MORPHOLOGICAL DIVERSITY AND EVOLUTION OF EGG AND
CLUTCH STRUCTURE IN AMPHIBIANS
RONALD ALTIG1,3 AND ROY W. MCDIARMID2
1Department of Biological Sciences, Mississippi State University, Mississippi State, MS 39762-5759, USA
2USGS Patuxent Wildlife Research Center, National Museum of Natural History, Washington, DC 20560-0111, USA
ABSTRACT: The first part of this synthesis summarizes the morphology of the jelly layers surrounding an
amphibian ovum. We propose a standard terminology and discuss the evolution of jelly layers. The second
part reviews the morphological diversity and arrangement of deposited eggs?the ovipositional mode; we
recognize 5 morphological classes including 14 modes. We discuss some of the oviductal, ovipositional, and
postovipositional events that contribute to these morphologies. We have incorporated data from taxa from
throughout the world but recognize that other types will be discovered that may modify understanding of
these modes. Finally, we discuss the evolutionary context of the diversity of clutch structure and present a first
estimate of its evolution.
Key words: Amphibia; Clutch; Eggs; Evolution; Jelly layers; Oviposition; Ovulation.
AMPHIBIANS surely have the most varied and
least known life histories of all terrestrial
vertebrates. Typically, terrestrial adults return
to aquatic sites where courtship, egg de-
position, and fertilization occur. Eggs hatch
into larvae that are mobile feeding forms.
After a period of growth and development,
these larvae or tadpoles usually undergo some
form of metamorphosis and move onto land
where they grow into reproductive adults.
Variations on this pattern most often repre-
sent evolutionary changes in developmental or
life history traits (e.g., paedomorphy and
pedotypy, egg placement, tadpole develop-
ment) expressed during the ontogeny of an
individual prior to its becoming an adult.
McDiarmid and Altig (1999) summarized the
biology of tadpoles, and we know even more
about the adult stage (e.g., Duellman and
Trueb, 1986). Although the research efforts of
embryologists and cell biologists have pro-
vided extensive information on ovum pro-
duction and early development, even if in-
volving a relative few taxa, nearly every facet
of the field biology of amphibian eggs is poorly
documented. In this paper we focus on egg
structure, particularly the jelly layers, and
patterns of egg deposition. We also consider
the characteristics of the physical and bi-
ological environments in which the immobile
eggs are laid that likely account for the
diversity of egg jellies and ovipositional
modes.
Field identification of amphibian eggs is
difficult at best, in part because authors of
published descriptions of eggs have used
inconsistent and inexact terminology and
misinterpreted certain structures. For exam-
ple, the vitelline membrane sensu lato actually
takes on three successive states with different
biochemical and physical properties and
functions: coelomic, vitelline, and fertilization
membranes (Carotenuto, 2001; Gerton and
Hedrick, 1986; Takamune et al., 1987), but
most authors fail to distinguish among them.
In addition, different observational techniques
can lead to different results, so that research-
ers often disagree on traits as seemingly easy
to observe as the number of jelly layers
around an ovum.
While writing a key to the eggs of North
American amphibians, we realized that egg
identifications based on properly described
ovipositional modes were likely to be more
accurate than those based on the more labile
and poorly documented features of individual
eggs. Clutch morphology is easier to see, more
readily definable, and usually less variable
within species. By combining these definitions
with careful field observations (e.g., Pombal
and Haddad, 2005) made under well-docu-
mented environmental conditions (e.g., Wright
and Wright, 1924), a good observer should be
able to identify the eggs of North American
amphibian taxa at least to genus with reason-3 CORRESPONDENCE: e-mail, raltig@biology.msstate.edu
Herpetological Monographs, 21, 2007, 1?32
E 2007 by The Herpetologists? League, Inc.
1
able confidence. We suspect that the same
could be done with other faunas as well.
Our initial goal in this review is to develop
a generalized framework for observed di-
versity of amphibian eggs and ovipositional
modes that will contribute to a broad un-
derstanding of the evolution of amphibian
reproduction. We believe that the oviposition-
al mode is a factor that can profitably augment
our notions of breeding or reproductive
modes (e.g., Crump, 1974; Duellman and
Trueb, 1986; Haddad and Prado, 2005). In the
process, we present a standardized terminol-
ogy for egg jellies and clutch structures and
discuss the evolution of these features. Al-
though data acquired by cell biologists, de-
velopmental geneticists, and particularly his-
tochemists will enhance the eventual
understanding of the biology of ova and egg
jellies, we do not delve into this extensive
literature.
Also, one should be constantly aware of the
integration of the data discussed herein with
the concept of breeding mode that is being
constantly revised and expanded (e.g., Crump,
1974; Duellman and Trueb, 1986). What we
present is a subset of the larger concept,
although this integration is left for a future
synthesis when egg biology is better under-
stood.
The morphological surveys of egg structure
by Salthe (1963) and Salthe and Duellman
(1973) suggested that intriguing morphologi-
cal and ecological patterns exist within am-
phibians. Variations in the surface morpholo-
gies of ovum coverings and the nature of the
arrangement and attachment of eggs in the
environment as reported in other organisms
(e.g., Mooi, 1990; Stiassny and Mezey, 1993;
Strathmann and Chaffee, 1984) surely exist in
amphibians, but certain factors obfuscate their
interpretation in this group. For example, the
number of jelly layers surrounding an ovum
and the number of secretory areas in an
oviduct may vary independently (Greven,
2003). In part, these variations can be
explained by oviductal (e.g., changes in
secretory regions in the oviduct; preoviposi-
tional changes in jelly; D. M. Hardy and
Hedrick, 1992), postovulatory (e.g., dissolu-
tion of some jelly layers) and postovipositional
(e.g., layers melding together; formation of the
capsular chamber in salamanders and some
frogs) events. Of greater import in essentially
all cases is the lack of data or the lack of
integration of those data across disparate
fields of research. Diagrams of eggs are
schematic and usually drawn in lateral view
taken at the equator with the animal pole
uppermost. Concentric circles drawn around
the ovum (e.g., continuous, dashed, or stip-
pled lines or zones; Hoyt, 1960; McDiarmid
and Worthington, 1970) represent visually
perceived jelly layers. Even so, no adequate
description of the arrangement of jelly layers
around freshly oviposited eggs based on
observations using standardized techniques
(i.e., proper illumination, dissection, section-
ing, staining) has been published.
We summarize the literature on amphibian
egg morphology, especially that addressing
the production and evolution of the jelly layers
surrounding the amphibian ovum. We follow
with a synthetic treatment of the morphology,
diversity, and evolution of the egg clutch. We
also propose a standardized terminology for
describing eggs and egg clutches that we
believe facilitates communication and ad-
vances the study of this important but
neglected stage of the amphibian life cycle.
EGG MORPHOLOGY AND ITS VARIATIONS
Definitions
We define ?egg? as an ovum (5 gamete
through gastrulation, stages 1?12; Gosner,
1960; other versions in Duellman and Trueb,
1986 and McDiarmid and Altig, 1999, Chap-
ter 2) and its vitelline membrane of ovarian
origin surrounded by one to several oviduc-
tally-produced jelly layer(s). The internal layer
is deposited first by an anterior region of the
oviduct, and as the egg moves down the
oviduct more layers are deposited sequentially
by more posterior oviductal regions.
Various terms have been used to refer to
the individual jelly layers, and they and the
entire complement of layers as a unit generally
lack discrete definitions; some of the terms
used in different research fields are inaccurate
(e.g., capsule, envelope). We suggest that the
entire assemblage of oviductal materials de-
posited around the ovum be referred to as
?jelly? or ?jelly layers? regardless of variations in
2 HERPETOLOGICAL MONOGRAPHS [No. 21
their apparent physical structure (e.g., tough-
ness, density, thickness, water content). Layer,
zone, and membrane refer to units within this
assemblage. A ?layer? (often referred to in the
cell biology literature by the letter ?J? with
a numerical subscript to denote position) is
a morphologically discrete, easily recognizable
region of jelly surrounding the ovum; it has
a discernible thickness along a radius and
typically has a uniform and visually apparent
optical density. Layers are numbered from
interior to exterior (e.g., Daniel, 1937) in the
order in which they are formed. The term
?layer? does not encompass any specific
function or physical characteristic.
