterns in paralarval oegopsids. The development of these patterns is even less well known than that of the chromatophores. The few published descriptions of photophore development that meet the requirements for confidence in field studies described above include the following:

Species |  | Publication
Abraliopsis felis McGowan and Okutani |  | Okutani and McGowan, 1969
Leachia dislocata Young |  | Young, 1972
Teuthowenia megalops (Prosch) |  | Dilly and Nixon, 1976
several cranchiids |  | Voss and Voss, 1983

Allometric changes during the early posthatching ontogeny of cephalopods have been used for identification of paralarvae. As presented above, comparisons of allometric growth also have been proposed to be an important source of evolutionary information. The following are some studies of cephalopod development that have included graphic analyses of allometric changes based on fairly large samples:

Species |  | Publication
Gonatus madokai Kubodera and Okutani |  | Kubodera and Okutani, 1977
Illex argentinus (Castellanos) |  | Vidal, 1994
Loligo pealeii Lesueur |  | Vecchione, 1981
Onychoteuthis spp. |  | Young and Harman, 1987
Sthenoteuthis oualaniensis (Lesson) |  | Yamamoto, 1980
Teuthowenia spp. |  | Voss, 1985

Hatchlings of Ancistrocheirus and Octopoteuthis are very similar in external morphology until allometric changes in relative fin length make them easily distinguishable. Throughout their development, however, these genera have very differently shaped digestive glands; in Ancistrocheirus it is elongate, whereas that of Octopoteuthis has an unusual disk shape. Paralarval oegopsids appear to hatch with digestive glands characterized by just a few distinctive shapes. As with many other characters, paralarval ommastrephids have a very distinctive, almost spherical digestive gland. Other characters of the digestive gland that may be of use in evolutionary studies include its location relative to (1) the head, either in direct contact with the cephalic cartilage or separated; (2) the posterior salivary gland, either embedded in the digestive gland or simply in contact with it; and (3) the ink sac, which may be separated from the digestive gland, in contact with it, or partially embedded in it. The digestive gland of loliginids is histologically different from those of other squids and cuttlefishes (Boucher-Rodoni and Boucaud-Camou, 1987), and this distinctive character can be detected even in the earliest paralarvae (Vecchione and Hand, 1990). Preliminary examination of a number of species indicates that differences occur in the development of the stomach and caecum that could be of use in systematics.

The gladii, cuttlebones, and cartilagenous fin-supports are particularly important characters in the higher-level systematics of cephalopods. Development of the gladius, especially the conus, is important at the family level (Toll, 1982). Voss and Voss (1983) used development of the conus in their cladistic analysis of the generic systematics of the Cranchiidae. I have seen similar evidence of differences in conus development among the genera of enoploteuthids. Bandel and Boletzky (1979) presented a very detailed comparative study of the development of chambered cephalopod shells, including cuttlebones.

Very few observations have been made on the development of statoliths, mostly as a potential method for determining the age of paralarvae. These limited observations indicate that there appear to be differences in the development of statoliths that may be of use in higher-level systematics. I have examined statoliths in paralarval Lolliguncula brevis and found that development of structures such as wings, domes, and others is retarded in this species when compared with the figures of statoliths from paralarval Illex illecebrosus (Lesueur) published by Balch et al. (1988). Many other potential characters are available from the study of paralarvae. Beak development, and particularly the patterns of serrations known as “larval teeth,” is promising. Very little is known about early development of the radula (see Nixon's review, 1998), one of the few hard structures in a cephalopod. To my knowledge, the only published presentation of gill development, other than Joubin's (1885) classic study, is Dilly and Nixon's (1976) description of Teuthowenia megalops. Development of the nervous system (e.g., the fusion of crossed giant nerve axons in paralarval Loligo) also holds potential as a systematic character. So does physiology and behavior (Vecchione, 1994), such as the development of euryhalinity in Lolliguncula brevis (Vecchione, 1991) or the physiological changes required for the ontogenetic vertical migrations common among oceanic species (Vecchione, 1987). The amount that we don't know about paralarval cephalopods is almost overwhelming, but that is balanced by the excitement of the potential advances that an investigator can make in almost any direction that he or she proposes to pursue.

Systematic revisions of many cephalopod families are long overdue (Voss, 1977; Roper, 1983; also see the “Family Accounts” of this workshop proceedings (Voss et al., 1998)). Those that have been accomplished throughout the past half century, with very few exceptions, have used traditional methods of subjective comparisons based on adult morphological characters. The most noteworthy exception to this pattern is the work of N. Voss on the family Cranchiidae. After detailed character analysis, including ontogenetic characters, Voss and Voss (1983) used modern cladistic methods to resolve the confused tangle of generic relationships among the cranchiids. Wormuth (1976) used numerical phenetic methods to examine relationships among Pacific ommastrephids, but he did not include ontogenetic characters, nor did he conduct worldwide comparisons.

Future monographic and revisionary studies of systematic groups should follow the cranchiid work in using all developmental stages, formal character analysis, and modern systematic methods, whether cladistic, phenetic, or evolutionary. In addition to the many extant problems at the family level of class Cephalopoda, many species and generic problems also remain to be resolved, and controversy remains even at the ordinal level. Regardless of the method of systematic analysis chosen, ontogenetic characters should be used whenever possible to help resolve questions at all of these levels.

Acknowledgments

Some of the ideas presented herein developed during work on National Science Foundation grant OCE8796218. Numerous colleagues have reviewed drafts and provided helpful comments; they include B.B. Collette, P.M. Mabee, G.D. Johnson, J.E. Olney, S.v. Boletzky, T. Okutani, R.E. Young, and C.F.E. Roper.

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The Systematic Value of the Digestive Organs

Katharina M. Mangold and Richard E. Young

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Katharina M. Mangold, Observatoire Océanologique de Banyuls, Laboratoire Arago, 66650 Banyuls-sur-Mer, France. Richard E. Young, Department of Oceanography, University of Hawaii, Honolulu, Hawaii 96822, United States.

ABSTRACT

The organs of the digestive tract include the buccal assemblage, oesophagus, crop, vestibulum, stomach, caecum, anterior and posterior salivary glands, digestive gland, and the digestive-gland ducts and their appendages. These organs have rarely been used as diagnostic characters or in identifications keys; however, they have been described and illustrated thoroughly for several taxa. The structures vary sufficiently among cephalopod taxa that they have potential as systematic characters at various taxonomic levels.

Introduction

Organs of the digestive tract figure only exceptionally among diagnostic characters of cephalopod taxa. As a rule, the organs are not used in identification keys (e.g., Roper et al., 1969; Roper et al., 1984; Nesis, 1987; Guerra, 1992). Taxonomic studies usually concentrate on external morphology with only an incidental treatment, if any, of the viscera (Voss and Voss, 1983). Other internal structures, however, such as those of the central nervous system and the statocysts and statoliths, have been given a good deal of attention in recent years (for a review, see Clarke and Trueman, 1988).

Although the taxonomic value of the digestive organs may have been largely ignored, these organs have by no means been neglected; many authors have described and illustrated them very carefully (e.g., Chun, 1910, 1915; Joubin, 1918, 1924; Sasaki, 1929; Robson, 1929, 1932; Thore, 1949). Ideally, the description of a new species or redescription of known species, as well as revisions of other cephalopod taxa, should include the description of the digestive organs as recommended by Roper and Voss (1983).

The digestive organs, their presence, absence, or degree of development of one or several of them, and their size and position, have played important roles in studies of adaptation to particular environments. For example, the papers by Grimpe (1921, 1922), Robson (1926, 1932), and G.L. Voss (1967, 1988) deal with different groups of Octopoda and with life in deep waters. Young (1977) emphasized the relationship among the mode of life, the nervous system, and some digestive organs, especially the foregut glands, in several cephalopod species. Moreover, a given organ functions differently in different taxa as a result of the kind of prey eaten (Boucher-Rodoni et al., 1987; Nixon, 1988a, 1988b). In the Traité de Zoologie, Mangold and Bidder (1989) described in detail the digestive systems of Nautilus and the four coleoid orders and pointed out the main differences existing between these taxa. The authors concluded that these differences are mainly related to the type of prey, mode of food intake, and processes of food storage and distribution at various stages of digestion (sensu lato). Although this conclusion is probably correct, it may not be the whole story.

A recent paper by N.A. Voss (1988), together with discussions and the advice and encouragement of colleagues during the 1988 Cephalopod International Advisory Council (CIAC) workshop, has expanded the “functional-morphology” perspective of the first author to larger horizons that consider other aspects of the digestive system. The reader should be warned, however; we have not been able to examine the digestive organs of all cephalopod families and genera, let alone species, and, as a rule, we consider adult and subadult animals only. The information herein, therefore, is not comprehensive.

ACKNOWLEDGMENTS.—We are deeply indebted to Anna M. Bidder, who shared her great knowledge about the cephalopod digestive system with us and allowed us to use the information. We are grateful to Eve Boucaud-Camou and Mike Vecchione, who read the manuscript and offered valuable suggestions.

Overview of the Digestive System

The digestive system of cephalopods is a conservative feature. It is basically mollusc-like, although the mode of life of this class is not (Mangold-Wirz and Fioroni, 1970; Packard, 1972), and a few major changes have occurred from the basic molluscan plan. The high activity and rapid growth of Recent cephalopods require a large amount of food and a high feeding and digestion efficiency. The development of powerful beaks, combined with the grasping capabilities of arms and tentacles, has enabled them to prey on large organisms, and the division of the primitive molluscan stomach into two distinct organs, the stomach proper and the caecum, allows a rapid processing of food. Readers interested in the differences in digestive organs among the molluscan classes should consult Salvini-Plawen (1988). The differences in the digestive systems among cephalopod orders, families, and genera, however, are no match for the spectacular diversity observed in other systems, such as locomotor (mantle, fins, arms), protective and support (shells and their derivatives), prey-capture (arms and tentacles), sensory (eyes, statocysts, etc.), and concealment (chromatophores, iridophores, photophores) systems.

The digestive tracts of representatives of the classical orders or suborders, namely those of Sepia officinalis Linnaeus (Sepioidea), Loligo vulgaris Lamarck (Myopsida), Abralia trigonura Berry (Oegopsida), Vampyroteuthis infernalis Chun (Vampyromorpha), and Octopus vulgaris Cuvier (Octopoda), are shown in Figure 1. The digestive tract is basically U-shaped; the oesophagus is oriented backward over the dorsal side of the digestive gland, opening into the stomach, which lies, together with the caecum, at the bend of the U. The intestine is oriented forward on the ventral side of the digestive gland, opening into the mantle cavity together with the duct of the ink sac (when present). There are minor variations in this basic arrangement, such as the size of the whole organ system, which may extend more or less posteriorly, filling the mantle cavity, or may be concentrated in the anterior one-half or so of the body. There is, however, a remarkable exception. In the bathypelagic incirrate families Amphitretidae and Vitreledonellidae, the oesophagus is very short, the stomach and caecum lie at the anterior end of the digestive gland, and the intestine lies dorsally along this gland before bending ventrally. Thore (1949:51, 57) used this character, “stomach in front of liver [digestive gland],” in the diagnosis of the two families. In the cirrate family Opisthoteuthidae, the intestine is posterior to rather than anterior to the stomach and caecum (Meyer, 1906), but this orientation is brought about by the dorsoventral compression of the animal.

The digestive organs (excluding the buccal mass with its structures) are listed in Table 1. The major differences among the higher taxa are indicated. These taxa, however, are often represented by only a few well-known species so the differences must be considered tentative. Table 2 summarizes the function(s) of these organs as currently known.

TABLE 1.—Digestive organs in cephalopods.

FIGURE 1.—Diagrammatic illustration of digestive systems from representatives of the four orders of Coleoidea. a, Octopoda: Octopus vulgaris; b, Teuthoidea Oegopsida: Abralia trigonura; c, Teuthoidea Myopsida: Loligo vulgaris; d, Vampyromorpha: Vampyroteuthis infernalis; e, Sepioidea: Sepia officinalis. (a, c, e modified from Bidder, 1966, and Boucaud-Camou and Boucher-Rodoni, 1983.) (Abbreviations: a, anus; asg, anterior salivary gland; bm, buccal mass; c, caecum; cr, crop; cs, caecal sac; dd, ducts of the digestive gland; dda, digestive-gland duct appendages; dg, digestive gland; i, intestine; l, lips; oe, oesophagus; psg, posterior salivary gland; s, stomach. Vestibule is not labelled.)

TABLE 2.—Function(s) of the digestive organs.

Oesophagus

Food transport to stomach.

Crop

Storage of intact food or predigested food.

Stomach

Mechanical and enzymatic breakdown of food.

Caecum

Enzyme production, nutrient absorption, nutrient storage in caecal sac at later stages of digestion, elimination of undigestible particles.

Vestibule

Storage at various stages of digestion, crossroad for transport between oesophagus, stomach, caecum, and intestine.

Intestine

Storage and elimination of fecal material, mucous production for envelopment of fecal material, intake of seawater.

Anterior salivary glands

Production of mucous and (?) proteolytic enzymes.

Posterior salivary glands

Production of proteolytic enzymes, chitinases, cephalotoxins, biogenic amines.

Digestive gland

Digestive enzyme production, nutrient absorption, excretion, lipid storage, temporary nutrient storage in lumina during later stages of digestion.

Digestive-gland ducts

Transport of digestive enzymes to stomach and caecum, nutrients from caecum to digestive gland, seawater to digestive-gland duct appendages, and waste products from digestive gland to intestine.

Appendages of digestive-gland ducts

Nutrient absorption, excretion, role in urine formation (?), principle site of water and digestive salt uptake.

Variations in Digestive Organs Among Taxa

The digestive tract consists of four organs that are present in all living cephalopods: the oesophagus, the stomach, the caecum, and the intestine. In addition there are four major organs connected with the digestive system, namely the digestive gland, the appendages of the digestive-gland ducts (the “pancreas”), and the anterior and the posterior salivary glands (Table 1). There are some additional structures associated with the buccal mass (for a review see Nixon, 1988a, 1988b).

The oesophagus in decapod cephalopods lacks a crop, whereas this organ is present in Vampyroteuthis and in most octopods, as well as in Nautilus. In cirrates and some deep-sea incirrates, the crop is reduced or absent; this reduction or absence is very likely correlated with the mode of life, or more precisely, with the mode of feeding in these benthic or benthopelagic deep-sea animals. The bathypelagic incirrate families, however, have retained the crop, which suggests that these deep-sea pelagic octopods either have a different mode of feeding from their relatives that live near the deep ocean floor or the difference is simply an artifact of their evolutionary history. The size and shape of the crop vary among taxa; the organ may be a clearly separated diverticulum with a small opening as in the bathypelagic incirrates (Bolitaena, Vitreledonella), a diverticulum with a large opening into the oesophagus (Octopus, Figure 1a. Eledone) that varies in size among species, or a mere swelling of the oesophagus as in Vampyroteuthis (Figure 1d), the cirrates, and some deep-sea octopodids.

The stomach is a strongly muscular organ in almost all cephalopods; in some oegopsids it is bipartite, consisting of a muscular part where the food is crushed and a relatively thin-walled very extensible “storage” part. In some cranchiids it is distinctly tripartite (Chun, 1910). Like the oesophagus, the stomach is lined by a cuticle, and, like the caecum, it is colorless when empty except in some oegopsid families (e.g., Histioteuthidae), where it is red purple. Variations in size and shape exist but are often due to the degree of fullness.

The caecum is a delicate, thin-walled structure with close-set leaflets filling most of the lumen. Its epithelium is folded, ciliated, and glandular. It is coiled or shows at least traces of coiling (in a few cirrates). The number of coils is of value in species determination in octopods, and their number should be indicated in species descriptions. Some cirrate octopods (Opisthoteuthis) have an additional sacculate diverticulum, the so-called “third stomach” (Meyer, 1906), which is the most proximal part of the intestine. In spite of variability due to feeding, differences in size between the stomach and the caecum can provide important systematic characters. Many authors have pointed out the size difference between the two organs in species descriptions (cf. Chun, 1910). Voss and Voss (1983) and N.A. Voss (1988) have used this character (i.e., caecum smaller or larger than stomach) in their papers on the evolution of the cranchiids. Generally the two organs are about equal in size in the octopods and the sepioids. The loliginids have, in addition to the spiral portion, a large caecal sac, which contains a clear liquid without any hard residues, lying on one side of the spiral (Figure 1e). A caecal sac of various size and shape is present in several oegopsid families (Figure 1b), and the liquid often contains hard fragments. Although the caecal sac in the loliginids is a well-defined, large structure that is clearly visible even when more or less empty, it is less obvious in the oegopsids and one may not notice its presence at all even in freshly fixed material (Bidder, pers. comm., 1989).

The following information on the caecum in oegopsids has been given to the authors by Anna M. Bidder. Because, except for a few families, little is known of the digestive system in this group, it seems appropriate to include it here. A caecal sac is known in six families, namely the Ommastrephidae, Octopoteuthidae, Chiroteuthidae, Mastigoteuthidae, Cranchiidae (Cranchiinae), and Enoploteuthidae. The sacs vary among families in their shape and position and in their size relative to the spiral caecum and the stomach. In the larger ommastrephids, with a spiral caecum of two to three coils, the sac lies between the last leaflet and the caecal opening; it does not appear to be of great size, but fully distended sacs have not been observed. In Illex and Todaropsis the sac involves the whole spiral caecum, and the leaflets are spread out into a spiral fan. The sac is approximately equal to the stomach in Todaropsis, and in Illex it is comparable in length to that of Loligo. In Onychoteuthis the leaflets are similarly spread out, but there is no sac beyond the leaflets. In Taningia and Chiroteuthis the sac is developed from a limited length of the last half whorl, whereas in Mastigoteuthis the caecum of one and one-half coils is undisturbed, and a sac is formed from the last one-quarter turn. In Cranchia the caecum is all sac, and the leaflet system is reduced to a tiny rosette. The groups seen that had no sac were the Lycoteuthidae, Onychoteuthidae, Gonatidae, Histioteuthidae, Grimalditeuthis, and Architeuthidae. The number of coils is only to some extent related to adult size. In Architeuthis there are five turns, but in Mesonychoteuthis there are about two turns, in Taningia and Moroteuthis two to three, but two to three also in Gonatus and Histioteuthis and two in the small-sized Lycoteuthis diadema (Chun). In species of small to medium size, one and one-half turns are usual.

The stomach and caecum are linked by the vestibule (the “magensinus” of Chun, 1910), which is a short tube in most species but is a more voluminous region in others, especially in Vampyroteuthis, the sepiolids, and in most if not all oegopsids (Figure 1b), where this organ forms a crossroad for the oesophagus, stomach, caecum, and intestine. The loliginids have no vestibule; the stomach and caecal openings are adjacent, the latter being protected by a special valve (Bidder, 1950, pers. comm., 1989).

The intestine is an organ of considerable variability among taxa. Its division in Nautilus into three distinct parts with highly elaborated structures is unmatched in the coleoids (Bidder in Mangold and Bidder, 1989). Impressed by this complex organ, Mangold and Bidder (1989) described the contrasting coleoid intestine as a simple tube, which as a rule is true for the teuthoids, Vampyroteuthis, and some cirrate octopods. It is, however, a slight understatement as applied to the sepioids, where the intestine often has a coiled part, and a rather grave understatement for the incirrates, where, in many species, the intestine is equally divided into three parts: a proximal intestine, loops, and a distal intestine (i.e., many Octopus spp.). The rectum is the terminal part of the distal intestine into which the duct of the ink sac opens (when present). Anal flaps are present in species with an ink sac and are absent in those that have none. Particular attention should be paid to the intestine when describing or redescribing an incirrate octopod species (cf. Hochberg and Mangold, in prep.). The ink sac has no digestive functions; it is simply topographically associated with the digestive system and is not represented in Figure 1. This organ is more or less embedded in the digestive gland in the octopods and is free from it in the sepioids and most teuthoids. In paralarvae of some teuthoid genera (Illex, Ancistrocheirus), however, the ink sac lies on or in the digestive gland (Vecchione, pers. comm., 1988). The cirrates, Vampyroteuthis, some deep-sea incirrates, and Neorossia caroli (Joubin) have no ink sac.

The digestive gland, also referred to as the midgut gland or the “liver,” is the most conspicuous organ of the digestive system by its sheer volume. This organ, paired in origin, varies in shape, size, and location (position). There are three to five main lobes in the gland of Nautilus. In most cephalopods it is the largest organ in the mantle cavity, except in mature females, where the reproductive organs become more voluminous. As a rule, one would expect species with a high metabolic rate to have a large digestive gland and species with a less active mode of life to have a smaller one. This organ is a solid single mass in the octopods, Vampyroteuthis, and most oegopsids. In most sepioids and in the loliginids, the paired nature of the organ is clearly visible, although at varying degrees. Apparently fusion of the separate lobes has occurred independently in different taxa.

In the coleoids the digestive gland is covered by a thin muscular and connective tissue envelope. The gland itself consists of tubules, the largest of which open to a pair of wide lumina that in turn open to the digestive ducts. The tubules are lined with a glandular epithelium. Several cell types have been described by various authors, but it is likely that in most, if not all, coleoids the various cell forms are functional stages of a single cell type, the digestive cell or “boules cell” (Boucaud-Camou and Yim, 1980; Boucher-Rodoni, 1981). The mature digestive cell is characterized by the “boules,” large proteinaceous inclusions that produce proteolytic enzymes, and by the frequent occurrence of brown bodies (Bidder, 1957), large masses containing crystals, often included in a vacuole. These cells undergo some histological changes that can be related to digestion (Bidder, 1950, 1957). The loliginids are exceptional in that they have no boules cells and few brown bodies (Bidder, 1950, pers. comm., 1989).

The appendages of the digestive-gland ducts are absent only in Nautilus. These appendages, referred to in older literature as “pancreas” (or “the so-called pancreas”), therefore, are characteristic of the coleoids. In the octopods they are enclosed in the sheath of the digestive gland, at its posterior end (Figure 1a). In Vampyroteuthis they abut the digestive gland as in octopods but are not enclosed in the digestive-gland sheath (Figure 1d). In decapod cephalopods they are generally spread along the ducts of the digestive gland where they form lobules that are often associated with renal epithelium (Figure 1b,c,e). In the sepioids the appendages are grape-like follicles individually covered by renal epithelium. In the myopsids the whole mass of follicles is covered by renal epithelium. In the oegopsids there is no overall renal coverage, and the appendages show great variability, which had not escaped the notice of the eminent zoologist C. Chun. In his monograph of the Oegopsida of the Valdivia expedition (1910), the author stated that these organs vary strikingly in shape, size, and location.

The anterior salivary glands appear to be mainly glands of mucous production and are present in all cephalopods with a few exceptions (Spirula, some cirrates). Their location is characteristic on the ordinal level. In Vampyroteuthis and in the octopods, the large anterior salivary glands lie externally on the buccal mass (i.e., they are extrabulbular). These glands have an extra-and an intrabulbular part in the teuthoids and are inclosed in the buccal mass (intrabulbular) in Nautilus and in the sepioids (except Rossia). Organ size and evolutionary history are, presumably, responsible for this arrangement. We cannot offer any additional functional explanations.

The posterior salivary glands, in contrast to their anterior counterparts, have many different functions (Table 2). These organs are lacking in Nautilus, are usually paired in incirrate octopods and sepioids, single (unpaired) in loliginids, Vampyroteuthis, and the cirrates, and bilobed in oegopsid teuthoids (Table 1, Figure 1b). The morphology of these organs is strongly affected by the mode of life and feeding of the different species; however, structural differences related to the systematic position do exist. In octopods the posterior salivary glands have glandular tubules with heterogenous mucous cells (some of them being enterochromaffin) and striated ducts, whereas there are no striated ducts in teuthoids and sepioids. In sepioids and in Loligo there is only one cell type with proteic granules and no enterochromaffin cells (Boucaud-Camou, 1968; Matus, 1971; Koueta and Boucaud-Camou, 1986, 1989). In oegopsids heterogenous mucous cells may occur, but further studies are needed (Boucaud-Camou, pers. comm., 1989).

The Digestive Organs and Systematics

Although there is a clear classification of the Recent cephalopods that is functionally adequate (i.e., that of Voss, 1977, adopted by Mangold and Portmann, 1989), alternative classifications have been proposed in recent years.

In 1981, Fioroni established two superorders, Octobrachia (the Octopoda) and Decabrachia, with the latter comprising Sepioidea, Teuthoidea, and Vampyromorpha. Within Decabrachia, the author raised the family Sepiolidae to ordinal level, the Sepiolioidea. Berthold and Engeser (1987) placed the sepiolids next to the loliginids after splitting off Spirula and the sepiids. Clarke (1988) derived his Sepiolioidea (not sensu Fioroni) from the teuthoids rather than putting them in line with the sepioids. The systematic position of the sepiolids, the “bobtail squids,” within the decapod cephalopods, has been discussed several times (e.g., Joubin, 1902; Grimpe, 1921, 1922; see also Boletzky, 1995, for literature and discussion). Among the recent authors. Fioroni is the only one to consider the digestive organs, and he concludes that these organs in the sepiolids are like those in the sepiids (Fioroni, 1981:189), thus confirming Boucaud-Camou's results (1968). There are, however, some important differences. Sepiola has a well-developed vestibule whereas Sepia has none. The digestive-duct appendages in Sepiola and Rossia are different in shape from those of Sepia; they are finger-like or sausage-shaped, and they are apparently muscular (Bidder, pers. comm., 1989). Berthold and Engeser's proposal to place the sepiolids next to the loliginids gains little support from the digestive organs. The loliginids have a large caecal sac, and they have no vestibule.

Young (1989) divided the coleoids into three infraclasses: Octobrachia, Decabrachia, and Vampyromorpha. The first includes two orders, Cirroctopoda (Cirrata) and Octopoda (Incirrata), and the latter includes three suborders, Benthoctopoda, Epipelagoctopoda, and Bathypelagoctopoda. His orders of the Decabrachia are Teuthida, Sepiida, Sepiolida, and Spirulida. M. Nixon and J.Z. Young will presumably provide evidence for this classification in their long awaited book on the life and brains of cephalopods. From the point of view of the digestive organs, the rank conferred on Vampyromorpha as a taxon of its own is more acceptable than Fioroni's classification. In his review of the evolution of recent Cephalopoda, Clarke (1988) has already recommended retaining the status of the Vampyromorpha as a separate taxon at the highest level within the Coleoidea. There is not much to be said about the ordinal level of the Spirulidae; their digestive system is Sepioidea-like. Spirula has no anterior salivary glands, but these organs also are absent in some cirrates. Presumably, their absence represents a secondary loss.

Although there is considerable speculation on the phylogeny and classification of Recent cephalopods, there are very few studies that combine careful character analyses with basic Hennigian principles for the determination of phylogenetic trees (e.g., Fioroni, 1981). There are, however, several exceptions in studies below the family level. In his evolutionary tree of the incirrates, G.L. Voss (1988) split his four groups, the new subfamily Graneledoninae, the emended Eledoninae and Bathypolypodinae, and the (not treated) Octopodinae first on the basis of one or two rows of suckers, leading to the Octopodinae and Bathypolypodinae as one group and to the Eledoninae and Graneledoninae as another. Each of these two groups were then split by the presence or absence of an ink sac. For the actual diagnosis of the subfamilies, G.L. Voss (1988) used digestive organs, namely the crop and the posterior salivary glands. The Octopodinae have a crop with a sac-like extension and have large posterior salivary glands, as do two genera of the Bathypolypodinae, Benthoctopus and Teretoctopus, both with moderately deep- and deep-water species, but they have no ink sac. The third genus of the subfamily, Bathypolypus. has a crop without a diverticulum, and its posterior salivary glands are small. The members of this genus are truly deep-water species. The Eledoninae, with an ink sac, also have large posterior salivary glands and a crop with a diverticulum. Eledone species live in shallow water. The other genera of this subfamily live in intermediate depths. The members of the Graneledoninae are deep-water animals; their crop is simple or absent, and the posterior salivary glands are small to vestigial.

The trend toward a simple crop or no crop and reduced posterior salivary glands in deep-sea octopods cannot be denied, but this reduction or loss has not occurred in all genera or species. A simple “functional” interpretation of this trend, therefore, is not clear enough, although G.L. Voss (1988) suggested that the reduction may involve octopods feeding on small or soft-bodied prey. How far, on the other hand, it could also call into question the validity of the evolutionary tree, especially the position of the genus Eledone, as G.L. Voss (1988) pointed out, cannot be debated herein. Voss considered the presence of a crop and large posterior salivary glands as an ancestral state (among others) in the Octopoda.

Voss and Voss (1983) and N.A. Voss (1988) used the digestive-duct appendages in their studies on phylogenetic relationships in the oegopsid family Cranchiidae. This character was selected on the basis of its within-genus constancy. The ancestral character state was appendages spread along the duct and the derived character state was appendages compacted against the digestive gland. The latter character evolved independently in several lines.

Another character of the digestive system used by these authors in their phylogenetic studies is the size of the caecum as compared to the size of the stomach. “Caecum smaller than stomach” is considered to be the ancestral character state because the majority of the members of the outgroup have a smaller caecum. In the three groups of the subfamily Taoniinae, the caecum is smaller than the stomach, whereas in the three Cranchiinae genera, it is larger. The caecum also is smaller than the stomach in the enoploteuthid families, the Ommastrephidae and Gonatidae (Chun, 1910).

The digestive gland is the third organ of the digestive system used by Voss and Voss (1983) and by N.A. Voss (1988) in their phylogenetic studies on the cranchiids. In the oegopsids this organ is usually stout and ovoid-shaped and lies parallel to the longitudinal axis of the body. In the cranchiids the digestive gland is usually spindle-shaped, stout, or elongate. The gland does not lie parallel to the body axis but is suspended at a right angle to it. In live cranchiids, however, the organ is rotated to remain vertical as the animal changes orientation (Seapy and Young, 1986). This oblique position, although common in oegopsid paralarvae, is probably absent in adults of all other families. In paralarval teuthoids the position and shape as well as the pigmentation of the digestive gland varies at many systematic levels, including the species level (e.g., in Gonatus onyx Young the gland is in a posterior position, spindle-shaped, and transversely positioned to the body axis, whereas in Gonatus berryi Naef the gland abuts the cephalic cartilage and is spherical (Young, 1972; see also Vecchione, 1998).

Digestive Organs and Mode of Life

In his paper on evolution and phylogenetic relationship in deep-sea octopods, G.L. Voss (1988) listed among the modifications that had occurred in the digestive system of these species the loss or reduction of the crop, reduction or loss of the radula (see Nixon, 1998), and the reduction of the posterior salivary glands. In the cirrates the crop is a mere swelling of the oesophagus or there is no crop at all. The posterior salivary gland in this group is single (unpaired) and small, or it is absent. Voss suggested that the loss of the crop and the reduction of the posterior salivary glands are correlated with the small, soft-bodied animals used as food in the deep sea. Prey dismemberment and partial external digestion are not needed, nor is a storage place (the crop) for the partially digested food before it is conveyed to the stomach. Incirrate species, especially the Octopodinae and Eledoninae, that feed on large prey, and often on large quantities at a given time, need venom from the posterior salivary glands to immobilize the prey. In addition, salivary gland secretions provide chitinases to detach the flesh from the cuticle (crustaceans; Grisley and Boyle, 1990) and provide proteolytic enzymes for external digestion (Nixon, 1984). Finally, a large crop is required as a storage organ.

Highly active swimmers, such as many oegopsids and the loliginids, probably feed more or less continuously or at least several times a day. The food is quickly processed and is stored, if necessary, in the stomach and vestibule (when present) or, at later stages of digestion, in the caecum (sac). In Sepia the fluid can be stored in the lumina of the digestive gland. The waste products are quickly eliminated through the simple intestine; there is no storage of waste. The octopodids, especially the shallow water species, accumulate a large amount of food within the arm crown, process it in installments, and retain waste products in the long and differentiated intestine from where they are periodically ejected after the digestion of the whole meal is completed. Digestion is distinctly slower than it is in teuthoids (at equal temperatures). The length and structure of the intestine provide a clear link between the morphology of the intestine and the mode of food processing (see also Nautilus). The length of this organ, however, also depends on the layout of the whole visceral complex in the mantle cavity (e.g., anterior or posterior location).

The appendages of the digestive-gland ducts show considerable morphological variation (see “Variations in Digestive Organs Among Taxa,” above), and they have multiple functions (Table 2). If the regulation of water and salt balance as shown by Wells and Wells (1989) for Octopus vulgaris were true for all coleoids, the high variability found in the oegopsids may, at least partially, be linked with that function.

Conclusions

Several organs of the digestive system appear to have value in cephalopod systematics and/or phylogeny. Sepioidea and Teuthoidea have no crop, whereas Nautilus, Vampyroteuthis, and Octopoda have a crop (the loss in some octopod species is secondary). The location of the anterior salivary glands also separates the orders Octopoda and Vampyromorpha from the orders Sepioidea and Teuthoidea.

The location of the appendages of the digestive-gland ducts separates orders as well as suborders, and they are variable within families and often within genera. This organ has potential in revealing phylogenetic relationships within the oegopsids, as Voss and Voss (1983) have clearly demonstrated.

The degree of fusion of the lobes of the digestive gland varies between orders and suborders. Variation in the shape of this organ does not appear to have been fully utilized in systematics. Another feature of the digestive gland that could be of some systematic value is its posterior extension. Does it occupy the first one-quarter or the first one-half or so of the mantle cavity? Some species, such as Batoteuthis skolops Young and Roper, have the viscera situated well forward in the mantle cavity (Young and Roper, 1968). In the pelagic ctenoglossan octopods the shape and position of the digestive gland is one of the most important familial characters. Vampyroteuthis has a large space anterior to the posteriorly situated digestive gland (Figure 1d). A similar space is present in some paralarval squids and in the ctenoglossan octopods, especially in the Bolitaenidae. The similarities appear to be superficial in the former but real in the latter. This, clearly, deserves further investigation.

Another valuable character appears to be the size of the caecum compared to the size of the stomach. The intestine probably has some additional potential for systematic investigations of octopods.

The isolated position of the Sepiolidae (= the Sepiolioidea of Fioroni, 1981) can be supported by characters of the digestive tract. Fioroni's proposal to include the order Vampyromorpha in the superorder Decabrachia is not supported from the point of view of the digestive organs.

The digestive organs emphasize the uniqueness of the Loliginidae. The members of this family have a large caecal sac that contains only transparent fluid and never contains any hard particles as are found in the Oegopsida. They have no trace of a vestibule, and the fine morphology of their digestive gland is different, as far as known, from that of all other coleoids by not having boules (see “Variations in Digestive Organs Among Taxa,” above). The fluid in the caecal sac, likely to be broken down to the amino-acid level, goes straight to the digestive gland where absorption takes place (Bidder, 1950, pers. comm., 1989; Boucher-Rodoni and Boucaud-Camou, 1987). It would be of great interest to know if the digestive system of species considered to be related to the Loliginidae (i.e., Chtenopteryx, see Young, 1989) shows these loliginid characters.

The characters of the digestive system have contributed to our understanding of both major and minor phylogenetic pathways and should continue to provide new information in the future.

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Vecchione, M.

1998.   Ontogenetic Characters and Cephalopod Systematics. In N.A. Voss, M. Vecchione, R.B. Toll, and M.J. Sweeney, editors, Systematics and Biogeography of Cephalopods. Smithsonian Contributions to Zoology. 586(1):11–20.

Voss, G.L.

1967.   The Biology and Bathymetric Distribution of Deep-sea Cephalopods. Studies in Tropical Oceanography, 5:511–535.

1977.   Classification of Recent Cephalopods. In M. Nixon and J.B. Messenger, editors. The Biology of Cephalopods. Symposia of the Zoological Society of London, 38:575–579.

1988.   Evolution and Phylogenetic Relationships of Deep-sea Octopods (Cirrata and Incirrata). In M.R. Clarke and E.R. Trueman, editors, The Mollusca, 12: Paleontology and Neontology of Cephalopods, pages 253–276. San Diego: Academic Press.

Voss, N.A.

1988.   Evolution of the Cephalopod Family Cranchiidae (Oegopsida). In M.R. Clarke and E.R. Trueman, editors, The Mollusca, 12: Paleontology and Neontology of Cephalopods, pages 293–314. San Diego: Academic Press.

Voss, N.A., and R.S. Voss

1983.   Phylogenetic Relationship in the Cephalopod Family Cranchiidae (Oegopsida). Malacologia, 23:397–425.

Wells, M.J., and J. Wells

1989.   Water Uptake in a Cephalopod and the Function of the So-called “Pancreas.” Journal of Experimental Biology, 145:215–226.

Young, J.Z.

1977.   Brains, Behaviour and Evolution of Cephalopods. Symposia of the Zoological Society of London, 38:377–343.

1989.   The Angular Acceleration Receptor System of Diverse Cephalopods. Philosophical Transactions of the Royal Society of London, series B, 325:189–238.

Young, R.E.

1972.   The Systematics and Areal Distribution of Pelagic Cephalopods from the Seas off Southern California. Smithsonian Contributions to Zoology, 97: 159 pages.

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Cephalic Cartilage of Cephalopoda

Marion Nixon

____________

Marion Nixon, Norfolk Road, New Barnet, Herts EN5 5LT, United Kingdom.

ABSTRACT

The structure of the cephalic cartilage of cephalopods at the light- and electron-microscope levels is briefly reviewed, together with its biochemical properties. The cartilage usually takes the typical hyaline form, but in some cephalopods it is reticulate. A systematic survey includes brief descriptions of the cephalic cartilage in the few cephalopods for which details are available. The very complexity of this structure suggests it could prove valuable as a systematic character.

Introduction

The majority of cephalopods possess a skeletal structure around the central nervous system. Owen (1832:16) noted that “this skeleton is cartilaginous, yields readily to the knife, and in texture and semi-transparency closely resembles the cartilage which constitutes the skeleton of the skate.” This interpretation of the tissue was accepted until about the turn of the century, when it was questioned as to whether invertebrates possessed “true” cartilage. A period of doubt and uncertainty lasted until the 1960s, when studies, using various techniques, confirmed the earlier belief that Cephalopoda do possess true cartilage, although it differs in some respects from vertebrate cartilage (for reviews see Person and Philpott, 1967, 1969; Person, 1983).

Although it is small or reduced in some, the cephalic cartilage occupies much of the region between the eyes in most cephalopods. Despite this its gross morphology has been overlooked and is rarely referred to in systematic descriptions. This is perhaps not surprising because isolation of the cartilage is not easy to do after fixation, and it necessitates the destruction of the head.

ACKNOWLEDGMENTS.—I am deeply grateful to the late G.L. Voss and to C.F.E. Roper for their invitation and hospitality during the meeting in Washington, D.C., and to M.R. Clarke, J.B. Messenger, and J.Z. Young for much helpful criticism of the manuscript.

Cephalic Cartilage

The word cartilage comes from the Latin cartilago, meaning gristle. Person and his colleagues, in a series of experimental studies, demonstrated that the criteria established for this tissue in vertebrates also apply to invertebrates (for reviews see Person and Philpott, 1963, 1967, 1969; Bairati, 1985). The results of these investigations led Person (1983:33) to modify the definition of cartilage to “an animal tissue, usually endoskeletal, but also exoskeletal….Physically, cartilages are gristle-like, relatively rigid, and resistant to forces of compression, shearing, and tension.”

The basic and constant component of cartilage is the cartilage cell surrounded by a territorial matrix it has itself secreted. Cartilage is a form of connective tissue with polymorphic cells suspended in a matrix (see Moss and Moss-Salentijn, 1983) and is chemically characterized by the presence of collagen, glycosaminoglycan complexes (= mucopolysaccharides) (see Lash and Vasan, 1983), and water.

Cartilage cells, the chondrocytes, are polymorphic and reside in lacunae. Each lacuna may contain one, two, or more chondrocytes, and when several are present it constitutes a cell nest. Young chondrocytes, the chondroblasts, are flattened, becoming rounded when fully mature. Each chondrocyte has a nucleus, well-developed rough endoplasmic reticulum, and Golgi complex; these were described in Loligo pealeii Lesueur (Person and Philpott, 1963; Philpott and Person, 1970) using the transmission electron microscope. The chondrocytes have branching processes forming a system of interconnecting canaliculi that extend into the matrix. The matrix consists largely of fibers and an amorphous substance. Ultrastructural studies of the cephalic cartilage of Loligo pealeii, Octopus vulgaris Cuvier, and Sepia officinalis Linnaeus have revealed the presence of collagen fibrils (Philpott and Person, 1970), 10–26 nm in diameter, with an indistinct periodicity and separated by a constant space (Bairati et al., 1987). The collagen fibrils were found to have a periodic structure similar to that of one of the types found in mammals (Bairati et al., 1989). The fibrils are arranged parallel to the surface in the superficial zones of the cephalic cartilage. Electron dense bodies of varying diameter and length are irregularly distributed among the collagen fibrils. These bodies are interpreted as anchoring devices for the collagen fibrils. Proteoglycan aggregates (30–45 nm in diameter, electron dense, and granular) adhere to the collagen fibrils, the anchoring devices, and the cellular surfaces (Bairati et al., 1987).

FIGURE 1.—a, Alloteuthis subulata (bar = 1 mm); b, Chtenopteryx sicula, note very thick dorsal portion of cartilage (bar = 0.5 mm); c, Gonatus fabricii (bar = 0.2 μm); d, Teuthowenia megalops (bar = 0.2 μm). Cephalic cartilage like that of vertebrate hyaline cartilage.

Few investigations have been made of the biochemistry of this cartilage in cephalopods, and the works by Person and Philpott (1969), Mathews (1967, 1975), Hunt (1970), Person (1983), and Kimura and Karasawa (1985) encompass most of the meager data available. Amino-acid analyses are available for Loligo pealeii (Philpott and Person, 1970) and Todarodes pacificus (Steenstrup) (Kimura and Karasawa, 1985); some differences are apparent between the two species. The composition of polyanionic glycosaminoglycans for four species of cephalopods is summarized by Person (1983).

The cephalic cartilage is glass-like in living cephalopods, being translucent, colorless, and clear to the naked eye, and cannot be discerned visually as a distinct structure. After death, or shortly after removal, this cartilage becomes opaque and bluish white. The cartilage encases the central nervous system and is perforated for the passage of nerves, blood vessels, and oesophagus (see Willey, 1900). Various sectors have muscle fibers and connective laminae deeply inserted in the superficial zone.

Histological sections of this cartilage in cephalopods have shown two types; the more usual form resembles hyaline cartilage (Figure 1) (Young, 1971), but the other form is reticulate (Figure 2). Reticulate cartilage is encountered mainly in the neutrally buoyant oegopsid squids (Clarke et al., 1979). In some squids the network is very loose (Figure 2), but at the surface, where growth occurs, the appearance is that of typical cartilage. From a study in progress (Nixon and Young, in prep.), the type of cartilage present in the head has been tabulated for a number of cephalopods (Table 1). It is notable that of the squids possessing reticulate cephalic cartilage most are neutrally buoyant, but Onychoteuthis and perhaps Lycoteuthis are nonbuoyant forms (Clarke et al., 1979).

FIGURE 2.—a, Abraliopsis sp. (bar = 0.5 mm); b, Architeuthis sp. (bar = 0.5 mm); c, Onychoteuthis sp. (bar = 0.5 mm); d, Mastigoteuthis (bar = 0.5 mm). Cephalic cartilage reticulate and differs notably from that of cephalopods shown in Figure 1.

METHODS.—The simplest method for extracting the cephalic cartilage without damage is to take fresh material and, after appropriate external measurements, remove the whole head and place it in sea water at room temperature until the tissues fall away to leave a clean skeleton. Animals frozen immediately after capture can be treated in the same way because the musculocartilage attachments are readily broken in cephalopods after such low temperature treatment. After fixation, proteolytic enzymes can be used to break down the tissues and adhering muscles, but, if possible, chemical macerating agents should be avoided because many lead to loss of skeletal material. An alternative is the use of thick serial sections of the whole head so that graphic reconstructions of the cephalic cartilage can be made (see Pantin, 1946), aided by a suitable computer program.

TABLE 1.—The distribution of reticulate cartilage among cephalopods for which histological sections are available (Nixon and Young, in prep.).

Systematic Survey

SUBCLASS NAUTILOIDEA

Nautilus.—Owen (1832:16) described the internal skeleton of the head region of N. pompilius Linnaeus as “incomplete behind and the brain is protected only by its membraneous sheath…. The central mass of the cartilage…is situated on the ventral aspect of the oesophagus.” Later, Keferstein (1862) sectioned the cartilage and illustrated its histological structure, and Griffin (1900) briefly described its morphology.

The cartilage is H-shaped and shows contiguity only with the more ventral parts of the central nervous system; its main relations are with the motor system and the funnel. The anterior pair of projections extend into the funnel and the posterior pair project upward to support the perioesophageal nerve ring. After examining and describing this structure, Willey (1900) commented that the cartilage surrounds no part of the central nervous system, is not perforated by any nerves, and is only traversed by one pair of blood vessels. The cartilage does, however, provide some support for the central nervous system and the statocysts.

ORDER SEPIOIDEA

Spirula spirula (Linnaeus).—The cephalic cartilage was described briefly by Huxley and Pelseneer (1895) and was included in their illustrations of the head region. It is a capsule, enveloping the central nervous system, from which prolongations extend laterally to support the optic lobes. Ventrally and anteriorly, the median projection provides attachment sites for brachial muscles. Anteriorly, the cartilaginous capsule is continued as an envelope of connective tissue at the junction of the pedal and brachial lobes of the brain. Retractor muscles of the funnel attach to the aboral face of the cartilage.

Sepia officinalis.—Early recognition and description of the cephalic cartilage was by Owen (1832:16), who wrote that “in Sepia this cartilaginous part completely encircles the oesophagus and on the dorsal aspect of that tube is dilated into a large cavity, which contains the brain.” Later, the cartilage was isolated and illustrated by Keferstein (1862), who noted foramina for the passage of the nerves, flanges forming cups for the eyes, and statocysts attached posteroventrally.

Tompsett (1939) provided the most detailed description of cephalic cartilage yet available for any cephalopod (Figure 3a). The cephalic cartilage is symmetrical and complicated in form, and it serves for the attachment of the head retractor, the funnel adductor, the oculomotor, and the brachial and tentacular muscles. The orbital cartilages are formed by posterior lateral expansions with thin, wing-like extensions. Anteriorly, a stout, triangular bridge of cartilage unites the orbital cartilages ventrally. From this bridge a pair of delicate, wing-like blades, the trochlear cartilages, project anteriorly and dorsolaterally. Posteriorly, the statocyst cartilage lies between the orbital cartilages. Dorsally, the cerebral cartilage partly encloses the central nervous system and connects the orbital cartilages.

A number of foramina are present of which the single foramen magnum is the largest (Figure 3a). Through it pass the oesophagus, the perioesophageal sinus, the paired buccal arteries, the single duct from the paired posterior salivary glands, the paired visceral and pallial nerves, and the posterior head retractor nerves. The rim of the foramen has slight grooves where the nerves emerge. The remaining foramina are paired, those for the optic nerve being the largest, and they are as follows:

FIGURE 3.—Cephalic cartilage: a, Sepia officinalis, ventral surface (redrawn from Tompsett, 1939); b, Gonatus fabricii, dorsal surface (redrawn from Hoyle, 1889); c, Vampyroteuthis infernalis, ventral surface, with eye remaining in position on one side (optic lobes, oesophagus, and statocysts (dotted outline) remain to show relationships to cartilage (redrawn from R.E. Young, 1964)); d, Eledone cirrhosa, dorsal surface and orbital cartilage (redrawn from Isgrove, 1909). (Abbreviations: c.b., brachial cartilage; c.o., orbital cartilage; c.o.w., wing of orbital cartilage; c.s., statocyst cartilage; c.t., trochlear cartilage; e., eye; f.a.fu., foramen of anterior funnel nerve; f.ol., foramen of olfactory nerve; f.p.fu., foramen of posterior funnel nerve; f.v., foramen for vein from head sinuses to cephalic vein; oe., oesophagus; n.br., brachial nerve; l.op., optic lobe.)

Optic tract foramen (incomplete), which also carries the olfactory, posterior oculomotor, and superior anterior ophthalmic nerves.

Superior posterior ophthalmic nerve foramen, on the posterodorsal surface of the orbit.

Inferior posterior ophthalmic nerve foramen.

Anterior oculomotor nerve foramen, close to the base of the trochlear cartilage.

Olfactory nerve foramen, which passes through the wing of the orbital cartilage.

Anterior funnel nerve foramen, which also carries the anterior funnel artery.

Posterior funnel nerve foramen, near the base of the posterior surface.

Postorbital nerve foramen, on the posterodorsal surface.

Collar nerve foramen, near the emergence of the palliai and posterior head retractor nerves.

Anterior head retractor nerve foramen, near the collar nerve foramen.

Crista nerve foramen and macular nerve foramen, which lead into the statocyst. Two further foramina permit blood vessels to pass through.

Ophthalmic vein foramen, on the posteroventral surface.

Large foramen for the vein from the head sinuses, anteromesial to the ophthalmic vein foramen.

The histological structure of the cartilage of Sepia was described by Nowikoff (1912) and is of typical hyaline form (Table 1). Transmission electron microscopy has revealed a network of collagen fibrils, with well-defined periodic banding, embedded in a great quantity of proteoglycans (Bairati et al., 1987).

ORDER TEUTHOIDEA

SUBORDER MYOPSIDA

A study of the cephalic cartilage, including a morphometric analysis, has been carried out in nine myopsid squids, namely Uroteuthis duvauceli (Orbigny), Doryteuthis plei Blainville, Loligo pealeii, Alloteuthis africana Adam, Loliolus investigatoris Goodrich, Loliopsis diomedeae (Hoyle), and Sepioteuthis sepioidea (Blainville) (deMaintenon, 1990). Anatomical landmarks on the posterior surface of the cranium were used to make a series of measurements. These were analyzed statistically and indicated that the morphology of the cephalic cartilage did differ between the species examined.

Loligo pealeii.—The cephalic cartilage was described by Williams (1909). It has a large foramen magnum through which the oesophagus, visceral nerves, and head arteries pass. Laterally, a concavity provides support for the eyes and the optic lobes. The preorbital cartilages, attached side by side, extend outward and forward between the eyes for attachment of the eye muscles. The statocysts are embedded in a pair of rounded projections posteroventrally.

Two or three pairs of foramina for statocyst nerves pierce the ventral wall of the capsule. A foramen at the edge of the depression for the pedal lobe allows the passage of the crista nerves. Close to this lies the macular nerve foramen. Two pairs of foramina penetrate the cartilage just anterior to the statocysts; one pair for the funnel nerves and the other for veins from the orbital sinuses to the anterior vena cava. The presence of several small foramina to allow the passage of blood vessels and nerves were noted but were not described.

SUBORDER OEGOPSIDA

Gonatus fabricii (Lichtenstein).—Hoyle (1889) illustrated the cephalic cartilage of this oceanic squid after reconstructing its form from serial sections of one specimen and the damaged head of another. The head cartilage resembles an elongated box, open anteriorly and with the statocysts attached posteriorly (Figure 3b). Lateral flanges provide support for the eyes. The cartilage is of the typical hyaline form (Figure 1c, Table 1).

Architeuthis sp.—The head of Architeuthis consists largely of cartilage, on either side of which lie cavities for the eyes and optic lobes. The central nervous system, which is relatively small, proved almost impossible to find and extricate from this massive cartilage (Nixon and Young, in prep.).

Many tissues of Architeuthis float, and analyses have shown an accumulation of ammonium ions so that the animal can achieve near-neutral buoyancy (Denton and Gilpin-Brown, 1973; Clarke et al., 1979). This chemical aid to buoyancy is augmented by reticulate tissues present even in the cephalic cartilage (Figure 2b, Table 1).

Todarodes sagittatus (Lamarck).—Posselt (1891) described the cephalic cartilage of this ommastrephid squid as a transversely oblong, flat, broad cup-shaped ring, with the dorsal and ventral surfaces strongly curved anteriorly, the lateral parts being flat (see also Knudsen and Roeleveld, 1991). There is a large foramen for the passage of the oesophagus, salivary duct, blood vessels, and nerves, and there are openings for the olfactory, collar, and other nerves. The concave anterior and lateral parts of the head cartilage support the eyes with, in addition, two delicate, curved cartilaginous supports on each side.

ORDER VAMPYROMORPHA

Vampyroteuthis infernalis Chun.—The central nervous system is encased on the posterior and ventral surfaces by the cartilage but not on the anterior and dorsal sides (Figure 3c) (R.E. Young, 1964). A foramen magnum, on the posterior surface, allows the oesophagus, major nerves, and arteries to pass through. A foramen for the cephalic vein lies on the ventral surface. Much of the posterior side of the cartilage is occupied by the statocysts. Three projections form the orbital fossa and provide support for the eye. The cartilage itself is reticulate in form (Table 1).

ORDER OCTOPODA

Eledone cirrhosa (Lamarck).—Isgrove (1909:66) described “a tubular cartilaginous capsule, the anterior and posterior ends of which are closed by tough membranes…pierced for the passage of the oesophagus, posterior salivary duct, pharyngeal arteries etc.,” but she did not indicate any foramina in her figure (Figure 3d). Sections of the cartilage were described as being “built up of oval cells surrounded by a clear matrix.” The cells have large oval nuclei and fine cytoplasmic processes that run down canals allowing intercommunication.

The cephalic cartilage of Eledone cirrhosa, E. moschata (Lamarck), and Octopus vulgaris is of the typical hyaline form (Young, 1971).

Discussion

This brief survey of the cephalic cartilage in cephalopods shows, from the most detailed account available, that it is a complex structure with many specialized features. It is difficult to make comparisons but some similarities can be seen in the cephalic cartilage of Vampyroteuthis and Sepia (Figure 3a,c), although the morphological details are insufficient to discuss their relationships. Reconstructions of the central nervous system of Nautilus (Young, 1965), Sepia (Tompsett, 1939), Loligo (Young, 1976), Mastigoteuthis (Young, 1977), Vampyroteuthis (R.E. Young, 1964; Young, 1977), Octopus (J.Z. Young, 1964), and Argonauta (Boycott and Young, 1956), for example, show that the morphology of the brain and the arrangement of the nerves do vary and, by implication, so must the gross morphology of the cephalic cartilage, although this remains to be investigated. The central nervous system differs markedly among the Coleoidea in its size and shape, as well as in the position of its major lobes and the emerging nerves (Nixon and Young, in prep.); by implication there are likely to be considerable variations in the shape and orifices of the cephalic cartilage. The eyes, buccal mass, encircling arms, and other features of the animal vary, as do the position and size of the foramina for the oesophagus and blood vessels in relation to the cephalic cartilage. Morphometric investigations of the relationships between various anatomical features of the cephalic cartilage and of the foramina should prove of value in taxonomic studies.

The cartilage may, or may not, enclose the central nervous system. The H-shaped cartilage of Nautilus lies below part of the ventral surface of the circumoesophageal nerve ring (Young, 1965), and Lankester (1891) named it the capitopedal cartilage. In the coastal coleoids, such as Octopus, Sepia, and Loligo, the cartilage does encase the brain and has been variously called perineural, cephalic, cranial, and head cartilage, and the chondrocranium. Although recognizing these two forms of cartilaginous skeleton associated with the brain, it is proposed that the term cephalic cartilage be used for both and for any new forms that may be found with further investigation.

Recommendations

An initial investigation of the cephalic cartilage as a systematic character should be a comparison of this structure in readily available cephalopods. The gross morphology of this structure in coastal genera, such as Sepia, Loligo, and Octopus, could be described, and selected features could be subjected to morphometric analyses to determine the value of the cephalic cartilage as a systematic character. If it should prove useful, the study could be extended to several genera of the same family and to species of the same genus. The major disadvantage in using the cephalic cartilage is the necessary destruction of the head region in order to extract it without damage.

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The Radulae of Cephalopoda

Marion Nixon

____________

Marion Nixon, 60 Norfolk Road, New Barnet, Herts EN5 5LT, United Kingdom.

ABSTRACT

The radula is described in Nautiloidea and Coleoidea, and a nomenclature is given for the teeth. The developmental changes that occur with growth are followed in the radula of an octopod and a squid. An illustrated survey of radulae belonging to many living Coleoidea shows an increasing complexity in tooth pattern from Sepioidea to Octopoda. The radula can be used to diagnose families, and in the future it could be of use at the generic and species level. It is a conservative character, retaining its two forms of either seven or nine teeth in each transverse row for some 300 million years.

Introduction

The radula is the hallmark of the phylum Mollusca, with the exception of the bivalves (Fretter and Graham, 1962; Boletzky, 1988), and it is the most characteristic feature within the buccal cavity (Figure 1a). Cephalopoda have possessed a radula for at least 400 million years (for reviews see Lehmann, 1981, 1990; Nixon, 1988, 1996).

The few studies of the cephalopod radula available include those of Robson (1925a, 1929) and Adam (1933, 1941, 1986a), who investigated seriation in the rhachidian teeth of several octopods and a sepioid. Naef (1923) described the radulae of numerous cephalopods. The growth of the radula and its teeth has been followed in ontogenetic series of Octopus vulgaris Cuvier and Teuthowenia megalops (Prosch), and morphometric and statistical analyses have been carried out for several parameters (Nixon, 1968a, 1968b, 1969, 1973; Dilly and Nixon, 1976). The diagnostic value of the radula and the structural patterns of the teeth of examples belonging to the major groups of the Cephalopoda have been investigated with the scanning electron microscope (Aldrich et al., 1971; Solem and Roper, 1975).

ACKNOWLEDGMENTS.—I should like to thank C.F.E. Roper and the late G.L. Voss for their kind invitation to the meeting and to thank The Royal Society of London for a travel grant to Washington, D.C.

The Radula

The radula is a ribbon with teeth regularly arranged alongside one another in transverse and longitudinal rows. It consists of a chitin-protein complex (Hunt and Nixon, 1981) that is formed within the radular sac, and it moves forward to the front of the buccal complex where it turns acutely ventroposteriorly at the bending plane (Figure 1a). One transverse row of teeth consists of a central (rachidian) tooth with a series of teeth on either side of it, each series being a mirror image of the other (Figure 1b–d). In Nautiloidea 13 elements, nine teeth and four plates, are present. Members of the Coleoidea generally have nine elements, seven teeth and two plates, although the plates may be present or absent. Exceptions are Spirula spirula (Linnaeus), from which the radula is absent (Kerr, 1931), some deep-sea octopods and cirrate octopods, in which the radula may be present, reduced, or absent (Robson, 1926; Voss, 1988), and species of the genus Gonatus, which have only five teeth in each transverse row (Okutani and Clarke, 1992).

NOMENCLATURE

The teeth and marginal plates of the radula have been given various names during the past century (e.g., see Mehl, 1984). It is proposed that a nomenclature be established for cephalopods, based mainly on that used for gastropod molluscs (Fretter and Graham, 1962). The teeth and marginal plates are named from the center to the periphery of each transverse row. The use of names that relate to the position of the teeth in each transverse row avoids any implications of function, for which there is as yet little evidence (Altman and Nixon, 1970). Furthermore, the names for the nine elements of the coleoid radula can be retained, without alteration, for the nine central elements of the 13 present in the nautiloid radula simply by omitting the two outer elements on either side (Figure 1b–d, Table 1).

FIGURE 1.—a, Diagram of buccal mass of Octopus vulgaris showing main features and position of radula within buccal cavity (bar = 2 mm). (Abbreviations: oes., oesophagus; rad., radula; rad. sac., radular sac). Transverse row of teeth: b, Nautilus macromphalus, 655 g tissue weight (bar= 1 mm), with 13 elements; c, Octopus vulgaris, 90 mm mantle length (bar = 1 mm), with 9 elements; d, Eledonella sp. (bar = 0.1 mm), with 9 elements, showing ctenodont multicuspid teeth. Element abbreviations given in Table 1.

The radula of Nautilus is wide, and its 13 elements are dominated by the relatively large, curved marginal teeth (M1, M2) (Figure 1b). The rachidian tooth and the lateral teeth are small and fairly simple.

In Coleoidea the central rachidian tooth ranges from being relatively tall to short when compared with the remaining teeth in each transverse row. In shape it varies from a simple cone to a central cone with lateral cusps and a distinct basal region, and there are others with teeth that are intermediate between the extremes (Figure 1b–d). The lateral teeth show wide variation, from those that are a simple cone to others that bear several cusps and are comb-like (ctenodont). The marginal teeth are more uniform and resemble a saber or a sickle in shape.

TABLE 1.—The names and abbreviations for the central tooth, lateral teeth, marginal teeth, and marginal plates on one side of the radula.

  Radular element | Abbreviation    
  Rachidian tooth |       R
  Lateral tooth 1 |       L1
  Lateral tooth 2 |       L2
  Marginal tooth 1 |       M1
  Marginal plate 1 |       MP1
  Marginal tooth 2 |       M2
  Marginal plate 2 |       MP2

TABLE 2.—The radula formula for three subclasses of Cephalopoda. Abbreviations are from Table 1.

Taxon | Radula formula
Nautiloidea | MP2 + M2 + MP1 + M1 + L2 + L1 + R
Coleoidea | MP1 + M1 + L2 + L1 + R
Ammonoidea | MP1+ M1 + L2 +L1+ R

A transverse row of teeth repeats in number and shape those in preceding and succeeding rows. This constancy makes it possible to use a formula (with abbreviations for each tooth) to represent the type of teeth in each transverse row, as done in Table 2.

The teeth possess a number of features. The rachidian tooth has a central cusp or cone, the mesocone, which may have one or more lateral cusps on each side (Figure 1c,d). The lateral cusps may show serial repetition as well as asymmetry of arrangement in some members of the Octopodidae (Naef, 1923). Successive rachidian teeth have the cusps on either side arranged in repeated groups of teeth. Figure 7 shows that in a series of rachidian teeth, the lateral cusps shift from a position high on the side of the mesocone downward and outward to become the outermost cusps, or ectocones. The phenomenon of regular changes over several transverse rows of rachidian teeth was called seriation by Robson (1925a). Furthermore, the arrangement of the cusps can be asymmetric, and one or both of these phenomena may be present in some octopods (Robson, 1925a; Adam, 1933, 1941). Robson (1925a) represented the change in position of the cusps by a formula, designating the inner and outer cusps on each side as a and b and the mesocone as I; by further modification this formula could be used to show symmetric and asymmetric seriation.

As the radula and its teeth are subjected to more detailed examination and additional features are found and described, new formulae can be devised or existing ones modified to include the information. For example, the teeth could be shown in order of diminishing height as R > M1 > L2 > L1; the height:width ratio of each tooth may prove useful, and the presence and site of cusps could be indicated for each tooth across a transverse row.

GROWTH AND DEVELOPMENT

Williams (1909:33) observed that in Loligo the teeth are “constantly produced at the base of the radula and gradually push outward until they reach the mouth of the sac.” Thiele (1915) commented on the size of the recently formed teeth compared with the old teeth on the same radula of Bolitaena (Figure 2), and Naef (1921) recognized that the radula grew with the animal. Teeth are added to the radular ribbon continuously, but slowly, by the odontoblasts, which lie at the blind end of the radular sac (Figure 3a,b) (Williams, 1909; Gabe and Prenant, 1957; Raven, 1958; Nixon, 1968a). The rachidian tooth is formed first, followed by the lateral teeth in mediolateral order (Williams, 1909). As the teeth pass forward in the sac, the development of cusps and articular surfaces takes place. The radula is U-shaped in cross section until it reaches the front of the buccal complex, where it spreads laterally, and at the most anterior point it turns acutely over the bending plane (see Nixon, 1988). Shortly beyond the bending plane the radula terminates, enclosed by the subradular gland, and the teeth are shed, presumably by enzymatic action.

ACTIONS OF THE RADULA AND ITS TEETH

The radula and its supporting structure, the buccal complex, undergo regular cycles of activity (Nixon, 1968a; Boyle et al., 1979a, 1979b). During protraction of the buccal complex, the teeth become erect at the bending plane, aligned as a series of spikes across the ribbon, on its anterior edge (Figures 1a, 3c). With relaxation of the buccal complex, the teeth return to their original, folded position. These actions involve spreading, interlocking, and folding of the teeth with the aid of articular surfaces, grooves, and ridges (Figure 4a–e). Ligaments between the bases of the teeth permit the numerous movements of the teeth on the radular ribbon (Figure 4e) (Solem and Roper, 1975).

The articular surfaces of the teeth are readily recognized in the scanning electron micrographs of Figure 4 (especially 4c,f). The convex posterior protuberance of each rachidian tooth fits into the anterior concavity of the one following. This tooth also has articular surfaces that interlock with lateral tooth 1 on either side. The two lateral teeth fold posteromedially toward the rachidian tooth, with which they interlock (Figure 4a). The marginal teeth fold mediolaterally across the lateral teeth and toward the rachidian tooth. Sites of articulation are present on all of the teeth; some may be small, others large. The frequent movement and the actions of the radula during feeding may contribute to the wear and breakage of teeth apparent in the region of, and beyond, the bending plane (Figure 4f). At the distal end of the ribbon, the teeth are finally lost, almost certainly as a result of the action of enzymes presumably secreted by the small subradular gland, which lies at the termination of the ribbon.

The role of the radula has been examined in Octopus vulgaris fed with shore crabs or dead fish in the laboratory (Altman and Nixon, 1970). Surgical ablation of the functional part of the radula, at the bending plane, commonly resulted in a reduction in the ability of the animal to perform the more delicate parts of the cleaning process.

FIGURE 2.—Teeth across one-half of 1 transverse row at distal (below, old and small teeth) and proximal (above, new and larger teeth) ends of various cephalopod radulae (Bolitaena microcotyla redrawn from Thiele, 1915).

FIGURE 3.—a,b, Octopus vulgaris: posterior end of radular sac with odontoblast cells on ventral part of posterior walls (a, bar = 500 μm; b, bar = 50 μm). c, Eledone moschata: radula photographed immediately after isolation of buccal mass and exposed by removal of rostra of upper and lower beaks. Teeth in transverse row at apical tip of bending plane erect, those in following row in a stage of erection (bar = 1 mm).

FIGURE 4.—Octopus vulgaris. Scanning electron micrographs of radulae from specimens of 84 mm (a,d,e), 78 mm (b,c), and 54 mm mantle length (f). Radulae extracted from buccal masses by immersion in sea water, and each prepared and mounted in its natural position on a stub. a, Bending plane showing mode of interlocking of teeth; note posterior convexity of rachidian tooth fits into anterior concavity of tooth immediately following (field width 710 μm). b, Ribbon and teeth, fully formed but not yet at bending plane; note ligaments between succeeding lateral teeth 1 (field width 710 μm). c, Rachidian teeth in region of bending plane exhibiting fracture and wear (field width 380 μm). d, Lateral view of rachidian and 2 lateral and marginal teeth at bending plane (field width 740 μm). e, Ligaments between bases of 2 marginal teeth and tips of 2 adjacent marginal plates (field width 15 μm). f, Distal end of radula with badly worn, fractured, and missing teeth no longer in neatly ordered array seen in (b) (field width 370 μm).

FIGURE 5.—Octopus vulgaris. Rachidian with 2 lateral and marginal teeth from 1 side of radula (all new, fully formed teeth) from ontogenetic series of animals captured in Bay of Naples, Mediterranean Sea, showing tooth growth (bar = 0.5 mm, all drawings at same magnification). Mantle length (mm), total body weight (g) as follows: a. 43 mm, 22 g; b, 53 mm, 50 g; c, 58 mm, 70 g; d, 79 mm, 167 g; e, 84 mm, 238 g; f, 98 mm, 360 g; g, 108 mm, 484 g; h, 126 mm, 750 g; i, 190 mm, 3110 g; j, 198 mm, 4440 g.

Systematic Survey

OCTOPODA

Octopus vulgaris.—At present, most of the information available on radulae is for this species. It has a world-wide distribution between 55°N and 40°S in the coastal waters of the upper continental shelf (Mangold, 1983). The radulae from specimens captured in widely different parts of the world display similar tooth patterns (Figure 6).

The growth, development, and change in size of the radular ribbon and its teeth have been followed in an ontogenetic series of animals captured in the bay of Naples, in the Mediterranean Sea (Figure 5) (Nixon, 1968a, 1968b, 1969, 1973). The teeth increase in size with growth, and the adult cusp pattern is already developed in animals as small as 10 mm mantle length (Figure 6a).

The entire longitudinal row of rachidian teeth from one specimen of 50 mm mantle length is illustrated in Figure 7. Initially the teeth, newly secreted by odontoblast cells, consist of only a base, but development of the mesocone and lateral cusps takes place as the radula moves forward in the radular sac. The first of the fully formed teeth has a sharp outline and is in pristine condition. Further forward, as the teeth approach and pass the bending plane, loss of cones and cusps is apparent, due to fracture and wear. At the distal end of the ribbon, where the oldest teeth are found, teeth may be reduced to the basal portion alone before being lost altogether from the end of the ribbon (Figure 4f), probably after enzymatic action of secretions of the subradular gland. The remains of the teeth at this terminal part of the ribbon are all smaller than the newly formed teeth at the proximal end of the radula and still in the radular sac (Figure 8). The change in size of the teeth along the ribbon is gradual (Figure 9). Various measurements of the ribbon and its teeth show close relationships with the body weight of Octopus vulgaris when tested statistically (Table 3).

FIGURE 6.—Octopus vulgaris: a, Bay of Naples, Mediterranean Sea; b, Sumatra, Indonesia; c, Atlantic coast of Africa. Differences occur mainly in arrangement of cusps on rachidian tooth but are not seen when only 1 rachidian tooth is illustrated because seriation pattern of cusps occurs on successive teeth (redrawn from Adam, 1954 (b); Adam, 1983 (c).

FIGURE 7.—Octopus vulgaris. All of rachidian teeth in central longitudinal row of radula (camera lucida outline drawing) (82 mm mantle length, 167 g body weight, captured in Mediterranean Sea) (bar = 0.2 mm). Proximal, radular sac end at top left and distal, terminal part at bottom right.

TABLE 3.—The correlation coefficient, r, for several parameters of the radula and its teeth in relation to the body weight (g) or mantle length (mm) in an octopod and an oegopsid squid, respectively (for details see Nixon, 1969, 1973; Dilly and Nixon, 1976).

Correlation coefficient (r)

Radular parameter

Octopus vulgaris
(1.1–4440 g)
Teuthowenia megalops
(9–134 mm)

Radula-ribbon length

0.98
0.96

Number of rachidian teeth

0.74
0.37

Proximal width of rachidian teeth

0.92
0.80

Distal width of rachidian teeth

0.97
0.72

FIGURE 8.—Octopus vulgaris: a, teeth at proximal end of radula newly formed, pale staining, in excellent condition, and larger than those at distal end (b) of the same radula; b, oldest part of radula shows wear, fracture, and loss of teeth (bar = 100 μm).

FIGURE 9.—Octopus vulgaris. Base widths of rachidian teeth, measured at 1 mm intervals along entire longitudinal row, from proximal to distal ends of radula, plotted against radula length; plots shown in descending order of mantle length (mm) and body weight (g), number of teeth is in parentheses. (Redrawn from Nixon, 1973.)

Octopus spp.—Radulae from several species of the genus Octopus are shown in Figure 10. Their teeth patterns are similar, but subtle differences are apparent.

The rachidian tooth has a tall mesocone that may be slender or quite stout. The height of the mesocone is usually greater than the width of the base of the tooth. The base can be broad or narrow. The lateral cusps vary in prominence and position on the rachidian tooth; these cusps may occur in a serial order over several teeth, a condition that has been described in a number of octopods (Robson, 1925a, 1929; Adam, 1933, 1941).

Lateral tooth 1 is the smallest tooth in each transverse row. It has a lateral cusp, or ectocone, either prominent or insignificant, that may be sited from the outer margin to almost the center of the tooth.

FIGURE 10.—Octopus spp. One transverse row of radular teeth shown from each of several species (redrawn from Burgess, 1966; Robson, 1929; Stranks, 1988; Taki, 1964; Voss, 1951; Voss and Solis Ramirez, 1966).

Lateral tooth 2 is very broad, and its base is usually wider than that of the rachidian tooth. A major cusp is present near the inner margin of the tooth. A small additional cusp is present on the inner margin of this tooth in Octopus tetricus Gould.

Marginal tooth 1 is a simple, sickle-shaped cone, ranging from robust to slender. This tooth is usually taller than the rachidian, but in some species it is equal in height to the rachidian, and in others it is shorter.

The marginal plate, which is not always present and is often not illustrated, varies from being wide and shallow to being narrow and deep.

In a recent paper Adam (1983:173) wrote: “Finally I believe to have found a reliable character to separate Octopus vulgaris and Octopus burryi in doubtful cases…the second lateral teeth of the radula of Octopus vulgaris show in all examined specimens a distinct ectocone at the base of the inner, whereas in Octopus burryi the inner side of the mesocone of these teeth slopes gradually down to the base without forming an inner cone. Even in very young specimens this difference can be observed.”

Euaxoctopus spp.—The comparison of radulae from a geminate congeneric pair of octopods now living on either side of the Panamanian Isthmus (Voight, 1988) is of special interest. These animals presumably have been separated for some 3–3.5 million years (Jones and Hasson, 1985). Their radulae have the typical octopodine tooth pattern, but differences are apparent (Figure 11). The mesocone of the rachidian tooth of Euaxoctopus panamensis Voss is quite stout, and its height is equal to the width of the base, whereas in E. pillsburyae Voss it is slender, and its height is less than the width of the base. The lateral teeth are more robust in the former than in the latter, and the position of their cusps differ. The marginal tooth of E. panamensis is relatively longer than that of E. pillsburyae. Most notable of all is the difference in the width of the marginal plate in the two species (Voss, 1971, 1975).

FIGURE 11.—a, Euaxoctopus panamensis; b, E. pillsburyae (redrawn from Voss, 1971, 1975).

TEUTHOIDEA

Teuthowenia megalops.—Growth of the radula and its teeth were followed in an ontogenetic series of specimens of this squid (Figure 12) (Dilly and Nixon, 1976; reported as Taonius megalops). It is notable that cusps do not develop on any teeth until a mantle length of about 60 mm is reached. Further development of cusps may take place in animals larger than 134 mm mantle length, but no mature specimens were available (Voss, 1988, reported on a number of mature animals). Several parameters of the radula show a close relationship with mantle length (Table 3).

FIGURE 12.—Teuthowenia megalops. Teeth of right side of radula and rachidian tooth of transverse row 8, numbered from proximal end of radula (mantle length, in mm, at left) (bar = 1 mm).

Enoploteuthis spp.—The radulae from several species of this genus display both similarities and differences in their tooth patterns (Figure 13). The rachidian tooth is usually shorter than the marginal tooth, although in Enoploteuthis anapsis Roper their height is almost equal. Lateral cusps can be either prominent or hardly apparent on the rachidian teeth. Lateral tooth 1 is usually shorter than lateral tooth 2, but in some species they are of almost equal height. The teeth of E. leptura (Leach) differ markedly in being slender and delicate in comparison with the others illustrated herein.

Comparative Survey

COLEOIDEA

The radulae from many living genera are shown in Figure 15. There is a trend of increasing complexity in the tooth pattern from the Sepioidea to the Octopoda. The greatest variety is seen in the Octopoda, including the most bizarre radula yet described, that of Vosseledone charrua Palacio (Palacio, 1978). Other members of the Octopoda show reduction or loss of teeth. In marked contrast three families of octopods, the Bolitaenidae, Amphitretidae, and Idioctopodidae, possess broad, multicuspid teeth (Robson, 1932).

The tooth pattern shows similarities within families (for example the Loliginidae, Figure 15), confirming previous findings (Aldrich et al., 1971; Solem and Roper, 1975).

NAUTILOIDEA

Nautilus is the only living representative of this subclass, and its radula possesses 13 elements (Figure 1b), four more than are present in members of the subclass Coleoidea.

FOSSIL FORMS

Paleocadmus herdinae Solem and Richardson and P. pohli Saunders and Richardson have radulae with distinct similarities, in the number as well as in the shape and form of the teeth, to the radulae of modern Nautilus (Solem and Richardson, 1975; Saunders and Richardson, 1979) (Figures 1b, 14). The radula of Paleocadmus has nine teeth and so is quite different from those found in ammonoid fossils, which possess only seven teeth (Figure 14).

The remaining radulae figured have seven teeth and belong to members of the Ammonoidea (see Lehmann, 1981; Nixon, 1988). The radula of another ammonoid, Aconeceras, has seven teeth, and notably the central and the lateral teeth have numerous cusps and are comb-like, whereas the marginal teeth are exceedingly long (about 3.5 times the length of the rachidian tooth) (Doguzhaeva and Mutvei, 1991).

FIGURE 13.—Enoploteuthis spp. Teeth from 1 side of 1 transverse row, with rachidian tooth from 8 species (redrawn from Roper, 1966 (a,d); Burgess, 1982 (b,c,e-g); Taki, 1964 (h)).

The oldest radula yet described is that of Michelinoceras, an orthocerid belonging to the Nautiloidea (Mehl, 1984). Seven teeth are present, and their shape and form are reminiscent of those of a nautiloid radula, but the small lateral teeth are apparently absent. It is possible that these small teeth and any marginal plates that may have been present were crushed or disintegrated during fossilization.

FIGURE 14.—Nautiloidea and Ammonoidea. Teeth from 1 side of 1 transverse row, with rachidian tooth, all of fossil forms. Numbers in parentheses = millions of years before present (redrawn from Lehmann, 1981 (a-d); Saunders and Richardson, 1979 (f,g); Mehl, 1984, (h)).

Discussion

Little is now known about the radula apart from the shape and form of the teeth, as, usually, only one row is depicted in taxonomic descriptions. Only rarely, however, is there any indication of which transverse row has been illustrated, and the magnification is usually omitted. The value of the radula as a taxonomic character will be understood only after detailed morphometric studies in ontogenetic series of numerous species have been carried out.

The teeth of the radula are varied in shape and form and possess numerous features, some of which may prove to be characteristic. Many of these features also lend themselves to measurements, proportional ratios, and statistical analyses. Further morphometric studies, like those for Octopus vulgaris (Nixon 1968a, 1968b, 1969, 1973) and Teuthowenia megalops (Dilly and Nixon, 1976), but extended to include many more details, would provide a foundation for the use of the radula as a diagnostic character. Light and scanning electron microscopical studies have already demonstrated the use of the radula as a systematic character in several families (Aldrich, 1969; Aldrich et al., 1971; Solem and Roper, 1975). Further investigations may indicate whether the radula can be used at the generic and even specific level for identification purposes. There is, however, a major disadvantage in its use, especially in the field, and that is the need to extract and prepare the radula before it is possible to magnify the small teeth sufficiently to visualize their diagnostic features.

