I'NIVFKSITY Natural Science Research Laboratory OCCASIONAL PAPERS Museum of Texas Tech University Number 269 8 October 2007 GLOBAL TRENDS AND BIASES IN NEW MAMMAL SPECIES DISCOVERIES DEEANNM. REEDER, KRISTOFERM. HELGEN, AND DON E. WILSON ABSTRACT Contrary to common perception, the number of living mammal species and the relationship of those species with one another are incompletely understood. Taxonomic revisions within mammals are frequent and are often motivated by the discovery of new species. In fact, an analysis of patterns of discovery suggests that complete alpha-taxonomic characterization of living mammals remains a far-off goal. Examination of chronological, geographical, and taxo- nomic trends in new species discoveries reveals interesting trends, telling biases, and priorities for further study. An average of 223 new valid species have been described per decade since the birth of modem taxonomic nomenclature in 1758, and this rate is increasing. Over 300 new mammal species are expected to be described this decade and some estimates suggest that 7,000+ living species of mammals will eventually be recognized. An analysis of 341 recently described species indicates that the great majority of them are restricted to threatened areas of high endemism?reiterating the biotic richness of these regions, but also indicating that most new species and the regions in which they occur require urgent conservation attention. That the global mammal fauna remains so incompletely characterized reflects the woeful state of knowledge of global biodiversity. Key words: biodiversity, conservation, mammals, new species discoveries, taxonomy INTRODUCTION The science of taxonomy provides the essential means for documenting the magnitude and distribution of biological diversity (Wilson 1992), and ultimately for prioritizing global and regional conservation initiatives aimed at preserving that diversity (Wilson 1992; Myers et al. 2000; Brooks et al. 2005). Indeed, in discerning the identity and evolutionary relationships of organ- isms, taxonomy ultimately provides the practical under- pinnings for all of biology (Wilson 1992,2004,2005). Despite its fundamental nature, scientific interest and investment in taxonomy appear to be waning (Wheeler 2004; Wilson 2004,2005; Schmidly 2005), even as evi- dence continues to mount that a large proportion of all living organisms remain uncharacterized by biologists (Wilson 2004, 2005). However, startling taxonomic ignorance afflicts not only megadiverse animal groups OCCASIONAL PAPERS, MUSEUM OF TEXAS TECH UNIVERSITY such as insects, nematodes, and marine invertebrates. Even in "flagship" groups like mammals, assumed by many biologists to be well understood taxonomically, a complete understanding of the diversity of living species remains a far-off goal. This is in part because new mammals, even large and relatively conspicuous species, continue to be discovered and described by field biologists and taxonomists at a rapid rate. Our goal was to quantify just how many species are being newly described, and to compare this with historical rates. Furthermore, as has been demonstrated in other taxonomic groups or in subsets of mammals (Patterson 2000, 2001; Collen et al. 2004), we predict that new species discoveries will be biased both in terms of which species are described and from what regions. MATERIALS AND METHODS The analysis of mammal species description rates per decade was performed with a database created fi-om the third edition of Mammal Species of the World (Wil- son and Reeder 2005). This database contains informa- tion on 5,339 extant (or presumably extant) mammals recognized as valid species (as of 1 January 2004, when Mammal Species of the World went to press), as well as the names of 6,351 recognized subspecies and an additional 15,881 species-level synonyms. To these data, we added the records of an additional 82 species that were described between 2004 and 1 July 2006. Figure 1 illustrates two things: 1 ) the number of species described per decade; and 2) the rise in the total number of species recognized over time (along with a linear regression analysis of this rise). It should be noted that the first and the last decade illustrated on this figure are incomplete. The formal scientifically recognized description of mammal species began with Linnaeus's Syslema Naturae in 1758, thus, the first decade column represents a shortened period and the last decade column, representing the 2000s, is still