Daniel (1937) and others pointed out that
some layers have discernible but less discrete
subdivisions. We designate these subdivisions
as ?zones? to suggest areas that are less easily
visualized than layers (see Steinke and Ben-
son, 1970), but we do not imply that all zones
of nonstained eggs are visible.
Finally, we use ?membrane? as a functional
term to describe what appears to be a delimit-
ing boundary between layers, exclusive of the
vitelline membrane. Data are currently in-
sufficient to determine if membranes are
actual structures or if they are merely an
optical representation of the plane along
which two layers of different densities abut.
In some instances two layers apparently abut
without a visible membrane, thereby suggest-
ing that the densities of the two layers must
reach some threshold before a visual mani-
festation of the transition appears. If the
?membranes? between layers are discrete
structures, we do not know if they are
independent of adjacent layers and produced
by a specific oviductal secretory region, the
result of some postovipositional reaction of
the jelly layers, or an outer or inner boundary
of a particular layer.
Structure
Clear jelly layers certainly are not as
structurally uniform (e.g., Carroll et al.,
1991) throughout their thickness as they
appear. The egg of Rana pipiens, for example,
has two, clear layers of jelly (Wright and
Wright, 1949:35). Studies (Steinke and Ben-
son, 1970) of the taxon of the same name with
immunological and histochemical techniques
revealed 5?6 layers, whereas dissections
(Salthe, 1963) and other techniques (Shaver,
1966; Shivers and James, 1970) indicated 3?5
layers. Descriptions of the eggs of Dicampto-
don sp., probably based on visual examina-
tion of intact eggs (Stebbins, 2003), indicated
2 jelly layers, whereas visual and tactile
detection of density differences noted dur-
ing dissection (Nussbaum, 1969) showed 5
layers.
More structure certainly exists in the jelly
layers than can be seen with simple micro-
scopy. Other observational techniques (e.g.,
differential interference contrast [DIC],
phase-contrast and fluorescence microscopy
and laser illumination) do not produce better
images. Laser confocal imaging and some
techniques of electron microscopy provide
better results but are costly and specimen
preparation is laborious (e.g., Bonnell and
Chandler, 1998; Larabell and Chandler,
2005). More refined zones, which can be
detected with histological and histochemical
techniques, likely will reveal patterns of
biological, ecological, or phylogenetic interest
(e.g., Hedrick and Katagiri, 1988; Smith et al.,
2002). Biochemical analyses show that egg
jellies consist of ??a fibrous glycoprotein
superstructure that acts as a scaffold to which
globular glycoproteins are bound?? (Fig. 5E;
Bonnell and Chandler, 1998); which of these
groups of molecules is structural and which is
biologically active is not known, but both are
expected to have species-specific qualities
(Maes et al., 1995). The three jelly layers of
the eggs of Xenopus laevis are composed of at
least nine glycoproteins (Yurewicz et al.,
1975).
These kinds of data, while interesting, are of
little use to field biologists who usually rely on
visual impressions of structure viewed under
incident, white light. Some data suggest that it
may not be possible to formulate a descriptive
model useful to all researchers. Accordingly,
field biologists, histochemists, and biologists
in other fields may find it expedient to use
their own sets of terms to describe observed
variations in jelly traits.
In summary, jelly occurs in layers and
a layer may be subdivided into less easily
discernible zones. Visually perceived layers
typically would be the morphological trait
2007] HERPETOLOGICAL MONOGRAPHS 3
most useful for identification. For example,
the basic egg structure consists of an ovum
with a vitelline membrane surrounded by jelly
layers 1 and 2 (Fig. 1A, E) of oviductally-
produced materials. Inner and outer mem-
branes are labeled, although oviductal secre-
tory zones for their production are not, and no
zones are shown.
EVOLUTION OF EGG JELLY
The evolution of additional layers of jelly
does not appear to result only from the
subdivision of ancestral layers. Thus, egg
diameter often is greater in species with more
layers rather than in those with fewer layers,
even though the thickness of each layer, or at
least of some, often decreases as the number of
layers increases. Although the thickness of jelly
layers must be mediated by the general trade-
offs between the requirements for gas ex-
change and need for mechanical support, other
factors (e.g., homospecific sperm attraction
[Al-Anzi and Chandler, 1998], heterospecific
sperm avoidance, heat conservation, and pred-
ator defense) likely have played roles in the
evolution of the number, thickness, and
physical characteristics of the layers. To
appreciate layer homologies one must ulti-
mately understand the morphology of the
secretory regions of the oviduct and presum-
ably have some notion of evolutionary relation-
ships among taxa. Presumably, selection for
differences in the number and characteristics
of the jelly layer has influenced oviductal
morphology rather than the reverse, although
other factors that seemingly are not related to
egg survival (e.g., Anderson et al., 2006) must
be considered. Evidence suggests that envi-
ronmental demands and phylogenetic con-
straints have influenced the evolution of egg
morphology, although little is known about the
FIG. 1.?Schematic drawings of an amphibian egg with its component parts, the oviductal regions a?c that produce
the jelly layers, and three hypothetical paths for adding a jelly layer. (A) An ovum with two membranes (see text) and two
jelly layers produced in sequence by oviductal sections a and b arranged anteriorly to posteriorly. (B) A hypothetical case
where a new layer is added directly external to the vitelline membrane; new numbering of the jelly layers and the
arrangement of the oviductal regions are shown. (C) A case where a new layer is added externally. (D) A case where
a new layer is added within the original first layer. Abbreviations: 1?4 5 jelly layers numbered from ovum to surface, ant
5 anterior, IM 5 inner membrane, O 5 ovum, OM 5 outer membrane, post 5 posterior, VM 5 vitelline membrane,
and VS 5 vitelline space.
4 HERPETOLOGICAL MONOGRAPHS [No. 21
selective factors involved, and details and
patterns of the morphology in most taxa are
still lacking (Salthe, 1963; Greven, 2003).
Hypothetical scenarios diagramed (Fig. 1B?
D, F?H; also Greven, 2002:fig. 11) illustrate
potential modifications in oviductal secretory
regions that would produce given changes in
jelly layers; the review by Wake and Dickie
(1998) provides informative discussions of
oviductal anatomy relative to breeding mode.
If we assume for heuristic purposes that
combinations of the following alternatives did
not occur, then a third jelly layer might be
added (1) between the vitelline membrane and
the first jelly layer; Fig. 1B, F), (2) between the
two original jelly layers), (3) external to the
second layer of the original egg; Fig. 1C, G), or
within an existing layer; Fig. 1D, H). If
a posterior (i.e., new layer added externally)
or anterior (i.e., new layer internally) region of
the oviduct were involved and a phylogenetic
scheme were known, one potentially could
track the products and thus hypothesize
homologies. Identification of other types of
additions may require histochemical tech-
niques, and examination of changes in oviduc-
tal regions. Which evolutionary pathway is
most likely can be debated and will depend
largely on the ease with which homologies can
be assigned. Layer thickness also is likely
influenced either by the length of the oviductal
region, passage rate of the ovum, rate of jelly
production, or differences in hygroscopic
qualities of the jelly. Although these parame-
ters are probably important, we have ignored
them because of the lack of data.
Salthe (1963) presented the only sugges-
tions of homologies of jelly layers in caudates.
His interpretations, based on 15 caudate
genera in 8 families suggest that (1) 8 jelly
layers (as in Hynobius lichenatus) is the
primitive condition; (2) changes in the num-
ber of layers occur only through (a) loss of the
most external layers (e.g., ambystomatids) or
(b) loss of more internal layers (i.e., elimina-
tion of layers somewhere within the series;
particularly plethodontids); and (3) eggs with
3 layers of undetermined homologies (as in of
Cryptobranchus) is the simplest condition. All
of these ideas are based on the assumption
that layers in discernible positions and of
similar construction are homologs.
We know of no proposed scheme of jelly
layer homologies for anurans, and phyloge-
netic patterns and possible selective factors
contributing to their evolution are often
discordant. For example, among North
American frogs (Moore, 1940), many cool-
water breeders deposit clumps of eggs with
either 2 or 4 jelly layers, whereas warm-water
breeders lay either clumps or films of eggs
with 2 layers. ?Wood frogs? (West Coast
endemics plus Rana sylvatica) produce
clumps of eggs with 2?3 jelly layers in cool
water. Members of the Rana catesbeiana
group breed in warm weather and deposit
eggs with 1?2 layers as clumps or surface
films. Members of the Rana pipiens complex
lay eggs with 2 jelly layers in clumps and
usually in cool water. Considering the four
options for layer homologies (Fig. 1B?D), one
can ask if the outer two or the inner two layers
of the wood frogs are homologous to the
two layers of the other groups of North
American ranids and which of the layers
might reflect responses to temperature or
ovipositional mode and which to phylogenetic
constraint.