FIGURE 15.—Coleoidea radulae from representatives of major groups. Species illustrated (source of figures in parentheses; figures without source original). a: Sepia officinalis; Sepiella cyanea (Robson, 1924); Sepioloidea pacifica (Dell, 1952); Rossia antillensis (Voss, 1956); Heteroteuthis tenera (Verrill, 1879); Euprymna stendodactyla (Adam, 1986b); Sepietta sp.; Rondeletiola sp.; Idiosepius sp.; Loligo vulgaris; Doryteuthis sibogae (Adam, 1954); Lolliguncula argus (Brakoniecki and Roper, 1985); Sepioteuthis bilineata (Dell, 1952); Alloteuthis subulata; Uroteuthis bartschi; Loliolus investigatoris (Adam, 1954); Enigmoteuthis dubia (Adam, 1973); Enoploteuthis anapsis (Roper, 1966); Abralia similis (Okutani and Tsuchiya, 1987); Pterygioteuthis giardi (Hoyle, 1904); Octopoteuthis (Rancurel, 1970). b: Onychoteuthis banksii (Adam, 1952); Onykia japonioca (Taki, 1964); Ancistroteuthis (Rancurel, 1970); Moroteuthis pacifica (Okutani, 1983); Cycloteuthis sirventi, Discoteuthis discus (Young and Roper, 1969a); Gonatus fabricii (Kristensen, 1981); Psychroteuthis (Thiele, 1925); Pholidoteuthis adami (Voss, 1956); Architeuthis sp. (Roper and Boss, 1982); Histioteuthis dofleini (Voss, 1969); Neoteuthis thielei (Adam, 1983); Bathyteuthis abyssicola (Roper, 1969); Ctenopteryx (Rancurel, 1970); Brachioteuthis beanii (Verrill, 1879); Batoteuthis skolops (Young and Roper, 1968); Illex coindetii; Todaropsis eblanae; Nototodarus sloanii (Dell, 1952); Ommastrephes sp.; Ornithoteuthis antillarum (Voss, 1957). c: Hyaloteuthis pelagica; Thysanoteuthis rhombus; Chiroteuthis veranyi (Naef, 1923); Valbyteuthis danae (Roper and Young, 1967); Mastigoteuthis cordiformis (Adam, 1954); Promachoteuthis sp. (Roper and Young, 1968); Joubiniteuthis portieri (Young and Roper, 1969b); Cranchia scabra (Robson, 1924); Liocranchia sp.; Teuthowenia sp.; Galiteuthis glacialis (McSweeny, 1978); Mesonychoteuthis hamiltoni (Robson, 1925b); Vampyroteuthis infernalis; Grimpoteuthis sp. (Voss, 1988); Japetella diaphana; Eledonella pygmaea; Dorsopsis taningia (Thore, 1949); Amphitretus thielei (Thore, 1949); Idioctopus gracilipes (Taki, 1963); Vitreledonella; Octopus sp. d: Enteroctopus megalocyathus (Robson, 1929); Robsonella australis (Dell, 1952); Pteroctopus tetracirrhus; Hapalochlaena maculosa (Adam, 1954); Berrya hoylei (Taki, 1963); Euaxoctopus panamensis (Voss, 1971); Benthoctopus sp. (Adam, 1954); Teretoctopus indicus (Robson, 1932); Bathypolypus arcticus (Perez-Gandaras and Guerra, 1978); Pareledone turqueti (Robson, 1932); Eledone moschata; Vosseledone charrua (Palacio, 1978); Velodona togata (Voss, 1988); Tetracheledone sp.; Thaumeledone sp. (Robson, 1932); Bentheledone rotunda (Robson, 1932); Graneledone (Voss, 1976); Tremoctopus violaceus; Ocythoe tuberculata; Argonauta argo; Alloposus mollis.

The radula is protected within the buccal cavity by the surrounding beak, and, like the beak, it is formed of chitin-protein complexes (Hunt and Nixon, 1981). This material is an important contributing factor to the resistance of the radula to break down under adverse external conditions, such as those encountered during capture (whether by predators or mechanically by man), digestive processes, or fossilization. The teeth survive such insults, making the radula a valuable character especially under circumstances where most of the animal's soft tissues have been lost.

There is now evidence that cephalopods have possessed a radula for at least 400 million years (Mehl, 1984). For at least 290 million years, two forms have existed, the nautiloid with 13 elements and the ammonoid and coleoid both with nine elements. This shows the radula to be an ancient and conservative character. Furthermore, its conservation may, as more evidence becomes available, allow relationships to be traced from fossil to recent forms, and so help toward evaluating evolutionary trends in Cephalopoda.

Recommendations

An outline drawing of at least one transverse row of teeth should be included with a description whenever possible. The tooth row selected should be of the most recent but fully formed teeth, those lying just beyond the radulogenic region of the radular sac. Drawings made with the aid of a camera lucida provide an excellent record. Scanning electron micrographs give greater detail, especially of individual teeth and their articular surfaces, but do not necessarily aid in elucidating the tooth pattern. Furthermore, this method is both time consuming and expensive when compared with that needed for simple outline drawings. It is essential that a scale, or magnification, accompanies all illustrations of the radula, as well as the mantle length of the animal from which it was extracted.

Morphometric studies of the radula should be carried out first on ontogenetic series of one species to determine the degree of individual variation. This type of investigation could then be extended to include all species of one family to ascertain its use as a diagnostic character and, if proved valuable, then extended to other families. A digitizing tablet may help in such investigations, and its use has been discussed by Clarke (1998).

Investigation of the radula in species with world-wide distributions may be of special interest, and certainly examination of the radula of other geminate congeneric pairs of cephalopods (Voight, 1988) should prove most exciting.

Literature Cited

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1941.   Notes sur les Céphalopodes, XV; Sur la valeur diagnostic de la radule chez les Cephalopodes Octopodes. Bulletin du Musée Royal d'Histoire Naturelle de Belgique, 17:1–19.

1952.   Cephalopodes. Résultats Scientifiques, Expédition Océanographique Belge dans les Eaux Côtiéres Africaines de I Atlantique Sud (1948–1949), 3:1–142.

1954.   Cephalopoda, 3e partie, IV: Céphalopodes à l'exclusion des genres Sepia, Sepiella et Sepioteuthis. Siboga-Expeditie, 55c: 123–193.

1973.   Cephalopoda from the Red Sea: Contributions to Knowledge of the Red Sea Number 47. Bulletin of the Sea Fisheries Research Station, Haifa, 60:9–47.

1983.   Cephalopoda from West and South Africa. Atlantide Report. 13:151–180.

1986a. La radule et les mandibules de quelques espéces d'Idiosepius Steenstrup, 1881 (Mollusca: Cephalopoda: Decapoda). Bulletin de l'Institut Royal des Sciences Naturelles de Belgique. Biologie. 56:149–154.

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The Gladius in Teuthoid Systematics

Ronald B. Toll

____________

Ronald B. Toll, Department of Biology, Wesleyan College, Macon, Georgia 31297-4299, United States.

ABSTRACT

A review of the historic use, current state of knowledge, and systematic value of the morphology of the teuthoid gladius is presented. Variation in gladius morphology across the order Teuthoidea is assessed in terms of current family-level classification. Techniques are given for gladius extraction and examination along with a glossary of standard measurements used in the systematic analysis of gladius morphology. Advantages and disadvantages relating to the use of the gladius as a systematic character are discussed. Finally, suggestions for future avenues of investigation of the teuthoid gladius are offered.

Introduction

The teuthoid gladius is a chitinous, spatulate structure that extends along the dorsal midline of squids beneath or partially embedded within the dorsal mantle musculature. Evolutionarily, the gladius is derived from the proostracum portion of the ancestral coleoid shell (Jeletzky, 1966). Vestiges of the ancestral conotheca are found in some Recent gladii. Most gladii are composed of two major components, the rachis and the vanes; both are variously modified across the order Teuthoidea. The rachis is the central axis of the gladius and typically extends along its entire length. The rachis can consist of one, two, or three primary longitudinal axes, arranged in various combinations, or can form a thin to thick medial, ventrally excavated channel with or without a dorsal keel. The vanes are thin lateral extensions of the rachis. Typically they are concave ventrally and display a diverse range of shapes across the Teuthoidea. Vanes are normally absent from the anterior portion of the rachis, which is called the free rachis. Posteriorly, the gladii of the majority of teuthoids terminate in one of a number of hollow conical, cup-shaped, or attenuate needle-shaped structures collectively referred to as conuses.

Three types of conuses were categorized by Toll (1982), the primary conus, secondary conus, and pseudoconus. The primary conus is small; its ventral length is rarely greater than 6% of the gladius length. This conus type is cup-shaped to slightly conical with a straight to broadly U-shaped ventral rim. The primary conus is found in association with the conus field, a laterally expanded posterior portion of the gladius that is, in some taxa, broadly contiguous with the vanes and usually set off from them by a pair of bilaterally symmetrical, oblique, longitudinal axes. In some taxa the conus field extends anteriorly, lateral and adjacent to the vanes. At least seven families of teuthoids, most notably the Ommastrephidae, Onychotcuthidac, Lycotcuthidae, and Gonatidae, are characterized as having a primary conus as part of the adult gladius. In other families a primary conus is associated with the paralarval or early juvenile gladius but is lost, presumably by overgrowth, during later ontogeny (e.g., Thysanoteuthidae). The secondary conus is long (ventral length from about 20% to over 50% (rarely as small as 8%) of the gladius length) and narrow and conical to filiform. It can be round, oval, triangular, or rectangular in cross section. Typically, the secondary conus is a broadly contiguous posterior extension of the vanes formed by the ventral flexion and fusion of the vanes along the ventral midline. The secondary-type conus is found in at least 10 teuthoid families and reaches its greatest development in the Mastigoteuthidae, Chiroteuthidae, Batoteuthidae, Joubiniteuthidae, and six genera of Cranchiidae. The pseudoconus is similarly formed by the ventral flexion of the posterolateral edges of the vanes but with the free edges approximating along or overlapping across the ventral midline. Fusion occurs occasionally but only in the posteriormost portion. The pseudoconus is found exclusively in six genera of cranchiids.

Rostrum-like structures occur as part of the gladius in some taxa with a primary conus (Toll, 1982, unpublished data). Similar to the guards, tela, and guard-like sheaths of the fossil Belemnitida, Aulacocerida, and Sepiida, respectively (see Jeletzky, 1966), modern rostrum-like structures are layered, solid, conical structures that extend from the posterior end of the gladius. The conus of the gladius rests in a matching conical depression in the anteroventral surface of the rostrum-like structure. The homology of rostrum-like structures is unknown.

The gladius is formed by successive deposition of chitin layers by the shell sac, a secretory endothelium that develops early in ontogenesis. The membranous shell sac forms an envelope that completely encloses the gladius. The shell sac also is the actual insertion layer for muscles upon the gladius. Various aspects of the teuthoid gladius have been discussed elsewhere, and interested readers are directed to those works: functional morphology (Toll, 1988); paleontology and evolution (Jeletzky, 1966; Donovan, 1977; Donovan and Toll, 1988); chemical composition (Lotmar and Picken, 1950; Rudall, 1955; Pervaiz and Abdul Haleem, 1975).

ACKNOWLEDGMENTS.—The late Gilbert L. Voss provided material for study and lent extensive encouragement and advice during the course of the study. Discussions with Richard E. Young, Stephen C. Hess, and Clyde F.E. Roper were of great value. Richard E. Young kindly provided unpublished data on the condition of the conus field in some taxa and made numerous constructive comments on an earlier draft of this manuscript. Clyde F.E. Roper, Michael Sweeney, and the staff of the Division of Mollusks assisted me during several visits to the National Museum of Natural History, which were supported in part by a Dissertation Improvement Grant (DEB–8012544) from the National Science Foundation and a Visiting Graduate Student Award from the Smithsonian Institution Office of Fellowships and Grants. George Davis and Robert Robertson made possible and assisted me during a visit to the Academy of Natural Sciences of Philadelphia, which was supported by a grant from the Jessup-McHenry Fund of the Academy. Ruth Turner assisted me during my stay at the Museum of Comparative Zoology, Harvard University, which was supported by a grant from the Lerner Fund for Marine Research (#5–19–80; 103045). The larger study of teuthoid gladii, of which this contribution is a part, also was supported in part by grants from the Bader Fund of the Rosenstiel School of Marine and Atmospheric Science, National Capital and Astronaut Trail shell clubs, and Key Biscayne Women's Club. Laura Bybee produced the photographic prints of most of the figures. I gratefully acknowledge the support provided to me from these many persons and institutions.

Historical Résumé

Current knowledge of the Recent teuthoid gladius is based on a few comparative monographic works, one specifically on the gladius, and on a large, somewhat diffuse body of literature pertaining to teuthoid systematics in general. Inclusion of the gladius in systematic studies has reflected the varying opinions of individual investigators regarding its systematic value, the uniqueness of the specimen(s) at hand, and previous records of the gladius from that particular taxon or closely related ones. The résumé below reflects those contributions that have made significant advances to our understanding of the gladius and several others that are significant historically.

Recorded study of the teuthoid gladius begins with Aristotle's Historia Animalium, wherein it is noted that squids possess a slim, horny pen, in contrast to the cuttlebone of the sepiids (Thompson, 1913; Gerhardt, 1966). During the middle ages, Redi (1684) and Lister (1692) provided stylized illustrations of the gladii of Loligo sp. and ?Alloteuthis sp. The first significant post-Linnean references to the teuthoid gladius are those by Lesueur (1821, 1824), who illustrated the gladii of eight species. Lesueur's accounts of teuthoid gladii are among the earliest to include examination of cross sections.

The beginning of the modern era of cephalopod systematics arguably can be traced to 1834 and the commencement of publication of the monographic work Céphalopodes Acétabulifères by Férussac and d'Orbigny (1834–1848), wherein the gladii of more than 30 species representing nine families of teuthoids were described, many with illustrations. Notable aspects of those accounts include determination of sexual dimorphism in the gladius of Loligo vulgaris Lamarck and post mortem discoloration of gladii.

The monographic works by Verany (1851) and Tryon (1879) added detailed information on comparative morphology of the gladius. Verany (1851:114) included mention of a “second ventral shell” in the gladius of Histioteuthis bonnellii (Férussac), now recognized as the gelatinous material regularly found within the ventral concavity of the rachis and vanes from histioteuthids and several other families. With respect to the loliginids, Tryon (1879) correctly cautioned against the use of minor differences in gladius morphology for establishing taxonomic distinctions among species.

Verrill's (1882:4) treatise is one of the first accounts to include detailed morphometric data on gladii. In particular, he noted, “The size and shape of the thin internal ‘bone’ or ‘pen’ is particularly desirable [for systematic study].” As part of an extensive anatomical account of Gonatus fabricii (Lichtenstein), Hoyle (1889) gave one of the most detailed descriptions of the gladius from any one taxon. His account included anatomical relationships of the gladius with respect to the surrounding mantle musculature and visceral sac.

The following four decades witnessed the publication of several monographic works on teuthoid systematics. Jatta (1896) included aspects of gladius morphology among a list of characters useful in teuthoid identification and in tabular diagnoses at the familial and subfamilial levels. Chun (1910:17) acknowledged that “the systematic importance of the gladius has been stressed by all earlier authors” and provided detailed drawings and descriptions of gladii from several species then poorly known. Pfeffer (1912) described the gladii from more than 25 teuthoid taxa. For many of these he also provided detailed illustrations, some with cross- and sagittal-section views. Naef (1921, 1923) devoted considerable attention to the Recent gladius and its antecedents as part of a hypothetical reconstruction of the fossil lineage of the modern teuthoids. Sasaki (1929) described the gladii from about 40 species.

Beginning with Voss (1962), a series of monographic familial revisions were produced by several authors. These were often based on large collections of comparative material that allowed evaluation of the comparative usefulness of various systematic characters, including the gladius. These monographs include Voss (1962, Lycoteuthidae), Young and Roper (1968, Batoteuthidae), Roper and Young (1968, Promachoteuthidae), Young and Roper (1969a, Cycloteuthidae; 1969b, Joubiniteuthidae), Roper (1969, Bathyteuthidae), and Voss (1969, Histioteuthidae; 1980, Cranchiidae). Toll (1982) comparatively surveyed the gladius across the Teuthoidea based on over 130 species representing all recognized families of squids. His results supported previous contentions that the gladius is a primary teuthoid systematic structure and included delineation of characters and character states, preliminary analyses of variability, and an evaluation of the usefulness of the gladius for systematics and phylogenetic reconstructions of the Teuthoidea.

Methods

The majority of information on the teuthoid gladius has been obtained from examples removed from preserved museum specimens. Gladii can be extracted from preserved material in two ways. The majority of gladii can be most easily removed via the ventral extraction method, begun by making an incision completely through the mantle wall along the entire ventral midline from the mantle aperture to the tip of the tail. The left gill should be severed from the mantle by cutting the gill-supporting membrane; the left stellate ganglion can be severed either proximally or distally. The visceral mass can then be rolled to the right to gain access to the shell sac containing the gladius. Beginning anteriorly and working in a posterior direction, the left edge of the shell sac should be cut and the free edges teased open to expose the gladius. Depending on taxon-specific anatomical relationships of the gladius to the the dorsal mantle musculature, the nuchal musculature and cartilage, and the tail and fin complexes, additional muscle attachments to the shell sac and overburdening muscles occasionally need to be severed in order to free the gladius completely. When freed, the gladius can be slid out to the left. Damage to the gladius incurred during capture or due to chemical preservation can require that the fragmented gladius be extracted and reconstructed following removal. With the gladius removed, the visceral mass can be rolled back to its normal position, leaving the specimen nearly intact.

In those taxa in which the dorsal mantle wall is bisected by a highly keeled rachis (e.g., Onychoteuthis), it can be useful to remove the gladius via a midsagittal incision through the dorsal mantle musculature. In order to avoid damage, extreme care must be exercised to free the entire gladius, including the delicate lateral portions of the vanes, prior to lifting the gladius straight up and out of the mantle.

A variety of morphometric data can be obtained from gladii depending on their overall shape and the presence of associated structures. The basic measurements obtainable from nearly all gladii are as follows (Figure 1):

Gladius Length (GL). The total length of the gladius measured from the anterior limit of the rachis (free rachis) to the posterior tip of the vanes, conus, or rostrum-like structure.

Free Rachis Length (FRL). The distance from the anterior tip of the free rachis to the anteriormost limit of the vane insertions.

Free Rachis Width (FRW). In those gladii in which the free rachis tapers anteriorly, the distance across the free rachis at the level of the anteriormost limit of the vane extensions measured perpendicular to the long axis of the gladius.

Gladius Width (GW). The greatest width across the vanes measured perpendicular to the long axis of the gladius.

In those gladii wherein the vanes are expanded anteriorly and posteriorly and are constricted medially, additional vane measurements should be taken as follows (Figure 2):

Vane Length Anterior (VLant). The length of the anterior expanded section of the vanes from the anterior limit of the vane insertions to the level of the narrowest point along the midsection of the vanes, measured along the long axis of the gladius.

Vane Length Posterior (VLpost). The length of the posterior expanded section of the vanes from the level of the narrowest point along the midsection of the vanes to their posterior limit, measured along the long axis of the gladius.

Gladius Width Anterior (GWant). The greatest width across the anterior expanded section of the vanes measured perpendicular to the long axis of the gladius.

Gladius Width Middle (GWmid). The least distance across the tapered midsection of the vanes, measured perpendicular to the long axis of the gladius.

Gladius Width Posterior (GWpost). The greatest width across the posterior expanded section of the vanes measured perpendicular to the long axis of the gladius.

In those gladii with some form of conus (primary, secondary, or pseudoconus), the following additional measurements should be taken (Figure 1):

Conus Length (CL). The length of the conus from its ventral rim to its posterior tip measured along the long axis of the gladius.

Conus Width (CW). The distance across the conus measured perpendicularly to the long axis of the gladius and intersecting the midventral anterior limit of the ventral rim of the conus.

FIGURES 1–3.—Hypothetical, stylized gladii showing standard measurements (see text for glossary).

In those gladii with a conus field, the following additional measurements should be taken (Figure 3):

Conus Field Length (CFL). The distance from the posterior tip of the conus to the anterior limit of the conus field (sometimes delineated by an oblique thickened axis, distinct narrowing of the gladius, or change in the orientation of the incremental growth lines) measured parallel to the long axis of the gladius.

Conus Field Width (CFW). The greatest distance across the conus field measured perpendicular to the long axis of the gladius.

In those gladii with a rostrum-like structure, the following measurements can be obtained (Figure 3):

Rostrum-like Structure Ventral Length (RVL). The distance from the midventral anterior rim of the concavity of the rostrum-like structure (containing the conus) to its posterior tip measured along its long axis.

Rostrum-like Structure Width (RSW). The greatest width of the rostrum-like structure measured perpendicular to its long axis.

In those gladii in which the free rachis broadens anteriorly, the following measurement should be taken in addition to FRW as defined above (Figure 2):

Free Rachis Width Anterior (FRWant). The greatest distance across the anterior expanded region of the free rachis measured perpendicular to the long axis of the gladius.

In those gladii in which the free rachis is tapered medially and broadens both anteriorly and posteriorly, the following measurements should be taken in addition to FRWant as defined above (Figure 3):

Free Rachis Width Middle (FRWmid). The least distance across the tapered middle region of the free rachis measured perpendicularly to the long axis of the gladius.

Free Rachis Width Posterior (FRWpost). The distance across the free rachis at the level of the anteriormost point of the vane extensions, measured perpendicularly to the long axis of the gladius.

In addition to morphometric data, notes reflecting details of the shape and construction of gladii should be taken. Features that should be examined include the degree of demarcation of the insertion of the vanes upon the rachis (distinct, indistinct), shape of the anterior shoulders of the vanes (concave, convex, scalloped), occurrence of axial ribs or bands along the vanes, and structure of the free rachis and rachis (number and placement of axial ribs, cross-sectional shape, etc.).

Systematic Analysis

Knowledge of the teuthoid gladius from most taxa remains incomplete. Although preliminary data suggest that the gladius is a primary structure in the systematic study of the Teuthoidea, its value appears to vary among taxa. In addition, assessment of the systematic value of the gladius cannot be made in isolation; rather, it must be made in terms of a comparison with classifications based on a synthesis of other characters. Typically, the basic shape of the teuthoid gladius is organized at either the generic or the familial level. All figures presented herein are taken from Toll (1982) and depict the overall shape and construction for representative species in all currently recognized families of squids. All figures are oriented in the same manner, ventral whole view with representative cross sections, and are drawn to the same size to facilitate direct comparisons among taxa. For a more complete systematic treatment of the teuthoid gladius, see Toll (1982).

At present, the higher-level classification within the Teuthoidea is not stable. The most recent listing of family-level taxa is that of Clarke and Trueman (1988), which includes 28 family-level taxa. One of these, the Grimalditeuthidae, later was placed in the Chiroteuthidae by Young (1992) as a genus-level taxon, thereby reducing the total of family-level taxa to 27. Of these, seven are currently monospecific: Pickfordiateuthidae, Batoteuthidae, Joubiniteuthidae, Thysanoteuthidae, Psychroteuthidae, Ancistrocheiridae, and Lepidoteuthidae (but see below). Each of these families has a unique gladius that is readily distinguishable from that of all other teuthoid taxa. The gladius of the Thysanoteuthidae (Figure 4) is the most distinctive and most easily recognized of all teuthoids; the anterior region of the vanes is modified into a pair of anteriorly projecting, free, subquadrangular lobes separated from the free rachis by well-formed hyperbolar zones (reentrants), reminiscent of the similar condition typical of the fossil order Loligosepiidae. The pickfordiateuthid gladius (Figure 5) is spoon-shaped and exceptionally broad. Taken together the vanes are acorn-shaped. The rachis is V-shaped in cross section and thickened throughout. Although the pickfordiateuthid gladius bears some resemblance to those of the Bathyteuthidae and Chtenopterygiidae (see below), it can be readily distinguished from the former by the structure of the rachis and from the latter by vane shape and free-rachis length. The gladius of the Ancistrocheiridae (Figures 6, 7) is relatively broad throughout, with a short, very broad free rachis. The primary conus is small. A small and slender but well-formed, rostrum-like structure is present. The gladii of the Batoteuthidae (Figures 8, 9) and Joubiniteuthidae (Figures 10, 11) are very narrow to filiform with long free rachises and secondary conuses. The rachis of the Batoteuthidae is a U-shaped channel bordered laterally by a pair of thickened axes. That of the Joubiniteuthidae is thickened throughout and strongly folded ventrally to where the free edges nearly meet to form a tube. The gladius of the Joubiniteuthidae is unique in the development of thickened, ventrolateral axes along the secondary conus, particularly along its anterior region. The gladius of the Lepidoteuthidae (Figure 12) is strongly constricted medially, has a secondary conus, and contains a “cartilaginous” axial rod within the ventral concavity of the rachis (Clarke and Maul, 1962; Toll, 1982) (see also Pholidoteuthidae, below). The gladius of the Psychroteuthidae (Figure 13) has long vanes that are widest in the anterior one-fifth to one-sixth of their length and taper regularly posteriorly. A small, concentrically coiled structure, similar to the medial portion of the histioteuthid cupped coil (see below), is contained within the exceptionally small secondary conus.

Three families that vary widely in number of species each have a unique, highly conservative gladius shape: Ommastrephidae (over 20 species), Bathyteuthidae (4 species (includes 1 undescribed species)), and Octopoteuthidae (about 5 species). Toll (1990) has shown that the exceptionally long free rachis of the ommastrephid gladius (Figure 14) has a complex cross-sectional structure that comprises numerous characters. Several generic groupings based on these characters are congruent with clades based on a large set of traditional soft tissue characters. Gladius morphology, however, does not support the currently accepted subfamilial classification Ommastrephinae, Illicinae, and Todarodinae. The unique gladius of Dosidicus gigas has a domed, layered mound of chitin that nearly fills the concavity of the conus. The bathyteuthid gladius is spoon-shaped (Figure 15) with a long free rachis composed of a thin, U-shaped median field bordered laterally by a pair of rod-like axes. The gladius of Bathyteuthis sp. A can be readily distinguished from those of the other bathyteuthids by the vane length, which is relatively greater than those of the other three taxa. The octopoteuthid gladius (Figure 16) is easily recognized based on a combination of characters that include exceptional thinness and general flaccidity of the vanes, short free rachis poorly demarcated from the anterior vane insertions, and exceptionally small secondary conus.

The gladius of the Loliginidae (Figures 17, 18) exhibits a wide range of variation across the family, and, with the exception of Sepioteuthis, generic groupings based on gladius morphology are difficult to establish. Concomitantly, the generic-level classification of the loliginids is a matter of considerable recent debate (see Vecchione et al., 1998.) Species of Sepioteuthis cannot be distinguished based on the gladius alone. In some cases, however, pairs of species in other genera that are sometimes confused based on other characters can be separated using the gladius. For example, Loligo pealeii and Doryteuthis plei can be distinguished based on the shape of the anterior vane shoulders immediately posterior to their insertions into the rachis (concave or convex, respectively, see arrows Figures 17, 18) and on the relative width of the gladius with respect to the free rachis width (above or below the critical value of 2.4, respectively). Toll (1982) indicated that the gladii of Loliolopsis diomedeae Hoyle and Lolliguncula spp. were similar in many regards and that these similarities suggest that the two genera were closely related. This assertion was supported by Brakoniecki (1986) who placed the former within Lolliguncula.

FIGURES 4–16.—4, Thysanoteuthis rhombus (Thysanoteuthidae), ventral whole view of gladius (188 mm GL). 5, Pickfordiateuthis pulchella (Pickfordiateuthidae), ventral whole view of gladius (∼22 mm GL). 6, 7, Ancistrocheirus lesueuri (Ancistrocheiridae): 6, ventral whole view of gladius (∼158 mm GL); 7, ventral view of posterior portion of gladius showing conus and rostrum (∼260 mm GL). 8, 9, Batoteuthis skolops (Batoteuthidae): 8, ventral whole view of gladius (∼151 mm GL); 9, cross section of conus immediately posterior to rim. 10, 11, Joubiniteuthis portieri (Joubiniteuthidae): 10, ventral whole view of gladius (195+ mm GL); 11, cross section of conus immediately posterior to rim. 12, Lepidoteuthis grimaldi (Lepidoteuthidae), ventral whole view of gladius (617 mm GL). 13, Psychroteuthis glacialis (Psychroteuthidae), ventral whole view of gladius (168 mm GL). 14, Sthenoteuthis pteropus (Ommastrephidae), ventral whole view of gladius (244 mm GL). 15, Bathyteuthis sp. A (Bathyteuthidae), ventral whole view of gladius (57 mm GL). 16, Octopoteuthis deletron (Octopoteuthidae), ventral whole view of gladius (90 mm GL).

Mastigoteuthid gladii also display a high degree of intrafamilial variation with regard to the length and width of the free rachis and the width of the vanes. All mastigoteuthid gladii have a long secondary conus. Intrafamilial variation, in part, is correlated with fin-complex morphology. Mastigoteuthis hjorti Chun (Figure 19) and M. cordiformis Chun have broad, sturdy gladii and large, massive fin complexes that extend along a large percentage of the mantle. Mastigoteuthis famelica (Berry) has an exceptionally slender gladius and a relatively small terminal-fin complex. The gladii of most of the nominal species of mastigoteuthids remain unknown.

The gladius of the Chiroteuthidae (Figure 20) is narrow with a long, slender free rachis that is expanded distinctly anteriorly. The secondary conus is long, attenuate, and rectangular to triangular in cross section with a small, rectangular to circular dorsal keel. Gladius morphology supports the recent inclusion of Grimalditeuthis into the Chiroteuthidae (see Young, 1992).

The gladii of several families of teuthoids are poorly known from few specimens; therefore, our current knowledge of the gladius is limited. Concomitantly, these families, Architeuthidae, Promachoteuthidae, Brachioteuthidae, and Neoteuthidae, are in need of systematic revision. With few exceptions, all known architeuthid gladii (Figure 21) display a pronounced reduction of the rachis along the majority of the length of the gladius. The gladius of the Promachoteuthidae (Figures 22, 23) is known from a total of three specimens, each tentatively considered to represent a distinct species (S.C. Hess, unpublished data). There are considerable differences in the shape and structure of the rachis and vanes among all three. In one, the free rachis tapers anteriorly to a weak filament. This high level of intrafamilial variation is difficult to assess systematically at present. The gladius of the Brachioteuthidae (Figure 24) is slender, the vanes are expanded anteriorly and posteriorly, and they end posteriorly in a moderately small secondary conus. The gladius of Neoteuthis (Neoteuthidae) (Figure 25) has a short, very broad free rachis. The rachis is U-shaped in cross section and is thickened medially and laterally. The conus field is small and the primary conus is minute.

The diagnostic character of the gladius of the Histioteuthidae (Figure 26) is the ventrally inrolled posterior end of the vanes, the so-called “cupped coil.” As noted above, a similar structure occurs within the posterior end of the conus of psychroteuthids. Based on gladius morphology, several species groups appear to exist within the Histioteuthidae. These are supported in part by other characters including tubercles along the arms and dorsal midline of the mantle. Across the family, however, there is a cline of vane shapes and unequivocal generic groupings cannot be defined. Therefore, the monogeneric classification of the histioteuthids, as proposed by Voss (1969), is supported by characters of the gladius.

The gladius of the Lycoteuthidae (Figures 27, 28) is well known with the exception of the monotypic genus Nematolampas. The lycoteuthine gladius has a broad free rachis. The vanes are expanded anteriorly and posteriorly and are constricted medially. The gladius ends posteriorly in a primary conus. The gladius of the sole lampadioteuthine, Lampadioteuthis megaleia Berry, differs considerably from all lycoteuthines in the shape of the vanes, absence of a medial axis along the rachis, and presence of a small, well-formed, rostrum-like structure. Therefore, characters of the gladius support the placement of this species in a separate subfamily and, in comparison to the levels of intrafamilial variation seen in other presumably closely related families, would further support its separation at the familial level, a proposal advanced previously by Berry (1916). The gladii of Lycoteuthis diadema (Chun) and Selenoteuthis scintillons (Berry) show sexual dimorphism in the relative length and width of the anterior expanded portion of the vanes and in the length of the free rachis (Toll, 1983).

The enoploteuthid gladius (Figure 29) is characterized by vanes that are relatively broad along their entire length (broadest near the anterior one-quarter to one-third of their length), concave medially, and that end posteriorly in a small, shallow primary conus. A strap-like axial rib begins anteriorly near the lateral edge of the vanes in the region of their greatest width and extends posteriorly and obliquely across the vanes toward the midline of the gladius, marking the inner limit of the expanded conus field. The free rachis is relatively short and broad.

The Pyroteuthidae, along with the Ancistrocheiridae, discussed above, were previously included within the Enoploteuthidae as subfamily-level taxa equal in rank with the Enoploteuthinae. Toll (198) noted that the gladii of each of the three subfamilies were morphologically distinct based on a variety of characters. The pyroteuthid gladius (Figure 30) is characterized by vanes that are relatively broad along the majority of their length. The vanes are slightly constricted medially. They taper abruptly in the posterior one-third to one-quarter of their length and terminate posteriorly in a thick-walled, narrow secondary conus. The free rachis comprises a complex set of axial ribs. The borders of the free rachis converge anteriorly. The morphologic distinctiveness of the gladii of each of the three previously recognized subfamilies of enoploteuthids supports their elevation to familial level.

The Onychoteuthidae is a speciose family, also in need of systematic revision. Toll (1982) found that onychoteuthid gladii can be divided into two basic types. One type is characterized by a small conus field separated from the remainder of the vanes by a long, narrow, medial constriction of the vanes as found in Onychoteuthis (Figure 31), Chaunoteuthis, Moroteuthis, Kondakovia, and Ancistroteuthis. The second type, found in Onykia (Figure 32), is characterized by relatively broad vanes, a small conus, and the constriction anterior to the conus field being highly reduced or lacking. Recently, however, Tsuchiya and Okutani (1992) determined that Onykia and Moroteuthis are synonyms; representatives of the former (with the exception of O. rancureli Okutani) are early growth stages of taxa included in the latter. Therefore, the differences in gladius morphology could be due to ontogenetic changes. All known onychoteuthid gladii contain a rostrum-like structure that reaches its greatest development in Moroteuthis and Kondakovia. The gladii of Onychoteuthis banksii (Leach) and Chaunoteuthis mollis Appellöf differ with respect to the length of the free rachis, size of the conus field and rostrum, and size and shape of the vanes. This would suggest that these two taxa are not synonyms, the latter representing the spawned-out condition of the former, as has been suggested by some workers.

FIGURES 17–28.—17, Loligo pealeii (Loliginidae), ventral whole view of gladius (145 mm GL) (arrow indicates site of insertion of anterior vane shoulders to rachis). 18, Doryteuthis plei (Loliginidae), ventral whole view of gladius (122 mm GL) (arrow indicates site of insertion of anterior vane shoulders to rachis). 19, Mastigoteuthis hjorti (Mastigoteuthidae), ventral whole view of gladius (166 mm GL). 20, Grimalditeuthis bomplandi (Chiroteuthidae), ventral whole view of gladius (composite based on specimens of 100 mm ML and 146 mm ML). 21, Architeuthis sp. (Architeuthidae), ventral whole view of gladius (798 mm GL). 22, Promachoteuthis megaptera (Promachoteuthidae), ventral whole view of gladius (∼20.7 mm GL). 23, Promachoteuthis sp. A (Promachoteuthidae), ventral whole view of gladius (∼93.5 mm GL). 24, Brachioteuthis sp. (Brachioteuthidae), ventral whole view of gladius (127.5 mm GL). 25, Neoteuthis sp. (Neoteuthidae), ventral whole view of gladius (∼216 mm GL). 26, Histioteuthis atlantica (Histioteuthidae), ventral whole view of gladius (83 mm GL). 27, Lycoteuthis diadema (Lycoteuthidae), ventral whole view of gladius (132 mm GL). 28, Lampadioteuthis megaleia (Lycoteuthidae), ventral whole view of gladius (18.5 mm GL).

FIGURES 29–40.—29, Enoploteuthis anapsis (Enoploteuthidae). ventral whole view of gladius (∼50 mm GL). 30, Pyroteuthis margaratifera (Pyroteuthidae), ventral whole view of gladius (∼37.2 mm GL). 31, Onychoteuthis banksii (Onychoteuthidae), ventral whole view of gladius (117 mm GL). 32, Onykia carriboea (Onychoteuthidae), ventral whole view of gladius (28.8 mm GL). 33, 34, Gonatus antarcticus (Gonatidae) (158 mm GL): 33, midsagittal section through conus; 34, ventral whole view of gladius. 35. Pholidoteuthis adami (Pholidoteuthidae), ventral whole view of gladius (648 mm GL). 36, Pholidoteuthis boschmai (Pholidoteuthidae), ventral whole view of gladius (610 mm GL). 37, Cycloteuthis sirventi (Cycloteuthidae), ventral whole view of gladius (163 mm GL). 38, Discoteuthis laciniosa (Cycloteuthidae), ventral whole view of gladius (146 mm GL). 39, Chtenopteryx sicula (Chtenopterygiidae), ventral whole view of gladius (122 mm GL). 40, Bathothauma lyromma (Cranchiidae), ventral whole view of gladius (167 mm GL).

The Gonatidae also is speciose. Considerable efforts at systematic revision have been applied to some taxa, particularly Gonatus; however, the gladii from many gonatids remain poorly known. The majority of gonatid gladii can be characterized as follows (Figure 34): vanes with long, narrow anterior shoulders, anterior vane insertions well demarcated from the rachis, vanes relatively narrow, broadest near the anterior one-third to one-half of their length, constricted posteriorly with a small- to moderate-sized conus field terminating in a primary conus. This is true of the gladii of Gonatus spp. (with the exception of G. madokai Kubodera and Okutani) and Berryteuthis spp. Of particular interest is the presence of serial, concave, septal-like structures that occur within the concavity of the primary conus in Gonatus antarcticus Lönnberg (Figure 33) and G. fabricii (Lichtenstein). Based on the presumed homology of the conus with the conotheca of ancestral coleoids, these structures would appear to be the vestiges of septal walls, yet further ultrastructural and histochemical analyses are necessary for confirmation.

The families Pholidoteuthidae and Cycloteuthidae, both small in terms of number of species, have gladii that show surprisingly high levels of intrafamilial variability. The gladii of the two pholidoteuthids are strongly dissimilar. That of Pholidoteuthis adami Voss (Figure 35) is characterized by having long vanes that are slightly expanded anteriorly, constricted medially, and greatly expanded posteriorly. The gladius ends posteriorly in a large, funnel-like secondary conus. The gladius of P. boschmai Adam (Figure 36) differs in the shape of the vanes and in the axial structure of the free rachis. The gladius of P. adami is strikingly similar to that of the sole lepidoteuthid, Lepidoteuthis grimaldii Joubin (see above), but it lacks the cartilagenous axis that is found in all examples of the latter. Based primarily on mantle morphology and in part on the morphology of the gladius, Roper and Lu (1989) recommended that Pholodoteuthis adami be replaced in the family Lepidoteuthidae. Among the cycloteuthids, the gladius of the monotypic Cycloteuthis (Figure 37) is relatively narrow with long vanes that are slightly expanded anteriorly and nearly twice as wide posteriorly. The gladius terminates in a moderately short secondary conus. The gladii of Discoteuthis discus Young and Roper and D. laciniosa Young and Roper (Figure 38) have long, broad vanes that are not constricted medially. The two differ in the length and width of the free rachis, the shape of the posterior outline of the vanes, and the structure of the terminus of the gladius. The gladius of D. discus is slightly ventrally inrolled whereas that of D. laciniosa ends in a small, blunt secondary conus. The ventral concavity of the gladius of Cycloteuthis contains a thin layer of stiff gelatinous material. A much thicker layer is present within the ventral concavity of the gladius of Discoteuthis spp. These differences could be related to fin-complex morphology, which differs between the two genera. The two fins are partially fused along the dorsal midline above the mantle musculature in Cycloteuthis, whereas in Discoteuthis they are completely separate and insert individually upon the mantle musculature.

The gladius of the chtenopterygiid Chtenopteryx sicula (Verany) (Figure 39) is characterized by broad vanes with shallowly concave anterolateral shoulders and strap-like thickened axes along the posterolateral margins. The gladius terminates posteriorly in a broadly rounded tip without indication of a conus. The gladius of the enigmatic C. sepioloidea Rancurel differs substantially from that of C. sicula in vane shape and free rachis structure (Toll, 1982).

In no other teuthoid family is the shape of the gladius so variable as it is in the Cranchiidae. Voss (1980) and Toll (1982) have shown that the shape of the cranchiid gladius is organized at the generic level; each genus is characterized by a particular gladius shape. Clades representing generic groupings proposed by Voss and Voss (1983) and based on a suite of soft tissue and gladius characters also are supported by characters of the gladius alone, particularly the pseudoconus, which is found exclusively in six genera of cranchiids recognized by Voss and Voss (1983) as forming a clade. The highly modified gladius of Bathothauma (Figure 40), characterized by a filamentous free rachis and broadly expanded transverse bar at the posterior limit of the gladius (which serves as the site of attachment for the fins), is unique among the Teuthoidea.

Advantages of the Use of the Gladius for Systematics

All squids possess a gladius; therefore, all taxa can be compared directly with respect to it. The shell sac, a glandular epithelium that secrets the gladius, is one of the earliest organs to develop during embryogenesis, and the gladius is present at the time of hatching. Therefore, in comparative studies of all teuthoid life stages with the exception of early prehatchling embryos, the gladius is available for comparative study. Furthermore, the gladii from all squids are strictly homologous to one another and to at least a portion of the ancestral coleoid shell. As noted by Jeletzky (1966:8), “The neglected proostracum is a fundamental morphological feature peculiar to coleoid cephalopods and represents a most important biological adaptation of their characteristically active, nektonic mode of life. [It]…is the only major comparable shell element common to both teuthid and belemnite-like coleoids. Without it no comparison of their shells would be possible.”

In comparison to soft tissues, chitin, the chemical constituent of gladii, is relatively immune to the potential distortional effects of chemical fixation and preservation. Indeed, some authors (see Kristensen, 1982; Voss, 1985) have adopted the use of gladius length as the standard measurement for squids in lieu of mantle length, which is more easily distorted by the action of chemical fixatives and preservatives. This is particularly true of soft bodied forms, such as the cranchiids, histioteuthids, chiroteuthids, and others. Similarly, chitin, as compared to soft tissues characters, is more resistant to the enzyme catabolism associated with the digestive processes of predators. Therefore, as with cephalopod beaks (also composed of chitin but of a different and more resistant form), gladii tend to have relatively long residence times within the digestive tracts of predators. As a result, gladius remains have been used successfully to identify squids taken by predators (see Toll and Hess, 1981; Hess and Toll, 1981). Even though some distortion can occur, an expanded use of gladii in the determination of predator stomach contents could be a valuable addition to knowledge gained from beak analyses.

The gladius is a complex skeletal structure that comprises a large suite of individual characters, some with several distinct character states. These include the number, position, and structure of axial thickenings of the rachis, presence and type of conus, vane shape, presence and length of a conus field, number and position of vane thickenings, relative lengths and widths of the rachis and vane components, and others. In addition, the anatomical relationship of the fin complex, fin cartilage, dorsal mantle musculature, and nuchal cartilage can be of potential systematic value and have been insufficiently examined to date (but see caution below).

Disadvantages of the Use of the Gladius for Systematics

Considerable difficulty can be incurred in obtaining precise measurements of some components of nearly all gladii. This is particularly true of width measurements of the rachis and vanes. In virtually all teuthoid taxa, the gladius is curved ventrally in cross section, particularly along the vanes, reflecting the curved surface of the dorsal-mantle musculature. To obtain precise width data, the gladius should be flattened in order to obtain a maximum value. In more sturdily constructed gladii, however, a compromise needs to be established whereby a practical maximum flattened gladius width is obtained without overmanipulation, which can result in breakage. The same situation pertains to the rachis of many teuthoid gladii. In many cases, well-developed, rigid rachises have a ventral channel. Variability in rachis-width measurements can be artificially introduced by either dorsoventral or lateral compression during measurement. With regard to the rachis, gladii from congeners or confamilials should always be treated in the same manner for purposes of obtaining measurements, and this treatment should be described explicitly for the benefit of future workers who wish to compare their own data to those found in published accounts.

Another complication involves the precise measurement of the free rachis and vane lengths. In the gladii of some taxa it is difficult to clearly delineate the anteriormost point of the anterior vane extensions along the rachis. In some gladii (e.g., Doryteuthis plei) the anterior limit of the vanes is discrete. In others (e.g., Loligo pealeii) the anterior extension of the vanes merge into the borders of the rachis, and a clear demarcation between the two is difficult if not impossible to resolve. Here, too, consistency of methodology is of paramount importance.

The precise function of the gladius is not known in many taxa; however, it can safely be concluded that, minimally, the gladius is inextricably tied to locomotory capabilities in most squids (see Toll, 1988). As such it forms, together with the fin complex, mantle musculature, and nuchal anatomy, a portion of the skeletomuscular complex as a whole. In view of the functional requirements and limitations placed upon it, the possibility of convergence of shape and construction among gladii from disparate groups must not be underestimated or ignored.

As a further caution, the use of the color of the gladius as a systematic character should be strictly avoided. With the exception of several of the large ommastrephids that have amber to brown gladii in life (T. Okutani, pers. comm., 1988), all gladii removed from living or recently dead specimens are colorless and transparent to white and translucent. Gladii held in preservation become more opaque and darken to various degrees from light amber to dark chocolate brown. These artifactual colors have no systematic value; however, this darkening can be useful in visualizing thickened axes or bands along the rachis and vanes, respectively. Here, too, caution must be exercised. Because of the optical properties of chitin and the complex three dimensional shape of the gladius, particularly along the rachis, actual cross sections should be made to determine accurately the three-dimensional structure of the gladius. At least three sections should be made, one along the free rachis near the midpoint of its length, one at the posterior limit of the free rachis, and a third at the level of the greatest width of the vanes. Gladii with more complex shapes (e.g., Lycoteuthidae) necessarily require additional sections at critical levels, such as the widest level of the anterior vanes, the tapered region between the anterior and posterior vane segments, and the level of the widest point of the posterior vane segment. In addition, conuses or rostrum-like structures, too, should be sectioned in order to study internal structure.

Future Directions

Despite renewed interest in the gladius there remain substantial voids in our knowledge that hinder its wider use in systematic applications. A fuller understanding of intra- and interspecific variability is sorely needed. Although it is known that the gladius of at least some taxa can display individual, sexually dimorphic, and what appears to be populational (geographic) differences within species, the levels of this variation are poorly understood in most teuthoids.

Larval gladii are known from only a small number of taxa. The difficulties associated with their removal pose obvious problems; however, the study of the larval gladius could yield valuable data on familial relationships that are obscured in the adult gladius.

The relationships between the conus field and the vanes need clarification. In some species the conus field extends well anteriorly along the vane. The presence and morphology of a conus field could yield data on phylogenetic relationships (see Young and Harman, 1998).

The anatomical relationships of the gladius to the fin complex and the dorsal mantle musculature, both anteriorly and posteriorly and especially in the nuchal area, have been investigated on a limited basis. Here, too, more information is needed.

The gladius is composed of chitin, specifically the X-ray crystallographic form known as Beta-chitin. Hunt and Nixon (1981), however, have shown that chitin can bind with proteins and amino acids to form specific chemical complexes. Hoyle (1889), Chun (1910), and Toll (1982) observed in a single gladius what appear to be different forms of chitin that have distinctly different optical properties. This is true for several species of squids, notably the Chiroteuthidae and allied taxa. In addition, nonchitinous structures are found associated with the gladii of many squids, such as the “cartilagenous” rod found along the ventral concavity of the rachis in Lepidoteuthis grimaldii and the ventral “infilling material” commonly found in the gladii of the Histioteuthidae, among others. Chemical analyses of these materials could prove to be of great value in determining homologies among Recent forms and between Recent forms and fossil antecedents.

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The Value of Statolith Shape for Systematics, Taxonomy, and Identification

Malcolm R. Clarke

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Malcolm R. Clarke, Ancarva, Southdown, Millbrook, Torpoint Cornwall, PLIO IEZ, United Kingdom.

ABSTRACT

Statoliths of cephalopods are small aragonitic structures found in the fluid-filled statocysts of the Coleoidea. Use of a digitizing tablet to measure the dimensions of statoliths shows considerable potential for studies of relationships among genera, species, and even subspecific groups.

Introduction

Statoliths of cephalopods are small, hard, aragonitic stones that lie in fluid-filled cavities, or statocysts, within the cartilaginous skulls of members of the Coleoidea (Figure 1). They measure less than 2 mm in length and vary greatly in shape, from a simple flat cone in some octopods, through a sausage shape, to a much more complex shape bearing several rounded protuberances in various planes in many teuthoids and sepioids. Because the complexity of form of these hard structures varies greatly between orders, families, and genera, and because there are some distinctive features linking the members within these taxa, the further analysis of the form of statolith shape is likely to be a fruitful line of research. The complication is that, in common with most taxonomic features, statoliths vary considerably within identified species, particularly during growth; however, the inflexible and hard nature of these stones allows very accurate and repeatable measurement. With these structures, techniques of mensuration and data handling can be developed without the difficulties involved with soft and flexible taxonomic characters (beaks, gladii, cartilages) or with characters that vary greatly within a single individual, such as radulae and sucker rings.

ACKNOWLEDGMENTS.—The author is very grateful to Linda Maddock of the Marine Biological Association of the United Kingdom, Plymouth, for her invaluable help in the statistical analysis of statoliths.

FIGURE 1.—Anterior view of statocysts of Loligo showing 2 opaque statoliths lying against anterior walls. (Courtesy of J.Z. Young.)

Observations

VARIATION.—Some of the variations in statolith shape are shown for octopods in Figure 2, for sepioids in Figure 4, and for teuthoids in Figure 3. Within any one species, adults show many similarities in statolith proportions and shape, but, as one would expect, hatchlings have statoliths of simpler shape that become more complex and more easily distinguished from related species with growth. Although variation among statoliths includes features that are absent from some taxa and present in others, on the whole such differences are between orders rather than between lower taxa. Analysis of variation within families, genera, and species must therefore depend largely upon analysis of proportion by methods of mensuration. Only by these means can one assess and use the stability of shape that lies within the natural variation of a species.

FIGURE 2.—A–E, Statoliths of Eledone cirrosa, statolith total length (STL) = 1.74 mm: A, anterolateral view; B, posterior view; C, ventral view; D, medial view; E, dorsal view. F, statolith of Eledonella pygmaea, STL = 0.42 mm (view uncertain). G, lateral view of ?Benthoctopus sp. statolith, STL = 0.31 mm.

DESCRIPTION.—Analysis of statolith shape has already been tackled at several complementary stages of complexity. First, a verbal description of the shape was necessary, and this was done by surveying a large range of statoliths to determine and name their various parts (Figure 5; Clarke, 1978). Although this nomenclature is satisfactory for teuthoids and sepioids, octopod statoliths are so different that the homologues of their parts have not been unequivocally determined. The description of statoliths made possible by this nomenclature is useful between some genera and species but does not always allow the verbal separation of species (Clarke and Fitch, 1979). At the same time, these descriptions were supported by relating selected measurements to total length or to other measurements.

FIGURE 3.—Anterior (upper) and lateral (lower) statolith views of 9 teuthoid species: A, Ommastrephes caroli, statolith total length (STL) = 1.37 mm; B, Mastigoteuthis sp., STL = 0.63 mm; C, Teuthowenia megalops, STL = 0.72 mm; D, Notodarus sloani, STL = 1.26 mm; E, Todarodes sagittatus, STL = 1.82 mm; F, Pyroteuthis margaritifera, STL = 0.58 mm; G, Histioteuthis bonnellii, STL = 0.97 mm; H, Abraliopsis sp., STL = 0.48 mm; I, Helicocranchia pfefferi, STL = 0.75 mm.

DATA ANALYSIS.—Separation of the various species by the above method was not very satisfactory. Better statistical methods, namely multiple discriminant analysis and principal component analysis, provided the means by which a number of measurements could be combined for the comparison of species. Multiple discriminant analysis was first used on statoliths to study the relationships between members of the Gonatidae (Clarke et al., 1980), with nine measurements used on four living and one fossil species. The analysis was found to have high potential for evaluating differences and similarities between genera, species, and species groups arranged geographically and by size (Figure 6). A similar analysis on Loligo species was useful in comparing fossil statoliths from Europe and North America with living species (Figure 7A, C).

FIGURE 4.—Anterior (upper) and lateral (lower) statolith views: A, Sepia elegans, statolith total length (STL) = 1.46 mm; B, Spirula spirula, STL = 0.92 mm.

Statistical methods rely upon measurements taken with a microscope, which involve very careful and painstaking manipulation and a subjective decision on the orientation and the exact points from which distances are measured. With an object like a statolith, which has protrusions in all directions and curved surfaces on which discrete points are not always distinct, such measurements often show considerable variability. The tedium of the measurement process also limits the number of measurements that can be taken, and the work cited above has shown that nine dimensions are probably near the practical limit for such comparisons.

FIGURE 5.—Generalized teuthoid right statolith showing dimensions and terms used in descriptions: A, anterior view; B, posterior view; C, lateral view; D, anterior view showing principal measurements and terms used to describe indentation forms.

FIGURE 6.—Multiple discriminant analysis of 11 geographical groups in the Gonatidae. art, Gonatus fabricii; art, G. makko; art, art, art, art Gonatopsis borealis; art, ×, art, art, Berryteuthis magister; art, fossil Berryteuthis species.

FIGURE 7.—Results of multiple discriminant analysis of micrometer measurements (A,C) and digitizer dimensions (B,D) of loliginid statoliths. In both cases all measurements were converted to dimensionless ratios by dividing by total length and were then standardized. In A and B, specimens are plotted on axes 1 and 2, which are in units of mean group standard deviation. Each species is positioned at its centroid, and its standard deviation on each axis is used to plot an ellipse. An indication of the position on axis 3 is given by the overlap of the ellipses, which are viewed as if from the positive side of axis 3, with a dashed outline signifying a positive score. C and D show weightings of respective measurements on first 2 axes (dashed line indicates negative value on axis 3); lower case letters refer to measurement, and capital letters in D refer to view (see Figure 8). Species are as follows (number of statoliths used in A and in B, respectively, are given in parentheses): Am, Alloteuthis media (6, 6); As, Alloteuthis subulata (62, 61); D, Doryteuthis bleekeri (3, 3); Lb, Lolliguncula brevis (12, 12); Lba, L. barkeri (166, 30); Le, Loligo European fossil (6, 6); Lf, L. forbesi (77, 77); Lm, L. mississippiensis (4, 1); Lo, L. opalescens (14, 14); Lp, L. plei (4, 4); Lpa, L. panamensis (3, 3); Lpe, L. pealeii (45, 45); Ls, L. stillmani (34, 18); Lv, Loligo vulgaris (53, 52).

FIGURE 8.—Photographs of 3 views and 5 tracings used in “digitizer” analysis of left statolith of Loligo sp. Arrows indicate point at which tracings were started. A, W, anterior views; L, D+R, lateral views; V, ventral view. Linear dimensions used in “measurement” analysis are shown on A.

AUTOMATIC MEASUREMENT.—The invention of computerized digitizing tablets has solved the problems of manipulation and measurement and provides a method by which a far greater number of parameters can be incorporated into a statistical analysis.

The statoliths must be carefully orientated on a pliable base beneath the microscope with regard to specified rules (e.g., the anterior view must show the largest possible area to the viewpoint, and the center of the field must be directly over the center of both axes of the statolith). The outlines of the views can then be drawn at a standard, convenient length together with outlines of several of the component parts (Figure 8). These drawings are then placed on a digitizing tablet and oriented in a standard way with the longitudinal and horizontal axes of the tablet. In one trial, three views provided five outlines of views or part views of each statolith (Figure 8, A, W, L, D+R, V). These were then traced and the computer calculated the area, perimeter, width, length, maximum distance across the outline from the point at which the tracing was started, and the position of the center of gravity from the left and from the bottom limits of the outline. To remove the effects of size, all measurements were divided by the statolith length. By this means, a total of 30 parameters were included in the first analysis and acquisition of these measurements involved no subjective decisions.

STATISTICAL HANDLING OF DATA.—In a broad analysis involving 72 species from 19 families, 1026 statoliths were measured by digitizing tablet, and the resulting data were then statistically analyzed by two methods, principal components analysis and multiple discriminant analysis. The results helped in an analysis of family relationships (Clarke and Maddock, 1987a, 1987b). The influence of the different parameters in separating the taxa is shown in Figure 9B. A long line shows that a feature is very influential in separating species parallel to the line. For example, feature A6 in Figure 9B, the area of the lateral dome in anterior view, separates Sepia officinalis Linnaeus from Ommastrephes caroli (Furtado). Parameters having short lines contribute little to the separation of species. After a preliminary trial, these can be left out of further analyses of the same data in order to achieve even better separation of species by relying only upon the most important parameters. To illustrate the information on form within the statistical figure showing multiple discriminant analysis (Figure 9), two views of several species were plotted in the same relation to the two axes (Figure 10).

FIGURE 9.—A, results of multiple discriminant analysis of outlines shown in C traced on a digitizing tablet to find 38 components of 992 statoliths (measurements converted to dimensionless ratios by dividing by statolith total length). (art, Ommastrephidae; art, Loliginidae; art, Sepiidae; art, Histioteuthidae; +, Cranchiidae; *, Sepiolidae; art, Gonatidae; 1, Bathyteuthidae; 2, Lycoteuthidae; 3, Mastigoteuthidae; 4, Onychoteuthidae; 5, Enoploteuthidae; 6, Valbyteuthidae; 7, Ancistrocheiridae; 8, Octopoteuthidae; 9, Brachioteuthidae; 10, Lepidoteuthidae). The larger the symbol, the farther it is from the third axis. Species of Illex (Ommastrephidae) and the Sepiidae, Sepiolidae (except 1 species), and Histioteuthidae (except 1 species) all have positive values on the third axis. All other Ommastrephidae, Gonatidae, Cranchiidae, and Loliginidae have negative values. B, weightings of measurements on 2 axes of A (letters refer to parameter, numbers refer to view in C; some small values excluded) (A, area; X, width; Y, length; position of center of gravity from left (CGX) and from bottom (CGY)). C, anterior and lateral views of right statolith showing outlines used in multiple discriminant analysis (1, whole statolith in anterior view; 2, wing; 3, lateral dome; 4, dorsal dome; 5, rostrum; 6, whole statolith in lateral view except for wing; 7, lateral dome; 8, dorsal dome; 9, rostrum). Center of gravity (x) for each whole view also included.

FIGURE 10.—Outlines of statoliths of some species analyzed in Figure 9 (placed approximately in same relationship to axes as in Figure 9A), illustrating trends in form shown by multiple discriminant analysis: L.f., Loligo forbesi; B.m., Berryteuthis magister; S.o., Sepia officinalis: O.c. Ommastrephes caroli; B.l., Bathothauma lyromma; G.s., Gonatus steenstrupi; H.b., Histioteuthis bonnellii.

COMPARISON OF METHODS.—A digitizing tablet became available after dimensions of 821 statoliths from 14 species in four genera of Loliginidae had been measured by micrometer. By processing the same statoliths with the tablet and analyzing both sets of parameters by multiple discriminant analysis, it was possible to directly compare the results from the two methods. From this comparison (Figure 7), it is clear that the digitizing tablet method led to far greater separation of the taxa.

PROSPECTS FOR TAXONOMY.—The methods outlined herein show considerable potential for studies of relationship between genera, species, and even subspecific groups. Use of the simple system described herein, with careful manipulation, will help with many taxonomic problems; however, many more developments in computer technology have taken place since these analyses were done. For example, more parameters can be examined involving simulated slices across the object, and this may well be helpful for some species separation.

An extension that we may expect in the near future is the identification of a statolith by referring its silhouettes to a data bank. The statistical probability of the statolith belonging to any closely related species could then be automatically computed.

Literature Cited

Clarke, M.R.

1978   The Cephalopod Statolith: An Introduction to Its Form. Journal of the Marine Biological Association of the United Kingdom, 58: 701–712.

Clarke, M.R., and J.E. Fitch

1979   Statoliths of Cenozoic Teuthoid Cephalopods from North America. Palaeontology, 22:479–511.

Clarke, M.R., J.E. Fitch, T. Kristensen, T. Kubodera, and L. Maddock

1980   Statoliths of One Fossil and Four Living Squids (Gonatidae: Cephalopoda). Journal of the Marine Biological Association of the United Kingdom, 60:329–347.

Clarke, M.R., and L. Maddock

1987a. Statoliths of Fossil Coleoid Cephalopods. In M.R. Clarke and E.R. Trueman, editors, The Mollusc, 12: Paleontology and Neontology of Cephalopods, pages 153–168. San Diego: Academic Press.

Clarke, M.R., and L. Maddock

1987b. Statoliths from Living Species of Cephalopods and Evolution. In M.R. Clarke and E.R. Trueman, editors, The Mollusca, 12: Paleontology and Neontology of Cephalopods, pages 169–184. San Diego: Academic Press.

A Synopsis of Sepiidae Outside Australian Waters (Cephalopoda: Sepioidea)

D.N. Khromov, C.C. Lu, A. Guerra, Zh. Dong, and S.V. Boletzky

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D.N. Khromov, All-Union Research Institute of Marine Fisheries and Oceanography (VINRO), V-Krasnoselskaya 17a, 107140 Moscow, Russia. C.C. Lu, Department of Zoology, National Chung Hsing University, Taichung, Taiwan. A. Guerra, Instituto de Investigaciones Marinas (CSIC), Eduardo Cabello 6, 36208 Vigo, Spain. Zh. Dong, Institute of Oceanology, Academia Sinica, 7 Nan-hai Road, Qingdao 266071, People's Republic of China. S.v. Boletzky, Observatoire Océanologique de Banyuls, URA 117 CNRS/UPMC, Laboratoire Arago, 66650 Banyuls-sur-Mer, France.

ABSTRACT

The cuttlefishes of the family Sepiidae outside Australian waters are reviewed. Three genera are recognized, Sepia, Sepiella, and Metasepia, with 84, 5, and 2 valid species, respectively. For a number of species, available data, including biological characteristics and distribution areas, are insufficient for a complete description. A key to species is provided in Appendix I. The rich type material housed in The Natural History Museum, London, is listed in Appendix II.

Introduction

The cuttlefish family Sepiidae Keferstein, 1866, is well defined and is rarely confused with other cephalopod groups. Occasional misidentifications of photographs in popular books and magazines are generally due to the vague overall similarity between cuttlefishes and loliginid squids of the genus Sepioteuthis (e.g., Dioleé and Cousteau, 1973:99); knowledge of the typical color patterns of these animals often helps to avoid such errors. Real difficulties arise only at the generic and specific taxonomic levels, and given the large number of nominal species known from the temperate and tropical waters of the Old World, Western Pacific, and Australia, it is not surprising to find the systematics of Sepiidae in a state of continuous change.

Many species are poorly known; only a few common inshore sepiids can be described comprehensively based on morphological features of eggs, embryos, and juvenile and adult animals, and in some instances also on behavioral characteristics (Corner and Moore, 1980; Hanlon and Messenger, 1988; Roper and Hochberg, 1988). The biology of a few common species, foremost Sepia officinalis Linnaeus, was covered in a recent symposium (Boucaud-Camou, 1991), and work done during similar scientific meetings will doubtless accelerate the accumulation of data allowing the species definitions to improve for wider areas.

The present contribution attempts to provide an overview of diagnostic features and distribution data for the clarification of sepiid systematics and biogeography, but it should not be mistaken as an exhaustive coverage of the whole group. Before, during, and after the International Workshop on the Systematics and Biogeography of Cephalopods, held at Washington, D.C., in July 1988, data and observations were gathered to complement the reviews by Adam and Rees (1966), Roeleveld (1972), Adam (1979), Khromov (1987b), and the sepiid section of the Cephalopods of the World by Nesis (1982 (in Russian), 1987 (translation)). A helpful guideline for our work was an early draft of the classification prepared by Sweeney and Roper (1998), and valuable information was taken from the catalog of specimens in the Paris museum prepared by Lu et al. (1995).

Expecting rapid accumulation of new material that will permit a more thorough revision of the family in the near future, we have kept changes to a minimum, making only the essential modifications in the current systematic arrangements. We recognize three genera: Sepia, Sepiella, and Metasepia. Within the genus Sepia, a subdivision is used as a basically typological “open system” of six species complexes. This tentative division allows species to be shifted to a different complex when new characters become known or when known characters are reassessed. Thus, the species complexes defined by Khromov in a key to the Recent genera and species complexes (Appendix I) are not entirely congruent with the groups used by Lu (1998b), as can be seen in Table 1. Ultimately, refined morphological, behavioral, and biogeographic analyses will have to be combined with biochemical and molecular studies to arrive at a truly phylogenetic system made of nested monophyletic groups with well-defined sister-group relationships.

TABLE 1.—List of sepiid species covered herein and in Lu, 1998a (Australian species); Lu, 1998b (sepion features of species groups 1 to 6; species group 3 divided into subgroups a–e). Species complexes are as defined by Khromov, 1998 (Appendix I, herein; Khromov, 1998 (distribution)): Aca = Acanthosepion, Sep = Sepia sensu stricto, Rho = Rhombosepion, Ano = Anomalosepion, Dor = Doratosepion, Hem = Hemisepius. T = type material examined during workshop, BM = type material in The Natural History Museum, London (see Appendix II). Species status: ++ = unquestioned, + = probably valid species but insufficiently described, ? = questionable.

The present contribution contains brief descriptions of accepted, or potentially acceptable, species with remarks on their status, plus the key mentioned above (Appendix I), and a list prepared by Lipinski and coworkers of the sepiid type specimens housed in The Natural History Museum, London, some of which were not available during the workshop (Appendix II). This joint coverage should be used in combination with the separate papers by Lu, one on Australian sepiids (1998a), the other on the use of cuttlebone (sepion) features in species identification (1998b), and with the biogeographic and bathymetric survey by Khromov (1998).

ACKNOWLEDGMENTS.—The authors gratefully acknowledge careful reviews of the manuscript by Martina Roeleveld (Cape Town) and Michael Sweeney (Washington, D.C.). Thanks are due to Dmitry Alexeyev (Moscow) for his help with the preparation of many of the figures. The special examination of several type specimens in The Natural History Museum, London, by Roger Villanueva also is gratefully acknowledged.

DEDICATION.—Professor William Adam was to be our group leader during the Washington workshop, but his frail health did not allow him to attend. He died on the 3rd of November, 1988. We dedicate this paper to his memory.

Systematics of the Family SEPIIDAE

Keferstein (1866) is recognized as the author of the family Sepiidae. The type genus is Sepia Linnaeus (1758).

FAMILY DIAGNOSIS.—Mantle oval to circular in outline, dorsoventrally flattened; fins lateral, occupying nearly all of mantle length, posteriorly separated (except male of Sepia confusa Smith); eye covered by cornea; hectocotylization (where present) on left arm IV (or both arms IV), expressed by reduction of suckers; tentacles retractable into pockets on ventrolateral sides of head; shell (cuttlebone or sepion) with phragmocone (“septal necks” only), usually calcified, flat (rarely bulging ventrally); funnel-mantle locking apparatus curved to angular, not straight (Figure 1).

GENERIC DIAGNOSES.—The three genera currently recognized in the family are Sepia Linnaeus, 1758, Sepiella Gray, 1849, and Metasepia Hoyle, 1885, with the following diagnostic features:

Sepiella: Posterior gland and pore present; locking apparatus with triangular tubercle on mantle component and corresponding depression in funnel component. Sepion elliptical in outline; inner cone wide and flat with very short limbs.

Metasepia: Posterior gland and pore absent; locking apparatus semicircular without tubercle on mantle component and without corresponding depression on funnel component. Sepion rhomboidal in outline, much shorter than mantle, and located in anterior images–images of mantle; inner cone narrow and thickened with very short limbs.

Sepia: Posterior gland and pore absent, locking apparatus with semicircular tubercle on mantle component and corresponding depression in funnel component. Cuttlebone (sepion) elliptical to subrhomboidal or lanceolate in outline; inner cone always with relatively long limbs (longer than in Sepiella and Metasepia). Note incomplete calcification of dorsal shield found in several species; see diagnostic features of species groups.

For the genus Sepia, the following subdivision into species complexes is considered in a typological fashion similar to the phenetic approach, for the reasons given earlier.

1. Sepia sensu stricto (Linnaeus, 1758) species complex (Figures 80h, 81, 82): Sepion broad to elongate with or without spine; outer cone moderately to markedly broad, never drawn out into wings; inner cone U-shaped, thick or flat posteriorly; cup-like cavity over posterior striated zone absent (secondary extension in S. pharaonis Ehrenberg); club suckers unequal, in 8 transverse rows (except S. simoniana Thiele, S. insignis Smith, S. gibba Ehrenberg, S. elobyana Adam); arm suckers quadriserial.

2. Acanthosepion (Rochebrune, 1884) species complex (Figures 78, 80a–g,): Sepion nearly elliptical, heavily calcified, with spine; outer cone wide (not drawn out into distinct wings, cf. Figure 85a–g); inner cone distinct, forming rounded, cap-like cavity; club suckers generally subequal (except S. prashadi Winckworth, S. recurvirostra Steenstrup); arm suckers quadriserial throughout arm length.

FIGURE 1.—Morphological elements of sepion (ventral view, upper left) and soft parts of animal (ventral view, mantle partly cut to expose “press button” components of funnel-mantle locking apparatus). Note 1 tentacle stretched out (as in prey capture), other tentacle retracted, with coiled tentacular shaft, in tentacle pocket (as in resting position).

3. Rhombosepion (Rochebrune, 1884) species complex (Figures 83, 84a–e,): Sepion nearly rhomboidal, with or without spine, dorsal shield thinner than in species complex 1 or 2, often incompletely calcified; outer cone demarcated by shallow notch or smoothly continuous with lateral margins; inner cone narrowly U-shaped, with narrow, thin (but rib-like) posterior part and inconspicuous lateral limbs; arms I–III slender, with quadriserial suckers enlarged in middle rows.

4. Anomalosepia (Khromov, 1987b) species complex (Figure 84f,g): Sepion elongate, teardrop-shaped, dorsal shield thin; spine present and keeled; outer cone thin, reduced; secondary wings may be formed by subterminal margins (S. omarni); inner cone as in species complex 3.

5. Doratosepion (Rochebrune, 1884) species complex (Figures 85a–g, 86a–e): Sepion broadly to narrowly lanceolate, dorsal shield very thin, often only calcified in medial part; spine present (except S. arabica); outer cone entirely represented by distinct wings; inner cone usually narrowly V- or U-shaped, posterior part forms ridge around posterior depression of striated zone.

6. Hemisepius (Steenstrup, 1875) species complex (Figures 85h–j, 86f,g): Sepion wide, oval, not longer than 25 mm in adult; dorsal shield very thin and usually not calcified; spine absent; outer cone wide, not drawn out into lateral wings; inner cone widely U-shaped, very reduced, with extremely short limbs; club suckers subequal; arm suckers biserial; ventral mantle rim with angular emargination below funnel (deeper than in other species complexes).

Characteristics of club and arm-sucker arrangements and size relationships in species complexes 4 and 5 cannot be given unambiguously. Major problems arise with the “gradational” expression of various features of the cuttlebone in ontogenetic development, resulting in continua across species. Future analyses should concentrate on the morphology of the embryonic part of the shell (especially with regard to the phragmocone structure and the number of septal lamellae) and its relation to egg size. Every effort should be made to identify the eggs (size of ovum at laying, structure and color of egg envelopes) and to describe their size and color changes during embryonic development for each species. Whenever possible, embryonic stages should be described using published descriptions as guidelines (Naef, 1923, 1928; Lemaire, 1970; Yamamoto, 1982).

Sepia Linnaeus, 1758

TYPE SPECIES.—Sepia officinalis Linnaeus, 1758:658.

Sepia officinalis Linnaeus, 1758

FIGURE 2

Sepia filliouxi Lafont, 1869:11.

Sepia mediterranea Ninni, 1884:159.

DIAGNOSIS.—Body flattened, fins starting at anterior edge of mantle. Arm suckers quadriserial, usually 5–8 rows of reduced suckers on hectocotylus. Tentacular club suckers in oblique series of 7 to 8 generally small suckers; only 5 to 6 median suckers greatly enlarged. Sepion oval, width 30%–40% of length in male, 33%–42% in female. Anterior striae rounded or rounded M-shaped. Inner cone without distinct ventral ledge. Outer cone wide. Spine more or less prominent, surrounded by chitinous shield. Shield covering dorsal side of outer cone.

FIGURE 2.—Sepia officinalis: a–c, ventral, dorsal, and lateral views of sepion; d, left tentacular club; e, geographical distribution. (d, after Roper et al., 1984.)

ORIGINAL REFERENCE.—Linnaeus, 1758:658.

TYPE LOCALITY.—? Eastern Atlantic.

TYPE.—Type not traced.

GEOGRAPHICAL DISTRIBUTION.—Eastern Atlantic, from the Shetland Islands and southern Norway south through the Mediterranean Sea to northwestern Africa (not present in the Baltic Sea).

DISCUSSION.—Five subspecies were designated by Adam (1940). The subspecies S. o. filliouxi Lafont, 1868, and S. o. mediterranea Ninni, 1884, are herein considered indistinct from S. o. officinalis Linnaeus, 1758, whereas S. o. hierredda Rang, 1837, and S. o. vermiculata Quoy and Gaimard, 1832, are herein considered distinct subspecies. The geographic distribution of S. officinalis thus is restricted to the subtropical and temperate waters of the eastern Atlantic in the northern hemisphere. Size is to 300 mm mantle length (ML). Usual depths are about 50–100 m. This species has large seasonal migrations and is of considerable commercial value.

Sepia aculeata Orbigny, 1848, in Férussac and Orbigny, 1834–1848

FIGURE 3

ILLUSTRATIONS.—Adam and Rees, 1966, pl. 4: fig. 21; pl. 42: fig. 251.

DIAGNOSIS.—Tentacular club with small equal suckers in 10–14 longitudinal rows. Tips of buccal membrane with few minute suckers. Sepion long-oval in outline. Striated zone without furrow. Anterior striae rounded. Inner cone with wide, convex, rounded ventral ledge around pocket-like cavity. Spine long, without keels.

ORIGINAL REFERENCE.—Orbigny, 1848, in Férussac and Orbigny, 1834–1848:287.

TYPE LOCALITY.—Java.

TYPES.—Syntype: Muséum National d'Histoire Naturelle, Paris, 1.6.186, 1 female, 106 mm ML, sepion 102 mm.

GEOGRAPHICAL DISTRIBUTION.—Indo-West Pacific from South India (Bombay?) to Timor Sea, including Indonesia; Tokyo, Japan; P'yönjyang, North Korea; Lüda and Tsingtao, China.

DISCUSSION.—This is a fully described species of unquestioned status. The size is to 230 mm ML, and the usual capture depth is to 60 m. This species is of commercial value in India, China, Indonesia, and Thailand.

Sepia acuminata Smith, 1916

FIGURE 4

ILLUSTRATIONS.—Adam and Rees, 1966, pl. 16: figs. 91, 92; pl. 43: fig. 261.

DIAGNOSIS.—Tentacular club with minute subequal suckers in 10 longitudinal rows. Sepion subrhomboidal. Striated zone flat, with many fine furrows. Anterior striae rounded. Outer cone with indistinct wings. Spine long, without keels.

ORIGINAL REFERENCE.—Smith, 1916:21.

TYPE LOCALITIES.—Port Elizabeth and Tongaat, South Africa.

TYPES.—Syntypes: The Natural History Museum, London, 1890.9.22.332–333, 2 sepions.

GEOGRAPHICAL DISTRIBUTION.—Southeast Africa from Port Elizabeth, South Africa, to Somalia (1°31′N).

FIGURE 3.—Sepia aculeata: a, right tentacular club; b, sepion, ventral view; c, geographical distribution.

DISCUSSION.—This is a fully described species of unquestioned status, very closely related to S. madokai Adam and fairly closely to S. rex (Iredale). There is geographical variation in the structure of the sepion dorsal surface (median furrow in South African specimens and rib in northern Mozambiquan specimens). The size is to 110 mm ML, and the usual capture depth is about 200–300 m. This species is potentially of commercial value in southeast Africa.

FIGURE 4.—Sepia acuminata: a,b, dorsal, ventral views of sepion; c, geographical distribution.

Sepia adami Roeleveld, 1972

FIGURE 5

DIAGNOSIS.—Arm suckers quadriserial, arms subequal in length, lateral arms not attenuated distally. Tentacular club short, slightly recurved, with about 5 median suckers enlarged. Skin sparsely papillose (not tuberculate) dorsally on head and mantle. Sepion long-oval, width ∼20% of length, with posterior wings. Spine without keels.

ORIGINAL REFERENCE.—Roeleveld, 1972:224, fig. 10.

TYPE LOCALITY.—S 79° E off Cape Natal, South Africa, depth 99 m.

TYPES.—Holotype: South African Museum A31394, 1 female, shell length 59 mm including spine, good condition. Sepion of holotype somewhat abnormal, apparently damaged and repaired.

Paratypes: South African Museum A30149, 5 females, in good condition except sepions. Same locality as holotype.

GEOGRAPHICAL DISTRIBUTION.—Known only from type locality.

DISCUSSION.—Only the female is known of this species, which is closely related to S. confusa, S. incerta Smith, S. burnupi Hoyle, and S. joubini Massy. It differs from the females of related species in that the arms are not attenuated distally. There are no further records.

FIGURE 5.—Sepia adami: a, sepion, ventral view; b, right tentacular club; c, geographical distribution. (a,b, after Roeleveld, 1972.)

Sepia andreana Steenstrup, 1875

FIGURE 6

DIAGNOSIS.—Mantle length 2.5 times width, elliptical and attenuated posteriorly, fins arising posterior to mantle margin. Arms II of male greatly elongated, bluntly rounded distally, with several chromatophore patches; left arm IV hectocotylized, with suckers of distal images reduced. Arm formula of female II > III > IV > I. Club suckers in 8 rows, median 4 rows about 3 times diameter of marginal row suckers. Sepion slender, lanceolate, anterior margin of striated zone L-shaped but often obtuse, especially in male, inner cone poorly developed. Spine present.

FIGURE 6.—Sepia andreana: a, male, dorsal view; b, left tentacular club; c, sepion, ventral view; d, geographical distribution. (a, after Okutani et al., 1987; b, after Roper et al., 1984.)

ORIGINAL REFERENCE.—Steenstrup, 1875:473, pl. I: figs. 11–19.

TYPE LOCALITY.—Hakodate, Japan.

TYPES.—Lectotype: Muséum National d'Histoire Naturelle, Paris, 1.6.178, 1 male, 65 mm ML; sepion 1.6.181, 65 mm. Designated by Rochebrune, 1884.

Paralectotypes: Zoological Museum, University of Copenhagen, 2 females, 3 males, Hakodate, Japan.

GEOGRAPHICAL DISTRIBUTION.—From northern coasts of Japan to Yellow Sea.

DISCUSSION.—This is a well-defined species characterized by extreme elongation of the second arm pair of the mature male (not differentiated in younger specimens). Size is to 120 mm ML.

Sepia angulata Roeleveld, 1972

FIGURE 7

DIAGNOSIS.—Sepion broad, width 50%–60% of length, with obtuse angle between striated and smooth zones in side view; both zones very flat across ventral surface. Posterior spine or knob absent.

ORIGINAL REFERENCE.—Roeleveld, 1972:242, pls. 44d, 45a–d.

TYPE LOCALITY.—Bloubergstrand, South Africa, 33°48′S, 18°27′E.

TYPES.—Holotype: South African Museum A31317, 1 sepion, 60 mm, in good condition, coll. Roeleveld, 9 Nov 1969.

Paratypes: South African Museum A31318, A31319, A31320, A31395, 11 sepions, in good condition.

GEOGRAPHICAL DISTRIBUTION.—South Africa, Bloubergstrand, 33°48′S, 18°27′E, to Still Bay, 34°23′S, 21°25′E.

DISCUSSION.—The soft parts of the species are not known. This species, attributable to the Sepia sensu stricto species complex, is insufficiently described. It resembles S. papillata and S. simoniana.

Sepia apama Gray, 1849

See Lu (1998a).

Sepia appellöfi Wülker, 1910

FIGURE 8

ILLUSTRATIONS.—Adam and Rees, 1966, pl. 17: fig. 102; pl. 43: fig. 259.

DIAGNOSIS.—Arms subequal in both sexes, suckers quadriserial along entire length. Tentacular club with small subequal suckers in 8 longitudinal rows. Sepion broadly lanceolate. Anterior striae broadly M-shaped. Spine present.

ORIGINAL REFERENCE.—Wülker, 1910:14, figs. 8, 15–18.

TYPE LOCALITY.—Misaki, Japan.