on- going. It also should be noted that Figure 1 represents those species described in each decade that are cur- rently accepted as valid (on average, for each species described, there are three other names that currently are considered synonyms or subspecies (Wilson and Reeder 2005)). As the field progresses, and more new mammals are described, some reorganization should be expected, and some "new" species will undoubtedly be synonymized with older, previously known species (Alroy 2002). Although often not perceived in this way, the description of a new species is a hypothesis that, like all other scientific hypotheses, should be subject to further studies and thus to rejection or confirmation (Baker et al. 2004). It is not our intention to address any taxonomic controversies anew in this paper. We have relied on taxonomic assessments defended in Wilson and Reeder (2005), regardless of subsequent developments, and have not evaluated the validity of subsequently introduced names. For example, the new- ly-described carnivore f^verra tainguensis Sokolov, Rozhnov and Pham Trong 1997 was synonymized with V. zibetha by Walston and Veron (2001 ) and Wozencraft (2005) and is excluded from our table. Balaenoptera omurai Wada, Oishi, and Omada 2003 was included in the synonymy of B. edeni by Mead and Brownell (2005), and thus is not included in our table, despite subsequent arguments (Sasaki et al. 2006). Our table includes some new names since identified as synonyms of earlier names (such as Pteropus baiiakrisi, argued to be a junior synonym of P. alecto (Helgen 2004)), because of their inclusion in Wilson and Reeder (2005). We also include names that postdate Wilson and Reeder (2005) but are probably synonymous with earlier names (such as Cebus queirozi, a junior synonym of C.flavia (de Oliveira and Langguth 2006)). We leave it to future reviewers to cement these and other nomenclatural updates. The analysis of potential biases in newly de- scribed taxa was performed with data from 341 newly described extant mammal species, each of which was formally described between July 1992 and June 2006. The July 1992 starting point was chosen because it represents the cut off of the second edition of Mam- mal Species of the World (Wilson and Reeder 1993), which was nearly universally accepted during the past decade as the standard checklist for mammal species. The 341 new species include those species reviewed by the authors of the most recent, third edition of Mammal Species of the World (Wilson and Reeder 2005) and accepted by these authorities as being valid new spe- cies (259 new extant species described and accepted as valid by other experts in the field between 1992 and REEDER ET AL.-NEW MAMMALS CONTINUE TO BE DISCOVERED 700 600 Tg 500 \? ?a 400 S. lidae approximately 44 Mya ago (Huchon et al. 2007). REEDER ET AL.-NEW MAMMALS CONTINUE TO BE DISCOVERED 27 Table 2.?Breakdown of numbers of previously named species (currently recognized as valid) and newly described species by Order of mammals. Expected numbers of new species were calculated by dividing the number of previously named spe- cies in an Order by the total number of previously named species in all mammals (5,080) and multiplying by the total num- ber of new species described (341). The allocation ofnetv species across all mammals was not what would be expected due to chance (X.- = 41.52, df = //, p < 0.0005): that is, there are biases in what types of mammals are being newly described. Total number of extant species named before New Extant Species New Extant Species Classification 1 July 1992 Observed Expected Class Mammalia 5080 341 Order Monotremata 4 1 0 Order Didelphimorphia 85 7 6 Order Paucituberculata 5 1 0 Order Microbiotheria 1 0 0 Order Notoryctemorphia 2 0 0 Order Dasyuromorphia 65 6 4 Order Peramelemorphia 19 1 1 Order Diprolodontia 131 9 9 Order Afrosoricida 45 7 3 Order Macroscelidea 15 0 1 Order Tubulidentata 1 0 0 Order Ilyracoidea 4 0 0 Order Proboscidea 3 0 0 Order Siren ia 4 0 0 Order Cingulata 20 I 1 Order Pilosa 9 1 1 Order Scandentia 20 0 1 Order Dermoptera 2 0 0 Order Primates 352 36 24 Order Rodentia 2113 155 142 Order Lagomorpha 86 5 6 Order Erinaceomorpha 23 1 2 Order Soricomorpha 398 20 27 Order Chiroptera 1055 78 71 Order Pholidota 8 0 1 Order Carn?vora 281 1 19 Order Perissodactyla 16 0 1 Order Artiodactyla 230 9 15 Order Cet?cea 83 2 6 28 OCCASIONAL PAPERS, MUSEUM OF TEXAS TECH UNIVERSITY RESULTS Trends in New Species Discoveries.?Between mid-1992 (when the second edition