A complete histochemical data set for an
amphibian egg might agree with Salthe?s
(1963) morphological data. One still would
not be sure of layer homologies, but his
hypotheses based on position and construc-
tion would have stronger support. Mapping
histochemical data onto appropriate clado-
grams would likely provide some insight about
the evolution of jelly layers, and information
on the ecological functions of egg jellies
should reveal correlations useful to interpret-
ing their evolution. Salthe (1963) suggested
that layer losses in plethodontids that lay
terrestrial eggs involve changes of internal
layers and that the tough outer layer is
retained for protection. Evaluations of the
hypotheses about jelly layer homologies will
have to wait additional data.
ANCILLARY SUBJECTS ON EGGS
Characteristics of Jelly Layers
Anyone who has handled eggs and espe-
cially those who have manually dejellied them
are familiar with features such as elasticity,
stickiness, toughness, turgidity, and wateri-
2007] HERPETOLOGICAL MONOGRAPHS 5
ness. Aquatic eggs usually are spherical when
submerged but sag when placed on a surface
in air. The jellies of most terrestrial forms that
do not lay suspended eggs have jelly with
sufficient tensile strength and turgidity to
remain spherical in air. The outer jelly of eggs
of Ambystoma opacum and other terrestrial
salamanders and frogs with direct develop-
ment is tough relative to that of aquatic eggs.
Tougher membranes and increased turgidity
of the enclosed fluids help to maintain the
spherical shape of these large eggs in air and
thereby allow proper development, oxygena-
tion, and protection from trampling by an
attendant parent. These terrestrial eggs can be
grasped with minimal distortion and will
bounce if dropped. If the outer layer is
removed, the remaining jellies spread out,
and the ovum usually ruptures. In some
aquatic eggs the most external visible layer is
surrounded by a transparent, watery gel that
appears to lack a defining exterior surface but
is crucial for flotation (see below).
Asymmetries of jellies caused by tensile
differences, such as the drooping of egg jellies
of terrestrial plethodontid eggs or the pentag-
onal appearance of jellies of eggs tightly
spaced in a film, are common. The observa-
tion by Wright and Wright (1949) that the
inner jelly layer of the eggs of Rana clamitans,
which is not under any tensile forces, may be
elliptical or pear-shaped needs verification.
We assume that the conical ova that Wright
and Wright (1949) observed in Bufo alvarius
resulted from tension on the jelly string.
There are cases of egg jelly asymmetries in
the absence of tension. The outer jellies of
some salamandrid eggs (Notophthalmus vir-
idescens; Bishop, 1943) are oval and attached
individually or in small groups to plants. Parts
of the outer jelly layers of the eggs of some Old
World microhylids (e.g., Kaloula rugifera and
K. macroptica, Fig. 2A, B, and Liu, 1950;
Kaloula borealis in Li, 1934; Kalophrynus
pleurostigma in Taylor, 1922; and Paradoxo-
phyla palmata in Glaw and Vences, 1992; RA,
personal observation) are asymmetrical and
form a flange or rim which allows the eggs to
float. Asymmetry in jelly layers seems at odds
with their mode of formation in the oviduct,
but the asymmetry results from differences in
hygroscopic properties of specific portions of
the jelly immediately after oviposition rather
than structural differences per se. The jelly that
forms the flange surely surrounds the entire
ovum, in contrast to being deposited as a band,
and is likely very watery. The pressure of the
water surrounding the egg as it sinks partway
through the water surface likely pushes this
flimsy jelly to the air-water interface and forms
the flange. Different flange positions (e.g.,
equatorial in Kaloula spp. and near the vegetal
pole in Paradoxophyla palmata) may reflect
interspecific differences in the density of the
egg-jelly complex or in the hygroscopic qual-
ities of the jelly. Li (1934) noted that the rim in
Kaloula borealis did not appear until about
1 min after oviposition, and Taylor (1922)
described the gelatinous flange in Kalophrynus
pleurostigma as gradually widening to about
6 mm diameter after extrusion.
Inclusions in Jelly
The structure, origin, and function of
various crystalline inclusions in the jelly of
salamanders (e.g., Ambystoma maculatum,
Salthe, 1963; Ruth et al., 1993; Siren lacertina
and Hynobius lichenatus, Salthe, 1963) need
further examination. For example, the egg
jelly of Ambystoma maculatum can be clear or
opaque white (L. M. Hardy and Lucas, 1991).
White jelly gets its color from glycoprotein
crystals that are produced with the jelly in
cells in the oviductal wall. Populations with
clear-jellied, white-jellied, or both types of egg
masses have been reported from northwestern
Louisiana and adjacent areas of Texas and
Arkansas. The function of the crystals is
unknown, but they may reflect light and
thereby offer some protection to the de-
veloping embryos or concealment from pred-
ators (L. M. Hardy, personal communication).
Similarly, the jelly of the eggs of the frog
Mantidactylus depressiceps (Mantellidae) is
milky white (RA, personal observation) al-
though the cause of the color is unknown.
What appear as striae, furrows, or corrugations
in the outer layer of jelly of some salamanders
(e.g., Hynobius lichenatus, Salthe, 1963) and
frog egg masses (e.g., Cochranella pulverata
[RWM, personal observation]) also deserve
attention.
Some ambystomatid eggs, notably those of
Ambystoma maculatum and A. gracile with
6 HERPETOLOGICAL MONOGRAPHS [No. 21
FIG. 2.?(A?C) Microhylid, (D?H) mantellid, and (I) arthroleptid frog eggs. Asymmetrical egg jellies of (A) Kaloula
rugifera (modified from Liu, 1950:fig. 58) and (B) K. macroptica (modified from Liu, 1950:fig. 60) caused by differential
hydration of specific parts of the jelly. (C) Part of a coherent film of Gastrophryne carolinensis eggs soon after
oviposition showing the upper hemisphere of jelly projecting above the water surface (1 5 downward flexed meniscus at
jelly margin, 2 5 glint on surface of ovum or vitelline membrane, and 3 5 trapezoidal reflection on curved, upper
hemisphere of outer egg jelly). Laminar array of a clutch of Guibemantis depressiceps eggs on a leaf (D) prior to
hydration (OV 5 ova; EJ 5 empty jellies), (E) the same clutch showing a large increase in volume after hydration, and
(F) the same clutch cut longitudinally after hydration, stained with Toluidine Blue, and viewed with transmitted light (L
5 cut leaf; OS 5 ovumless stalk, OV 5 ova, and S 5 limits of one stalk with an ovum; stalks slightly darkened
electronically for better visibility). (G) Recently laid clutch of ?Mantidactylus? sp. on a leaf showing structure when
hydration is normally less extensive, and (H) older clutch of ?Mantidactylus? sp. attached to the bark of a tree with clear
jelly and a large increase in jelly with hydration (embryos that appear deep in the jelly are actually on the sides of the
jelly). (I) Terrestrial clump of Arthroleptis schubotzi found in leaf litter (photo by R. C. Drewes).
2007] HERPETOLOGICAL MONOGRAPHS 7
exceptionally dense jellies, have a symbiotic
green alga (Oophila amblystomatis) within the
inner jelly layers of the egg (e.g., Bachmann et
al., 1986; Hammen, 1962).
Capsular Chamber
In salamanders and a few primitive frogs
(Salthe, 1963:165), the jelly layer abutting the
vitelline membrane dissolves soon after ovi-
position to form the capsular chamber;
remnant debris, termed ?white plac?, puddles
at the bottom of the capsular chamber
(Daniel, 1937). Eggs with a capsular chamber
are less confined than those without such
a chamber so that the ova lie slightly below
center in the remaining jelly; if the egg mass is
inverted, the ova immediately turn so that the
animal pole is uppermost. In eggs without
a capsular chamber the ova are constrained by
the jelly layers and take several minutes to
right themselves (Salthe, 1963). Embryos
usually exit the vitelline membrane long
before they hatch from the jelly (Salthe,
1963), and one can often see the vitelline
membrane crumpled up at the bottom of the
inner jelly layer in advanced embryos.