TYPES.—Holotype: Bayrische Staats-Sammlung, Munich.

Paratypes: None.

GEOGRAPHICAL DISTRIBUTION.—Japan, Kyushu to South Honshu.

FIGURE 7.—Sepia angulata: a,b, ventral, lateral views of sepion; c, geographical distribution. (a,b, after Roeleveld, 1972.)

DISCUSSION.—This is a fully described species of unquestioned status. Size is to 90 mm ML.

Sepia arabica Massy, 1916

FIGURE 9

ILLUSTRATIONS.—Adam and Rees, 1966, pl. 23: figs. 152–155; pl. 46: fig. 278.

DIAGNOSIS.—Tentacles very slender, club small, crescent-shaped, with relatively small, subequal suckers in 5 to 6 longitudinal rows. Sepion narrowly teardrop-shaped, width ∼15% of length, very narrow posteriorly, markedly curved ventrally. Inner cone with calcareous ridges radiating from posterior part. Spine absent, keel present posteriorly.

FIGURE 8.—Sepia appellöft: a,b, ventral, dorsal views of sepion; c, geographical distribution. (a,b, after Wülker, 1910.)

FIGURE 9.—Sepia arabica: a, female, dorsal view; b, sepion, ventral view; c, right tentacular club; d, geographical distribution, (a,c, after Massy, 1916; b, after Massy, 1916, and Adam and Rees, 1966.)

ORIGINAL REFERENCE.—Massy, 1916:228, pl. XXIII: figs. 1–5; pl. XXIV: fig. 10.

TYPE LOCALITIES.—Laccadive Sea, 11°14′30″N, 74°57′15″E, depth 125–272 m; Persian Gulf, 26°20′N, 53°54′E, depth 99 m.

TYPES.—Syntypes: Zoological Museum, Calcutta, 2 females, 28 mm ML, 29 mm ML.

GEOGRAPHICAL DISTRIBUTION.—Southern Indian Ocean; Red Sea.

DISCUSSION.—This is a fully described species of unquestioned status. Size is to 70 mm ML.

Sepia aureomaculata Okutani and Horikawa, 1987

FIGURE 10

DIAGNOSIS.—Mantle conical, dorsoventrally compressed. Fins with 6 maculae each. Arms short except arms I. Arms IV flat, without distinct sucker reduction. Tentacular club with 7 rows of suckers, medial 3 suckers huge, 4 to 5 surrounding suckers moderately larger than others. Sepion lanceolate. Inner cone narrowly U-shaped, limbs forming slender ridge anteriorly, reaching broadest part of sepion. Outer cone cup-shaped with deep, L-shaped notch ventrally. Spine present.

FIGURE 10.—Sepia aureomaculata: a, male, dorsal view; b, sepion, ventral view; c, geographical distribution, (a,b, after Okutani et al., 1987.)

ORIGINAL REFERENCE.—Okutani, Tagawa, and Horikawa, 1987:62, figs. A–F.

TYPE LOCALITY.—Tosa Bay, Japan, depth 190–300 m.

TYPES.—Holotype: National Science Museum, Tokyo, Mo.64224, male, 139 mm ML.

Paratypes: National Science Museum, Tokyo: 1 male, Mo.64225, 160 mm ML; 1 male, Mo.64226, sepion, 143 mm including spine.

GEOGRAPHICAL DISTRIBUTION.—Japan, Kii Channel, Tosa Bay, Hyuga-Nada; East China Sea.

DISCUSSION.—This is a fully described species of unquestioned status. The maculae on the fin surface are similar to those observed in Sepia incerta Smith, 1916; the hectocotylus morphology and the inner and outer cone shapes are very different. Size is to 160 mm ML, and the usual capture depth is about 200–400 m.

Sepia australis Quoy and Gaimard, 1832

FIGURE 11

Sepia capensis Orbigny, 1845:278, in Férussac and Orbigny, 1834–1848.

Sepia sinope Gray, 1849:106.

ILLUSTRATIONS.—Adam and Rees, 1966, pl. 21: figs. 138–142; pl. 45: fig. 270. Roeleveld, 1972, pl. 40a: fig. 1, pl. 40b: fig. 3a.

DIAGNOSIS.—Body purple, pigmented as heavily ventrally as dorsally. Tentacular club short, slightly recurved, with 5 suckers in each transverse row, 4 suckers per row proximally; median 3 suckers greatly enlarged, 1 or 2 additional suckers somewhat enlarged. Sepion broadly lanceolate, somewhat oval anteriorly, sharply pointed posteriorly. Striated zone with 3 deep, narrow grooves. Spine with dorsal keel.

FIGURE 11.—Sepia australis: a, sepion, ventral view; b, right tentacular club; c, geographical distribution, (a, after Roeleveld, 1972; b, after Adam and Rees, 1966.)

ORIGINAL REFERENCE.—Quoy and Gaimard, 1832:70.

TYPE LOCALITY.—Agulhas Bank.

TYPES.—Syntypes: Muséum National d'Histoire Naturelle, Paris: 1.6.211, 1 female, 39 mm ML, in poor condition, without sepion; 1.6.194, 1 sepion, 77 mm, damaged.

GEOGRAPHICAL DISTRIBUTION.—Southeastern Atlantic and western Indian Ocean from Namibia (∼26°S) to South Africa; possibly Red Sea. Occurrence in China (as Sepia sinope Gray, 1849) very doubtful.

DISCUSSION.—This species of the Anomalosepia species complex is abundant on the upper shelf from 50–100 m. Size is to 80 mm ML, and the usual capture depth is about 150–300 m.

Sepia bandensis Adam, 1939

FIGURE 12

ILLUSTRATIONS.—Adam and Rees, 1966, pl. 26: figs. 165, 166, pl. 44: fig. 266 .

DIAGNOSIS.—Tentacular club with 5 longitudinal rows of suckers differing in size. Sepion broadly oval in outline, dorsal shield with reticular striation, without ribs. Inner cone relatively narrow, slightly convex. Spine represented by broad, cone-shaped knob.

ORIGINAL REFERENCE.—Adam, 1939a:1.

TYPE LOCALITY.—Banda Neira, Indonesia.

TYPES.—Syntypes: Institut Royal des Sciences Naturelles de Belgique: I.G. 10542, 1 male, 47 mm ML; I.G. 10652, 1 female, 48 mm ML; 3 juveniles, 23 mm ML, 32.5 mm ML, 33 mm ML.

GEOGRAPHICAL DISTRIBUTION.—West Pacific from Philippines to probably North Australia, and from Sulawesi to Marshall Islands.

DISCUSSION.—This is a fully described species of unquestioned status. Size is to 70 mm ML.

Sepia bartletti (Iredale, 1954)

DIAGNOSIS.—Sepion oval with calcareous outer cone, dorsal surface without sculpture. Inner cone resembling that of S. baxteri but smaller. Striated zone without sulcus or groove, last loculus with shallow depression medially and never more elevated than margin. Spine absent.

ORIGINAL REFERENCE.—Iredale, 1954:67, pl. 5: figs. 15, 16.

TYPE LOCALITY.—Misima, Louisiade Archipelago, southeast of Papua New Guinea.

TYPES.—Holotype: Australian Museum, Sydney, C133318, 1 sepion extant, 73.3 mm.

Paratypes: ? 6 sepions deposited in Australian Museum.

GEOGRAPHICAL DISTRIBUTION.—Misima, Louisiade Archipelago.

FIGURE 12.—Sepia bandensis: a, sepion, ventral view; b, geographical distribution; c, right tentacular club. (a,c, after Adam and Rees, 1966.)

DISCUSSION.—This species was originally described as Blandosepia bartletti and is known only from the type and six other specimens reported by Iredale (1954); the soft parts are unknown. This species is known only from the waters of Papua New Guinea, and it is removed from the Australian fauna; its status is uncertain at present.

Sepia bathyalis Khromov, Nikitina, and Nesis, 1991

FIGURE 13

DIAGNOSIS.—Body elongate. Arms I–III of female with 2 widely separated rows of suckers; protective membranes at end of arms widened and curved orally. Tentacular club suckers unequal, in about 5 longitudinal rows, middle row with 3 greatly enlarged suckers. Sepion nearly 4 times longer than wide, with rather indistinct medial groove on ventral side. Anterior striae very shallowly M-shaped. Inner cone reduced, with barely noticeable limbs. Spine spindle-shaped.

FIGURE 13.—Sepia bathyalis: a, male, dorsal view; b,c, dorsal, ventral views of sepion; d, left tentacular club, e, geographical distribution, (a–d, from Khromov et al., 1987b.)

ORIGINAL REFERENCE.—Khromov, Nikitina, and Nesis, 1991:18, pl. 3: figs. a–m.

TYPE LOCALITY.—Madagascar, 22°19′–22°23′S, 43°06′E, depth 325–332 m.

TYPES.—Holotype: Zoological Museum, Moscow University, N Y361, male, 56 mm ML.

Paratypes: Zoological Museum, Moscow University, 4 males, 22–61 mm ML, 3 females, 36–76 mm ML.

GEOGRAPHICAL DISTRIBUTION.—Northwestern and southwestern Madagascar.

DISCUSSION.—This is a fully described species of unquestioned status. Size is to 80 mm ML, and the usual capture depth is about 300–350 m.

Sepia baxteri (Iredale, 1940)

See Lu (1998a).

Sepia bertheloti Orbigny, 1839

FIGURE 14

Sepia verrucosa Lönnberg, 1896:697 [Teneriffe, Canary Islands].

Sepia mercatoris Adam, 1937:56 [Rufisque, Senegal, 14°43′N, 17°16′W].

DIAGNOSIS.—Tentacular club slender, swimming keel not extended beyond base; protective membranes not united proximally and not extended onto stalk; suckers arranged in 8 oblique transverse rows, third in series slightly enlarged. Hectocotylus with 2–5 normal suckers at base and 9–13 rows of minute, spaced-out suckers on proximal images; dorsal protective membrane very broad. Sepion long-oval, limbs of inner cone flat, narrow. Spine present.

ORIGINAL REFERENCE.—Orbigny, 1839:21, pl. II.

TYPE LOCALITY.—Teneriffe, Canary Islands.

TYPES.—Syntypes: Muséum National d'Histoire Naturelle, Paris: 1.4.75, 1 mature female, 90 mm ML. in poor condition, without sepion; 1.4.76, 1 mature male, without sepion; 1.4.77, 3 sepions, 37.5 mm, 56.6 mm, 82+ mm (incomplete).

GEOGRAPHICAL DISTRIBUTION.—Eastern Atlantic, from Canary Islands to 14°S.

DISCUSSION.—Maximal mantle length is 175 mm in the male, 130 mm in the female, and the usual capture depth is about 50–150 m.

FIGURE 14.—Sepia bertheloti: a, sepion, ventral view; b, right tentacular club; c, geographical distribution.

Sepia braggi Verco, 1907

See Lu (1998a).

FIGURE 15.—Sepia brevimana: a, sepion, ventral view; b, geographical distribution. (a, after Adam and Rees, 1966.)

Sepia brevimana Steenstrup, 1875

FIGURE 15

Sepia winckworthi Adam, 1939d:1.

ILLUSTRATIONS.—Adam and Rees, 1966, pl. 2: fig. 6 .

DIAGNOSIS.—Arm suckers quadriserial. Tentacular club with small equal suckers in 5 longitudinal rows. Sepion oval, sometimes with dorsal and ventral keels, and with slight anterior protuberance. Striated zone with thin median furrow. Anterior striae rounded. Inner cone with wide, flat, trapezoidal ventral ledge around pocket-like cavity. Spine long.

ORIGINAL REFERENCE.—Steenstrup, 1875:475.

TYPE LOCALITY.—Indian Ocean.

TYPES.—Lectotype: Zoological Museum, University of Copenhagen, 4–3–1867, male, 46 mm ML.

Paralectotype: Zoological Museum, University of Copenhagen, male, 45 mm ML, same locality.

GEOGRAPHICAL DISTRIBUTION.—Indo-West Pacific from Andaman Sea to Gulf of Tonkin, including Java, Sulu, and Celebes seas. (Absent in Arabian Sea and probably west of 93°E; all data on geographical distribution in this region based on sepions only.)

DISCUSSION.—This is a fully described species of unquestioned status. Animals described from the Arabian Sea and Bengal Bay (Silas et al., 1985:6) are S. thurstoni, not S. brevimana. Size is to 110 mm ML, and the usual capture depth is about 20–100 m. This species is commercially important in the South China Sea and Gulf of Thailand.

Sepia burnupi Hoyle, 1904

FIGURE 16

Sepia exsignata Barnard, 1962:250 [off Umhlanga River, South Africa].

ILLUSTRATIONS.—Adam and Rees, 1966, pl. 20: fig. 128; Roeleveld, 1972, fig. 8 a,c-e.

DIAGNOSIS.—Arms I and IV of male with peculiar transformed protective membranes, membranes represented by spear-like processes. Left arm IV longer than right arm. Arms of female with quadriserial suckers along entire length. Club suckers in oblique rows of 8; 5 very large suckers in proximal images. Sepion elongate-lanceolate. Striated zone shallow, M-shaped in cross section (i.e., with median ventral groove). Anterior striae L-shaped. Inner cone low posteriorly, limbs raised, lying on striated zone margins. Spine present.

FIGURE 16.—Sepia burnupi: a, sepion, ventral view; b, hectocotylized left ventral arm of male; c, modified dorsal arm of male; d, left tentacular club; e, geographical distribution. (a–d, after Roeleveld, 1972.)

ORIGINAL REFERENCE.—Hoyle, 1904a:27.

TYPE LOCALITY.—Umkomaas, Natal, South Africa.

TYPES.—Holotype: The Natural History Museum, London, 1905.1.19.5, sepion.

Paratype: The Natural History Museum, London, 1904.2.13.5, sepion.

GEOGRAPHICAL DISTRIBUTION.—Southeast Africa from Port Elizabeth, South Africa, to Zambezi estuary, South Mozambique.

DISCUSSION.—The first description of the species was published by Barnard (1962) as S. exsignata (caught at 40–48 m depth). The species is of unquestioned status; however, the female is insufficiently described. The female and the sepion are similar to S. trygonina. Marked sexual dimorphism occurs in the length of the arms and the structure of protective membranes, with females having normal arms. Size is to 60 mm ML, and the usual capture depth is about 100–200 m.

Sepia carinata Sasaki, 1920

FIGURE 17

ILLUSTRATIONS.—Sasaki, 1929, pl. XVII: fig. 6 a,d; Khromov, 1988b, fig. la.

DIAGNOSIS.—All arms of both sexes subequal in length, with quadriserial suckers along entire length. Club suckers in 8 longitudinal rows, at least 3 suckers in proximal part of submedial row greatly enlarged. Sepion broadly lanceolate (close to Rhombosepion form but with small, distinct wings typical of Doratosepion). Anterior striae rounded. Inner cone more or less flattened, with narrow, flat limbs. Spine present.

ORIGINAL REFERENCE.—Sasaki, 1920:192.

TYPE LOCALITY.—Japan, Sagami Sea, R/V Albatross station 5092, 35°04′50″N, 139°38′18″E, depth 128 m.

TYPES.—Holotype: National Museum of Natural History, Washington, D.C., USNM 332849, male, 26 mm ML.

Paratype: National Museum of Natural History, Washington, D.C., USNM 332848, 1 female, 25 mm ML.

GEOGRAPHICAL DISTRIBUTION.—Southern Japan.

DISCUSSION.—This species is of unquestioned status, but the adult female has not been described. The adult male was described by Khromov (1988b). It is an atypical species of the Doratosepion species complex (transitional to Rhombosepion). Size is to 60 mm ML.

Sepia chirotrema Berry, 1918

See Lu (1998a).

FIGURE 17.—Sepia carinata: a, sepion, ventral view; b, geographical distribution; c, male, dorsal view; d, left tentacular club.

Sepia confusa Smith, 1916

FIGURE 18

Sepia burnupi Hoyle, 1904a:27 [in part].

ILLUSTRATIONS.—Adam and Rees, 1966, pl. 18: figs. 112, 113; pl. 42: fig. 248; Roeleveld, 1972, figs. 4, 5.

DIAGNOSIS.—Male with posteriorly fused and greatly elongated fins forming “tail.” Protective membranes on tips of arms I in female expanded, covering suckers. Club suckers in 8 longitudinal rows distally, 9 median suckers variously enlarged, 5 very large. Sepion long, lanceolate. Anterior striae M-shaped. Inner cone strongly raised posteriorly. Posterior margin of outer cone rather sharp, turned outward and backward. Spine present.

ORIGINAL REFERENCE.—Smith, 1916:24.

FIGURE 18.—Sepia confusa: a, male, ventral view; b, sepion, ventral view; c, detail of sepion inner and outer cones; d, left tentacular club; e, geographical distribution. (a, after Roeleveld, 1972; b,d, after Adam and Rees, 1966.)

TYPE LOCALITY.—Port Elizabeth, Natal, South Africa.

TYPES.—Holotype: The Natural History Museum, London, 1920.3.23.1, sepion.

Paratype: The Natural History Museum, London, 1890.12.14.42, sepion fragment.

GEOGRAPHICAL DISTRIBUTION.—Southeast Africa from Port Elizabeth, South Africa, to South Mozambique and east to South Madagascar.

DISCUSSION.—This is a fully described species of unquestioned status. The animal was described by Massy and Robson (1923). A marked sexual dimorphism occurs in the fin structure and protective membranes of the arms. The female is similar to S. joubini and S. ivanovi. Size is to 150 mm ML (excluding “tail”), and the usual capture depth is about 100–300 m.

Sepia cottoni Adam, 1979

See Lu (1998a).

Sepia cultrata Hoyle, 1885

See Lu (1998a).

Sepia dannevigi Berry, 1918

See Lu (1998a).

Sepia dollfusi Adam, 1941

FIGURE 19

Sepia lefebrei Hoyle, 1907:35.

DIAGNOSIS.—Swimming membrane of tentacular club extended slightly beyond base of club, protective membranes separated at base of club. Tentacular club suckers subequal, in 8 longitudinal rows, median suckers of 4th row from dorsal margin slightly larger than others. Left arm IV hectocotylized with 5 rows of normal suckers basally, followed by 8 rows of smaller suckers distally, remaining suckers normal. Sepion broadly oval, rounded at both ends; ventral surface keeled in middle along nearly entire length of striated zone except flat posterior part, narrow groove in middle of rounded keel. Limbs of inner cone broad and completely fused to outer cone. Striated zone concave on both sides of keel. Last loculus convex in posterior central part, flattened toward anterior and lateral margins. Spine or knob absent.

ORIGINAL REFERENCE.—Adam, 1941a:12, pl. II: fig. 3 .

TYPE LOCALITY.—Périm Island, Red Sea, M. Jousseaume, coll., 1891–1893.

TYPES.—Holotype: Muséum National d'Histoire Naturelle, Paris, 1.6.182, female, 103 mm ML.

Paratype: Muséum National d'Histoire Naturelle, Paris, sepion, 92 mm, Suez, Ph. Dautzenberg, coll., 8-X-1892.

GEOGRAPHICAL DISTRIBUTION.—Red Sea; Suez Canal.

FIGURE 19.—Sepia dollfusi: a,b, ventral, lateral views of sepion; c, right tentacular club; d, geographical distribution, (c, after Adam and Rees, 1966.)

DISCUSSION.—The holotype was originally identified as S. lefebrei by Férussac. The mantle of the holotype was opened during the workshop, and mature eggs ∼5 mm in diameter were in the ovary. The sepion in this specimen is T-shaped in cross section (similar to S. gibba) but is more triangular in other specimens. This is a rarely found species. The size is to 110 mm ML.

Sepia dubia Adam and Rees, 1966

FIGURE 20

DIAGNOSIS.—Mantle as in S. typica but fleshy ridges on ventral surface of mantle without pores. Ventral mantle emargination trapezoidal. Anterior end of sepion with nose-like tip but less acuminate than in S. typica.

ORIGINAL REFERENCE.—Adam and Rees, 1966:119, pl. 34: figs. 198–201, pl. 46: fig. 272 .

TYPE LOCALITY.—South Africa, False Bay, 34°11′S, 18°27′E, depth 25 m.

TYPES.—Holotype: The Natural History Museum, London, 1963.103W, female, 17 mm ML, in good condition, sepion damaged (only known specimen).

Paratypes: None.

GEOGRAPHICAL DISTRIBUTION.—Same as type locality.

DISCUSSION.—This species falls into the Hemisepius species complex; however, it is insufficiently described.

FIGURE 20.—Sepia dubia: a,b, dorsal, ventral views of sepion; c, left tentacular club; d, geographical distribution. (a–c, after Adam and Rees, 1966.)

Sepia elegans Blainville, 1827

FIGURE 21

Sepia biserialis Blainville, 1827:284.

Sepia italica Risso, 1854:13.

Sepia rupellaria Férussac and Orbigny, 1835–1848:275, 280 [Bay of Biscay].

ILLUSTRATIONS.—Adam and Rees, 1966, pl. 23: figs. 148–151; Adam, 1952, fig. 7 .

DIAGNOSIS.—Mantle elongate, more than 2 times longer than wide, dorsal margin projecting strongly. Arms subequal, with biserial suckers basally. Tentacular club short, blunt, with ∼80 suckers distally in 6–8 rows, 1 median longitudinal series with 3 greatly enlarged suckers. Sepion lanceolate, length ∼3.5 times width. Spine absent but ridge present, small lateral wings present.

ORIGINAL REFERENCE.—Blainville, 1827:284.

FIGURE 21.—Sepia elegans: a,b, ventral, lateral views of sepion; c, right tentacular club; d, geographical distribution. (a,b, after Adam and Rees, 1966; c, after Adam, 1952.)

TYPE LOCALITY.—Sicily, Mediterranean Sea.

TYPES.—Holotype: Muséum National d'Histoire Naturelle, Paris, missing.

GEOGRAPHICAL DISTRIBUTION.—Eastern Atlantic (around British Isles) from 50°N through Mediterranean to 15°S, West Africa; Agulhas Bank.

DISCUSSION.—The size is to 90 mm ML, and the usual capture depth is about 100–400 m.

Sepia elliptica Hoyle, 1885

See Lu (1998a).

Sepia elobyana Adam, 1941

FIGURE 22

ILLUSTRATIONS.—Adam, 1952, fig. 11; Adam and Rees, 1966, pl. 25: figs. 162–164.

DIAGNOSIS.—Animals mature at small size (maximal ML 53 mm); mantle broad, dorsal surface with scattered tubercles and peculiar reticulate pattern of ridges. Fins broad. Tentacular club with small subequal suckers (but see “Discussion”) in about 8 longitudinal rows. Suckers on arms I of female biserial proximally and quadriserial distally. Spine represented by blunt knob.

ORIGINAL REFERENCE.—Adam, 1941c:121, fig. 12 .

TYPE LOCALITY.—West Africa, Gulf of Guinea, Eloby Island, 01°01′N, 09°29′E.

TYPES.—Holotype: Zoologisches Museum der Universitat Hamburg E.K.7453, mature male, 41 mm ML.

Paratypes: None.

GEOGRAPHICAL DISTRIBUTION.—Eastern Atlantic along West African coast from Senegal to Gulf of Guinea (southern limits undetermined).

DISCUSSION.—The tentacular club suckers in the holotype differ from those of the Senegal specimens by having some enlarged suckers and were thought by Adam (1952) to be anomalous. If the combined specimens constitute more than one species, the name must remain with the holotype, which clearly has some enlarged club suckers. The differences of relative width of the sepion in the holotype and in male specimens from other localities or Senegal strongly suggest different species.

Sepia elongata Orbigny, 1845, in Férussac and Orbigny, 1835–1848

FIGURE 23

ILLUSTRATIONS.—Adam and Rees, 1966, pl. 21: figs. 132, 133.

DIAGNOSIS.—Mantle elongate, pointed posteriorly, dorsal margin slightly projecting. Tentacular club small, crescent-shaped, with unequal suckers, 5 central suckers enlarged. Sepion very elongate, width about 16% of length, thickness nearly 12% of length. Inner cone sharply V-shaped with elevated, narrow limbs. Outer cone forming posterior expansion between inner cone and spine.

ORIGINAL REFERENCE.—Orbigny, 1845, in Férussac and Orbigny, 1835–1848:289.

TYPE LOCALITY.—Near Cosseir, Red Sea.

TYPES.—Lectotype: Muséum National d'Histoire Naturelle, Paris, 1–6–197, damaged sepion.

GEOGRAPHICAL DISTRIBUTION.—Red Sea.

FIGURE 22.—Sepia elobyana: a, sepion, ventral view; b, left tentacular club; c, geographical distribution. (a, after Adam and Rees. 1966; b, after Adam, 1952.)

DISCUSSION.—This species is known only from the type (sepion) and one male specimen described by Adam (1941b). The sepion is distinct from other Red Sea species and is similar (although much thicker anteriorly) to S. braggi of Australian waters. The species is probably valid but is poorly known and apparently is uncommon. The size is to about 100 mm ML.

FIGURE 23.—Sepia elongata: a,b, ventral, lateral views of sepion; c, geographical distribution. (a,b, after Adam and Rees, 1966.)

Sepia erostrata Sasaki, 1929

FIGURE 24

ILLUSTRATIONS.—Okutani et al., 1987:44.

DIAGNOSIS.—Mantle about twice as long as wide; fins starting slightly behind anterior edge of mantle. Arm formula I>IV>II = III; arms I and IV of male much longer than other arms, keel very prominent. Tentacular club oval to crescent-shaped, with low aboral web and about 100 suckers in 7 to 8 longitudinal rows, a few enlarged suckers in central rows. Sepion lanceolate. Anterior margin of striated zone with indentations shallow to nearly semicircular. Inner cone narrow, outer cone cup-shaped, slanting, with very distinct wings. Spine obtuse.

ORIGINAL REFERENCE.—Sasaki, 1929:183, pl. 17: figs. 7–9.

TYPE LOCALITY.—Japan, Sagami Bay, Manazuru.

TYPES.—Holotype: National Science Museum, Tokyo, male, 45 mm ML.

Paratypes: None.

GEOGRAPHICAL DISTRIBUTION.—Sagami Bay to Kii Peninsula, Japan; intertidal.

DISCUSSION.—The species is distinguished from S. kobiensis by the more rounded mantle, thicker tentacular stalk, and very obtuse spine on the sepion (Okutani et al., 1987). The description of the tentacular club in Okutani et al. (1987) is in contradiction with the photograph (Okutani et al., 1987:44), which clearly shows a few enlarged suckers. The size is to 90 mm ML.

FIGURE 24.—Sepia erostrata: a,b. ventral, lateral views of sepion; c, tentacular club; d, geographical distribution. (a–c, after Sasaki, 1929.)

Sepia esculenta Hoyle, 1885

FIGURE 25

?Sepia elliptica Hoyle, 1885:189 [not Sepia whitleyana Iredale, 1926a].

ILLUSTRATIONS.—Adam and Rees, 1966, pl. 6: figs. 30–33, pl. 43: fig. 263; Adam, 1979: pl. 9: fig. 2 .

DIAGNOSIS.—Tentacular club with subequal suckers in 10–12 longitudinal rows. Sepion oval. Striated zone with deep, broad median furrow. Anterior striae L-shaped. Inner cone with wide, flat, trapezoidal ventral ledge behind pocket-like cavity. Spine present.

ORIGINAL REFERENCE.—Hoyle, 1885:188.

TYPE LOCALITY.—Japan, Yokohama market.

TYPES.—Syntypes: The Natural History Museum, London: 1889.4.24.69, 1 male, 160 mm ML; 1889.4.24.70, 1 female, 143 mm ML.

GEOGRAPHICAL DISTRIBUTION.—West Pacific to Tokyo and Tsingtao, including Indonesia (taking into account geographical distribution of S. elliptica). Probably absent west of 100°E in the Indian Ocean because Indian data on the animal of S. elliptica (Silas et al., 1985) relate to S. stellifera.

DISCUSSION.—A fully described species of unquestioned status. The size is to 180 mm ML, and the usual capture depth is about 10–100 m. It is of great commercial value in Korea, Japan, China, and Thailand.

FIGURE 25.—Sepia esculenta: a, right tentacular club; b, male, dorsal view; c, sepion, ventral view; d, geographical distribution.

FIGURE 26.—Sepia faurei: a, female, ventral view; b, sepion, ventral view; c, right tentacular club; d, geographical distribution. (a–c, after Roeleveld, 1972.)

Sepia faurei Roeleveld, 1972

FIGURE 26

DIAGNOSIS.—Anterior mantle margin deeply emarginate ventrally, skin densely papillose dorsally on head, mantle, and arms. Fleshy ridge present on either side of mantle ventrally, without pores. Tips of arms I finger-like, devoid of suckers and protective membranes, suckers biserially arranged on all arms. Tentacular club broad, with few (30–35) subequal suckers in transverse rows of 4–6; swimming membrane very broad, continuing along stalk.

ORIGINAL REFERENCE.—Roeleveld, 1972:251–257, figs. 15, 16.

TYPE LOCALITY.—South Africa, S 14°E of Cape Seal 88 km, 35°00′S, 23°07′E, depth 168 m.

TYPES.—Holotype: South African Museum A30144, female, 21 mm ML, in good condition; sepion mounted on slide.

Paratypes: None.

GEOGRAPHICAL DISTRIBUTION.—Same as type locality.

DISCUSSION.—This species falls into the Hemisepius species complex. The anterior margin of the phragmocone is convex. The biology of the species is unknown.

Sepia foliopeza Okutani and Tagawa, 1987

FIGURE 27

DIAGNOSIS.—Mantle oval in outline, with round posterior end. Mantle width 60% of length. Fins very narrow, starting several mm behind anterior mantle margin. Arms I in male transformed, without aboral keel, with sparsely set quadriserial suckers. Club suckers in about 8 longitudinal rows, minute and subequal in size. Sepion lanceolate, width about 27% of length. Anterior margin of striated zone shallow, M-shaped. Inner cone forming U-shaped sharp ridge. Outer cone shallow, with nearly straight ventral margin. Spine present.

ORIGINAL REFERENCE.—Okutani, Tagawa, and Horikawa, 1987:66, figs. A–D.

TYPE LOCALITY.—East China Sea.

TYPES.—Holotype: National Science Museum, Tokyo, 64232, male, 106 mm ML.

Paratype: National Science Museum, Tokyo, 64233, 1 male, 100 mm ML, from East China Sea.

GEOGRAPHICAL DISTRIBUTION.—East China Sea.

DISCUSSION.—The fairly wide and pinkish sepion of this species suggests a relationship to the Sepia lorigera group within the Doratosepion species complex, but the fern-leaf-like modification of arms I in the male is unique (other Doratosepion species have equally unusual and unique arm modifications, all different from each other). The size is to 110 mm ML.

FIGURE 27.—Sepia foliopeza: a, male, dorsal view; b, dorsal arm of male; c, sepion, ventral view; d, geographical distribution. (a,c, after Okutani et al., 1987.)

Sepia gibba Ehrenberg, 1831

FIGURE 28

ILLUSTRATIONS.—Adam and Rees, 1966, pl. 25: figs. 159–161.

DIAGNOSIS.—Mantle broadly conical, widest at opening. Ventral margin slightly emarginate. Swimming membrane of tentacular club same length as club, protective membrane separated at base of club. Arm suckers in adults tetraserial except at extreme tips where suckers biserial. Left arm IV of male hectocotylized with 7 rows of normal suckers basally followed by 7 or 8 rows of modified suckers, ventral pairs slightly smaller, dorsal pairs minute. Sepion elongate, dorsal surface granulose, nearly flat with faint indication of median rib; ventral surface dominated by abruptly raised, central striated area, broadening anteriorly toward last loculus. Last loculus as very high protuberance. Striae strongly convex on both sides of protuberance. Inner cone with wide limbs completely fused to outer cone, forming rounded marginal rim, slightly raised in rounded posterior part. Spine absent.

ORIGINAL REFERENCE.—Ehrenberg, 1831: unpaginated.

TYPE LOCALITY.—Red Sea.

TYPES.—Holotype: Zoologisches Museum der Humboldt-Universität Berlin, No. 92.

GEOGRAPHICAL DISTRIBUTION.—Red Sea.

DISCUSSION.—This is a rarely encountered species closely related to S. dollfusi. The size is to 100 mm ML.

Sepia hedleyi Berry, 1918

See Lu (1998a).

Sepia hieronis (Robson, 1924)

FIGURE 29

ILLUSTRATIONS.—Adam and Rees, 1966, pl. 43: fig. 262; Roeleveld, 1972, fig. 13 a, pl. 43.

DIAGNOSIS.—Tentacular club with subequal suckers in 5 longitudinal rows. Lateral arms with several medial suckers enlarged, especially in male. Sepion without spine but with blunt knob. Anterior striae with 3 rounded peaks.

ORIGINAL REFERENCE.—Robson, 1924b:645.

TYPE LOCALITIES.—South Africa, Cape Town, 32°32′–33°03′S, 17°29′–17°42′E.

TYPES.—Syntypes: The Natural History Museum, London: 1924.9.9.54–55, 1 male, 44 mm ML, without sepion, 1 female, 50 mm ML, without sepion, 1 sepion, 48 mm, 1 sepion, 58 mm; 1924.9.9.56, 1 ?female, without sepion, in very poor condition, 31 mm ML, 1 sepion, 42 mm. Soft parts more or less shrunken!

GEOGRAPHICAL DISTRIBUTION.—South and East Africa from 17°S (Atlantic) to Kenya (Indian Ocean).

FIGURE 28.—Sepia gibba: a,b, ventral, lateral views of sepion; c, geographical distribution. (a,b, after Adam and Rees, 1966.)

DISCUSSION.—This is a fully described species and is possibly two species (M. Roeleveld, pers. comm.). There is geographical variation in size (Atlantic specimens attain larger size) and in shape of the sepion. The size is to 70 mm ML, and the usual capture depth is about 200–400 m.

FIGURE 29.—Sepia hieronis: a, left tentacular club; b,c, ventral, lateral views of sepion; d, geographical distribution.

FIGURE 30.—Sepia hierredda: a,b, dorsal, ventral views of sepion; c, left tentacular club; d, geographical distribution. (a–c, after Adam, 1952.)

Sepia hierredda Rang, 1837

FIGURE 30

Acanthosepion goreense Rochebrune, 1884:109.

Acanthosepion oculifera Rochebrune, 1884:107.

DIAGNOSIS.—Maximal mantle length 450 mm. Left arm IV hectocotylized, with 8–13 rows of reduced suckers and 6 normal suckers. Tentacular club length 19%–24% of mantle length, with 8 oblique rows of suckers, median suckers of proximal rows moderately enlarged.

ORIGINAL REFERENCE.—Rang, 1837:75, pl. 100.

TYPE LOCALITY.—Western Africa.

TYPES.—Syntypes: Muséum National d'Histoire Naturelle, Paris: 1.4.66, 1 female, 98 mm ML; 1.6.195, 1 male, 76 mm ML.

GEOGRAPHICAL DISTRIBUTION.—From Cape Blanc, Mauritania, 19°N, to Tigres Bay, Angola, 16°30′S.

DISCUSSION.—This species has been long considered as a subspecies of S. officinalis. The sepion has a concave lateral outline in the anterior one-third, in contrast to a convex outline in S. officinalis; see S. vermiculata, below, for differences between these closely related species. It is a neritic species caught to depths of around 120 m with a size to nearly 500 mm ML. Females mature at 130 mm ML. Spawning takes place from February to September and the life span is two years. The species is of commercial importance.

Sepia incerta Smith, 1916

FIGURE 31

Sepia burnupi Hoyle, 1904a:27 [in part].

ILLUSTRATIONS.—Roeleveld, 1972, fig. 6 c,d, pl. 39.

DIAGNOSIS.—Arms I of male much longer than other arms, with transformed protective membranes of thick, narrow, fleshy ribs separated by membranous parts. Tentacular club with suckers in 6–8 longitudinal rows, about 5 suckers greatly enlarged in proximal art of medial rows. Sepion long, with narrow furrow on ventral side. Anterior striae L-shaped. Inner cone with longitudinal groove in transverse posterior ledge. Outer cone with fringe-like excrescence posteriorly. Spine present.

ORIGINAL REFERENCE.—Smith, 1916:23.

TYPE LOCALITY.—South Africa, Tongaat and Port Elizabeth.

TYPES.—Syntypes: The Natural History Museum, London, 1890.12.14.43–44, fragments of sepions.

GEOGRAPHICAL DISTRIBUTION.—South and East Africa from Port Elizabeth to Zambezi River mouth.

DISCUSSION.—This is a fully described species of unquestioned status. Massy (1925) described the animal. Sexual dimorphism occurs in arm length and in the structure of the protective membranes (females have normal arms). The size is to 150 mm ML, and the usual capture depth is about 100–350 m.

Sepia insignis Smith, 1916

FIGURE 32

ILLUSTRATIONS.—Adam and Rees, 1966, pl. 31: figs. 189–191; Roeleveld, 1972, fig. 14 , pl. 44: figs. a-c.

DIAGNOSIS.—Tentacular club small, with subequal suckers in about 8 longitudinal rows; male animal unknown. Sepion elongate, sharply acuminate anteriorly, posterior art-art about equal in width, rounded posteriorly. Striated zone long, narrowing markedly posteriorly; median longitudinal groove present over striated zone, continuing along last loculus. Anterior striae L-shaped. Inner cone well developed posteriorly, completely reflexed and fused to outer cone; with increasing size, limbs of inner cone increasingly distant from edge of phragmocone. Spine absent but blunt knob present.

ORIGINAL REFERENCE.—Smith, 1916:25, pl. II: fig. 10 .

TYPE LOCALITY.—South Africa, Natal, Tongaat, on beach, 29°35′S-31°07′E. Sepions only.

TYPES.—Syntypes: The Natural History Museum, London, 1920.3.23.5, sepion 26 mm; second syntype apparently lost.

GEOGRAPHICAL DISTRIBUTION.—Animal: South Africa, False Bay, 34°15′S-18°47′E, depth 42 m. Sepions: South Africa, Bloubergstrand to Tongaat (on beach).

FIGURE 31.—Sepia incerta: a,b, lateral, ventral views of sepion; c, arm I of male; d, posterior sepion, ventral view; e, geographical distribution. (a–d, after Roeleveld, 1972.)

DISCUSSION.—Until Roeleveld (1972) studied the species, only sepions were known. The species is insufficiently described; one poorly preserved female (SAM-A31247) was found in the collections of the University of Cape Town Ecological Survey. This species is related to S. hieronis.

FIGURE 32.—Sepia insignis: a,b, dorsal, lateral views of sepion; c, right tentacular club; d, geographical distribution. (a–c, after Roeleveld, 1972.)

Sepia irvingi Meyer, 1909

See Lu (1998a).

Sepia ivanovi Khromov, 1982

FIGURE 33

ILLUSTRATIONS.—Khromov, 1982, figs. 1, 4, 5, 6a, 7a.

DIAGNOSIS.—Arms of both sexes, except arms I, as long as mantle, with transformed protective membranes of thick, narrow, fleshy ribs separated by membranous parts. Sepion long, with narrow furrow on ventral side. Anterior striae M-shaped, posterior striae almost straight. Inner cone U-shaped. Outer cone with distinct lateral wings. Spine prominent.

ORIGINAL REFERENCE.—Khromov, 1982:137.

TYPE LOCALITY.—Kenya, Mombasa, 04°03′S, 40°00′E, depth 44 m.

TYPES.—Holotype: Zoological Museum, Moscow University, N 172.

Paratype: Zoological Museum, Moscow University, N 173.

GEOGRAPHICAL DISTRIBUTION.—Kenya, Mozambique, probably throughout central East Africa.

DISCUSSION.—This is a fully described species of unquestioned status. The size is to 70 mm ML.

Sepia joubini Massy, 1927

FIGURE 34

DIAGNOSIS.—Animals mature at small size (maximal ML 50 mm). Tentacular club with many small subequal suckers distally in obliquely set transverse rows of 8, 4 median basal suckers greatly enlarged. Male with red spots on arms, unmodified arms I, and rounded fins. Female with expanded protective membranes distally on arms. Sepion with narrow inner cone, limbs lying on lateral smooth zones. Anterior striae L-shaped, with small indentation in median furrow. Spine present.

ORIGINAL REFERENCE.—Massy, 1927:161, pl. XVIII: figs. 1–10.

TYPE LOCALITIES.—South Africa, Tugela River mouth, NW by N, artN, 25 km, depth 66–77 m; Cape Natal (The Bluff, Durban, 29°53′S, 31°03′E), W by N, 10.5 km, depth 99 m.

TYPES.—Syntypes: The Natural History Museum, London: 1926.10.20.38, 1 female, 47 mm ML, Tugela River; 1926.10.2039–40, 1 male, 1 female, Cape Natal, sepions damaged.

GEOGRAPHICAL DISTRIBUTION.—South Africa, off Tugela River mouth, ∼29°11′S, 31°25′E, to South Mozambique.

DISCUSSION.—The biology of this species is unknown. The size is to 65 mm ML.

Sepia kobiensis Hoyle, 1885

FIGURE 35

Sepia andreanoides Hoyle, 1885:193.

Sepia kobiensis Sasaki, 1929:204.

Sepia kobiensis var. andreanoides Sasaki, 1929:206.

Sepia kobiensis var. toyamensis Sasaki, 1929:209.

Sepia kobiensis var. beppuana Sasaki, 1929:211.

Sepia kobiensis var. crassa Sasaki, 1929:213.

Sepia kobiensis var. albatrossi Sasaki, 1929:214.

?Sepia kiensis Hoyle, 1885:194.

DIAGNOSIS.—Mantle width less than art length; fins narrow, with slightly acute posterior ends. Arms short, suckers globular, quadriserial, those of median rows larger; left arm IV of male hectocotylized by reduction of distal suckers. Tentacular club narrow, suckers small, in 8 longitudinal rows; suckers of third row enlarged. Sepion lanceolate. Anterior striae shallowly M-shaped. Inner cone forming thick, posteriorly U-shaped structure. Spine prominent.

ORIGINAL REFERENCE.—Hoyle, 1885:193.

TYPE LOCALITY.—Japan, Kobe Bay, 34°39′N, 135°14′E, depth 15 m.

TYPES.—Holotype: The Natural History Museum, London, 1889.4.24.81, female.

OTHER TYPE MATERIAL.—Syntypes: Sepia andrenoides Hoyle, 1885, The Natural History Museum, London, 1889.4.24.78–79, 1 male, 1 female, Japan, Yokohama market.

FIGURE 33.—Sepia ivanovi: a, male, dorsal view; b, geographical distribution; c, arm I of male; d, arm III of male; e, sepion, ventral view; f, posterior sepion, ventral view (a–f, after Khromov, 1982).

FIGURE 34.—Sepia joubini: a, sepion, ventral view; b, left tentacular club; c, geographical distribution. (a, after Roeleveld, 1972; b, after Adam, 1952.)

Holotype: Sepia kobiensis albatrossi Sasaki, 1920, National Museum of Natural History, Washington, D.C., USNM 332862, male, 34 mm ML, poor condition.

GEOGRAPHICAL DISTRIBUTION.—East China Sea, South China Sea, waters of Japan, Indo-Malayan waters.

DISCUSSION.—The size is to 90 mm ML, and the usual capture depth is about 100–200 m.

Sepia latimanus Quoy and Gaimard, 1832

See Lu (1998a).

FIGURE 35.—Sepia kobiensis: a,b, dorsal, ventral views of sepion; c, left tentacular club; d, geographical distribution. (a–c, after Sasaki, 1929.)

Sepia longipes Sasaki, 1914

FIGURE 36

DIAGNOSIS.—Mantle wide, roughly oval in outline; fins wide, maximal width of fin muscles about art that of body, free margin much narrower. Arms I of male about twice as long as other arms; arm formula I > II > III > IV. Arms subequal in female. Left arm IV of male hectocotylized, suckers reduced on distal 40% of length. Tentacular club large, with 4 or 5 longitudinal rows of suckers, central 4 suckers greatly enlarged. Sepion lanceolate. Striated zone with high medial ridge continuing into longitudinal groove on last loculus. Anterior striae on ventral side roughly M-shaped but with rounded tips. Inner cone slender, with V-shaped ridge. Outer cone cup-shaped with concave ventral rim. Spine present.

FIGURE 36.—Sepia longipes: a,b, dorsal, ventral views of sepion; c, geographical distribution. (a,b, after Sasaki, 1929.)

ORIGINAL REFERENCE.—Sasaki, 1914:619, pl. 12: figs. 4, 5.

TYPE LOCALITY.—Japan, Kozusa Province, Choshi.

TYPES.—Holotype: Museum of the Science College, University of Tokyo.

GEOGRAPHICAL DISTRIBUTION.—Japan, South of Choshi to southern Kyushu; East China Sea.

DISCUSSION.—This species is apparently related to S. lorigera W¨ker but differs from it in the broader body, relatively shorter arms I of male, and carinated sepion. For discussion of hectocotylization of both ventral arms, see Adam and Rees (1966:69); according to Okutani et al. (1987), only the left ventral arm of the male is hectocotylized. The size is to 240 mm ML, and the usual capture depth is about 100–300 m.

Sepia lorigera Wülker, 1910

FIGURE 37

DIAGNOSIS.—Arms of male differ in length, formula I>II>III>IV, arms I three times as long as other arms, tapering to very slender middle portion; distal portions of arms I characterized by enlarged protective membrane supported by trabeculae; left arm IV hectocotylized, suckers reduced on distal art and sucker stalks swollen. Arms of female subequal. Tentacular club with 4 or 5 longitudinal rows of suckers, medial 4 suckers extraordinarily large. Sepion lanceolate. Anterior margin of striated zone approximately M-shaped, distal end somewhat rounded. Inner and outer cones as in S. longipes. Spine present.

FIGURE 37.—Sepia lorigera: a.b, dorsal, ventral views of sepion; c, geographical distribution. (a,b, after W¨ker, 1910.)

ORIGINAL REFERENCE.—Wüker, 1910:12, figs. 3, 4, 11–14.

TYPE LOCALITY.—Japan, Misaki.

TYPES.—Holotype: Museum der Universität, München.

GEOGRAPHICAL DISTRIBUTION.—From Japan, Sagami Bay, to East China Sea; Vietnam (?) along Pacific coast of Shikoku.

DISCUSSION.—For discussion of double hectocotylization (both arms IV in male) see Adam and Rees (1966:69). The size is to 250 mm ML, and the usual capture depth is about 100–300 m.

Sepia lycidas Gray, 1849

FIGURE 38

Sepia subaculeala Sasaki, 1914:609.

ILLUSTRATIONS.—Adam and Rees, 1966, pl. 3: fig. 13 , pl. 41: fig. 236 .

DIAGNOSIS.—Arms stout, suckers quadriserial throughout. Tentacular club with small subequal suckers in 8 longitudinal rows. Sepion elongate-oval in outline. Striated zone with deep, wide groove. Anterior striae L-shaped. Inner cone relatively narrow posteriorly, with ventral ledge of pocket-like cavity rounded and very thick convex limbs. Spine long.

ORIGINAL REFERENCE.—Gray, 1849:103.

TYPE LOCALITY.—China, Canton.

TYPES.—Holotype: The Natural History Museum, London, 1963.119W, male, ∼230 mm ML, very poor condition (dehydrated), sepion removed, placed in dry collection.

FIGURE 38.—Sepia lycidas: a, male, dorsal view; b, sepion, ventral view; c, left tentacular club; d, geographical distribution. (a, after Roper et al., 1984.)

Paratypes: None.

GEOGRAPHICAL DISTRIBUTION.—West Pacific Ocean from South Honshu, Japan, and Tsingtao, China, to the Philippines, Vietnam, Borneo, and Gulf of Thailand.

DISCUSSION.—This is a fully described species of unquestioned status. The size is to 380 mm ML, and the usual capture depth is about 0–90 m. This species is commercially important in Japan, China, Vietnam, and Thailand. A well-preserved female specimen (175 mm ML, from Japan), identified by W. Adam, is in The Natural History Museum, London (BMNH 1904.10.28.5).

Sepia madokai Adam, 1939

FIGURE 39

Sepia robsoni Sasaki, 1929:179 [not Massy, 1927].

Sepia elliptica Hoyle, 1885:189.

ILLUSTRATIONS.—Sasaki, 1929, pl. 17: figs. 2, 3; Okutani et al., 1987:38.

DIAGNOSIS.—Arm formula IV > I > III > II; suckers quadriserial throughout. Tentacular club with small subequal suckers in 8–10 longitudinal rows. Sepion nearly rhomboidal, rounded posteriorly, without keels. Striated zone with thin median furrow. Anterior striae rounded or widely L-shaped. Outer cone with indistinct wings. Spine long.

ORIGINAL REFERENCE.—Adam, 1939b:77.

TYPE LOCALITY.—Japan, Tokyo Bay.

TYPES.—Holotype: Museum of the Science College, University of Tokyo.

OTHER TYPE MATERIAL.—See Appendix II for syntypes of Sepia elliptica; see also Lu (1998a).

GEOGRAPHICAL DISTRIBUTION.—Northwestern Pacific from South Vietnam to South Honshu, Japan.

DISCUSSION.—This is a fully described species of unquestioned status, very close to S. acuminata, less so to S. rex. The size is to 150 mm ML, and the usual capture depth is about 100–300 m. It is a commercial species in Japan.

Sepia mascarensis Filippova and Khromov, 1991

FIGURE 40

ILLUSTRATIONS.—Filippova and Khromov, 1991, fig. l.

DIAGNOSIS.—Male with all arms long, arms not modified. Tentacular club with suckers distinctly differing in size. Sepion very narrow and long, with keel in anterior part of striated zone in adult male. Median ventral furrow deep on last loculus and indistinctly expressed in posterior part of striated zone. Anterior striae narrowly M-shaped. Inner cone low posteriorly. Outer cone with very delicate, scalloped, uncalcified rim. Spine prominent.

FIGURE 39.—Sepia madokai: a, left tentacular club; b, sepion, ventral view; c, geographical distribution.

FIGURE 40.—Sepia mascarensis: a, male, dorsal view; b–d, dorsal, ventral, lateral views of sepion; e, posterior sepion, ventral view; f, left tentacular club; g, geographical distribution. (a–f, from Filippova and Khromov, 1991.)

FIGURE 41.—Sepia mirabilis: a, right tentacular club; b, head and arms of male, dorsal view; C, cross section of sepion; d,e, ventral, dorsal views of sepion; f, posterior sepion, ventral view; g, geographical distribution. (a–f, from Khromov, 1988a.)

ORIGINAL REFERENCE.—Filippova, and Khromov, 1991:63.

TYPE LOCALITY.—Indian Ocean, Saya-de-Malha Bank, 11°31′S, 61°00′E, depth 195 m.

TYPES.—Holotype: Zoological Museum, Moscow University, N 349.

Paratypes: Zoological Museum, Moscow University, N 350, 14 males.

GEOGRAPHICAL DISTRIBUTION.—Indian Ocean, Saya-de-Malha Bank; Cargados-Carajos Shoals.

DISCUSSION.—This is a fully described species of unquestioned status. The size is to 120 mm ML, and the usual capture depth is about 0–325 m.

Sepia mestus Gray, 1849

See Lu (1998a); Khromov (1988b).

Sepia mira (Cotton, 1932)

See Lu (1998a).

Sepia mirabilis Khromov, 1988

FIGURE 41

DIAGNOSIS.—Arms III of male twice as long as other arms, with transformed protective membranes of thin fleshy ribs separated by membranous parts. Other arms with only slightly transformed protective membranes of same general form. Female smaller than male, with normal arms. Tentacular club with suckers differing in size. Sepion long, with very narrow striated zone. Anterior striae low L-shaped. Inner cone narrowly U-shaped. Outer cone forming lateral wings. Spine prominent.

ORIGINAL REFERENCE.—Khromov, 1988a:785, figs. la, 2a–k.

TYPE LOCALITY.—Arabian Sea, Sokotra Island, 12°22′N, 54°28′E, depth 50 m.

TYPES.—Holotype: Zoological Museum, Moscow University, N 300, male, 70 mm ML.

Paratypes: Zoological Museum, Moscow University, N 301: 11 males, 42–65 mm ML; 6 females, 44–52 mm ML; 1 juvenile, 36 mm ML.

GEOGRAPHICAL DISTRIBUTION.—From western Indian Ocean near Sokotra Island probably to East Africa.

DISCUSSION.—This is a fully described species of unquestioned status. Sexual dimorphism occurs in size, sepion shape, arm length, and protective membrane structure. Size is to 70 mm ML.

Sepia murrayi Adam and Rees, 1966

FIGURE 42

DIAGNOSIS.—Only female known. Distal ends of arms bluntly pointed, protective membranes wide and folded over inner arm surface, minute, widely spaced, and distinctly biserial suckers near arm tips. Tentacular club with 5 longitudinal rows of subequal suckers. Sepion lanceolate, widest in anterior images, with deep, narrow median furrow ventrally. Anterior striae M-shaped. Inner cone sharp, with V-shaped ledge. Outer cone small, cup-shaped. Spine prominent.

ORIGINAL REFERENCE.—Adam, and Rees, 1966:63, pl. 18:figs. 107–111, 260.

TYPE LOCALITY.—Gulf of Oman, R/V John Murray expedition station 71, 25°35′N, 56°42′18″E, to 25°43′N, 56°30′18″E, depth 106 m.

TYPES.—Holotype: The Natural History Museum, London, 1963.81.W, female, 40 mm ML.

Paratypes: The Natural History Museum, London, 1963.82–3. W, 2 females, 40 mm ML, 41 mm ML. Same locality as holotype.

GEOGRAPHICAL DISTRIBUTION.—Known only from type locality.

FIGURE 42.—Sepia murrayi: a,b, dorsal, ventral views of sepion; c, geographical distribution. (a,b, after Adam and Rees, 1966.)

DISCUSSION.—This species is insufficiently described and its biology is unknown.

Sepia novaehollandiae Hoyle, 1909

See Lu (1998a).

Sepia omani Adam and Rees, 1966

FIGURE 43

DIAGNOSIS.—Arm suckers quadriserial throughout; lateral suckers smaller than median suckers proximally, larger distally, except on arms IV. Tentacular club suckers in 8 longitudinal rows, 3–5 very strongly enlarged suckers in proximal part of third row. Sepion long, drop-shaped, with secondary wings of outer cone on level of limbs of inner cone. Anterior striae M-shaped. Spine present.

ORIGINAL REFERENCE.—Adam, and Rees, 1966:92, pl. 22: fig. 144, pl. 41: fig. 244.

TYPE LOCALITY.—Gulf of Oman.

TYPES.—Holotype: The Natural History Museum, London, 1963.107.W, male, 62 mm ML.

Paratypes: The Natural History Museum, London, 1963.108–114.W, 7 males, 6 females.

GEOGRAPHICAL DISTRIBUTION.—Gulf of Oman.

DISCUSSION.—This is a fully described species of unquestioned status. This is not the species listed as S. omani from Hong Kong in Voss and Williamson (1972). The size is to 100 mm ML, and the usual capture depth is about 100–200 m.

FIGURE 43.—Sepia omani: a, geographical distribution; b, left tentacular club; c, sepion, ventral view (after Adam and Rees, 1966).

Sepia opipara (Iredale, 1926)

See Lu (1998a).

Sepia orbignyana Férussac in Orbigny, 1826

FIGURE 44

ILLUSTRATIONS.—Adam and Rees, 1966, pl. 21: figs. 134–137.

DIAGNOSIS.—Mantle strongly projecting dorsally; posterior end of mantle with prominent tip between fin lobes (skin-covered spine of sepion). Tentacular club short, with suckers in 5 to 6 rows, middle series with 3 to 4 greatly enlarged suckers. Sepion long-oval, with distinct lateral wings and very prominent spine. Anterior striae very broadly M-shaped.

ORIGINAL REFERENCE.—Orbigny, 1826:156.

TYPE LOCALITY.—France, La Rochelle.

TYPES.—Holotype: Muséum National d'Histoire Naturelle, Paris, 1.4.88, sepion, 88 mm.

Paratypes: None.

GEOGRAPHICAL DISTRIBUTION.—Eastern Atlantic from Bay of Biscay to 17°S, including Mediterranean.

FIGURE 44.—Sepia orbignyana: a,b, dorsal, ventral views of sepion; c, left tentacular club; d, geographical distribution. (a–c, after Adam, 1952.)

DISCUSSION.—This is a fully described species of unquestioned status. Despite differences (e.g., in sepion structure, spine, etc.), this species is often confused with S. elegans. The size is to 95 mm ML, and the usual capture depth is about 150–300 m.

Sepia papillata Quoy and Gaimard, 1832

FIGURE 45

Sepia tuberculata Férussac and Orbigny, 1834–1848:277 [not Lamarck, 1798:130].

FIGURE 45.—Sepia papillata: a,b, dorsal, ventral views of sepion; c, left tentacular club; d, geographical distribution. (a–c, after Roeleveld, 1972.)

DIAGNOSIS.—Skin tuberculate dorsally and laterally on arms, head, and mantle, wrinkled in 2 patches on ventral surface of mantle and arms IV. Arm suckers always quadriserial in female; in 8 series on attenuated tips in male. Tentacular club with mostly small suckers in 8 longitudinal rows, 4 suckers enlarged medially, middle 2 suckers with diameter equal to width of sucker-bearing surface of club; protective membranes separate. Sepion broadly oval. Striated zone with (form A) or without (form B) median furrow; striae L-shaped. Spine generally absent, broad knob present.

ORIGINAL REFERENCE.—Quoy, and Gaimard, 1832:61, pl. I: figs. 6–14.

TYPE LOCALITY.—South Africa, Cape of Good Hope.

TYPES.—Holotype: Lost (originally in Muséum National d'Histoire Naturelle, Paris).

Paratypes: None.

Topotypes: The Natural History Museum, London, and the South African Museum (see Adam and Rees, 1966:108; Roeleveld, 1972:235).

GEOGRAPHICAL DISTRIBUTION.—South Africa, from Lüderitz Bay, 26°38′S, 15°10′E, to Natal coast, off Tugela and Umvoti rivers, 29°11′S, 31°25′E; Indian Ocean, Mascarene Ridge.

DISCUSSION.—This is a very common species around western Cape of Good Hope, South Africa. It is closely related to S. tuberculata, which differs by the diameter of the large tentacular club suckers being less than the width of the tentacular club, having protective membranes joined proximally, and a sepion with no median ridge on the dorsal surface, no posterior knob, no distinct median furrow ventrally, and no well-developed inner cone posteriorly, limbs being narrow. The size is to 140 mm ML, and the usual capture depth is about 50–200 m.

Sepia papuensis Hoyle, 1885

See Lu (1998a).

Sepia pardalis Sasaki, 1914

FIGURE 46

Sepia pardex Sasaki, 1913 [in Japanese] [fide Okutani et al., 1987:49].

DIAGNOSIS.—Mantle elongated, with 100 or more streaklike, well-defined spots on dorsal surface. Arms unequal, arm formula I > II > III > IV, left arm IV hectocotylized with suckers reduced on distal images. Tentacular club with 8 rows of minute, subequal suckers. Sepion slender, lanceolate. Anterior striae M-shaped, marked with numerous streaks. Inner cone rim comparatively broad but flattened into slightly elevated, V-shaped ridge. Spine present.

ORIGINAL REFERENCE.—Sasaki, 1914:614, pl. 12: figs. 1–3. (The original description in Japanese appeared in Sasaki, 1913; see “Discussion.”)

TYPE LOCALITY.—Awa Province, Japan.

TYPES.—Holotype: Museum of the Science College, University Tokyo, No. 101, male, 231 mm ML.

Paratypes: None.

GEOGRAPHICAL DISTRIBUTION.—Japan, Honshu (west of Boso Peninsula and at Toyama Bay) and Kyushu; southern Korea.

FIGURE 46.—Sepia pardalis: a,b, dorsal, ventral views of sepion; c, geographical distribution.

DISCUSSION.—This species is easily distinguished from others by its elongated mantle with spotted dorsum. Okutani et al. (1987) redescribed this species as Sepia pardex, indicating that Sasaki used this name in his original description published in Japanese, in 1913. Because Sasaki used “Sepia pardalis Sasaki, 1914,” in all his other publications, the question of whether Sepia pardex Sasaki, 1913, has priority should be brought to the attention of the International Commission on Zoological Nomenclature.

Sepia peterseni Appellöf, 1886

FIGURE 47

ILLUSTRATIONS.—Okutani et al., 1987:4; Khromov, 1988b: 177.

DIAGNOSIS.—Arms II of male much longer than other arms, tapering to extremity without suckers. Fins of male triangular posteriorly. Tentacular club with suckers differing in size. Sepion long, narrow. Anterior striae L-shaped. Spine present.

ORIGINAL REFERENCE.—Appellöf, 1886:23.

TYPE LOCALITY.—Japan.

TYPES.—Syntypes: Zoological Museum of Uppsala University, Sweden, No. 148a, 1 male, 105 mm ML. Whereabouts of remaining 2 syntypes not known.

GEOGRAPHICAL DISTRIBUTION.—Kyushu to central Honshu, Japan; South Korea.

DISCUSSION.—This is a fully described species of unquestioned status. Females were described by Khromov (1988b). Sexual dimorphism occurs in fin structure and in arm end and length (female with normal fins and arms). The size is to 120 mm ML, and the usual capture depth is about 20–100 m.

Sepia pharaonis Ehrenberg, 1831

FIGURE 48

Sepia rouxi Férussac and d'Orgigny, 1841:271 [Bombay].

Sepia torosa Ortmann, 1888:652 [Tokyo Bay].

Sepia framea Ortmann, 1891:675 [Ceylon].

Sepia singalensis Goodrich, 1896:3 [Colombo].

Sepia koettlitzi Hoyle and Standen, 1901:1 [Zeila, Somalia].

Sepia formosana Berry, 1912:420 [Takao, Formosa].

Sepia hulliana Iredale, 1926b:239 [Howick Island].

Sepia tigris Sasaki, 1929:168 [Formosa].

Sepia ursulae Cotton, 1929:90 [W. Australia].

Sepia sinope Voss, 1962:3 [not Gray, 1849].

DIAGNOSIS.—Tentacular club with protective membranes separate at base, suckers in 8 longitudinal rows, 5 or 6 median ones (3rd and 4th in series) markedly enlarged. Left arm IV hectocotylized, with basal 12 quadriserial transverse rows normal, next 10 transverse rows with ventral suckers (2 longitudinal rows) normal, those in dorsal 2 longitudinal rows minute and separated from ventral rows by fleshy, transversely grooved ridge. Marked transverse, tiger-stripe pattern on dorsal mantle and head; light, interrupted line along fin bases. Sepion oval. Posterior part of striated zone covered by broadly U-shaped, dark (calcitic) deposit on inner cone (also called secondary inner cone). Anterior striae rounded L-shaped. Spine present.

ORIGINAL REFERENCE.—Ehrenberg, 1831: pl. 8.

TYPE LOCALITY.—Tor, Sinai.

TYPES.—Holotype: Unknown. Type was probably deposited in the Natural History Museum of Strasbourg.

Topotype: The Natural History Museum, London.

GEOGRAPHICAL DISTRIBUTION.—Indo-Pacific from Red Sea through Arabian Sea to South China Sea, East China Sea, and northern and northwestern Australia.

DISCUSSION.—For a full discussion, see Adam and Rees (1966:25). Maximal mantle length is 430 mm in the male and 330 mm in the female. The usual capture depth is 0–120 m. See also Lu (1998a).

Sepia plangon Gray, 1849

See Lu (1998a).

Sepia plathyconchalis Filippova and Khromov, 1991

FIGURE 49

DIAGNOSIS.—Tentacular club suckers in ∼6 longitudinal rows, several proximal suckers greatly enlarged. Sepion oval in outline, very flat. Striated zone very narrow, about images–images width of sepion, with narrow, indistinct median furrow. Anterior striae rounded. Inner cone flat, very wide laterally. Outer cone without posterior wings. Spine absent but knob present.

FIGURE 47.—Sepia peterseni: a, male, dorsal view; b, female, ventral view; c, geographical distribution.

ORIGINAL REFERENCE.—Filippova and Khromov, 1991:66, fig. 2.

FIGURE 48.—Sepia pharaonis: a,b, dorsal, ventral views of sepion; c, right tentacular club; d, geographical distribution. (a,b, after Adam and Rees, 1966; c, after Voss and Williamson, 1971.)

FIGURE 49.—Sepia plathyconchalis: a, male, dorsal view; b, hectocotylus; c,d, ventral, lateral views of sepion; e, left tentacular club; f, geographical distribution. (a–e, from Filippova and Khromov, 1991.)

FIGURE 50.—Sepia prashadi: a–c, dorsal, lateral, ventral views of sepion; d, right tentacular club; e, geographical distribution.

TYPE LOCALITY.—Indian Ocean, Saya-de-Malha Bank, 9°42′S, 61°08′E.

TYPES.—Holotype: Zoological Museum, Moscow University, No. 351, female, 61 mm ML.

Paratypes: Zoological Museum, Moscow University, No. 352, 8 females, 5 males, 37–63 mm ML.

GEOGRAPHICAL DISTRIBUTION.—Western Indian Ocean, Saya-de-Malha Bank; Cargados-Carajos Shoals; St. Brandon Shoals.

DISCUSSION.—This is a fully described, shallow-water species of unquestioned status. The size is to 100 mm ML.

Sepia prashadi Winckworth, 1936

FIGURE 50

ILLUSTRATIONS.—Adam and Rees, 1966, pl. 9: figs. 44–48, pl. 41: figs. 245, 246.

DIAGNOSIS.—Arm suckers quadriserial. Tentacular club with greatly differing suckers in 5 longitudinal rows; 2 median suckers enormously enlarged. Sepion rhomboidal anteriorly, rounded posteriorly. Anterior striae M-shaped. Inner cone with wide, convex, rounded ventral ledge. Outer cone not forming posterior wings. Spine with ventral and dorsal keels.

ORIGINAL REFERENCE.—Winckworth, 1936:16.

TYPE LOCALITY.—India, Madras, Bay of Bengal.

TYPES.—Holotype: Zoological Museum Calcutta, Indian Museum, sepion, 80 mm, Madras Beach, Jan 1927.

Paratype: The Natural History Museum, London, 1952.11.24.59, sepion, 84 mm, Madras, 1 Apr 1930.

GEOGRAPHICAL DISTRIBUTION.—Western Indian Ocean from South Mozambique to Calcutta; Red Sea; Gulf of Oman; Madagascar; Mauritius.

DISCUSSION.—This is a fully described species of unquestioned status. The size is to 140 mm ML, and the usual capture depth is about 50–200 m.

Sepia pulchra Roeleveld and Liltved, 1985

FIGURE 51

DIAGNOSIS.—Mantle with numerous complex dorsal papillae and fleshy ventral keels. Arm suckers biserial on arms I–III and distally on arms IV, quadriserial proximally on arms IV; sexual dimorphism involves sucker enlargement on arms II and sometimes III and modification of sucker shape and size on right arm IV in male. Tentacular club with subequal suckers. Sepion not calcified, delicate, with reflexed inner cone. Striae broadly M-shaped. Spine absent.

ORIGINAL REFERENCE.—Roeleveld and Liltved, 1985:1–18, figs. 1–14.

TYPE LOCALITY.—South Africa, Cape Peninsula, Llandudno, depth 25 m.

FIGURE 51.—Sepia pulchra: a,b, dorsal, ventral views of sepion; c, right tentacular club; d, geographical distribution, (a–c, after Roeleveld and Liltved, 1985.)

TYPES.—Holotype: South African Museum SAM S1036, male, 17 mm ML.

Paratypes: South African Museum: SAM S822, SAM S1034, 2 males, 22 mm ML, 15 mm ML, Hottentots Huisie, Cape Peninsula, depth 15 m; SAM S982, 1 female, 21 mm ML, Bakoven, Cape Peninsula, depth 21 m; SAM S1007, SAM S1029–1033, SAM S1038–9, 6 males, 7 females, 16–22 mm ML, Llandudno, depth 25-∼50 m.

GEOGRAPHICAL DISTRIBUTION.—South Africa, Cape Peninsula, depth 15–50 m.

DISCUSSION.—This species of the Hemisepius species complex is related to S. robsoni, S. faurei, S. typica, and S. dubia; all five species are small, maturing at a size of about 20 mm ML. They have a very broad mantle (mantle width 60%–90% of length), a deeply emarginate ventral anterior margin, fleshy keels ventrally on the mantle, and biserial arm suckers (at least on arms I, II, and III); the tentacular club bears small suckers, and the protective membranes separate proximally. In contrast to S. pulchra, S. typica, S. dubia, and S. faurei have a phragmocone shorter than the dorsal shield on the sepion. The sepion of S. robsoni is practically unknown. Some biological observations are given in the original description.

Sepia recurvirostra Steenstrup, 1875

FIGURE 52

ILLUSTRATIONS.—Adam and Rees, 1966, pl. 9: figs. 49–52, pl. 10: figs. 53, 54; Voss and Williamson, 1972, figs. 4d, 7f, 12, pl. 12.

DIAGNOSIS.—Tentacular club with suckers of variable sizes in 5 to 6 longitudinal rows. Sepion subrhomboidal anteriorly, rounded posteriorly. Striated zone with thin median furrow. Anterior striae rounded. Inner cone connected posteriorly to outer cone by thick callous substance. Spine present.

ORIGINAL REFERENCE.—Steenstrup, 1875:479.

TYPE LOCALITY.—South China Sea.

TYPES.—Lectotype: Zoological Museum, University of Copenhagen, 1 sepion, 77.5 mm; designated by Adam (1965:170).

Paralectotype: Zoological Museum, University of Copenhagen, 1 sepion, 47.8 mm.

GEOGRAPHICAL DISTRIBUTION.—Indo-West Pacific from the Andaman Sea to Celebes Sea and from Java Sea to Yellow Sea, near Tsingtao.

FIGURE 52.—Sepia recurvirostra: a, geographical distribution; b, sepion, ventral view.

DISCUSSION.—This is a fully described species of unquestioned status. The size is to 170 mm ML, and the usual capture depth is about 50–150 m. This is one of the commercial species in the Gulf of Thailand, South and East China seas, and Japan.

Sepia reesi Adam, 1979

See Lu (1998a).

Sepia rex (Iredale, 1926)

See Lu (1998a).

Sepia robsoni (Massy, 1927)

FIGURE 53

DIAGNOSIS.—Animals mature at small size (17 mm ML). Mantle broad, ventrally deeply emarginate, and with fleshy ridges on either side of ventral mantle surface. Arms 1 with finger-like tips without suckers. Tentacular club with about 53 small, subequal suckers in 4–6 transverse rows. Sepion uncalcified.

ORIGINAL REFERENCE.—Massy, 1927:159, pl. XVII: figs. 1–8.

TYPE LOCALITY.—South Africa, Hout Bay, depth 17–37 m.

TYPES.—Holotype: The Natural History Museum, London, 1926.10.20.8, mature male, 17 mm ML, sepion in poor condition.

Paratypes: None.

GEOGRAPHICAL DISTRIBUTION.—Known only from type locality.

DISCUSSION.—This is an insufficiently described species, known only from the holotype, that was originally described as Rhombosepion robsoni, but it clearly belongs to the Hemisepius species complex. The sepion probably has the phragmocone covering the entire ventral surface of the dorsal shield.

FIGURE 53.—Sepia robsoni: a, left tentacular club; b, geographical distribution. (a, after Adam and Rees, 1966.)

Sepia rozella (Iredale, 1926)

See Lu (1998a).

Sepia savignyi Blainville, 1827

FIGURE 54

DIAGNOSIS.—Mantle broadly oval, slightly acuminate posteriorly. Dorsal mantle margin projecting bluntly. Tentacular club narrow, with subequal suckers in 8 oblique rows. Sepion broadly oval, with very short spine. Anterior striae L-shaped.

ORIGINAL REFERENCE.—Blainville, 1827:285.

TYPE LOCALITY.—Red Sea.

TYPES.—Neotype: Muséum National d'Histoire Naturelle, Paris: 1.6.188, male, sepion, 95 mm; 1.6.188bis, soft parts. Neotype designation, Rochebrune (1884).

Paratypes: None.

GEOGRAPHICAL DISTRIBUTION.—Red Sea; Gulf of Aden; Arabian Sea.

DISCUSSION.—This species has been confused with S. pharaonis by Férussac and Orbigny (1848:281 (in 1834–1848)), and confused with S. pharaonis, S. gibba, and S. lefebrei by Tryon (1879:194, 279, 281, 287). The size is to 130 mm ML, and the usual capture depth is 20–50 m.

FIGURE 54.—Sepia savignyi: a, sepion, ventral view; b, geographical distribution.

Sepia saya Khromov, Nikitina, and Nesis, 1991

FIGURE 55

DIAGNOSIS.—Arms III of male shorter than other arms, arm suckers quadriserial. Tentacular club with 5 longitudinal rows of unequal suckers, some median suckers in proximal images somewhat enlarged. Sepion lanceolate, length 4 times width. Striated zone narrow, flanked by smooth marginal zones. Anterior striae shallow, M-shaped. Outer cone forming wings posteriorly. Spine prominent.

ORIGINAL REFERENCE.—Khromov, Nikitina, and Nesis, 1991:13, fig. 1.

TYPE LOCALITY.—Western Indian Ocean, Saya-de-Malha Bank, 10°30′–10°32′S, 61°10′–61°11′E, depth 110–115 m.

TYPES.—Holotype: Zoological Museum, Moscow University, No. Y357, male, 64 mm ML.

Paratypes: Zoological Museum, Moscow University: 10 males, 40–86 mm ML; 5 females, 41–46 mm ML. Same locality as holotype.

GEOGRAPHICAL DISTRIBUTION.—Known only from Sayade-Malha Bank, Western Indian Ocean.

DISCUSSION.—This is a fully described species of unquestioned status. The size is to 90 mm ML.

Sepia sewelli Adam and Rees, 1966

FIGURE 56

DIAGNOSIS.—Arm suckers quadriserial in female. Tentacular club suckers minute, subequal, in 6–8 longitudinal rows. Sepion widely elongate, ventral surface with narrow groove, anterior striae L-shaped (Figure 56). Inner cone with narrow limbs forming rounded posterior ledge, limbs limited by smooth marginal zones. Outer cone forming wings posteriorly. Spine present, directed dorsally.

ORIGINAL REFERENCE.—Adam and Rees, 1966:61, pl. 17: figs. 104–106, pl. 46: fig. 273.

TYPE LOCALITY.—R/V John Murray expedition station 27, 11°57′12″N, 50°35′E, to 11°56′42″N, 50°39′12″E, near Cape Guardafui, Somalia, depth 37 m.

TYPES.—Holotype: The Natural History Museum, London, 1963.78, female, 24 mm ML, in good condition.

Paratypes: The Natural History Museum, London: 1963.79, 1 female, in poor condition, R/V John Murray expedition station 105, Zanzibar area, depth 238 m; 1963.80, 17 juveniles, in poor condition, R/V John Murray expedition station 106, Zanzibar area, depth 212 m.

GEOGRAPHICAL DISTRIBUTION.—East Africa, from 11°57′N, 50°35′E, to 5°40′S, 39°17′E.

DISCUSSION.—This species is in the Doratosepion species complex but is insufficiently described. It is apparently related to S. kobiensis, S. murrayi, and S. appellöfi.

FIGURE 55.—Sepia saya: a, male, dorsal view; b,c, dorsal, ventral views of sepion; d, posterior sepion, ventral view; e, right tentacular club; f, geographical distribution. (a–e, from Khromov et al., 1991.)

FIGURE 56.—Sepia sewelli: a,b, dorsal, ventral views of sepion; c, geographical distribution. (a,b, after Adam and Rees, 1966.)

Sepia simoniana Thiele, 1920

FIGURE 57

Sepia natalensis Massy, 1925:212.

ILLUSTRATIONS.—Adam and Rees, 1966, pl. 29: figs. 179–182, pl. 42: fig. 254.

DIAGNOSIS.—Arm suckers quadriserial. Arm tips I–III attenuated. Tentacular club very long, with minute subequal suckers in about 24 longitudinal rows. Sepion oval in outline with short, thick knob. Striated zone with broad, deep groove. Anterior striae L-shaped. Inner cone flat, wide, limbs abruptly tapering anteriorly. Outer cone broad, not forming posterior wings.

ORIGINAL REFERENCE.—Thiele, 1920:436.

TYPE LOCALITY.—South Africa, Simon's Bay.

TYPES.—Syntypes (5): Zoologisches Museum, Humboldt Universität Berlin.

GEOGRAPHICAL DISTRIBUTION.—Western Indian Ocean from Agulhas Bank to North Kenya.

DISCUSSION.—This is a fully described species of unquestioned status. The size is to 190 mm ML, and the usual capture depth is to 190 m. It is a potentially commercial species in Southeast Africa.

Sepia smithi Hoyle, 1885

See Lu (1998a).

FIGURE 57.—Sepia simoniana: a,b, ventral, lateral views of sepion; c, geographical distribution.

Sepia sokotriensis Khromov, 1988

FIGURE 58

DIAGNOSIS.—Arms II of male with attenuated tips, markedly longer than other arms; both arms IV hectocotylized. Tentacular club with slightly differing suckers in about 6 longitudinal rows, median suckers distinctly larger. Sepion very narrow. Anterior striae L-shaped. Inner cone narrow, U-shaped, with narrow limbs. Outer cone forming posterior wings. Spine prominent.

ORIGINAL REFERENCE.—Khromov, 1988a:788.

TYPE LOCALITY.—Arabian Sea, Sokotra Island, 12°10′N, 54°25′E, depth 100 m.

TYPES.—Holotype: Zoological Museum, Moscow University, No. 302, male, 77 mm ML.

Paratypes: Zoological Museum, Moscow University, No. 303: 1 male, 58 mm ML; 1 female, 51 mm ML; 2 males, 47 mm ML and 63 mm ML; same location as holotype.

GEOGRAPHICAL DISTRIBUTION.—Western Indian Ocean near Sokotra Island; probably eastern coast of Africa.

DISCUSSION.—This is a fully described species of unquestioned status; it is illustrated in the original description. Sexual dimorphism occurs in adult size and arm length (female is smaller and has normal arms). The size is to 80 mm ML.

Sepia stellifera Homenko and Khromov, 1984

FIGURE 59

DIAGNOSIS.—Arm suckers quadriserial. Tentacular club with small, subequal suckers in 10 longitudinal rows. Sepion oval in outline, subrhomboidal in anterior art. Striated zone with 3 deep, broad grooves; grooves separated by 2 ribs. Anterior striae with 3 peaks. Inner cone with moderately wide, relatively thick, sickle-shaped ventral ledge over pocket-like cavity. Outer cone not forming wings. Spine long, with ventral and dorsal keels.

ORIGINAL REFERENCE.—Homenko and Khromov, 1984:1150, figs. 1–9.

TYPE LOCALITY.—East Arabian Sea, 13°59′N, 73°58′E, depth 53–55 m.

TYPES.—Holotype: Zoological Museum, Moscow University, No. 260, male.

Paratypes: Zoological Museum, Moscow University, Nos. 261–262, 34 females, 90 males, 13 female sepions, and 24 male sepions from various locations in Arabian Sea.

GEOGRAPHICAL DISTRIBUTION.—Arabian Sea; Bay of Bengal; Andaman Sea; Gulf of Thailand.

DISCUSSION.—This is a fully described species of unquestioned status. The size is to 120 mm ML, and the usual capture depth is 50–100 m. This is one of the commercial species in India and probably is included in statistical data as S. brevimana.

Sepia subtenuipes Okutani and Horikawa, 1987

FIGURE 60

DIAGNOSIS.—Arms I of male markedly prolonged, attenuated distally. Arms of female subequal in length. Arm suckers quadriserial except on distal part of arms I in male where about 50 pairs are biserial. Left arm IV hectocotylized, with suckers reduced on middle portion. Tentacular club with 8 longitudinal rows of minute subequal suckers. Sepion lanceolate, anterior striae of siphuncular zone M-shaped. Inner cone becoming slender rib. Outer cone cup-shaped, forming posterior wings. Spine prominent.