o? Mammal Species of the World (Wilson and Reeder 1993) was compiled) and mid-2006, 341 new living mammal species were described?a rate of 24+ new descriptions per year. In total, the number of living mammal species currently recognized is 5,421, an 18% increase in the number of species recognized just over a decade ago (Wilson and Reeder 1993, 2005). This increase represents not only the new species described in the last decade (alone an astounding six percent of the global mam- mal fauna), but also a considerable body of revisionary taxonomic research, which has critically re-elevated the status of many nominal species previously held in taxonomic synonymy (Wilson and Reeder 2005). All signs indicate that these trends toward new discovery, description, and redescription will continue, and that a comprehensive understanding of extant mammalian taxonomic diversity remains a remote goal (Patterson 2000, 2001; Wilson and Reeder 2005; Baker and Bradley 2006). Some recently-described mammals are highly distinctive?28 newly-named species were described in new genera, 18 of which are still considered mono- typic. A most striking example, the Laotian Rock Rat (Laonasles aenigmamus), originally was described not only in a new genus, but in a new family, Laonastidae (Jenkins et al. 2005); in fact, it is now known to be the only known living member of the otherwise extinct Diatomyidae, previously known most recently from Miocene fossils (Dawson et al. 2006). This "living fossil" currently is believed to be related to the Cteno- dactylidae, having diverged from them approximately 44 Mya (Huchon et al. 2007). At the turn of the twentieth century, 147 of the 150 currently-recognized extant mammal families were known to science as living animals, and only two were added to the roster during the 1900s (the monotypic Craseonycteridae, the bumblebee or hog-nosed bat of Myanmar and Thailand, in 1974 and the Near Eastern rodent family Calomysci- dae, in 1979 (containing the single genus Calomyscus Thomas 1905). The 2005 description of Laonasies is thus truly astonishing (from a mammalogist's perspec- tive, it may truly be the discovery of the century). That both of the most recently discovered extant mammalian families are endemic to south-east Asian forests is a strong indication that other major zoological novelties await discovery in that region's increasingly threatened natural habitats. Examining rates of taxonomic description of mammals (from the birth of modem taxonomic nomen- clature in 1758 (Linnaeus 1758) to the present) dem- onsfrates that, on average, 223 currently-recognized species have been described each decade, with peaks in the mid 1800s and early 1900s (Fig. 1 ). These early peaks are likely driven by major expeditions to previ- ously unknown areas (such as the arrival of the "first fleet" and subsequent exploration in Australia, French and German explorations of the Neotropics, and Dutch and British explorations worldwide). Declines from the 1920s to 1950s may be the result of Worid Wars I and II. Since the 1960s, the number of species described per decade has continually increased (likely due to a variety of factors, including the phylogenetic species concept and the genetic species concept, increases in world-wide travel, etc.; see discussion). For the cur- rent decade (the 2000s), if the pace of description from recent years continues unabated, we expect at least 300 new species to be described. Notably, the "species-ac- cumulation" curve for mammals gives no indication of reaching an asymptote, and there is a significant linear relationship between total cumulative number of species and time by decade (r = .974, p < 0.0005; y = 253.79X - 776.03; Fig. ]). Taxonomic and Geographic Biases.?Unsurpris- ingly, new species of mammals described since 1992 are globally but not randomly distributed. Patterns of recent description demonstrate both taxonomic and geographic biases (Fig. 2). Across the 29 orders of mammals, new mammal species are described in numbers greater than expected for some groups and less for others (A^ = 41.52, df=ll,p< 0.0005), all else being equal (Table 2). Greater than expected numbers of new species were described amongst afrotherian insectivores, primates, bats, rodents, monotremes, and marsupials. Less than expected numbers of new species were described amongst eulipotyphlan insec- tivores, carnivores, ungulates (i.e., Perissodactyla and Artiodactyla), and cetaceans. Correcting for species diversity, the largest relative discrepancies (positive or negative) between observed and expected numbers REEDER ET AL.