Functions of Egg Jelly
Suggested functions of egg jellies (Greven,
2002, 2003) include mechanical support for
the ovum, attachment of eggs to each other or
a structure in the environment, enhancement
or prevention of entry by conspecific and
heterospecific sperm respectively (e.g., Bar-
bieri and Del Pino, 1970), prevention of
polyspermy, sperm capacitation, differential
protection from water molds Saprolegnia and
Achlys (Gomez-Mestre et al., 2006), pro-
tection from contaminants (Marquis et al.,
2006), and protection from predators, patho-
gens, and environmental stressors such as
temperature and UV light (Hunter and Vogel,
1986; Itoh et al., 2002; McLaughlin and
Humphries, 1978; Ward and Sexton, 1981).
Incubation in birds helps to inhibit growth of
bacteria and fungi on egg shells (Cook et al.,
2005); jelly layers may be a prepackaged way
to protect ova from these perils after they exit
from the relatively sterile oviduct. The in-
fluence of jelly on light refraction is thought to
be insignificant (Cornman and Grier, 1941)
but possibly needs further study (Bragg,
1964).
Hatching
Hatching occurs when a developmental
threshold is reached in concert with various
biotic and environmental cues. Hypoxia (e.g.,
Petranka et al., 1982) likely is the proximal
trigger, but factors such as pathogens and
predators (e.g., Chivers et al., 2001; Touchon
et al., 2006; Warkentin, 1995) or low pH
(Dunson and Connell, 1982) can modify
timing. Thumm and Mahony (2002) demon-
strated that the stage and degree of de-
velopment at hatching in Pseudophryne aus-
tralis (Myobatrachidae) is variable. Hatching
mechanisms seemingly are universal (Noble,
1926; Duellman and Trueb, 1986) and fall into
two groups. In most amphibians enzymes
from the frontal (5 hatching) glands on the
head and snout cause at least partial chemical
degradation of the jelly (e.g., Carroll and
Hedrick, 1974; Urch and Hedrick, 1981),
which may often be augmented by simple
writhing and pushing by the embryo to break
through the layers (also Bragg, 1940; Gollman
and Gollman, 1993; Lutz, 1944) or by rain
(Noble, 1926). In some direct developing
frogs an egg tooth on the snout or other part
of the body mechanically ruptures the mem-
branes and jelly layers to allow hatching (e.g.,
J. D. Hardy, 1984; Noble, 1926).
Ovum Pigmentation
Even though the pigments in most ova are
melanic and not contained in cellular orga-
nelles, data on this pigmentation of maternal
origin are confusing. In large part this is
because there are no standards for describing
color, intensity (e.g., dark, diffuse, pale),
pattern, location, or the gradation from dorsal
darkness to ventral paleness. In addition,
apparent changes in pigmentation with de-
velopment or after preservation have rarely
been documented. Potential influences on
ovum coloration include age of female, stage
of oogenesis, changes during development
(i.e., when and how maternally-provided
pigment is supplanted during oogenesis by
that from the developing embryo), and egg-
laying site (i.e., geographical and elevational
variation). Likewise, color and pattern and
8 HERPETOLOGICAL MONOGRAPHS [No. 21
their development in hatchlings (e.g., Altig,
1972) that are useful for species identifications
(e.g., hylid hatchlings commonly are strikingly
patterned, ranids usually unicolored) are
poorly documented.
Nevertheless, some general correlates of
ovum pigmentation are apparent (Salthe,
1963). Eggs laid in open, exposed areas,
regardless of the specific site, taxon, or
ovipositional mode, usually have melanic
pigment at the animal pole (e.g., Ambystoma,
Bufo, Hyla, and Rana of North America). As
the number of embryonic cells increases and
the cells move during gastrulation, the fertil-
ized ova become more uniformly pigmented
and paler because the ovum pigment is
dispersed among more cells until embryonic
pigment appears. Eggs laid in secluded sites
(e.g., Amphiuma in burrows near lentic sites,
Cryptobranchus, Dicamptodon, numerous
plethodontids, and Ascaphus hidden among
rocks in streams, some dendrobatid and
microhylid frogs among forest debris and
phytotelmata, some centrolenids on leaves)
tend to be pale to nonpigmented regardless of
ovipositional mode. Biologists working in
temperate areas often assume that amphibian
eggs are pigmented because those the taxa
most commonly encountered are pigmented,
but in fact, many taxa in tropical regions have
nonpigmented ova.
Several functions of egg pigmentation and
adult behaviors associated with that trait have
been proposed. Communal oviposition of
masses of dark eggs apparently enhances
absorption of heat thereby increasing de-
velopmental rate in early breeding species of
some North American ranids (Hassinger,
1970). Pigmentation in eggs can also provide
protection from deleterious effects of specific
wavelengths of light or heat (Barrio, 1965;
Jones, 1967). Biliverdin and lutein can pro-
duce greenish to bluish ova in some phyllo-
medusines (Pyburn, 1963; Marinetti and
Bagnara, 1983), some hyperoliids (Wager,
1965), some rhacophorids (Liu, 1950), and
certain centrolenids (RWM, personal obser-
vation). These pigments are housed in the yolk
platelets (Barrio, 1965) and are from a differ-
ent source than the melanic pigments. The
greenish color can enhance concealment of
frog eggs from some predators (e.g., greenish
eggs deposited on the tops or undersides of
leaves) or provide infrared camouflage
(Schwalm et al., 1977; also see Saito, 2001).
Falchuk et al. (2002) have shown that
biliverdin IXa functions as a cytoplasmic de-
terminant that is essential to normal embryo-
genesis in early stages of Xenopus laevis. The
destruction of biliverdin via some wavelengths
of UV light may provide a mechanism for
understanding their detrimental effects (e.g.,
Blaustein et al., 1994). The omission of
melanic pigment in ova surely conserves some
reproductive energy, and embryos developing
from nonpigmented eggs sometimes do not
develop pigment until well after hatching.
CLUTCH MORPHOLOGY
Definitions
?Clutch? describes the total number of eggs
deposited per ovulation event independent of
the number or presence of a male(s), re-
productive or ovipositional mode, oviposition-
al behavior of parents, or number of ?groups?
(5 aggregate of eggs produced in a single
ovipositional bout; this term is useful when
one does not know the taxon or ovipositional
mode or number of bouts [i.e., single egg
laying event]) that occurred. The number of
ova ovulated sometimes exceeds the number
of eggs oviposited. For example, if a female
oviposits her ovulated complement in multiple
bouts, the total number of eggs deposited
makes up the clutch (i.e., a group in this case
is not the clutch). A pair of Smilisca phaeota
may deposit eggs among one to several
puddles in a single night (RWM, personal
observation); the eggs in each puddle com-
prise a group, are produced during a single
bout, and are only part of the clutch. Female
Ambystoma tigrinum may partition their
clutches into multiple discreet groups which
may be sired by one or more males; distances
between these groups in a single pond may
exceed 40 m (Gopurenko et al., 2006). Thus,
the organization of the total clutch, and not
the number or manner in which eggs emerge
from the female in a single bout, is important.
If a female ovulates and oviposits more than
once a year or in multiple years, she has
produced multiple clutches.
2007] HERPETOLOGICAL MONOGRAPHS 9
?Ovipositional mode? describes the mor-
phology of an aggregation of deposited eggs
(i.e., the clutch structure). Explanations of
how egg aggregates are produced and postu-
lates about the evolution of different struc-
tures are largely lacking. It seems apparent
that oviductal (i.e., jelly formation), oviposi-
tional (i.e., parental behavior), and postovipo-
sitional (e.g., jelly dissolution) processes are
involved. Differences in the rate or pattern of
release of eggs from a female also can
influence clutch structure. Oviposition site,
ovum number and size (Bernardo, 1996;
Pombal and Haddad, 2005; Salthe and Duell-
man, 1973; Summers et al., 2007), energy
content (e.g., Komoroski and Congdon, 2001;
Komoroski et al., 1998), pigmentation, sub-
sequent characteristics of development, larval
ecomorphology, and other such factors are not
directly considered in this review. In part, this
is because the functional roles of oviductal
(e.g., Greven, 2002, 2003) and especially
ovipositional (e.g., Aronson, 1943) factors are
not understood in sufficient detail. Likewise,
inaccurate, nonstandard terminology is a con-
stantly confounding problem. Livezey and
Wright (1947) and Wright and Wright (1949)
presented at least 14 terms, many of which
were ill-defined, to describe some arrange-
ment of a group of eggs. Several other workers
(e.g., Stebbins, 1951, 2003; Corkran and
Thoms, 1996) have used similar terms in the
same or different ways. A notable recent
exception is Anstis (2002) who clearly defined
the terms she used to describe the types of
egg aggregations of frogs from southeastern
Australia. In the interest of clarity and with no
implication of discrete organization, we use
?tier(s)? to describe a two- or three-dimen-
sional arrangement of eggs and restrict ?layer?
to descriptions of jelly morphology.