ORIGINAL REFERENCE.—Okutani, Tagawa, and Horikawa, 1987:56, figs. A–F.

TYPE LOCALITIES.—Japan, Tosa Bay, Shikoku, and Kii Channel, depth 90–170 m.

TYPES.—Holotype: Natural Science Museum, Tokyo, 64227, male, 93.6 mm ML.

Paratypes: Natural Science Museum, Tokyo: 64228, 1 male, 93.0 mm ML; 64229, 1 male, sepion length 88.4 mm.

GEOGRAPHICAL DISTRIBUTION.—Tosa Bay; Kii Channel; East China Sea.

DISCUSSION.—This species is a sympatric sibling species with Sepia tenuipes Sasaki, 1929. The size is to 90 mm ML, and the usual capture depth is about 100–200 m.

Sepia sulcata Hoyle, 1885

FIGURE 61

ILLUSTRATIONS.—Hoyle, 1886, pl. 19: figs. 1–13.

DIAGNOSIS.—Swimming membrane of tentacular club broad, extending beyond base of club for art of club length. Tentacular club suckers minute, subequal in 8 longitudinal rows. Left arm IV hectocotylized, basal art with series of 24 small suckers on both sides, series separated by convex fleshy ridge. Arms I suckers biserial, arrangement of suckers on other arms indistinct. Sepion broadly oval, acuminate at both ends, especially posterior end; dorsal surface with 3 flat, rounded ribs separated by wide grooves; ventral surface flat with 3 wide, shallow grooves over entire length, grooves separated by 2 broad, low ribs. Striated zone flanked by 2 narrow, smooth, marginal zones. Striae vary in anterior part of striated zone. Inner cone degenerate, chitinous limbs narrow, raised as thin ledge toward posterior end. Spine present, keel on dorsal surface of sepion not continuing onto spine. Posterior end of sepion in type missing.

FIGURE 58.—Sepia sokotriensis: a, left ventral arm of male; b, male, dorsal view; c, right ventral arm of male; d, right tentacular club; e,f, ventral, dorsal views of sepion; g, posterior sepion, ventral view; h, cross section of sepion; i, geographical distribution. (a–h, from Khromov, 1988a.)

FIGURE 59.—Sepia stellifera: a, male, dorsal view; b, sepion, ventral view; c, left tentacular club; d, geographical distribution. (a–c, from Homenko and Khromov, 1984.)

FIGURE 60.—Sepia subtenuipes: a,b, dorsal, ventral views of sepion; c, geographical distribution. (a,b, after Okutani et al., 1987.)

FIGURE 61.—Sepia sulcata: a, sepion, dorsal view; b, right tentacular club; c, geographical distribution. (a,b, after Nesis, 1987.)

ORIGINAL REFERENCE.—Hoyle, 1885:192.

TYPE LOCALITY.—Arafura Sea, off Ki Islands, H.M.S. Challenger station 192, 5°49′S, 132°14′15″E, depth 250 m.

TYPES.—Holotype: The Natural History Museum, London, 1889.4.24.77, male, 53 mm ML.

Paratypes: None.

GEOGRAPHICAL DISTRIBUTION.—Known only from the type locality.

DISCUSSION.—This insufficiently known species belongs to the Anomalosepia species complex and is known only from the type specimen. Posterior wings cannot be ruled out; the sepion apparently was damaged subsequent to the original description (M. Roeleveld, pers. comm., 1988).

Sepia tala Khromov, Nikitina, and Nesis, 1991

FIGURE 62

DIAGNOSIS.—Arms I shorter than other arms in both sexes; ends of arms IV in male crescent-like, widened and curved ventrally. Arm suckers quadriserial. Tentacular club suckers in about 5 longitudinal rows, median 3–5 suckers enlarged. Sepion with wide, shallow, M-shaped anterior striae. Inner cone caudally submerged in outer cone, latter forming posterior wings. Spine spindle-shaped.

ORIGINAL REFERENCE.—Khromov, Nikitina, and Nesis, 1991:17, pl. 2: figs. a–m, pl. 3: fig. n.

TYPE LOCALITY.—Southwest Madagascar off Cape Tala, R/V Vityaz station 2644, 22°19′–22°23′S, 43°06′E.

TYPES.—Holotype: Zoological Museum, Moscow University: No. 359, male, 59 mm ML.

Paratypes: Zoological Museum, Moscow University: 2 males, 57 mm ML, 59 mm ML; 5 females, 54–78 mm ML, same locality as holotype.

GEOGRAPHICAL DISTRIBUTION.—Known only from type locality.

DISCUSSION.—This is a fully described species of unquestioned status. The size is to 80 mm ML.

Sepia tenuipes Sasaki, 1929

FIGURE 63

Sepia andreanoides, Sasaki, 1914:614.

DIAGNOSIS.—Arms I of male about twice as long as other subequal arms. Left arm IV hectocotylized, with suckers reduced on distal art. Arms of female about equal in length. Arm suckers quadriserial, biserial only on distal part of arms I in male. Club suckers subequal, in 8 longitudinal rows. Sepion slender, lanceolate, anterior striae roughly M-shaped. Inner cone slender, V-shaped. Outer cone cup-shaped, with shallow excavation in ventral margin. Spine prominent.

FIGURE 62.—Sepia tala: a, male, dorsal view; b.c, dorsal, ventral views of sepion; d, posterior sepion, ventral view; e, left tentacular club; f, geographical distribution. (a–e, from Khromov et al., 1991.)

ORIGINAL REFERENCE.—Sasaki, 1929:193, pl. 18: figs. 1–9.

TYPE LOCALITY.—Ibaraki Prefecture, Japan.

TYPES.—Holotype: Museum of the Science College, University of Tokyo.

Paratypes: None.

GEOGRAPHICAL DISTRIBUTION.—Japan, western Sea of Japan from eastern Honshu to south of Kyushu.

DISCUSSION.—Okutani et al. (1987) reported a dark brown color for the mantle dorsum. The size is to 100 mm ML.

FIGURE 63.—Sepia tenuipes: a, male, dorsal view; b, right tentacular club; c, sepion, ventral view; d, geographical distribution. (a–c, after Sasaki, 1929.)

Sepia thurstoni Adam and Rees, 1966

FIGURE 64

Sepia rouxii, Hoyle, 1904b:198.

DIAGNOSIS.—Arm suckers quadriserial. Tentacular club with 8 longitudinal rows of subequal suckers. Sepion oval in outline, rounded at both ends, ventral surface with broad median depression, smooth zone between striated area and outer cone. Anterior striae L-shaped. Inner cone broad, forming cup-shaped ledge posteriorly. Outer cone not forming posterior wings. Spine present.

ORIGINAL REFERENCE.—Adam and Rees, 1966:2, pl. 1: figs. 1–4, pl. 41: fig. 235.

TYPE LOCALITY.—India, Madras, Ramesvaram Island, 9°18′N, 79°19′E.

TYPES.—Holotype: The Natural History Museum, London, 1894.9.6.2–4, 1 male, 84 mm ML, in good condition.

FIGURE 64.—Sepia thurstoni: a,b, dorsal, ventral views of sepion; c, right tentacular club; d, geographical distribution. (a–c, after Roeleveld and Liltved, 1985.)

Paratypes: The Natural History Museum, London, 1947.5.5.36, 1 female, 74 mm ML (det. Hoyle, 1904, as S. rouxii), off Negombo, Sri Lanka, depth 22–36 m.

GEOGRAPHICAL DISTRIBUTION.—From Madras, India, to off Negombo and Hambantota, Sri Lanka.

DISCUSSION.—The dorsal surfaces of head, arms, and mantle are fairly uniformly bluish black and are faintly striated transversely. This species belongs to the Acanthosepion species complex and resembles S. brevimana, but the latter species has the anterior end of the sepion acuminate. Sepia thurstoni differs from S. lycidas in its club and in the presence of smooth zones between striated area and outer cone, and it differs from S. zanzibarica in its club suckers, the median suckers of S. thurstoni being distinctly larger than the marginal ones. Additional specimens deposited in the Musée Royal d'Histoire Naturelle de Belgique include two sepions from Hambantota, Sri Lanka. The biology is unknown. The size is to 85 mm ML, and the usual capture depth is 20–40 m.

Sepia tokioensis Ortmann, 1888

FIGURE 65

Sepia misakiensis Wülker, 1910:15.

DIAGNOSIS.—Fins of male thickened posteriorly and expanded into distinct lobes. Arms I of male longer than other arms; left arm IV only slightly modified in male, with distal suckers smaller than proximal suckers. Arm suckers quadriserial. Tentacular club small, crescent-shaped, with unequal suckers in 8 longitudinal rows, 4 or 5 median suckers enlarged. Sepion with spine.

ORIGINAL REFERENCE.—Ortmann, 1888:653, pl. 23: fig. 3.

TYPE LOCALITY.—Japan, Tokyo Bay.

TYPES.—Syntypes: Musée d'Histoire Naturelle de Strasbourg, France.

GEOGRAPHICAL DISTRIBUTION.—Known only from Japan.

DISCUSSION.—Okutani et al. (1987) considered S. misakiensis Wülker, 1910, to be a valid species, but they mentioned the very close similarity to S. tokioensis. The size is to 90 mm ML.

FIGURE 65.—Sepia tokioensis: a, male, ventral view; b.c, ventral, dorsal views of sepion; d, geographical distribution. (a, after Sasaki, 1929; b,c, after Wülker, 1910.)

Sepia trygonina (Rochebrune, 1884)

FIGURE 66

ILLUSTRATIONS.—Adam and Rees, 1966, pl. 20: figs. 129–131, pl. 37: figs. 220, 221, pl. 46: fig. 277.

DIAGNOSIS.—Arms I of male shorter than other arms; all arm suckers quadriserial. Lateral arms of female with widely separated biserial suckers distally. Tentacular club with unequal suckers. Sepion long, with raised, plateau-shaped striated zone. Anterior striae L-shaped. Limbs of inner cone raised, following the lateral margins of this plateau. Spine present.

ORIGINAL REFERENCE.—Rochebrune, 1884:97.

TYPE LOCALITY.—Red Sea.

TYPES.—Holotype: Missing; deposited in Muséum National d'Histoire Naturelle, Paris, sepion only.

Paratypes: None.

GEOGRAPHICAL DISTRIBUTION.—Indian Ocean from Saya-de-Malha Bank and Zanzibar to southern India, Red Sea, and possibly Persian Gulf.

FIGURE 66.—Sepia trygonina: a, left tentacular club; b, male, dorsal view; c, sepion, ventral view; d, geographical distribution. (c, after Adam and Rees, 1966.)

DISCUSSION.—This is a fully described species of unquestioned status. The female is very similar to S. sokotriensis and the sepion is similar to S. burnupi. Sexual dimorphism occurs in the length and armament of the arms. The size is to 90 mm ML, and the usual capture depth is 20–200 m. See also Silas et al. (1985) and Filippova and Khromov (1991).

Sepia tuberculata Lamarck, 1798

FIGURE 67

ILLUSTRATIONS.—Adam and Rees, 1966, pl. 26: figs. 169, 170, pl. 27: figs. 171, 172, pl. 28: figs. 173, 174, pl. 44: figs. 265, 268.

DIAGNOSIS.—Skin tuberculate dorsally and laterally on arms, head, and mantle, with 2 wrinkled patches on ventral surfaces of mantle and arms IV. Tips of arms I–III attenuated; arm suckers quadriserial. Tentacular club with 4 or 5 median suckers enlarged, larger ones with diameters less than width of tentacular club, protective membranes joined proximally. Sepion very thin, with long striated zone. Anterior striae convex. Inner cone reflexed, fused to outer cone. Outer cone broad laterally, without wings. Spine absent.

ORIGINAL REFERENCE.—Lamarck, 1798:130.

TYPE LOCALITY.—Unknown.

TYPES.—Holotype: Lost; originally deposited in Muséum National d'Histoire Naturelle, Paris.

Paratypes: None.

Topotypes: The Natural History Museum, London (see Adam and Rees, 1966), and South African Museum (see Roeleveld, 1972).

GEOGRAPHICAL DISTRIBUTION.—South Africa, Melbosstrand, 33°43′S, 18°26′E, to Knysna, 34°03′S, 23°03′E. Sepions have been found in Madagascar. Depth 0–3 m.

DISCUSSION.—See S. papillata for differences between the species. The biology is unknown. Size is to 82 mm ML.

FIGURE 67.—Sepia tuberculata: a, sepion, ventral view; b, left tentacular club; c, geographical distribution. (a,b, after Roeleveld, 1972.)

Sepia typica (Steenstrup, 1875)

FIGURE 68

ILLUSTRATIONS.—Adam and Rees, 1966, pl. 32: figs. 192–195, pl. 33: figs. 196, 197.

DIAGNOSIS.—Animals mature at small size (maximal ML to 25 mm). Ventral surface of mantle with 2 fleshy ridges, each with 5–15 (usually 10–12) pores. Skin very sparsely papillose dorsally. Arm suckers biserial. Basal art of left arm IV hectocotylized, bearing 9–13 pairs of minute suckers in 2 widely spaced series separated by fleshy transverse ridges. Tentacular club small, with numerous, subequal suckers in 6 oblique, transverse rows. Sepion very thin, degenerate, not calcified. Phragmocone much shorter than dorsal shield, triangular in shape.

ORIGINAL REFERENCE.—Steenstrup, 1875:468, figs. 1–10, pl. I, pl. II: fig. 1.

TYPE LOCALITY.—South Africa, Table Bay, 33°50′S, 18°27′E.

TYPES.—Holotype: Zoological Museum, University of Copenhagen, female, 26 mm ML.

Paratypes: None.

GEOGRAPHICAL DISTRIBUTION.—From Saldanha Bay (33°00′S, 17°56′E), South Africa, to southern Mozambique.

DISCUSSION.—This is the type species of Steenstrup's genus Hemisepius. Adam and Rees (1966) relegated Hemisepius to subgeneric status and included S. dubia, which is very closely related to S. typica but has fleshy ridges without pores. Sepia typica also is related to S. faurei, S. pulchra, and S. robsoni. Thore (1945:50) proposed that the eastern forms, which are smaller, be named Hemisepius typicus var. chuni. The known capture depth is 2–250 m.

FIGURE 68.—Sepia typica: a,b, dorsal, ventral views of sepion; c, geographical distribution. (a,b, after Roeleveld, 1972.)

Sepia vercoi Adam, 1979

See Lu (1998a).

Sepia vermiculata Quoy and Gaimard, 1832

FIGURE 69

Sepia jousseaumi Rochebrune, 1884:117.

ILLUSTRATIONS.—Adam and Rees, 1966, pl. 10: figs. 55, 56, pl. 45: fig. 271; and Roeleveld, 1972, pls. 35c,d, 36a,b.

DIAGNOSIS.—Animals mature at 150 mm ML, with maximal mantle length 250 mm. Arm suckers quadriserial. Left arm IV of male hectocotylized, with 6 normal suckers at base followed by 8–13 rows of modified suckers. Tentacular club length roughly art of mantle length, with 8 longitudinal rows of suckers arranged in oblique, transverse series, median suckers of proximal part enlarged, 2.0–2.5 times as large as marginal suckers. Sepion broadly oval, tapering somewhat anteriorly and posteriorly, dorsal surface tuberculate. Striated zone with median longitudinal ridge. Anterior striae rounded, M-shaped. Spine present, surrounded by chitinous covering.

ORIGINAL REFERENCE.—Quoy, and Gaimard, 1832:64, pl. I: figs. 1–5.

FIGURE 69.—Sepia vermiculata: a, sepion, ventral view; b, left tentacular club; c, geographical distribution. (a,b, after Adam and Rees, 1966.)

TYPE LOCALITY.—South Africa, Cape of Good Hope.

TYPES.—Holotype: Lost; originally deposited at Muséum National d'Histoire Naturelle, Paris.

Paratypes: None.

Topotypes: The Natural History Museum, London, and the South African Museum.

GEOGRAPHICAL DISTRIBUTION.—From South Africa, 30°42′S, 15°59′E, to central Mozambique; Saya-de-Malha Bank. The limits of the geographical distribution of this species are not well known because the western Indian Ocean has been poorly sampled.

DISCUSSION.—This species was long considered a subspecies or geographical race of S. officinalis (cf. Adam, 1941b: 1–4). It is closely related to S. hierredda Rang, 1837; however, more detailed studies will probably confirm the separation as marked differences are already recognized, such as maximal adult size much smaller than in S. hierredda, tentacular club relatively longer, some features of the sepion (wider and thicker in S. vermiculata, with stronger tuberculation on dorsal side, generally shorter striated zone), and geographical distribution. Little is known about the biology of the species. The usual capture depth is about 30–100 m.

Sepia vietnamica Khromov, 1987

FIGURE 70

Sepia nanshiensis Li and Chen, 1989:6, figs. 1–4.

DIAGNOSIS.—Arms of both sexes subequal. Arm suckers quadriserial. Tentacular club with slightly unequal suckers in 5 longitudinal rows. Sepion long, anteriorly rounded, posteriorly lanceolate. Anterior part of striated zone with median ventral furrow lying on keel. Anterior striae M-shaped. Inner cone surrounding but not overhanging posterior depression. Outer cone forming wings posteriorly. Spine present.

ORIGINAL REFERENCE.—Khromov, 1987a:35, fig. 1.

TYPE LOCALITY.—South China Sea, Gulf of Tonkin, 18°00′N, 107°08′E, depth 70 m.

TYPES.—Holotype: Zoological Institute, Academy of Sciences, Saint Petersburg, No. 7–1962, male, 41 mm ML.

Paratypes: Zoological Institute, Academy of Sciences, Saint Petersburg, 6 females, 32–50 mm, 9 males, 29–56 mm, from 12 stations in the Gulf of Tonkin, depths 0–104 m.

GEOGRAPHICAL DISTRIBUTION.—Gulf of Tonkin, central Vietnam; South China Sea, Nansha Islands, 13°N-18°N, 111°E–115°E (reported as S. nanshiensis, see “Discussion”).

DISCUSSION.—This is a fully described species of unquestioned status. The size is to 50 mm ML. The more recent description of Sepia nanshiensis by Li and Chen (1989) reports identical features and thus appears to relate to S. vietnamica.

Sepia whitleyana (Iredale, 1926)

See Lu (1998a).

FIGURE 70.—Sepia vietnamica: a, male, dorsal view; b, right tentacular club; c, sepion, ventral view; d, geographical distribution; e, sepion, anterior striated zone. (a-c,e, from Khromov, 1987a.)

FIGURE 71.—Sepia zanzibarica: a, right tentacular club; b, sepion, ventral view; c, geographical distribution.

Sepia zanzibarica Pfeffer, 1884

FIGURE 71

ILLUSTRATIONS.—Adam and Rees, 1966, pl. 2: figs. 9–11, pl. 41: fig. 247.

DIAGNOSIS.—Tentacular club with small, slightly unequal suckers in 6 rows, median suckers a little enlarged. Arm suckers quadriserial. Sepion elongate. Striated zone with wide, deep groove. Anterior striae L-shaped. Inner cone with moderately wide, rounded, ventral ledge over pocket-like cavity. Outer cone not forming posterior wings. Spine with lateral expansions at base.

ORIGINAL REFERENCE.—Pfeffer, 1884: fig. 11.

TYPE LOCALITY.—East Africa, Zanzibar.

TYPES.—Holotype: Zoological Museum, University of Hamburg, female, 186 mm ML.

Paratypes: None.

GEOGRAPHICAL DISTRIBUTION.—Western Indian Ocean from Port Elizabeth, South Africa, to the Gulf of Aden, including Madagascar and Saya-de-Malha Bank.

DISCUSSION.—This is a fully described species of unquestioned status. The size is to 250 mm ML, and the usual capture depth is about 30–50 m. This is one of the commercially important species in the Gulf of Aden.

Sepia sp. A

Sepia omani.—Voss and Williamson, 1971:37–38, pl. 9: figs. 5, 13 [not Adam and Rees, 1966:56].

Sepia rex.—Khromov, 1988b: 188–189, fig. 1 [not Iredale, 1926:193; Adam, 1979:177].—Lu, 1998a.

GEOGRAPHICAL DISTRIBUTION.—Known from Hong Kong to South Vietnam.

DISCUSSION.—This species, of the Rhombosepion species complex, was incorrectly identified as S. omani Adam and Rees by Voss and Williamson (1972), who described and illustrated Hong Kong specimens. The same specimens were later redescribed as S. rex (Iredale, 1926) by Khromov (1988b). Given the established error in Adam's (1979) redescription of the true S. rex (see Lu, 1998a), Khromov's specimens of S. rex from Vietnamese waters (see paratypes and specimens in the collections of the Zoological Institute, Russian Academy of Sciences, St. Petersburg) clearly represent a new species. This species closely resembles S. rex in sepion structure, but its tentacular club differs greatly and resembles that of S. omani (see discussions in Khromov, 1988b; Lu, 1998a). The species is currently being described by Khromov (in prep.).

Metasepia Hoyle, 1885

TYPE SPECIES.—Metasepia pfefferi Hoyle, 1885:199.

Metasepia pfefferi Hoyle, 1885

See Lu (1998a).

Metasepia tullbergi Appellöf, 1886

FIGURE 72

ILLUSTRATIONS.—Sasaki, 1929, pl. 18: figs. 16–19; Voss and Williamson, 1971, figs. 6, 15, pl. 10.

FIGURE 72.—Metasepia tullbergi: a,b, dorsal, ventral views of sepion; c, left tentacular club; d, geographical distribution. (a–c, after Sasaki, 1929.)

DIAGNOSIS.—Mantle oval, dorsal margin bluntly triangular, ventral margin shallow, emarginated. Tentacular club short, with 50–60 suckers in 6 longitudinal rows; 4 to 5 suckers on second dorsal series largest. Swimming membrane extends far beyond carpus. Arm suckers quadriserial. Left arm IV of male hectocotylized by reduction of sucker size in middle of arm. Sepion shorter than mantle, rhomboidal, length 2 times width, acute anteriorly, extending to keel-shaped spine posteriorly. Dorsal surface chitinous. Striated zone with shallow, median furrow. Inner cone vestigial. Outer cone absent.

ORIGINAL REFERENCE.—Appellöf, 1886:26, pl. 2: figs. 7–14.

TYPE LOCALITY.—Japan, Nagasaki.

TYPES.—Holotype: Zoological Museum of Uppsala University, Sweden, No. 295, animal in poor condition, 41 mm ML, sepion separate, 34.5 mm, in good condition.

Paratypes: Unknown.

GEOGRAPHICAL DISTRIBUTION.—Southern Honshu, Japan; Taiwan; Hong Kong; Gulf of Tonkin.

DISCUSSION.—The size is to 65 mm ML, and the usual capture depth is 0–100 m. A color photograph of a living animal showing the flamboyant pattern is reproduced in Roper and Hochberg (1988, fig. 42). See also Lu (1998a) on M.pfefferi.

Genus Sepiella Gray, 1849

TYPE SPECIES.—Sepia ornata Rang, 1837:76.

Sepiella ornata (Rang, 1837)

FIGURE 73

ILLUSTRATIONS.—Adam, 1939c, figs. 9–11; Adam, 1952, fig. 12, pl. II: figs. 3–5.

DIAGNOSIS.—Mantle elongate, oval. Fins with row of 7 red spots along bases. Arm suckers quadriserial. Left arm IV of male hectocotylized in basal art, with fleshy, transverse ridges carrying total of about 40 minute suckers in 2 double series of alternating suckers. Tentacular club narrow, with minute, subequal suckers in 10–14 longitudinal rows. Sepion width 24%–30% of length. Inner cone broadly V-shaped. Outer cone broad, wing-like.

ORIGINAL REFERENCE.—Rang, 1837:76.

TYPE LOCALITY.—Gulf of Guinea.

TYPE.—Type not traced.

GEOGRAPHICAL DISTRIBUTION.—Eastern Atlantic, off West Africa from Cape Blanco to Cape Frio.

DISCUSSION.—The size is to 100 mm ML, and capture depth is to 150 m (usually deeper than 30 m, exceptionally 20 m).

Sepiella cyanea Robson, 1924

FIGURE 74

ILLUSTRATIONS.—Adam and Rees, 1966, pl. 36: figs. 208–215.

DIAGNOSIS.—Mantle elongate, oval, bluntly rounded posteriorly. Fins fairly wide, arising few millimeters behind mantle margin and extending beyond posterior end of mantle where fused at fin bases. Arm suckers quadriserial. Left arm IV of male hectoctylized in basal art, with fleshy ridges and two dozen alternate pairs of minute suckers. Tentacular club suckers subequal, in 10–14 longitudinal rows. Sepion width 29%–36% of length. Inner cone forming knob posteriorly between short narrow limbs. Outer cone very broad.

ORIGINAL REFERENCE.—Robson, 1924a: 13.

TYPE LOCALITY.—South Africa, S.S. Pickle station 476, 29°17′S, 31°33′E, depth 51 m.

TYPES.—Lectotype: The Natural History Museum, London, 1924.9.9.40, male, 74 mm ML (designated by Adam and Rees (1966)).

Paralectotype: Missing (S.S. Pickle station 389, 29°27′S, 31°89′E, depth 73 m).

GEOGRAPHICAL DISTRIBUTION.—From Port Elizabeth, South Africa, to central Mozambique.

FIGURE 73.—Sepiella ornata: a,b, dorsal, ventral views of sepion; c, geographical distribution, (a,b, after Adam, 1939c.)

FIGURE 74.—Sepiella cyanea: a,b, dorsal, ventral views of sepion; c, geographical distribution, (a,b, after Adam, 1939c.)

DISCUSSION.—This species is closely related to S. ornata from the West African coast. The size is to 80 mm ML, and the usual capture depth is 25–50 m.

Sepiella inermis Orbigny, 1848, in Férussac and Orbigny, 1934–1848

FIGURE 75

ILLUSTRATIONS.—Adam, 1939c, figs. 1–5, pl. IV: figs. 5, 6; Adam and Rees, 1966, pl. 38: figs. 222–227, pl. 40: figs. 233, 234.

FIGURE 75.—Sepiella inermis: a,b, dorsal, ventral views of sepion; c, tentacular club; d, geographical distribution, (a,b, after Adam, 1939c; c, after Orbigny, 1848, in Férussac and Orbigny, 1834–1848.)

DIAGNOSIS.—Mantle elongate, oval. Fins with row of more than 7 red spots along bases. Arms stout, arms I indistinctly keeled, other arms with outer keel. Arm suckers quadriserial. Left arm IV of male hectocotylized. Medial tentacular club with minute, subequal suckers in 16–24 longitudinal rows. Sepion broadly oval, ventral surface strongly convex in lateral view, dorsal surface with low median rib. Sepion width 35%–45% of length. Inner cone forming thick, narrow, rounded posterior ridge. Outer cone forming semicircular, wing-like posterior portion.

ORIGINAL REFERENCE.—Orbigny, 1848:286, in Férussac and Orbigny, 1834–1848.

TYPE LOCALITY.—Indian Ocean.

TYPES.—Syntypes (9): Muséum National d'Histoire Naturelle, Paris: 1–7–235, 1 female, 60 mm ML; 1–7–254, 1 sepion, 57 mm; 1–7–255, 1 sex indet., 27 mm ML; 1–7–256, 3 sepions, damaged; 1–7–257, 1 female, 51 mm ML; 1–7–258, 1 sepion, 57 mm; 1–7–259, 1 female, 48 mm ML; 1–7–1200, 1 male, 57 mm ML; 1–7–1201, 1 sepion, damaged.

GEOGRAPHICAL DISTRIBUTION.—From Persian Gulf and southern Red Sea to mouth of Zambezi River, east to eastern Indonesia and Gulf of Tonkin.

DISCUSSION.—This is a fully described species of unquestioned status. The size is to 120 mm ML, and the usual capture depth is about 20–40 m.

Sepiella japonica Sasaki, 1929

FIGURE 76

Sepiella maindroni Rochebrune, 1884:89.

Sepiella heylei Sasaki, 1929:221.

ILLUSTRATIONS.—Adam and Rees, 1966, pl. 39: figs. 228–231.

DIAGNOSIS.—Mantle broadly oval. Fins relatively narrow anteriorly, begining about 10 mm behind mantle margin, with whitish line along fin base and white spots scattered on entire dorsal surface. Arm suckers quadriserial. Left arm IV of male hectocotylized in proximal art–art, with distinct size reduction of 40–50 suckers. Tentacular club slender, art–art of tentacle, with uniform minute suckers in 16–32 longitudinal rows. Sepion elliptical, somewhat drawn out posteriorly, width 30%–35% of length. Inner cone broadly V-shaped, with short limbs. Outer cone broad.

ORIGINAL REFERENCE.—Sasaki, 1929:219, fig. 170, pl. 18: figs. 20–23, pl. 19: fig. 28.

TYPE LOCALITY.—Japan, Etchu province (= Toyama Prefecture).

TYPES.—Holotype: Designation unclear; deposited at Fisheries Museum, Faculty of Fisheries, Hokkaido University, Hakodate, Japan.

Paratypes: Not known.

GEOGRAPHICAL DISTRIBUTION.—From central Honshu, Japan, to Canton, China, and Philippine Islands.

DISCUSSION.—This is a fully described species of unquestioned status. The size is to nearly 200 mm ML, and the usual capture depth is about 20–50 m. The first successful rearing experiments were done by Choe (1966) under the name Sepiella maindroni. This is an important fisheries species in Japan, South Korea, and China.

FIGURE 76.—Sepiella japonica: a,b, dorsal, ventral views of sepion; c. geographical distribution, (a,b, after Sasaki, 1929.)

Sepiella ocellata Pfeffer, 1884

ILLUSTRATIONS.—Adam, 1939c, figs. 12, 13.

DIAGNOSIS.—Not diagnosed.

ORIGINAL REFERENCE.—Pfeffer, 1884:13, figs. 17, 17a, 17b.

TYPE LOCALITY.—Java.

TYPES.—Holotype: Zoological Museum, University of Hamburg, male, 49.5 mm ML (not examined).

Paratypes: None.

GEOGRAPHICAL DISTRIBUTION.—Known only from type locality.

DISCUSSION.—Sepiella ocellata is known from a single male specimen. The general aspect of the animal is very similar to S.ornata of the West African coast, but the sepion is narrower, and the number of longitudinal sucker rows on the tentacular club is 8–10. The sepion of S. ocellata is less pointed anteriorly and posteriorly, and the outer cone is wider than in S. ornata (Adam, 1939c: 105). In spite of differences in sepion proportions (see Adam and Rees, 1966, pl. 35) and tentacular club characteristics, this species could be placed in the synonymy of Sepiella ornata if the type locality were not so far removed from the distribution area of S. ornata. Until the holotype is reexamined and more material from Java becomes available for study, S. ocellata is best considered a species of questionable status.

FIGURE 77.—Sepiella weberi: a.b, dorsal, ventral views of sepion; c, geographical distribution, (a,b. after Adam, 1939c.)

Sepiella weberi Adam, 1939

FIGURE 77

Sepiella metwardi Iredale, 1954:78.

DIAGNOSIS.—Mantle elongate, broadly rounded posteriorly. Anterior mantle margin pointed. Fins starting 5–6 mm behind mantle margin and narrowing anteriorly, broader posteriorly but not as broad as in Sepiella inermis. Fin with row of 5 to 6 spots dorsally along base. Left arm IV of male hectocotylized. Tentacular club with minute, subequal suckers in 10–12 longitudinal rows. Sexual dimorphism in arm sucker denticulation and sepion shape. Sepion bluntly pointed anteriorly, lateral rims of posterior art almost parallel, width about 30% of length. Outer cone broadly rounded.

ORIGINAL REFERENCE.—Adam, 1939c:98, figs. 6–8, pl. 4: figs. 1, 2.

TYPE LOCALITIES.—Indonesia, Timor (8°35′S, 126°00′E) and Sumba (10°00′S, 119°56′E) islands, depth 18 m.

TYPES.—Syntypes: Zoological Museum, University of Amsterdam: 1 male, 60 mm ML, Timor; 1 female, 67 mm ML, Sumba.

GEOGRAPHICAL DISTRIBUTION.—Sumba and Timor islands and Timor Sea (around 12°S, 127°E), eastern Indonesia; northern Australia near Darwin (12°27′S, 130°50′E). Depth 1–88 m.

DISCUSSION.—Examinations of the holotype of Sepiella melwardi Iredale, 1954, and of new material in the collections of the National Museum of Victoria (Melbourne) from the Timor and Arafura Seas confirm the synonymy of S. melwardi.

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Appendix I

Taxonomic Keys

D.N. KHROMOV

Key to the Genera and Species Complexes of Sepiidae

FIGURE 78.—Sepions in dorsal (a,d), lateral (b,e), and ventral (c,f) views from 2 representatives of Acanthosepion species complex: a–c, Sepia zanzibarica; d–f, S. prashadi.

FIGURE 79.—Some key features of mantle and sepion outlines, funnel cartilages, and arm and tentacle club patterns. a–d, dorsal views of mantle, sepion outlines indicated by dashed lines; e–h, ventral views of anterior mantle and funnel; i–k, funnel cartilages; I, arm with transformed protective membrane; m, club. a,f,i,m, Sepia sensu stricto; c,k, Sepiella; b,g,h, Hemisepius; d,e,j, Metasepia; I, Doratosepion.

FIGURE 80.—Schematic representations of sepion in ventral view. a–g, 7 representatives of Acanthosepion species complex; h, juvenile form of Sepia pharaonis, Sepia sensu stricto species complex. a, Sepia esculenta; b, S. thurstoni (after Adam and Rees, 1966); c, S. recurvirostra; d, S. savignyi; e. S. lycidas; f, S. stellifera; g, S. brevimana.

FIGURE 81.—Sepions in ventral and/or lateral view from representatives of Sepia sensu stricto species complex: a, Sepia latimanus; b, S. apama; c, S. insignis; d, S. plangon; e, S. bertheloti; f,g, S. simoniana; h, S. mestus; i, S. dollfusi (a,c,i, after Adam and Rees, 1966).

FIGURE 82.—Sepions in dorsal (a,d), lateral (b,e), and ventral (c,f) views from 2 representatives of Sepia sensu stricto species complex: a–c, Sepia vermiculata; d–f, S. pharaonis.

FIGURE 83.—Sepions in dorsal (d,e), lateral (b,f), and ventral (c,g) views from 2 representatives of Rhombosepion species complex: a–d. Sepia acuminata (d, atypical sepion with dorsal furrow, from Kenya); e–g. S. hieronis.

FIGURE 84.—Sepions in ventral view from 5 representatives of Rhombosepion species complex (a–e) and 2 representatives of the Anomalosepia species complex (f,g): a, Sepia elegans; b, S. orbignyana; c, S. sp. A; d, S. madokai; e, S. reesi (after Adam, 1979); f, S. australis; g, S. omani.

FIGURE 85.—Sepions in ventral view from 7 representatives of Doratosepion species complex (a–g) and 3 representatives of Hemisepius species complex (h–j): a, Sepia carinata; b, S. appellöfi; c, S. longipes; d, S. kobiensis; e, S. erostrata; f, S. mira; g, S. arabica; h, S. typica; i. S. faurei; j. S. pulchra. (b,c,e, after Sasaki, 1929; f, after Iredale, 1954; h,i, after Roeleveld, 1972; j, after Roeleveld and Liltved, 1985.)

FIGURE 86.—Sepions in ventral and/or lateral and dorsal views from 2 representatives of Doratosepion species complex (a–e) and 1 representative of Hemisepius species complex (f,g): a,b, Sepia ivanovi; c–e, S. incerta; f–g, S. dubia, (f,g, after Adam and Rees, 1966.)

FIGURE 87.—Sepions in ventral view from 4 species of Sepiella (a–d) and 2 species of Metasepia (e–g): a, Sepiella japonica; b, S. weberi; c, S. ornata; d, S. ocellata; e,f, Metasepia tullbergi (f, lateral view); g, M. pfefferi.

FIGURE 88.—Sepions in dorsal (a,d), lateral (b,e), and ventral (c,f) views from 2 species of Sepiella: a–c, S. inermis: d–f, S. cyanea.

Key to Species of Sepia, Species Complex Sepia sensu stricto

Key to Species of Sepia, Species Complex Anomalosepia

Key to Species of Sepia, Species Complex Rhombosepion

Key to Species of Sepia, Species Complex Anomalosepia

Key to Species of Sepia, Species Complex Doratosepion

Key to Species of Sepia, Species Complex Hemisepius

Key to Species of Metasepia

Key to Species of Sepiella

Appendix II

Nominal Type Specimens of Sepiidae in The Natural History Museum, London (BMNH)

M.R. LIPINSKI, F.A. NAGGS, AND M.A. ROELEVELD

acuminata, Sepia; Smith, 1916: BMNH 1890.9.22.332–3, syntypes.

andreanoides, Sepia; Hoyle, 1885 (= Sepia kobiensis Hoyle, 1885) emend. Adam: BMNH 1889.4.24.78–79, syntypes.

apama, Sepia; Gray, 1849: BMNH 1846.5.25.2, holotype.

burnupi, Sepia; Hoyle, 1904: BMNH 1905.1.19.5, holotype; BMNH 1904.2.13.5, paratype.

confusa, Sepia; Smith, 1881: BMNH 1920.3.23.1, holotype.

cultrata, Sepia; Hoyle, 1885: BMNH 1889.4.24.75, holotype.

cyanea, Sepiella; Robson, 1924: BMNH 1924.9.9.40, lectotype.

dubia, Sepia (Hemisepius); Adam and Rees, 1966: BMNH 1963.103W, holotype.

elliptica, Sepia; Hoyle, 1885: BMNH 1889.4.24.71–72, syntypes; BMNH 1889.4.24.73–74, syntypes.

esculenta, Sepia; Hoyle, 1885: BMNH 1889.4.24.69–70, syntypes.

foxi, Ascarosepion singhalensis var.; Robson, 1927 (= Sepia pharaonis Ehrenberg, 1931): BMNH 1926.4.8.5, holotype; BMNH 1926.4.8.5, paratype.

hieronis, Rhombosepion; Robson, 1924 (= Sepia hieronis (Robson, 1924)): BMNH 1924.9.9.54–56, syntypes.

incerta, Sepia; Smith, 1916: BMNH 1890.12.14.43–44, syntypes.

insignis, Sepia; Smith, 1916: BMNH 1920.3.23.5, holotype.

joubini, Sepia (Doratosepion); Massy, 1927: BMNH 1926.10.20.38, syntype; BMNH 1926.10.2039–40, syntypes.

kiensis, Sepia; Hoyle, 1885: BMNH 1889.4.24.80, holotype.

kobiensis, Sepia; Hoyle, 1885: BMNH 1889.4.24.81, holotype.

koettlitzi, Sepia; Hoyle, 1901 (= Sepia pharaonis Ehrenberg, 1831): BMNH 1903.1.2.1, holotype.

lycidas, Sepia; Gray, 1849: BMNH 1963119W, holotype.

mestus, Sepia; Gray, 1849: BMNH 1842.11.9.84, syntype; BMNH 1842.11.11.13, syntype.

murrayi, Sepia; Adam and Rees, 1966: BMNH 196381W, holotype; BMNH 196383W, paratype.

myrsus, Sepia; Gray, 1849 (nomen dubium; specimen abnormal): BMNH 1841.4.6.89, holotype.

omani, Sepia; Adam and Rees, 1966: BMNH 1963107W, holotype; BMNH 1963108–114W, paratypes.

papuensis, Sepia; Hoyle, 1885: BMNH 1889.4.24.68, syntype.

pfefferi, Sepia; Hoyle, 1885: BMNH 1890.1.24.11, holotype.

plangon, Sepia; Gray, 1849: BMNH 1963126W, syntype; BMNH 1842.11.9.85, syntype.

prashadi, Sepia; Winckworth, 1936: BMNH 1952.11.24.59, paratype.

robsoni, Rhombosepion; Massy, 1927 (= Sepia robsoni (Massy, 1927)): BMNH 1926.10.20.8, holotype.

sewelli, Sepia; Adam and Rees, 1966: BMNH 196378W, holotype; BMNH 196379W, paratype; BMNH 196380W, paratypes.

sinope, Sepia; Gray, 1849 (? = Sepia australis Quoy and Gaimard, 1832): BMNH 196385W, holotype.

sulcata, Sepia; Hoyle, 1885: BMNH 1889.4.24.77, holotype.

thurstoni, Sepia; Adam and Rees, 1966: BMNH 1894.9.6.2–4, holotype; BMNH 1947.5.5.36, paratype.

vicellius, Sepia; Gray, 1849 (= Sepia officinalis Linnaeus, 1758): BMNH 1963120W (Gray's catalog number 29a,b), holotype.

A Synopsis of Sepiidae in Australian Waters (Cephalopoda: Sepioidea)

C.C. Lu

_____________

C.C. Lu, Department of Zoology, National Chung Hsing University, Taichung, Taiwan.

ABSTRACT

The Australian cuttlefish fauna (Family Sepiidae) is reviewed. Twenty-six species are considered distinct; of these, three species are known from the sepions only and are considered to be of uncertain status at present. The species are Sepia apama, S. baxteri, S. braggi, S. chirotrema, S. cottoni, S. cultrata, S. dannevigi, S. elliptica, S. hedleyi, S. irvingi, S. latimanus, S. mestus, S. mira, S. novaehollandiae, S. opipara, S. papuensis, S. pharaonis, S. plangon, S. reesi, S. rex, S. rozella, S. smithi, S. vercoi, S. whitleyana, Metasepia pfefferi, and Sepiella weberi.

For each species, where data are available, diagnoses, including characters of the tentacular club, hectocotylization, and sepion, as well as information on type specimens, distribution, and synonyms are provided.

Introduction

The family Sepiidae is speciose. According to Adam and Rees (1966) there are approximately 101 possibly valid species in the genus Sepia, and seven valid species in the genus Sepiella. The systematics of the family, and especially of the genus Sepia, has been in a state of confusion for many years. Many species are known only fragmentarily. Often the descriptions are based on single specimens, or even more often, on cuttlebones (sepions) collected on the beach. The international Workshop on the Biology and Resource Potential of Cephalopods (Roper et al., 1983) designated the family Sepiidae as one of the four major families of commercially and ecologically important cephalopods that require immediate and comprehensive systematic research.

The identification of the Australian sepiids is particularly difficult. The wholesale naming of species by Iredale (1926a, 1926b, 1940, 1954) and Cotton (1929, 1931, 1932) created a chaotic situation. Of the 63 nominal species and subspecies of Sepiidae recorded from Australia, Iredale and Cotton were responsible for the naming of 29 and seven, respectively (Lu and Phillips, 1985). All of these species/subspecies were described solely on the basis of sepions; the soft parts of the animals were not described. The masterful review of the Sepiidae by Adam and Rees (1966) is limited by the fact that little Australian material was studied. The value of Adam's (1979) review of the Sepiidae collection in the Western Australian Museum again is reduced by his exclusion of the eastern Australian material, particularly the type material held in the Australian Museum. A critical study of the Australian sepiids based on new material from all state museum collections is now in progress.

The present synopsis is based on the checklist of cephalopods from Australian waters by Lu and Phillips (1985) and on the above study in progress. The classification system follows that of Adam and Rees (1966) and Adam (1979), although a different classification has been proposed more recently by Khromov (1987a). The present work includes information on type specimens and remarks on species validity resulting from study of the type specimens. All type specimens have been examined by the author, unless otherwise stated. Photographs of all type specimens examined are included. The information on geographical and bathymetric distributions are based on material examined to date.

ACKNOWLEDGMENTS.—I am grateful to all curators and collection managers responsible for the cephalopod collections in all Australian state and territory museums for their help in providing information, type specimens, and other material for study. I am in debt to R. Start and C. Rowley for their contribution in taking the photographs and to P. Storer who patiently typed the various versions of the manuscript. Sigurd Boletzky, Nancy Voss, and two anonymous reviewers read the manuscript and gave valuable advice for which I am grateful.

ABBREVIATIONS AND DEFINITIONS

Museums

AM

Australian Museum, Sydney

BMNH

The Natural History Museum, London, formerly British Museum (Natural History)

MNHNP

Museum National d'Histoire Naturelle, Paris

NMV

Museum of Victoria, Melbourne

SAM

South Australian Museum, Adelaide

WAM

Western Australian Museum, Perth

ZMA

Zoological Museum, University of Amsterdam

Localities

Vic

Victoria

SA

South Australia

WA

Western Australia

NT

Northern Territory

Qld

Queensland

NSW

New South Wales

Tas

Tasmania

NW Shelf

North West Shelf of Western Australia

Morphometrics

ML

Mantle length

SL

Sepion length, excluding spine unless otherwise stated

LocLI

Loculus length index: length of loculus as percentage of sepion length

StrZI

Striated zone length index: length of striated zone as percentage of sepion length

Species Accounts

Family SEPIIDAE Keferstein, 1866

DIAGNOSIS.—Animal small to medium-sized (although several species reach 500 mm ML), bearing characteristic calcareous sepion. Sepion porous, finely laminated, and located at dorsal side of mantle underneath skin. Spine at posterior end of sepion may be absent in some species. Mantle broad or slender, robust, elongate-oval to circular in outline, slightly flattened dorsoventrally. Fins narrow, lateral to mantle, occupying almost entire length of mantle. Posterior end of fins not connected to mantle, forming free lobe. Arm suckers biserial to quadriserial. Tentacles retractable into pockets on ventrolateral sides of head. Tentacular clubs with 4–8 or more rows of suckers. Funnel-mantle locking apparatus curved to angular.

Sepia Linnaeus, 1758

DIAGNOSIS.—Posterior gland and pore absent, locking apparatus with semicircular tubercle on mantle component and corresponding depression in funnel component.

Sepion elliptical to subrhomboidal or lanceolate; inner cone always with relatively long limbs (longer than in Sepiella and Metasepia). Note: incomplete calcification of phragmocone found in several species (Khromov et al., 1998).

Sepia apama Gray, 1849

FIGURE 1

Sepia palmata Owen, 1881:134. [Norfolk Island (29°05′S, 168°00′E), type lost.]

Amplisepia verreauxi Iredale, 1926a:194. [Not Rochebrune, 1884; Sydney, NSW (33°53′S, 151°13′E), specimen not traced.]

Amplisepia parysatis Iredale, 1954:71. [Holotype, AM C133307, 194 mm SL (spine obscured by outer cone), Shark Bay, WA (26°07′S, 113°25′E).]

DIAGNOSIS.—Mantle broadly oval; anterior dorsal margin broadly convex, projecting to level of anterior border of eye; ventral margin emarginate. Dorsal surface of head with 3 flat, semicircular, flap-like papillae posterior to each eye. Swimming membrane of tentacular club slightly longer than club length. Protective membranes fused at base of club, completely surrounding sucker-bearing face of club. Club suckers in 5 longitudinal series, those on median series largest (Figure 1a). Arm suckers quadriserial. Left arm IV hectocotylized, suckers on proximal part in 6–10 rows and slightly smaller than corresponding suckers on right arm IV.

Sepions (Lu, 1998, figs. 2, 3) in juveniles broadly oval, wider in anterior art. Dorsal surface flat anteriorly, ribs faint. Ventral surface flat with faint linear median groove in striated zone and broad, shallow depression in last loculus. Inner cone well developed, lateral limbs broad, fused to outer cone; limbs on posterior art of outer cone as large as those of inner cone, continuous between spine and inner cone as narrow ledge. Spine of subadult sepion straight, without keels; with growth, posterior sepion becomes more acuminate, spine disappears, and V-shaped callus develops on posterior inner edge of inner cone. Adult sepion elongate, spine completely covered by chitin, callus on posterior end of inner cone very pronounced.

ORIGINAL REFERENCE.—Gray, 1849:103.

TYPE LOCALITY.—Port Adelaide, SA (34°50′S, 138°30′E).

TYPE.—Holotype: BMNH 1846.5.252, by monotypy, only sepion extant, 286 mm long, 102 mm wide.

GEOGRAPHICAL DISTRIBUTION.—Southern Australia from southern Qld at least from Moreton Bay (27°25′S, 153°20′E) to Point Cloates, WA (22°43′S, 113°40′E), at depths of 1–100 m.

DISCUSSION.—Sepia apama is endemic in southern Australian waters, and it grows to large size (largest specimen examined 520 mm ML).

Sepia baxteri (Iredale, 1940)

FIGURE 2

Blandosepia baxteri Iredale, 1940:442. [Holotype, AM C133317, 79 mm SL.]

DIAGNOSIS.—Sepion elongate-oval, roundly pointed anteriorly, broadly oval posteriorly, width 41%–48% of length. Dorsal surface with finely reticulate sculpturing, china white. Ventral surface slightly concave toward long median groove. Striae slightly wavy posteriorly, strongly arched anteriorly. Striated zone long; StrZI 75.7 in holotype. Limbs of inner cone narrow, thin, reaching about art length of striated zone, broadened posteriorly. Spine replaced by small, obtuse, pinkish brown tubercle.

FIGURE 1.—a, Sepia apama Gray, 1849, left club of male subadult specimen (102 mm ML), Westernport, Vic, NMV F30233 (scale = 20 mm). b,c, Amplisepia parysatis Iredale, 1954, holotype, sepion only (194 mm SL), Shark Bay, WA, AM C133307 (scale = 100 mm): b, dorsal view; c, ventral view.

ORIGINAL REFERENCE.—Iredale, 1940:442.

TYPE LOCALITY.—Lord Howe Island, NSW (31°33′S, 159°05′E).

FIGURE 2.—Blandosepia baxteri Iredale, 1940, holotype, sepion only (79 mm SL), Lord Howe Island, NSW, AM C133317 (scale = 20 mm): a, dorsal view; b, ventral view.

TYPE.—Holotype: AM C133317, by original designation, only sepion extant, 74 mm SL, no spine (Figure 2).

GEOGRAPHICAL DISTRIBUTION.—Lord Howe Island, NSW (31°33′S, 159°05′E).

DISCUSSION.—This species is known only from the type specimen and seven other sepions reported by Iredale (1954); the soft parts are unknown. The status of this species is uncertain at present.

Sepia braggi Verco, 1907

FIGURES 3, 4

Arctosepia limata Iredale, 1926a:193. [Holotype, AM C133316, 36.2 mm SL (37.5 mm including spine), Manly Beach, NSW (33°48′S, 151°17′E).]

Arctosepia versuta Iredale, 1926a:194. [Holotype, AM C133313, 31.4 mm SL (32.3 mm including spine), Manly Beach, NSW (33°48′S, 151°17′E).]

Arctosepia rhoda Iredale, 1954:75. [Holotype, AM C133319, 47.7 mm SL (51.3 mm including spine), Point Cloates, WA (22°43′S, 113°40′E).]

Arctosepia treba Iredale, 1954:75. [Syntypes (2), AM C133324, missing anterior ends, not measured, Stanley, Tas (40°46′S, 145°18′E).]

Arctosepia braggi xera Iredale, 1954:74. [Holotype, AM C133310, 77 mm SL, Stanley, Tas (40°46′S, 145°18′E).]

DIAGNOSIS.—Mantle elongate; anterior dorsal margin acuminate, reaching midlevel of eye; ventral margin deeply emarginate around funnel. Swimming membrane of tentacular club well developed, extended beyond base of club. Protective membranes separated at base of club. Club suckers in 5 longitudinal series, 5 or 6 suckers of middle series twice as wide as others (Figure 3a). Arm suckers quadriserial on arms IV of both sexes, suckers on other arms quadriserial basally, biserial on effilated tips, especially on arms II of female and arms III of male where suckers are minute and well spaced. Mature male without trace of hectocotylization on arms.

FIGURE 3.—a, Sepia braggi Verco, 1907, left club of male adult specimen (49 mm ML), 39°07.6′S, 143°25.0′E, NMV F55066 (scale = 5 mm). b,c, Sepia braggi Verco, 1907, holotype, sepion only (59 mm SL), Glenelg, SA, SAM D14130 (scale = 20 mm): b, dorsal view; c, ventral view. d,e, Arctosepia limata Iredale, 1926, holotype, sepion only (36.2 mm SL), Manly Beach, NSW, AM C133316 (scale = 20 mm): d, dorsal view; e, ventral view. f,g, Arctosepia versuta Iredale, 1926, holotype, sepion only (31.4 mm SL), Manly Beach, NSW, AM C133313 (scale = 20 mm): f, dorsal view; g, ventral view.

FIGURE 4 (scale = 20 mm).—a,b, Arctosepia rhoda Iredale, 1954, holotype, sepion only (47.7 mm SL), Point Cloates, WA, AM C133319: a, dorsal view; b, ventral view. c,d, Arctosepia treba Iredale, 1954, syntype, sepion only, Stanley, NW Tas, AM C133324: c, dorsal view; d, ventral view. e,f, Arctosepia treba Iredale, 1954, syntype, sepion only, Stanley, NW Tas, AM C133324: e, dorsal view; f, ventral view. g,h, Arctosepia braggi xera Iredale, 1954, holotype, sepion only (77 mm SL), Stanley, NW Tas, AM C133310: g, dorsal view; h, ventral view.

Sepion (Figures 3, 4) elongate, broadest in anterior art, acutely rounded at anterior end and acuminate posteriorly. Dorsal surface with distinct, low, narrow median ribs, calcareous covering weakly granulose, rose posteriorly, white anteriorly. Ventral surface with distinct, narrow median groove along entire length, widening in anterior part of last loculus; median groove with slightly convex rib on each side, in anterior striated zone rib abruptly sloping flat or concave laterally, separated from outer cone by smoother, narrow, marginal zone, separated from striated zone by narrow limit of inner cone; limbs of inner cone descended into middle of smooth marginal zone. Striae convex on each side of median groove and incurved V-shaped in groove. Limbs of inner cone narrow, with rounded ridges, posteriorly forming slightly sharper ledge, and surrounding shallow posterior excavations. Outer cone narrow, forming 2 short posterior wings surrounding posterior part of inner cone and constituting cup-like formation. Spine slightly constricted at base, without keels, turned upward.

ORIGINAL REFERENCE.—Verco, 1907:213, pl. 27: fig. 6.

TYPE LOCALITY.—Glenelg, SA (34°58′S, 138°32′E).

TYPE.—Holotype: SAM D14130, by monotypy, sepion only, 59 mm SL (62.0 mm including spine) (Figure 3b,c).

GEOGRAPHICAL DISTRIBUTION.—Southern Australia from southern Qld (26°30′S, 153°44′E) to Point Cloates, WA (22°43′S, 113°40′E), at depths of 30–146 m.

Sepia chirotrema Berry, 1918

FIGURE 5

Solitosepia hendryae Cotton, 1929:87. [Holotype, SAM D13625, 74 mm SL (78 mm including spine), Rottnest Island, WA (32°00′S, 115°30′E).]

Solitosepia glauerti Cotton, 1929:87. [Holotype, SAM D13628, 49.5 mm SL (51 mm including spine), Rottnest Island, WA (32°00′S, 115°30′E).]

DIAGNOSIS.—Anterior dorsal margin of mantle large, triangular, rostrum-like; ventral margin broadly emarginate without distinct lateral angle. Head with group of 3 conspicuous tubercles on each side between eye and nuchal cartilage, 3 smaller tubercles in arcuate line in front of cartilage. Swimming membrane on tentacular club strong, reaching beyond base of club for short distance. Protective membranes fused at base of club, attached to tentacular stem by short membrane, dorsal protective membrane thick and wide, separated from swimming membrane by deep cleft and perforated by 3 large openings, each situated opposite 1 of 3 large tentacular suckers. Three very large suckers occupy main part of club, median sucker largest, distal sucker slightly smaller, and proximal sucker smaller still, each with long slender stalk attaching sucker to bottom of deep pit; pits separated by transverse membranes bearing 1 small sucker on dorsal side and 2 smaller suckers on ventral side; distal club with 40–50 small, quadriserial suckers (Figure 5a). Left arm IV hectocotylized, distal end attenuated, narrow, and compressed laterally, bearing microscopic suckers.

Sepion sexually dimorphic, wider in males (Figure 5b,c) than in females of same size. Anterior end of male sepion acuminate, posterior end broadly rounded. Dorsal surface granulose, with very distinct, well-defined median rib and 2 less-developed lateral ribs separated from median rib on either side by flat surface about as wide as ribs. Ventral surface flat, with shallow median sulcus along entire length. Striae convex in posterior striated zone, weakly angular, reversed V-shaped near last loculus. Inner cone well developed, lateral limbs reflected and fused with outer cone. Spine strong, rounded, without keel, straight and directed upward; base of spine thickened, forming thick collar in large sepions, separated from spine by circular, radially striated groove; dorsal surface of sepion and spine separated by deep cleft.

ORIGINAL REFERENCE.—Berry, 1918:268, pl. 74: figs. 3–9, pls. 75–77.

TYPE LOCALITY.—Investigator Strait area (35°25′S, 137°22′E), south of Kangaroo Island, SA (35°50′S, 137°15′E), F.I.S. Endeavour sta E2459.

TYPE.—Type missing from Australian Museum. According to Berry (1918), holotype (by original designation) male, 183.0 mm ML.

GEOGRAPHICAL DISTRIBUTION.—Southern Australia from Investigator Strait (35°25′S, 137°22′E) to Dirk Hartog Island, WA (25°45′S, 113°03′E), at depths of 120–210 m.

DISCUSSION.—Adam (1979) considered Solitosepia hendryae Cotton, 1929, to be a junior synonym (young female of Sepia chirotrema) of Sepia chirotrema. This is confirmed by the present study after the reexamination of the type of S. hendryae (Figure 5d,e).

After studying the type and new materials in the collections of NMV, the present study also reveals that Solitosepia glauerti Cotton, 1929 (Figure 5f,g), represents a young male specimen of S. chirotrema. Solitosepia glauerti also is a junior synonym of Sepia chirotrema.

Sepia cottoni Adam, 1979

FIGURE 6

DIAGNOSIS.—Mantle elongate, more than twice as long as wide, posterior end acuminate; anterior dorsal margin strongly projected; ventral margin deeply emarginate. Swimming membrane well developed, extended slightly beyond base of tentacular club. Protective membranes separated at base of club. Club suckers in 5 longitudinal series, about 6 suckers in middle series twice as wide as other suckers (Figure 6a). Strong sexual dimorphism in arms. Female arms subequal in length, short, stout, arm suckers quadriserial along most of arm length, biserial at base and distal end. Male arms IV not hectocotylized, arms twice as long as those of female, basal art of arms with few biserial suckers followed by 7 to 8 rows of quadriserial, large suckers, distal art of arms gradually narrower, distal art thread-like in all arms except arms III; basal arm with normal suckers, distally suckers diminish in size rapidly, become biserial, and disappear on thread-like tip; protective membranes on all arms except on arms III wide on basal art, lost on transformed distal art; protective membranes on middle part of male arms III thickened and widened, with thick, transverse ridges alternating with ridges uniting inner margin of one membrane and outer margin of opposite membrane, each transverse ridge bearing 2 small suckers.

FIGURE 5 (scale = 30 mm).—a, Sepia chirotrema Berry, 1918, left club of male adult specimen (157 mm ML), 33°45.2′S, 114°28.6′E, NMV F66201. b,c, Sepia chirotrema Berry, 1918, sepion of male adult specimen (113 mm ML), 28°30.5′S, 113°27.02′E, NMV F66202: b, dorsal view; c, ventral view. d,e, Solitosepia hendryae Cotton, 1929, holotype, sepion only (74 mm SL), Rottnest Island, WA, SAM D13625: d, dorsal view; e, ventral view. f,g, Solitosepia glauerti Cotton, 1929, holotype, sepion only (49.5 mm SL), Rottnest Island, WA, SAM D13628: f, dorsal view; g, ventral view.

FIGURE 6.—Sepia cottoni Adam, 1979, paratype, male (45.5 mm ML), 27°40′S, 113°20′E, WAM 424–65. a, left club (scale = 4 mm). b,c, sepion (scale = 20 mm): b, dorsal view; c, ventral view.

Sepion (Figure 6b,c) very elongate, broadest in anterior art, acutely rounded at anterior end and acuminate posteriorly. Dorsal surface weakly granulose, with distinct, low, narrow median rib vanishing toward posterior end. Ventral surface with shallow, narrow median groove along entire length. Striae slightly convex, nearly straight in middle of striated zone, with slight incurvation in median groove. Spine slightly constricted at base, without keels, directed upward, sometimes slightly curved with ventral side concave.

ORIGINAL REFERENCE.—Adam, 1979:193, pl. 11: figs. 1–6.

TYPE LOCALITY.—West of Lancelin, WA (31°54′S, 114°55′E), depth 114–122 m.

TYPE.—Holotype: WAM 435–65, by original designation, male specimen in alcohol, 43.5 mm ML.

GEOGRAPHICAL DISTRIBUTION.—Western Australia from Hassall Beach (34°49′S, 118°24′E) on the south coast to NW Broome (17°31.5′S, 121°27′E), at depths of 83–164 m. One sepion was collected from North Stradbroke Island, Qld (27°35′S, 153°27′E), implying a northern Australian distribution (Adam, 1979).

DISCUSSION.—This species is known only from the original description. No new material has been studied.

Sepia cultrata Hoyle, 1885

FIGURE 7

Glyptosepia gemellus Iredale, 1926a:192. [Holotype, AM C133306, 87 mm SL (92 mm including spine), Manly Beach, NSW (33°48′S, 151°17′E).]

Glyptosepia macilenta Iredale, 1926a:192. [Holotype, AM C133305, 83.5 mm SL (90 mm including spine), Manly Beach, NSW (33°48′S, 151°17′E).]

DIAGNOSIS.—Anterior dorsal mantle margin strongly projected beyond level of eye opening; ventral margin slightly emarginate. Strong swimming membrane about 1art times length of tentacular club. Dorsal protective membrane as wide as sucker-bearing surface of club and separated from ventral protective membrane at base. Club suckers small, subequal, in 5 to 6 longitudinal series (Figure 7a). Arm suckers quadriserial. Left arm IV of male hectocotylized; suckers on basal art and distal art of arm normal, 2 dorsal series of median arm suckers greatly reduced in size.

Sepion (Figure 7b,c) elongate-oval, attaining greatest width anterior of middle, anterior end triangular, posterior end acuminate and narrow. Dorsal surface color cream or salmon, flat anteriorly, with distinct, narrow median rib and 2 indistinct lateral ribs. Ventral surface flat, extreme posterior striated zone concave, anteriorly slightly convex; striae slightly convex. Limbs of inner cone very narrow, rounded ridges; posterior part forming slightly longer ledge surrounding posterior excavation. Outer cone narrow anteriorly, wider posteriorly, continuous between inner cone and spine. Spine without keels, turned upward, sometimes slightly curved with concave ventral side.

FIGURE 7.—a-c, Sepia cultrata Hoyle, 1885. a, left club of female adult specimen (93 mm ML), 38°12.7′S, 149°42.2′E, NMV F51923 (scale = 5 mm). b,c, sepion of female adult specimen (67 mm ML), 35°15.40′S, 149°19.50′E, NMV F66203 (scale = 30 mm): b, dorsal view; c, ventral view. d,e, Glyptosepia gemellus Iredale, 1926, holotype, sepion only (87 mm SL), Manly Beach, NSW, AM C133306 (scale = 30 mm): d, dorsal view; e, ventral view. f,g, Glyptosepia macilenta Iredale, 1926, holotype, sepion only (83.5 mm SL), Manly Beach, NSW, AM C133305 (scale = 30 mm): f, dorsal view; g, ventral view.

ORIGINAL REFERENCE.—Hoyle, 1885:198.

TYPE LOCALITY.—Off Twofold Bay, Australia, H.M.S. Challenger sta 163A (36°59′S, 150°20′E), 150 fathoms (274.5 m).

TYPE.—Holotype: BMNH 1889.4.24.75, by monotypy, female specimen in alcohol, 84 mm ML. Not examined.

GEOGRAPHICAL DISTRIBUTION.—Southern Australia from southern Qld (26°35′S, 153°45′E) to Houtman Abrolhos, WA (28°49′S, 114°04′E), including Tas (42°43′S, 148°22′E), at depths of 132–803 m, with majority of catches at 300–500 m.

Sepia dannevigi Berry, 1918

FIGURE 8

DIAGNOSIS.—Anterior dorsal mantle margin broad, conspicuous, triangular; ventral margin slightly emarginate below funnel. Swimming membrane of tentacular club extended beyond base of club. Tentacular club small, flattened, suckers numerous and minute in 10–12 longitudinal series at middle of club (Figure 8b). Arm suckers quadriserial throughout. Known only from 3 females; hectocotylized arm unknown.

Sepion unknown.

ORIGINAL REFERENCE.—Berry, 1918:264, figs. 51–54, pl. 73, pl. 74: figs. 1, 2.

TYPE LOCALITY.—Investigator Strait area (35°25′S, 137°22′E), south of Kangaroo Island, SA (35°50′S, 137°15′E), F.I.S. Endeavour sta E2466.

TYPE.—Holotype: AM 2466, by original designation, female specimen in alcohol, 82 mm ML (Figure 8a). Sepion missing.

FIGURE 8.—Sepia dannevigi Berry, 1918, holotype, female specimen (82 mm ML, sepion missing), Kangaroo Island, SA, AM 2466 (from Berry, 1918): a, dorsal view; b, club.

GEOGRAPHICAL DISTRIBUTION.—Known only from the original description of material collected from F.I.S. Endeavour; Investigator Strait area, south of Kangaroo Island, SA, and between Cape Naturaliste (33°32′S, 115°01′E) and Geraldton, WA (28°46′S, 114°37′E), in 20–100 fathoms (36.6–183 m).

DISCUSSION.—Adam (1979) suggested that this species may be synonymous with Sepia elliptica Hoyle, 1885; however, S. elliptica is an Indo-West Pacific species and extensive collections in southern Australia have not captured specimens identifiable to S. elliptica. I believe S. dannevigi is closer to, and may be conspecific with, S. hedleyi Berry, 1918, because of the similarity of the tentacular clubs, which possess 10–12 rows of minute suckers in both species, and because both species are known from the Great Australian Bight.

Sepia elliptica Hoyle, 1885

FIGURE 9

Acanthosepion ellipticum adjacens Iredale, 1926b:239. [Holotype, AM C133302, 98.7 mm SL (103.7 mm including spine), North-West Islet, Qld (23°18′S, 151°42′E).]

DIAGNOSIS.—Mantle broadly oval, broadest art from anterior margin, narrowing posteriorly; anterior dorsal margin produced, reaching midlevel of eye; ventral margin slightly emarginate. Swimming membrane extended beyond base of club. Protective membranes separated at base of club in smaller specimens, fused in large specimens; connected at base of club by a membranous ridge so that club is distinctly separable from tentacular stalk. Median tentacular club suckers (Figure 9a) in 10–12 longitudinal series; suckers minute, subequal in size. Arm suckers quadriserial, no sexual dimorphism in sucker size detected. Left arm IV of male hectocotylized, basal 7 to 8 rows of suckers normal, followed by 7 rows of modified suckers distally, 2 ventral suckers in each row slightly smaller, whereas 2 dorsal suckers on distal arm normal.

Sepion (Figure 9b,c) oval, acuminate anteriorly, slightly broader posteriorly, broadest art from anterior end, gradually narrowing posteriorly. Dorsal surface granulose, with broad median rib; median rib separated by 2 depressions from 2 lateral ribs, each lateral rib flanked by another depression along outer side. Ventral surface with shallow sulcus. Striated area concave, StrZI about 70 in mature specimens; striae arched. Limbs of inner cone large, posterior inner cone raised as flat, thin ledge with thickened rim. Outer cone large, posterolateral edges slightly flared. Spine slightly pointed upward, without keels.

ORIGINAL REFERENCE.—Hoyle, 1885:189.

TYPE LOCALITIES.—H.M.S. Challenger sta 188 (9°59′S, 139°42′E), Arafura Sea, South of Papua, 28 fathoms (53 m). H.M.S. Challenger sta 190 (8°56′S, 136°5′E), Arafura Sea, South of Papua, 49 fathoms (89.7 m).

FIGURE 9.—a, Sepia elliptica Hoyle, 1885, left club of female subadult specimen (78 mm ML), Cleveland Bay, off Townsville, Qld, NMV F66204 (scale = 10 mm). b,c, Acanthosepion ellipticum adjacens Iredale, 1926, holotype, sepion only (98.7 mm SL), North-West Islet, Qld, AM C133302 (scale = 50 mm): b, dorsal view; c, ventral view.

TYPES.—Syntypes: BMNH 1889.4.24.71–72, 1 male, 44 mm SL, 1 female, 72 mm SL (sta 188) (fide Hoyle, 1886; Adam and Rees, 1966); BMNH 1889.4.24.73–74, 1 male, 72 mm ML, 1 female, 54 mm ML (sta 190). Animals in alcohol (fide Adam and Rees, 1966); not examined.

GEOGRAPHICAL DISTRIBUTION.—Indo-West Pacific; Northern Australia from Exmouth Gulf, WA (22°23′S, 114°06′E), to Capricorn Group, Qld (23°30′S, 152°00′E), including Gulf of Carpentaria, at depths of 16–142 m.

DISCUSSION.—Adam (1979) considered Acanthosepion whitleyanum Iredale, 1954, to be a possible synonym of Sepia elliptica; however, examinations of the type and new material in the collections of AM and NMV reveal A. whitleyanum to be a different species (see Figure 26b,c). Adam (1979) also considered the possibility of Sepia dannevigi and S. elliptica being synonymous. Although I have no direct evidence to reject this suggestion, it must be pointed out that extensive collections of southern Australian sepiids in the collections of AM, NMV, and SAM do not contain S. elliptica from southern Australia.

Sepia hedleyi Berry, 1918

FIGURE 10

DIAGNOSIS.—Mantle with anterior dorsal margin conspicuous, triangular, projected, reaching level of anterior margin of eyes; ventral margin evenly emarginate below funnel, forming distinct angle at each side of funnel base. Tentacular club (Figure 10a) with numerous minute suckers of subequal size in 12 series. Arm suckers quadriserial, those of inner series larger than those of marginal series. Left arm IV hectocotylized; suckers in basal and distal art of arm normal, quadriserial, those in middle art greatly reduced in size and in 3 series only.

Sepion poorly known. Reconstructed sepion (Figure 10b) shows large chitinous margin and striated zone. LocLI 25–26. Striae nearly straight.

ORIGINAL REFERENCE.—Berry, 1918:258, figs. 48–50, pls. 71, 72.

TYPE LOCALITY.—Investigator Strait area (35°25′S, 137°22′E), south of Kangaroo Island (35°50′S, 137°15′E), SA.

TYPE.—Holotype: AM E2464, by original designation, male specimen in alcohol, 81 mm ML (Figure 10c). No sepion.

GEOGRAPHICAL DISTRIBUTION.—Great Australian Bight, S.A.

DISCUSSION.—This species is known only from the original description, and the sepion is imperfectly known. Following my reexamination of some of the material housed in the collection of the NMV, I have no doubt that the record of Bell and Plant (1977:118) represents Sepia cultrata.

Sepia irvingi Meyer, 1909

FIGURE 11

DIAGNOSIS.—Mantle acuminate posteriorly; anterior dorsal margin broadly rounded, slightly emarginate ventrally. Tentacular club (Figure 11a) resembles that of Sepia apama; sucker-bearing surface completely surrounded by protective membranes, membranes fused at base. Swimming membranes extended slightly beyond base of tentacular club. Club suckers in 8 series, 2nd and especially 3rd sucker of each row, from dorsal side, larger than others. Arm suckers quadriserial. Male arms without trace of hectocotylization.

FIGURE 10.—Sepia hedleyi Berry, 1918 (from Berry, 1918). a,c, holotype, male, sepion missing (81 mm ML), Investigator Strait, south of Kangaroo Island, SA, AM E2464: a, left tentacular club; c, dorsal view. b, reconstructed sepion, female, AM E4377.

FIGURE 11.—Sepia irvingi Meyer, 1909. a, right club of adult female (167 mm ML), southwest of Shark Bay, WA, NMV F66205 (scale = 30 mm). b,c, sepion of adult female (158 mm ML), NW Shelf, WA, NMV F56768 (scale = 50 mm): b, dorsal view; c, ventral view.

Sepion (Figure 11b,c) slightly acuminate anteriorly, more acuminate posteriorly, widest in anterior art. Dorsal surface slightly convex, with very weak but broad median rib and 2 ill-defined lateral ribs; median dorsal surface curved downward at beginning of striated zone, with strong keels radiating from this point in all directions, those toward spine and those on outer cone well developed. Ventral surface flat, with weak indication of narrow median groove on striated zone. Striae convex, StrZI 55–67. Inner cone completely fused with outer cone. No smooth area between striated zone and outer cone; deep groove with strong, calcareous, sharp-edged keels between base of spine and posterior outer cone. Spine strong, straight, without keels.

ORIGINAL REFERENCE.—Meyer, 1909:333, figs. 7–10.

TYPE LOCALITY.—Cockburn Sound, Garden Island (32°11′S, 115°43′E), Port Royal (King George Sound, 35°03′S, 117°58′E), and Warnbro Sound, WA (32°20′S, 115°43′E).

TYPE.—Syntype: WAM 4203, 1 female specimen in alcohol, 97 mm ML. Sepion missing. See “Discussion.”

GEOGRAPHICAL DISTRIBUTION.—West coast of WA from Cockburn Sound (32°11′S, 115°43′E) to NW Shelf (18°49′S, 118°29′E), at depths of 130–170 m.

DISCUSSION.—In his original description, Meyer (1909) mentioned four female specimens as study material; however, there was no mention of a type specimen. Adam (1979:139) studied one sepion belonging to one of the four specimens in Meyer's material and referred to it as “Type.” Slack-Smith (1983:75) listed the Warnbro Sound specimen (WAM 4203) as a paratype, but no other type specimen of S. irvingi was listed. I examined the same specimen (WAM 4203) and found a label bearing the word “Holotype” in the jar. Because Meyer did not specify any type specimen, I consider all four specimens studied by Meyer to be syntypes.

Sepia latimanus Quoy and Gaimard, 1832

FIGURE 12

Ponderisepia eclogaria Iredale, 1926b:239. [Holotype, AM C19085, 320 mm SL (337 mm including spine), Masthead Island, Capricorn Group, Qld (23°32′S, 151°44′E).]

Sepia rappiana Férussac, 1835:283, in Férussac and Orbigny, 1835–1848. [Type lost, type locality unknown, probably Celebes (2°S, 121°E).]

DIAGNOSIS.—Mantle with anterior dorsal margin acuminate, reaching midlevel of eyes; ventral margin emarginate. Swimming membrane extended slightly beyond tentacular club; protective membranes fused at base of club, completely surrounding sucker-bearing face of club. Tentacular club (Figure 12c) resembles that of S. apama (Figure 1a); club suckers in 5 to 6 series, those in median series larger than other suckers, those in dorsal marginal series smallest, about art size of largest on same row. Arm suckers quadriserial. Mature male without trace of hectocotylization in any arm.

Sepion (Figure 12d,e) elongate-oval. Dorsal surface convex, strongly rugose, showing faint indication of 3 dorsal ribs. Ventral surface with distinct median groove. Striae strongly reversed V-shaped in anterior striated zone; StrZI about 58–83, generally increasing with SL. Inner cone completely fused to outer cone, outer margin forming distinct, flat, shiny zone slightly raised posteriorly. Outer cone continuous behind inner cone as very narrow, chitinous margin. Spine strong, straight, without keels, and with ventral notch at base.

ORIGINAL REFERENCE.—Quoy and Gaimard, 1832:68, pl. 2: fig. 2.

TYPE LOCALITY.—Port Dorey, New Guinea (0°51′S, 134°01′E).

TYPE.—Holotype: MNHNP 1–6–192, by monotypy, animal in alcohol, male, 138 mm ML. Sepion and upper beak removed and not found.

GEOGRAPHICAL DISTRIBUTION.—Indo-West Pacific; Northern Australia from Shark Bay, WA (25°25′S, 113°35′E), to southern Great Barrier Reef (about 23°S), Qld.

DISCUSSION.—Sepia rappiana was reported to have been collected by Peron and Lesueur from Kangaroo Island, SA (35°50′S, 138°03′E) (Rochebrune, 1884); however, the accuracy of this locality record is doubtful. Sepia latimanus is an Indo-West Pacific species and does not occur in southern Australia.

Although sepions of this species are commonly found on the beaches of northern Great Barrier Reef islands, such as Lizard Island (14°40′S, 145°28′E), there are no specimens with soft parts from Australian waters in the collection of any Australian museum.

Sepia mestus Gray, 1849

FIGURE 13

Solitosepia liliana Iredale, 1926a:188. [Holotype, AM C133300, 110.4 mm SL (116 mm including spine), Manly Beach, NSW (33°48′S, 151°17′E).]

Ascarosepion verreauxi Rochebrune, 1884:98. [Syntypes, MNHNP 1–6–175, 130 mm ML, MNHNP 1–6–176, sepion, 131 mm SL (139 mm including spine), Sydney, NSW (33°53′S, 151°13′E).]

DIAGNOSIS.—Mantle broadly oval; anterior dorsal margin broadly rounded, projecting to level of anterior borders of eyes; ventral margin shallowly emarginate. Swimming membrane of tentacular club (Figure 13a) about 1art times club length. Protective membranes fused at base of club, completely surrounding sucker-bearing face of club. Club suckers in 6 longitudinal series, those in median series slightly larger than other suckers on same row. Arm suckers quadriserial. Mature male without trace of hectocotylization in any arm.

Sepion (Figure 13b,c) oval, broadest in posterior art, anterior end slightly acuminate. Dorsal surface convex, with indistinct median rib. Ventral surface flat with narrow, shallow median groove in striated zone. Striae convex, very close together; StrZI about 60–70. Posterior art of limbs of inner cone very large, completely fused to outer cone. Spine strong, ventrally keeled, directed upward.

ORIGINAL REFERENCE.—Gray, 1849:108.

TYPE LOCALITY.—Australia.

TYPES.—Syntypes: Sepions only, BMNH 1842.11.9.84, 67 mm SL (71 mm including spine), BMNH 1842.11.11.13, smaller specimen, anterior end missing.

FIGURE 12.—a,b, Ponderisepia eclogaria Iredale, 1926, holotype, sepion only (320 mm SL), Masthead Island, Capricorn Group, Qld, AM C19085 (scale = 150 mm): a, dorsal view; b, ventral view. Sepia latimanus Quoy and Gaimard, 1832. c, tentacular club (from Roper et al., 1984). d,e sepion, Lizard Island, Qld (183 mm SL), NMV F69202 (scale = 100 mm): d, dorsal view; e, ventral view.

GEOGRAPHICAL DISTRIBUTION.—Sepions found in eastern Australia from northern Qld (Lizard Island, 14°40′S, 145°28′E) to southern NSW (Twofold Bay, Eden, 37°05′S, 149°54′E). Animals collected only from Sydney region, from rock pools to 146 m deep.

DISCUSSION.—Sepia mestus of Iredale, 1926, is not the same species as S. mestus Gray, 1849. Dong (1988) does not list this species in his Fauna Sinica. Adam and Rees (1966:45) reported the only non-Australian record of this species, a female specimen from northern China (BMNH 1863.5.1.6); however, they questioned the accuracy of the locality, and I concur with their opinion.

Khromov (1987b) reported five specimens under this species name from three localities in Vietnam. The figures provided bear some resemblance to the specimens from Australia, but the striae are much less arched. Further studies are required to decide if the specimens from Vietnam are conspecific with the Australian specimens. At present, I consider S. mestus to be an Australian species.

FIGURE 13.—a, Sepia mestus Gray, 1849, left club of subadult female (68 mm ML), Bottle and Glass Cove, Port Jackson, NSW, NMV F56769 (scale = 10 mm). b,c, Solitosepia liliana Iredale, 1926, holotype, sepion only (110.4 mm SL), Manly Beach, NSW, AM C133300 (scale = 50 mm): b, dorsal view; c, ventral view.