-NEW MAMMALS CONTINUE TO BE DISCOVERED 29 ?a _; s ei '^ M ?as ? ?= o -2 i ^ ?o s ?s le- a B ? a ?o o '3 '5 > u ?i! o >^ -M ?^-* II ? 'S ? .a . o 2 o ?1 ?o (L> ^ a I 60 S'a "S? 11 -- i ?o ?? 13 ?-^ ^1 ?M 8 ^ o [i< -S cN g) 30 OCCASIONAL PAPERS, MUSEUM OF TEXAS TECH UNIVERSITY of new species were found in afrotherian insectivores (7 new species described, 4 expected), primates (36 new species described, 24 expected), carnivores (1 new species described, 19 expected), ungulates (9 new species described, 17 expected), and cetaceans (2 new species described, 6 expected). In part, these discrepancies are explained by issues of body size and conspicuousness: the probability of discovering new whales or antelopes today is intuitively less than the probability of encountering additional small species, such as bats and rodents?though surprises clearly remain a possibility. Within the species-rich Rodentia (2,268 species), descriptions of the 155 new species were strongly biased at the subordinal level (A^ = 36.68, df^ A,p< 0.0005), with large relative discrepancies between observed and expected numbers of new spe- cies in the Sciuromorpha (1 new species described, 23 expected), Castorimorpha (3 new species described, 7 expected), and Hystricomorpha (32 new species described, 18 expected). Geographic biases also are evident: 28% of newly-described species occur only on islands, 71 % are continental, and 1 % are marine (Fig. 2). Though the world's islands comprise only five percent of global land area, they host a rich complement of biodiversity (and especially threatened diversity) vastly dispropor- tionate to their area, as these new discoveries continue to illuminate (Wilson and Reeder 2005; da Fonseca et al. 2006). Of new insular species, almost all (95%) are from the Old World, primarily from the species-rich archipelagos of south-east Asia and Melanesia (the Philippines, Malaysia, Indonesia, Papua New Guinea, Solomon Islands) and from Madagascar (an astound- ing 33 new species). An overwhelming majority (Fig. 2) of all new mammals are known only from regions of high threat and irreplaceability (Mittermeier et al. 2004; Brooks et al. 2005). Geographie and taxonomic biases are often clearly intertwined. Madagascar, with its highly diverse animal assemblages and high degree of endemism (Yoder et al. 2005), provides a striking example of the disproportionate richness of island biodiversity, and continues to yield stunning discoveries (Goodman and Benstead 2004). Description of six new species of shrew-tenrecs {Microgale, endemic to Madagascar), is almost fially responsible for the higher than expected numbers of new afrotherian insectivores; likewise, the description of 15 new lemuriform primates (see Table 1) explains in significant part the higher-than-expected number of primate discoveries. Of the new mammals from continental land- masses, 62% were described from the New World (151 species), primarily from South America (140 species). In South America, most were described from Brazil or from the Andes (corresponding roughly to the Tropical Andes Hotspot (Myers et al. 2000)). Of continental Old World species, 41 were from Africa (40 sub-Saharan), 6 from temperate Asia, 24 fi-om the Asian tropics (including 18 from Vietnam, Laos, and Cambodia), 8 from Australia, and 12 fi-om Europe and the Middle East. DISCUSSION The rapid rate of new species discoveries, which shows no indication of slowing down, suggests that there is a tremendous amount of work remaining to be done in the biotic inventory and alpha-level character- ization of mammals. The data also allow for extrapo- lative predictions regarding discoveries in decades to come. One recent estimate has suggested that as many as 2,000 additional taxonomically valid species remain to be characterized in the global mammal fauna (Baker and Bradley 2006), depending on the species concepts employed. We concur that the "ultimate" number of recognizable mammal species is likely to approximate 7,500. If, as in recent decades, about 220-300 species are newly named per decade, and a similar proportion of critical "splits" accompanies these newly-named taxa, an increase of 2,000 recognized species might be expected by about 2050. The biases apparent in new species discoveries are surely influenced by many factors, including geo- political considerations. For example, discovery of the many new species described from Vietnam and Laos is linked to the opening of these regions to scientific exploration after years of being closed off" to such in- quiry (Groves and Schaller 2000). Conversely, other potentially diverse areas have not been explored for de- REEDER ET AL.