Other Considerations
Accurate observations and descriptions of
ovipositional events and the appearance of
deposited groups of eggs are lacking for most
amphibians but deemed essential for under-
standing amphibian reproduction in a broader
context. Difficulties stem from a general lack
of knowledge of the natural history of
amphibians, problems with egg and species
identifications, comparisons of eggs of differ-
ent ages, and inadequate observational tech-
niques. The mere presence of multiple,
confusing reflections and refractions from
various water and egg surfaces and the
extreme transparency of egg jellies can in-
terfere with accurate observations. For exam-
ple, Alcala and Brown (1956) reported that
Rana microdisca lays eggs on moist surfaces
on stream banks in a ??twice-coiled string.??
This note, presuming correct identifications of
the adult, the eggs, and the ovipositional
mode, is particularly vexing for the following
reasons: a moist surface on a stream bank is
a rare site for ranid egg deposition, to our
knowledge a string is unknown among ranid
frogs, and ?twice-coiled? is difficult to envision
(i.e., single string coiled upon itself versus two
strings with simple coils that are intertwined)
and possibly the result of disturbance.
The notion that each species oviposits in
one mode is usually sound (see Williams and
Tyler, 1994 for an interesting exception;
Marsh and Borrell, 2001), but some oviposi-
tional modes seem to blend from one into
another. This apparent blending frequently is
the result of variations in the ovipositional
behavior of the adults, disturbance at the
deposition sites, comparisons of eggs of
different ages, or a misinterpretation of the
mode. For example, an investigator who
observes single eggs deposited close together
or on top of each other, but with the presence
of single, disjunct eggs, might conclude (in-
accurately in our opinion, see below) that the
eggs are a clump. Eggs deposited by different
taxa as surface films float by different means
and must be observed closely to determine
whether the outer jellies are adherent or
coherent. Pairs of frogs that produce surface
films must have adequate room to maneuver;
movements in confined spaces sometimes
cause the eggs to sink. Species that deposit
egg masses and those depositing single eggs
must have suitable substrates to which to
attach their eggs. Eggs and clutches deposited
under artificial conditions (e.g., laboratory
containers, terrariums, plastic bags) may differ
from those deposited in the wild. As embryos
in clumps and masses approach hatching and
jelly layers begin to break down, a group of
eggs may rise to the water surface. Any
environmental condition that produces lots
10 HERPETOLOGICAL MONOGRAPHS [No. 21
of bubbles (e.g., increase in temperature,
bottom fermentation) can also raise eggs to
the surface where they may appear as a film.
Eggs in films often sink even during light rain,
strings and particularly rosaries often are
broken, and egg clusters commonly become
detached from their suspension points by
activities of attendant parents. All such con-
tingencies must be taken into account. Addi-
tionally, more observations on the actual
ovipositional behavior of adults (e.g., Aronson,
1943, 1944; Norris and Hosie, 2005; Pyburn,
1967, 1970, 1971) would add immeasurably to
our collective knowledge and facilitate a better
understanding of ovipositional modes.
Alytid (Alytes and Discoglossus) and pipid
(Pipa) frogs have a capsular chamber, and the
direct-developing ?Eleutherodactylus? may al-
so have such a chamber (Salthe, 1963). It may
be imperative that large eggs turn over quickly
when inverted to keep the embryo from being
damaged; the morphology of the jellies of
more direct developing eggs need to be
examined.
Information on the eggs of caecilians is
particularly scarce, but large eggs laid as
a rosary seem to prevail (Exbrayat, 2006; M.
Wake and M. Wilkinson, personal commu-
nications): Caecilia, Funk et al., 2004; Epi-
crionops niger, A. Lathrop, personal commu-
nication; Gegeneophis carnosus, Exbrayat and
Delsol, 1988; Seshachar, 1942; Hypogeophis,
RA, unpublished data); Ichthyophis ??glutino-
sus/malabarensis,?? Balakrishna et al., 1983;
Breckenridge and de Silva, 1973; Brecken-
ridge and Jayasinghe, 1979; Breckenridge et
al., 1987; Seshachar et al., 1982; I. cf.
kohtaoensis, Kupfer et al., 2004; Idiocranium
russeli, Sanderson, 1937; Siphonops annula-
tus, Cei, 1980; Go?ldi, 1899; S. paulensis, Gans,
1961; Montero et al., 2005; and Typhlonectes
compressicaudus, Sammouri et al., 1990).
These descriptions lack certain details, and
some are surely inaccurate. For example,
certain drawings of eggs of Ichthyophis spp.
(Himstedt, 1996:fig. 57; Sarasin and Sarasin,
1887?90, as reprinted in Angel, 1947:fig. 107)
suggest a cluster, but others (e.g., Himstedt,
1996:fig. 47) seemingly show a rosary. Con-
sidering that the preponderance of recent data
countering the likelihood of a cluster mor-
phology, we suggest that the earlier inter-
pretations are in error or the result of artistic
license.
Some aquatic (e.g., Dicamptodon, pletho-
dontines) and terrestrial (e.g., Aneides) sala-
manders ?suspend? (i.e., usually attach them to
the lower surfaces of substrates) their eggs.
The eggs may be ?pendant? (i.e., ovum is not
centered in the drooping outer jelly layer;
Fig. 3A) or not (i.e., ova centered within outer
jelly; Fig. 3B). As defined here, a ball with the
turgidity to maintain its spherical shape that is
stuck directly to a ceiling is suspended but not
pendant. A small area termed the ?pedicel?
attaches a suspended egg to a substrate, and
1?2 jelly layers may be involved in the
supporting part of the jelly.
Deposition Sites
Similar ovipositional modes are scattered
across amphibian groups and breeding sites,
and egg deposition site often has little to do
with clutch structure (e.g., foam nests are
placed in aquatic, arboreal, subterranean, and
terrestrial microhabitats; clumps are laid in
many different sites). Even so, the site of egg
deposition is a useful adjunct to egg identifi-
cation and species biology and has been
incorporated in the definitions of breeding
modes (Crump, 1974; Haddad and Prado,
2005). No available classification easily ac-
commodates all variations of oviposition sites
without being excessively complex. We sug-
gest that the environmental conditions to
which eggs are exposed would be a more
informative feature than specifically where the
eggs are deposited. Because eggs and embryos
associated with a mobile parent?s body (i.e., in
or on a parent?s body for all or part of
development, whether terrestrial or aquatic;
all endotrophic categories of Altig and John-
ston, 1989), especially those with a physiolog-
ical association with the parent, are subjected
to a different set of environmental variables
than eggs and embryos in the environment.
We place them in a separate general category
and note that their jellies, development, and
morphology are different from other types.
We thus recognize four major categories of
oviposition sites (parent-associated, terrestrial,
semiterrestrial, and aquatic) based on the
suite of biological (i.e., predators) and physical
(i.e., temperature and oxygen as mediated by
2007] HERPETOLOGICAL MONOGRAPHS 11
water and light; Cohen and Strathmann, 1996)
conditions that the eggs experience. Obviously
each category can be divided into subcate-
gories based on biological and physical factors.
Eggs in the parent-associated category
experience a unique and species-specific
range of physical conditions whether they
are exposed to the air (e.g., Alytes: wound
around legs of terrestrial male parent; Hemi-
phractus: attached openly on back of terres-
trial female parent; Fig. 4A) or not (e.g.,
Gastrotheca: dorsal pouch of terrestrial fe-
male; Pipa: embedded in back of aquatic
female). These conditions influence develop-
ment more than whether the eggs are
considered terrestrial or aquatic.