Sepia mira (Cotton, 1932)

FIGURE 14

Tenuisepia mira Cotton, 1932:546. [Holotype, SAM D10507, 53 mm SL (55 mm including spine), North-West Islet, Qld (23°18′S, 151°42′E).]

DIAGNOSIS.—Sepion elongate, sharply rounded at anterior end, widest in anterior art, slightly tapered posteriorly, broadly round at posterior end of outer cone. Dorsal surface cream, without ribs or furrows, smooth except for finely pustulose area near posterior end, chitinous margin narrow. Ventral surface convex, with very long striated zone without median groove; StrZI about 70. Striae slightly arched, almost straight. Inner cone narrow, with long limbs occupying about 50% of SL. Outer cone narrow anteriorly, widened posteriorly. Spine straight, rounded, without keels.

ORIGINAL REFERENCE.—Cotton, 1932:546.

TYPE LOCALITY.—North-West Islet, Capricorn Group, Qld (23°18′S, 151°42′E).

TYPE.—Holotype: SAM D10507, by original designation, sepion only, 53 mm SL (55 mm including spine) (Figure 14).

GEOGRAPHICAL DISTRIBUTION.—Lizard Island (14°40′S, 145°28′E) and North-West Islet (23°18′S, 151°42′E), Qld, and Trial Bay, NSW (30°53′S, 153°04′E).

DISCUSSION.—This species is known only from sepions. Soft parts of the animal are unknown.

FIGURE 14.—Tenuisepia mira Cotton, 1932, holotype, sepion only (53 mm SL), North-West Islet, Capricorn Group, Qld, SAM D10507 (scale = 20 mm): a, dorsal view; b, ventral view.

Sepia novaehollandiae Hoyle, 1909

FIGURE 15

Mesembrisepia macandrewi Iredale, 1926a:191. [Holotype. AMC133328, 159 mm SL (168 mm including spine), Shell Harbour, NSW (34°35′S, 150°52′E).]

Mesembrisepia ostanes Iredale, 1954:69. [Holotype, AM C133311, 132 mm SL (139 mm including spine), Stanley, Tas (40°46′S, 145°17′E).]

DIAGNOSIS.—Mantle with anterior dorsal margin rounded, projecting to midlevel of eyes; ventral margin emarginate. Tentacular club (Figure 15a) short, distinct swimming membrane extended slightly beyond base of club. Protective membranes well developed, separated at base in young specimens, usually united in larger ones, but character variable. Tentacular club suckers in 8 series, suckers of 2nd and 3rd series from dorsal side distinctly larger than other suckers. Largest tentacular suckers only slightly larger than arm suckers. Arm suckers quadriserial throughout. Left arm IV of male with minute transformation that might be interpreted as hectocotylization, with suckers of 7th and 10th transverse rows smaller than others.

FIGURE 15.—a, Sepia novaehollandiae Hoyle, 1909, left club of adult male (144 mm ML), 39°07.6′S, 143°25.0′E, NMV F56914 (scale = 20 mm). b,c, Mesembrisepia macandrewi Iredale, 1926, holotype, sepion only (159 mm SL), Shell Harbour, NSW, AM C133328 (scale = 100 mm): b, dorsal view; c, ventral view. d,e, Mesembrisepia ostanes Iredale, 1954, holotype, sepion only (132 mm SL), Stanley, NW Tas, AM C133311 (scale = 100 mm): d, dorsal view; e, ventral view.

Sepion (Figure 15b–e) elongate-oval, acuminate toward both ends, widest anterior of middle. Dorsal surface granulose, with median rib and 2 less-defined lateral ribs separated from median rib by flat portions. Ventral surface with median sulcus; sulcus wide and deep along striated zone, slight depression on last loculus, flanked by 2 rounded ribs, longitudinal depression along outer side of each rib. Posterior end of last loculus thick. Striated area long, StrZI 62–78; striae broadly V-shaped, with wavy limbs joining at midgroove. Inner cone completely fused to outer cone. Outer cone expanded posteriorly. Spine strong, without keels, straight or slightly turned upward. Base of spine swollen on dorsal and lateral sides, with deep, radially striated groove on ventral side and in large specimens separated from dorsal surface of sepion by another groove.

ORIGINAL REFERENCE.—Hoyle, 1909:266.

TYPE LOCALITY.—Kangaroo Island, SA (35°50′S, 138°03′E).

TYPE.—Syntype: MNHNP 1-6-194, only 1 damaged sepion extant, 77 mm SL (incomplete).

GEOGRAPHICAL DISTRIBUTION.—Southern Australia from Shell Harbour, NSW (34°35′S, 150°52′E), to NW Shelf (18°57′S, 118°45′E), WA, at depths of 15–348 m.

DISCUSSION.—The species collected by Peron from Kangaroo Island, SA, was given the name Sepia australis by Férussac in 1835, a name previously given to a South African species by Quoy and Gaimard (1832). In 1909, Hoyle renamed the Kangaroo Island species Sepia novaehollandiae. The damaged sepion collected by Peron was recently found in the collection of MNHNP (Lu et al., 1995).

Sepia opipara (Iredale, 1926)

FIGURE 16

Glyptosepia opipara Iredale, 1926a:191. [Holotype, AM C133330, 106.7 mm SL (116.5 mm including spine), Masthead Island, Capricorn Group, Qld (23°32′S, 151°44′E).]

DIAGNOSIS.—Anterior dorsal mantle margin projecting to midlevel of eyes; ventral margin slightly emarginate. Tentacular club (Figure 16a) short, swimming membrane extended beyond base of club. Protective membranes well developed, not fused at base of club. Median club with suckers in 8 series, 4 to 5 large suckers, 2nd proximal sucker largest; obliquely, 1 small lateral sucker and 1 minute marginal sucker dorsal to largest sucker, 1 small lateral sucker and 4 minute marginal suckers ventral to it. Suckers proximal and distal to large suckers small. Arm suckers quadriserial. Left arm IV of male hectocotylized with basal 5 or 6 rows of suckers normal, followed distally by 6 or 7 rows of suckers reduced in size, remaining distal suckers normal. Suckers in each row arranged in 2 pairs of widely spaced suckers, ventral suckers smaller.

Sepion (Figure 16b–e) elongate-oval, twice as long as broad. Dorsal surface coarsely pustulose, flat with distinctly raised, rounded median rib, lateral ribs distinct. Ventral surface with shallow, narrow median groove. Anterior swelling (last loculus) pronounced. Striated zone long, StrZI 73, in figured specimen (Figure 16e) striae slightly arched. Inner cone with narrow limbs, fused with outer cone. Outer cone enlarged posteriorly, forming 2 poorly developed, calcareous wings united by chitinous membrane between spine and inner cone. Spine long, ventrally keeled.

ORIGINAL REFERENCE.—Iredale, 1926a:191, pl. 22: figs. 7, 8.

TYPE LOCALITY.—Masthead Island, Capricorn Group, Qld (23°32′S, 151°44′E).

TYPE.—Holotype: AM C133330, by original designation, sepion only, 106.7 mm SL (116.5 mm including spine) (Figure 16b,c).

GEOGRAPHICAL DISTRIBUTION.—Northern Australia from Dirk Hartog Island, WA (25°45′S, 113°03′E), to southern Qld (36°57′S, 151°45′E), at depths of 83–184 m.

DISCUSSION.—In his synopsis of sepiid collections in the Western Australian Museum, Adam (1979) erroneously described the animal of this species under the name Sepia rex. Examinations of the types of both species and examination of new material in NMV leave no doubt that they are different species; tentacular clubs and sepions of both species bear no resemblance to each other (cf. Figure 22). The club suckers of S. opipara are in eight series and have four or five very large suckers in the middle of the tentacular club, whereas the club suckers of S. rex are minute, subequal in size, and in 10–12 series. The dorsal surface of the sepion in S. opipara is flat with prominent borders slanting ventrolaterally and with a prominent, rounded median rib running the entire length of the flat surface. The dorsal surface of the sepion in S. rex is not flat, the median rib is indistinctly raised, and the ventrolateral borders are not distinct. The species was originally described as Glyptosepia opipara and as the type species of Iredale's genus Glyptosepia.

Sepia papuensis Hoyle, 1885

FIGURES 17, 18

?Sepia galei Meyer, 1909:332. [Type not traced.]

Solitosepia submestus Iredale, 1926b:238. [Holotype, AM C133325, 67.7 mm SL (70.2 mm including spine), Masthead Island, Capricorn Group, Qld (23°32′S, 151°44′E).]

Solitosepia occidua Cotton, 1929:88. [Holotype, SAM D13627, 45 mm SL (48 mm including spine), Rottnest Island, WA (32°00′S, 115°30′E).]

Solitosepia genista Iredale, 1954:66. [Holotype, AM C133309, 62 mm SL (64.8 mm including spine), Broome, WA (17°31.5′S, 121°27′E).]

Solitosepia lana Iredale, 1954:66. [Holotype, AM C133301, 94.5 mm SL (98.7 mm including spine), Low Isles, Qld (16°23′S, 145°34′E).]

DIAGNOSIS.—Anterior dorsal mantle margin acuminate; ventral mantle margin emarginate. Swimming membrane of tentacular club (Figure 17a) broad, extended art club length beyond club base. Protective membranes narrow, fused at base in adults, separate in young specimens. Club suckers in 5 longitudinal series, suckers in median series largest, followed in size by suckers in ventromedian series. Arm suckers quadriserial except suckers biserial, small, on attenuated distal parts of male arms I–III. Left arm IV of male shows no trace of hectocotylization. Swimming membranes of arms I–III with series of semicircular lappets. Small papillae covering dorsal and ventral surfaces of mantle and dorsal and lateral surfaces of head and arms, lacking on ventral surface of head and arms IV.

Sepion (Figures 17b–g, 18) oval, widest anterior of middle, anterior end bluntly rounded, posterior end acuminately rounded. Dorsal surface with 3 longitudinal ribs separated by 2 grooves, chitinous margins broad. Ventral surface with distinct median groove. Striated zone narrow, long, StrZI 57–73 (fide Adam, 1979); striae broadly arched. Limbs of inner cone fused to outer cone, forming chitinous ledge surrounding posterior excavation. Spine straight, with ventral keel.

FIGURE 16.—Sepia opipara (Iredale, 1926). a, left club of male adult specimen (150 mm ML), east of Moolooabah, Qld, NMV F30983 (scale = 20 mm). b,c, holotype, sepion only (106.7 mm SL), Masthead Island, Capricorn Group, Qld, AM C133330 (scale = 40 mm): b, dorsal view; c, ventral view. d,e, sepion of adult female (133 mm ML, 128 mm SL), east of Moolooabah, Qld, NMV F30983 (scale = 40 mm): d, dorsal view; e, ventral view.

FIGURE 17.—a, Sepia papuensis Hoyle, 1885, left club of subadult male (80 mm ML), off Townsville, Qld, NMV F56945 (scale = 10 mm). b,c, Solitosepia submestus Iredale, 1926, holotype, sepion only (67.7 mm SL), Masthead Island, Capricorn Group, Qld, AM C133325 (scale = 30 mm): b, dorsal view; c, ventral view. d,e, Solitosepia occidua Cotton, 1929, holotype, sepion only (45 mm SL), Rottnest Island, WA, SAM D13627 (scale = 30 mm): d, dorsal view; e, ventral view. f,g, Solitosepia genista Iredale, 1954, holotype, sepion only (62 mm SL), Broome, WA, AM C133309 (scale = 30 mm): f, dorsal view; g, ventral view.

FIGURE 18.—Solitosepia lana Iredale, 1954, holotype, sepion only (94.5 mm SL), Low Isles, Qld, AM C133301 (scale = 30 mm): a, dorsal view; b, ventral view.

ORIGINAL REFERENCE.—Hoyle, 1885:197.

TYPE LOCALITY.—H.M.S. Challenger sta 188 (9°59′S, 139°42′E), Arafura Sea, South of Papua, 28 fathoms (51.2 m).

TYPE.—Syntype: BMNH 1889.4.24.68, 1 male, 64 mm ML, 63 mm SL, animal in alcohol (fide Adam and Rees, 1966). Not examined.

GEOGRAPHICAL DISTRIBUTION.—Indo-West Pacific; Northern Australia from southern WA (Freemantle, 32°03′S, 115°44′E) to southern NSW (36°35′S, 150°16′E), including Gulf of Carpentaria, at depths of 17–155 m.

DISCUSSION.—Adam (1979) listed Sepion galei (type not traced), Solitosepia submestus, Solitosepia occidua, Solitosepia genista, and Solitosepia lana as synonyms of Sepia papuensis. Examinations of available type specimens confirm this opinion except for S. galei, the status of which remains to be verified.

Sepia pharaonis Ehrenberg, 1831

FIGURE 19

Crumenasepia hulliana Iredale, 1926b:239. [Holotype, AM C133333, 173 mm SL (180.4 mm including spine), Howick Island, Qld (14°30′S, 144°59′E).]

Crumenasepia ursulae Cotton, 1929:90. [Holotype, SAM D10013, 247 mm SL, spine broken off, Cottesloe, WA (31°59′S, 115°45′E).]

DIAGNOSIS.—Anterior dorsal mantle margin acuminate, projected to level of anterior border of eyes; ventral mantle margin emarginate. Swimming membrane of tentacular club (Figure 19a) narrow, extended slightly beyond base of club. Protective membranes narrow, separated at base of club. Club suckers small, in 8 series at middle of club, 3rd and 4th suckers from dorsal margin much larger than other suckers in row. Arm suckers quadriserial. Left arm IV in male hectocotylized, basal 12 rows of suckers normal, followed by 10 rows of suckers in which dorsal parts minute, separated from normal-sized ventral pairs by fleshy ridge.

Sepion (Figure 19b–e) elongate-oval. Dorsal surface granulose, with 3 longitudinal ribs. Ventral surface with shallow groove in middle of striated zone, last loculus faintly grooved. Striated zone bordered on both sides by narrow, smooth area. Posterior inner-cone limbs forming long, ventral ledge, convex posteriorly, flat or slightly concave anteriorly. Spine without keels, with 2 thick, lateral expansions at base.

ORIGINAL REFERENCE.—Ehrenberg, 1831, pl. 8.

TYPE LOCALITY.—Massaouah, Gulf of Suez.

TYPE.—Not traced.

GEOGRAPHICAL DISTRIBUTION.—Indo-West Pacific. In northern Australia, sepions recorded from Cap Le Grande, WA (33°55′S, 122°30′E), to Masthead Island, Capricorn Group, Qld (23°32′S, 151°44′E), animals recorded from Monte Bellow Island, WA (20°26′S, 115°37′E), to at least Townsville, Qld (19°16′S, 146°41′E), including Gulf of Carpentaria, at depths of 25–102 m.

DISCUSSION.—Adam (1979) listed Crumenasepia hulliana and Crumenasepia ursulae as synonyms of Sepia pharaonis. Examinations of both type specimens confirm this opinion. This species is widely distributed throughout the Indo-West Pacific region, hence it carries many junior synonyms. For details of these non-Australian synonyms see Adam and Rees (1966) and Adam (1979). Records from the western Great Australian Bight given by Zeidler and Smith (1989) represent sepions cast ashore only.

Sepia plangon Gray, 1849

FIGURE 20

Solitosepia plangon adhaesa Iredale, 1926b:238. [Holotype, AM C133304, 82.7 mm SL (88.3 mm including spine), North-West Islet, Qld (23°18′S, 151°42′E).]

DIAGNOSIS.—Mantle elongate-oval; anterior dorsal margin projected, reaching midlevel of eyes; ventral margin slightly emarginate. Swimming membrane of tentacular club (Figure 20a) extended art of club length beyond club base. Protective membranes fused at club base. Club suckers in 5 longitudinal series, those in median series largest, followed in size by immediately bordering ventral series. Arm suckers quadriserial. Left arm IV of male hectocotylized, suckers on proximal 5 transverse rows normal, followed by 5 rows of slightly smaller suckers, remaining suckers normal.

Sepion (Figure 20b,c) elongate, acuminate anteriorly, rounded posteriorly. Dorsal surface granulose, with 2 broad, chitinous marginal bands, median portion with 3 longitudinal ribs. Ventral surface with deep median groove along length of striated zone and last loculus; median groove flanked by 2 lateral ribs giving striae wavy appearance; striae projected acutely anteriorly in midline. Striated zone separated from outer cone by 2 concave, transversely striated, lateral zones. Posterior portion of inner cone broadened, flattened, and nearly completely fused with outer cone except posterior margin slightly raised into ledge. Outer cone widened posteriorly, surrounding inner cone. Spine with ventral keel.

FIGURE 19.—a, Sepia pharaonis Ehrenberg, 1831, left club of adult male (178 mm ML), NW Shelf, WA, 19°44′S, 116°25′E, NMV F57526 (scale = 30 mm). b,c, Crumenasepia hulliana Iredale, 1926, holotype, sepion only (173 mm SL), Howick Island, north Qld, AM C133333 (scale = 100 mm): b, dorsal view; c, ventral view. d,e, Crumenasepia ursulae Cotton, 1929, holotype, sepion only (247 mm SL), Cottesloe, WA, SAM D10013 (scale = 100 mm): d, dorsal view; e, ventral view.

FIGURE 20.—a, Sepia plangon Gray, 1849, left club of subadult female (98 mm ML), 27°42′S, 153°35′E, NMV F57273 (scale = 5 mm). b,c, Solitosepia plangon adhaesa Iredale, 1926, holotype, sepion only (82.7 mm SL), North-West Islet, Qld, AM C133304 (scale = 30 mm): b, dorsal view; c, ventral view.

ORIGINAL REFERENCE.—Gray, 1849:104.

TYPE LOCALITY.—Port Jackson, Australia (33°51′S, 151°16′E).

TYPES.—Syntypes: BMNH 1963.I.26.W, 1 animal without sepion; BMNH 1842.II.9.85, 1 broken sepion (fide Adam and Rees, 1966). Not examined.

GEOGRAPHICAL DISTRIBUTION.—Eastern Australia from Gulf of Carpentaria, along Qld, to Sydney, NSW (33°53′S, 151°13′E); intertidal zone to 83 m.

Sepia reesi Adam, 1979

FIGURE 21

DIAGNOSIS.—Sepion (Figure 21) elongate, acuminate anteriorly, broadly rounded posteriorly. Dorsal surface salmon colored, with distinct median rib, surface smooth anteriorly, weakly granulose on remaining part. Ventral surface with narrow median groove along entire striated zone and on greater part of last loculus. Striated zone long, StrZI 71–78 (fide Adam, 1979); striae nearly straight, transverse in posterior portion, becoming more reversed V-shaped anteriorly. Inner cone with long, narrow, rounded limbs, bluntly rounded posteriorly surrounding shallow depression, limbs disappearing gradually toward middle of striated zone. Outer cone narrow, slightly enlarged posteriorly as 2 small lateral wings; posterior outer cone continuous between spine and inner cone. Spine rounded, turned upward but not curved.

ORIGINAL REFERENCE.—Adam, 1979:200, pl. 4: fig. 3.

TYPE LOCALITY.—Salmon Bay, Rottnest Island, WA (32°00′S, 115°30′E).

TYPE.—Holotype: WAM 497-76, by original designation, sepion only, 45.2 mm SL.

GEOGRAPHICAL DISTRIBUTION.—Known only from the type locality of Salmon Bay, Rottnest Island, WA.

DISCUSSION.—The soft parts of this species are unknown.

Sepia rex (Iredale, 1926)

FIGURE 22

Decorisepia rex Iredale, 1926a:193. [Holotype, AM C127593, 107 mm SL (113.3 mm including spine), Manly Beach, Sydney, NSW (33°48′S, 151°17′E).]

Decorisepia cottesloensis Cotton, 1929:90. [Holotype, SAM D13681, 40 mm SL (43 mm including spine), Cottesloe, WA.]

Decorisepia jaenschi Cotton, 1931:41. [Holotype, SAM D10163, 97 mm SL (101 mm including spine), Robe, SA (37°10′S, 139°45′E).]

FIGURE 21.—Sepia reesi Adam, 1979. a,b, holotype, sepion only (45.2 mm SL), Salmon Bay, Rottnest Island, WA, WAM 497-76 (scale = 30 mm): a, dorsal view; b, ventral view. c,d, paratype, incomplete sepion only, Salmon Bay, Rottnest Island, WA, WAM 498-76 (scale = 30 mm): c, dorsal view; d, ventral view.

DIAGNOSIS.—Anterior dorsal mantle margin acutely projected, reaching midlevel of eyes; ventral margin slightly emarginate. Swimming membrane of tentacular club (Figure 22a) extended slightly beyond base of club. Protective membranes separate at base of club. Club suckers minute, subequal in size, in approximately 10–12 longitudinal series at middle of club. Arm suckers quadriserial. Left arm IV of male hectocotylized, suckers on basal and distal images of arm normal, quadriserial, those in middle images greatly reduced in size, suckers sparse and widely spaced, giving appearance of being only 2 to 3 series.

Sepion (Figure 22b–g) elongate-oval, narrow anteriorly, width 50% of length. Dorsal surface pustulose, with 3 ribs, median rib rounded, prominent, lateral ribs rounded, divergent, less distinct; most of outer cone occupied by large, chitinous margin around sepion. Ventral surface slightly swollen anteriorly, with shallow median groove along entire length of sepion. Striated zone long, StrZI over 70; striae rounded. Inner cone V-shaped, long limbs narrow, raised, prominent. Spine pointed slightly upward, round, without keel.

ORIGINAL REFERENCE.—Iredale, 1926a:193, pl. 22: figs. 9, 10.

TYPE LOCALITY.—Manly Beach, NSW (33°48′S, 151°17′E).

TYPE.—Holotype: AM C127593, by original designation, sepion only, 107 mm SL (Figure 22b,c).

GEOGRAPHICAL DISTRIBUTION.—Southern Australia from southern Qld (22°35′S, 153°46′E) to the Great Australian Bight (33°17′S, 127°44′E), including Tas (southernmost record 43°38′S, 147°49′E), at depths of 55–400 m.

DISCUSSION.—Adam (1979:178) listed Decorisepia cottlesloensis and Decorisepia jaenschi as synonyms of Sepia rex. Examinations of all type specimens and new materials confirm that these two species are conspecific with Sepia rex (Iredale, 1926). The animal described by Adam (1979:178) as S. rex is a distinct species, S. opipara.

Sepia rozella (Iredale, 1926)

FIGURE 23

Solitosepia rozella Iredale, 1926a:190. [Holotype, AM C133336, 132 mm SL (141 mm including spine), Manly Beach, NSW (33°48′S, 151°17′E).]

Solitosepia rozella peregrina Iredale, 1926b:238. [Holotype, AM C133322, 81.3 mm SL (88.3 mm including spine), North-West Islet, Qld (23°18′S, 151°42′E)].

DIAGNOSIS.—Anterior dorsal mantle margin strongly acuminate, projected forward to level of anterior borders of eye; ventral margin emarginate. Swimming membrane of tentacular club (Figure 23a) well developed, extended beyond base of club. Protective membranes wide, fused at base of club. Club suckers in 8 longitudinal series, suckers in 3rd series from dorsal margin larger than those in same transverse row. Arm suckers quadriserial. Left arm IV of mature male slightly modified, basal images of arm slightly thicker and oral surface of arm wider than corresponding portion of right arm IV.

FIGURE 22.—a, Sepia rex (Iredale, 1926), left club of subadult female (92 mm ML), 37°50′S, 139°46′E, NMV F57293 (scale = 10 mm). b,c, Decorisepia rex Iredale, 1926, holotype, sepion only (107 mm SL), Manly Beach, NSW, AM C127593 (scale = 40 mm): b, dorsal view; c, ventral view. d,e, Decorisepia cottesloensis Cotton, 1929, holotype, sepion only (40 mm SL), Cottesloe, WA, SAM D13681 (scale = 20 mm): d, dorsal view; e, ventral view. f,g, Decorisepia jaenschi Cotton, 1931, holotype, sepion only (97 mm SL), Robe, SA, SAM D10163 (scale = 20 mm): f, dorsal view; g, ventral view.

FIGURE 23.—a–c, Sepia rozella (Iredale, 1926). a, left club of adult male (122 mm ML), 27°45.5′S, 153°27′E, NMV F57319 (scale = 10 mm). b,c, holotype, sepion only (132 mm SL), Manly Beach, NSW, AM C133336 (scale = 100 mm): b, dorsal view; c, ventral view. d,e, Solitosepia rozella peregrina Iredale, 1926, holotype, sepion only (81.3 mm SL), North-West Islet, Qld, AM C133322 (scale = 40 mm): d, dorsal view; e, ventral view.

Sepion (Figure 23b–e) solid, elongate-oval, broadest in middle, rounded acuminate at both ends. Dorsal surface granulose, with 3 faint longitudinal ribs, marginal areas broad, chitinous, with thin calcareous covering. Ventral surface with deep median groove in striated zone and narrow, shallow median depression on last loculus; deep median groove flanked by 2 strongly convex, rounded ribs. Striae V-shaped anteriorly, slightly arched at posterior end; StrZI approximately 64–71. Inner cone rose colored, with broad limbs, fused with outer cone. Outer cone large, broadened to form wing-like expansion posteriorly, continuous between inner cone and spine. Spine strong, directed upward, with distinct, straight, ventral keel and ventral notch at base.

ORIGINAL REFERENCE.—Iredale, 1926a:190, pl. 21: figs. 6, 7.

TYPE LOCALITY.—Manly Beach, NSW (33°48′S, 151°17′E).

TYPE.—Holotype: AM C133336, by original designation, sepion only, 132 mm SL (141 mm including spine), anterior tip, approximately 4 mm, missing (Figure 23b,c).

GEOGRAPHICAL DISTRIBUTION.—Southeastern Australia from southern Qld (27°42′S, 153°32′E) to NSW (36°45′S, 150°02′E), at depths of 27–183 m. Adam (1979) recorded one sepion fragment from Shark Bay, WA (25°25′S, 113°35′E), tentatively identified as this species.

FIGURE 24.—a, Sepia smithi Hoyle, 1885, left club of subadult female (86 mm ML), 12°53.92′S. 125°35.03′E, NMV F57324 (scale = 20 mm). b,c, Acanthosepion pageorum Iredale, 1954, holotype, sepion only (127 mm SL), Keppel Bay, Qld, AM C133315 (scale = 100 mm): b, dorsal view; c, ventral view.

Sepia smithi Hoyle, 1885

FIGURE 24

Acanthosepion pageorum Iredale, 1954:76. [Holotype, AM C133315, 127 mm SL (133 mm including spine), Keppel Bay, Qld (23°25′S, 150°55′E).]

DIAGNOSIS.—Anterior dorsal mantle margin projected, reaching midlevel of eyes; ventral mantle margin emarginate. Swimming membrane of tentacular club (Figure 24a) extended beyond base of club. Protective membranes not fused at base of club. Club suckers minute, numerous, arranged in about 20 longitudinal series. Arm suckers quadriserial. Left arm IV of male hectocotylized, basal 8 rows of suckers normal, followed by about 8 rows of very small suckers, suckers on distal part of arm normal.

Sepion (Figure 24b,c) oval. Dorsal surface granulose, with 3 distinct longitudinal ribs, posterior outer margins covered with chitinous, glaze-like substance. Ventral surface flat, with broad median groove on striated zone. Striae rounded in posterior portion, more angular in anterior part; StrZI 72–85. Inner cone well developed, with thick posterior ridge surrounding posterior depression; lateral limbs fused with outer cone to form rounded, strong ridge, edge of ridge thickened, rounded. Posterior outer cone wide, continuous behind rim of inner cone. Spine without keels, curved upward.

ORIGINAL REFERENCE.—Hoyle, 1885:190.

TYPE LOCALITY.—H.M.S. Challenger sta 188, 9°59′S, 139°42′E, Arafura Sea, South of Papua, 28 fathoms (51.2 m).

TYPES.—Syntypes: BMNH 1889.4.24.66–67, 2 females in alcohol, 85 mm ML and 57 mm ML (fide Adam and Rees, 1966); not examined. Sepion figured by Hoyle (1886, pl. 16: figs. 10–12); no longer extant (Adam and Rees, 1966:20).

GEOGRAPHICAL DISTRIBUTION.—Northern Australia from Shark Bay, WA (25°25′S, 113°35′E), to Moreton Bay, Qld (27°25′S, 153°20′E), at depths of 33–138 m.

Sepia vercoi Adam, 1979

FIGURE 25

DIAGNOSIS.—Mantle elongate-oval; anterior dorsal mantle margin acutely acuminate, reaching beyond midlevel of eyes; ventral margin slightly emarginate. Tentacular club (Figure 25a) short, swimming membrane wide, thin, extended slightly beyond base of club. Protective membranes separated at base of club. Club suckers in 5 longitudinal series, 5 or 6 suckers in median series twice as wide as neighboring ones. Largest club sucker less than images of wide as largest arm sucker. Arms I effilated, suckers biserial throughout. Arms II and III shorter, stouter, suckers quadriserial. Arms IV shorter than arms I but longer than arms II and III, suckers quadriserial. Left arm IV hectocotylized, 6 rows of large suckers on basal images of arm, suckers on distal images abruptly smaller, widely spaced, closer together near tip of arm.

Sepion (Figure 25b,c) elongate, widest in anterior images, tapering gradually toward posterior end. Dorsal surface flattened, slightly convex, with very low median rib; posterior end covered by smooth, glaze-like material. Ventral surface with narrow, shallow median sulcus along entire length. Striae weakly convex, nearly straight in middle. Limbs of inner cone very narrow, forming rounded, shiny ridges limiting striated zone, vanishing toward middle of sepion; posterior inner cone forming slightly wider ledge, surrounding weak posterior depression. Outer cone forming cup-like widening, separating inner cone from spine. Spine straight, without keels, slightly directed upward. (Based on original description of holotype and paratypes.)

FIGURE 25.—Sepia vercoi Adam, 1979, northeast of Monte Bello Island, WA, WAM 3101-83. a, left club of adult male (53 mm ML) (scale = 5 mm). b,c, sepion of adult male (53 mm ML) (scale = 30 mm): b, dorsal view; c, ventral view.

ORIGINAL REFERENCE.—Adam, 1979:190, pl. 10: figs. 5, 6.

TYPE LOCALITY.—West of Shark Bay, WA (25°31′S, 112°29′E), 130 m.

TYPES.—Holotype: WAM 441-65, by original designation, male specimen in alcohol, 31 mm ML; not examined.

Paratypes: WAM 770-75, N shore of Broke Inlet, WA (34°56′S, 116°27′E), 1 incomplete sepion; WAM 772–75, NW of Carnarvon, WA (24°04′S, 112°59′E), 1 sepion. Not examined.

GEOGRAPHICAL DISTRIBUTION.—Known only from the original description, southwestern Australia from Broke Inlet (34°56′S, 116°27′E), on the south coast, to Carnarvon (24°04′S, 112°59′E), on the west coast.

DISCUSSION.—The animal of this species is known only from the holotype, a mature male specimen. The extent of sexual dimorphism, particularly on the arms, is unknown.

Sepia whitleyana (Iredale, 1926)

FIGURE 26

Acanthosepion whitleyanum Iredale, 1926a:195. [Holotype, AM C133331, 168 mm SL (174 mm including spine), Port Macquarie, NSW (31°27′S, 152°55′E).]

DIAGNOSIS.—Mantle elongate-oval; anterior dorsal margin reaching midlevel of eyes; ventral margin slightly emarginate. Swimming membrane of tentacular club (Figure 26a) same length as club. Protective membranes not fused at base of club. Club suckers subequal in size, minute, in about 20 series. Arm suckers quadriserial. Both arms IV of male hectocotylized. Left arm IV with 7 to 8 rows of normal suckers basally, followed by 5 to 6 rows of minute suckers (reduction of size due to hectocotylization) distally, remaining suckers normal. Right arm IV with 4 to 5 rows of minute suckers distally, remaining suckers normal. Sucker series on modified portions of both arms well separated.

Sepion (Figure 26b,c) elongate-oval, slightly narrowed anteriorly, width 50% of length. Dorsal surface coarsely pustulose, ribs indistinct, with large chitinous margin; posterior portion with thin, horny (chitinous) covering. Ventral surface slightly swollen anteriorly, deeply excavated posteriorly, becoming very thin. Striae strongly arched; StrZI ∼74–86. Inner cone forming shallow ledge near posterior end, with faint glaze laterally, more pronounced posteriorly. Outer cone semichitinous, posterior outer cone flared dorsoposteriorly. Spine long, without keel, curved.

FIGURE 26.—Sepia whitleyana (Iredale, 1926). a, right club of subadult female (82 mm ML), Moreton Bay, Qld, NMV F57337 (scale = 20 mm). b,c, holotype, sepion only (168 mm SL), Port Macquarie, NSW, AM C133331 (scale = 100 mm): b, dorsal view; c, ventral view.

ORIGINAL REFERENCE.—Iredale, 1926a:195, pl. 23: figs. 9, 10.

TYPE LOCALITY.—Port Macquarie, NSW (31°27′S, 152°55′E).

TYPE.—Holotype: AM C133331, by original designation, sepion only, 168 mm SL (174 mm including spine) (Figure 26b, c).

GEOGRAPHICAL DISTRIBUTION.—Eastern Australia from Qld (16°45′S, 145°54′E) to NSW (32°42′S, 152°06′E), at depths of 23–160 m.

DISCUSSION.—Adam (1979) suggested Acanthosepion whitleyanum to be a synonym of Sepia elliptica. Examinations of the type and new material of this species housed in NMV refute this proposition. The club suckers in S. elliptica are in 10–12 series, whereas those of S. whitleyana are in 20 series. The posterior ledge of the sepion of S. elliptica is thin and flat; that in S. whitleyana is thick and slanted dorsally. The ledge is wider in S. elliptica and narrower in S. whitleyana. Sepia whitleyana is closely related to S. smithi, but the two species are distinct, the most prominent difference being in the posterior end of the sepion. The limbs of the inner cone are wider in S. smithi, and the ledge is wide and has a thick, rounded edge. The ledge in S. whitleyana is narrow and is not prominent (cf. Figures 24c, 26c).

Metasepia Hoyle, 1885

DIAGNOSIS.—Posterior gland and pore absent; locking apparatus semicircular, without tubercle on mantle component and without corresponding depression on funnel component.

Sepion rhomboidal in outline, much shorter than mantle, and located in anterior images–images of mantle; inner cone with very short limbs (Khromov et al., 1998).

Metasepia pfefferi (Hoyle, 1885)

FIGURE 27

Sepia (Metasepia) pfefferi Hoyle, 1885:199. [Holotype, BMNH 1890.I.24.II, female, 52 mm ML, in alcohol; not examined.]

Metasepia pfefferi laxior Iredale, 1926b:240. [Syntypes: AM C133326, sepion, 50.5 mm SL, Masthead Island, Qld (23°32′S, 151°43′E); AM C19084, 2 sepions, 26.4 mm SL and 1 incomplete specimen, Masthead Island, Qld (23°32′S, 151°43′E).]

Metasepia pfefferi wanda Iredale, 1954:78. [Holotype, AM C133314, sepion, 30 mm SL, Denham Bay, Shark Bay, WA (25°31′S, 112°29′E).]

DIAGNOSIS.—Mantle broadly oval; anterior dorsal margin slightly angular; ventral margin broadly emarginate. Tentacular club (Figure 27a) short, swimming membrane twice club length. Protective membranes separated at base of club. Club suckers in 5 to 6 longitudinal series, 4 median suckers much larger than others. Arm suckers quadriserial. Left arm IV of male hectocotylized.

FIGURE 27.—a, Metasepia pfefferi (Hoyle, 1885), right club of subadult female (49 mm ML), 11°57.5′S, 141°22′E, NMV F57140 (scale = 5 mm). b,c, Metasepia pfefferi laxior Iredale, 1926, syntype, sepion only (50.5 mm SL), Masthead Island, Capricorn Group, Qld, AM C133326 (scale = 10 mm): b, dorsal view; c, ventral view. d,e, Metasepia pfefferi wanda Iredale, 1954, holotype, sepion only (30 mm SL), Denham Bay, Shark Bay, WA, AM C133314 (scale = 10 mm): d, dorsal view; e, ventral view.

Sepion (Figure 27b–e) rhomboidal diamond-shaped, acuminate at both ends, more so on posterior end, much shorter than mantle. Dorsal surface completely chitinous, without ribs, slightly convex in middle, flatter toward margins. Ventral surface thick in anterior images, with deep median groove in anterior part of striated zone. Striae reversed V-shaped. Last loculus short. Inner cone forming narrow, rounded ridge, ridge diminishing toward posterior end. Outer cone narrow, surrounding inner cone.

ORIGINAL REFERENCE.—Hoyle, 1885:199.

TYPE LOCALITY.—H.M.S. Challenger sta 188, 9°59′S, 139°42′E, South of Papua, Arafura Sea, 28 fathoms (51.2 m).

TYPE.—Holotype: BMNH 1890.I.24.II, by original designation, female specimen in alcohol, 52 mm ML (fide Adam and Rees, 1966); not examined.

GEOGRAPHICAL DISTRIBUTION.—Northern Australia from Mandurah, WA (32°33′S, 115°04′E), to Moreton Bay, southern Qld (27°25′S, 151°43′E), at depths of 3–86 m.

DISCUSSION.—The species was originally described as Sepia (Metasepia) pfefferi by Hoyle in 1885. Iredale (1954) elevated Metasepia from subgeneric to generic rank. Adam and Rees (1966) and Adam (1979) retained Hoyle's original name and considered Metasepia to be a subgenus of the genus Sepia. Recently, Khromov (1987a), after studying the sepion, reelevated the subgenus Metasepia to generic rank. After studying the color pattern and locomotory behaviour of the species, Roper and Hochberg (1988) reached the same conclusion.

Sepiella Gray, 1849

DIAGNOSIS.—Posterior gland and pore present; locking apparatus with triangular tubercle on mantle component and corresponding depression in funnel component.

Sepion elliptical in outline, without posterior spine; outer cone expanded posteriorly, inner cone with very short limbs. (After Khromov et al., 1998).

Sepiella weberi Adam, 1939

FIGURE 28

Sepiella melwardi Iredale, 1954:78. [Holotype, AM C133320, sepion only, 48 mm SL, Condon Bay, Melville Island, NT (11°35′S, 131°10′E).]

DIAGNOSIS.—Mantle elongate; anterior dorsal margin pointed, projecting to midlevel of eye. Gland located at posterior end of mantle between fins. Tentacular club (Figure 28a) with 10–12 series of minute, subequal suckers. Left arm IV of male hectocotylized.

Sepion (Figure 28b,c) narrow, tongue-like, width about 30% of length; posterior end broad, thin, chitinous, without spine.

ORIGINAL REFERENCE.—Adam, 1939:98, pl. 4: figs. 1, 2.

TYPE LOCALITY.—Timor (8°35′S, 126°00′E) and Soemba, eastern Indonesia.

TYPES.—Syntypes: ZMA, 1 female, Soemba, 67 mm ML; ZMA, 1 male, Timor, 60 mm ML. Not examined.

GEOGRAPHICAL DISTRIBUTION.—East Indonesia (Soemba, Timor). NMV collection, Timor Sea (∼12°S, 127°E), northern Australia, near Darwin, NT (12°27′S, 130°50′E), at depths of 1–88 m.

DISCUSSION.—I have examined the holotype specimen of Sepiella melwardi Iredale, 1954, and new material (whole animals in the NMV collection) from the Timor Sea and the Arafura Sea area, and I have no doubt that Sepiella melwardi is a junior synonym of Sepiella weberi.

General Discussion

The taxonomy of Sepiidae in Australian waters has been in confusion since Iredale and Cotton's prolific creation of new names based solely on cuttlebones. The present contribution is an attempt to bring order to this confused state. My detailed study, on which this contribution is based, is not completed; however, the present data indicates that the Australian sepiid fauna is very rich in endemic species.

My study to date records 26 species of sepiids from the Australian Fishing Zone (200 nautical miles from the coast). Of these, Sepia baxteri, S. mira, and S. reesi are known only from the sepions and are considered of uncertain status at present. Of the remaining 23 species, S. hedleyi and S. dannevigi are known only from the soft parts of the animals; the sepion of S. dannevigi is unknown, and that of S. hedleyi is fragmented and is poorly known. The present study indicates that there is strong similarity between the soft parts of these two species as well as those of S. rex. Further work may prove these three taxa conspecific. The remaining 20 species are known from both soft parts and sepions, and all except S. vercoi are known from both sexes. Only the male of S. vercoi is known.

FIGURE 28.—a, Sepiella weberi Adam, 1939, left club of adult female (51 mm ML), 12°39′S, 127°03′E, NMV F65576 (scale = 5 mm). b,c, Sepiella melwardi Iredale, 1954, holotype, sepion only (48 mm SL; posterior end missing), Condon Bay, Melville Island, NT, AM C133320 (scale = 20 mm): b, dorsal view; c, ventral view.

The Australian marine fauna is considered to consist of two distinct latitudinal elements separated by zones of intermixing. Wilson and Gillett (1971) termed these the fauna of the Northern Australian Region, the Southern Australian Region, and the Eastern and Western Overlap zones. The Northern Australian Region is part of the Indo-West Pacific Faunal Region and is characterized by high species diversity, with large numbers of these species having wide distribution in the Indian and Western Pacific oceans. The fauna of the Southern Australian Region is characterized by low diversity and high species endemicity. Overlap zones are long stretches of coast between the Northern and Southern regions where there is a gradual replacement of tropical forms with temperate forms and some local endemism (Wilson and Allen, 1987).

Although our knowledge of the species distribution is far from complete, the Australian cuttlefish fauna generally conforms with the distributional pattern outlined above. Based on the present data, the geographical distribution of Australian sepiids can be summarized as follows. The exact limits of each species do not necessarily conform with the limits of the zone.

1. Northern Australian Region: Sepia cottoni, S. elliptica, S. latimanus, S. opipara, S. papuensis, S. pharaonis, S. smithi, Metasepia pfefferi, Sepiella weberi.

2. Southern Australian Region: Sepia apama, S. braggi, S.chirotrema, S. cultrata, S. dannevigi, S. hedleyi, S. novaehollandiae, S. rex.

3. Eastern Overlap Zone: Sepia mestus, S. plangon (extends to Gulf of Carpentaria), S. rozella, S. whitleyana, S. baxteri, S. mira.

4. Western Overlap Zone: Sepia irvingi, S. vercoi, S. reesi.

Of the nine species listed for the Northern Australian region, Sepia cottoni, S. opipara, S. smithi, and Metasepia pfefferi are known only from Australia at present; the remaining five species are known also to occur elsewhere in the Indo-West Pacific region.

The eight species listed for the Southern Australian Region are known only from Australia. Similarly, none of the nine species listed for the Eastern and Western Overlap zones is known to occur elsewhere.

Thus, of the 23 species (excluding the 3 species known only from sepions), 21 species are considered to be endemic to Australian waters, a figure (91%) supporting the assertion of Adam and Rees (1966) that the Australian fauna is the richest known in endemic species. The figure of endemism remains high even if S. hedleyi and S. dannevigi are excluded from consideration (19 of the 21 species, or 90%).

Literature Cited

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Distribution Patterns of Sepiidae

D.N. Khromov

_________________

D.N. Khromov. All-Union Research Institute of Marine Fisheries and Oceanography (VNIRO). V. Krasnoselskaya 17a, 107140 Moscow, Russia.

ABSTRACT

The family Sepiidae is found primarily in tropical and warm temperate waters of near oceanic islands and shelf and upper slope areas of the Old World. The family comprises widely distributed species as well as local endemics. Within the range of the family, sepiids show very uneven distributions; regions with high diversity (Indo-West Pacific region) alternate with regions characterized by low diversity (East Atlantic region). In spite of limited sampling, the present study of sepiid distribution helps to define some new biogeographic boundaries (e.g., a separate Arabian province).

Sepia (Acanthosepion) diversity is highest in the tropical zone; about one-half of S. (Acanthosepion) species are caught at depths of 25–50 m, with the overall bathymetric distribution being 0–220 m. Sepia sensu stricto is only moderately diverse in the tropics; the species are widely distributed and are relatively eurybathic. Sepia (Rhombosepion) is relatively diversified in the Central East Atlantic and near South Africa and South Australia but is absent from the tropical zone of the Indo-West Pacific; the species occur in deep water (to 400–500 m). Sepia (Anomalosepia) species inhabit waters near South and East Africa, the Gulf of Oman, and the Arabian Sea; they are abundant in the upper water layers but can occur to depths of 400–500 m. Sepia (Doratosepion) reaches the highest species diversity in the Sino-Japanese Province; the species are never as abundant as the above-mentioned groups and are eurybathic. Sepia (Hemisepius) is limited generally to shallow waters of South Africa. Metasepia species occur in shallow waters of the tropical West Pacific and southern Japan. Sepiella species are widely distributed in the tropical zone and are markedly shallow-water animals.

Five main stages can be seen in Recent sepiid colonization. The first stage, in the Paleocene and Eocene, was occasioned by the development of Belosepia and Pseudosepia in the warm waters of the Tethys Sea. The second, in the Paleogene, was related to the extinction of Belosepia and Pseudosepia and the emergence of Sepia (Acanthosepion) and S. (Sepia). The third phase was related to the emergence of S. (Rhombosepion) and a marked acceleration of taxonomic radiation in the Miocene and Lower Pliocene. The fourth stage, in the Pliocene, was preceded by the extinction of the greater part of the Mediterranean (Tethys) fauna. The fifth stage was related to the emergence of S. (Anomalosepia), Metasepia, S. (Hemisepius), S. (Doratosepion), and Sepiella, the secondary colonization of the East Atlantic, and the origination of the Northwest Pacific fauna.

Introduction

Data on distribution are incomplete for the majority of sepiid species. Many descriptions of sepiids are based solely on the characters of the inner shell, the so-called sepion, and generally the distribution of species remains unknown.

Based on recorded distributions of species for which the soft parts of the animal are known, I have compiled a distribution map for the family (Figure 1). Sepiidae are primarily warm-water animals and are found in tropical, subtropical, and warm temperate regions of the Old World, with a small percentage of species occuring in waters of the north temperate region. They occur primarily in waters of the continental shelf and upper slope and around near oceanic islands. See Table 3 for a list of species.

The present northern boundary of the family distribution range in the Atlantic is near Oslo, Norway, where Sepia officinalis occurs (Adam and Rees, 1966). In the Pacific, the northern boundary is from the Gulf of Peter the Great, Russia, where drifted Sepiella japonica occur, to southern Hokkaido, Japan, where S. kobiensis, S. andreana, and S. tokioensis are found. The southern boundary of the range is from the Agulhas Bank, where S. australis, S. hieronis, S. papillota, S. simoniana (Roeleveld, 1972; Adam, 1983), and S. elegans (Filippova and Khromov, 1991) have been recorded, to southern Tasmania, where several Australian species have been observed (Adam, 1979; Watson-Russel, 1981; Lu, 1998). The western limit of sepiids is the eastern Atlantic at Madeira and the Cape Verde Islands (Rees and Maul, 1956); at the eastern boundary, cuttlefishes reach the Marshall Islands (S. bandensis) and Guam and Fiji (S. latimanus) (Voss, 1954; Adam and Rees, 1966; Corner and Moore, 1980).

Sepiid shells drift at the sea surface and are widely dispersed by oceanic currents; thus, they reach many distant islands as well as North America. They have been reported from the beaches of Florida, the West Indies, New Zealand, and Hawaii, as well as in the Baltic Sea (Voss, 1974; Kay, 1979; Lacourt and Huwae, 1981; Nesis, 1985, 1987), all areas outside of the distribution range of the family.

FIGURE 1.—Recent distribution range of Sepiidae. Species numbers, as percentage of total number of species in family (98), represented as follows: broken hatch lines, < 5%; sparse hatch lines, 5%–10%; dense hatch lines, 11%–15%; crossed hatch lines, > 15%.

There are widely distributed species as well as local endemics among the Sepiidae. The distribution ranges of S. latimanus and S. pharaonis, for example, extend from the northeastern Indian Ocean to the West Pacific. In contrast, S. dubia is found only in False Bay near the Cape of Good Hope, South Africa (Adam and Rees, 1966). It seems, however, that the putative endemism of certain sepiid species has been greatly exaggerated due to our poor knowledge of their true distribution. This can be concluded from many modern data. For example, Filippova and Khromov (1991) found many so-called South African endemics near Mozambique and Tanzania (S. confusa, S. incerta, S. acuminata) and even on the Saya-de-Malha Bank (S. vermiculata, S. papillatta). From the waters of St. Brandon Shoals, Filippova and Khromov (unpublished data) made the second known capture of S. plathyconchalis, which was originally described from this bank (Filippova and Khromov, 1991). Four well-known species (S. vermiculata, S. hieronis, S. elegans, S. australis) were recently reported from off Namibia (Sanchez and Moli, 1984), an area where Sepiidae were never before encountered.

Within the range of the family, sepiids show very uneven distributions (Figure 1). Regions with high sepiid diversity alternate with regions characterized by low diversity. In the latter, living conditions may be relatively unfavorable to sepiids; these are the natural hydrological barriers that divide or limit different faunas. The low diversity of Sepiidae at the northern limit, north of Great Britain and in the Sea of Japan, may be explained by the low winter temperatures. The same explanation may hold for Namibian waters, which are influenced by the cold Benguela Current, upwelling, and the oxygen deficiency observed near the bottom. By contrast, the apparently low diversity of sepiids around remote islands of central Indonesia is probably due to our poor knowledge of this region, for there seem to be no major obstacles to penetration of sepiids from Java, Sumatra, and North Australia into central Indonesia. On the other hand, the absence of sepiids around very distant islands is a biological fact. The ecological conditions of very wide, deep-water zones appear to form true obstacles to colonization by sepiids (Adam and Rees, 1966; Roeleveld, 1972).

FIGURE 2.—Schematic presentation of shelf divisions. Solid lines are after Briggs (1974) (based on numerous groups); hatch lines are after Nesis (1985) (based on Recent cephalopod groups); ticks represent author's data (based on Recent Sepiidae).

The decrease in species numbers in the West Pacific from inshore waters to the open sea is obvious. Eighteen species occur off Vietnam, but there are only seven or eight species at the Philippines, one at Guam, and one at the Marshall Islands; there are no sepiid species in Hawaii. This absence was reported by Voss (1974). An analogous situation is observed in the western part of the Indian Ocean. There are 16 species of sepiids near southeast Africa and nine or ten species on the Saya-de-Malha Bank (including new species awaiting descriptions) (Filippova and Khromov, unpublished data), but, according to my data, there is not a single species at the Seychelles or the Chagos Archipelago.

ACKNOWLEDGMENTS

I wish to express my gratitude to Yulia A. Filippova, Vadim N. Semionov, Anita A. Neiman, and Kir N. Nesis, who for many years have helped me in my work and who have critically read the draft of this paper. I am indebted to Sigurd v. Boletzky and Clyde F.E. Roper, who discussed my work. Finally my gratitude goes to the anonymous reviewers of this paper, to Gilbert Voss who intended to be the senior editor of this volume but whose sudden death prevented him from being such, and to Nancy Voss, who fulfilled the role.

Results

FAUNAL REGIONS

It appears that regions of different species diversities are limited by zones of so-called boundary compression (Semionov, 1982), where the boundaries of many species ranges meet. Such zones that show a high boundary gradient are found in many places (Figure 2). Among these zones, those of the Java, Sulu, and Banda seas, the Torres Strait, and the Mozambique Channel may reflect our poor knowledge of the regions, perhaps being the boundaries of regions explored by systematists rather than actual species range boundaries.

TABLE 1.—Characteristics of the main zoogeographical regions and subregions of Sepiidae distribution.

The zones lying on a line connecting Shanghai, Pusan, South Honshu, Taiwan, Philippines, New Guinea, and northern Australia represent the natural distribution limits of the majority of sepiids. The first part of this line (Shangai-Honshu) coincides with a hydrological (thermal) boundary; the second part (Honshu-eastern coast of Australia) coincides with a geological (slope) boundary that confines the penetration of shallow-water sepiids into the open ocean. East of this line endemics are absent, and only a few widely distributed species are present.

I have divided the entire range of Sepiidae into regions, provinces, and subprovinces limited by boundary compression zones. This is done in a descending scale, from the regions that are limited by a high boundary gradient (many boundaries of species ranges meet) to those limited by a low boundary gradient (few boundaries meet). The number of species and endemics is listed for each region as well as the value of the corresponding boundary gradients (Table 1, Figure 2). One can see from Table 1 that there are two regions of high zoogeographic rank defined by high boundary gradients (13–15), high degrees of endemism (55%–93%), and high species numbers (9–91); they correspond to the East Atlantic and the Indo-West Pacific. The zoogeographical boundary separating them is from near Cape Town, South Africa, to Suez, in accordance with the generally accepted biogeographical pattern of marine shelf fauna (Ekman, 1953; Hedgepeth, 1957; Briggs, 1974).

In the Atlantic, which has relatively few species, only three subregions or provinces can be defined. The first province extends from the northern boundary of the family range to an area of 21°N-Cape Verde, the second extends from 21°N–Cape Verde to the Tropic of Capricorn, and the third extends from the Tropic of Capricorn to Cape Town. The second province contains a high number of endemics for the Atlantic and should be viewed as an independent center of speciation, whereas the others are characterized by faunal loss (and mixing with Indo-West Pacific fauna in the case of the third province).

The picture in the Indo-West Pacific is more complex. According to the great number of species (20–27), the degree of endemism (26%–63%), and the boundary gradient (10–13), there are four main provinces with independent centers of speciation: (1) South-East Africa, extending from Cape Town to Zanzibar Island (including Madagascar and the Mascarena Ridge); (2) Arabia, extending from Zanzibar to Sri Lanka (including the Red Sea and the Persian Gulf); (3) Indo-Malaysia, extending from Sri Lanka to the Gulf of Tonkin (including Australia and Indonesia), and (4) Sino-Japan, extending from the Gulf of Tonkin to southern Korea and Honshu. These four provinces are further subdivided into subprovinces as shown in Table 1.

In addition to the provinces with assumed independent centers, there are others (Northern Japan and Polynesia) that have no endemic species and thus are defined as zones of faunal loss in the Indo-West Pacific, as indicated above.

Boundaries between the provinces in the East Atlantic can not always be clearly defined because of the rather inadequate material; however, two of them (Cape Verde area and South Angola) coincide with the boundaries of other zoogeographic systems described by Briggs (1974) and Nesis (1985).

Sepiid diversity is rather high in the Indo-West Pacific, and the distribution patterns reflect known biogeographical boundaries, which have been determined quite well from distributions of other groups (Figure 2). Moreover, the study of sepiid distribution helps in defining some new boundaries in spite of limited samples. The faunas of the South-East African and Arabian provinces differ greatly, according to the data. Of the 31 species inhabiting these two provinces, only eight are found in both provinces. Each province contains many endemics; this fact suggests the presence of independent speciation centers. Thus, we can distinguish the northern part of the West Indian Ocean, which was poorly defined by Briggs (1974), or that part of the East African province described by Nesis (1985), as a separate Arabian Province. The southern boundary of this province should follow the line from Zanzibar to Saya-de-Malha Bank. The presence of a faunistic boundary at this location is supported by data from crabs and cowries (Schilder, 1956; Forest and Guinot, 1961).

The above data also support Filippova and Khromov's (1991) biogeographical boundaries in the Mozambique Channel and the separation of the Madagascar-Mascarene fauna, but this separation is not as distinct as in the foregoing case.

FAUNAL COMPOSITION AND DIVERSITY

It is important to appreciate the faunal composition in the above-mentioned regions and their subdivisions, and the distribution of different genera and subgenera (Figures 3–9). Describing such a distribution, I use the following terms: narrowly tropical species = species known from the equatorial and/or tropical zones; widely tropical = species known from equatorial, tropical, subtropical, and sometimes part of the temperate zones; subtropical = known only from the subtropical or subtropical plus boreal zones.

In Sepia (Acanthosepion), diversity is highest in the tropical zone, in the Indo-Malaysian and Arabian provinces (Figure 3). There are clearly fewer species of S. (Acanthosepion) in the waters of northern Australia and southern Japan, and they are absent from the Atlantic and the periphery of the family range near South Africa, southern Australia, and northern Japan. There are no subtropical species in S. (Acanthosepion) and only a few widely tropical species. The great majority of the species are narrowly tropical (Table 2).

The range of Sepia (Sepia) covers nearly the entire family range (Figure 4). In contrast to S. (Acanthosepion), its diversity is not very high in the tropics. The number of species is highest near southeast Africa and southern Australia. There are nearly equal numbers of subtropical, widely tropical, and narrowly tropical species in S. (Sepia (Sepia) (Table 2).

TABLE 2.—Zoogeographical characteristics of genera and subgenera of the family Sepiidae.

FIGURE 3.—Recent distribution ranges of Sepiidae: Sepia (Acanthosepion), total species = 11. (Species numbers, as percentage of total number of species of each subgenus, represented as follows: broken hatch lines, < 10%; sparse hatch lines, 11%–20%; dense hatch lines, 21%–30%; crossed hatch lines, > 30%.)

FIGURE 4.—Recent distribution ranges of Sepiidae: Sepia (Sepia), total species = 24. (See Figure 3 for explanation of hatching.)

Sepia (Rhombosepion) is relatively diversified in the central East Atlantic, near South Africa, and, especially, southern Australia (Figure 5). It is completely absent from the tropical zone of the Indo-West Pacific. The majority of S. (Rhombosepion) species are widely tropical (Table 2).

Sepia (Anomalosepia) species inhabit waters near South and East Africa, the Gulf of Oman-Arabian Sea, and the waters between northern Australia and Irian Jaya, Indonesia; they are not found in any other area (Figure 6). Two of the three species of this group are narrowly tropical, the other (S. australis) is widely tropical (Table 2).

According to available data, Sepia (Doratosepion) reaches the highest species diversity in the Sino-Japanese province (Figure 7). If species described solely on the basis of sepion characters are included, it can be concluded that S. (Doratosepion) species diversity is the same on Australian coasts (but see Lu, 1998). Many species of this subgenus are found near southeast Africa and Arabia, fewer are found in the Indo-Malaysian province, and none are found in the Atlantic. The majority of S. (Doratosepion) species are subtropical and narrowly tropical (Table 2).

Sepia (Hemisepius) is limited to the waters of South Africa (Figure 8). The majority of the species are subtropical; S. typica is a tropical species (Khromov et al., 1991) (Table 2).

Metasepia occurs in the tropical West Pacific and in southern Japan (Figure 8). Both species of Metasepia should be considered widely tropical (Table 2).

FIGURE 5.—Recent distribution ranges of Sepiidae: Sepia (Rhombesepion), total species = 11. (Species numbers, as percentage of total number of species of each subgenus, represented as follows: broken hatch lines, < 10%; sparse hatch lines, 11%–20%; dense hatch lines, 21%–30%; crossed hatch lines, > 30%.)

FIGURE 6.—Recent distribution ranges of Sepiidae: Sepia (Anomalosepia), total species = 3. (Species numbers, as percentage of total number of species of each subgenus, represented as follows: broken hatch lines, < 10%; sparse hatch lines, 11%–20%; dense hatch lines, 21%–30%; crossed hatch lines, > 30%.)

FIGURE 7.—Recent distribution ranges of Sepiidae: Sepia (Doratosepion), total species = 33. (See Figure 6 for explanation of hatching.)

Sepiella is recorded from the tropical zones of all the oceans, but species diversity is high only in the Indo-Malaysian province (Figure 9). A majority of Sepiella species are narrowly tropical (Table 2).

From the above material, it can be concluded that each genus (Sepia, Metasepia, Sepiella) and each subgenus of Sepia has its characteristic distribution. It is interesting to note that the ancient Sepia (Acanthosepion) and Sepia (Sepia) are relatively diversified in the central part of the family range, which reflects the distribution of the fossil forms exclusive of the New World (Belosepia, Pseudosepia, Sepia) (Figure 11), whereas the more recently derived subgenera (Rhombosepion, Doratosepion, Hemisepius) are diversified near the periphery of the area.

BATHYMETRIC DISTRIBUTION

The bathymetric distribution of the Sepiidae is not as uniform as it first appears. As a whole, the Sepiidae are typically shallow-water animals inhabiting the continental shelf and upper slope. Most of the species are able to enter the littoral zone and do so, especially during spawning, but only a few species descend beyond 200–250 m of depth.

Table 3 shows the vertical distribution of the Sepiidae compiled from all of the available literature and from my own data on the maximal depths of catch. It is important to note that the vertical distribution of rarely caught species (Sepia dollfusi, S. gibba, and others) has not yet been worked out in detail. The actual maximal depths are probably greater than are presently recorded. On the other hand, reports of sepiid catches deeper than 600 m are probably incorrect and are called into question by experimental data (Ward and Boletzky, 1984). Taking all of this into account, I believe that the general bathymetric distribution of Sepiidae set forth below is fairly accurate and reflects the natural picture.

FIGURE 8.—Recent distribution ranges of Sepiidae: Sepia (Hemisepius) (left) in South Africa, total species = 5. Metasepia (right) in Indo-West Pacific, total species = 2. (Species numbers, as percentage of total number of species of each subgenus and genus, represented as follows: broken hatch lines, < 10%; sparse hatch lines, 11%–20%; dense hatch lines, 21%–30%; crossed hatch lines, > 30%.)

FIGURE 9.—Recent distribution range of Sepiella. (Species numbers, as percentage of total number of species of genus (6), represented as follows: broken hatch lines, < 10%; sparse hatch lines, 11%–20%; dense hatch lines, 21%–30%; crossed hatch lines, > 30%.)

Only one of the 11 Sepia (Acanthosepion) species is found deeper than 200 m, and more than 50% of the species of this subgenus have not been recorded beyond a depth of 100 m. Sepia (Sepia) species, however, appear to be relatively eurybathic, having been found from about 10 m to more than 300 m in depth.

Sepia (Rhombosepion) and S. (Anomalosepia) are capable of relatively deep “diving.” Nearly all species of these subgenera are found deeper than 200 m, and more than 50% of the species are found deeper than 300 m.

Sepia (Doratosepion) species appear to be more markedly deep-water forms than species of either S. (Acanthosepion) or S. (Sepia) but less so than species of S. (Rhombosepion) and S. (Anomalosepia). Many S. (Doratosepion) species are insufficiently known, and their reported vertical distribution is doubtful. The majority of species, however, are caught deeper than 100 m, and more than one-third of the species have been recorded deeper than 200 m.

Of the five species of S. (Hemisepius), only two are found deeper than 100 m. The same is true for Sepiella. Available data indicate that Metasepia does not occur deeper than 120 m.

It is clear that the bathymetrical distribution of a species cannot be defined solely on maximal depth of catches, although general features of such a distribution seem to be confirmed by quantitative data from trawling (Relini et al., 1985; Sanchez, 1986; Okutani et al., 1987). According to data from the Japanese expeditions in Tosa Bay reported in Okutani et al. (1987), S. lycidas, S. esculenta (S. (Acanthosepion)), and Metasepia tullbergi occur on the upper shelf to a depth of 100 m. Sepia madokai (S. (Rhombosepion)) and the S. (Doratosepion) species S. kobiensis occur on the lower shelf and near the very upper slope, whereas all other species of S. (Doratosepion) (S. tenuipes, S. subtenuipes, S. lorigera, S. longipes) occur on the slope to a depth of 400 m. According to Roeleveld (1972), S. (Sepia), S. (Hemisepius), and Sepiella are abundant off southeast Africa at depths of 0–100 m; S. (Rhombosepion) exhibit the greatest abundance at depths of 200–400 m, and S. (Anomalosepia) and S. (Doratosepion) are most abundant between depths of 25–250 m.

FIGURE 10.—Histograms of bathymetrical distributions of different genera and subgenera of Recent Sepiidae in different geographic regions.

I have assessed the frequency of occurrence of Sepiidae genera and subgenera in the material collected during the Belgian Expedition to the eastern Atlantic (Adam, 1952) and the Russian expeditions to the western Indian Ocean (1975–1976) and the Northwest Pacific (1984). It is noteworthy that the frequency of occurrence depends on depth and, in most cases, not on region or year (Figure 10). About one-half of the S. (Acanthosepion) spp. were caught between depths of 25–50 m, with the overall bathymetrical distribution being 0–200 m. Sepia (Sepia) spp. were most abundant at depths of 50–100 m and occurred to 300 m in depth. A majority of S. (Rhombosepion) spp. were found at depths of 200–400 m, with a few specimens of some species being caught between 25 m and 200 m and between 400 m and 500 m. Sepia (Doratosepion) spp. were abundant at depths 50–300 m off East Africa and 25–100 m off East Asia, the maximum capture depth recorded being 400 m. The highest number of Sepiella spp. was recorded in shallow waters above 25 m, but the vertical range of some species was seen to extend to 200 m in depth.

These findings lead to the conclusion that Sepia (Acanthosepion) species are primarily shallow-water animals, whereas S. (Sepia) species are relatively eurybathic (although they are abundant only in the sublittoral zone), and S. (Rhombosepion) species clearly inhabit deep-water. Sepia (Anomalosepia) species are abundant in the upper layers but can occur to depths of 400–500 m. Sepia (Doratosepion) species, which are never as abundant as species in the above-mentioned groups, are eurybathic and are often recorded at depths ranging from 50 to 200 m (with differences between species and regions), whereas Metasepia (at least M. tullbergi) is a shallow-water form. In comparison to other sepiids, S. (Hemisepius) is primarily a shallow-water form and Sepiella is markedly such.

TABLE 3.—Bathymetrical distribution of Sepiidae.

Genera and subgenera | Maximum depth (m)
Sepia (Acanthosepion) |
S. aculeata Van Hasselt in Férussac and Orbigny |   60
S. brevimana Steenstrup |   90
S. esculenta Hoyle | 105
S. lycidas Gray | 100
S. prashadi Winckworth | 220
S. recurvirostra Steenstrup | 157
S. savignyi Blainville |   73
S. smithi Hoyle |   51
S. stellifera Homenko and Khromov | 200
S. thurstoni Adam and Rees |   37
S. zanzibarica Pfeffer |   35
Sepia (Sepia)
S. apama Gray |   50
S. bandensis Adam |   12
S. bertheloti Orbigny | 156
S. chirotrema Berry | 220
S. dollfusi Adam | 6(?)
S. gibba Ehrenberg | 1(?)
S. insignis Smith |   42
S. latimanus Quoy and Gaimard |   30
S. mestus Gray |   95
S. novaehollandiae Hoyle | 310
S. officinalis Linnaeus | 250
S. papillata Quoy and Gaimard | 127
S. papuensis Hoyle |   51
S. pharaonis Ehrenberg | 110
S. plangon Gray | 9(?)
S. plathyconchalis Filippova and Khromov |   25
S. rozella Iredale | 160
S. simoniana Thiele | 185
S. tuberculata Lamarck | 3(?)
Sepia (Hemisepius)
S. dubia Adam and Rees |   25
S. faurei Roeleveld | 168
S. pulchra Roeleveld and Liltved |   50
S. robsoni Sasaki |   37
S. typica Steenstrup | 156
Sepiella
S. cyanea Robson |   73
S. inermis Van Hasselt in Férussac and Orbigny |   40
S. japonica Sasaki | 110
S. ornata Rang | 153
S. weberi Adam |   32
Metasepia
M. pfefferi (Hoyle) |   51
M. tullbergi (Appellöf) | 120
Sepia (Rhombosepion)
S. acuminata Smith | 350
S. cultrata Hoyle | 610
S. elegans Blainville | 430
S. hedleyi Berry | 170
S. hieronis (Robson) | 459
S. madokai Adam | 430
S. opipara (Iredale) | 184
S. orbignyana Férussac | 275
S. rex (Iredale) | 160
Sepia (Anomalosepia)
S. australis Quoy and Gaimard | 457
S. omani Adam and Rees | 201
S. sulcata Hoyle | 256
Sepia (Doratosepion)
S. adami Roeleveld | 100
S. andreana Steenstrup |   50
S. appellöfi Wülker | 355
S. aureomaculata Okutani and Horikawa | 400
S. bathyalis Khromov, Nikitina, and Nesis | 500
S. braggi Verco | 176
S. burnupi Hoyle | 240
S. carinata Sasaki | 170
S. confusa Smith | 350
S. cottoni Adam | 128
S. elongata Tate and May | 165
S. incerta Smith | 167
S. ivanovi Khromov |   44
S. joubini Massy | 170
S. kiensis Hoyle | 256
S. kobiensis Hoyle | 425
S. longipes Sasaki | 300
S. lorigera Wülker | 425
S. mascarensis Filippova and Khromov | 325
S. mirabilis Khromov |   50
S. murrayi Adam and Rees | 106
S. nanshiensis Li and Chen | 111
S. peterseni Appellöf | 100
S. saya Khromov, Nikitina, and Nesis | 117
S. sewelli Adam and Rees | 238
S. sokotriensis Khromov | 100
S. subtenuipes Okutani and Horikawa | 170
S. tala Khromov, Nikitina, and Nesis | 332
S. tenuipes Sasaki | 300
S. tokioensis Ortmann | 154
S. trygonina (Rochebrune) | 413
S. vercoi Adam | 130
S. vietnamica Khromov | 104

HISTORICAL SHIFTS OF DISTRIBUTION AND COLONIZATION

The last question to be examined is that of regional colonization by Sepiidae. Given the very fragmentary data on Mesozoic sepiids, colonization during this period will not be discussed herein. The earliest Jurassic sepiids, Voltzia and Sepialites venustus (= Sepia venusta), are known from Cuba and western Europe, respectively (Bülow-Trummer, 1920; Schevill, 1950). The Cretaceous Plathylithophycus is found in North America. Actinosepia is found in the same area and in Arabia (Figure 11) and could be a transitional form between the Mesozoic and the Cenozoic sepiids (Jeletzky, 1966; Miller and Walker, 1968; Donovan, 1977; Khromov, 1987).

FIGURE 11.—Sites of fossil sepiid localities: A, Actinosepia; B, Belosepia; P, Pseudosepia; Pl, Plathylithophycus; S, Sepia; V, Voltzia.

Eocenic Belosepia (including Stenosepia as a subgenus) and Pseudosepia were already widely distributed Sepiidae (Figure 11). The warm climate of the Eocene probably promoted sepiid colonization along the shores of the Tethys Sea. Decreasing temperatures in the Oligocene (Budjiko, 1974) strongly restricted latitudinal distribution. This also is reflected at relatively low latitudes. According to some climatological data (Verbitsky and Tchalikov, 1982), the surface temperature of the equatorial region of the ocean in the Oligocene was about 8°C below present temperatures. This temperature difference is particularly distinct in the West Atlantic (Emiliani, 1966) where the temperate zone reaches the central district (Mexico) of North America (Ushakov and Yasamanov, 1984).

Belosepia and Pseudosepia, inhabiting the Caribbean province (Jones, 1985), probably became extinct due to the temperature decrease in the Oligocene. At the same time, sepiid (Sepia) development continued in the oceans of the Old World. The presence of this genus in post-Eocene strata only in Europe (Bellardi, 1872; Bülow-Trummer, 1920) supports the hypothesis of the development of Recent Sepiidae in the Old World (Khromov, 1987).

The observed limitation of the sepiid range to the Mediterranean during the entire Neogene may be attributed to the incompleteness of the fossil record. On the other hand, the closure of the Tethys Sea about 30 million years ago (Bilal, 1985) and the isolation of the Mediterranean Sea from the Indian and Atlantic oceans (Monin, 1980; Ushakov and Yasamanov, 1984) could have blocked the way out of the Mediterranean for sepiids for relatively short periods.

According to the fossil data (Bellardi, 1872; Bülow-Trummer, 1920), the range of Sepia in the Paleogene was rather narrow. This does not seem to be an artifact of paleontological data because of the absence of the most primitive Recent Sepia (Acanthosepion) at the periphery of the family range and in the Atlantic Ocean. It is likely that this subgenus never occurred in the Atlantic.

Five main stages can be made out in Cenozic sepiid colonization. The first stage, in the Paleocene and Eocene, was occasioned by the development of Belosepia and Pseudosepia in the warm waters of the Tethys Sea. The second stage, in the Oligocene, was related to the extinction of both these genera and to the emergence of Sepia (Acanthosepion) and Sepia (Sepia). A latitudinal expansion of the family within the limits of the tropical zone apparently occurred during this period. Sepiids that were able to go out from the Mediterranean radiated to the northern part of the developing Indian Ocean. There they formed the Recent regions of high diversity and then radiated to Southeast Asia. The waters of the northwestern Pacific and Australia were not occupied by sepiids during this time, probably due to the low temperatures (Kafanov, 1981, 1982). Sepiids began to colonize the rising Mascarene Ridge, however, as suggested by the location of the present ranges of apparently conservative species of Sepia (Acanthosepion), such as S. prashadi and S. zanzibarica, that inhabit the western part of the Indian Ocean.

The third phase of colonization, in the Miocene and Lower Pliocene, was related to the emergence of Sepia (Rhombosepion) and to a marked acceleration of taxonomic radiation (Eocene, two species of Sepia; Oligicene, three spp.; Miocene, 20 spp.) (Bellardi, 1872; Bülow-Trummer, 1920). These radiations were accompanied by the colonization of greater depths and of the peripheral zones of the present family range. Sepiids penetrated into the Atlantic during this period and probably then colonized Australian and adjacent waters that became warmer at the end of the Lower Miocene and Middle Miocene (Kvasov, 1980; Ivanova, 1988).

The longitudinal expansion of the sepiid range took place because of the plate tectonic movements that resulted in the growth of the South Fiji Basin and in the removal of the Tonga-Fiji islands from Australia (Springer, 1982). Thus, sepiids were able to extend their range to near oceanic islands like New Caledonia, Fiji, and Guam (however, there is no satisfactory geological explanation for the presence of sepiids near the Marshall Islands).

Sepia (Rhombosepion) evaded competition with S. (Acanthosepion) and S. (Sepia), formed zones of high species diversity near southeast Africa and Australia, and moved to greater depths, a process possibly facilitated by the thorough modification of the sepion. I believe that this modification (Ward and Boletzky, 1984) is directly related to the origin of S. (Rhombosepion).

The Northwest Pacific was not indisputably colonized. Sepiids probably penetrated into this region during the Lower Miocene but then left when temperatures decreased, about 12 million years ago, in the Middle Miocene; indeed, this temperature decline affected the fauna of the entire Northwest Pacific (Kafanov, 1982).

The fourth stage of colonization, in the Pliocene, was preceded by the extinction of the greater part of the Mediterranean fauna, the last occurrence of fossil Sepia in Western Europe being observed in the Lower Pliocene when the Messinian Crisis started (Por, 1985). The greater part of the former Tethys shelf fauna disappeared during this crisis in the Mediterranean Sea (Nesis, 1982; Por, 1985).

Finally, the fifth stage of sepiid colonization was related to the emergence of Sepia (Anomalosepia), S. (Hemisepius), S. (Doratosepion), Metasepia, and Sepiella. The secondary colonization of the East Atlantic around the Cape of Good Hope probably took place in rather recent times. The populations (isolated?) of the Indo-oceanic S. australis and S. hieronis found off Namibia (Sanchez and Moli, 1984) support this hypothesis. The recency of the Atlantic fauna also is demonstrated by the absence of the older, primitive S. (Acanthosepion) species in this region.

Specific thermal hydrological conditions near the South African coast (Briggs, 1974) probably favored the development of the endemic barrier species found there, mainly the shallow-water Hemisepius. The hydrological barrier near the Cape of Good Hope, however, promoted species diversification, as suggested by the marked difference between subspecies of S. officinalis and by the morphological variants of S. hieronis inhabiting the west and east coasts of South Africa (Adam and Rees, 1966; Roeleveld, 1972).

The sepiid fauna of the Northwest Pacific (in the Sino-Japanese province) is probably also of fairly recent origin. In the Pleistocene, the water temperatures near Japan were about 6°–8°C lower than present temperatures (CLIMAP, 1976), and such conditions were not favorable for warm-adapted sepiids. Not only Sepia (Acanthosepion) and S. (Sepia) but also S. (Rhombosepion) are absent from the endemics of the Sino-Japanese province. These groups, however, are represented there by a few widely distributed species. The fauna of this province is represented mainly by S. (Doratosepion) (70% of the species), which are mostly endemics and are not found in the fossil record.

The recent origin of the Japan Sea fauna, where endemics are absent (Kubodera, 1986), is undoubted. The origin of cold-resistant northern Japanese, Capian (South African), and southern Australian species probably also is related to the same Pleistocene ocean temperatures.

A depth stratification of taxa occurred simultaneously with the southern expansion of the family area in the Quaternary. Sepia (Anomalosepia) colonized the lower shelf and upper slope more deeply than S. (Acanthosepion) and S. (Sepia) did, and it reached a maximum depth of about 500–600 m. Conversely, Sepiella occupied the sublittoral zone and became very abundant at this level.

Of the other events of recent sepiid history, the origin of the Red Sea endemics with their very thick phragmocones should be briefly mentioned. These species (S. gibba, S. dollfusi, S. elongata, S. arbica) have no analogs among fossil Sepia. Their likely origin lies in the Pleistocene when salinity greatly increased (up to 50%) in the Red Sea (Ivanova and Kiselev, 1985). Such salinity values make weight increase necessary for the achievement of neutral or negative buoyancy, so phragmocone capacity of the above-mentioned species was greatly increased.

The recent radiation of Sepiidae along the periphery of the family range (near South Africa, South Australia, and Japan) is demonstrated by the presence of a great number of S. (Doratosepion) species that have similar sepions but differ mainly in the sexual dimorphism of other body parts (especially in males). This radiation was probably related to the process of colonization.

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Use of the Sepion in the Taxonomy of Sepiidae (Cephalopoda: Sepioidea) with an Emphasis on the Australian Fauna

C.C. Lu

____________

C.C. Lu, Department of Zoology, National Chung Hsing University, Taichung, Taiwan.

ABSTRACT

The use of sepions (cuttebones) in the taxonomic study of Sepiidae is reviewed and the pitfalls are discussed. These pitfalls include the failure to consider individual and geographical variation and the changes associated with growth and sexual dimorphism. Recommendations are made on the study and curation of sepion collections. These recommendations are (1) to study a large series of specimens in order to cover individual and geographical variations and changes due to growth and sexual dimorphism; (2) to describe new taxa using both soft parts and sepions, not sepions alone; (3) to store sepions in 70% alcohol with 5% glycerol added in order to prevent cracking and chipping of the specimens.

Introduction and Historical Résumé

The use of sepions or cuttlebones in the taxonomic study of cuttlefishes dates back to Linnaeus (1758), who created the genus Sepia for all cephalopods without an external shell. The genus was restricted by Lamarck (1798) to the cephalopods with an internal calcareous shell. In their monumental work, Férussac and Orbigny (1835–1848) described and illustrated many more species of Sepia and their sepions.

Gray (1849), using shape and other characters of the sepion, grouped the species in Férussac and Orbigny's monograph into an orderly scheme. Gray realized that this scheme did not correspond with relationships among the species with respect to external features. Thus, he also presented a classification using external features, such as sucker arrangement on arms and tentacles, as well as using the internal shells. He established Sepiella for those animals with numerous, equal-sized suckers in eight or 10 rows on the tentacles and with “shell oblong, posterior end expanded, produced, cartilaginous, not beaked, convex beneath” (Gray, 1849:106). Although Gray had been credited as the author of the genus Sepiella, the name was sunk in obscurity for 30 years after its creation. Steenstrup (1880) redescribed the group, raising it to “one of much greater importance…at least to a subgenus” (Volsøe et al., 1962:49, English translation of Steenstrup, 1880).

In 1875, Steenstrup erected Hemisepius for his new species H. typicus, based on the following characters: (1) ventral mantle surface with deep pores in two lines of 12 pores each; (2) shell poorly developed, with very rudimentary, calcareous loculi not covering anterior part of dorsal lamella, their anterior borders not parallel to corresponding sides of thin lamella; (3) arm suckers biserial, very flattened, almost smooth, disc-like.