-NEW MAMMALS CONTINUE TO BE DISCOVERED 31 cades due to polirical reasons (e.g., Sudan, East Timor, Cuba), and are likely to yield important discoveries in the future. Geopolitical influences are clearly only part of the answer, in part because many new, sometimes 'cryptic', species have been "discovered" in older mu- seum collections, as well as in the field^?^reiterating the importance of museums in the long-term preservation and maintenance of voucher collections. That many new species discovered in the last decade have been described by scientists in developing countries also highlights the increasing and ever-more-important globalization of systematic research. Conservation priorities (and threats) can influ- ence which species are described, and from where. New species discoveries continue to emphasize the conservation importance of particular regions of high endemism (e.g.. Groves and Schaller 2000; Patterson 2001 ; Voss and da Silva 2001 ; Goodman and Benstead 2004; Mittermeier et al. 2004; Cotterill 2005; Helgen 2005; Yoder et al. 2005; Beehler 2006; da Fonseca et al. 2006). Many new species described from the tropics (and many in the process of being described (Wilson and Reeder 2005; Beehler 2006)) were discovered in 'rapid assessments' involving intensive sampling in relatively little-studied regions. Although difficult for many to believe, biotas of some relatively expansive areas of the globe, especially in the tropics, remain entirely or largely unexplored and unsurveyed. For example, a recent expedition to the Foja Mountains in western New Guinea (2 million acres of undisturbed tropical forest) represents the first major biotic explora- tion of this area (Beehler 2006). Paradoxically, some activities that potentially threaten species survival are facilitating the discovery of new species; for example, new logging roads and hydroelectric projects have pro- vided easier scientific access into previously unstudied regions of Amazonia (e.g., Voss and da Silva 2001). Previous research on primates and carnivores indicates that mammal species described in recent years tend to be relatively small-bodied, and have small geographic ranges (CoUen et al. 2004). Although the great majority of recently-described mammals are in- deed small (as are the great majority of all mammals), a surprising number of newly-characterized mammals are relatively large (including primates, ungulates, and even cetaceans; see Table 1). And while most newly- discovered species do indeed have quite small geo- graphic ranges (at least as so far recorded), others are now known to be distributed across insular archipelagos or throughout relatively expansive montane regions (e.g., Nyctimene keasti Kitchener 1993; Aepeomys reigi Ochoa G., Aguilera, Pacheco, and Soriano 2001 ; Wilson and Reeder 2005). Clearly, the age of basic fieldwork is far from over. Taxonomy provides one of the most important tools in rallying efforts against extinctions in the mod- em era. By delineating salient units of biodiversity, basic taxonomic research is critical to sound biogeo- graphic assessment, and a critical tool in establishing geographic priorities for protection and study (Mace 2004; Wilson 2004). Fully one-quarter of all currently- recognized mammals are considered threatened with extinction in the near future (Cardillo et al. 2006). Most recently-described species of mammals are found in developing regions highly impacted by ongoing human population increases, habitat conversion, and other en- vironmental pressures (Fig. 2), as, we predict, are the great majority of currently undescribed mammals. The importance of sustained work in mammalian taxonomy and field biology is clear: there remains much to leam, even within this group of seemingly familiar animals, and conservation threats impart an urgent impetus toward fiirther research. Although many 'end users' of taxonomic information are eternally fi^strated with taxonomic flux (e.g., Isaac et al. 2004), continual updates to our understanding of biodiversity, including that of charismatic and well-studied groups such as mammals, signal the need for patience within the biological community as taxonomists continue to come to terms with the overwhelming richness of the global