Terrestrial eggs, including those in foam
nests and in arboreal, fossorial, and sub-
FIG. 3.?Ovipositional modes. (A) A suspended, pendant egg, a group of which would form an array or cluster
depending on their arrangement, (B) a suspended, nonpendant egg, (C) an array, (D) a melded clump, (E) a mass, (F)
part of an open clump with interstices blackened for emphasis, (G) single eggs attached to submerged vegetation, (H)
a rosary, (I?K) egg strings that are (I) staggered in a unilayered tube, (J) uniserial in a bilayered tube, (K) uniserial in
a bilayered tube with partitions and scalloped margins, a (L) schematic of two adjacent eggs in a string showing how jelly
layers around each egg form partitions within the outer tube, and (M) a strand. A?B, D: modified from Stebbins, 2003,
C, E, G, H: modified from Pfingsten and Downs, 1989; F: modified from Liu, 1950; I?K: modified from Wright and
Wright, 1949, and M: redrawn by P. C. Ustach from Arnold and Burton, 1978.
12 HERPETOLOGICAL MONOGRAPHS [No. 21
terranean sites, are exposed to little or no free
water at least at the time of oviposition. Both
endotrophic and exotrophic forms deposit
eggs in the terrestrial environment. The
deposition sites often are near or above water,
but they are not part of an aquatic habitat. As
a result, predators on terrestrial eggs are
usually very different from those in aquatic
systems.
Semiterrestrial eggs are usually placed
adjacent to some source of free water but
are not submerged (e.g., in natural crevices or
constructed burrows in a stream bank, natural
or constructed depressions or chambers next
to or in an area where a pond will form,
among moss at the edge of a bog, in a seepy
talus). The nest site is sometimes temporary in
that it may become part of an aquatic system
FIG. 4.?Ovipositional modes. (A) Eggs attached to the back of a female Hemiphractus fasciatus (Hemiphractidae:
photo by E. Griffith), inset, most anterior embryo at larger size, (B) a cluster of Plethodon albagula (Plethodontidae;
photo by S. E. Trauth), (C) an array of Ambystoma barbouri (Ambystomatidae) on the underside of a stone in flowing
water (arrows 5 egg laid most recently by same or different female have less silt attached), and an (D) array of Spea
multiplicata (Scaphiopodidae) placed haphazardly on vegetation in a desert pool.
2007] HERPETOLOGICAL MONOGRAPHS 13
either through flooding or some form of adult
behavior.
Aquatic eggs that are placed in a lentic or
lotic site, in bromeliads or other phytotelms,
and in tree holes are submerged or nearly so
and experience distinct conditions particularly
associated with oxygenation. Within this
context, the differences between a stream
and a temporary puddle are obvious, but some
cases can be subjective. Water at lentic sites
may flow temporarily after heavy rains, and
the flow rate of some lotic sites is so slow that
they effectively represent lentic habitats.
Consideration of how an aquatic system
functions as a unit through time (e.g., bank
configuration, basin shape, vegetation pat-
terns, and debris distributions) and the bi-
ology of the amphibians that breed in them
usually will resolve conflicts in microhabitat
classification.
OVIPOSITIONAL MODES
In the following pages we describe five
categories of ovipositional modes: various
arrangements of independent eggs, three-di-
mensional arrangements, floating arrange-
ments, froth nests, and linear arrangements.
Among these categories, the constructs of the
14 ovipositional modes are summarized in
Table 1. Although the specific events that
occur during oviposition were not instrumental
in defining the modes, knowing that informa-
tion often enhances one?s understanding of the
how the final clutch structure was formed.
TABLE 1.?Summary of the various ovipositional modes (i.e., clutch structure) discussed in the text.
Independent Eggs
Single (Fig. 3G)?eggs free or attached to substrates, singly or haphazardly grouped; arrangements governed by
movement of parents during oviposition
Array (Figs. 3C, 4C, D)?singly placed eggs in some order, usually on a flat substrate; arrays on vegetation are more
haphazardly arranged; eggs on lower surfaces of submerged object usually suspended and pendant
Laminar array (Figs. 2D?H, 5D)?outer jellies of most, closely-spaced eggs independently contact a substrate (i.e., one
tier); various degrees of jelly hydration cause eventual shape of group.
Cluster (Figs. 3A, 4B)?small number of independently oviposited, suspended, pendant eggs with adjacent or
overlapping pedicels; usually terrestrial
Three-dimensional Arrangements
Clump (Fig. 2I, 3D, F)?a multitiered stack of aquatic or terrestrial eggs that lack a common, surrounding surface or
matrix; interstices among eggs common at least early in development; adjacent jellies remain distinct even if melded;
adjacent eggs adherent or not
Mass (Fig. 3E)?each egg has an individual jelly layer(s) plus an outer jelly layer that melds imperceptibly with its
neighbors so that ova appear embedded in a jelly matrix (i.e., the eggs and their jelly layers are like marbles
embedded in a volume of gelatin, the matrix); interstices between adjacent eggs absent
Sac (Fig. 5F?G)?a turgid, sausage-shaped covering formed by the basal portion of the oviduct that enclose all ova once
the jelly layers around individual eggs are formed by more anterior zones of the oviduct
Floating
Film (Fig. 2A?C)?adherent or coherent, usually single-tiered, group of eggs that float at or on the surface
Froth Nests
Foam (Fig. 5B?C)?each ovum with an independent jelly layer(s) embedded in a foam formed by many, small bubbles
being trapped throughout more fluid parts of the jelly by leg motions of the parents
Bubble (Fig. 5A)?a film or multitiered group of eggs supported by relatively few, larger bubbles captured by the
undersurface of the jelly; hind limbs of parents not involved in bubble production; limnodynastid females paddle with
the front limbs and pass bubbles beneath their bellies that float upwards under the eggs; one or both parents of some
microhylids expel bubbles from the nares beneath a film
Linear Arrangements
Bar?a short string, sometimes multiple short strings of eggs attached at their bases; may result at times when the outer
jelly layers of adjacent single eggs adhere to each other temporarily
String (Fig. 3I?L)?lengthy, uni- or bilayered outer jelly tube encasing a uniserial or biserial series of ova; each ovum
with independent jelly layer(s)
Strand (Fig. 3M)?lengthy, multiserial group of eggs in a large diameter, flimsy tube
Rosary (Fig. 3H)?lengthy, uniserial group of eggs in a string with jelly constricted between successive ova
14 HERPETOLOGICAL MONOGRAPHS [No. 21
Independent Eggs
We identified four arrangements of in-
dependent eggs that are most often oviposited
singly or a few at a time and do not produce an
organized clutch structure. The arrangement
of the eggs most often results from the
behavior of the breeding pair.
Single eggs.?Single eggs can be scattered
free, attached to substrates (Fig. 3G) in the
open or wrapped in aquatic leaves (Orizaola
and Bran?a, 2003) but usually are not pendant.
These eggs may be positioned singly or in
haphazard groups (i.e., as individuals placed
onto substrates); eggs deposited close to or on
top of each other usually have associated
outliers (e.g., Ambystoma mavortium, Pseu-
dacris crucifer; Fig. 3G) that signal that such
a group is not a clump.
Array.?An array is a group of eggs
suspended individually from the lower (under
surface of rocks - some plethodontine sala-
manders [Fig. 3C] and Ambystoma barbouri
[Fig. 4C]) or attached to the upper side of
rocks or tree roots (e.g., some cycloramphid
and phrynobatrachid frogs). Each egg that is
oviposited and attached independently may be
pendant or not and often has a distinct pedicel
composed of various jelly layers. The eggs may
be placed in an area with a diameter as large
or larger than the length of the adult, and
individual eggs may or may not contact
neighboring eggs. Arrays attached to a single
surface are orderly, but the group appears
more haphazard if it is deposited on multiple
stones or vegetation. The orderliness of the
egg arrangement is also likely a function of the
female?s behavior (e.g., Giaretta and Facure,
2004). Eggs of some Spea form a haphazard
array on sprigs of vegetation (Fig. 4D), and
differential hydration of the jelly around each
ovum forms a stalk without the ovum being
suspended or confined by other eggs.