Rochebrune (1884) proposed a classification of Sepiidae based principally on the characters of the shell. He divided the family into 10 genera: Hemisepion, Diphtherosepion, Rhombosepion, Sepiella, Lophosepion, Spathidosepion, Doratosepion, Ascarosepion, Acanthosepion, and Sepia. This classification was deemed to be unworkable and was criticized by Hoyle (1886), Sasaki (1929), and Adam (1944, 1964) and more recently by Adam and Rees (1966).

Hoyle (1885) created the subgenus Metasepia for his new species, Sepia (Metasepia) pfefferi, on the basis of its peculiar shell in which the chitinous portion is visible over the entire dorsal surface.

In 1923, Naef proposed the division of the family into three genera: Sepiella, Hemisepius, and Sepia. The genus Sepia was further divided into seven subgenera: Eusepia, Parasepia, Acanthosepia, Doratosepia, Platysepia, Lophosepia, and Metasepia. This classification was based on morphological characters of both the soft tissues and the shell.

In an attempt to classify sepions found on the Sydney beaches, Iredale (1926a) recognized seven genera, six of them new, and 13 species, nine of which were new. Iredale (1926a, 1926b, 1940, 1954) and his contemporary, B.C. Cotton (1929, 1932), described 10 new genera and 36 new species/subspecies of cuttlefishes from Australia. All of these descriptions were based entirely on characters of the sepions, many of them beach collected, and the animals were not described. In 1954, Iredale presented a checklist of Australian cuttlefishes, recognizing three families: Sepiidae, Metasepiidae, and Sepiellidae. The Sepiidae were further subdivided into four subfamilies: Solitosepiinae, Doratosepiontinae, Tenuisepiinae, and Acanthosepiontinae.

Adam (1939a, 1939b) revised the Indo-Malayan species of Sepia and all of the species of Sepiella. He concluded that the sepion and the tentacular club represented the best characters for distinguishing the species of Sepia.

The monograph of Adam and Rees (1966) is a milestone of Sepiidae taxonomy. Most of the 65 species included were described in detail, with the structures of sepions and tentacular clubs analyzed and illustrated. The authors considered the presence of a well-developed ventral inner cone and the presence of a posterior spine to be primitive characters of the sepion, and they considered the striated area of the phragmacone to be of little systematic value. Adam and Rees considered the family Sepiidae to comprise two genera, Sepia and Sepiella, with the former composed of three subgenera, Sepia, Metasepia, and Hemisepius. The species of the subgenus Sepia were divided into several groups. Adam and Rees (1966:133) were highly critical of Iredale's prolific creation of new names based solely on sepions. They stated that Iredale's “concepts of systematic categories seem to differ so considerably from ours. Most of the species of his genera are in our opinion only individual, sexual or geographical variations of a same species; some of his genera and even subfamilies or families have only generic or probably subgeneric or specific value.”

Roeleveld (1972), in her comprehensive work on the Sepiidae of Southern Africa, adopted the classification of Adam and Rees (1966). She described and illustrated the 20 species in detail. All except one were known from both the soft parts and the sepion. The exception, Sepia angulata Roeleveld, was known only from several sepions.

Adam (1979) reported on the Sepiidae in the collections of the Western Australian Museum. Of the 16 species recorded from Western Australia, 14 had been described and illustrated based on both the soft parts and the sepion; however, Adam (1979) did not have the animal of Sepia rozella (Iredale) and, surprisingly, described a new species, Sepia reesi, based only on three sepions!

Recently, Roper and Hochberg (1988) described the color pattern and locomotory behavior of Sepia (Metasepia) pfefferi and on the basis of this analysis elevated the subgenus Metasepia to generic rank.

A comprehensive systematic revision of the Australian Sepiidae is being undertaken by the author. A large series of specimens, including both sepions and soft parts, from all parts of Australian waters as well as all available type specimens, have been studied. Of the 63 nominal species reported from Australia (see Lu and Phillips, 1985), 22 valid species have been confirmed on the evidence of animal and shell, and seven species known only from shells are considered to be of uncertain status. The remaining 34 names are all junior synonyms of some other species or are of doubtful status.

ACKNOWLEGMENTS.—I am grateful to S. Boletzky, M. Roeleveld, S. Slack-Smith, D.T. Donovan, and an anonymous reviewer for reviewing the manuscript and providing valuable advice. I am also grateful to the Smithsonian Institution for the financial support that enabled me to participate in this workshop. Thanks also are due to R. Start, C. Rowley, E. Giuliani, and P. Storer of the Museum of Victoria for preparing the photographs and typing the manuscript.

Description and Character Status

The evolution of the sepion from the shell of the fossil Spirulirostrina to the Recent Sepia was discussed in detail by Naef (1923). The sepion of the Recent Sepiidae is a calcareous structure. Figure 1 shows the general morphology of the sepion of Sepia mestus.

The Recent sepiid sepion is oval, elongate, or rhomboidal in outline. The dorsal shield is formed from the periostracum. The dorsal side of the sepion can be smooth or can have longitudinal ribs. Ventral to this is the phragmocone, consisting of the anterior, usually convex smooth zone (last loculus) and the posterior, concave striated zone.

FIGURE 1.—Cuttlebone of Sepia mestus and terminology used: A, dorsal view; B, ventral view. (a, longitudinal groove; b, last loculus; c, locular boundary; d, chitinous margin; e, striated area; f, inner cone; g, outer cone; h, spine.)

A longitudinal groove (sulcus), sometimes flanked by two low ridges, usually runs along the ventral midline of the sepion. The phragmocone is fringed by a rim that usually is chitinous anteriorly and calcareous posteriorly, forming the outer cone.

The inner cone is located between the inner side of the outer cone and the posterior end of the phragmocone. It is a V-shaped or U-shaped, narrow elevation in the form of a cord or a small, bent wall. The limbs of the inner cone extend anteriorly to the striated zone. At the posterior end of the sepion, dorsal to the outer cone, a spine (reduced rostrum) is present in some species of sepiids.

Naef (1923:498, English translation) stated that “the shell of the common Sepia is a time-honored object of study, but its systematic morphological and ecological significance is still incompletely understood because there has been no basis for its understanding.” Although our knowledge of the morphological and ecological significance of the sepion has increased since Naef's work, it is still insufficient to enable us to be certain of the sepion's significance in the natural classification of the Sepiidae. Despite this, the sepion has continuously been regarded as having important taxonomic value.

The taxonomic value of the sepion lies in the many characters found on it. The sum total of the information expressed by these character states is the taxonomic information required in species identification.

Shape and Size: The sepion of a particular species of cuttlefish has a specific shape at a given size and at maximum size. Consideration of these factors would enable a quick, gross grouping/classification. Some of the shape factors to be considered are as follows: (1) outline oval, elongate, rhomboid, slender, etc.; (2) ratio of sepion length to sepion width; (3) anterior and posterior ends broad, blunt, acuminate, pointed, etc.; (4) thickness.

Dorsal Surface: (1) convex or flat; (2) longitudinal ribs present or absent; (3) texture smooth or granulose.

Ventral Surface: (1) presence and depth of longitudinal median groove; (2) presence and height of lateral ridges associated with median groove; (3) length of last loculus and striated zone, ratio between them, and their relation to total length of sepion; (4) shape of striae; (5) shape and development of outer cone and chitinous limbs; (6) shape and development of inner cone and its posterior limbs; (7) coloration.

Spine: (1) posterior spine present or absent; (2) dorsal or ventral keel on spine present or absent.

Analysis of Uses

As mentioned earlier, the sepion has been used by various authors as a major and sometimes the sole character in the diagnosis of species (and genera). Iredale, and to a lesser extent Cotton, were the two notable proponents of this approach. Many of the genera and species recognized by these two authors undoubtedly represent individual variations. Table 1 lists some of the established valid species from Australian waters and the various names (junior synonyms) used by Iredale and Cotton, based on the report by Adam (1979) and this author's study (Lu, 1998).

Examination of the data presented by Iredale reveals that most, if not all, of the types of his species differ from other congeners mainly in the size and relative dimensions (length-width ratio) of the sepion. Cuttlefishes, like other animal groups, exhibit individual variation in various measurements. Individual sepions of a given species can vary in length and width. Failing to observe this tendency is likely to lead to recognizing individual variation as species characters. Absolute size of the sepion is meaningless unless the sepion is removed from a mature specimen, and a specimen's maturity is rarely known if only beach-collected specimens are available. In cuttlefishes, as in many other animals, morphological changes occur in some structures during growth. Naef (1923) and Mangold (1966) described changes of this type in sepions of Sepia officinalis.

Nesis (1982) pointed out the differences in the formation of septa (seen as stripes on the striated zone) between animals in tropical waters and those in temperate waters. In tropical waters, new septa are formed daily, the number of striae corresponding roughly with the age in days of the animal. In temperate waters, two or three striae are formed each week in summer, but their formation nearly stops in winter. Nesis (1982) also pointed out that although the relative length between the smooth and striated zones of the phragmocone is characteristic for many species, it can change seasonally. Sepia apama from Australia exhibits dramatic changes during growth. The sepion of S. apama juveniles is broadly oval with a posterior spine. With growth, the sepion elongates, the posterior spine is gradually covered by a chitinous substance, and a V-shaped callus begins to develop on the posterior inner edge of the inner cone. The adult sepion is elongate, the posterior spine is completely covered by chitin, the posterior end of the inner cone is greatly extended, and the callus is pronounced (Figures 2, 3). Clearly, wrong conclusions could be reached if only isolated sepions were studied without the growth factor being considered.

Naef (1923) also described the sexual dimorphism of the sepion of Sepia officinalis. Sexual dimorphism in the morphology of sepions appears to occur in many species. In some species this difference is pronounced, as was observed by Adam (1979:126), who reported, “before having examined the animals, I had separated the above mentioned dry shells in two species: Sepia chirotrema and Sepia hendryae (the animal of the latter had never been described). When I studied the animals, it turned out that the only male specimen possessed a ‘chirotrema'-like shell, whereas the young females had a ‘hendryae'-like shell.” This adequately illustrates that reliance on sepions alone may lead to a wrong conclusion.

Based on sepion features and the arrangement of tentacular suckers, which Adam (1939a, 1939b) considered to be the best features for distinguishing the species, Adam and Rees (1966) proposed a classification (grouping) of Sepiidae that was amended by Roeleveld (1972). The following grouping is based on that of Roeleveld (1972) and incorporates the list from Adam and Rees (1966) and a list of Australian representatives based on this author's work.

FIGURE 2.—Cuttlebones of Sepia apama showing changes in morphology during growth; dorsal views: A, 18 mm, female; B, 29 mm, female; C, 44 mm, female; D, 58 mm, female; E, 70 mm, female; F, 79 mm, male; G, 120 mm, female; H, 128 mm, male; 1,200 mm, female; J, 230 mm, male.

GROUP 1.—Sepion with well-developed posterior spine; ventral part of inner cone strongly developed.

a. Tentacular suckers subequal in size, in 8–20 series.

Indo-Pacific: S. aculeata, S. lycidas.

Indo-Malayan: S. brevimana.

Japan: S. esculenta.

Indian Ocean: S. thurstoni.

Red Sea, Persian Gulf: S. savignyi.

East Africa: S. zanzibarica.

Australia: S. elliptica, S. smithi, S. whitleyana.

b. Tentacular suckers unequal in size, in 8 series.

Red Sea, Indo-Pacific, Australia: S. pharaonis.

Red Sea, Indian Ocean: S. prashadi.

Species in Group 1a,b have previously been placed in various genera and subgenera as follows: Acanthosepion, Ascarosepion, Crumenasepia, Fiscisepia, and Platysepia.

GROUP 2.—Sepion with well-developed posterior spine that can be covered by chitinous hood in adult; inner cone well developed, with wide limbs, but completely reflexed onto and fused with outer cone. Tentacular suckers unequal in size, usually in 8 longitudinal series.

Europe to South Africa: S. officinalis and all subspecies.

Indo-Pacific: S. latimanus, S. papuensis.

Australia: S. apama, S. latimanus, S. mestus, S. novaehollandiae, S. papuensis, S. plangon.

FIGURE 3.—Cuttlebones of Sepia apama showing changes in morphology during growth; ventral views: A, 18 mm, female; B, 29 mm, female; C, 44 mm, female; D, 58 mm, female; E, 70 mm, female; F, 79 mm, male; G, 120 mm, female; H, 128 mm, male; I, 200 mm, female; J, 230 mm, male.

Species in Group 2 have previously been placed in the following genera or subgenera: Acanthosepion, Amplisepia, Ascarosepion, Eusepia, Mesembrisepia, Ponderisepia, and Solitosepia.

GROUP 3.—Sepion with posterior spine that can be keeled dorsally, ventrally, or both; inner cone reduced with narrow limbs; in most species outer cone with 2 posterior wings forming, in narrower sepions, cup-like expansion. Tentacular suckers nearly always arranged in 8 longitudinal series.

a. Outer cone without wings; posterior spine with or without keels. Tentacular suckers minute and subequal or unequal in size.

Japan: S. madokai.

South Africa: S. acuminata.

West Africa: S. bertheloti.

Australia: S. cultrata, S. rex.

Species of Group 3a have previously been placed in the following genera or subgenera: Acanthosepion. Decorisepia, Glyptosepia, and Rhombosepion.

b. Outer cone with wings; posterior spine not keeled. Tentacular suckers unequal in size.

Japan: S. appellöfi, S. pardalis, S. tenuipes.

c. Outer cone with wings; posterior spine not keeled. Tentacular suckers unequal in size. In some species ventral part of inner cone forms short, round ledge.

Japan: S. andreana, S. kobiensis, S. longipes, S. lorigera, S. peterseni, S. tokioensis.

South Africa: S. adami (East Africa), S. burnupi, S. confusa, S. incerta, S. joubini.

Australia: S. braggi, S. cottoni, S. vercoi.

Red Sea: S. elongata, S. trygonina (also Indian Ocean).

TABLE 1.—Valid species from Australian waters and junior synonyms used by Iredale and Cotton.

Valid name
Junior synonyms

Sepia apama Gray, 1849

Amplisepia verreauxi Iredale, 1926 (not Rochebrune, 1884)

Amplisepia parysatis Iredale, 1954

Sepia braggi Verco, 1907

Arctosepia limata Iredale, 1926

Arctosepia versuta Iredale, 1926

Arctosepia rhoda Iredale, 1954

Arctosepia treba Iredale, 1954

Arctosepia braggi xera Iredale, 1954

Sepia chirotrema Berry, 1918

Solitosepia glauerti Cotton, 1929

Solitosepia hendryae Cotton, 1929

Sepia cultrata Hoyle, 1885

Glyptosepia gemellus Iredale, 1926

Glyptosepia macilenta Iredale, 1926

Sepia elliptica Hoyle, 1885

Acanthosepion (Friscisepia) ellipticum adjacens Iredale, 1926

Sepia latimanus Quoy and Gaimard, 1832

Ponderisepia eclogaria Iredale, 1926

Sepia mestus Gray, 1849

Solitosepia liliana Iredale, 1926

Sepia novaehollandiae Hoyle, 1909

Mesembrisepia macandrewi Iredale, 1926

Mesembrisepia ostanes Iredale, 1954

Sepia papuensis Hoyle, 1885

Solitosepia submestus Iredale, 1926

Solitosepia occidua Cotton, 1929

Solitosepia genista Iredale, 1954

Solitosepia lana Iredale, 1954

Sepia plangonis Ehrenberg, 1831

Crumenasepia hulliana Iredale, 1926

Crumenasepia ursulae Cotton, 1929

Sepia plangon Gray, 1849

Solitosepia plangon adhaesa Iredale, 1926

Sepia rex (Iredale, 1926)

Decorisepia rex Iredale, 1926

Decorisepia cottesloensis Cotton, 1929

Sepia rozella (Iredale, 1926)

Solitosepia rozella peregrina Iredale, 1926

Sepia smithi Hoyle, 1885

Acanthosepion pageorum Iredale, 1954

Metasepia pfefferi (Hoyle, 1885)

Metasepia pfefferi laxior Iredale, 1926

Metasepia pfefferi wanda Iredale, 1954

Species in Group 3b,c have previously been placed in the genus or subgenus Doratosepion. The Australian species was placed in the genus Arctosepia by Iredale.

d. Outer cone with or without wings; posterior spine keeled. Tentacular suckers unequal or subequal in size.

South Africa: S. australis.

Arafura Sea: S. sulcata.

Gulf of Omar: S. omani.

Species in Group 3d have previously been placed in the genus or subgenus Rhombosepion.

e. Outer cone with wings; posterior spine absent. Tentacular suckers subequal or unequal in size.

Indian Ocean, Red Sea: S. arabica.

Europe, West Africa: S. elegans.

Japan: S. erostrata.

Species in Group 3e have previously been placed in the genera or subgenera Rhombosepion and Parasepia.

GROUP 4.—Sepion relatively broad, with developed inner cone and without posterior wings at outer cone; posterior spine absent. Tentacular suckers unequal or subequal in size.

Central Indo-West Pacific: S. bandensis.

Red Sea: S. dollfusi, S. gibba.

South Africa: S. angulata, S. elobyana (West Africa), S. hieronis, S. insignis, S. papillata, S. tuberculata.

Species of Group 4 have previously been placed in the genera or subgenera Lophosepion, Spathidosepion, and Rhombosepion.

GROUP 5.—Sepion completely chitinous, oval, acuminate anteriorly. Tentacular suckers subequal in size; dorsal arms with finger-like tips, devoid of suckers.

South Africa: S. faurei, S. robsoni.

Sepia robsoni was described as Rhombosepion robsoni by Massy.

GROUP 6.—Subgenus Hemisepius. Sepion very thin, without posterior spine, phragmocone considerably shorter than dorsal shield; inner cone reduced. Tentacular suckers subequal in size.

South Africa: S. dubia, S. typica.

Sepia typica has been placed in the genus Rhombosepion by Massy.

GROUP 7.—Genus Metasepia. Sepion rhomboidal, much shorter than mantle, with completely chitinous dorsal surface. Tentacular suckers few, unequal in size. Inner cone very narrow; posterior spine absent.

Arafura Sea, Northern Australia: M. pfefferi.

Japan: M. tullbergi.

GROUP 8.—Genus Sepiella. Mantle with posterior gland and characteristic locking apparatus. Tentacular suckers subequal in size, in 8–32 longitudinal series. Sepion with outer cone expanded, inner cone reduced, posterior spine absent.

Members of this genus are restricted to the Indo-West Pacific, Red Sea, South Africa, and West Africa. Rochebrune (1884) has placed individuals of Sepiella inermis in the genera Sepiella, Diphtherosepion, and Rhombosepion.

Recommendations

As discussed earlier, characters of the sepion are important in the species identification of cuttlefish. The following cautions and recommendations are made in order to avoid or minimize some of the pitfalls discussed earlier.

(1) Care must be taken in identifying cuttlefish using sepions alone. All character components described above must be examined, and consideration must be given to individual and geographical variations and to changes due to growth and sexual dimorphism. For comparison, a large series of specimens is recommended.

(2) Descriptions of cuttlefish taxa must contain information on both the sepion and the soft parts of the animal. Avoid describing a new taxon based on beach-collected sepions alone. Taxa based on beach-collected sepions, although permitted by the International Code of Zoological Nomenclature (ICZN, 1985), are incompletely known and often leave gaps in our knowledge that may not be filled for years. For example, Sepia bartletti (Iredale, 1954), Sepia baxteri (Iredale, 1940), Sepia glauerti (Cotton, 1929), and Sepia mira (Cotton, 1932), are still in question as they are only known from the sepion types. Beach-collected specimens do not provide either gender information or adequate distribution information because sepions can be carried over long distances by ocean currents.

(3) To prevent decalcification of sepions during specimen preparation and storage, cuttlefish specimens must be fixed in 10% buffered formalin and stored in 70% alcohol with glycerol (5% concentration) added. Adding two or three marble chips as a chemical buffer in the jar is beneficial. Liquid storage also is beneficial because sepions stored in dry conditions often suffer damages, such as cracking and chipping.

Literature Cited

Adam, W.

1939a. Cephalopoda, II: Révision des espèces Indo-Malaises du genre Sepia Linn. 1759. Siboga-Expeditie, 55b:35–92.

1939b. Cephalopoda, III: Révision du genre Sepiella (Gray) Steenstrup, 1880. Siboga-Expeditie, 55b:93–122, 4 plates.

1944.   Révision de 1′ “Étude Monographique de la Famille des Sepiadae” d'A.T. de Rochebrune (1884). Mémoires du Muséum National d'Histoire Naturelle, Paris, new series, 18(6):219–242.

1964.   Considérations sur la systématique des Sepiidae (Cephalopoda). Zoologische Mededelingen, Leiden, 39:263–278.

1979.   The Sepiidae (Cephalopoda, Decapoda) in the Collections of the Western Australian Museum. Records of the Western Australian Museum, 7(2):111–212, plates 1–13.

Adam, W., and W.J. Rees

1966.   A Review of the Cephalopod Family Sepiidae. Scientific Reports of the John Murray Expedetition 1933–34, 11(1):1–165, 46 plates.

Berry, S.S.

1918.   Report on the Cephalopoda Obtained by the F.I.S. “Endeavour” in the Great Australian Bight and Other Australian Localities. Biological Results of the Fishing Experiments Carried Out by the F.I.S. Endeavour, 1909–1914, 4(5):201–298, 67 figures, 29 plates.

Cotton, B.C.

1929.   Contributions to the Fauna of Rottnest Island, 4: Western Australian Sepiidae. Journal of the Royal Society of Western Australia, 15:87–94, plates 14–16.

1932.   Notes on Australian Mollusca with Descriptions of New Genera and Species. Records of the South Australian Museum, 4(4):543–547.

Ehrenberg, C.G.

1831.   Animalia invertebrata exclusis insects. In C.G. Ehrenberg, Symbolae Physicae, seu Icones et descriptiones Corporum Naturalium novorum aut minus cognitorum, quae ex itineribus per Libyam, Aegyptum, Nubiam, Dongalam, Syriam, Arabiam et Habessiniam…P.C. Hemprich et C.G. Ehrenberg…studio annis 1820–25 redierunt…Pars Zoologica, [4]:126 unnumbered pages. Berolini.

Férussac, A.d., and A. d'Orbigny

1835–1848.   Histoire naturelle générale et particulière des Céphalopods Acétabulifères vivants et fossiles. 1vi + 361 pages, atlas of 144 plates. Paris: J.B. Bailliere.

Gray, J.E.

1849.   Catalogue of the Mollusca in the Collection of the British Museum. I: Cephalopod Antepedia. viii + 164 pages. London: British Museum (Natural History).

Hoyle, W.E.

1885.   Diagnoses of New Species of Cephalopoda Collected during the Cruise of H.M.S. “Challenger,” 2: The Decapoda. Annals and Magazine of Natural History, (5)16:181–203.

1886.   A Catalogue of Recent Cephalopoda. Proceedings of the Royal Physical Society of Edinburgh, 9:205–267.

1909.   A Catalogue of the Recent Cephalopoda, Second Supplement, 1897–1906. Proceedings of the Royal Physical Society of Edinburgh, 17(6):254–299.

Iredale, T.

1926a. The Cuttlefish “Bones” of the Sydney Beaches. The Australian Zoologist, 4:186–196, figures 1–3, plates 21–23.

1926b. The Biology of North-West Islet, Capricorn Group, D Marine Mollusca. The Australian Zoologist, 4:237–240, plate 35.

1940.   Marine Mollusca from Lord Howe Island, Norfolk Island, Australia and New Caledonia. The Australian Zoologist, 9:429–443, plates 32–34.

1954.   Cuttlefish “Bones” Again. The Australian Zoologist, 12:63–82. plates 4, 5.

Lamarck, J.B.

1798.   Extrait d'un mémoire sur les genres de la Seche, du Calmar et du Poulpe, vulgairement nommés polypes de mer. Bulletin des Sciences, par la Société Philomathique de Paris, 2:129–131. Linnaeus, C.

1758.   Systema Naturae. Volume 1, edition 10, 824 pages. Holmiae [= Stockholm].

Lu, C.C.

1998.   A Synopsis of Sepiidae in Australian Waters (Cephalopoda: Sepioidea). In N.A. Voss, M. Vecchione, R.B. Toll, and M.J. Sweeney, editors, Systematics and Biogeography of Cephalopods. Smithsonian Contributions to Zoology, 586(1):159–190.

Lu, C.C., and J.U. Phillips

1985.   An Annotated Checklist of the Cephalopoda from Australian Waters. Occasional Papers from the Museum of Victoria, 2:21–36.

Mangold, K.

1966.   Sepia officinalis de la Mer Catalane. Vie et Milieu, 17(2):961–1012.

Naef, A.

1921–1923.   Die Cephalopoden. Fauna e Flora del Golfo di Napoli, 35: 863 pages. [English translation, Israel Program for Scientific Translations, 1972. 917 pages.]

Nesis, K.N.

1982.   Abridged Key to the Cephalopod Mollusks of the World's Oceans. 385 pages. Moscow: Light and Food Industry Publishing House. [English translation, B.S. Leviton, Cephalopods of the World. 351 pages. T.F.H. Publications, Inc., Neptune City, New Jersey, 1987.]

Quoy, J.R, and J.P. Gaimard

1824–1826.   Zoologie. In L. de Freycinet, Voyage autour de monde…exécuté sur…lUranie et la Physicienne, pendant 1817–1820, 712 pages, atlas of 96 plates. Paris.

Rochebrune, A.T.d.

1884.   Éude monographique de la famille des Sepiadae. Bulletin des Sciences, par la Socieété Philomathique de Paris, (7)8:74–122, plates 3–6.

Roeleveld, M.A.

1972.   A Review of the Sepiidae (Cephalopoda) of Southern Africa. Annals of the South African Museum, 59(10): 193–313, 20 figures, 11 plates, 53 tables.

Roper, C.F.E., and F.G. Hochberg

1988.   Behavior and Systematics of Cephalopods from Lizard Island, Australia, Based on Color and Body Patterns. Malacologia, 29(1):153–193.

Sasaki, M.

1929.   A Monograph of the Dibranchiate Cephalopods of the Japanese and Adjacent Waters. Journal of the College of Agriculture, Hokkaido Imperial University, supplement, 20:1–357, 150 figures, 30 plates.

Steenstrup, J.

1875.   Hemisepius, en ny Slaegt of Sepia-Blaeksprutternes Familie. Videnskabernes Selskab. Skrifter. Naturvidenskabelig og Mathematisk Afdeling, 10(7):465–482, 2 plates.

1880.   [See Volsøe et al., 1962.]

Verco, J.C.

1907.   Notes on South Australian Marine Mollusca, with Descriptions of New Species, Part VI. Transactions of the Royal Society of South Australia, 31:213–230, 2 plates.

Voløe, A., J. Kundsen, and W. Rees, translators

1962.   The Cephalopod Papers of Japetus Steenstrup. 330 pages. Copenhagen: Danish Science Press Ltd. [English translation of Sepiella Gray, Stp. Videnskabelige Meddelelser fra Dansk Naturhistorisk Forening i Kjøbenhavn, 1879–1880:347–356.]

A Provisional Generic Classification of the Family Loliginidae

Michael Vecchione, Thomas F. Brakoniecki, Yutaka Natsukari, and Roger T. Hanlon

_____________

Michael Vecchione, National Marine Fisheries Service Systematics Laboratory, National Museum of Natural History, Washington, D.C. 20560, United States. Thomas F. Brakoniecki, 734 NE 113 St., Miami, Florida 33161, United States. Yutaka Natsukari, Faculty of Fisheries, Nagasaki University, Bunkyo-cho, Nagasaki 852, Japan. Roger T. Hanlon, Marine Resources Center, Marine Biological laboratory, Woods Hole, Massachusetts 02543, United States.

ABSTRACT

This paper attempts to resolve the substantial confusion in the generic classification of the myopsid squid family Loliginidae. Forty-two loliginid species are grouped phenetically based on the morphology of the hectocotylus and of the spermatophore, the presence of visceral photophores, the structure of arm-sucker rings, relative fin length, elongation of the posterior mantle into a tail-like structure, and egg size. With few exceptions, the groups thus formed are assigned to genera and subgenera. We recognize nine groups of species and tentatively assign them to five genera and four subgenera. These are Sepioteuthis, Lolliguncula (Lolliguncula), Lolliguncula (Loliolopsis), Uroteuthis (Uroteuthis), Uroteuthis (Photololigo), Loliolus (Loliolus), Loliolus (Nipponololigo), Loligo (Loligo), and Loligo (Alloteuthis).

Introduction

The systematics of the myopsid squid family Loliginidae has long been in disorder. In addition to many problems with differentiation of species, loliginid systematics has been hampered throughout the past several decades by the presence of two systems of generic-level classification. The differences between these two systems primarily involve a question of the importance of gladius structure at the generic level. Both systems have been used widely in the scientific literature, although many authors have consistently qualified their use by stating that the family is badly in need of revision based on a worldwide review.

Three separate revisions have recently been completed (Natsukari, 1984b; Brakoniecki, 1986; Alexeyev, 1991); all concluded that a correct generic-level classification of the family is radically different from either of the previous classifications (Table 1). Unfortunately, these new classifications also differed substantially from each other, were presented in unpublished dissertations and were not widely disseminated, and none has gained full acceptance.

The family Loliginidae includes many species that are important in trophic systems, fisheries, and biomedical studies. Obviously, the existence of five conflicting systems of classification can cause hopeless confusion among researchers working in these fields, in addition to obfuscating real relationships among the species (Dubois, 1988). This paper attempts to resolve the differences among the systems of generic-level classification of the Loliginidae and thus to stabilize the taxonomy at this level. We do not deal with species-level problems herein. Rather, for purposes of this discussion, 42 nominal species are included herein; to date, none of these have been placed in the synonymy of any other nominal species. Some of these species names are likely to change in light of future work. We also do not address the question of whether Pickfordiateuthis should be considered a member of the family Loliginidae rather than constituting a second family within the Myopsida.

Results of Group Deliberations

The authors of this paper converged on a tentative classification acceptable to all of us after two weeks of intense discussions and the study of type and other specimens assembled from collections worldwide. Not all problems were resolved, however. We failed to agree on the generic affinities of two species, and a third species has since been called into question. The subgeneric relationships of the species that we have placed in the genus Loligo sensu lato also remain unresolved. Furthermore, one of us (YN) questions the use of subgenera within this family and feels that the subgenera should be elevated to full generic status. As Mayr (1988:281) noted, however, “rank determination is one of the most difficult and subjective decision processes in classification,” and “the best classification is the one that permits the most useful comparative investigations” (Mayr, 1988:303). Currently, there are no commonly accepted objective criteria for determination of taxonomic rank above the species level (Allmon, 1992). This problem is particularly important at the genus level for the practical reason that the generic name forms part of the binomial nomenclature that all biologists use to communicate about the organisms with which they work (Dubois, 1988). Elevation of the subgenera presented here to generic rank would not change our fundamental grouping of species.

TABLE 1.—Generic classifications for Loliginidae. Alexeyev (1991) treated only those species with photophores; see text for discussion of his classification.

The classification presented below is based on phenetic similarity; it does not represent a thorough phylogenetic analysis of the family. There was general acknowledgment among the authors that other methods, such as ontogenetic development and biochemical genetics, should be pursued to augment existing morphological observations on relationships among taxa.

Characters that we agreed were of generic importance include the morphology of the hectocotylus and of the spermatophore, the presence of photophores on the viscera, the structure of sucker rings on the arm suckers, relative fin length, and egg size (Table 2). It is noteworthy that we all agreed that the morphology of the gladius, as used to distinguish the genus Doryteuthis, is not of generic importance, although it is important at the specific level (see also Alexeyev, 1989). The gladius is quite variable both within and among species and could be highly adaptive in response to differences in swimming behavior. Other traditional characters that we feel are too variable to be of use in the generic systematics of the Loliginidae include spermatophore deposition site, presence of suckers on the buccal lappets, adult chromatophore patterns (e.g., lateral “flame stripes”), and presence of a longitudinal midventral ridge.

Family LOLIGINIDAE Lesueur, 1821

Loliginidae Lesueur, 1821 [not Steenstrup, 1861; not Orbigny, 1839].

See Brackoniecki (1986:5) for a discussion of authorship of the familial name.

1. Sepioteuthis Blainville, 1824

TYPE SPECIES.—Loligo sepioidea Blainville, 1823, by original designation.

DIAGNOSIS.—Fins occupying almost entire lateral margin of mantle, except in paralarvae. Posterior mantle not elongated into tail-like structure. Eggs large, length > 5 mm. Arm-sucker rings with pointed teeth around entire margin. Proximal suckers on hectocotylus unmodified. Hectocotylus without crest, hectocotylization consists of reduction in sucker size and elongation of sucker stalks along modified portion of arm to form papillae on both dorsal and ventral rows. Photophores absent. Spermatophore with short cement body.

SPECIES INCLUDED.—Sepioteuthis australis Quoy and Gaimard, 1832; Sepioteuthis lessoniana Lesson, 1830; Sepioteuthis loliginiformis (Rüppell and Leuckart, 1828); Sepioteuthis sepioidea (Blainville, 1823).

DISTRIBUTION.—Because of their association with coral reefs, the common name for these species is “reef squids.” The distribution of the genus generally follows that of coral reefs, i.e., warm, clear, tropical and subtropical waters, but coral reefs are not a habitat requirement for all of these squids. For example, S. lessoniana is common around the southern part of Honshu and Kyushu in Japan, but it is not associated with coral reefs in those areas. There is one species, S. sepioidea, in the western Atlantic; the remaining species are found in the Indo-West Pacific.

DISCUSSION.—The systematic status of the genus Sepioteuthis has long been stable and without controversy. Although fin length varies greatly throughout the family, and the hectocotylization of Sepioteuthis is similar to that of some other species, the Sepia-like body form, together with the large eggs and distinctive sucker dentition, seems to define a natural group of species that are very different from all other loliginids. It has been proposed that S. lessoniana is actually a complex of several species (Segawa et al., 1993).

TABLE 2.—Characters and states used for phenetic grouping of loliginid species.

1.
Fins

(a) lateral

(b) posterior

2.
Tail-like extension of posterior mantle

(a) extending beyond fins

(b) fins along sides to posterior tip

(c) absent

3.
Eggs

(a) large (longest axis > 5 mm)

(b) small (longest axis < 4 mm)

4.
Arm-sucker rings, proximal margin

(a) semicrescent plate

(b) square teeth

(c) pointed teeth

5.
Arm-sucker rings, distal margin

(a) square teeth

(b) pointed teeth

6.
Hectocotylus, ventral row of suckers

(a) reduction in sucker size or loss of suckers; elongation of sucker stalks along modified portion of arm to form papillae

(b) ventral crest formed by fusion of protective membrane with ventral row of papillae such that original form of conical papillae completely obscured

(c) unmodified

7.
Hectocotylus, proximal region

(a) suckers and/or stalks modified

(b) unmodified

8.
Photophores on ventral ink sac

(a) one pair present

(b) absent

9.
Spermatophore, cement body

(a) short

(b) long

2. Lolliguncula Steenstrup, 1881

TYPE SPECIES.—Loligo brevis Blainville, 1823, by original designation.

DIAGNOSIS.—Fins posterior and broadly rounded, wider than long in adults. Mantle without tail-like posterior elongation. Eggs small (<3 mm). Arm-sucker rings with square, plate-like teeth around entire margin. Modified prtion of hectocotylus varies between subgenera. Hectocotylus without crest, hectocotylization consists of reduction in sucker size and elongation of sucker stalks to form papillae on either dorsal or both dorsal and ventral rows. Photophores absent. Spermatophore with long cement body.

2a. (Lolliguncula) Steenstrup, 1881

TYPE SPECIES.—Loligo brevis Blainville, 1823, by original designation.

DIAGNOSIS.—Characters of genus, with modified portion of hectocotylus less than entire arm, proximal portion not modified, hectocotylized arm may be slightly elongate.

SPECIES INCLUDED.—Lolliguncula (Lolliguncula) brevis (Blainville, 1823); Lolliguncula (Lolliguncula) mercatoris Adam, 1941; Lolliguncula (Lolliguncula) panamensis Berry, 1911a.

2b. (Loliolopsis) Berry, 1929

TYPE SPECIES.—Loligo diomedeae Hoyle, 1904, by monotypy and synonymy with original designation, Loliolopsis chiroctes Berry, 1929.

DIAGNOSIS.—Characters of genus, with hectocotylus modified along entire length and greatly elongate.

SPECIES INCLUDED.—Lolliguncula (Loliolopsis) diomedeae (Hoyle, 1904).

REMARKS ON GENUS Lolliguncula

DISTRIBUTION.—With the exception of Lolliguncula mercatoris, these are all North and South American species that have their low-latitude distributions centered at Panama. One species, L. brevis, is found on the Atlantic side of the Americas, whereas two, L. panamensis and L. diomedeae, are found on the Pacific side. The remaining species, L. mercatoris, is distributed at similar latitudes along the Atlantic coast of Africa. All of these species are found in warm, shallow, inshore waters. The genus is noteworthy among cephalopods for its euryhalinity.

DISCUSSION.—The genus Lolliguncula was established to distinguish L. brevis from the species of Loligo then known, based on body and fin shape and on spermatophore deposition site. These characters have since proven to exhibit considerable variability, both within and among species. All of the species in this genus, however, are united and distinguished from all other loliginids by the long cement body of their spermatophores. Variability exists in hectocotylus morphology, and this led Berry (1929) to erect the genus Loliolopsis and led Brakoniecki (1986) to erect Afrololigo. This variability is extreme in L. diomedeae, but Brakoniecki (1986) has pointed out the similarities in hectocotylization between this species and the others of Lolliguncula. We now consider all of these species to represent a natural, although variable, genus-level group.

Alexeyev (1992) reported examining a sample of L. mercatoris from Sierra Leone in which the seven females possessed paired structures on the ink sac that appeared to be similar to the photophores of other loliginids. Unlike recognized luminescent loliginid species, the males he examined lacked these structures. He therefore proposed to use the name Afrololigo and to consider this species to be more closely related to the recognized luminescent loliginids than to Lolliguncula. Because actual luminescence has not been observed in L. mercatoris, however, and because it shares other characters, such as the long cement body of the spermatophore, with the other species of Lolliguncula, we consider it prudent to be conservative and retain mercatoris within Lolliguncula. This would require reconsideration if further evidence on the putative photophores indicates that they are homologous with those of the luminescent species that we consider to be Uroteuthis.

3. Uroteuthis Rehder, 1945

TYPE SPECIES.—Uroteuthis bartschi Rehder, 1945, by original designation.

DIAGNOSIS.—Fins lateral or posterior. Elongation of posterior mantle variable, extreme in subgenus Uroteuthis. Eggs small. Proximal margin of arm-sucker rings with semicrescent plate; distal margin with square teeth. Proximal suckers on hectocotylus unmodified. Hectocotylus with two rows of papillae. One pair of photophores present on ventral surface of ink sac. Spermatophore with short cement body.

3a. (Uroteuthis) Rehder, 1945

TYPE SPECIES.—Uroteuthis bartschi Rehder, 1945, by monotypy and original designation.

DIAGNOSIS.—Characters of genus, with tail-like elongation of posterior mantle extending beyond lateral fins.

SPECIES INCLUDED.—Uroteuthis (Uroteuthis) bartschi Rehder, 1945.

3b. (Photololigo) Natsukari, 1984

TYPE SPECIES.—Loligo edulis Hoyle, 1885, by original designation.

DIAGNOSIS.—Characters of genus. Elongation of posterior mantle variable but not tail-like; when mantle elongated, fins extend along sides to posterior tip.

SPECIES INCLUDED.—Uroteuthis (Photololigo) abulati (Adam, 1955); Uroteuthis (Photololigo) arabica (Ehrenberg, 1831); Uroteuthis (Photololigo) bengalensis (Jothinayagam, 1987); Uroteuthis (Photololigo) chinensis (Gray, 1849); Uroteuthis (Photololigo) duvaucelii (Orbigny, 1835, in Férussac and Orbigny, 1834–1848); Uroteuthis (Photololigo) edulis (Hoyle, 1885); Uroteuthis (Photololigo) noctiluca (Lu, Roper, and Tait, 1985); Uroteuthis (Photololigo) reesi (Voss, 1962); Uroteuthis (Photololigo) robsoni (Alexeyev, 1992); Uroteuthis (Photololigo) singhalensis (Ortmann, 1891); Uroteuthis (Photololigo) vossi (Nesis, 1982).

REMARKS ON GENUS Uroteuthis

DISTRIBUTION.—The Indo-West Pacific distribution of all these species supports our contention that these species constitute a natural, closely related species group.

DISCUSSION.—The photophores on the ventral surface of the ink sac in all these species is perhaps the strongest indication to be found in this family of a close relationship among species. This relationship is further supported by similarities in the hectocotylus and in arm-sucker dentition. These characters led Natsukari (1984a) to establish the genus Photololigo for the Indo-West Pacific species with photophores, formerly assigned to either Loligo or Doryteuthis. Uroteuthis bartschi, however, has similar photophores and arm suckers, as well as a similar hectocotylus, and has an Indo-West Pacific distribution. The elongation of the posterior mantle, which was given generic status in the description of Uroteuthis, is the extreme example in a cline of mantle elongation, similar to the cline found in the eastern Atlantic where Alloteuthis is the extreme example. This elongation is so extreme in Uroteuthis as to cause a discontinuity in the cline, consequently it warrants separate taxonomic status. The sole recognized species in this taxon, however, possesses all of the generic characters of Photololigo; therefore, it should be included in the genus that Natsukari described. Unfortunately, priority goes to Uroteuthis as the name of the genus, rather than the more descriptive Photololigo. Aside from the photophores, Uroteuthis sensu stricto and Alloteuthis can be separated based on position of the fins, lateral versus terminal, respectively, and tentacular ring dentition. Therefore, elongation of the mantle end in these two taxa appears to be analogous, not homologous.

In a revision of Loliolus, Lu et al. (1985) described a new species, L. noctiluca. They included this species in Loliolus because its hectocotylization was a modification of the entire length of the arm, the original diagnostic character of the genus Loliolus. The hectocotylus of L. noctiluca is otherwise very different from those of the other species of Loliolus in that it lacks a ventral crest and both the dorsal and ventral rows of suckers are modified into papillae. The hectocotylus of L. noctiluca is thus similar to those of the Uroteuthis and Photololigo species except that more of the arm is modified, making it the extreme in a cline of the percentage of arm length that is modified by hectocotylization. Furthermore, L. noctiluca was so named because of structures on the ink sac believed to be photophores. These characters, together with similarity in arm-sucker dentition, indicate that this species should be included in the subgenus Photololigo of the genus Uroteuthis.

In his revision of the family, Alexeyev (1991, 1992) retained Uroteuthis as a separate genus and separated the species that we include in the subgenus Photololigo into a new genus and two new subgenera as follows:

Subfamily UROTEUTHINAE

Genus Uroteuthis

Uroteuthis bartschi

Uroteuthis pickfordi (see comments below)

Uroteuthis reesi

Uroteuthis singhalensis

Genus Photololigo

Subgenus Photololigo

Uroteuthis edulis

Subgenus Pteroteuthis

Uroteuthis arabica

Uroteuthis chinensis

Uroteuthis robsoni

Subgenus Vossia

Uroteuthis duvaucelii

Loligo forbesii (see comments below)

Uroteuthis vossi

Genus Aestuariolus

Uroteuthis noctiluca

Genus Afrololigo

Lolliguncula mercatoris (see comments above)

Alexeyev used characters such as fin length and shape, dentition of sucker rings on arm and club suckers, and reduction of conus flags on the gladius to develop this classification. With the exceptions of Loligo pickfordi, Loligo forbesii, and Lolliguncula mercatoris (U. bengalensis was recently described and was not included in Alexeyev's work), his subfamily Uroteuthinae contains the same species that we include in genus Uroteuthis. This again raises the question of what level is appropriate when establishing taxonomic ranks above species. Because the grouping of species generally matches ours, however, we will not modify our classification now.

Yeatman (1993) has presented evidence that some species of Uroteuthis (Photololigo) are actually species complexes.

4. Loliolus Steenstrup, 1856

TYPE SPECIES.—Loligo hardwickei Gray, 1849, by synonymy with original designation, Loliolus typus Steenstrup, 1856.

DIAGNOSIS.—Fins posterior, mantle without tail-like elongation. Eggs small. Arm-sucker rings with square, plate-like teeth around entire margin. Modification of proximal portion of hectocotylus varies between subgenera. Hectocotylization includes crest along portion of ventral surface of arm and modification of part of dorsal row of suckers into papillae. Photophores absent. Spermatophore with short cement body.

4a. (Loliolus) Steenstrup, 1856

TYPE SPECIES.—Loligo hardwickei Gray, 1849, by synonymy with original designation, Loliolus typus Steenstrup, 1856.

DIAGNOSIS.—Characters of genus, with hectocotylus modified along entire arm.

SPECIES INCLUDED.—Loliolus (Loliolus) affinis Steenstrup, 1856; Loliolus (Loliolus) hardwickei (Gray, 1849).

4b. (Nipponololigo) Natsukari, 1983

TYPE SPECIES.—Loligo japonica Hoyle, 1885, by original designation.

DIAGNOSIS.—Characters of genus, with less than entire arm modified by hectocotylization, proximal part with unmodified suckers.

SPECIES INCLUDED.—Loliolus (Nipponololigo) beka (Sasaki, 1929); Loliolus (Nipponololigo) japonica (Hoyle, 1885); Loliolus (Nipponololigo) sumatrensis (Orbigny, 1835); Loliolus (Nipponololigo) uyii (Wakiya and Ishikawa, 1921).

REMARKS ON GENUS Loliolus

DISTRIBUTION.—The species in this genus are all found in the Indo-West Pacific.

DISCUSSION.—Loliolus was originally erected to include species of small loliginids with heart-shaped fins in which the entire left ventral arm of the males is modified. As discussed above under Uroteuthis and by Brakoniecki (1986), clines exist in the percentage of the arm hectocotylized within species groups with similar hectocotyli. Thus, we do not feel that this character state is sufficient for generic status, although the presence of a distinctive character of the hectocotylus (Table 2, character 6(b)) indicates a close relationship among these species (Natsukari, 1983). Because the percentage of the arm hectocotylized is considered to be a cline within this group of species with otherwise similar hectocotyli and arm-sucker dentition, Loliolus and Nipponololigo are combined herein to form a single genus that, by priority, is named Loliolus.

5. Loligo Lamarck, 1798

TYPE SPECIES.—Loligo vulgaris Lamarck, 1798, by subsequent designation of Hoyle (1910).

DIAGNOSIS.—Fins posterior. Some species with posterior elongation of mantle, especially in males. Eggs small to medium-sized, <4 mm. Arm-sucker ring dentition variable. Proximal suckers on hectocotylus unmodified. Hectocotylus without ventral crest, hectocotylization consists of reduction in sucker size and elongation of sucker stalks to form papillae on either dorsal or both dorsal and ventral rows. Photophores absent. Spermatophore with short cement body.

5a. (Loligo) Lamarck, 1798

TYPE SPECIES.—Loligo vulgaris Lamarck, 1798, by subsequent designation of Hoyle (1910).

DIAGNOSIS.—Characters of genus, without tail-like elongation of posterior mantle. (As stated below, the authors failed to agree on other characters to distinguish subgeneric groups of species other than Alloteuthis.)

SPECIES INCLUDED.—Loligo (Loligo) vulgaris Lamarck, 1798.

5b. (Alloteuthis) Wülker, 1920

TYPE SPECIES.—Loligo media (Linnaeus, 1758), by original designation of Naef in an unpublished manuscript cited by Wülker (1920).

DIAGNOSIS.—Characters of genus, with posterior mantle an elongated tail-like structure. Fins extend posteriorly along sides of tail-like structure.

SPECIES INCLUDED.—Loligo (Alloteuthis) africana (Adam, 1950); Loligo (Alloteuthis) media (Linnaeus, 1758); Loligo (Alloteuthis) subulata Lamarck, 1798.

5c. Species with Unresolved Subgeneric Affinities

SPECIES INCLUDED.—Loligo bleekeri Keferstein, 1866; Loligo gahi Orbigny, 1835; Loligo ocula Cohen, 1976; Loligo opalescens Berry, 1911b; Loligo pealeii LeSueur, 1821; Loligo plei Blainville, 1823; Loligo roperi Cohen, 1976; Loligo sanpaulensis Brakoniecki, 1984; Loligo surinamensis Voss, 1974.

REMARKS ON GENUS Loligo

DISTRIBUTION.—This genus includes species of the eastern and western Atlantic, eastern Pacific, and northwest Pacific. Although this could seem somewhat disjunct, it is actually a nearly continuous distribution from southern Africa, around the North Atlantic, around South America and the west coast of the Americas, to Japan. The gaps in this distribution, from Iceland to Newfoundland and from Alaska to Hokkaido, Japan, are high-latitude barriers to this temperate-tropical group of species.

DISCUSSION.—This genus is the least resolved within this classification. The species that we consider here to be Loligo sensu lato are unified in their lack of the distinctive characters of the other genera (photophores, spermatophore with long cement body, large eggs, hectocotylus with ventral crest, etc.). Morphologically, however, these species are very similar, so much so that it is often very difficult to assign specimens to species, especially if the location of capture is unknown. The most distinctive species are those with a tail-like elongation of the posterior mantle. This elongation is unlike that of Uroteuthis in that the fins extend posteriorly along the entire tail-like structure in Loligo (Alloteuthis) but not in Uroteuthis. As we discussed above under Uroteuthis, we consider the posterior extension to be of subgeneric rather than generic importance, and thus we have retained Alloteuthis as a subgenus.

The existence of subgenus Alloteuthis within the genus Loligo necessitates a subgenus Loligo. The fact that we have included only the type species within this subgenus does not indicate that we consider the subgenus to be monotypic. It indicates, rather, that we did not reach agreement on the subgeneric affinities of the remaining species.

Opinions differed among the authors of this paper about the relative importance of characters other than “tail” length in establishing subgenera of Loligo. Very preliminary biochemical analyses indicate that there may be sufficient evolutionary distance among groups of these species to establish separate taxa (Brierley and Thorp, 1994). The species listed above with unresolved subgeneric affinities comprise the species that Brakoniecki (1986) included in redefining the genus Doryteuthis. If these species prove to be a natural evolutionary group, then they should be considered to belong to the subgenus Doryteuthis of the genus Loligo.

6. Species with Unresolved Generic Affinities

SPECIES INCLUDED.—Lolliguncula argus Brakoniecki and Roper, 1985; Loligo forbesii Steenstrup, 1856; Doryteuthis pickfordi Adam, 1954.

DISCUSSION.—We failed to reach agreement as to whether Lolliguncula argus should be assigned to Loligo or to Lolliguncula. If its spermatophores have long cement bodies, it belongs in the latter genus.

The taxonomic characters of Doryteuthis pickfordi are not sufficiently well known to assign it to a genus. Alexeyev (1992) believes this species to possess photophores. If he is correct, it would properly be assigned to Uroteuthis (Photololigo).

A more disturbing problem is Alexeyev's (1992) report of a single juvenile specimen of Loligo forbesii (67 mm mantle length) from the Mediterranean Sea near Port Said that he believed to have photophores. This species has been very well known throughout cephalopod history and has never been reported to luminesce. Naef (1921), however, mentioned accessory-gland structures on the ink sacs of both sexes that he thought might have a bioluminescent function. Furthermore, Lum-Kong and Hastings (1992) reported that one bacterial isolate (of 21) from the accessory nidamental glands of the females was luminescent. If L. forbesii typically has photophores, and if they are homologous with those of Uroteuthis, then this species belongs in that genus. This, in turn, would imply a biogeographical extension of the genus into the Mediterranean Sea and eastern Atlantic Ocean, an extension that is difficult to understand in this stenohaline group of squids.

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1984b. Morphological and Taxonomical Studies on the Family Loliginidae Steenstrup, 1861 (Cephalopoda: Mollusca). 288 pages, 16 plates. Doctoral dissertation, University of Kyushu, Japan.

Nesis, K.N.

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Ortmann, A.

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Rehder, H.A.

1945.   A New Genus and Species of Squids from the Philippines. Proceedings of the Biological Society of Washington, 58:21–26, 1 plate.

Sasaki, M.

1929.   A Monograph of the Dibranchiate Cephalopods of the Japanese and Adjacent Waters. Journal of the College of Agriculture, Hokkaido Imperial University, supplement, 20: 357 pages, 159 figures, 30 plates.

Segawa, S., S. Hirayama, and T. Okutani

1993.   Is Sepioteuthis lessoniana in Okinawa a Single Species? In T. Okutani, R.K. O'Dor, and T. Kubodera, editors, Recent Advances in Cephalopod Fisheries Biology, pages 513–521. Tokyo: Tokai University Press.

Steenstrup, J.

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Generic and Specific Names Introduced in the Squid Family Loliginidae (Cephalopoda: Myopsida)

Michael J. Sweeney and Michael Vecchione

_________________

Michael J. Sweeney, Department of Invertebrate Zoology, Division of Mollusks, National Museum of Natural History, Smithsonian Institution, Washington, D.C. 20560, United States. Michael Vecchione, National Marine Fisheries Service Systematics Laboratory, National Museum of Natural History, Washington, D.C. 20560, United States.

ABSTRACT

The cephalopod genus Loligo and family Loliginidae are among the earliest Linnaean names used for squids. The history of the nomenclature in this family is long and confused, at least in part because of its worldwide distribution, the diversity of the group, the lack of comprehensive collections, and the scattered and often isolated literature dating from the 18th and 19th centuries. We review the current nomenclatural status of 205 names of nonfossil taxa that have been assigned to the squid family Loliginidae.

Introduction

According to Lesueur (1821:90), use of the name “loligo” for squids can be traced to the classical Roman philosopher, Pliny the Elder (see also Naef, 1923:197). Linnaeus established Sepia loligo in 1758 to encompass all cephalopods with fins and a cylindrical body (Hoyle, 1910:410). Subsequently, squids in general were often referred to as “loligos” (e.g., Lesueur, 1821). Many authors have interpreted Schneider's (1784) use of the name “Loligo” (capitalized and not preceded by a generic name) as the establishment of the genus Loligo. Hemming (1954), however, showed that Loligo Schneider, 1784, resulted from a misinterpretation of Schneider's work. Schneider's intent was to remove Nautilus Linnaeus, 1758, and Argonauta Linnaeus, 1758, from the univalve molluscs and to include them with all other cephalopods in a new genus. Octopodia. Thus, Schneider actually proposed the new combination Octopodia loligo but did not follow the conventions of always using the generic name and not capitalizing the species. Loligo was formally described by Lamarck in 1798 to distinguish four squid species, L. vulgaris, L. subulata, L. sagittata, and L. sepiola, from the octopods (for which he erected the genus Octopus Lamarck, 1798) and from the cuttlefishes of the genus Sepia (see end of “Discussion” for correct authorship of Loligo).

The only other squid genera that predate 1821 are Onychoteuthis Lichtenstein, 1818, which was established to distinguish cephalopods in which hooks replace some of the suckers on the arms or tentacles, and Cranchia Leach, 1817, a very unusual squid. Lesueur (1821) erected a family that he called Loligoidea (afterwards emended to Loliginidae, see Vecchione et al., 1998) to fit the “Loligos” (Leachia, Loligo, and Onykia) into Cuvier's “natural order.” Lesueur (1821:88) stated that “it is of little consequence what characters we select for the distribution of these animals into families and genera, if our arrangement is the most convenient, and exhibits, as near as possible, a graded transition from one to the other.”

A consequence of the age of this family, as well as its early inclusion of all squids, is that many taxa, both correctly and incorrectly described, have been considered loliginids at one time or another. Therefore, taxonomic nomenclature in the squid literature can be very confusing. We review the 205 taxa that were initially described in the Loliginidae and indicate their current status.

METHODS

We include only nonfossil, post-Linnean names. We do not include names that, subsequent to their original description, were simply listed incorrectly or were generic misidentifications, such as Loligo fabricii in Blainville, 1823. The presentation is divided into two sections: (1) nominal genera and subgenera and (2) nominal species, subspecies, varieties, and formae. The names are listed alphabetically within each section. We have included for each name the introduced name, author, year of publication, page, and illustration; the type species of the genus; and current status, including, for synonyms, the first authority to synonymize the introduced name with the current valid name, followed by the current generic association (if different). When status is listed as “nomen nudum” or “incertae sedis” with no published authority listed, the decision as to the status of the taxon is that of the present authors. The “Literature Cited” includes all cited references.

Several comments regarding literature citation are required. There has been some confusion as to the availability of new taxa names contained in the dissertation of Brakoniecki (1986). Our investigation of the circumstances surrounding its publication and distribution has determined that production was by standard ink-on-paper printing methods, copies in excess of those required by the University of Miami were printed (records exist at Rosenstiel School of Marine and Atmospheric Science, University of Miami), and copies were simultaneously distributed to experts worldwide. Consultation with a member of the International Commission on Zoological Nomenclature (ICZN) (F.M. Bayer, 30 Sep 1992) led to the conclusion that Brakoniecki (1986) fulfilled the requirements of the ICZN for publication to make names available.

Publication dates for two of Orbigny's works have been cited in a wide variety of ways. His Voyage dans l'Amérique Méridionale was printed with title page dates of 1835–1843. Dates of publication for paginated sections and plates were determined by Sherborn and Griffin (1934). Because dates determined after publication should be cited in brackets, the publication date should be cited as [1834]1835–1843[1847]. Similarly, Férussac and Orbigny's monograph, Histoire naturelle générale et particulière des Céphalopodes Acétabulifères vivants et fossiles, was printed with title page dates of 1835–1848. Dates of publication for paginated sections and plates were determined by Winckworth (1942), and the publication date should be cited as [1834]1835–1848. We have elected to use 1834–1847 and 1834–1848, respectively, when referring to date of publication so as not to make the species citation overly cumbersome.

ACKNOWLEDGMENTS.—The authors wish to thank Clyde Roper, National Museum of Natural History, and Bruce Collette, National Marine Fisheries Service, for their critical reviews of this paper. We also thank Frederick M. Bayer, National Museum of Natural History, for several very helpful discussions.

Nominal Genera and Subgenera of Loliginidae

Acrololigo Grimpe, 1921:299.

Type species: Sepia media Linnaeus, 1758.

Status: = Alloteuthis Wülker, 1920 (fide Naef, 1923:209).

Remarks: Replacement name for Acroteuthis Berry, 1913 (preoccupied), therefore taking the same type species.

Acroteuthis Berry, 1913:590.

Type species: Sepia media Linnaeus, 1758, by original designation.

Status: = Alloteuthis Wülker, 1920 (fide Naef, 1923:209).

Remarks: Replacement name for Teuthis Schneider, 1784 (preoccupied), as used by Naef, 1912.

Acruroteuthis Berry, 1920:67.

Type species: Sepia media Linnaeus, 1758.

Status: = Alloteuthis Wülker, 1920 (fide Naef, 1923:209).

Remarks: Replacement name for Acroteuthis Berry, 1913 (preoccupied), therefore taking the same type species.

Aestuariolus Alexeyev, 1992:21.

Type species: Loliolus noctiluca Lu, Roper, and Tait, 1985.

Status: = Uroteuthis (Photololigo) (fide Vecchione et al., 1998).

Afrololigo Brakoniecki, 1986:92.

Type species: Lolliguncula mercatoris Adam, 1941.

Status: = Lolliguncula (fide Vecchione et al., 1998.

Alloteuthis Wülker, 1920:56.

Type species: Loligo media (Linnaeus, 1758), by monotypy.

Status: Valid loliginid subgenus of Loligo (fide Vecchione et al., 1998).

Remarks: See “Discussion,” below, concerning authorship of this genus.

(Amerigo) Brakoniecki, 1986:106.

Type species: Loligo pealeii Lesueur, 1821, by original designation.

Status: Incertae sedis; possible subgenus of Loligo (see “Discussion”).

Chondrosepia Rüppell and Leuckart, 1828:21.

Type species: Chondrosepia loliginiformis Rüppell and Leuckart, 1828, by monotypy.

Status: = Sepioteuthis Blainville, 1824 (fide Ehrenberg, 1831:[3]).

Doryteuthis Naef, 1912:742.

Type species: Loligo plei Blainville, 1823, by subsequent designation of Grimpe (1920:209).

Status: = Loligo Lamarck, 1798, sensu lato (in part), with unresolved subgeneric status (fide Vecchione et al., 1998).

Heterololigo Natsukari, 1984a:234.

Type species: Loligo bleekeri Keferstein, 1866, by original designation.

Status: Incertae sedis; possible subgenus of Loligo (see “Discussion”).

Loligo Huddesford in Lister, 1770: appendix pl. 9.

Type species: None designated.

Status: Valid loliginid genus (see “Discussion” concerning correct authorship of genus).

Loligo Schneider, 1784:110.

Type species: None; originally published as species (Octopodia Loligo).

Status: = Sepia loligo Linnaeus, 1758 (fide Hemming, 1954).

Remarks: Rejected generic name (ICZN Opinion 233, 1954:291).

Loligo Lamarck, 1798:130.

Type species: Loligo vulgaris Lamarck, 1798, by subsequent designation of Children (1823:254).

Status: See “Discussion.”

Loligopsis Lamarck, 1822:659.

Type species: Loligopsis peronii Lamarck, 1822, by monotypy.

Status: Nomen dubium (fide Berry, 1932:50).

Loliolopsis Berry, 1929:266.

Type species: Loliolopsis chiroctes Berry, 1929; = Loligo diomedeae Hoyle, 1904, by monotypy.

Status: Valid loliginid subgenus of Lolliguncula (fide Vecchione et al., 1998).

Loliolus Steenstrup, 1856:193.

Type species: Loliolus typus Steenstrup, 1856; = Loligo hardwickei Gray, 1849, by original designation.

Status: Valid loliginid genus.

Lolliguncula Steenstrup, 1881:242.

Type species: Loligo brevis Blainville, 1823, by original designation.

Status: Valid loliginid genus.

Naefidium Grimpe, 1920:210.

Type species: Loligo picteti Joubin, 1894, by original designation.

Status: = Idiosepius Steenstrup, 1881 (Idiosepiidae) (fide Sasaki, 1929:132).

Remarks: Originally described as loliginid genus, transferred by Grimpe later in same paper into Idiosepiidae.

Nipponololigo Natsukari, 1983:313.

Type species: Loligo japonica Hoyle, 1885, by original designation.

Status: Valid loliginid subgenus of Loliolus (fide Vecchione et al., 1998).

Photololigo Natsukari, 1984a:230.

Type species: Loligo edulis Hoyle, 1885, by original designation.

Status: Valid loliginid subgenus of Uroteuthis (fide Vecchione et al., 1998).

Pteroteuthis Blainville, 1824:174.

Type species: Loligo vulgaris Lister, 1770 (not Lamarck, 1798), by monotypy.

Status: Nomen dubium; see “Discussion” concerning synonymy.

Pteroteuthis Ehrenberg, 1831:[3].

Type species: Pteroteuthis arabica Ehrenberg, 1831, by monotypy.

Status: = Doryteuthis (fide Naef, 1912:742); = Loligo (fide Natsukari, 1984a:234).

Sepioteuthis Blainville, 1824:175.

Type species: Loligo sepioidea Blainville, 1823, by monotypy.

Status: Valid loliginid genus. Sepioteuthis sepiacea Blainville, 1824, is a lapsus calami for Loligo sepioidea (fide Hoyle, 1910:412).

Teuthis Schneider, 1784:112.

Status: Rejected generic name (ICZN, Opinion 233, 1954:292).

Remarks: Originally published as species (Octopodia Teuthis). Preoccupied in Pisces by Teuthis Linnaeus, 1767.

Uroteuthis Rehder, 1945:21.

Type species: Uroteuthis bartschi Rehder, 1945, by original designation.

Status: Valid loliginid genus.

(Vossia) Alexeyev, 1992:21.

Type species: Loligo (Loligo) vossi Nesis, 1982.

Status: = Uroteuthis (Photololigo) (fide Vecchione et al., 1998).

Nominal Species of Loliginidae

abulati, Lolliguncula Adam, 1955:185, pl. 50: fig. 1.

Status: Valid loliginid species; = Uroteuthis (Photololigo) abulati (fide Vecchione et al., 1998).

aequipoda, Loligo Rüppell, 1844:132.

Status: = Ommatostrephes sagittatus (fide Naef, 1923:445); = Todarodes sagittatus (Lamarck, 1798) (fide Adam, 1939:1), family Ommastrephidae.

affinis, Loligo Lafont, 1871:273, pl. 13.

Status: = Loligo vulgaris Lamarck, 1798 (fide Naef, 1923:197).

affinis, Loliolus Steenstrup, 1856:194, pl. 1: fig. 6.

Status: Valid loliginid species (fide Vecchione et al., 1998).

affinis, Sepia Orbigny, 1826:156.

Status: = Sepioteuthis? sepioidea (Blainville, 1823) (in part) (fide Adam and Rees, 1966:149).

africana, Alloteuthis Adam, 1950:1.

Status: Valid loliginid species; = Loligo (Alloteuthis) africana (fide Vecchione et al., 1998).

alessandrinii, Loligo Verany, 1847:514. Figured in Verany, 1846, [additional] pl. 2: fig. 2.

Status: = Ancistrocheirus alessandrinii (fide Nesis, 1982:173); = Ancistrocheirus lesueuri Orbigny, 1835, in Férussac and Orbigny, 1834–1848 (fide Young et al., 1998), family Ancistrocheiridae.

arabica, Pteroteuthis Ehrenberg, 1831:[3].

Status: Valid loliginid species; = Uroteuthis (Photololigo) arabica (fide Vecchione et al., 1998).

arctipinnis, Sepioteuthis Gould, 1852:479, fig. 593.

Status: = Sepioteuthis lessoniana Lesson, 1830 (in part) (fide Adam, 1939:29).

argus, Lolliguncula Brakoniecki and Roper, 1985:47, figs. 1, 2.

Status: Valid loliginid species with unresolved generic affinity (fide Vecchione et al., 1998).

aspera, Loligo Ortmann, 1888:661, pl. 25.

Status: = Loligo? uyii (fide Nesis, 1987:155); = Loliolus (Nipponololigo) uyii Wakiya and Ishikawa, 1921 (fide Vecchione et al., 1998).

australis, Loligo Gray, 1849:71.

Status: Nomen dubium (fide Lu and Phillips, 1985:28).

australis, Sepioteuthis Quoy and Gaimard, 1832:77, pl. 4: fig. 1.

Status: Valid loliginid species (fide Vecchione et al., 1998).

banksii, Loligo Leach, 1817:141.

Status: = Onychoteuthis banksii (Leach, 1817) (fide Orbigny, 1845:386), family Onychoteuthidae.

bartlingii, Loligo Lesueur, 1821:95, unnumbered plate labeled L. bartlingii.

Status: = Onychoteuthis banksii (Leach, 1817) (fide Orbigny, 1845:386), family Onychoteuthidae.

bartramii, Loligo Lesueur, 1821:90, pl. 7.

Status: = Ommastrephes bartramii (Lesueur, 1821) (fide Orbigny, 1835:55, in 1834–1847), family Ommastrephidae.

bartschi, Uroteuthis Rehder, 1945:22, pl. 3.

Status: Valid loliginid species (fide Vecchione et al., 1998).

beka, Loligo Sasaki, 1929:121, pl. 13.

Status: Valid loliginid species; = Loliolus (Nipponololigo) beka (fide Vecchione et al., 1998).

bengalensis, Loligo Jothinayagam, 1987:48, pl. 3: fig. 17.

Status: Valid loliginid species; = Uroteuthis (Photololigo) bengalensis (fide Vecchione et al., 1998).

berthelotii, Loligo Verany, 1839a:96, pl. 6.

Status: = Loligo vulgaris Lamarck, 1798 (fide Orbigny, 1845:337).

beryllae, Loligo singhalensis Robson, 1928:15, figs. 4–10.

Status: = Photololigo singhalensis (fide Korzun and Alekseev, 1991:26); = Uroteuthis (Photololigo) singhalensis (Ortmann, 1891) (fide Vecchione et al., 1998).

bianconii, Loligo Verany, 1847:514. Figured in Verany, 1846, [additional] pl. 2: fig. 3.

Status: = Onychoteuthis sp. (fide Steenstrup, 1880:100), family Onychoteuthidae.

biangulata, Sepioteuthis Rang, 1837:73, pl. 98.

Status: = Sepioteuthis sepioidea (Blainville, 1823) (fide Adam, 1939:30).

bilineata. Sepia Quoy and Gaimard, 1832:66, pl. 2: fig. 1.

Status: = Sepioteuthis bilineata (fide Orbigny, 1845:300); nomen dubium (fide Lu and Tait, 1983:199).

blainvilliana, Sepioteuthis Ferussac, 1835:303, in Férussac and Orbigny, 1834–1848, Sepioteuthis pl. 2.

Status: = Sepioteuthis, species uncertain (fide Adam, 1939:17).

bleekeri, Loligo Keferstein, 1866:1402, pls. 122, 127.

Status: Valid loliginid species; = Loligo (subgenus undetermined) bleekeri (fide Vecchione et al., 1998).

bomplandii, Loligopsis Verany, 1839b:99, pl. 1.

Status: = Grimalditeuthis bonplandii (Verany, 1839) (fide Pfeffer, 1900:188), family Grimalditeuthidae; now family Chiroteuthidae (fide Young, 1992:181).

borealis (var.), Loligo pealeii Verrill, 1880a:292.

Status: = Loligo pealeii Lesueur, 1821 (fide Cohen, 1976:306).

bouyeri, Loligo Crosse and Fischer, 1862:138.

Status: = ?Architeuthis (fide Gervais, 1875:93).

brasiliensis, Loligo Blainville, 1823:132.

Status: Nomen dubium (fide Brakoniecki, 1984b:436).

Remarks: See sanpaulensis, below.

brasiliensis, Loligo Ferussac, 1823:67?

Status: = Ommastrephes todarus (fide Orbigny, 1845:423); =Todarodes sagittatus (Lamarck, 1798) (fide Steenstrup, 1880:83), family Ommastrephidae.

breviceps, Loligo Steenstrup, 1862:288.

Status: = Loligo vulgaris Lamarck, 1798 (fide Pfeffer, 1908:27).

brevipinna, Loligo Lesueur, 1824:282, pl. 10.

Status: = Lolliguncula brevis Blainville, 1823 (fide Voss, 1956:110).

brevipinnis, Loligo Pfeffer, 1884:5, figs. 4, 4a.

Status: Nomen dubium (fide Nesis, 1987:155).

brevis, Loligo Blainville, 1823:133.

Status: Valid loliginid species; = Lolliguncula brevis (fide Steenstrup, 1881:242).

brevis, Sepioteuthis Owen, 1881:137, pl. 26: fig. 1.

Status: = Sepioteuthis lessoniana Lesson, 1830 (in part) (fide Adam, 1939:29).

brevitentaculata. Loligo Quoy and Gaimard, 1832:81.

Status: = Symplectoteuthis oualaniensis (fide Pfeffer, 1900:180), family Ommastrephidae.

brongnartii, Loligo Blainville, 1823:130.

Status: = Illex illecebrosus (Lesueur, 1821) (fide Pfeffer, 1912:390), family Ommastrephidae.

budo, Loligo Wakiya and Ishikawa, 1921:285, figs. 1, 10.

Status: = Loligo edulis Hoyle, 1885 (fide Sasaki, 1929:107); = Uroteuthis (Photololigo) edulis (fide Vecchione et al, 1998).

buitendijki, Loliolus Grimpe, 1932:471.

Status: = Loliolus typus Steenstrup, 1856 (in part) (fide Grimpe, 1932:471); = Loliolus hardwickei (Gray, 1849) (fide Lu et al, 1985:70).

cardioptera, Loligo Lesueur and Petit, 1807, pl. 30, fig. 5.

Status: = Onykia carriboea Lesueur, 1821 (fide Steenstrup, 1880:96), family Onychoteuthidae.

chinensis, Loligo Gray, 1849:74.

Status: Valid loliginid species; = Uroteuthis (Photololigo) chinensis (fide Vecchione et al, 1998).

chiroctes, Loliolopsis Berry, 1929:267, figs. 1–9, pls. 32, 33.

Status: = Loliolopsis diomedeae (fide Voss, 1971:7); = Lolliguncula (Loliolopsis) diomedeae (Hoyle, 1904) (fide Vecchione et al., 1998).

coindetii, Loligo Verany, 1839a:94, pl. 4.

Status: = Illex coindetii (Verany, 1839) (fide Steenstrup, 1880:82), family Ommastrephidae.

communis (forma), Loligo edulis Sasaki, 1929:109.

Status: Nomen nudum.

corolliflora, Loligo Tilesius, 1831:286, pl. 73: figs. 4–7.

Status: Nomen oblitum (fide Voss, 1965:156).

cranchii, Loligo Blainville, 1823:123.

Status: = Cranchia scabra Leach, 1817 (fide Orbigny, 1845:240), family Cranchiidae.

diomedeae, Loligo Hoyle, 1904:29, pls. 5, 6.

Status: Valid loliginid species; = Loliolopsis diomedeae (fide Voss, 1971:7); = Lolliguncula (Loliolopsis) diomedeae (fide Vecchione et al, 1998).

doreiensis, Sepioteuthis Orbigny, 1835, Sepioteuthis pl. 3: fig. 2, in Ferussac and Orbigny, 1834–1848.

Status: = Sepioteuthis lunulata (fide Orbigny, 1845:323); = Sepioteuthis lessoniana Lesson, 1830 (fide Lu and Tait, 1983:197).

duvaucelii, Loligo Orbigny, 1835:318, Loligo pls. 14, 20, in Ferussac and Orbigny, 1834–1848.

Stanis: Valid loliginid species; = Uroteuthis (Photololigo) duvaucelii (fide Vecchione et al, 1998).

eblanae, Loligo Ball, 1841:364, figs. 1–7.

Status: = Todaropsis eblanae (Ball, 1841) (fide Pfeffer, 1900:179), family Ommastrephidae.

edulis, Loligo Hoyle, 1885b: 186.

Status: Valid loliginid species; = Uroteuthis (Photololigo) edulis (fide Vecchione et al, 1998).

ehrhardti, Sepioteuthis Pfeffer, 1884:3, figs. 1, 1a.

Status: = Sepioteuthis sepioidea (Blainville, 1823) (in part) (fide Adam, 1939:26).

ellipsoptera, Loligopsis Adams and Reeve, 1848:2, pl. 2: fig. 1.

Status: = Leachia cyclura Lesueur, 1821 (in part) (fide Naef, 1923:409), family Cranchiidae.

ellipsura, Loligo Hoyle, 1885b:182.

Status: Nomen dubium (fide Brakoniecki, 1984b:435).

emmakina, Loligo Gray, 1849:71.

Status: = Loligo brasiliensis Blainville, 1823 (fide Nesis, 1982:140); nomen dubium (fide Brakoniecki, 1984b:436).

etheridgei, Loligo Berry, 1918:243, figs. 28–38, pls. 67–69.

Status: = Photololigo chinensis (fide Natsukari, 1984a:232); = Uroteuthis (Photololigo) chinensis (Gray, 1849) (fide Vecchione et al, 1998).

felina, Loligo Blainville, 1823:127.

Status: = Onychoteuthis banksii (Leach, 1817) (fide Steenstrup, 1845:386), family Onychoteuthidae.

forbesii, Loligo Steenstrup, 1856:189, pl. 1: fig. 2.

Status: Valid loliginid species with unresolved generic affinity (fide Vecchione et al, 1998).

formosana, Loligo Sasaki, 1929:109, pl. 30.

Status: = Photololigo chinensis (fide Natsukari, 1984a:232); = Uroteuthis (Photololigo) chinensis (Gray, 1849) (fide Vecchione et al., 1998).

fusus, Loligo Risso, 1854:19, pl. 8.

Status: = Loligo forbesii Steenstrup, 1856 (in part?) (fide Adam, 1942:9, 34).

gahi, Loligo Orbigny, 1835:60, pl. 3: figs. 1, 2, in 1834–1847.

Status: Valid loliginid species; = Loligo (subgenus undetermined) gahi (fide Vecchione et al, 1998).

galatheae, Loligo Hoyle, 1885b: 183.

Status: = Loligo duvaucelii (fide Voss, 1963:71); = Uroteuthis (Photololigo) duvaucelii (Orbigny, 1835, in Ferussac and Orbigny, 1834–1848) (fide Vecchione et al, 1998).

gotoi, Loligo Sasaki, 1929:116, pl. 14.

Status: = Nipponololigo uyii (fide Natsukari, 1983:314); = Loliolus (Nipponololigo) uyii (Wakiya and Ishikawa, 1921) (fide Vecchione et al, 1998).

grandipes (forma), Loligo edulis Sasaki, 1929:109.

Status: = Loligo edulis forma budo (fide Okutani et al, 1987:101); = Uroteuthis (Photololigo) edulis (Hoyle, 1885) (fide Vecchione et al, 1998).

gronovii, Loligo Férussac, 1845:352.

Status: = Ommastrephes gronovii (fide Gray, 1849), family Ommastrephidae; incertae sedis.

guinensis, Sepioteuthis Quoy and Gaimard, 1832:72, pl. 3: figs. 1–7.

Status: = Sepioteuthis lessoniana Lesson, 1830 (in part) (fide Adam, 1939:29).

guttata, Loligopsis Grant, 1833:22, figs. 2–10.

Status: =Leachia cyclura Lesueur, 1821 (fide Pfeffer, 1912:650), family Cranchiidae.

hardwickei, Loligo Gray, 1849:69.

Status: Valid loliginid species; = Loliolus (Loliolus) hardwickei (fide Vecchione et al., 1998).

hartingii, Loligo Verrill, 1875:86, fig. 28.

Status: = Architeuthis hartingii Verrill, 1875 (fide Verrill, 1880b:240), family Architeuthidae.

hemiptera, Loligo Howell, 1867:239, pl. 13.

Status: = Lolliguncula brevis (Blainville, 1823) (fide Voss, 1956:110).

hemprichii, Sepioteuthis Ehrenberg, 1831:[2].

Status: = Sepioteuthis lessoniana Lesson, 1830 (in part) (fide Adam, 1941a: 1).

illecebrosus, Loligo Lesueur, 1821:95, unnumbered pl. labeled L. illecebrosus.

Status: = Illex illecebrosus (Lesueur, 1821) (fide Steenstrup, 1880:82, 90), family Ommastrephidae.

indica, Loligo Pfeffer, 1884:4, figs. 3, 3a.

Status: = Loligo duvaucelii (fide Adam, 1934:7); = Uroteuthis (Photololigo) duvaucelii (Orbigny, 1835, in Férussac and Orbigny, 1834–1848) (fide Vecchione et al., 1998).

indica, Sepioteuthis Goodrich, 1896:5, pl. 1: figs. 9–19.

Status: = Sepioteuthis lessoniana Lesson, 1830 (in part) (fide Adam, 1939:18).

investigatoris, Loliolus Goodrich, 1896:8, pl. 2: figs. 29–37.

Status: = Loliolus hardwickei (Gray, 1849) (fide Lu et al., 1985:70).

japonica, Loligo Hoyle, 1885b: 187.

Status: Valid loliginid species; = Loliolus (Nipponololigo) japonica (fide Vecchione et al., 1998).

kensaki, Loligo Wakiya and Ishikawa, 1921:283, fig. 4, pl. 1: fig. 9.

Status: = Photololigo edulis (fide Natsukari, 1984a:230); =Uroteuthis (Photololigo) edulis (Hoyle, 1885) (fide Vecchione et al., 1998).

kobiensis, Loligo Hoyle, 1885b: 184.