biota as a whole. With our increasing understanding of evolution- ary processes and the variety of scientific opinions about what really constitutes a distinct species, whether one uses the biological species concept, morphological species concept, phylogenetic species concept, or now the genetic species concept, has profound implications for what species we can expect to see described in the coming years and decades (for review of species cocepts see Cracraft (1997) and Baker and Bradley (2006)). While some consider the elevation of species 32 OCCASIONAL PAPERS, MUSEUM OF TEXAS TECH UNIVERSITY numbers due to changes in the species concept "taxo- nomic inflation" that may or may not result in accurate species lists (Alroy 2002; Isaac et al. 2004), others (e.g., Bakerand Bradley 2006) contend that these increases in species number are valid (especially when derived from statistically supported phylogenetic analyses, which are often corroborated by morphological and geographical data). In fact, a number of the species highlighted in Table 1 would be recognized as valid species regardless of the species concept employed. The headquarters of taxonomic efforts are natural history museums, which need unrelenting support in their fundamental goals to maintain present collections, accumulate new ones, and support alpha-taxonomic and revisionary studies now and into the ftiture (Baker 1994; Wheeler 2004; Wheeler et al. 2004; Wilson 2004, 2005; Schmidly 2005). Our ability to move forward in understanding biological diversity, so critical to the future of ecosystems, is contingent upon sustained funding for museum collections and field collecting, and support and encouragement for new generations of systematists?be they botanists, entomologists, or mammalogists. ACKNOWI.EDGMENTS We thank Dan Cole, Thomas M. Brooks, Lauren E. Helgen, Linda K. Gordon, Scott M. Wasilko, and Cassandra J. Ostroski for assistance in preparing figures and data compilation, and Gary N. Bronner, Robert L. Brownell Jr., Michael D. Carleton, Fritz Dieterlen, Al- fred L. Gardner, Colin P. Groves, Peter Grubb, Robert S. Hoffmann, Mary Ellen Holden, Rainer Hutterer, Paula D. Jenkins, C. William Kilpatrick, James G. Mead, Guy G. Musser, James L. Patton, Duane A. Sch?tter, Jeheskel Shoshani, Nancy B. Simmons, Andrew T. Smith, Brian J. Stafford, Richard W. Thorington Jr., Charles A. Woods, and W. Christopher Wozencraft for taxonomic input. Generation of the database underly- ing this analysis was supported by a grant from the Electronic Catalogue of Names of Known Organisms program of the Global Biodiversity Information Facility (GBIF) to DEW. REEDER ET AL.-NEW MAMMALS CONTINUE TO BE DISCOVERED 33 LITERATURE CITED Alroy, J. 2002. How many named species are valid? Pro- ceedings of the National Academy of Sciences 99:3706-3711. Baker, R. J. 1994. Some thoughts on conservation, biodi- versity, museums, molecular characters, system- atics, and basic research. Journal of Mammalogy 75:277-287. Baker, R. J., and R. D. Bradley. 2006. Speciation in mam- mals and the genetic species concept. Journal of Mammalogy 87:643-662. Baker, R. J., R. M. Fonseca, D. A. Parish, C. J. Phillips, and F. G. Hoffmann. 2004. New bat of the genus Lophostoma (Phyllostomidae: Phyllostominae) from northwestern Ecuador. Occasional Papers, Museum of Texas Tech University 232:1+1-16. Beehler, B. M. 2006. Foja Mountains, discovering a lost world. 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Ranivo, V. Soari- malala, K. P. Karanth, A. P. Raselimanana, and S. M. Goodman. 2005. A multidimensional approach for detecting species patterns in Malagasy verte- brates. Proceedings of the National Academy of Sciences 102 (suppl. l):6587-6594. REEDER ET AL.-NEW MAMMALS CONTINUE TO BE DISCOVERED 35 Addresses of authors: DEEANN M. REEDER Department of Biology Bucknell Universit)' Lewisburg. PA 17837 USA dreeder@buchiell. edu KRISTOFER M. HELGEN Division of Mammals National Museum of Natural History NHB 390. MRC 108 Smithsonian Institution P.O. Box 37012 Washington. D.C. 20013-7012 USA helgenk@si.edu DON E. WILSON Division of Mammals National Museum of Natural History NHB 390, MRC 108 Smithsonian Institution P.O. Box 37012 Washington. D.C. 20013-7012 USA wilsond@si. edu PUBLICATIONS OF THE MUSEUM OF TEXAS TECH UNIVERSITY Institutional subscriptions are available through the Museum of Texas Tech University, attn: NSRL Publications Secretary, Box 43191, Lubbock, TX 79409-3191. 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