Laminar array.?A laminar array is defined
by the method of egg attachment to a sub-
strate?all eggs are attached individually to
a substrate, usually in a single tier?like on
a leaf overhanging a water body. The shape of
the array may change dramatically depending
on whether the top or underside of a leaf is
used and on the subsequent pattern of
hydration. Eggs on the upper surface of leaves
frequently absorb water from rain and swell
considerably. Those on the undersides of
leaves (e.g., Lima et al., 2007) have less direct
contact with rain water, may not swell
appreciably, and are relatively spherical or
planar. Jelly layers of adjacent hydrated eggs
often meld imperceptibly to produce what
appears to be a melded clump or even a mass,
but eggs in clumps and masses are laid in
multiple tiers. Ova in laminar arrays may be
pigmented or not.
A hydrated clutch of Guibemantis depressi-
ceps (Mantellidae) looks like a clump, but in
fact, all the ova are usually in a single tier
(Fig. 2D) and a ?stalk? from each egg (Fig. 2F)
partially supports their attachment to the
upper surface of a vertically-oriented leaf
overhanging a pool (Fig. 2E). Only by observ-
ing oviposition and subsequent effects of
hydration is the real structure revealed. Based
on pictures of hydrated clutches from other
species, we assume that all species of ?Man-
tidactylus? (Fig. 2G?H) have stalked eggs and
produce this sort of laminar array. Other
species that produce similar arrays include
phrynobatrachids (e.g., Phrynodon sander-
soni, Amiet, 1981), many centrolenids (Ku-
bicki, 2005; RA and RWM, personal observa-
tions; Fig. 5D), some microhylids (e.g.,
Oreophryne spp., Johnston and Richards,
1993), and many hylids (e.g., species in the
leucophyllatus, microcephalus, and parviceps
groups of Dendropsophus, Faivovich et. al.,
2005, RA and RWM, personal observations).
The closeness of the eggs, consistency of the
jelly, and amount of hydration may influence
clutch shape. If the jelly is relatively stiff
(Figs. 2F, H, 5D) and becomes significantly
hydrated, the clutch may be thick and variously
shaped; in contrast, a clutch with watery jelly
with rather little hydration may be quite thin
(Fig. 2G). In all cases, the jelly becomes more
watery as embryos approach hatching. The
entire jelly volume of some centrolenid and
hylid eggs with this ovipositional mode droops
well beyond the original boundary of the
attached array and forms a ??drip-tip?? (Schlu?ter,
2005:figs. 64 and 65); tadpoles frequently hatch
from the eggs during rainstorms and slide
downwards off the tip of the leaf or exit the drip
tip into water below.
Cluster.?A cluster (Figs. 3A, 4B) is a group
of a few, individually suspended, pendant eggs
2007] HERPETOLOGICAL MONOGRAPHS 15
in one tier (dependent on the substrate) that
are typically laid by terrestrial salamanders.
The pedicels of the few large eggs lie close to
or on top of each other, and adjacent eggs
usually contact their neighbors (e.g., Paine,
2005).
Three-dimensional Arrangements
Eggs are arranged in some sort of three-
dimensional arrangement in three oviposition-
al modes.
Clump.?A clump (Fig. 3D, F) is a multi-
tiered stack of aquatic or terrestrial (Fig. 2I)
eggs, that lack a common, surrounding surface
or matrix; adjacent jellies remain distinct even
if melded and may be adherent or not. A
clump is analogous to a stack of marbles,
although in terrestrial settings, the stack
sometimes slides into a single tier (e.g.,
plethodontids). The surfaces of adjacent eggs
may be turgid enough to form interstices (i.e.,
?open clump?; Fig. 3F) or sag or fit together
without interstices (i.e., ?melded clump?;
Fig. 3D) either at the time of oviposition or
later. One can pour colored water over an
open clump and see the water percolating
through the interstices. A similar morphology
results when single eggs are haphazardly
placed close to or on top of each other;
however, clumps do not have outlier eggs.
FIG. 5.?Ovipositional modes. (A) Bubble nest of Limnodynastes sp. (Limnodynastidae) (B) foam nest of Physalaemus
pustulosus (Leiuperidae), (C) foam nest of Chiromantis xerampelina (Rhacophoridae) with attendant parent (arrow),
(D) arboreal clump of Hyalinobatrachium fleischmanni (Centrolenidae) on the underside of a leaf, (E) electron
micrograph of outer jelly layer of Xenopus laevis (modified from Bonnell and Chandler, 1998), (F) sac of Batrachuperus
karlschmidti (Hynobiidae) with embryos shaded for emphasis (modified from Liu, 1950), and (G) sac of Hynobius
kimurae (Hynobiidae; Southern Illinois University H-07590).
16 HERPETOLOGICAL MONOGRAPHS [No. 21
Thus, one must examine clumps closely to
determine their actual morphologies.
Most clumps involve relatively few eggs. In
contrast, many ranids lay eggs in large, aquatic
clumps that are open at least at oviposition
and deposited as a single unit. Adjacent jellies
are adherent. Even after the jellies swell or
sag enough to obliterate the interstices,
a regularly lobate surface is different from
the smooth to irregular surface of a mass (see
below). Some aquatic and terrestrial clumps
commonly have one surface attached to a sub-
strate or surrounded by a folded leaf (e.g.,
Phyllomedusa hypochondrialis, Pyburn, 1971)
and may result from multiple oviposition
bouts (e.g., Pachymedusa dacnicolor, Bagnara
et al., 1986). Other aquatic clumps are
typically rounded in top view, horizontally
oblong, and commonly surround a piece of
aquatic vegetation. Old, aquatic clumps with
embryos nearing hatching may break free
from their supports and float to the surface,
often with many bubbles trapped in the jelly;
the bubbles and multitiered structure distin-
guish them from surface films.
Mass.?In a mass of eggs (Fig. 3E), each
egg has an individual jelly layer(s) that appears
to be embedded in a jelly matrix (i.e., the eggs
and their jelly layers are like marbles embed-
ded in a volume of gelatin, the matrix; see
below). Colored water poured over a mass
flows only over the surface, which may be
irregular but is never regularly lobed like that
of a melded clump. The matrix may be
moderately sparse or voluminous relative to
the volume of the ova, which gives the
impression of the ova either being uniformly
distributed within the mass (e.g., Pseudacris)
or absent from the periphery of the mass (e.g.,
Ambystoma). The material forming the matrix
is not extruded separately from the outer
layers of jelly surrounding the ova (see below).
The egg jelly of most species of Ambystoma or
Pseudacris is watery and usually falls apart if
handled. In contrast, masses of Ambystoma
gracile and A. maculatum have a voluminous,
dense matrix and retain their shape when
removed from the water. Most masses start to
disintegrate at or immediately after hatching,
but the dense masses of these two Ambystoma
often persist for more than a month after the
embryos hatch (Regester et al., 2005; Regester
and Whiles, 2006). Most masses are vertically
oblong and usually attached to vegetation, and
females of Ambystoma tigrinum and others
may deposit a clutch among several, widely-
spaced masses (Gopurenko et al., 2006).
The fact that a mass may involve an entire
or a partial clutch reveals something about its
formation. The inner jelly layer(s) around
each ovum is distinct, but the more volumi-
nous outer layer is indistinct, seemingly
homogeneous, lacks a defining outer mem-
brane, and melds imperceptibly with neigh-
boring jellies. Thus, the outer egg jellies form
the seemingly homogeneous matrix of the
mass. The widths of the hydrated outer layers
determine the distribution and spacing of the
ova within a mass. If the width of the outer
jelly layer is thin, eggs appear uniformly
distributed throughout the mass (e.g., Pseu-
dacris); if the layer is thick, peripheral eggs
appear more widely spaced and particularly
isolated from the margin of the mass (e.g.,
Ambystoma).
Sac.?Sacs (Fig. 5F, G) are unique to
hynobiid salamanders. They are turgid sacs
that enclose all ova once the layers around
individual eggs are formed by the penultimate
zones of the oviduct (Greven, 2002, 2003).
Females usually extrude two unfused sacs per
ovulation event, one from the ovisac of each
oviduct. The sac is usually shaped like a curved
or spiraled sausage with a pointed distal end,
which emerges first and serves as the pedicel.
According to Liu (1950; also Sato, 1992) the
wall of the sac of Batrachuperus karlschmidti
is striated longitudinally, the embryos lie at
90u to the axis of the sac, and hatchlings
escape by forcing off the distal cap. Hasumi
(1996) noted that it took about 18 h for the sac
to form in Hynobius nigrescens after all eggs
arrived in the ovisac. The secretory mechanics
that form a sac around a group of eggs needs
further study.