Status: = Nipponololigo sumatrensis (fide Natsukari, 1984b:262); = Loliolus (Nipponololigo) sumatrensis (Orbigny, 1835, in Férussac and Orbigny, 1834–1848) (fide Vecchione et al., 1998).

krempfi, Sepioteuthis Robson, 1928:28, figs. 13–16.

Status: = Sepioteuthis lessoniana Lesson, 1830 (in part) (fide Adam, 1939:21).

laevis, Loligo Blainville, 1823:123.

Status: = Cranchial sp. (fide Steenstrup, 1861:79), family Cranchiidae.

lanceolata, Loligo Rafinesque, 1814:29.

Status: Nomen nudum (fide Hoyle, 1886:31).

laticeps, Loligo Owen, 1836:20.

Status: = Onykia carriboea Lesueur, 1821 (fide Steenstrup, 1880:96), family Onychoteuthidae.

leachii, Loligo Blainville, 1823:124.

Status: = Leachia cyclura Lesueur, 1821 (fide Hoyle, 1885a:326), family Cranchiidae.

lepturo, Loligo Leach, 1817:141.

Status: = Enoploteuthis leptura (Leach, 1817) (fide Orbigny, 1845:399), family Enoploteuthidae.

lessoniana, Sepioteuthis Orbigny, 1826:155.

Status: Nomen nudum.

lessoniana, Sepioteuthis Lesson, 1830:244, pl. 11.

Status: Valid loliginid species (fide Vecchione et al., 1998).

loliginiformis, Chondrosepia Rüppell and Leuckart, 1828: 21, pl. 6.

Status: Valid loliginid species; = Sepioteuthis loliginiformis (fide Ehrenberg, 1831:[3]).

loligo, Sepia Linnaeus, 1758:659.

Status: = Loligo vulgaris Lamarck, 1798 (fide Naef, 1923:197).

Remarks: See “Discussion” concerning suppression in favor of Loligo vulgaris.

lunulata, Sepioteuthis Quoy and Gaimard, 1832:74, pl. 3: figs. 8–13.

Status: = Sepioteuthis lessoniana Lesson, 1830 (fide Adam, 1939:25).

macrophthalma, Loligo Lafont, 1871:274, pl. 15.

Status; Incertae sedis.

madagascariensis, Sepioteuthis Gray, 1849:80.

Status: Nomen dubium (fide Adam, 1939:26).

major, Sepioteuthis Gray, 1828:3, pl. 4: fig. 1.

Status: = Thysanoteuthis rhombus Troschel, 1857 (fide Adam, 1939:26), family Thysanoteuthidae.

malayana, Sepioteuthis Wülker, 1913:478, fig. 7.

Status: = Sepioteuthis lessoniana Lesson, 1830 (fide Sasaki, 1929:127).

marmorae, Loligo Verany, 1839a:95, pl. 5.

Status: = Loligo media (Linnaeus, 1758) (fide Hoyle, 1886:30).

mauritiana, Seploteuthis Quoy and Gaimard, 1832:76, pl. 4: figs. 2–6.

Status: = Sepioteuthis lessoniana Lesson, 1830 (fide Adam, 1939:30).

maxima, Loligo Blainville, 1823:129.

Status: = Ommastrephes? sp. (fide Steenstrup, 1880:105), family Ommastrephidae.

media, Sepla Linnaeus, 1758:659.

Status: Valid loliginid species; = Loligo media (fide Steenstrup, 1862:289); = Loligo (Alloteuthis) media (fide Vecchione et al., 1998).

mediterranea, Loligo Targioni-Tozzetti, 1869:593.

Status: =Loligo vulgaris Lamarck, 1798 (fide Hoyle, 1886:28).

meneghinii, Loligo Verany, 1847:513. Figured in Verany, 1846, [additional] pl. 2: fig. 1.

Status: “Young of a hooked cephalopod” (fide Steenstrup, 1880:99).

mercatoris, Lolliguncula Adam, 1941b:125, figs. 13–18, pl. 3.

Status: Valid loliginid species; = Lolliguncula (Lolliguncula) mercatoris (fide Vecchione et al, 1998).

microcephala, Loligo Lafont, 1871:273, pl. 14.

Status: = Loligo vulgaris Lamarck, 1798 (fide Naef, 1923:197).

minima, Loligo Orbigny, 1835:319, Cranchia pl. 1: figs. 4, 5, in Férussac and Orbigny, 1834–1848.

Status: = Idiosepius minimus (fide Berry, 1932:49), family Idioseplidae.

moulinsi, Loligo Lafont, 1871:274.

Status: = Loligo forbesii Steenstrup, 1856 (fide Naef, 1923:203.

nagasakensis, Loligo edulis Sasaki, 1929:109, fig. 59, pl. 13.

Status: = Loligo edulis (fide Okutani et al, 1987:99); = Uroteuthis (Photololigo) edulis (Hoyle, 1885) (fide Vecchione et al, 1998).

neglecta, Loligo Gray, 1849:72.

Status: = Loligo vulgaris Lamarck, 1798 (fide Hoyle, 1886:28).

neoguinaica, Sepioteuthis Pfeffer, 1884:4, figs. 2, 2a,

Status: = Sepioteuthis lessoniana Lesson, 1830 (fide Adam, 1939:28).

noctiluca, Loliolus Lu, Roper, and Tait, 1985:59, figs. 4–6.

Status: Valid loliginid species; = Uroteuthis (Photololigo) noctiluca (fide Vecchione et al, 1998).

occidentalis, Seploteuthis Robson, 1926:352, figs. 2–5.

Status: = Sepioteuthis sepioidea (Blainville, 1823) (in part) (fide Adam, 1939:30).

ocellata, Loligopsis Owen, 1881:139, pls. 26, 27.

Status: = Histioteuthis species dubia (fide Voss, 1969:856), family Histioteuthidae.

ocula, Loligo Cohen, 1976:330, figs. 15–30.

Status: Valid loliginid species; = Loligo (subgenus undetermined) ocula (fide Vecchione et al, 1998).

odagadium, Loligo Rafinesque, 1814:29.

Status: Nomen nudum (fide Hoyle, 1886:31).

opalescens, Loligo Berry, 1911b:591.

Status: Valid loliginid species; = Loligo (subgenus undetermined) opalescens (fide Vecchione et al, 1998).

oshimai, Loligo Sasaki, 1929:123, pl. 30.

Status: = Photololigo duvauceli (fide Natsukari, 1984a:232); = Uroteuthis (Photololigo) duvaucelii (Orbigny, 1835, in Férussac and Orbigny, 1834–1848) (fide Vecchione et al., 1998).

oualaniensis, Loligo Lesson, 1830:240, pl. 1: fig. 2.

Status: = Sthenoteuthis oualaniensis (Lesson, 1830) (fide Verrill, 1881:387), family Ommastrephidae.

ovata, Sepioteuthis Gabb, 1869:193, pl. 17.

Status: = Sepioteuthis sepioidea (Blainville, 1823) (fide Adam, 1939:30).

Remarks: Date not 1868 as on plate; published February 1869.

pallida, Loligo Verrill, 1874:635, pl. 20: figs. 101, 101a.

Status: = Loligo pealeii Lesueur, 1821 (fide Cohen, 1976:306).

panamensis, Lolliguncula Berry, 1911a: 100, figs. 1–7, pl. 7.

Status: Valid loliginid species; = Lolliguncula (Lolliguncula) panamensis (fide Vecchione et al, 1998).

parva, Loligo Leach, 1817:141.

Status: = Loligo media (Linnaeus, 1758) (fide Hoyle, 1886:30).

Remarks: Pre-Linnaean use by Rondeletius, 1554.

patagonica, Loligo Smith, 1881:24, pl. 3.

Status: = Loligo gahi Orbigny, 1835, in Férussac and Orbigny, 1834–1848 (fide Brakoniecki, 1984b:435).

pavo, Loligo Lesueur, 1821:96, unnumbered pl. labeled L. pavo.

Status: = Taonius pavo (Lesueur, 1821) (fide Steenstrup, 1861:70, 84), family Cranchiidae.

pealeii, Loligo Lesueur, 1821:92, pl. 8.

Status: Valid loliginid species; = Loligo (subgenus undetermined) pealeii (fide Vecchione et al, 1998).

perlatus, Loligopsis Risso, 1854:39, pl. 18: figs. 1, 2.

Status: = Chiroteuthis veranyi (Férussac, 1834) (fide Adam, 1952:111), family Chiroteuthidae.

peronii, Loligopsis Lamarck, 1822:660.

Status: = Idiosepius? (fide Berry, 1932:51), family Idioseplidae?

pfefferi, Loligo Hoyle, 1886:29.

Status: New name for Loligo brevipinnis Pfeffer, 1884. Nomen dubium (fide Nesis, 1987:155).

pickfordi, Doryteuthis Adam, 1954:149, figs. 19–21, pl. 1.

Status: Valid loliginid species with unresolved generic affinity (fide Vecchione et al., 1998).

picteti, Loligo Joubin, 1894:60, pls. 3, 4.

Status: = Idiosepius picteti (Joubin, 1894) (fide Berry, 1932:47), family Idioseplidae.

pillae, Loligo Verany, 1851:112, pl. 36: figs. d–g.

Status: = Illex coindetii (Verany, 1839) (fide Naef, 1923:430), family Ommastrephidae.

pironneauii, Loligo Souleyet, 1852:20, pl. 2: figs. 1–5.

Status: = Ommastrephes bartramii (Lesueur, 1821) (fide Pfeffer, 1912:466), family Ommastrephidae.

piscatorum, Loligo LaPylaie, 1825:319.

Status: = Illex illecebrosus (Lesueur, 1821) (fide Steenstrup, 1880:90), family Ommastrephidae.

plagioptera, Loligo Souleyet, 1852:24, pl. 2: figs. 14–22.

Status: =Onykia carriboea Lesueur, 1821 (fide Clarke, 1966:149), family Onychoteuthidae.

plei, Loligo Blainville, 1823:132.

Status: Valid loliginid species; = Loligo (subgenus undetermined) plei (fide Vecchione et al., 1998).

poeyianus, Loligo Férussac, 1835, pl. 19: figs. 1–3, in Férussac and Orbigny, 1834–1848.

Status: = Loligo brasiliensis Blainville, 1823 (fide Orbigny, 1845:344); nomen dubium (fide Brakoniecki, 1984b:436).

pulchra, Loligo Blainville, 1823:131.

Status: = Loligo vulgaris Lamarck, 1798 (fide Orbigny, 1845:337).

punctata, Loligo DeKay, 1843:3, pl. 1: fig. 1.

Status: = Loligo pealeii Lesueur, 1821 (fide Verrill, 1881:306).

rangii, Loligo Férussac, 1835, pl. 19: figs. 4–6, in Férussac and Orbigny, 1834–1848.

Status: = Loligo vulgaris Lamarck, 1798 (fide Orbigny, 1845:337).

reesi, Doryteuthis Voss, 1962:173.

Status: Valid loliginid species; = Uroteuthis (Photololigo) reesi (fide Vecchione et al., 1998).

reynaudii, Loligo Orbigny, 1841, pl. 24: figs. 1–8, in Férussac and Orbigny, 1834–1848.

Status: = Loligo vulgaris reynaudii (fide Augustyn and Grant, 1988:230).

rhomboidalis, Loliolus Burgess, 1967:319, figs. 1–5.

Status: = Nipponololigo sumatrensis (fide Natsukari, 1984b:262); = Loliolus (Nipponololigo) sumatrensis (Orbigny, 1835, in Férussac and Orbigny, 1834–1848) (fide Vecchione et al., 1998).

robsoni, Photololigo Alexeyev, 1992:13, pl. 1.

Status: Valid loliginid species; = Uroteuthis (Photololigo) robsoni (fide Vecchione et al., 1998).

roperi, Loligo Cohen, 1976:346, figs. 27–30.

Status: Valid loliginid species; = Loligo (subgenus undetermined) roperi (fide Vecchione et al., 1998).

sagittata, Loligo Lamarck, 1798:130.

Status: = Todarodes sagittatus (Lamarck, 1798) (fide Steenstrup, 1880:83), family Ommastrephidae.

sanpaulensis, Loligo Brakoniecki, 1984a: 102, 3 figs.

Status: New name for Loligo brasiliensis Blainville, 1823. Valid loliginid species; = Loligo (subgenus undetermined) sanpaulensis (fide Vecchione et al., 1998).

schneehagenii, Loligopsis Pfeffer, 1884:23, fig. 31.

Status: = Pyrgopsis schneehagenii (fide Pfeffer, 1912:658), family Cranchiidae.

sepiacea, Sepioteuthis Blainville, 1824:175.

Status: Misprint of Loligo sepioidea Blainville, 1823; = Sepioteuthis sepioidea (Blainville, 1823).

sepioidea, Loligo Blainville, 1823:133.

Status: Valid loliginid species; = Sepioteuthis sepioidea (fide Orbigny, 1845:320).

sibogae, Doryteuthis Adam, 1954:146, figs. 16–18, pl. 1.

Status: = Photololigo singhalensis (fide Korzun and Alekseev, 1991:26); = Uroteuthis (Photololigo) singhalensis (Ortmann, 1891) (fide Vecchione et al., 1998).

sicula, Sepioteuthis Verany, 1851:75, pl. 27.

Status: = Chtenopteryx sicula (fide Pfeffer, 1900:172), family Chtenopterygidae.

sieboldi, Sepioteuthis Joubin, 1898:27.

Status: = Sepioteuthis lessoniana Lesson, 1830 (fide Sasaki, 1929:127).

sinensis, Sepioteuthis Orbigny, 1848:304, in Férussac and Orbigny, 1834–1848.

Status: = Sepioteuthis lessoniana Lesson, 1830 (in part) (fide Adam, 1939:29).

singhalensis, Loligo Ortmann, 1891:676, pl. 46: fig. 3a–d.

Status: Valid loliginid species; = Uroteuthis (Photololigo) singhalensis (fide Vecchione et al., 1998).

sloanii, Sepioteuthis Gray, 1849:81.

Status: = Sepioteuthis sepioidea (Blainville, 1823) (in part) (fide Adam, 1939:30).

smythii, Loligo Leach, 1817:141.

Status: = Enoploteuthis leptura (Leach, 1817) (fide Roper, 1966:5), family Enoploteuthidae.

spectrum, Loligo Pfeffer, 1884:5, figs. 5, 5a.

Status: Incertae sedis.

spiralis, Loligo Férussac, 1823:67.

Status: = Loligo media (Linnaeus, 1758) (fide Hoyle, 1886:30).

stearnsii, Loligo Hemphill, 1892:51.

Status: Name suppressed by ICZN (fide Voss, 1974:51).

steenstrupi, Loliolus Dall, 1871:97.

Status: Nomen dubium (fide Lu et al., 1985:78).

subulata, Loligo Lamarck, 1798:130.

Status: Valid loliginid species; = Loligo (Alloteuthis) subulata (fide Vecchione et al, 1998).

sumatrensis, Loligo Orbigny, 1835:317, Loligo pl. 13: figs. 1–3, in Férussac and Orbigny, 1834–1848.

Status: Valid loliginid species; = Loliolus (Nipponololigo) sumatrensis (fide Vecchione et al, 1998).

surinamensis, Loligo Voss, 1974:43, figs. 1–3.

Status: Valid loliginid species; = Loligo (subgenus undetermined) surinamensis (fide Vecchione et al, 1998).

tagoi, Loligo Sasaki, 1929:118, pl. 14.

Status: = Nipponololigo uyii (fide Natsukari, 1983:314); = Loliolus (Nipponololigo) uyii (Wakiya and Ishikawa, 1921) (fide Vecchione et al, 1998).

tetradynamia, Loligo Ortmann, 1888:659, pls. 23, 25.

Status: = Loligo japonica (fide Sasaki, 1929:112); = Loliolus (Nipponololigo) japonica (Hoyle, 1885) (fide Vecchione et al., 1998).

teuthis, Octopodia Schneider, 1784:113 (as Octopodia Teuthis).

Status: Rejected specific name (ICZN, Opinion 233, 1954:291).

Remarks: Replacement name for Sepia media Linnaeus, 1758.

todarus, Loligo Rafinesque, 1814:29.

Status: Nomen nudum.

Remarks: See also Steenstrup, 1880:103.

touchardii, Loligo Souleyet, 1852:22, pl. 2: figs. 6–13.

Status: = Ommastrephes bartramii (Lesueur, 1821) (fide Pfeffer, 1912:466), family Ommastrephidae.

tricarinata, Loligo Gray, 1849:73.

Status: Incertae sedis.

tydeus, Lolliguncula Brakoniecki, 1980:424, figs. 1, 2.

Status: = Lolliguncula panamensis Berry, 1911 (fide Brakoniecki, 1986:47).

typus, Loliolus Steenstrup, 1856:194, pl. 1: fig. 5.

Status: = Loliolus hardwickei (Gray, 1849) (fide Lu et al, 1985:70).

uncinata, Loligo Quoy and Gaimard, 1825:410, pl. 66: fig. 7.

Status: = Onychoteuthis banksii (Leach, 1817) (fide Orbigny, 1845:387), family Onychoteuthidae.

urceolatus, Loligo Risso, 1854:25, pl. 10: figs. 1–4.

Status: = Alloteuthis media (in part) (fide Adam, 1942:10); = Loligo (Alloteuthis) media (Linnaeus, 1758) (fide Vecchione et al, 1998).

uyii, Loligo Wakiya and Ishikawa, 1921:286, fig. 12a–h.

Status: Valid loliginid species; = Loliolus (Nipponololigo) uyii (fide Vecchione et al, 1998).

vanikoriensis, Loligo Quoy and Gaimard, 1832:79, pl. 5: figs. 1, 2.

Status: = Symplectoteuthis oualaniensis (Lesson, 1830) (fide Pfeffer, 1900:180), family Ommastrephidae.

veranyi, Loligopsis Férussac, 1834:355.

Status: = Chiroteuthis veranyi (fide Orbigny, 1845:373), family Chiroteuthidae.

vermicolaris, Loligopsis Rüppell, 1844:133.

Status: = Chiroteuthis veranyi (Férussac, 1834) (fide Naef, 1923:381), family Chiroteuthidae.

vitreus, Loligo Rang, 1837:71, pl. 96.

Status: = Ommastrephes bartramii (Lesueur, 1821) (fide Orbigny, 1845:420), family Ommastrephidae.

vossi, Loligo (Loligo) Nesis, 1982:144.

Status: Valid loliginid species; = Uroteuthis (Photololigo) vossi (fide Vecchione et al., 1998).

vulgaris, Loligo Lamarck, 1798:130.

Status: Valid loliginid species (fide Vecchione et al, 1998).

Remarks: Includes subspecies vulgaris and reynaudi. See comments in “Discussion” concerning Loligo loligo.

yokoyae, Loligo Ishikawa, 1926:30, fig. 1.

Status: = Nipponololigo sumatrensis (fide Natsukari, 1984b:262); = Loliolus (Nipponololigo) sumatrensis (Orbigny, 1835, in Férussac and Orbigny, 1834–1848) (fide Vecchione et al, 1998).

zygaena, Loligopsis Verany, 1847:513. Figured in Verany, 1846, [additional] pl. 1: fig. 2.

Status: Unidentified cranchiid, family Cranchiidae (fide Voss, 1980:403).

Discussion

We encountered numerous problems during this review. A number of taxa above are categorized as incertae sedis. The authors of the paper on loliginid genera (Vecchione et al, 1998) in this work were unable to reach consensus concerning the taxonomic status of some taxa, such as Heterololigo, (Amerigo), and “Lolliguncula” argus. Additional specimen-oriented research is needed to resolve these uncertainties. In reviewing the older literature, other taxa were encountered (e.g., Loligo macrophthalma and Loligo tricarinata) that were properly described according to the International Code of Zoological Nomenclature but, to our knowledge, subsequently have been neither synonymized nor recognized by other authors. These species could prove to be distinct from other species or could be either junior or senior synonyms of currently recognized species.

Some taxa currently considered to be nomina dubia could prove to be valid. For instance, there is a small loliginid, distinct from Loligo gahi, found on the Pacific coast of South America and referred by Nesis (1987) to L. patagonica (= L. gahi according to Brakoniecki, 1984b), but which quite likely is Hoyle's enigmatic species L. ellipsura. On the other hand, the genus Loligopsis is a classic example of a nomen dubium. The type species, L. peronii, was ambiguously described and poorly figured and has been the subject of much speculation (e.g., Berry, 1932). The genus served for years as a “catch-all” name for bizarre squids. Species assigned to Loligopsis by various authors have included idiosepiids, cranchiids, histioteuthids, and chiroteuthids.

Even the establishment of the name of the type species for the type genus, Loligo vulgaris, was not without procedural problems. Lamarck (1798) erected the genus Loligo to distinguish squids from cuttlefishes. The common European squid (“Calmar commun” of Lamarck 1798:130) had been named Sepia loligo by Linneaus in 1758. When he established the genus, Lamarck renamed the species Loligo vulgaris. Therefore, the correct name for the species should have been the new combination, Loligo loligo (Linneaus, 1758). Guerra and Alonso-Zarazaca (1995) applied to the International Commission on Zoological Nomenclature for suppression of Sepia loligo in favor of Loligo vulgaris under Article 79(c) (ICZN, 1985). The opinion rendered by the Commission (ICZN, 1997) included the following. The specific name loligo Linnaeus, 1758, as published in the binomen Sepia loligo, was suppressed for the purposes of the principle of priority but not for those of the principle of homonymy. The name vulgaris Lamarck, 1798, as published in the binomen Loligo vulgaris (specific name of the type species of Loligo Lamarck, 1798), was placed on the Official List of Specific Names in Zoology. Finally, the name loligo Linneaus, 1758, as published in the binomen Sepia loligo and as suppressed above was placed on the Official List of Rejected and Invalid Specific Names in Zoology.

As is true in the systematics of most families, some species names have changed several times. Although the reader can follow these changes through the list of names, two cases warrant special mention because type species for genera were originally designated by junior synonyms. Berry (1929) described a new species that he named chiroctes and erected the genus Loliolopsis because of the distinctiveness of the new species. Voss (1971) recognized that L. chiroctes is a junior synonym of Hoyle's Loligo diomedeae but that Berry was correct in establishing a new genus. Therefore, the type species of Loliolopsis (now a subgenus of Lolliguncula) is Loliolopsis diomedeae (Hoyle, 1904). Similarly, Steenstrup (1856) erected the genus Loliolus for his new species typus. Lu et al. (1985) showed that L. typus is a junior synonym for Loligo hardwickei Gray, 1849, making the latter species the type for the genus Loliolus.

There may be questions about our choice of author for some names. For pre-Linnaean names, such as Loligo parva Rondeletius, 1554, we attempted to find the first author who made the name available by concretely associating the name with a species after 1758. Pre-Linnaean names are included in Naef's (1923) thorough synonymies.

The authorship of Alloteuthis deserves special explanation. Naef (1923) argued that Alloteuthis Naef held priority as a replacement for Acroteuthis (which, in turn, was a replacement name for Teuthis) over Acruroteuthis Berry, October 1920, because of Wülker's use in a May 1920 publication of the name from an unpublished manuscript by Naef. Wülker's use consisted solely of the following line in a species list:

13. Loligo (Alloteuthis NAEF) media L.

According to the ICZN, Article 12(b)(5) (1985:35), for names published before 1931, “in the case of a new genus-group name, the use of one or more available species-group names in combination with it” satisfies the requirement that the new name be accompanied by an “indication.” Thus, Alloteuthis indeed has priority over Acruroteuthis, although Wülker used it parenthetically for Loligo media and included no description, and Naef did not formally publish his name until 1921 (Naef, 1921a). Furthermore, Wülker is the author of the name because it was first published in his paper, even though he credited Naef (F.M. Bayer, Smithsonian Institution, pers. comm., 1990).

The justifications for some synonymies are not completely clear. Apparently Naef (1912) synonymized Pteroteuthis Blainville, 1824, with Doryteuthis Naef, 1912, solely because Ehrenberg's (1831) species arabica was originally described as a Pteroteuthis. Naef did not justify the use of his newer genus name rather than Blainville's older name. The question of priority in this case is somewhat involved. Blainville's description of the genus consisted only of a species listed as follows:

“Pteroteuthis

Ex. Le C. commun. L. vulgaris. Lister,
Anat., t.ix f.1.”

Lister's original publication (1685–1692) did not contain the figure cited by Blainville; however, a later, post-Linnaean edition (Editio altera. Recensuit et indicibus auxit Gulielmus Huddesford) was published in 1770 with additional material. This material included 22 plates with the cited figure within three plates of external and internal anatomy of a squid labeled “Loligo a Sleeve” (i.e., Loligo commonly named “sleeve”). Thus, Blainville's citation of L. vulgaris Lister is incorrect and his Pteroteuthis is a nomen dubium. We therefore believe that Ehrenberg's description of arabica as a Pteroteuthis was the first “indication” fulfilling the requirements of Article 12(b)(5) of the ICZN (1985). Under this interpretation, Pteroteuthis Ehrenberg, 1831, would have priority over Doryteuthis Naef, 1912. As neither name is currently recognized as valid, however, we do not believe it necessary to apply to the Commission for resolution of this matter.

This part of the investigation led us unexpectedly to the revelation that Huddesford's figure, published 28 years prior to Lamarck's establishment of the genus Loligo, fulfills the requirements of the ICZN (1985) under Article 12(b)(7) to make a genus-group name available. Because the 1770 edition uses binomial names, we (Vecchione and Sweeney, 1995) interpreted the name Loligo to be intended as a genus-group name as defined by Article 12 of the ICZN (1985). This would make Loligo Lamarck, 1798, a junior synonym of Loligo Huddesford, 1770, in Lister. Children's (1823) designation of Loligo vulgaris as the type species would still be valid (see Kennard et al., 1931). These circumstances differ from the case, cited above, of the authorship of Alloteuthis because Huddesford actually authored the appendix containing the first “indication” for Loligo, whereas Naef was simply cited by Wülker in his list of names. The Commission, however, disagreed with us (ICZN, 1997) and formalized the authorship of the genus Loligo as follows. The name Loligo Lamarck, 1798 (gender: masculine), type species Loligo vulgaris Lamarck, 1798, by subsequent designation of Children (1823), was placed on the Official List of Generic Names in Zoology.

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Classification of the Enoploteuthidae, Pyroteuthidae, and Ancistrocheiridae

Richard Edward Young, Lourdes Alvina Burgess, Clyde F.E. Roper, Michael J. Sweeney, and Stephen J. Stephen

_______________

Richard Edward Young, Department of Oceanography, University of Hawaii, Honolulu, Hawaii 96822, United States. Lourdes Alvina Burgess, 106 Lexington Court, Red Bank, New Jersey 07701, United States. Clyde F.E. Roper and Michael J. Sweeney, National Museum of Natural History, Smithsonian Institution, Washington, D.C. 20560, United States. Stephen J. Stephen, Inspection Services Branch, 200 Kent Street Station 1100, Ottawa, Ontario, K1A 0E6 Canada.

ABSTRACT

The present status of the systematics of the squid families Enoploteuthidae, Pyroteuthidae, and Ancistrocheiridae is reviewed. The nomenclatural history of higher taxa is given. Diagnoses are presented for families and genera. Species assumed to be valid are listed along with information on type specimens. Data on the general distribution of each species is reviewed.

Introduction

Traditionally, the Enoploteuthidae, Pyroteuthidae, and Ancistrocheiridae have been considered subfamilies of the Enoploteuthidae. Clarke (1988) raised each subfamily to familial status. In this paper we summarize the history and the diagnostic features of these three families and their genera, list the presently accepted species, and annotate their general distribution.

We have introduced one new term, “buccal crown,” in our diagnoses. The buccal crown is composed of the buccal membrane and the buccal supports. Formerly, the term “buccal membrane” referred to the buccal membrane as well as to the combination of buccal membrane and buccal supports.

Distribution records are derived primarily from taxonomic papers where the validity of identifications most often can be confirmed. Our objective is to provide only general information on distributions and not a thorough evaluation of all records. A biogeographical analysis is premature due to considerable taxonomic uncertainty. Where possible we have used only the most recent records; early records can be found in Clarke (1966). More extensive information on distribution can be found in Nesis (1982, 1985a), Starobogatov and Nesis (1983), and in many other untranslated, Russian-language papers. Tsuchiya (1993) provided a careful analysis of the zoogeography of enoploteuthids known to occur in the Northwest Pacific.

MATERIAL AND METHODS

In the three families treated herein, each species that is presumed to be valid is reported in the text along with information on the deposition of type specimens. Type species are given first, and the remaining species in the genus are listed alphabetically. This information is presented as follows:

Primary type (Holotype, Syntype): museum, catalog number, sex, size (as mantle length (ML), gladius length (GL), dorsal mantle length (DML), or ventral mantle length (VML)), collector, locality, date of collection, and condition of specimen(s). The same sequence of information is listed for secondary types.

A list of the acronyms used to designate museums where types are deposited is as follows:

AMS

Australian Museum, P.O. Box A285, Sydney South, New South Wales 2000, Australia

BMNH

The Natural History Museum, Cromwell Road, London SW7 5BD, England

CASIZ

California Academy of Sciences, Golden Gate Park, San Francisco, California 94118, United States

FMT

Taiwan Provincial Museum, 2 Siangyang Road, Taipei, Taiwan

IMC

Zoological Museum Calcutta, Indian Museum, 27 Jawaharlal Nehru Road, Calcutta 700016, India

IOS

Institute of Oceanographic Sciences, Brook Road, Wormley, Godalming, Surrey GU8 5UB, England

IRSNB

Institut Royal des Sciences Naturelles de Belgique, Rue Vautier 29, B-1040 Brussels, Belgium (formerly Musée Royal d'Histoire Naturelle de Belgique)

MCZ

Museum of Comparative Zoology, Harvard University, Cambridge, Massachusetts 02138, United States

MNHN

Museum National d'Histoire Naturelle, 55, rue de Buffon, 75005 Paris 05, France

MSUT

Museum of the Science College, University of Tokyo, Hongo 7-3-1, Bunkyo-ku, Tokyo 113, Japan

NMNZ

National Museum of New Zealand, P.O. Box 467, Wellington, New Zealand (formerly Dominion Museum)

NMW

Naturhistorisches Museum, Burgring 7, Postfach 417, A-1014 Vienna, Austria

NSMT

National Science Museum, 3-23-1 Hyakunin-cho, Shinjukuku, Tokyo 169, Japan

ORSTOM

Centre O.R.S.T.O.M., B.P. A 5, Noumea-Cedex, New Caledonia

SBMNH

Santa Barbara Museum of Natural History, 2559 Puesta del Sol Road, Santa Barbara, California 93105, United States

SFI

Morski Instytut Rybacki (Sea Fisheries Institute), Aleja Zjednoczenia 1, 81–345 Gdynia, Poland

SIO

Scripps Institution of Oceanography, Marine Invertebrate Collection, University of California, La Jolla, California 92093, United States

UMML

Marine Invertebrate Museum, University of Miami, 4600 Rickenbacker Cswy., Miami, Florida 33149, United States

USNM

National Museum of Natural History (collections of the former United States National Museum), Smithsonian Institution, 10th and Constitution Ave. N.W., Washington, D.C. 20560, United States

ZMB

Zoologisches Museum, Museum fur Naturkunde der Humboldt-Universitat, Invalidenstrasse 43, D-1040 Berlin, Germany

ZMH

Zoologisches Museum, Universitat Hamburg, Martin Luther King Platz 3, 2000 Hamburg 13, Germany

ZMUC

Zoologisk Museum, Universitetsparken 15, DK 2100 Kobenhavn, Denmark

A number of obscure species have been described in the families treated herein that were later synonymized or were treated as though they had been synonymized. In the latter case, they have not been treated since their original description. Both groups are listed herein with their synonymies when known. The status of some of these species probably will never be resolved as they are based on paralarval forms or on poor descriptions; frequently, the types no longer are extant (e.g., many of the species described by Pfeffer in 1912). We encourage future researchers to resolve these names rather than overlook them as has been the tendency in the past.

Abralia megalops Verrill, 1882:364.

= Thelidioteuthis alessandrini (Verany, 1847) (fide Sasaki, 1929:253).

= Ancistrocheirus lesueurii (Orbigny, 1842), herein.

Enoploteuthis pallida Pfeffer, 1884:18, fig. 23.

= Thelidioteuthis alessandrini (fide Sasaki, 1929:253).

= Ancistrocheirus lesueurii, herein.

Ancistrocheirus megaptera Verrill, 1885:399, pl. 42.

= Octopoteuthis megaptera (Verrill, 1885) (fide Voss, 1956:125).

Compsoteuthis lonnbergi Pfeffer, 1900:167.

= Abraliopsis morisii (Verany, 1839) (fide Naef, 1916:18).

Abralia (Prodromoteuthis) isseli Pfeffer, 1912:165.

Synonymy uncertain.

Abralia (Nepioteuthion) mediterranea Pfeffer, 1912:149, pl. 15: figs. 5–7.

= Abraliopsis morisii (fide Naef, 1916:18).

Abralia (Compsoteuthis) jattai Pfeffer, 1912:150.

= Abraliopsis morisii (fide Naef, 1916:18).

Abralia (Compsoteuthis) nishikawae Pfeffer, 1912:162.

= Watasenia scintillans (Berry, 1911) (fide Sasaki, 1929:249).

Abralia (Nepioteuthion) lonnbergi Pfeffer, 1912:150, pl. 15: figs. 1–4.

= Abraliopsis morisii (fide Naef, 1916:18).

Abralia (Nepioteuthion) nishikawae Pfeffer, 1912:149.

= Watasenia scintillans (fide Sasaki, 1929:249).

Abralia (Nepioteuthion) panamensis Pfeffer, 1912:150.

Synonymy uncertain.

Enoploion eustictum Pfeffer, 1912:170, pl. 15: figs. 15, 16.

= Abralia veranyi (Rüppell, 1844) (fide Nesis, 1982:178).

Asthenoteuthion planctonicum, Pfeffer, 1912:172, pl. 15: figs. 8–14.

= Lycoteuthis diadema (Chun, 1900) (fide Voss, 1959:374).

= Lycoteuthis lorigera (Steenstrup, 1875) (fide Villanueva and Sanchez, 1993:31).

Pyroteuthis (Pterygonepion) mediterranea Pfeffer, 1912:193.

= Pyroteuthis margaritifera (Rüppell, 1844) (fide Naef, 1916:17).

Pyroteuthis (Pterygonepion) planctonica Pfeffer, 1912:210, pl. 19: figs. 33, 34.

Synonymy uncertain.

Pyroteuthis (Pterygonepion) atlantica Pfeffer, 1912:193.

Synonymy uncertain.

Pyroteuthis (Pyroteuthis) margaritifera oceanica Pfeffer, 1912:211.

Synonymy uncertain.

Pyroteuthis (Pterygioteuthis) giardi hoylei Pfeffer, 1912:206.

Synonymy uncertain.

Pyroteuthis (Ioteuthion) schnehageni Pfeffer, 1912:209, pl. 19: figs. 31, 32.

Synonymy uncertain.

Carybditeuthis maculata Vivanti, 1912:91, figs. 1–5.

= Pyroteuthis margaritifera (fide Naef, 1921:269).

Pyroteuthis margaritifera aurantiacus Joubin, 1924:52, pl. 10.

= Pyroteuthis margaritifera (fide Voss in Young, 1972:24).

Historical Review of Higher Taxa

The first species described in what now is the Enoploteuthidae was Loligo lepturo Leach, 1817, from the Gulf of Guinea, eastern Atlantic. This species was subsequently designated the type species of Enoploteuthis Orbigny in Rüppell, 1844. In 1832 Quoy and Gaimard described Onychoteuthis armata from the Moluccas Islands, Indian Ocean, and in 1849 Gray erected the genus Abralia for this species. Onychoteuthis morisii was named by Verany in 1839 (the oldest species in Abraliopsis) from off the Azores, eastern North Atlantic; it was placed in Abralia by Gray, 1849, and much later was placed in Abraliopsis Joubin, 1896, by Pfeffer (1908). Joubin (1896) erected Abraliopsis for his new species Abraliopsis pfefferi and included with it Enoploteuthis hoylei Pfeffer, 1884. In 1844 Rüppell described Enoploteuthis veranyi and Enoploteuthis margaritifera from off Messina, Mediterranean Sea. Enoploteuthis veranyi was placed in Abralia by Pfeffer (1908), and E. margaritifera was placed in Pterygioteuthis Fischer, 1896 (actual publication date of the paper was 1 September 1896; not 1895 as indicated on the journal), by Pfeffer in 1900 and, subsequently, was designated by Hoyle (1904) as the type species of Pyroteuthis Hoyle, 1904. Orbigny described Enoploteuthis lesueurii in 1842 (in Férussac and Orbigny, 1834–1848) (date of “Onychoteuthis” pl. 14, on which E. lesueurii was based, is 1839–1842, species description published in 1848:339; see Bello, 1992; Tillier and Boucher-Rodoni, 1993) from the Indian Ocean, and Gray (1849) designated it the type species of his genus Ancistrocheirus. In 1851 Verany described Loligo alessandrinii from off Messina, Mediterranean Sea; it was first placed in Calliteuthis Verrill, 1880, by Appellöf (1890), then, in 1900, placed by Pfeffer in his new genus Thelidioteuthis. Subsequently, Thelidioteuthis was synonymized with Ancistrocheirus (Nesis, 1978).

The familial placement of these first-named species in the enoploteuthid complex generally associated them with the Onychoteuthidae Gray, 1847, the designation for all the hooked forms. The correct publication date for Onychoteuthidae Gray is 1847:206, when a clear concept of the family based on Onychoteuthis and other included genera appeared. Description of the familial characters did not appear until 1849 (Gray, 1849:45) (see International Code of Zoological Nomenclature (ICZN), 1985, Article 11(f)). The Onychoteuthidae frequently was referred to as a subfamily of the family Onychii Steenstrup, 1861. These familial designations continued throughout the 19th century.

Pfeffer (1900) introduced a classification of the Oegopsida in which he was able to subdivide the few large “families” of earlier authors into a more natural, manageable scheme that forms the basis of modern familial nomenclature. In all, Pfeffer (1900) presented 12 families, among them the Enoploteuthidae (new family) and the Onychoteuthidae Gray, 1847. These replaced Steenstrup's improperly named family, Onychii. Pfeffer suggested that the genera in the Enoploteuthidae may eventually separate into five subfamilies, but, although he listed the generic groups, he did not give them formal status. In that paper, he described a new genus and species of onychoteuthid, Lycoteuthis jattai. Chun, also in 1900, described a new species, Enoploteuthis diadema, and in 1903 (Chun, 1903a) placed the species in Pfeffer's genus Lycoteuthis. Later in the same year, however, Chun (1903b) changed his opinion and created a new genus, Thaumatolampas, for his species and placed it in a new family, Thaumatolampadidae.

In 1908 Pfeffer established the subfamily Lycoteuthinae within the family Onychoteuthidae for his genus Lycoteuthis and asserted that Thaumatolampas diadema (Chun, 1900) was a synonym of L. jattai Pfeffer, 1900.

In 1908 Chun moved his Thaumatolampadidae into the Enoploteuthidae and placed the remaining species into two tribes, Enoplomorphae and Pterygiomorphae. The latter tribe included Pterygioteuthis and Pyroteuthis. In 1910 Chun clarified this arrangement as follows:

Family ENOPLOTEUTHIDAE

Subfamily THAUMATOLAMPADINAE

Genus Thaumatolampas

Species Thaumatolampas diadema (Lycoteuthis jattai listed as a questionable junior synonym)

Subfamily ENOPLOTEUTHINAE

Tribe Enoplomorphae

Genera Abralia, Abraliopsis, Enoploteuthis, Ancistrocheirus (his Ancistrocheirus and Thelidioteuthis)

Tribe Pterygiomorphae

Genera Pterygioteuthis, Pyroteuthis

Pterygiomorphae (Chun, 1908) is the first designation of a suprageneric group to include Pterygioteuthis and Pyroteuthis. The name Pterygiomorphae, however, has no nomenclatural standing because familial and subfamilial names must be based on a valid genus and there is no genus Pterygiomorpha.

In his 1912 monograph, Pfeffer maintained the Lycoteuthinae as a subfamily of the Onychoteuthidae and placed his species, Lycoteuthis jattai, as a junior synonym of Chun's Thaumatolampas diadema, but he maintained the genus Lycoteuthis over Thaumatolampas. In that study, Pfeffer formalized some of his earlier suspicions by dividing the Enoploteuthidae into four subfamilies as follows:

Family ENOPLOTEUTHIDAE

Subfamily ENOPLOTEUTHINAE

Genera Enoploteuthis, Abralia (his Asteroteuthis), Abraliopsis (his Abralia)

Subfamily ANCISTROCHEIRINAE

Genera Ancistrocheirus (his Ancistrocheirus and Thelidioteuthis)

Subfamily PYROTEUTHINAE

Genus Pyroteuthis (he considered Pterygioteuthis as a subgenus along with several other subgenera based on paralarvae)

Subfamily OCTOPOTEUTHINAE

Genus Octopoteuthis (his Octopodoteuthis and Octopodoteuthopsis) and Taningia (his Cucioteuthis)

Berry (1913a) described Nematolampas regalis and by inference related it to Thaumatolampas diadema and Lycoteuthis jattai but gave no familial designation. Then, in 1914, Berry (1914a) adopted Pfeffer's use of Lycoteuthis and Lycoteuthinae and elevated the Lycoteuthinae to familial status, separate from the Enoploteuthidae. Voss (1962a:267) analyzed the nomenclatural history of the Lycoteuthidae and concluded that the name Thaumatolampadidae should be dropped due to its long, continuous disuse, in spite of “possible claims to priority.” In order to establish the Lycoteuthidae as the accepted name, we will apply to the ICZN for official suppression of the names Thaumatolampadidae and Thaumatolampadinae. Under the rules of the ICZN, when a case is pending the current usage of the name under discussion prevails. Therefore, Lycoteuthidae Pfeffer, 1908, is the correct current usage.

In 1911 Berry described Abraliopsis scintillans from Japanese waters; Ishikawa (1913) later placed it in the genus Watasea. Watasea, however, was preoccupied by a fish name, and Ishikawa (1914a) proposed the replacement name Watasenia.

Naef's 1921 influential study on cephalopod systematics and evolution divided the Enoploteuthidae into the Pyroteuthinae, Enoploteuthinae, and Lycoteuthinae, which was in basic agreement with Chun's classification.

The classification proposed by Thiele (1935) maintained Lycoteuthidae as a separate family and listed four subfamilies under Enoploteuthidae, including the Abraliinae. Thiele did not provide authors or dates for his suprageneric taxa.

Family ENOPLOTEUTHIDAE

Subfamily ABRALIINAE

Genera Abralia, Abraliopsis, Watasenia

Subfamily ENOPLOTEUTHINAE

Genus Enoploteuthis

Subfamily ANCISTROCHEIRINAE

Genus Ancistrocheirus (his Ancistrocheirus and Thelidioteuthis)

Subfamily PYROTEUTHINAE

Genera Pyroteuthis, Pterygioteuthis

More recently, the Enoploteuthidae has been considered to be composed of three subfamilies, Enoploteuthinae, Ancistrocheirinae, and Pyroteuthinae (Roper et al., 1969; Voss, 1977). In 1988 Clarke raised all three subfamilies to the family level. This change has been supported by Young and Harman (1998).

Classification

ENOPLOTEUTHIDAE Pfeffer, 1900

TYPE GENUS.—Enoploteuthis Orbigny in Rüppell, 1844.

DIAGNOSIS.—Buccal crown with 8 supports. Buccal connectives attached to dorsal margins of arms IV. No secondary buccal connectives attached to ventral margins of arms I and II. Gladius with small, blunt conus and elongate cone field; rostrum absent. Hooks present on all arms; tentacular clubs with 1 or 2 series of hooks on manus (arrangement varies with genus); armature on manus in 2 or 3 series. Photophores present on mantle, funnel, head, eyeballs, and arms. Photophores absent from tentacles, viscera, and most of fins. Nidamental glands absent; oviducal glands enlarged. Oviducts unpaired. Fins usually terminal; always lacking posterior lobes. Tail fleshy, extending well beyond conus of gladius; vesicles present. Nuchal folds present. Tentacle not modified near base; stalk “ligament” and vein leave tentacle at base in membrane. Ink sac not embedded in digestive gland.

Enoploteuthis Orbigny in Rüppell, 1844

TYPE SPECIES.—Loligo lepturo Leach, 1817, by subsequent designation (Pfeffer, 1900).

DIAGNOSIS.—Manus of club with 2 series of hooks, marginal suckers absent. No enlarged photophores at tips of arms IV. Fins subterminal. Buccal crown with typical chromatophores on aboral surface, possibly with light epithelial pigmentation on oral surface (needs confirmation). Nine to 10 photophores on eyeball. Right arm IV hectocotylized. Suckers present distally on arms IV. Spermatophore receptacles at posterior junction of retractor muscles of funnel and head. Complex photophores of integument, in life, without red color filters. Radula with heterodont rhachidian tooth. Large arm hooks with open apertures.

COMMENTS.—No species of Enoploteuthis has been recorded from the Mediterranean Sea (Mangold and Boletzky, 1988).

Enoploteuthis leptura (Leach, 1817)

ORIGINAL REFERENCE.—Loligo lepturo Leach, 1817:141.

DEPOSITION OF TYPES.—Holotype: BMNH 1993017, female, 25 mm ML, J. Cranch Congo Expedition, Gulf of Guinea, 01°08′N, 07°26′30″E, condition unknown.

Paratypes: Undetermined.

GEOGRAPHICAL DISTRIBUTION.—Central Atlantic (Roper, 1966; Nesis, 1974; Cairns, 1976; Stephen, 1982); Pacific (Nesis, 1982; Tsuchiya, 1993); Indian Ocean (Tsuchiya, 1993).

COMMENTS.—This species was illustrated by Leach (1918). Loligo smythii Leach, 1817, is a synonym (Roper, 1966). Nesis (1982) suggested that the illustrations, pl. 6, pl. 11: figs. 6–14, and pl. 12: figs. 10–24, of E. leptura by Orbigny (in Férussac and Orbigny, 1834–1848) from the Pacific Ocean (exact locality unknown) represent a new subspecies, E. I. magnoceani, which is supported by his own catches from the Indian Ocean and western and central Pacific Ocean. Tsuchiya (1993) agrees with this conclusion.

Enoploteuthis anapsis Roper, 1964

ORIGINAL REFERENCE.—Enoploteuthis anapsis Roper, 1964:140, figs. 1, 2.

DEPOSITION OF TYPES.—Holotype: USNM 575605, female, 68 mm ML, R/V Oregon sta 1887, Caribbean Sea, 16°55′N, 81°10′W, 23 Aug 1957, good condition.

Paratypes: BMNH 1958.12.30.22, female, 76 mm ML, Madeira, date unknown, condition unknown. BMNH 1958.12.30.23, female, 69 mm ML, Madeira, 1 Jun 1946, condition unknown. USNM 576155, female, 27 mm ML, R/V Dana sta 1292-V, Caribbean Sea, 17°43′N, 64°56′W, 16 Apr 1922, good condition. USNM 576606, female, 73 mm ML, R/V Oregon sta unknown, Gulf of Mexico, date unknown, good condition. UMML 31.237, female, 29 mm ML, R/V Gerda, Caribbean Sea, 16°55′N, 74°16′W, 10 May 1959, good condition. ZMUC, 2 females, 11 mm ML, 16 mm ML, R/V Dana sta 1168-V, Atlantic, 9°30′N, 42°41′W, 12 Nov 1921, good condition. ZMUC, female, 10 mm ML, R/V Dana sta 1180-II, Atlantic, 12°11′N, 57°12′W, 20 Nov 1921, good condition. ZMUC, female, 9 mm ML, R/V Dana sta 1202-IV, Atlantic, 9°40′N, 79°56′W, 10 Jan 1922, good condition. ZMUC, female, 14 mm ML, R/V Dana sta 1238-III, Atlantic, 26°13′N, 78°48′W, 11 Feb 1922, good condition. ZMUC, female, 13 mm ML, R/V Dana sta 1247-IV, Atlantic, 17°57′N, 72°51′W, 20 Feb 1922, good condition. ZMUC, female, 13 mm ML, R/V Dana sta 1269-II, Atlantic, 17°13′N, 64°58′W, 15 Mar 1922, good condition. ZMUC, female, 13 mm ML, R/V Dana sta 1287-III, Atlantic, 16°04′N, 61°52′W, 8 Apr 1922, good condition. IOS, 2 males, 54 mm ML, 79 mm ML, Discovery sta 4743, Atlantic, 32°34′N, 16°45′W, 20 Sep 1961, condition unknown.

GEOGRAPHICAL DISTRIBUTION.—Central Atlantic (Roper, 1966; Nesis, 1974; Cairns, 1976; Stephen, 1982).

Enoploteuthis chunii Ishikawa, 1914

ORIGINAL REFERENCE.—Enoploteuthis chunii Ishikawa, 1914b:401, pls. 38, 39.

DEPOSITION OF TYPES.—Syntypes: ?MSUT, 5 specimens, sex undetermined, 68 mm ML, 70 mm ML, 72 mm ML, 75 mm ML, 90 mm ML, Toyama Bay, Etchu Province, Japan, condition unknown.

GEOGRAPHICAL DISTRIBUTION.—Waters off Japan (Sasaki, 1929; Okutani, 1967; Okutani et al., 1987; Tsuchiya, 1993).

COMMENTS.—Enoploteuthis theragrae Taki, 1964, has been placed in the synonymy of E. chunii (Nesis, 1982; Tsuchiya and Okutani, 1988). Tsuchiya (1993) considers this to be a mesopelagic-boundary species.

Enoploteuthis galaxias Berry, 1918

ORIGINAL REFERENCE.—Enoploteuthis galaxias Berry, 1918:211, figs. 1–4, pls. 59, 60.

DEPOSITION OF TYPES.—Holotype: AMS C148251, female, 72 mm ML, F.I.S. Endeavour no. 5273, Gabo Island to Everard Grounds, Tasman Sea, Australia, Oct 1914.

Paratypes: USNM, 816352, male, 73 mm ML, same lot as holotype, good condition. USNM 816355, female, 78 mm ML, same lot as holotype, specimen completely dissected by Berry.

GEOGRAPHICAL DISTRIBUTION.—Off eastern Australia and New Zealand (Riddell, 1985).

COMMENTS.—Riddell (1985) suggests that this species is associated with the continental shelf (i.e., a mesopelagic-boundary species; see Reid et al., 1991).

Enoploteuthis higginsi Burgess, 1982

ORIGINAL REFERENCE.—Enoploteuthis higginsi Burgess, 1982:718, figs. 2E,G, 5.

DEPOSITION OF TYPES.—Holotype: USNM 729710, male, 37 mm ML, R/V Teritu sta 6, off Waianae, Oahu Island, Hawaiian Islands, Sep 1969, good condition.

Paratypes: USNM 729714, male, 35 mm ML, R/V Charles H. Gilbert sta 89-11, central Pacific, 06°04′S, 157°36′W, 2 Feb 1966, good condition. USNM 729723, female, 53 mm ML, R/V Townsend Cromwell sta 32-22, central Pacific, 21°02′N, 158°29′W, 21 Jul 1967, good condition. USNM 577609, female, 45 mm ML, R/V Townsend Cromwell sta 32-56, central Pacific, 21°22′N, 158°14′W, 23 Aug 1967, good condition.

GEOGRAPHICAL DISTRIBUTION.—Hawaiian waters and equatorial region of the central Pacific (Burgess, 1982); Indian Ocean (Tsuchiya, 1993).

Enoploteuthis jonesi Burgess, 1982

ORIGINAL REFERENCE.—Enoploteuthis jonesi Burgess, 1982:713, figs. 2D,F, 4.

DEPOSITION OF TYPES.—Holotype: USNM 729717, male, 47 mm ML, R/V Townsend Cromwell sta 7–12, off Milolii, Hawaii, 16 Aug 1964, good condition.

Paratypes: USNM 729699, male, 35 mm ML, R/V Charles H. Gilbert sta 89-24, central Pacific, 14°55′S, 164°02′W, 10 Feb 1966, good condition. USNM 577608, female, 82 mm ML, same lot as holotype, good condition. USNM 729707, female, 40 mm ML, R/V Townsend Cromwell sta 32-28, Hawaiian Islands, 20°58′N, 158°33′W, 25 Jul 1967, good condition.

GEOGRAPHICAL DISTRIBUTION.—Hawaiian waters and equatorial region of the central Pacific (Burgess, 1982).

COMMENTS.—Nesis (1982) considers E. jonesi to be a subspecies of E. anapsis.

Enoploteuthis obliqua Burgess, 1982

ORIGINAL REFERENCE.—Enoploteuthis obliqua Burgess, 1982:704, figs. 1, 2A.

DEPOSITION OF TYPES.—Holotype: USNM 729722, male, 55 mm ML, R/V Townsend Cromwell sta 48–11, central Pacific, 11°47′N, 144°47′W, 31 Mar 1970, good condition.

Paratypes: USNM 577605, female, 50 mm ML, R/V Townsend Cromwell sta 46–9, central Pacific, 11°49′N, 144°51′W, 14 Oct 1969, good condition. USNM 729713, male, 41 mm ML, same lot as preceding, good condition. USNM 729688, male, 58 mm ML, R/V Townsend Cromwell sta 48–19, central Pacific, 11°34′N, 144°54′W, 3 Apr 1970, good condition.

GEOGRAPHICAL DISTRIBUTION.—Equatorial regions of the central and eastern Pacific (Burgess, 1982; Okutani and Tsukada, 1988).

Enoploteuthis octolineata Burgess, 1982

ORIGINAL REFERENCE.—Enoploteuthis octolineata Burgess, 1982:708, figs. 2C, 3.

DEPOSITION OF TYPES.—Holotype: USNM 577607, female, 71 mm ML, R/V Hugh M. Smith sta 47–58, central Pacific, 02°56′N, 150°03′W, 4 Nov 1958, good condition.

Paratypes: USNM 729721, female, 75 mm ML, R/V Townsend Cromwell sta 43–52, central Pacific, 00°01′N, 145°03′W, 28 May 1969, good condition. USNM 729720, female, 56 mm ML, R/V Townsend Cromwell sta 46–37, central Pacific, 03°23′N, 145°04′W, 26 Oct 1969, good condition. USNM 729708, male, 46 mm ML, R/V Townsend Cromwell sta 48–50, central Pacific, 03°29′N, 144°58′W, 17 Apr 1970, good condition.

GEOGRAPHICAL DISTRIBUTION.—Equatorial region of the central Pacific (Burgess, 1982).

Enoploteuthis reticulata Rancurel, 1970

ORIGINAL REFERENCE.—Enoploteuthis reticulata Rancurel, 1970:45, figs. 31–37.

DEPOSITION OF TYPES.—Syntypes: Depository unknown, ?ORSTOM, 17 specimens, New Caledonia and central South Pacific, 0°02′S, 135°48′W; 0°02′S, 135°14′W; 0°15′S, 144°07′W (from Alepisaurus ferox stomachs), condition unknown.

GEOGRAPHICAL DISTRIBUTION.—Pacific from 28°N to 28°S and from 164°E to 126°W (Burgess, 1982; Riddell, 1985); Indian Ocean (Okutani and Tsukada, 1988); pantropical to subtropical Indo-Pacific (Tsuchiya, 1993).

Abralia Gray, 1849

TYPE SPECIES.—Onychoteuthis armata Quoy and Gaimard, 1832, by indication.

DIAGNOSIS.—Manus of club with 1 series of hooks, 2 series of suckers. Enlarged photophores on tips of arms IV generally absent; when present, photophores not covered by black chromatophores. Fins terminal. Buccal crown with typical chromatophores on aboral surfaces, no other pigmentation present (needs confirmation). Five to 12 photophores on eyeball. Right or left arm IV hectocotylized. Suckers present distally on arms IV. Spermatophore receptacle(s) located under collar, in median pocket at posterior end of nuchal cartilage, or between stellate ganglia. Complex photophores of integument, in life, without red color filters. Radula with homodont teeth. Large arm hooks with apertures closed.

Abralia armata (Quoy and Gaimard, 1832)

ORIGINAL REFERENCE.—Onychoteuthis armatus Quoy and Gaimard, 1832:84, pl. 5: figs. 14–22.

DEPOSITION OF TYPES.—Holotype: MNHN 2–14–1943 (gladius 2–14–607), sex undetermined, 13 mm GL, Quoy and Gaimard, Molucca Sea, near Celebes Island, 1829, dried out. See Pfeffer (1912:763) for discussion of type.

Paratypes: None.

GEOGRAPHICAL DISTRIBUTION.—Indonesia; Philippines (Casto de Elera, 1896; Voss, 1963).

COMMENTS.—Abralia armata of Voss, 1963, is a synonym of A. spaercki Grimpe, 1931 (see Tsuchiya and Okutani, 1988).

Abralia andamanica Goodrich, 1896

ORIGINAL REFERENCE.—Abralia andamanica Goodrich, 1896:9, pl. 2: figs. 38–45.

DEPOSITION OF TYPES.—Syntypes: IMC M539/1, female, 38 mm VML (40 mm DML), R/V Investigator sta 224, Andaman Sea, 14°54′30″N, 96°13′E, 23 Feb 1897, “not very good condition” (Massy, 1916:239). IMC M9321/2, male, 24 mm DML, R/V Investigator sta 590, Mergui Archipeligo, Andaman Sea, condition unknown. IMC M9320/2, female, 35 mm ML, same as preceding lot, condition unknown.

GEOGRAPHICAL DISTRIBUTION.—Northeast Indian Ocean; Philippines (Voss, 1963); off Japan (Sasaki, 1929; Kubota et al., 1982; Okutani et al., 1987; Tsuchiya, 1993); eastern tropical Pacific (Okutani, 1974); off southern Japan to Tasman Sea (Nesis and Nikitina, 1987).

COMMENTS.—Tsuchiya (1993) considers this to be a mesopelagic-boundary species. This may be a species complex (see Burgess, 1992).

Abralia astrolineata Berry, 1914

ORIGINAL REFERENCE.—Abralia astrolineata Berry, 1914a:145, pl. 10: figs. 1, 2.

DEPOSITION OF TYPES.—Holotype: USNM 816428, female, 34 mm ML, R.S. Bell, on beach of Sunday Island, Kermadec Islands, dried and in poor condition.

Paratypes: None.

GEOGRAPHICAL DISTRIBUTION.—Off Kermadec Islands (Riddell, 1985).

COMMENTS.—Data of Riddell (1985) indicate that this is a mesopelagic-boundary species.

Abralia astrosticta Berry, 1909

ORIGINAL REFERENCE.—Abralia astrosticta Berry, 1909:412, figs. 4–7.

DEPOSITION OF TYPES.—Holotype: USNM 214313, female, 34 mm ML, R/V Albatross sta 4122, off Oahu Island, Hawaiian Islands, 26 Jul 1902, dried and in very poor condition.

Paratypes: None.

GEOGRAPHICAL DISTRIBUTION.—Hawaiian Islands (Burgess, 1992); Marshall Islands (Voss, 1954; Burgess, 1992); (?) off eastern Australian coast (Allan, 1945); Philippine Sea, Kuroshio (Japan Current) (Nesis, 1982; Nesis and Nikitina, 1987); off Japan (Tsuchiya and Okutani, 1988; Tsuchiya, 1993).

COMMENTS.—A specimen of this species was described (USNM 587132) from the Marshall Islands by Voss in Burgess (1992). Reid et al. (1991) found this to be a mesopelagic-boundary species.

Abralia dubia (Adam, 1960)

ORIGINAL REFERENCE.—Enoploteuthis dubia Adam, 1960:12, figs. 2a–d.

DEPOSITION OF TYPES.—Holotype: IRSNB, male 36 mm ML, Ch. Lewinsohn sta NS195, Eilat, Red Sea, May 1955, condition unknown.

Paratypes: None.

GEOGRAPHICAL DISTRIBUTION.—Red Sea.

COMMENTS.—Additional illustrations are in Adam (1973, fig. 20). See comments under Abralia fasciolata.

Abralia fasciolata Tsuchiya, 1991

ORIGINAL REFERENCE.—Abralia fasciolata Tsuchiya, 1991:69, figs. 1–16, table 1.

DEPOSITION OF TYPES.—Holotype: USNM 817660, male, 24 mm ML, R/V Beinta sta 8–1 (GJS-28), western Indian Ocean, 11°14′06″N, 47°38′12″E, 15 Feb 1986, good condition.

Paratypes: USNM 817759, 41 specimens (including paratypes 1–3, 5–8), 21–37 mm ML, same lot as holotype. NSMT Mo-67140, male, 27 mm ML, same lot as holotype. NSMT Mo-67141, female, 31 mm ML, same lot as holotype. NSMT Mo-67142, 1 specimen, sex and size undetermined, same lot as holotype. NSMT Mo-67143, 1 specimen, sex and size undetermined, same lot as holotype.

GEOGRAPHICAL DISTRIBUTION.—Gulf of Aden, Indian Ocean.

COMMENTS.—Adam (1973) placed Enoploteuthis dubia in a new genus, Enigmoteuthis, because it was unique in having buccal connectives that attach to the dorsal margins of arms III. Riddell (1985) expressed doubts that Enigmoteuthis and Abralia should be separate taxa. Tsuchiya (1991) noted that A. fasciolata, as well as A. marisarabica Okutani, 1983, also has connectives of this type. As a result, he placed Enigmoteuthis in the synonymy of Abralia, although he retained the taxon as a subgenus.

Abralia grimpei Voss, 1959

ORIGINAL REFERENCE.—Abralia grimpei G.L. Voss, 1959:375, figs. 2, 3.

DEPOSITION OF TYPES.—Holotype: MCZ, female, 27 mm ML, R/V Atlantis sta RHB551, off Florida, 26°25′N, 79°45′W, 6 Feb 1954, condition unknown.

Paratypes: None.

GEOGRAPHICAL DISTRIBUTION.—Western North Atlantic.

COMMENTS.—The publication date for this species is 4 February 1959 (see Bulletin of Marine Science, 12(3):543), not 1958 as printed on the title page of the journal.

Abralia heminuchalis Burgess, 1992

ORIGINAL REFERENCE.—Abralia heminuchalis Burgess, 1992:120, figs. 2a–n.

DEPOSITION OF TYPES.—Holotype: USNM 729683, female, 37 mm ML, R/V Hugh M. Smith sta 47–51, equatorial central Pacific, 0°44′S, 149°46′W, 2 Nov 1958, good condition.

Paratypes: USNM 729719, 3 males, 27–32 mm ML, 5 females, 31–35 mm ML, 8 juveniles, 17–20 mm ML, same lot as holotype, good condition.

GEOGRAPHICAL DISTRIBUTION.—Central Pacific from 16°N to 15°S and from 144°W to 168°W (Burgess, 1992).

Abralia marisarabica Okutani, 1983

ORIGINAL REFERENCE.—Abralia marisarabica Okutani, 1983a:161, figs. 1–14.

DEPOSITION OF TYPES.—Holotype: NSMT Mo-31359, male, 20 mm ML, R/V Shoyo-Maru, Arabian Sea, 24°48′N, 63°20′E, 2 Dec 1976, condition unknown.

Paratypes: NSMT Mo-31360, 4 males, 20 mm ML, 20 mm ML, 20 mm ML, 21 mm ML, same lot as holotype, condition unknown. NSMT Mo-31361, 5 females, 22 mm ML, 23 mm ML, 24 mm ML, 24 mm ML, 25 mm ML, same lot as holotype, condition unknown.

GEOGRAPHICAL DISTRIBUTION.—Arabian Sea; Seychelles, Indian Ocean (Nesis and Nikitina, 1987).

Abralia multihamata Sasaki, 1929

ORIGINAL REFERENCE.—Abralia multihamata Sasaki, 1929:245, figs. 173–175, pl. 29: figs. 6, 7.

DEPOSITION OF TYPES.—Holotype: FMT, sex and size undetermined, M. Oshima, Okocho, Formosa (Taiwan), 20 Apr 1920, condition unknown.

Paratypes: None designated.

GEOGRAPHICAL DISTRIBUTION.—Off Taiwan; Philippines (Voss, 1963); Northwest Pacific (Tsuchiya, 1993).

COMMENTS.—Grimpe (1931) states this species is probably conspecific with A. armata (Quoy and Gaimard, 1832). Abralia lucens Voss, 1963, is a synonym (Tsuchiya and Okutani, 1988). Tsuchiya (1993) considers this to be a mesopelagic-boundary species.

Abralia redfieldi Voss, 1955

ORIGINAL REFERENCE.—Abralia redfieldi Voss, 1955:99, fig. 4A–H.

DEPOSITION OF TYPES.—Holotype: MCZ 203979, female, 29 mm ML, UMML sta SL23B, off Gun Cay, Bahama Islands, 10 Dec 1953, condition unknown.

Paratypes: MCZ 203980, female, 28 mm ML, R/V Atlantis sta 3436, off Caibarién, Cuba, 2 May 1939, condition unknown.

GEOGRAPHICAL DISTRIBUTION.—Western North Atlantic; western Atlantic from New England to Argentina (Voss, 1955; Nesis, 1975; Cairns, 1976; Lu and Roper, 1979; Stephen, 1982; Lipinski, 1983; Nesis and Nikitina, 1987); eastern Atlantic (Lu and Clarke, 1975b).

Abralia renschi Grimpe, 1931

ORIGINAL REFERENCE.—Abralia renschi Grimpe, 1931:149, figs. 1–9.

DEPOSITION OF TYPES.—Holotype: ZMB, female, 41 mm ML, B. Rensch, Sabang Harbor, Sumatra, Indonesia, 1927, condition unknown.

Paratypes: Deposition uncertain, 2 females, 37 mm ML, 45 mm ML, same lot as holotype, condition unknown.

GEOGRAPHICAL DISTRIBUTION.—Off Sumatra; Java, Maldives (Nesis, 1982).

COMMENTS.—Nesis and Nikitina (1987) consider this species a subspecies of A. steindachneri Weindl.

Abralia robsoni Grimpe, 1931

ORIGINAL REFERENCE.—Abralia robsoni Grimpe, 1931:156.

DEPOSITION OF TYPES.—Holotype: ZMUC, female, 51 mm ML, Th. Mortensen, leg., Bonomisaki, Japan, 13 May 1914, condition unknown.

Paratypes: Uncertain.

GEOGRAPHICAL DISTRIBUTION.—Off Japan.

COMMENTS.—Grimpe (1931) states this species is possibly identical to A. andamanica sensu Sasaki, 1929. Nesis (1982) considers this species a form of A. andamanica. Tsuchiya and Okutani (1988) consider this to be a valid species.

Abralia siedleckyi Lipinski, 1983

ORIGINAL REFERENCE.—Abralia siedleckyi Lipinski, 1983:255, figs. 1–8.

DEPOSITION OF TYPES.—Holotype: SFI IXEN212, male, 31 mm ML, R/V Professor Siedlecki sta 98/43, South Atlantic, 39°05′08″S, 13°43′E, 3 Jul 1978, condition unknown.

Paratypes: SFI IXEN213, male, 30 mm ML, same lot as holotype, condition unknown. SFI IXEN214, female, 33 mm ML, same lot as holotype, condition unknown.

GEOGRAPHICAL DISTRIBUTION.—Southeast Atlantic.

Abralia similis Okutani and Tsuchiya, 1987

ORIGINAL REFERENCE.—Abralia similis Okutani and Tsuchiya, 1987:141, figs. 1–15.

DEPOSITION OF TYPES.—Holotype: NSMT Mo-66642, male, 18 mm ML, R/V Kaiyo-Maru sta 13, southern Japan, 30°03′12″N, 134°03′30″E, 13 Jul 1986.

Paratypes: NSMT Mo-66643, female, 21 mm ML, same lot as holotype. NSMT Mo-66644, male, 17 mm ML, R/V Kaiyo-Maru sta MT14, southern Japan, 30°04′30″N, 143°46′36″E, 9 Jun 1979. NSMT Mo-66645, female, 32 mm ML, R/V Kaiyo-Maru sta 35, southern Japan, 30°04′36″N, 134°27′54″E, 31 Jul 1986. NSMT Mo-66646, male, 19 mm ML, R/V Kaiyo-Maru sta MT30, southern Japan, 29°58′48″N, 143°53′06″E, 18 Jun 1979. NSMT Mo-66647, female, 25 mm ML, R/V Kaiyo-Maru sta 28, southern Japan, 30°08′42″N, 144°13′12″E, 17 Jun 1979. Condition unknown for type series.

GEOGRAPHICAL DISTRIBUTION.—Shikoku Basin, Northwest Pacific; off Tonga Islands (Riddell, 1985); possibly equatorial western Indian Ocean and eastern Pacific (Nesis and Nikitina, 1987).

COMMENTS.—Abralia n. sp. Riddell, 1985, is a synonym (Burgess, 1992). Nesis and Nikitina (1987) assigned Riddell's form to A. japonica Ishikawa, 1929. The latter was subsequently found to be a synonym of Watasenia scintillans by Tsuchiya and Okutani, 1988.

Abralia spaercki Grimpe, 1931

ORIGINAL REFERENCE.—Abralia spaercki Grimpe, 1931:150 (footnote).

DEPOSITION OF TYPES.—Holotype: ZMUC, female, 47 mm ML, Th. Mortensen, off Saparua, near Amboina, Banda Sea, Feb 1922, condition unknown.

Paratypes: None.

GEOGRAPHICAL DISTRIBUTION.—Indonesia; Philippines (Voss, 1963).

COMMENTS.—This species was redescribed and was illustrated from the holotype by Voss (1963:112).

Abralia steindachneri Weindl, 1912

ORIGINAL REFERENCE.—Abralia steindachneri Weindl, 1912:271.

DEPOSITION OF TYPES.—Holotype: NMW 55.887, female, 49 mm ML, POLA, Shadwan, Red Sea, 19 Feb 1896, condition unknown.

Paratypes: NMW, 3 females, 48 mm ML, 53 mm ML, 57 mm ML, same lot as holotype, condition unknown. Measurements of type series made by G. Voss.

GEOGRAPHICAL DISTRIBUTION.—Red Sea (Adam, 1942, 1955, 1959, 1973); Seychelles (Adam, 1973); Gulf of Aden, Indian Ocean (Nesis and Nikitina, 1987).

COMMENTS.—This species was redescribed and was illustrated by Nesis and Nikitina (1987). Their remarks indicate that this is a mesopelagic-boundary species.

Abralia trigonura Berry, 1913

ORIGINAL REFERENCE.—Abralia trigonura Berry, 1913b:565.

DEPOSITION OF TYPES.—Neotype: USNM 730631, male, 37 mm ML, R/V Townsend Cromwell sta 32–56, central Pacific (Hawaiian waters), 21°22′24″N, 158°14′36″W, 19 Aug 1967.

Paratypes: None.

GEOGRAPHICAL DISTRIBUTION.—Hawaiian Islands (Young, 1978); Northwest Pacific (Tsuchiya, 1993).

COMMENTS.—The original type specimen is illustrated in Berry (1914b:329–330, fig. 33). The species was redescribed, illustrated, and a neotype was designated in Burgess (1992). Reid et al. (1991) demonstrated that this is a mesopelagic-boundary species.

Abralia veranyi (Rüppell, 1844)

ORIGINAL REFERENCE.—Enoploteuthis verany Rüppell, 1844:131, fig. 2.

DEPOSITION OF TYPES.—Holotype: BMNH, sex and size undetermined, off Messina, Italy, condition unknown.

Paratypes: None.

GEOGRAPHICAL DISTRIBUTION.—Mediterranean Sea (Pfeffer, 1912); Atlantic (Berry, 1926; Adam, 1952; Voss, 1955, 1956; Rees and Maul, 1956; Cairns, 1976; Lu and Roper, 1979; Okutani, 1983b; Nesis, 1987; Nesis and Nikitina, 1987).

Abraliopsis Joubin, 1896

TYPE SPECIES.—Abraliopsis pfefferi Joubin, 1896, by original designation.

DIAGNOSIS.—Manus of club with 2 series of hooks, 1 series of suckers. Two to 4 large photophores covered by black chromatophores on tips of arms IV. Fins terminal. Buccal crown without typical chromatophores, with dark epithelial pigmentation on oral surface (needs confirmation). Eyeball with 5 photophores. Right or left arm IV hectocotylized. Suckers absent from arms IV. Spermatophore receptacle(s) located under collar or between stellate ganglia. Complex photophores of integument, in life, with red color filters. Radula with homodont teeth. Large arm hooks with apertures closed.

COMMENTS.—Burgess (pers. comm., 1988) is describing three new species of Abraliopsis from the central Pacific, and Tsuchiya (1993) suggests that at least four unnamed species exist in the Northwest Pacific.

Abraliopsis pfefferi Joubin, 1896

ORIGINAL REFERENCE.—Abraliopsis pfefferi Joubin, 1896:20, figs. 1–10.

DEPOSITION OF TYPES.—Holotype: Depository unknown, sex undetermined, ∼42 mm ML, Mediterranean Sea, near Villefranche-sur-Mer, condition unknown.

Paratypes: None.

GEOGRAPHICAL DISTRIBUTION.—Mediterranean Sea; Northeast Atlantic (Joubin, 1920, 1924; Clarke and Lu, 1974); Northwest Atlantic (Cairns, 1976; Lu and Roper, 1979); Southwest Atlantic (Nesis, 1974); Indian Ocean (Voss, 1967).

COMMENTS.—Nesis (1982) considered A. pfefferi to be a subspecies of A. hoylei.

Abraliopsis affinis (Pfeffer, 1912)

ORIGINAL REFERENCE.—Abralia (Micrabralia) affinis Pfeffer, 1912:160.

DEPOSITION OF TYPES.—Syntypes (depositories unknown): male, R/V Albatross sta 3375, off Ecuador, 02°34′N, 82°29′W, 4 Mar 1891. Female, R/V Albatross sta 3382, Gulf of Panama, 06°21′N, 80°41′W, 7 Mar 1891. Female, R/V Albatross sta 3414, eastern tropical Pacific, 10°14′N, 96°28′W, 8 Apr 1891. Male, R/V Albatross sta 3415, off Mexico, 14°46′N, 98°40′W, 10 Apr 1891. Condition of type series unknown.

GEOGRAPHICAL DISTRIBUTION.—Eastern tropical Pacific (Hoyle, 1904; Nesis, 1972; Okutani, 1974).

COMMENTS.—Three of the types are illustrated in Hoyle (1904, pl. 1: fig. 3, pl. 8: figs. 1–9).

Abraliopsis atlantica Nesis, 1982

ORIGINAL REFERENCE.—Abraliopsis (Micrabralia) atlantica Nesis, 1982:172 (footnote).

DEPOSITION OF TYPES.—Holotype: ZMB, male, 20 mm ML, S.S. Valdivia sta 54, Gulf of Guinea, 01°51′N, 00°31′E, date unknown, condition unknown.

Paratypes: None.

GEOGRAPHICAL DISTRIBUTION.—Eastern tropical Atlantic (Chun, 1910, as A. morisii; Cairns, 1976, as Abraliopsis sp.).

COMMENTS.—The holotype is illustrated (as Abraliopsis morisii Verany) in Chun (1910, pl. VI: fig. 1, pl. VIII: figs. 1, 5, pl. X: fig. 1).

Abraliopsis chuni Nesis, 1982

ORIGINAL REFERENCE.—Abraliopsis (Micrabralia) chuni Nesis, 1982:172 (footnote).

DEPOSITION OF TYPES.—Holotype: ZMB, female, 38 mm ML, S.S. Valdivia sta 256, western Indian Ocean, 01°49′N, 45°29′E, date unknown, condition unknown.

Paratypes: None.

GEOGRAPHICAL DISTRIBUTION.—Tropical Indo-West Pacific, from eastern Africa to the Line Islands (Nesis, 1982).

COMMENTS.—The holotype is illustrated (as Abraliopsis morisii Verany) in Chun (1910, pl. V, pl. VIII: fig. 3, pl. IX: figs. 3, 4).

Abraliopsis falco Young, 1972

ORIGINAL REFERENCE.—Abraliopsis falco Young, 1972:13, pls. 1A,B, 2A–G.

DEPOSITION OF TYPES.—Holotype: SBMNH 34947, male, 37 mm ML, R/V Velero IV sta 10679, off Baja California, 28°54′N, 118°08′W, 28 Aug 1965, good condition.

Paratypes: SBMNH 34958, 3 females, 41 mm ML, 43 mm ML, 46 mm ML, and 1 male, 35 mm ML, R/V Velero IV sta 9899, off Baja California, 29°58′N, 119°12′W, 7 Aug 1964, good condition. SBMNH 34959, male, 37 mm ML, R/V Velero IV sta 9901, off Baja California, 29°33′N, 118°59′W, 7 Aug 1964, good condition. SBMNH 34960, male, 36 mm ML, R/V Velero IV sta 10677, off Baja California, 29°05′N, 118°06′W, 28 Aug 1965, good condition. USNM 727480, female, 36 mm ML, male, 37 mm ML, same lot as holotype, good condition.

GEOGRAPHICAL DISTRIBUTION.—Off Baja California; eastern tropical Pacific (Okutani, 1974).

COMMENTS.—The record listed by Young (1972) from off Hawaii is probably based on a misidentification because a very similar species (Burgess, pers. comm., 1988) occurs there. The latter is also the species mentioned by Nesis (1985b, 1987) as A. cf. falco (Nesis, pers. comm., 1988).

Abraliopsis felis McGowan and Okutani, 1968

ORIGINAL REFERENCE.—Abraliopsis felis McGowan and Okutani, 1968:72, pls. 9, 10.

DEPOSITION OF TYPES.—Holotype: USNM 678792, male, 36 mm ML, CalCOFI sta 25–87.90, eastern North Pacific, 31°59′N, 122°24′W, 25 May 1951, good condition.

Paratypes: USNM 678793, female, 41 mm ML, CalCOFI, eastern North Pacific, 32°39′18″N, 117°37′12″W, Aug 1953, good condition. CASIZ 310, male, 33 mm ML, CalCOFI, eastern North Pacific, 32°49′N, 117°43′W, Aug 1953, condition unknown. SIO, male, 39 mm ML, CalCOFI sta 5704–93.90, eastern North Pacific, 30°49′30″N, 121°32′W, Apr 1957, condition unknown.

GEOGRAPHICAL DISTRIBUTION.—Off west coast of North America from about 27°N to 43°N (Okutani and McGowan, 1969); Northwest Pacific (Tsuchiya, 1993).

Abraliopsis gilchristi (Robson, 1924)

ORIGINAL REFERENCE.—Abralia gilchristi Robson, 1924a:3.

DEPOSITION OF TYPES.—Syntypes: BMNH 1924.9.9.41–2, male, 40 mm ML, Pickle sta 48, off Cape Town, South Africa, thoroughly dissected fide Voss (1962b:264). Male, 40 mm ML, Pickle sta 81, South Africa, condition unknown.

GEOGRAPHICAL DISTRIBUTION.—Indian Ocean (Robson, 1924a; Voss, 1967; Silas, 1968); off New Zealand (Riddell, 1985); central South Pacific (Polezhaev, 1986).

COMMENTS.—The syntypes are illustrated by Robson (1924b, figs. 6, 7, pl. 1: fig. 1). Enoploteuthis neozelanica Dell, 1959, is a synonym (Nesis, 1982; Riddell, 1985).

Abraliopsis hoylei (Pfeffer, 1884)

ORIGINAL REFERENCE.—Enoploteuthis hoylei Pfeffer, 1884:17, pl. 3: figs. 22, 22a, 22b.

DEPOSITION OF TYPES.—Holotype: ZMH (no longer extant), 29 mm ML, Mascarene Islands, Indian Ocean (purchased from specimen dealer).

Paratypes: None.

GEOGRAPHICAL DISTRIBUTION.—Indian Ocean; Caribbean Sea (Nesis, 1975, as A. pfefferi hoylei).

COMMENTS.—The holotype was redescribed and was illustrated in Pfeffer (1912:153, pl. 17: figs. 1–9).

Abraliopsis lineata (Goodrich, 1896)

ORIGINAL REFERENCE.—Abralia lineata Goodrich, 1896:10, pl. 3: figs. 46–50.

DEPOSITION OF TYPES.—Holotype: IMC, male, 15 mm ML, R/V Investigator, Andaman Sea, poor condition.

Paratypes: IMC, female, ML unknown, R/V Investigator, off Ganjan (?India, Bay of Bengal), not extant.

GEOGRAPHICAL DISTRIBUTION.—Indian Ocean.

COMMENTS.—G. Voss (unpublished) examined the holotype and found it similar to A. gilchristi; however, most specific characters could not be determined from the type. Tsuchiya et al. (1991) were able to redescribe A. lineata on the basis of new material from the Arabian Sea, and they agree that its closest relative is A. gilchristi.

Abraliopsis morisii (Verany, 1839)

ORIGINAL REFERENCE.—Onychoteuthis morisii Verany, 1839:100, pl. 2.

DEPOSITION OF TYPES.—Holotype: Depository unknown, dolphin stomach taken at 39°N, 20°E, condition unknown.

Paratypes: ?None.

GEOGRAPHICAL DISTRIBUTION.—Northeast Atlantic.

COMMENTS.—According to Nesis (1982), Chun's (1910) description of “A. morisii” included three species, A. lineata Goodrich and two undescribed species that Nesis named A. atlantica and A. chuni. Nesis (1982) states that it is impossible to determine the real A. morisii due to the incomplete original description. We list it herein among the valid species although its status is uncertain. Clarification depends on either locating the holotype or confirming its loss and on a more complete understanding of the taxonomy of this genus in the North Atlantic.

Abraliopsis pacificus Tsuchiya and Okutani, 1990

ORIGINAL REFERENCE.—Abraliopsis pacificus Tsuchiya and Okutani, 1990:48, figs. 1–21.

DEPOSITION OF TYPES.—Holotype: NSMT Mo-66998, male, 26 mm ML, R/V Kaiyo-Maru sta 49-5, off Japan, 32°47′18″N, 147°58′42″E, 26 Apr 1987, good condition.

Paratypes: NSMT Mo-66999, female, 36 mm ML, R/V Kaiyo-Maru sta MT15B, off Japan, 30°02′42″N, 143°33′00″E, 9 Jun 1979, good condition. NSMT Mo-67000, male, 25 mm ML, same lot as holotype, good condition. NSMT Mo-67001, female, 34 mm ML, same lot as holotype, good condition. NSMT Mo-67002, male, 24 mm ML, R/V Kaiyo-Maru sta 1(D), Northwest Pacific 36°04′30″N, 157°55′30″E, 25 Jul 1972, good condition. NSMT Mo-67003, female, 34 mm ML, same lot as holotype, good condition. USNM 817632, male, 24 mm ML, same lot as holotype, good condition. USNM 817633, female, 32 mm ML, male, 23 mm ML, R/V Kaiyo-Maru sta 49-5–2, off Japan, 32°47′48″N, 147°59′24″E, 26 Apr 1987, good condition. USNM 817634, female, 28 mm ML, R/V Kaiyo-Maru sta KOC16, off Japan, 30°00′N, 147°00′E, 10 Jun 1982, good condition.

GEOGRAPHICAL DISTRIBUTION.—Northwest Pacific Basin and Shikoku Basin, between latitudes 30°N and 35°N (Tsuchiya and Okutani, 1990); Hawaiian waters (Tsuchiya, 1993).

Abraliopsis tui Riddell, 1985

ORIGINAL REFERENCE.—Abraliopsis tui Riddell, 1985:37, figs. 28, 29.

DEPOSITION OF TYPES.—Holotype: ?NMNZ, male, 28 mm ML, R/V James Cook sta 17–71, off Kermadec Islands, 28°18′S, 174°56′W, 14 Dec 1976, condition unknown.

Paratypes: ?NMNZ, male, 29 mm ML, same lot as holotype, condition unknown. ?NMNZ, 3 females, 19–30 mm ML, same lot as holotype, condition unknown.

GEOGRAPHICAL DISTRIBUTION.—South Pacific off New Zealand, 170°E, 20°S to 170°W, 40°S.

COMMENTS.—Riddell (1985) found this species both north and south of the subtropical convergence.

GENERAL REMARKS

The large number of species in the genera Enoploteuthis, Abralia, and Abraliopsis has resulted in the common use of subgenera to group together various related species. We suspect, however, that when a phylogenetic analysis is made of these groups, relationships will prove to be more complex than now suggested by subgeneric designation. As a result, we have chosen not to include subgenera in this paper. Discussions of the subgenera of various enoploteuthid genera can be found in Burgess (1982), Nesis and Nikitina (1987), and Tsuchiya and Okutani (1988).

Watasenia Ishikawa, 1914a

TYPE SPECIES.—Abraliopsis scintillans Berry, 1911, by indication.

COMMENTS.—Watasea Ishikawa, 1913, is a synonym (preoccupied).

DIAGNOSIS.—Manus of club with hooks in 1 series (2 to 3 in number), 1 series of suckers. Two to 4 large photophores covered by black chromatophores on tips of arms IV. Fins terminal. Buccal crown without typical chromatophores, with dark epithelial pigmentation on oral surface. Five photophores on eyeball. Hectocotylus on right arm IV with 1 dorsal and 1 ventral flap. Suckers absent from arms IV. Spermatophore receptacles located under collar. Complex photophores of integument, in life, apparently with red color filters. Radula with homodont teeth. Large arm hooks with apertures closed.

Watasenia scintillans (Berry, 1911)

ORIGINAL REFERENCE.—Abraliopsis scintillans Berry, 1911:93.

DEPOSITION OF TYPES.—Holotype: CASIZ 21667 (previously 453), female, 59 mm ML, Japan (label lost, exact locality and date unknown), SSB no. 147.

Paratypes: USNM 816498, 2 females, 52 mm ML, 55 mm ML, same lot as holotype, dried and in very poor condition.

GEOGRAPHICAL DISTRIBUTION.—Off Japan (Okutani, 1967; Okutani et al., 1987; Tsuchiya, 1993).

COMMENTS.—Considerable confusion exists concerning the type locality of this species. In the original description, Berry (1911:94) gave measurements and locality (Japan) for only one specimen. In a subsequent paper, Berry (1912:425, figs 3, 4, pls. 7–9: figs. 1–6) expanded the species description, elaborated on the locality (Japan, probably off Misaki (Alan Owston?)), and gave his catalog number (SSB 147, cotypes, 3 females) for the type lot. In addition, he listed three other females examined (taken at Misaki by Ishikawa, SSB 279). The following year Berry (1913c:591) attempted to correct his locality information and wrote that “I had supposed my specimens to have been taken at Misaki, Sagami, but Drs. Ijima and Ishikawa have written me that this locality is probably erroneous. Ishikawa states that my specimens No. 279 really came from Uwotu on the Japan Sea, Watase quotes Toyama as a locality, and I have recently received specimens from Namerigawa, Ecchiu.” The correction of the locality of SSB 279, however, does not change the type locality, as SSB 279 is not part of the type series. Berry's entry for SSB 147, on 18 February 1911, in his specimen card-catalog states that (1) the specimens were found in the L.S.J.U. collections without any label and (2) Dr. Heath thinks them R/V Albatross material and most probably from Monterey Bay, California. Therefore, the type locality must simply be Japan with the more exact locality unknown.

Abralia japonica Ishikawa, 1929, is a synonym (Tsuchiya and Okutani, 1988). Data of Sasaki (1914) indicate that this is a mesopelagic-boundary species.

PYROTEUTHIDAE Pfeffer, 1912

TYPE GENUS.—Pyroteuthis Hoyle, 1904.

DIAGNOSIS.—Buccal crown with 7 or 8 supports. Buccal connectives attached to dorsal margins of arms IV. Secondary buccal connectives attached to ventral margins of arms I and II. Gladius with small, strongly pointed conus and elongate cone field; rostrum absent. Hooks present on (at least) arms I–III; presence on tentacular club varies with genus; armature on manus always in 4 series. Photophores present on viscera, eyeballs, and tentacles. Photophores absent from fins, mantle, funnel, head, and arms. Nidamental glands present; oviducal glands normal on one side, may be reduced or absent on other side. Oviduct single or unpaired. Fins subterminal; posterior lobes present. Tail not fleshy; vesicles absent. Nuchal folds absent. Tentacles with permanent constriction and bend near base; stalk “ligament” and vein leave tentacle distal to base and not in membrane. Ink sac embedded in digestive gland.

Pyroteuthis Hoyle, 1904

TYPE SPECIES.—Enoploteuthis marqaritifera Rüppell, 1844, by indication.

DIAGNOSIS.—More than 13 hooks per arm; hooks in 2 series; hooks present on arms IV. Tentacular club with 1 series of hooks on manus, 3 series of suckers on manus. Eyeball photophore number 6 (= lidded photophore) absent (numbering based on Pterygioteuthis eye, Chun 1910, pl. XIV: fig. 6). Six or 7 separated photophores in tentacular stalk. Oviducts unpaired (right oviducal gland may be reduced in size depending on species). Right arm IV hectocotylized; toothed plate absent.

Pyroteuthis margaritifera (Rüppell, 1844)

ORIGINAL REFERENCE.—Enoploteuthis margaritifera Rüppell, 1844:130, fig. 1.

DEPOSITION OF TYPES.—Syntypes: BMNH 62a, 62b, 2 specimens, sex and size undetermined, off Messina, Italy, condition unknown.

GEOGRAPHICAL DISTRIBUTION.—Mediterranean Sea; North Atlantic (Voss, 1956; Roper and Young, 1975; Cairns, 1976); Southwest Atlantic (Nesis, 1974); central Pacific (Hoyle, 1886); South Pacific (Riddell, 1985; Polezhaev, 1986); southeastern Indian Ocean (Voss, 1967).

COMMENTS.—Riddell (1985) noted possible differences in the arrangement of tentacle photophores between P. marqaritifera taken in the Atlantic and specimens taken off New Zealand. Nesis (1982) distinguished three forms on the basis of this character, one of which was P. serrata Riddell, 1985. Young (1972) considered P. margaritifera oceanica Pfeffer, 1912, which was based on specimens described by Hoyle (1886) from the South Pacific, as invalid; in light of the variability found by both Riddell and Nesis, this form needs a reevaluation.

Pyroteuthis addolux Young, 1972

ORIGINAL REFERENCE.—Pyroteuthis addolux Young, 1972:22, pls. 3B, 4I–Q,S.

DEPOSITION OF TYPES.—Holotype: SBMNH 34962, female, 45 mm ML, R/V Swan sta 27A, Northeast Pacific, 31°39′N, 133°16′W, 1966, good condition.

Paratypes: SBMNH 34963, male, 30 mm ML, R/V Swan sta 13A, Northeast Pacific, 26°N, 147°W, 1966, good condition. SBMNH 34964, female, 20 mm ML, R/V Velero IV sta 8238, off Santa Catalina Island, California, 33°28′N, 118°48′W, good condition. SBMNH 34965, female, 23 mm ML, R/V Velero IV sta 10838, off Baja California, 31°14′N, 118°45′W, good condition.

GEOGRAPHICAL DISTRIBUTION.—Eastern North Pacific; off Hawaiian Islands (Young, 1978).

Pyroteuthis serrata Riddell, 1985

ORIGINAL REFERENCE.—Pyroteuthis serrata Riddell, 1985:10, figs. 3, 4a,b,d,f.

DEPOSITION OF TYPES.—Holotype: ?NMNZ, male, 27 mm ML, R/V James Cook sta 17–32, Kermadec Islands, 28°08′S, 177°22′30″W, 6 Dec 1976, condition unknown.

Paratypes: ?NMNZ, 4 females, 22 mm ML, 28 mm ML, 34 mm ML, 40 mm ML, R/V James Cook sta 17–47, Southwest Pacific, 23°00′S, 175°31′W, 8 Dec 1976, condition unknown.

GEOGRAPHICAL DISTRIBUTION.—All known specimens come from within a 4° radius of 26°S, 177°W (Riddell, 1985).

COMMENTS.—Riddell (1985) found P. serrata off New Zealand only north of the tropical convergence (roughly 30°S); it was replaced by P. margaritifera south of the convergence.

Pterygioteuthis Fischer, 1896

TYPE SPECIES.—Pterygioteuthis giardi Fischer, 1896, by indication.

DIAGNOSIS.—Less than 8 hooks per arm; hooks in 1 or 2 series depending on species; hooks absent from arms IV. Tentacular clubs without hooks; 4 series of suckers on manus. Eyeball photophore number 6 (= lidded photophore) present (numbering based on Pterygioteuthis eye, Chun 1910, pl. XIV: fig. 6). Two or 4 separate photophores in tentacular stalk. Oviduct present on right side only. Left arm IV hectocotylized; toothed plate present.

COMMENTS.—We suspect that Pterygioteuthis giardi and P. gemmata are each complexes of species. Riddell (1985) captured P. gemmata between New Zealand and the subtropical convergence; it was replaced by P. microlampas north of the convergence.

Pterygioteuthis giardi Fischer, 1896

ORIGINAL REFERENCE.—Pterygioteuthis giardi Fischer, 1896:211, pl. IX: figs. 1–7.

DEPOSITION OF TYPES.—Holotype: MNHN 3-7-727, female, 19 mm ML, off Morocco, condition unknown.

Paratypes: None.

GEOGRAPHICAL DISTRIBUTION.—North and South Atlantic (Voss, 1956; Nesis, 1974; Clarke and Lu, 1974; Lu and Clarke, 1975a, 1975b; Cairns, 1976); Caribbean Sea (Nesis, 1975); eastern tropical Pacific (Hoyle, 1904; Okutani and McGowan, 1969; Nesis, 1972; Okutani, 1974); central Pacific (Young, 1978); South Pacific (Riddell, 1985); Indian Ocean (Okutani and Tsukada, 1988).

COMMENTS.—Riddell (1985) found this species to be common north of 32°S, less common to 35°S, and absent between 35°S and 40°S off New Zealand. Pfeffer (1912) considered that Hoyle's (1904) specimens from the eastern tropical Pacific represented a subspecies, P. giardi hoylei. The validity of this has been supported by Nesis (1982).

Pterygioteuthis gemmata Chun, 1908

ORIGINAL REFERENCE.—Pterygioteuthis gemmata Chun, 1908:87.

DEPOSITION OF TYPES.—Holotype: ZMB, sex and size undetermined, S.S. Valdivia, “South Atlantic Ocean,” condition unknown.

Paratypes: Undetermined.

GEOGRAPHICAL DISTRIBUTION.—South Atlantic (Nesis, 1974); North Atlantic (Clarke and Lu, 1974; Lu and Clarke, 1975b; Cairns, 1976; Lu and Roper, 1979); South Pacific (Riddell, 1985; Polezhaev, 1986); eastern North Pacific (Young, 1972); Indian Ocean (Chun, 1910; Voss, 1967).

COMMENTS.—This species has not been recorded from the Mediterranean Sea (Mangold and Boletzky, 1988).

Pterygioteuthis microlampas Berry, 1913

ORIGINAL REFERENCE.—Pterygioteuthis microlampas Berry, 1913b:566.

DEPOSITION OF TYPES.—Holotype: USNM 214386 (no longer extant), female 18 mm ML, R/V Albatross sta 4105, Kaiwi Channel off Molokai Island, Hawaiian Islands, 24 Jul 1902.

Paratypes: None designated.

GEOGRAPHICAL DISTRIBUTION.—Central Pacific (Berry, 1914b; Young, 1978); South Pacific (Riddell, 1985).

COMMENTS.—The holoype is illustrated in Berry (1914b, figs. 35, 36, pl. LII: figs. 1–3).

ANCISTROCHEIRIDAE Pfeffer, 1912

TYPE GENUS.—Ancistrocheirus Gray, 1849.

DIAGNOSIS.—Buccal crown with 8 supports. Buccal connectives attached to dorsal margins of arms IV. No secondary buccal connectives attached to ventral margins of arms I and II. Gladius with pointed conus and elongate cone field; long pointed rostrum present. Hooks present on all arms; tentacular clubs with 2 series of hooks on manus; armature on manus in 2 series (suckers absent). Photophores present on fins, mantle, funnel, head, arms, and tentacles. Photophores absent from viscera and eyeballs. Nidamental glands present; oviducal glands normal. Oviducts unipaired. Fins slightly subterminal, without posterior lobes. Tail fleshy; vesicles absent. Nuchal folds present. Tentacles not modified near base; stalk “ligament” and vein leave tentacle at base and in membrane. Ink sac not embedded in digestive gland.

Ancistrocheirus Gray, 1849

TYPE SPECIES.—Enoploteuthis lesueurii Orbigny, 1842, in Férussac and Orbigny, 1834–1848, by indication.

DIAGNOSIS.—Same as for family.

Ancistrocheirus lesueurii (Orbigny, 1842, in Férussac and Orbigny, 1834–1848)

ORIGINAL REFERENCE.—Enoploteuthis lesueurii Orbigny, 1842:339, pl. 11: figs. 1–5, pl. 14: figs. 4–10, in Férussac and Orbigny, 1834–1848.

DEPOSITION OF TYPES.—Holotype: MNHN 2-14-614, 2-14-615 (gladius), 2-14-616 (beaks), male, 125 mm ML, locality not indicated (dolphin stomach content), condition unknown (fide Lu et al., 1995).

Paratypes: None.

GEOGRAPHICAL DISTRIBUTION.—Southeast Pacific (Adam, 1954; Riddell, 1985); Northwest Pacific (Okutani, 1976); central Pacific (Young, 1978); eastern tropical Pacific (Okutani, 1974); western tropical Pacific (Nesis, 1978); Indian Ocean (Silas, 1968; Okutani and Tsukada, 1988); North Atlantic (Clarke and Lu, 1975; Lu and Roper, 1979; Toll and Hess, 1981); South Atlantic (Pfeffer, 1912; Clarke, 1980).

COMMENTS.—The date of the species originates from publication of the plates (1835 and 1839–1842) (see Bello, 1992; Tillier and Boucher-Rodoni, 1993); publication of the description followed in 1848 (Orbigny, 1848:339, in Férussac and Orbigny, 1834–1848). Insufficient material has been available for critical species-level comparisons of specimens from different regions. A second species, A. alessandrinii (Verany, 1851), has been described, but, at present, we considered it a synonym of A. lesueurii because characters adequate to separate them have not been confirmed.

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Phylogeny of the “Enoploteuthid” Families

Richard Edward Young and Robert F. Harman

____________

Richard Edward Young, Department of Oceanography, University of Hawaii, Honolulu, Hawaii 96822, United States. Robert F. Harman, Western Pacific Regional Fishery Management Council, Honolulu, Hawaii 96813, United States.

ABSTRACT

Thirteen species of the Enoploteuthidae, related families, and other families bearing arm and/or tentacle hooks were examined in order to determine the phylogenetic relationships among the Enoploteuthidae, Pyroteuthidae, Ancistrocheiridae, and Lycoteuthidae. Thirteen characters were examined, with special emphasis placed on hook morphology. We conclude that the former Enoploteuthidae is not monophyletic, and that the proposed elevation of the three subfamilies of Enoploteuthidae to familial status is warranted.

Introduction

In 1861 Steenstrup erected the family Onychii for hook-bearing squids. Hoyle (1886) included in this family the present members of the Enoploteuthidae, Onychoteuthidae, Gonatidae, Ancistrocheiridae, and Octopoteuthidae. Chun (1910) suggested a more accurate relationship among species would be revealed by the number of their buccal supports and the location of their buccal connectives on arms IV. He considered the Enoploteuthidae to be a separate family and included within it the Lycoteuthinae (his Thaumatolampadinae) and the Enoploteuthinae. The latter subfamily he subdivided into the tribes Pterygiomorphae and Enoplomorphae, with Ancistrocheirus in the latter.

Naef (1921, 1923), in his classic studies on cephalopod evolution, presented an arrangement similar to that of Chun, although he divided the Enoploteuthidae into three subfamilies, the Lycoteuthinae, Pyroteuthinae, and Enoploteuthinae. He included Ancistrocheirus as a genus within the latter subfamily. He placed most remaining hooked squids in the families Onychoteuthidae, Gonatidae, and Octopoteuthidae. The Lycoteuthinae was first elevated to familial status by Chun (1903) (as Thaumatolampadidae), then by Berry (1914), and finally by Thiele (1935). Ancistrocheirus was placed in its own subfamily by Pfeffer (1912) and again by Thiele (1935). Clarke (1988) raised the three enoploteuthid subfamilies (Enoploteuthinae, Pyroteuthinae, and Ancistrocheirinae) to familial status.

The objective of this paper is to evaluate the relationships among these “enoploteuthid” groups in order to determine whether or not the change by Clarke (1988) is warranted. Relationships should be determined by the sequence in which the groups in question arose. A phylogenetic analysis of this type was not attempted by Clarke. Our study places particular emphasis on hook morphology, although this was not the most revealing character studied.

MATERIALS AND METHODS.—Hooks taken from preserved specimens were prepared for scanning electron microscopy (SEM) by soaking for one to several hours in a saturated trypsin solution buffered with borax. The sheathing tissue was then dissected away and the hook was cleaned with a fine brush. After coating, hooks were viewed with an I.S.I. 40 scanning electron microscope. Two specimens each of Gonatus sp. and Lycoteuthis diadema (Chun) were borrowed from the National Museum of Natural History (NMNH), Smithsonian Institution. A total of 17 species were examined as representatives of 10 families (see Table 2). These species were chosen because the desired number of specimens was available only for those species common in Hawaiian waters (see Young, 1978). Specimen size is expressed as dorsal mantle length (ML). Searches for the most parsimonious phylogenetic trees were made using the computer program PAUP (Swofford, 1993) on a Macintosh II computer.

ACKNOWLEDGMENTS.—We thank C. Roper and M. Sweeney, National Museum of Natural History, Smithsonian Institution, for supplying some of the specimens examined, and we thank J. Cowen, University of Hawaii, for assistance with SEM.

Analysis of Characters

The characters Naef (1921, 1923) used to unite the four present-day “enoploteuthid families” (i.e., Lycoteuthidae, Pyroteuthidae, Enoploteuthidae, Ancistrocheiridae) included the following: buccal crown with 8 supports, buccal connectives that attach to the dorsal margin of arms IV, gladius with a terminal cone but without a true rostrum, small carpal cluster at the base of the tentacular club, presence of photophores, and presence of hooks (except in “Lycoteuthinae”).

We discuss each of these characters and add a few others, namely, connections of the buccal pockets, size and structure of the tail, morphology of the oral surface of the buccal membrane, position of the spermatophore receptacle in females, and location of the hectocotylus.

Unfortunately, phylogenetic relationships among teuthoid families are poorly known. We could not even be certain that the enoploteuthid families represented a monophyletic group. As a result, we picked a variety of families that were treated as part of an ingroup. We included therein two families with dorsal connectives to arms IV (Ommastrephidae, Histioteuthidae) and the other families of the “onychii” (Gonatidae, Onychoteuthidae, and Octopoteuthidae), all of which belong to the Oegopsida. For outgroup comparison we used the Loliginidae (Myopsida), which was a safe but more distantly related choice than would have been desirable.

EXAMINATION OF CHARACTERISTICS OF ARM AND TENTACLE HOOKS

In addition to the original groups present in the onychii, several other squids bear hooks. These belong to the cranchiid genera Galiteuthis (hooks on the tentacles), Mesonychoteuthis (hooks on the arms and tentacles), and Taonius (hooks on the tentacles). In the neoteuthid genus Alluroteuthis, the arms have suckers with enlarged teeth that could be called hooks. We did not include these groups in the present survey because this character does not seem to be primitive in the Cranchiidae (Voss, 1988) or in the Neoteuthidae. The latter family is polymorphic for structures that only marginally qualify as hooks.

Within the onychii there is considerable variety in the structure of the hooks. Even within a single species, hook structure can vary among individuals, sexes, arms, arms and clubs, and relative positions on the arms or clubs. This variability is compounded by variation among species in all of these features. We were unable to resolve all the variability due to both logistic constraints and a lack of material in some groups. As a result, our analysis is restricted.

To reduce the problem to a manageable size, we compared only the larger arm hooks (usually from arms III of females) and the smaller hooks from the tentacular clubs. We treated both arm and club hooks because one family (Onychoteuthidae) has only club hooks and one family (Octopoteuthidae) has only arm hooks. We selected the small club hooks for two reasons: (1) they are more similar to the arm hooks, and (2) the range of variability is less than in the large hooks. These features lead us to believe that the small club hooks are the most generalized and are the most likely to reveal relationships at the familial level.

FIGURE 1.—Diagramatic composite illustration of hook to define hook terminology.

We identified six characters on the arm hooks and two characters on the club hooks. The terminology used is defined in Figure 1, and the data are summarized in Table 1. Representative hooks are seen in Figures 2 and 3.

The six characters of the arm hooks are as follows:

APERTURE.—Character States: 0 = remnant of sucker aperture remains open in mature hook; 1 = sides of sucker aperture fused in mature hook.

Comments: Species of Enoploteuthis differ from other members of the enoploteuthid families in having an open aperture. The aperture, however, is a narrow slit that is small compared to the apertures of the hooks from non-enoploteuthid families.

FIGURE 2.—Scanning electron micrographs of arm hooks in various orientations (scale bar = 0.25 mm). A, Octopoteuthis nielseni, 60 mm ML; B, Pterygioteuthis giardi, male, 20 mm ML; C, Abralia trigonura, female, 40 mm ML; D, Enoploteuthis jonesi, female, 65 mm ML; E, Gonatus sp., 60 mm ML, tip of claw distorted by fixative; F, Pyroteuthis addolux, female, 48 mm ML; G, Abraliopsis sp. A, female, 40 mm ML; H, Ancistrocheirus lesueurii, 35 mm ML.

TABLE 1.—Character states for arm- (A–F) and tentacular-club (a,b) hook characters (N = not applicable). Characters: A = aperture; B = skirt; C = lateral lobes; D = belly; E = claw; F = accessory hooks; a = lateral lobes; b = skirt.

SKIRT.—Character States: 0 = lacking thin, broad, chitinous ledge (skirt) around aperture region; 1 = skirt around aperture region present.

Comments: This distinctive structure is found only on the arm hooks of Gonatus sp. (Figure 2E).

LATERAL LOBES.—Character States: 0 = margin of hook base produced into 2 large lateral lobes and 1 smaller proximal lip; 1 = margin of hook base not clearly differentiated into lateral lobes and proximal lip.

Comments: Character state 1 is shared by Gonatus sp. and Octopoteuthis nielseni Robson, although the base of the hook is very different in these species. In O. nielseni (Figure 2A) the margin is virtually the circular edge of a conical base, whereas in Gonatus sp. (Figure 2E) the margin configuration is more similar to that of the other families, i.e., low bulges, similar to reduced lateral lobes, lie distal to (above) the lateral margin, which is formed by an extended lip that covers two-thirds of the distance around the base.

BELLY.—Character States: 0 = belly of hook gently rounded; 1 = belly of hook distinctly ridged.

Comments: Pterygioteuthis spp. differ from other members of the enoploteuthid families in this character. The shape of the hooks in these species is highly variable, however, and the belly is often strongly arched although not ridged.

CLAW.—Character States: 0 = concave surface of claw contains longitudinal grooves and ridges; 1 = concave surface of claw smooth.

Comments: This character proved to be of little value. The only species without ornamentation on the claw were species of Pterygioteuthis and Octopoteuthis.

ACCESSORY HOOKS.—Character States: 0 = secondary claws in aperture region absent; 1 = pair of secondary claws present in aperture region.

Comments: This distinctive feature is found only in Octopoteuthis nielseni (Figure 2A)

The two characters of the tentacular-club hooks are as follows:

LATERAL LOBES.—Character States: 0 = margin of hook base with 2 large lateral lobes and 1 proximal lip; 1 = margin of hook base not clearly differentiated into lateral lobes and proximal lip.

Comments: This character separates Gonatus sp. (Figure 3I) from all other species examined.

SKIRT.—Character States: 0 = thin, broad, chitinous ledge (skirt) surrounding much of aperture region absent; 1 = skirt present.

Comments: The presence of a skirt is shared by Gonatus sp. (Figure 3I) and Onychoteuthis borealijaponicus Okada (Figure 3B).

Five species (“first group”), Pyroteuthis addolux Young, Abralia trigonura Berry, Abraliopsis sp. A, Abraliopsis sp. B, and Ancistrocheirus lesueurii (Orbigny), were identical in all eight characters. Enoploteuthis spp. agreed with the first group in seven of the eight characters. Gonatus sp. agreed with the first group in two of the eight characters. Among species with hooks only on the arms, Pterygioteuthis spp. agreed with the first group in four of six characters, and Octopoteuthis nielseni agreed with it in but one of the six characters. Onychoteuthis borealijaponicus, the only species with hooks only on the tentacles, agreed with the first group in one of two tentacular-hook characters.

Among the species in the enoploteuthid families, species of Enoploteuthis had somewhat different arm hooks, as did species of Pterygioteuthis. In the latter case, we attribute differences to the extremely small sizes of these squids. The hooks of Gonatus sp. and Octopoteuthis nielseni bear little resemblance to those of the species of the enoploteuthid families. Onychoteuthis borealijaponicus differs from the latter by the lack of arm hooks and by the distinctive feature of a skirt on the club hooks, a feature known otherwise only in Gonatus sp. Gonatus sp. and Onychoteuthis borealijaponicus exhibit another feature that appears different from the other groups, namely, the gradual transition, during ontogeny, from the presence of suckers to their replacement by hooks. This feature was not examined carefully; however, the differences are indicated by the ease of finding transitional stages in Gonatus sp. and Onychoteuthis borealijaponicus and by the difficulty in finding them in the other groups. We suspect that a careful study of the mechanism of transformation would provide more insight into phylogeny than does the structure of the fully formed hook.

FIGURE 3.—Scanning electron micrographs of tentacle-club hooks (A–E) and proximal views (i.e., underside) of arm hooks (F–I) in various orientations (scale bar = 0.25 mm). A, Abraliopsis sp. A, male, 35 mm ML; B, Onychoteuthis borealijaponicus, 46 mm ML; C, Pyroteuthis addolux, male, 30 mm ML; D, Ancistrocheirus lesueurii, 35 mm ML; E, Gonatus sp., 60 mm ML, tip of claw distorted by fixative; F, Abraliopsis sp. B. female, 27 mm ML; G, Octopoteuthis nielseni, 60 mm ML; H, Ancistrocheirus lesueurii, 35 mm ML; I, Gonatus sp., 60 mm ML.

The arm hooks of the enoploteuthid families (except for the Lycoteuthidae, which lack hooks) are characterized by closed apertures (except in species of Enoploteuthis), lateral lobes and small lips, and a ridged belly (except in species of Pterygioteuthis). These similarities combined with the very different features of the hooks of the other families (e.g., skirts, accessory hooks, circular bases) suggest that hooks evolved independently in the lineage leading to the enoploteuthid families. This brief analysis does not warrant a closer look at evolution within the “enoploteuthid” families due to the general similarity of the hooks and the large degree of variability remaining to be investigated in these groups.

We reduced the above character sets on hooks to only two characters for the phylogenetic analysis below in order to eliminate characters with polymorphic states, or that are autapomorphic, and to reduce excessive weight on hook characters.

CHARACTERS AND CHARACTER STATES FOR PHYLOGENETIC ANALYSIS

The following 13 characters were used in the phylogenetic analysis of the enoploteuthid families.

1. STRUCTURE OF ARM HOOKS.—Character States: 0 = arms without hooks; 1 = arm hooks with skirt in aperture region and with lateral lobes on margin of base; 2 = arm hooks lack skirt and lateral lobes; 3 = arm hooks lack skirt but possess lateral lobes.

Comments: The data for the species examined here are presented in Table 2.

2. STRUCTURE OF TENTACULAR-CLUB HOOKS.—Character States: 0 = tentacular clubs without hooks; 1 = club hooks with skirt in aperture region; 2 = club hooks lack skirts.

Comments: The data for the species examined here are presented in Table 2.

3. NUMBER OF BUCCAL SUPPORTS.—Character States: 0 = buccal crown contains 7 buccal supports; 1 = buccal crown contains 8 buccal supports or their remnants; 2 = buccal crown contains six buccal supports.

Comments: Members of the Decapoda typically have seven buccal supports that, apparently, are derived from an eight-support condition by the fusion of the dorsal pair; the latter condition can be recognized as a transient stage in the development of some species (Naef, 1921, 1923). The four enoploteuthid families are unique in the Teuthoidea in having eight buccal supports, although the dorsal supports have secondarily undergone nearly complete fusion in some pyroteuthids. In Pterygioteuthis microlampas Berry the supports are adjacent but distinct; separate lappets are present. In P. giardi Fischer and Pyroteuthis addolux, however, the lappets appear fused, but separate nerves along the support confirms its double nature. We are unaware of a recent survey of the number of buccal supports in the Teuthoidea; however, in the Octopoteuthidae and some Histioteuthidae (Voss, 1969) fusion of the ventral supports occurs. Naef (1921, 1923) believed that the eight-support condition in the enoploteuthid families represents reversion to the primitive condition, and outgroup comparison supports this contention. The data for the species examined herein are presented in Table 2.

TABLE 2.—Character states for characters 1–13 for the species examined (N = not applicable; ? = character state unknown). Characters: 1 = arm hooks; 2 = tentacular-club hooks; 3 = buccal supports; 4 = buccal connectives; 5 = gladius; 6 = tentacle locking-apparatus; 7 = photophores; 8 = light guides; 9 = buccal pockets; 10 = tail; 11 = buccal membrane surface; 12 = spermatophore receptacles; 13 = hectocotylus.

4. POSITION OF BUCCAL CONNECTIVES.—Character States: 0 = muscular connectives between buccal supports and arms IV attach to ventral borders of arms (IV-v); 1 = muscular connectives between buccal supports and arms IV attach to dorsal borders of these arms (IV-d).

Comments: Character state 1 (IV-d) is found in all members of the enoploteuthid families as well as in the Ommastrephidae, Histioteuthidae, Psychroteuthidae, Architeuthidae, Neoteuthidae, and Bathyteuthidae (Young and Roper, 1968). The ventral attachment is probably the primitive condition because it is widespread in the Oegopsida and is present in the Myopsida and most Sepioidea (Naef, 1921, 1923). This character appears to be one of the most important keys to phylogenetic relationships within the Oegopsida (Chun, 1910; Young and Roper, 1968). See Table 2 for a summary of the character states of species examined.

5. STATUS OF THE CONUS OF THE GLADIUS.—Character States: 0 = primary conus (= true conus) and/or conus field present on gladius; 1 = secondary conus present on gladius; 2 = gladius without primary or secondary conus.

Comments: Members of the enoploteuthid families (with the exception of the Pyroteuthidae) have a gladius (pen) with a primary conus (sensu Toll, 1982). This feature is shared with the Gonatidae, Onychoteuthidae, Architeuthidae, Ommastrephidae, and Neoteuthidae (Toll, 1982). The enoploteuthid families also share the character of an elongate conus field (see Figure 4), although considerable variability exists in the length and shape of the conus field. The conus field (“cone field” of Toll, 1982) is herein defined as an expanded posterior portion of the gladius that is broadly contiguous with the vanes and the small cup-like conus when the latter is present (modified from Toll, 1982). An elongate conus field is found in the Architeuthidae and Neoteuthidae as well. In the Oegopsida a long, pointed rostrum is present on the gladius in members of the Onychoteuthidae, Ancistrocheiridae, and Lampadioteuthis (Lycoteuthidae) (Toll, 1982). Some specimens of Enoploteuthis, Abralia, and Abraliopsis examined, however, had a thickened region at the (posterodorsal) surface of the conus. In Selenoteuthis scintillans Voss a knob is present at the posterior end of the conus (Toll, 1982). If these structures represent reduced rostra, the sporadic occurrence of more typical rostra in the enoploteuthid families does not seem so peculiar.

In the Pyroteuthidae the posterior tip of the squid is highly modified. Toll (1982) suggests that the conus in this group is secondarily derived. If so, it is derived from the cone field rather than from the vane proper and, therefore, differs from the secondary conus of other squids. The presence of an elongate cone field in the pyroteuthid pen indicates an origin in an enoploteuthid-like gladius.

In Loligo opalescens Berry the gladius lacks a conus and conus field; however, the tip of the pen folds back on itself ventrally and gives the false impression of a small conus.

FIGURE 4.—Diagramatic illustration of gladius of Abraliopsis sp. A showing elongate conus field.

Although considerable variability exists in the gladius structure among species of the enoploteuthid families, the long broad vanes, the conus, and the elongate conus field typify this group. These characters, however, are present among the Architeuthidae and Neoteuthidae as well (see Toll, 1982). We have been unable to detect a single derived (apomorphic) character of the gladius unique to the enoploteuthid families. Although the structure of the gladius shows some uniformity among the enoploteuthid families, it exhibits distinctive features within each family (Toll, 1982). See Table 2 for a summary of character states of species examined.

6. POSITION OF THE TENTACLE LOCKING-APPARATUS.—Character States: 0 = tentacle locking-apparatus absent; 1 = tentacle locking-apparatus present on carpus and manus; 2 = tentacle locking-apparatus occurs only on carpus.

Comments: Of the 28 families of the Teuthoidea listed by Clarke (1988), 15 are known to have tentacles with a series of suckers and knobs at the base of the club that form a locking apparatus (i.e., Lycoteuthidae, Enoploteuthidae, Pyroteuthidae, Ancistrocheiridae, Onychoteuthidae, Ommastrephidae, Histioteuthidae, Psychroteuthidae, Architeuthidae, Neoteuthidae, Gonatidae, Thysanoteuthidae, Cycloteuthidae, Brachioteuthidae, and Cranchiidae). The organization of the locking apparatus varies greatly among families. The character states defined herein are simplified. A phylogenetic study of more families will need to define additional character states. In the Ommastrephidae a locking apparatus is absent except for members of the Ommastrephinae. A locking apparatus that consists only of a carpal cluster (state 2) is found exclusively in the enoploteuthid families and in the Onychoteuthidae. All members of the enoploteuthid families examined herein have compact, oval carpal clusters except Enoploteuthis reticulata Rancurel, which has a compressed tentacle and, as a result, a compressed locking apparatus (Burgess, 1982), and Lycoteuthis diadema (of the two specimens examined only the small 25 mm ML squid had an intact tentacle), which has a compact cluster that is skewed toward the anteriodorsal margin of the stalk and, thereby, approaches character state 0. In families that have a locking apparatus on the manus, the locking apparatus is usually found along the proximal dorsal margin. See Table 2 for a summary of character states of species examined.

7. POSITION AND STRUCTURE OF PHOTOPHORES.—Character States: 0 = all 4 “pyroteuthid” features absent; 1 = all 4 “pyroteuthid” features present (i.e., photophores present on surface of tentacles, eyeballs, and viscera at gill bases, on either side of anus, and in posterior midline; some tentacle photophores double; photogenic tissue with microvillous blood vessels; some photophores with caps of iridiophore plates).

Comments: Photophores are present in all families of concern to this study, although in the Gonatidae photophores are known in only one species (Gonatus pyros Young with one photophore per eye), and in the Onychoteuthidae they are known in only one genus, Onychoteuthis (also Chaunoteuthis for those that retain this taxon as distinct). Photophores are lacking in Loligo opalescens and in most loliginids, although some species have bacterial photophores on the viscera (Herring, 1977). Photophores in the Histioteuthidae, Ommastrephidae, Lycoteuthidae, Enoploteuthidae, and Pyroteuthidae have been well studied (Arnold and Young, 1974; Arnold et al., 1974; Girsch et al., 1976; Dilly and Herring, 1981; Butcher et al., 1982; Young and Arnold, 1982; Herring et al., 1985; Young and Bennett, 1988), and the basic structure is known in the Ancistrocheiridae (Young, 1977). Although the photophores in the Onychoteuthidae and Gonatidae have not been examined with electron microscopy, their photophores appear, at least superficially, to be very different from those of the other families (pers. obs.). We have based character states for the species examined herein (Table 2) on the literature and on unpublished histological and ultrastructural studies of the ocular photophores of Pyroteuthis addolux, the mantle photophores of Ancistrocheirus lesueurii, Enoploteuthis reticulata, Enoploteuthis higginsi Burgess, Abraliopsis sp. A, Abraliopsis sp. B, and Histioteuthis dofleini (Pfeffer), and the dorsal mantle photophore of Sthenoteuthis oualaniensis (Lesson).

In the Ancistrocheiridae, Enoploteuthidae, Histioteuthidae, and Ommastrephidae (subfamily Ommastrephinae), numerous photophores are present on the surfaces of the mantle, head, and arms. In addition, they are located on the funnel, fins, and tentacles in the Ancistrocheiridae, on the eyes in the Enoploteuthidae, and in a wide variety of locations in the Ommastrephidae (Herring, 1977). In the first three of these families, the surface photophores appear to have originated within the integument as evidenced by both their superficial position and the incorporation of chromatophores into the organs. In the Ommastrephidae they seem to be subintegumental in origin, being generally found embedded in the mantle musculature and lacking incorporation of chromatophores within the structure of the organs. In all four families, the photophores are very different in structure. In the Histioteuthidae photocytes contain massive arrays of rough endoplasmic reticula, iridophores in the posterior cup reflector have platelets with central membranes, and a distal color filter is present that is composed of dense whorls of smooth endoplasmic reticula (Butcher et al., 1982). In ommastrephids the photocytes have not been identified with certainty. The photogenic tissue contains large areas of amorphous, electron-dense material and the general photophore structure is not highly organized optically (Girsch et al., 1976). Photophores in the Enoploteuthidae are extremely complex and are characterized by precisely structured collagen reflectors, collagen light guides, diffusers, and filters of stacked or rolled plasma membranes, and photocytes with large crystalloids (Young and Arnold, 1982; Young and Bennett, 1988; pers. obs.). In ancistrocheirids photocytes do not have a distinctive appearance. The simple photophores in these squids have a photogenic mass backed by a simple reflector composed of iridophore platelets with central membranes. The larger, more complex photophores have additional light guides consisting of concentric iridophores positioned like closely packed petals on a flower (Young, 1977; pers. obs.).

In the Lycoteuthidae and the Pyroteuthidae, photophores are located in nearly identical positions on the viscera, eyes, and tentacles. In addition, photophores can be present in the integument of some lycoteuthids (Förch and Uozumi, 1990). In both families the ocular photophores are represented during development first by a single, centrally located photophore on each eye (Nesis, 1975; Voss and Stephen, 1992; pers. obs.). This contrasts with the condition in the Enoploteuthidae in which ocular photophores first appear as a set of two or three organs (Young et al., 1992). Features that are unique to the Lycoteuthidae and Pyroteuthidae are the double nature of some tentacular photophores, the photogenic tissue consisting of roughly spherical photocytes with rather uniform cytoplasm and with interspersed microvillous blood vessels, and the presence of oval iridophore platelets without central membranes that form caps over some photophores (ocular and anal). The striking similarity in the structure of the photophores of these two families was first noted by Herring et al. (1985). The presence of collagen as light guides in some photophores in these two families is also seen in the Enoploteuthidae.

The Histioteuthidae, Ommastrephidae, Enoploteuthidae, Ancistrocheiridae, Gonatidae, and Onychoteuthidae exhibit little similarity in the structure of their photophores. Except in the enoploteuthid + pyroteuthid + lycoteuthid line, therefore, photophores apparently have evolved separately within each family lineage. Although enoploteuthid photophores are very different from those of the Pyroteuthidae and Lycoteuthidae, the common presence of collagen fibers as light guides in the photophores of these three families is a shared characteristic (synapomorphy). See Table 2 for a summary of character states of species examined.

8. COLLAGEN LIGHT-GUIDES IN PHOTOPHORES.—Character States: 0 = photophores lack collagen light-guides; 1 = some photophores possess collagen light-guides.

Comments: As indicated by comments under character 7, collagen light-guides are known only in photophores of the families Enoploteuthidae, Lycoteuthidae, and Pyroteuthidae. See Table 2 for a summary of character states of species examined.

9. CONNECTIONS OF THE BUCCAL POCKETS.—Character States: 0 = all buccal pockets separate with possible exception of pockets IV; 1 = “ring-canal” present that joins with pockets II and IV and passes beneath pockets III; 2 = “ring-canal” present that joins with pockets IV and passes beneath pockets II and III.

Comments: The buccal membrane attaches to an adjacent arm by a buccal connective. From this connective a delicate, transparent membrane extends to the base of the arm and buccal mass. In this manner a pocket is formed between successive connectives and the arm and the buccal mass. The pockets are sealed from one another by the membranes. In species where the dorsal buccal supports have fused, pocket I does not exist. Pocket II is associated with arm I (between the dorsal margin of arm I and the dorsal margin of arm II). Pocket III is associated with arms II and III (because the buccal connective attaches to the dorsal margin of arm II and the ventral margin of arm III). Pocket IV includes the tentacle (between the ventral margin of arm III and either the dorsal or ventral margin of arm IV). Pocket IV is not to be confused with the “tentacular pocket,” which is a different structure, although the two are physically connected. Pocket V lies between the two arms IV. The latter pocket is often not well developed when the attachments to arms IV are ventral or when the ventral buccal supports have fused. In some cases, the floor of a pocket, a membrane, is not as deep as it could be, and in some cases, individual pockets are not sealed. Thus, in some species, large spaces or “canals” exist that allow pockets to be in communication near their bases. Sometimes this communication between pockets extends beneath the floor of some intervening pockets and encircles the buccal mass to form a “ring canal.”

The connection between pockets IV is obvious in some species but is difficult to detect in others. As a result we have not differentiated between these conditions. States 1 and 2 are similar in having a continuous space or ring canal that surrounds the buccal mass and connects with some pockets but passes beneath others. The only difference between these two states is whether or not pocket II is continuous with the ring.

There is considerable variability in the occurrence of the different states among genera and families (Table 2). Nevertheless, within the enoploteuthid families, the derived condition of a ring canal occurs only in the Pyroteuthidae and Lycoteuthidae. The familial character states (Table 3) for this character were derived solely from data on the species examined and are presented in Table 2.

10. LENGTH OF THE FLESHY TAIL.—Character States: 0 = fleshy tail extends 3% or less of gladius length (GL) from posterior tip of gladius (excepting rostrum) to tip of tail; 1 = fleshy tail extends more than 6% of GL from posterior tip of gladius (excepting rostrum) to tip of tail.

Comments: Naef (1921, 1923) termed a structure at the posterior end of the mantle the fleshy apex to the mantle, and indicated that, primitively, it was supported by the rostrum of the gladius. A tail includes any extension of the body posterior to the fins proper (see Young and Roper, 1968). In some cases, the tail is only the conus (often a “secondary conus” sensu Toll, 1982) covered by integument, whereas in others it is a long fleshy projection without a conus or rostrum. In many cases, the “fleshy apex” and “fleshy tail” are synonymous; however the relationship between these in all cases is unclear. The fleshy tail has an operational definition; more careful study of this region of squid may eventually allow more precise character definitions. Although the fleshy tail can be very muscular, it is a distinct structure and is not a continuation of the mantle musculature.

Considerable variation exists in the length of the fleshy tail beyond the tip of the gladius. A large tail extends well posterior to the tip of the gladius (i.e., 13%–15% of GL) in the Enoploteuthidae and is characterized by having a vacuolated structure. A narrow extension of the fins reaches to the tip of the tail in all specimens except species of Enoploteuthis. Members of Enoploteuthis are noted within the Enoploteuthidae for their long tails, although the tail is only marginally longer than in other genera. The fin, however, is situated a bit more forward than in other genera, and its extension terminates posteriorly at the level of the conus of the gladius. This position gives the impression of a longer tail.

TABLE 3.—Character states for characters 1–13 for the species examined (N = not applicable; ? = character state unknown). Characters: 1 = arm hooks; 2 = tentacular-club hooks; 3 = buccal supports; 4 = buccal connectives; 5 = gladius; 6 = tentacle locking-apparatus; 7 = photophores; 8 = light guides; 9 = buccal pockets; 10 = tail; 11 = buccal membrane surface; 12 = spermatophore receptacles; 13 = hectocotylus.

In the female specimen of Lycoteuthis diadema that we examined, the fleshy tail was damaged but extended well beyond the gladius (7% GL) and was very muscular except for a solid homogeneous core that could be extracellular material. In male L. diadema the tail is even longer (Toll, 1983). In Onychoteuthis borealijaponicus the fleshy tail extends beyond the conus (3% GL) and is supported for most of its length by the rostrum of the gladius. In some onychoteuthids (e.g., Ancistroteuthis and Moroteuthis), however, a long tail supported by a large rostrum is present. In Sthenoteuthis oualaniensis the muscular fleshy tail extends only a short distance beyond the conus (2% GL) and attaches anteriorly to a cartilaginous ring that surrounds the conus. In all three of these genera, the fin appears to extend to the tip of the tail. In Gonatus sp. a long fleshy tail is present that extends well posterior to the tip of the gladius (13% GL). It is muscular but less so than in Lycoteuthis diadema, and it possesses a gelatinous core. The extension of the fins reaches to the tip of the tail. In the Pyroteuthidae the tail, which extends posterior to the fins, consists only of the conus of the gladius covered by the integument so that no fleshy extension is present. In Ancistrocheirus lesueurii the broad tail is gelatinous but contains numerous isolated muscle fibers and no vacuoles. In the adult the fleshy tail extends well posterior to the conus (about 15% GL) and is partially supported by the rostrum. The fin extensions appear to terminate slightly in advance of the tail tip. In Histioteuthis dofleini the tail is nearly absent, whereas in Octopoteuthis nielseni the posterior body superficially resembles the tail of Ancistrocheirus in size and shape; however, both the pen and the mantle muscle extend nearly to the posterior tip leaving at best a very small tail (∼2% GL). In Loligo opalescens a fleshy tail is virtually absent.

Enoploteuthids and ancistrocheirids have similar large, fleshy, weakly muscular tails; however, they differ in the occurrence of vesicles. See Table 2 for a summary of character states of species examined.

11. ORNAMENTATION OF THE BUCCAL MEMBRANE SURFACE.—Character States: 0 = oral surface of buccal membrane smooth or raised into series of ridges; 1 = oral surface of buccal membrane raised into numerous papillae or ridges and papillae.

Comments: Little is known about the function of the buccal membrane in general or about the ridges that usually cover its oral surface. Because the latter are covered with secretory cells (Chun, 1910), however, and because a mucous-like material is frequently found over this surface in preserved specimens, mucous secretion is, apparently, one function of these structures. In state 1 the surface may be raised into long, conical or club-shaped papillae that, in general, do not join other papillae at their base or, occasionally, it may be raised into mostly ridges but with scattered, club-shaped papillae. The unusual occurrence of the papillae in enoploteuthids and lycoteuthids was first noted by Chun (1910).

Enoploteuthis (as usual) differs from other members of the Enoploteuthidae in being polymorphic for this character (Table 2). Enoploteuthis reticulata has slender ridges and some specimens approach a smooth state (i.e., lack of all ornamentation). Enoploteuthis jonesi Burgess has ridges, but E. higginsi has short, broad papillae, some of which, however, are irregular in shape. Other members of the family have state 1, with virtually only papillae. This papillate state is shared with the specimens of Lycoteuthis diadema. The buccal membrane of Pterygioteuthis microlampas is covered mostly with broad but short papillae sometimes with irregular shapes or forming short ridges. In contrast, Pterygioteuthis giardi and Pyroteuthis addolux have mostly ridges on their membranes. Clearly, this character is polymorphic in the Pyroteuthidae. See Table 2 for a summary of character states of species examined. In addition to the families represented in Table 2, we were able to examine representatives of 14 more families for this feature. The only families in the Teuthoidea that we did not examine were the Architeuthidae, Batoteuthidae, and Promachoteuthidae. Joubiniteuthis portieri (Joubin) is the only species in these 14 families that has papillae. In this species, scattered papillae are interspersed among ridges. As a result, we place considerable phylogenetic significance on the presence of papillae.

12. LOCATION OF THE SPERMATOPHORE RECEPTACLES.—Character States: 0 = discharged spermatophores or sperm masses attached to oral surface of buccal membrane or to lips; 1 = discharged spermatophores attached in nuchal region; 2 = discharged spermatophores attached at posterior junction of retractor muscles of head and funnel; 3 = discharged spermatophores attached to long slits on ventral surface of mantle wall.

Comments: Discharged spermatophores are frequently found attached to female squids after copulation. The sites of attachment are sometimes modified as distinct receptacle organs. Unfortunately, in order to determine storage sites, generally one must examine mature females; in many species mature females are unknown.

The precise position of the specialized, rugose, and usually pigmented pockets that are found in the nuchal region of enoploteuthids, ancistrocheirids, and lycoteuthids can be one of several locations where spermatophores are attached along the nuchal cartilage (see Burgess, 1998). Spermatophore attachment sites often occur beneath the collar or posteriorly between the stellate ganglia (i.e., immediately ventral to the gladius and just above the digestive gland). In state 2, found only in Enoploteuthis, the receptacles also are specialized pockets. These pockets are similar in appearance to those in the nuchal region of other enoploteuthids but are located farther posteriorly and laterally. Although our specimens of Onychoteuthis and Gonatus were immature, data from the literature indicate state 3 for the former (Nesis, 1970; Okutani and Ida, 1986) and state 0 for the latter (Young, 1973). In the ommastrephid Illex coindetii (Verany), discharged spermatophores are found attached to the inner surface of the mantle wall on either side of the gill (Steenstrup, 1881). In Loligo opalescens, as in other loliginids, discharged spermatophores or sperm masses can be found in a pouch on the midventral, oral surface of the buccal membrane.

States 1 and 2 were found only in the enoploteuthid families (Table 2). In the Enoploteuthidae, variation in the exact location of the pockets can be found in different species in the same genus (Abralia and Abraliopsis). We suspect that the unique position of the receptacles in Enoploteuthis (state 2) is secondarily derived from a nuchal position. The Pyroteuthidae, in contrast, exhibited a consistent arrangement of the receptacle with the opening to the pocket always between the stellate ganglia. See Table 2 for a summary of character states of species examined. Not all character states are represented by the species examined; the unutilized character state 3 is needed when literature data is added to compile Table 3.

13. POSITION OF HECTOCOTYLIZED ARMS.—Character States: 0 = hectocotylization lacking; 1 = one or both arms IV hectocotylized.

Comments: Hectocotylization involves modification of the arms for the purpose of transferring spermatophores. A variety of sexually dimorphic modifications may occur on the arms of males or females; however, these could serve purposes such as sexual attraction or grasping for copulation and, therefore, do not meet the definition of hectocotylization. Hectocotylization is unknown in the families Onychoteuthidae (Naef, 1921, 1923), Octopoteuthidae, and Gonatidae. One (rarely both) of the ventral arms (arms IV) is hectocotylized in the Loliginidae, Ommastrephidae, Enoploteuthidae, and Pyroteuthidae (Naef, 1921, 1923). The condition in the Ancistrocheiridae is unknown, and in the Lycoteuthidae the condition is polymorphic for character states 0 and 1 (Young, 1964). In the Histioteuthidae symmetrical modification of arms I, termed secondary sexual modification (Voss and Voss, 1983), in the males of all species (Voss et al., 1998) is thought not to be hectocotylization (N. Voss, pers. comm., 1988). See Table 2 for a summary of character states of species examined.

CLADISTIC ANALYSIS OF CHARACTERS

We constructed a data matrix for families (Table 3) based on Table 2 and the literature. We analyzed this matrix using PAUP (N in the data matrix is not allowable in PAUP and was replaced by a “?”) under an exhaustive search for the shortest tree lengths (i.e., trees that required the fewest number of evolutionary changes in their construction). Character states were defined as unordered, reversible, undirected, unpolarized, and unweighted. Multistate taxa were interpreted as uncertain for the purpose of computing tree lengths. Trees were unrooted for searching but were rooted for printing by the outgroup (Loliginidae). Comments concerning possible polarization, above, are for informational purposes; characters were not polarized in the final PAUP analysis. Tree lengths ranged from 28–48. Surprisingly, a unique tree was found at the minimum tree length of 28 (consistency index (C.I.) = 0.75). This tree supported the monophylogeny of the enoploteuthid families, defined interrelationships among these four families (Figure 5), and defined the relationships of all other families. At a tree length of 29, 23 trees were found (C.I. = 0.724). The trees showed considerable variation in the placement of families outside the enoploteuthid line, and a strict consensus tree (Figure 5; tree length = 33, C.I. = 0.636) constructed from the 23 trees showed the non-enoploteuthid relationships to be unresolved. The four internal nodes on this tree are designated 1 through 4 in Figure 5. Between the Loliginidae and node 1, changes occur in characters 5, 6, and 13. Between nodes 1 and 2, which defines the enoploteuthid line, changes occur in characters 1, 2, 3, 4, 6, 10, 12, and 13. Between nodes 2 and 3, which defines the enoploteuthid + pyroteuthid + lycoteuthid lineage, changes occur in characters 8 and 11. Between nodes 3 and 4, which defines the pyroteuthid + lycoteuthid lineage, changes occur in characters 2, 7, and 9. At a tree length of 30, 194 trees were found (tree length = 37, C.I. = 0.568). A strict consensus tree of this set showed that the monophylogeny of the enoploteuthid families was maintained but revealed no other phylogenetic relationships. At a tree length of 31, 836 trees were retained, and a strict consensus tree (tree length = 48, C.I. = 0.438) contained no phylogenetic information.

FIGURE 5.—Strict consensus phylogenetic tree generated by PAUP from data in Table 3.

Discussion

We consider the single tree found by the cladistic analysis at a tree length of 28 not to be a true reflection of the phylogenetic relationships of all the families analyzed. The number of characters analyzed is insufficient to produce a definitive phylogeny of all these families. We consider the consensus tree (Figure 5) derived from trees with a length of 29 to most accurately reflect our present understanding of the phylogeny of these families.

All trees of a length of 28, 29, or 30 supported the monophylogeny of the enoploteuthid families. Their relationships are especially supported by the apparent synapomorphic features of eight buccal supports, similarity of arm and tentacle hooks, possession of a carpal locking-apparatus on the tentacles, and the nuchal position of the spermatophore receptacles. The consensus tree includes three other character changes (i.e., characters associated with the buccal connectives, the tail, and the hectocotylus). A broader analysis of more families, however, may show these to be pleisiomorphic at this level. Within this group of families, all trees of lengths less than 30 supported a sister relationship between the Lycoteuthidae and Pyroteuthidae. The close relationship between these two families was demonstrated by synapomorphies in the distribution and structure of the photophores and in the presence of a buccal canal. An additional character that was not included in the analysis, the appearance first of a single midventral photophore in the developmental sequence of the ocular photophores, also separates these families from the Enoploteuthidae. The similarity in photophore characters between the Lycoteuthidae and Pyroteuthidae is remarkable in view of the very different general morphology exhibited by these species. The photophore features could have been coded as a series of separate characters, which would have united these families even more strongly in the analysis. The monophyly of the enoploteuthid + lycoteuthid + pyroteuthid lineage is supported by the presence of buccal membrane papillae and the presence of collagen light-guides in the photophores.

This analysis is a first look at the relationships of the enoploteuthid families. Future analyses should add new characters as well as extend characters used here to additional species. A broader-based analysis that includes more families and could reliably assign polarity to each character should be able to better define some of the relationships left weakly resolved (i.e., position of the Ancistrocheiridae). Of special importance would be the determination of a sister group to the enoploteuthid families.

The phylogeny presented here is inconsistent with the classification in use prior to Clarke's changes because the Enoploteuthidae, as previously defined, was not monophyletic because it excluded the lycoteuthids. One solution to this problem is to raise all three subfamilies of the Enoploteuthidae to familial status as Clarke (1988) has done.

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A Survey of Seminal Receptacles in the Enoploteuthidae

Lourdes Alvina Burgess

____________

Lourdes Alvina Burgess, 106 Lexington Court, Red Bank, New Jersey 07701, United States.

ABSTRACT

The structure and location of the seminal receptacles of 14 species of Abralia, eight species of Abraliopsis, three species of Enoploteuthis, and Watasenia scintillans (Berry), of the family Enoploteuthidae, are described. Although the receptacles in Abralia, Abraliopsis, and Watasenia are situated on the dorsal side of females in the proximity of the collar, they exhibit variability in specialization and position. The receptacles of Enoploteuthis are less specialized and are situated elsewhere within the mantle cavity.

Introduction

HISTORICAL REVIEW

When Steenstrup (1880:67, pl. 3) discussed the differences in the placement of discharged spermatophores between myopsid and oegopsid families, he gave as examples the enoploteuthid Enoploteuthis veranyi Rüppell (= Abralia veranyi) and the ommastrephid Illex coindetii (Verany). He found that the seminal vesicles (sperm reservoirs of discharged spermatophores) are deposited in the nuchal area of A. veranyi. A cushion-shaped pad lies posterior to the nuchal cartilage. The seminal vesicles are deposited there in the form of a rosette. Another cluster of seminal vesicles is attached on the inner surface of the mantle near the gladius. The first location was confirmed by both Berry (1926) and Adam (1952).

Ishikawa (1913:171) found that mature females of Watasenia scintillans (Berry) bear a number of discharged spermatophores in a pocket-like depression on each side of the neck or nape. Sasaki (1914, pl. 2: fig. 6) illustrated in detail the structure of these depressions. The seminal vesicles are deposited beneath the collar on the uppermost corner on each side of the nuchal cartilage (see Figure 1f).

The recently described Abraliopsis pacificus Tsuchiya and Okutani, 1990, has seminal receptacles similar to those of Watasenia scintillans. The authors’ description included comments on the structure (p. 53) and an illustration (fig. 12) of the receptacles.

In the genus Enoploteuthis, the presence of spermatophores (seminal vesicles) on the dorsal side of the neck below the mantle, close to the nuchal cartilage, was reported by Ishikawa (1914:409, pl. 38: fig. 6) in his description of Enoploteuthis chunii. Burgess (1982:713) mentioned the presence of seminal vesicles in Enoploteuthis octolineata; spent spermatophores were attached to the inner wall of the funnel retractor muscle.

Young and Harman (1998) stressed the importance of the seminal receptacles of enoploteuthids in support of the elevation of the subfamily Enoploteuthinae to family level by Clarke (1988). They found (1) a specialized pocket just beneath the gladius between the stellate ganglia in Abralia trigonura and in Abraliopsis sp. A, (2) pockets underneath the collar on each side of the nuchal cartilage in Abraliopsis sp. A and sp. B, with sp. A having both median and side pockets present, and (3) a pocket at the junction of the head retractor and funnel retractor muscles in two species of Enoploteuthis, E. jonesi and E. reticulata (see Young and Harman, 1998).

MATERIAL EXAMINED

Specimens, including holotypes and paratypes, of several enoploteuthid genera from various institutions were examined during the Cephalopod International Advisory Council (C.I.A.C.) Workshop sponsored by the Smithsonian Institution, in Washington, D.C., during July 1988. Female specimens examined are listed below for each genus; specimen size is reported as dorsal mantle length (ML).

The following abbreviations refer to depositories of specimens examined: ANSP, Academy of Natural Sciences, Philadelphia; IOM, l'Institute Oceanographique, Monaco; MCZ, Museum of Comparative Zoology, Harvard University; MVA, Museum of Victoria, Australia; NMNH, National Museum of Natural History, Smithsonian Institution (which houses the collections of the former United States National Museum (USNM)), Washington, D.C.; NMV, Naturhistorischen Museum, Vienna; NSMT, National Science Museum, Tokyo; UMML, Rosenstiel School of Marine and Atmospheric Science, University of Miami, Florida; ZMUC, Zoological Museum, University of Copenhagen.

FIGURE 1.—a, diagrammatic illustration of median seminal receptacle in Abralia spp., mantle pulled back; b, lateral view of (a) with attached seminal vesicles, mantle lifted off; c, exposed seminal receptacle under collar in Abralia spp.; d, dorsal view of (c), undissected; e, lateral and median positions of seminal receptacles in Abraliopsis spp. exposed as in (a);f, exposed seminal receptacle with attached vesicles in Watasenia.

Structure and Location of Seminal Receptacles in the Enoploteuthidae

(The data presented in this section are summarized in Table 1.)

Abralia Gray, 1849

SPECIMENS EXAMINED.—Abralia andamanica Goodrich: 41 mm ML, MVA F50745, NW shelf, S. DeLa sta 82/19, S02/82, 18°08′S, 118°04′E, ident. by C.C. Lu. Abralia armata (Quoy and Gaimard): 35 mm ML, MVA, “Hai Kung,” 12°39′S, 127°03′E, a 12°39′S, 127°06′E, Mar 1981, ident. by C.C. Lu. Abralia astrolineata Berry: holotype, 34 mm ML, NMNH, USNM 816428, South Pacific, Kermadec Ids.; NMNH, no cat. no, 45 mm ML, New Zealand (from D. Riddell). Abralia grimpei Voss: holotype, 27 mm ML, MCZ, R/V Atlantis sta RHB-551, 20°25′N, 79°45′W, 6 Feb 1967. Abralia marisarabica Okutani: paratype, 25.5 mm ML, NSMT Mo-31361, R/V Shoyo-Maru, Arabian Sea, 24°48′N, 63°20′E, 2 Dec 1976. Abralia multihamata Sasaki (= lucens Voss): paratype, 48 mm ML, ANSP, Fanning Id., J. McGowan, leg., 5 Jun 1951; paratype, 43 mm ML, ANSP, Christmas Id., Line Ids., 6 May 1937. Abralia redfieldi Voss: holotype, 29 mm ML, MCZ 203979, UMML sta SL23B, off Gun Cay, Bahamas, 10 Dec 1953. Abralia robsoni Grimpe: holotype, 51 mm ML, ZMUC, Bonomisaki, Japan, Mortensen's Pacific Exped. 1914–1915, 13 May 1914. Abralia similis Okutani and Tsuchiya: 29 mm ML, NMNH, USNM 729686, R/V Townsend Cromwell sta 46–85, 0°02′N, 144°55′W, 10 Nov 1969. Abralia spaercki Grimpe: holotype, 47 mm ML, ZMUC, Amboina Bugten, Kysten von Sawrude, Th. Mortensen, leg., 1922; 48 mm ML, NMNH, R/V Albatross, Bagacay Bay, Escarpada Id., Naranjon between Samar and Masbate, 12 Mar 1909. Abralia steindachneri Weindl: holotype, 49 mm ML, NMV 5587, “Pola” Exped., Shadwan, Red Sea, 19 Feb 1896. Abralia trigonura Berry: 35 mm ML, NMNH, USNM 729728, R/V Townsend Cromwell sta off Kawaihai, Hawaii, 23 Aug 1964. Abralia veranyi (Rüppell): 35 mm ML, UMML 31.2244, R/V Pillsbury sta 263, 2°37′N, 8°36′E, 16/17 May 1965, ident. by G.L. Voss. Abralia sp. A (Burgess, MS): 5 specs, 31–35 mm ML, NMNH, USNM 729719, R/V H.M. Smith sta 47–51, 0°56′N, 149°46′W, 2 Nov 1958.

TABLE 1.—Location of seminal receptacles in Abralia, Watasenia, Abraliopsis, and Enoploteuthis.

OBSERVATIONS.—A distinct, deep pocket attached to the inner wall of the mantle, near the anterior end of the gladius and the posterior edge of the nuchal cartilage, between the stellate ganglia, was observed in A. andamanica, A. robsoni, and A. trigonura (Figure 1a). The receptacle of A. trigonura has very rugose walls. The seminal vesicles (3–4 mm long, about 0.16 mm in diameter) are attached close together, like a rosette, to the inner wall of the mantle near the gladius (Figure 1b). Some receptacles have thin walls and require careful handling. In contrast, a deep pocket is absent in a specimen of Abralia veranyi from the Atlantic identified by G.L. Voss and is absent in Abralia sp. A (Burgess, MS). In both of these species a thick, almost round, slightly rugose pad is firmly attached to the posterior one-half of the nuchal cartilage. The inner wall of the mantle just ventral to the gladius also is rugose. Seminal vesicles are present in the form of a rosette on the surface of the pad. One Abralia sp. A specimen (31 mm ML) has a distinct but almost smooth pad, smooth inner mantle surface, and is missing seminal vesicles, but it possibly is not a fully mature specimen.

Other species of Abralia have the seminal receptacles in a different area. The seminal vesicles are attached on each side of the nuchal cartilage, under the collar, as in Watasenia, but not in the identical positions. In Watasenia the seminal receptacle is a dark and rugose pocket that is located on the inner surface of the collar at the anterior corner of the nuchal cartilage (Figure 1f). In the remaining species of Abralia (A. armata, A. astrolineata, A. astrosticta. A. grimpei, A. marisarabica, A. multihamata, A. redfieldi, A. similis, A. spaercki, A. steindachneri), the receptacles are oval, rugose pockets on the inner surface of the collar on each side of the nuchal cartilage (Figure 1c), often very dark in color. These pockets are not firmly attached and are easily damaged in preserved specimens. In mature specimens either the seminal vesicles or remnants of vesicles are present. These receptacles could be observed through the thin collar in some specimens (Figure 1d).

Seminal vesicles were rarely present in the specimens examined (possibly already spent). When present, they are opaque, white, and small, about 3 mm long, and are completely concealed under the collar. The seminal receptacles of the specimen of A. astrolineata from D. Riddell are well developed, very darkly pigmented, and have a rugose surface, whereas the holotype of this species has indistinct pockets. This is certainly related to an age difference between a mature female of 45 mm ML and an immature one of 29 mm ML. The receptacles of A. marisarabica and A. spaercki are light in color (possibly the effect of preservation) and have only small chromatophores. From the outside of the collar, they appear as whitish oval areas on each side of the nuchal cartilage. The receptacles of A. armata, A. multihamata (= lucens), and A. similis are very dark. They can be detected externally as dark spots on the surface of the collar. The receptacles of A. redfieldi are soft and are not firmly attached. The holotype of A. grimpei has darkened in preservation so that the exact condition of the receptacles is difficult to determine; however, a mass of whitish material is present under the collar. The receptacles of A. astrosticta are almost round rather than the predominant oval shape (pers. obs.). According to K. Tsuchiya (Tokyo Univ., pers. comm.), the seminal receptacles also are situated under the collar in Abralia similis from the Northwest Pacific. The receptacles are almost triangular in outline, and the surfaces are slightly rugose.

Watasenia Ishikawa, 1914

SPECIES EXAMINED.—Watasenia scintillans (Berry): 48 mm ML, NMNH, USNM 332900, R/V Albatross, North Pacific, Japan, Honshu, Sendai, Kinka San Lt., 38°09′24″N, 141°52′30″E; 3 females, NMNH, North Pacific, Japan, 36°46′N, 139°20′E, 1913.

OBSERVATIONS.—The above specimens all have seminal receptacles under the collar in the exact location illustrated and described by Sasaki (1914). The seminal vesicles are small and are attached very close together (Figure 1f). The area of attachment is rugose and is dark in color.

Abraliopsis Joubin, 1896,

SPECIES EXAMINED.—Abraliopsis affinis (Pfeffer): 25 mm ML, NMNH, USNM 813134, R/V Townsend Cromwell sta 44–24, 07°32.9′N, 144°58′W, 13 Aug 1969. Abraliopsis gilchristi Robson: 35 mm ML, M94104, R/V Kaiyo Maru sta km/106/B/85, 42°08.6′S. 170°29.9′E, 23 Jul 1985 (from E. Förch, Ministry of Agriculture and Fisheries, New Zealand). Abraliopsis lineata Goodrich: 29 mm ML, Hol-Nr2, sta 501, 18°57′N, 66°36′E, 13 May 1987 (from U. Piatkowski, Kiel University, Germany). Abraliopsis pfefferi (Joubin): 35 mm ML, IOM 235306, sta 3202. Abraliopsis sp. A, Burgess, MS: 35 mm ML, NMNH, USNM 729709, R/V Townsend Cromwell sta 7–5, North Pacific, off Waianae, Oahu, Hawaii, 12 Aug 1971. Abraliopsis sp. B, Burgess, MS: 23 mm ML, NMNH, USNM 729703, R/V Townsend Cromwell sta 7–18, North Pacific, off Keahole Pt., Hawaii, 19 Aug 1964. Abraliopsis sp. C, Burgess, MS: 33 mm ML, NMNH, USNM 729715, R/V Townsend Cromwell sta 44–18, North Pacific, 11°53.2′N, 144°58′W, 11 Jul 1969, Abraliopsis sp. D, Burgess, MS: 40 mm ML, NMNH, USNM 729705, R/V Townsend Cromwell sta 44–56, 0°16.2′S, 144°43.9′W, 29 Jul 1969.

OBSERVATIONS.—Three conditions of spermatophore placement were observed: (1) two pockets under the anterior end of the collar, one on each side of the nuchal cartilage, similar to Watasenia (Figure 1f); (2) under the collar as in (1) and in a median receptacle at the posterior end of the nuchal cartilage, thus totaling three sites (Figure 1e); and (3) in a single median position, similar to the condition found in some Abralia spp. (Figure 1a).

Abraliopsis pfefferi and Abraliopsis sp. B have receptacles under the collar, one on each side of the nuchal cartilage, and do not have a median receptacle. The surface of the area where the seminal vesicles are attached is rugose and darkly pigmented. A dark spot (concentration of chromatophores) is present on each side of the nuchal cartilage directly above the rugose area. These dark spots were described and illustrated by Joubin (1896:24, fig. 3) in the holotype of A. pfefferi.

FIGURE 2.—a, seminal receptacles with vesicles in Abraliopsis gilchristi. mantle pulled back and collar muscle on right side dissected; b, exposed seminal receptacle in Enoploteuthis galaxias, posterior at bottom; c. seminal vesicles in position in Enoploteuthis reticulata.

The species examined that have three sites for seminal vesicle deposition are Abraliopsis affinis, A. gilchristi, A. lineata, A. sp. A, and A. sp. D. The seminal vesicles, except those of A. gilchristi, are very small. They are rarely more than 3.0 mm long and are only about 0.2 mm in diameter. Those situated under the collar, being small and short, are completely hidden from view. The seminal vesicles of A. gilchristi are quite large, 5–6 mm long and 0.5 mm in diameter, and extend beyond the edge of the collar and median receptacle (Figure 2a). The dark spot on each side of the nuchal cartilage is prominent in all the specimens.

Only Abraliopsis sp. C has a well-developed median receptacle posterior to the nuchal cartilage. This median pocket has rugose walls, and the seminal vesicles are 2.0 mm long and 0.2 mm in diameter. Dissection of the collar showed neither seminal vesicles nor a dark pigmented rugose surface.

Enoploteuthis Orbigny, 1848

SPECIES EXAMINED.—Enoploteuthis galaxias Berry: 125 mm ML, MVA, South Pacific, 33°36′S, 153°00′E. Enoploteuthis higginsi Burgess: adult female, North Pacific, Hawaii, 40°N, 157°W, 75 m deep (from R.E. Young). Enoploteuthis reticulata Rancurel: adult female, North Pacific, Hawaii (from R.E. Young).

OBSERVATIONS.—The placement of seminal vesicles at the junction of the funnel and head retractor muscles is characteristic of the following species: Enoploteuthis galaxias, E. higginsi, and E. reticulata. Separation of the funnel and head retractor muscles at their junction was required (Figure 2b, c) to expose the seminal receptacle. The area is only slightly rugose. The same area is smooth in a male E. galaxias examined from the same locality for comparison. Enoploteuthis jonesi has the same kind of receptacle (Young and Harman, 1998).

Discussion

The seminal vesicles are stored in the nuchal region in Abralia, Watasenia, Abraliopsis, and in one species of Enoploteuthis (E. chunii). A deep pocket may be present in a medial position (ventral to the gladius. between the stellate ganglia) in Abralia and Abraliopsis, but it is absent in Watasenia. In Abralia veranyi and Abralia sp. A, a median pocket is absent; however, the seminal vesicles are attached to the posterior part of the nuchal cartilage and to the inner wall of the mantle, ventral to the gladius. The storage of seminal vesicles under the collar, lateral to the nuchal cartilage, occurs in Abralia, Abraliopsis, and Watasenia but not in Enoploteuthis. Pocket-like oval receptacles under the collar, however, are found only in some Abralia species. Deposition of seminal vesicles under the collar, in the location seen in Watasenia, occurs in several species of Abraliopsis but is not seen in Abralia. The presence of both lateral and median receptacles in the same specimen occurs only in Abraliopsis. The storage of seminal vesicles in a more posterior location, away from the nuchal region, occurs only in Enoploteuthis.

This survey, although limited by the scarcity of mature females and by the limited time of investigation, indicates that the examination of seminal receptacles should be included in the character analysis of enoploteuthids. The shape of the receptacle can vary from oval to round to almost triangular. The receptacle can be dark or only slightly pigmented. The surface may be very or only slightly rugose. The measurement of the receptacle expressed as an index in relation to mantle length may prove significant. The size and number of seminal vesicles exhibit specific differences as does the structure of the spermatophore. Morphological differences of the seminal receptacles and their sites may be useful in the evaluation of closely related species groups. Resolution of the Abralia andamanica species complex, for example, may be aided by a close comparison of the seminal receptacles.

Literature Cited

Adam, W.

1952.   Céphalopodes. Résultats Scientifiques, Expéditions Océanographiques Belge dans les Eaux Côtières Africaines de l'Atlantique Sud 3(3): 1–142.

Berry, S.S.

1926.   A Note on the Occurrence and Habits of a Luminous Squid (Abralia veranyi) at Madeira. Biological Bulletin (Woods Hole), 51:257–268.

Burgess, L.A.

1982.   Four New Species of Squid (Oegopsida, Enoploteuthis) from the Central Pacific and a Description of Adult Enoploteuthis reticulata. Fishery Bulletin, U.S., 8:703–734.

MS. Squids of the Genus Abralia (Cephalopoda) from the Central Equatorial Pacific.

Clarke, M.R.

1988.   Evolution of Recent Cephalopoda—A Brief Review. M.R. Clarke and E.R. Trueman, editors, The Mollusca. 12: Paleontology and Neontology of Cephalopods, pages 331–340. New York: Academic Press.

Gray, J.E.

1849.   Catalogue of the Mollusca in the Collection of the British Museum, 1: Cephalopoda Antipedia. vii + 164 pages. London: British Museum (Natural History).

Ishikawa, C.

1913.   Einige Bemerkungen über den leuchtenden Tintenfisch, Watasea nov. gen. (Abraliopsis der Autoren) scintillons Berry, aus Japan. Zoologischer Anzeiger, 42:162–173.

1914.   Über eine neue Art von Enoploteuthis, Enoploteuthis chunii spec, nov. aus Uwodu, japanische Meer. Journal of the College of Agriculture, Imperial University, Tokyo. 4:401–413, plate 38.

Joubin, M.L.

1896.   Observations sur diverse Céphalopodes, premier note: Abraliopsis Pfefferi (nov. gen. et spec.). Bulletin de la Sociéteé Scientifique et Médicale de l ‘Ouest. 5:19–35, 10 figures.

Orbigny, A. d’

1835–1848.   In A. Férussac and A. d'Orbigny, Histoire naturelle géenérale et particuliére des Céphalopodes Acétabuliferes vivants et fossiles. lvi + 361 pages, atlas of 144 plates. Paris: J.B. Bailliere.

Sasaki, M.

1914.   Observations on Hotaru-ika, Watasenia scintillons. Journal of the College of Agriculture. Tohoku Imperial University, Sapporo. Japan, 6:75–105, plate 2.

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Tsuchiya, K., and T. Okutani

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1962.   The Cephalopod Papers of Japetus Steenstrup. 330 pages. Copenhagen: Danish Science Press.

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1998.   Phylogeny of the “Enoploteuthid” Families. In N.A. Voss. M. Vecchione, R.B. Toll, and M.J. Sweeney, editors, Systematics and Biogeography of Cephalopods. Smithsonian Contributions to Zoology. 586(1):257–270.

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