Floating Arrangement
A single mode of floating eggs is described.
Film.?A film is usually a single sheet (i.e.,
a two-dimensional or planar tier) of either
?adherent?(i.e., outer jelly surface sticky so that
adjacent eggs adhere to each other; some
hyline and pelodryadinine hylids and ranid
frogs) or ?coherent? (i.e., outer jelly surface not
2007] HERPETOLOGICAL MONOGRAPHS 17
sticky so that adjacent eggs merely cohere and
can be pushed apart easily; many microhylid
frogs) dark or black eggs that float at or above
the water surface of a puddle or pond. Some
pelodryadinines deposit what appear to be
multi-tiered surface films (RA, personal ob-
servation). The statement by Schlu?ter and
Salas (1991) that the ??entire clutches [of
Chiasmocleis ventrimaculatus and Cteno-
phryne geayi] are held together by a thin
layer of viscous jelly?? needs verification; the
??layer of viscous jelly?? they observed may
actually be the meniscus distorted by the egg
jellies. Even light rain causes surface films to
sink, and eggs wetted by rain usually do not
float again. Films also may sink when the
embryos approach hatching. In either case,
a sunken film appears as a sheet draped over
vegetation or lying on the bottom. A film may
consist of part or all of the eggs in a clutch.
Films appear as single groups of eggs in
species (e.g., some microhylids) whose am-
plectant pairs do not move around much
between ovipositional bouts. In other species
(e.g., some hylids and other microhylids) the
amplectant parents may move around the
pond or even between puddles with each egg-
laying bout, splitting the clutch among multi-
ple ovipositional groups of eggs (5 ?rafts?). In
most cases, egg films remain afloat until after
the embryos hatch, but they may sink at an
earlier stage if they are physically disturbed or
rained upon.
Outer layers of jelly deposited in water are
somewhat hydrophobic at the moment of
oviposition. If eggs that typically are deposited
below the water happen to be extruded above
the water surface, part of the outer jelly
surface may remain unwetted, causing some
of the eggs to float (e.g., Scaphiopus holbroo-
kii; RA, personal observation). Although these
are not films, one must conclude that species
that produce films must have some behavior
whereby the vents of the parents are tempo-
rarily lifted above the water surface. In hylids
and microhylids, this is accomplished by the
amplectant pair tipping head-downward for
a few seconds while eggs are extruded (e.g.,
Pyburn, 1967; Webb, 1971). In at least some
North American ranids, the female arches her
back downwards, briefly placing her vent
above the water surface (Aronson, 1943). In
either case, extruded eggs, presumably sur-
rounded with either hydrophobic fluids or
flimsy jelly layers, spread outwards as they fall
upon the water surface. Eggs in such films
may rest entirely on the water surface (some
microhylids), be partially submerged (other
microhylids), or be submerged so that the
upper surface of the outer jelly lies at the
water surface (some hylids and ranids). Eggs
that rest on the surface have asymmetrical egg
jellies that likely facilitate floatation (e.g.,
species of Kaloula, Liu, 1950).
Eggs of Hyla chrysoscelis are laid as
multiple rafts of single-tiered, adherent films.
The rafts may drift together and adhere, and if
a breeze occurs, all films may end up on one
side of a pond and not at the actual
ovipositional sites. In freshly laid eggs, the
top part of the upper hemisphere of the outer
jelly layer is at the water surface but not
flattened; the ovum is centered at the radius
of the outer layer. An amorphous, very watery
gel that is not visible except by careful
examination in the laboratory lies external to
what appears as the outer jelly layer. This
adherent gel is more or less equidimensional
around the more discernible next inner layer
in submerged eggs. Observations through
a microscope suggest that pressure caused
by the weight of the egg sinking through the
surface distorts this flimsy gel toward the top
of the outer jelly layer to form a flat,
hydrophobic, surface that affords flotation
for the egg.
Eggs of Gastrophryne carolinensis are
oviposited as coherent films and lack the
rim-like protrusion of the outer jelly that is
found in several Old World microhylids. The
eggs float with about the upper fifth of the
outer jelly hemisphere above the water
surface (Fig. 2C). The jellies apparently lose
turgidity after a few hours, and the top of the
outer jelly then lies flattened and nonwetted
at the surface. The ovum remains centered
within the jelly so that its upper surface lies
slightly below the plane of the water surface.
Wright and Wright?s (1949; also Noble, 1927)
notations that the jellies of G. carolinensis
and Hypopachus variolosus are flat-topped
spheres apparently was based on observations
of eggs a number of hours after oviposition.
This nonstructural configuration apparently is
18 HERPETOLOGICAL MONOGRAPHS [No. 21
a function of surface tensions and hydropho-
bic characteristics of the jelly. Jellies of
submerged eggs are spherical.
Froth Nests
Froth nests are mixtures of oviductal
secretions (Bhaduri, 1932; Kabisch et al.,
1998) and air that have groups of eggs
dispersed through them. Such nests are pro-
duced by certain hylids (Haddad et al., 1990),
hyperoliids (Amiet, 1974), leptodactylids (e.g.,
Ho?dl, 1990; Schlu?ter, 1990; Shepard and
Caldwell, 2005), limnodynastids (e.g., Little-
john, 1963; Tyler and Davies, 1979), micro-
hylids (e.g., Glaw and Vences, 1992; Haddad
and Ho?dl, 1997), and rhacophorids (e.g., Coe,
1974; Fukuyama, 1991; Liu, 1950); and see
Duellman and Trueb (1986). Suggested func-
tions for froth nests include: escape from the
aquatic environment (Heyer, 1969), protec-
tion of eggs and embryos from desiccation and
thermal damage (Gorzula, 1977; Heyer, 1969;
Ho?dl, 1986), floatation for aquatic eggs
(Haddad and Ho?dl, 1997), protection from
aquatic predators and cannibals (Ho?dl, 1990;
but see Drewes and Altig, 1996 and Menin
and Giaretta, 2003), and enhanced oxygena-
tion of the eggs and embryos either from
being held near the meniscus (Haddad and
Ho?dl, 1997) or from the air trapped in the
bubbles per se. There are two types of froth
nests: foam and bubble.
Foam nests.?Foam nests typically are
formed when one or both parents whip
oviductal secretions with the hind legs to trap
numerous small air bubbles. The foam of
Scinax rizibilis is produced by the pair
jumping onto the jelly. The elaborate se-
quence of kicking and wiping behavior (e.g.,
Heyer and Rand, 1977; Ho?dl, 1990), which
enhances the mixing of sperm and eggs, varies
among species. This behavior likely evolved
from general movements used by the parents
to stabilize or maintain their positions in the
water (e.g., Rabb, 1973; Pipa pipa). Ho?dl
(1990; Physalaemus ephippifer), Liu (1950;
Polypedates leucomystax, and Coe (1974;
Chiromantis rufescens) indicated that the
foam-forming material is distinct from and
released prior to egg extrusion. In contrast,
Heyer and Rand (1977, Leptodactylus penta-
dactylus, Physalaemus pustulosus), Ryan
(1985, Physalaemus pustulosus, Fig. 5B), and
seemingly Schlu?ter (1990, Edalorhina perezi)
pointed out that it is a jelly-ova mixture that is
whipped into foam. Further detailed observa-
tions are needed in all cases. Perhaps the ova
with their jelly layers and an oviductal
secretion(s) that is whipped are released at
the same time. Simultaneous release of eggs
and secretions has been reported for Poly-
pedates bambusicola by Liu (1950). Coe
(1974) described and illustrated a discrete
structure called a ?foam gland? that formed
from three large oviductal folds along the
posterior sections of the oviduct in Chiroman-
tis rufescens; secretory cells lining the lumen
reportedly contained ?foam parent material.?
Similar structures present in foam-nesting
Leptodactylus spp. (RWM, personal observa-
tion) will be reported elsewhere.
Foam nests are formed in aquatic, arboreal,
subterranean, and terrestrial sites, and are
generally the result of a single reproductive
bout. Schlu?ter (1990) reported up to three
nestings by single pairs of Edalorhina perezi
(Leiuperidae) in a single night in captivity.
Whether this happens in other species is not
known. Males of E. perezi also are reported to
smooth the surface of the foam between egg
laying bouts (Schlu?ter, 1990). In most species,
a foam platform is built before the ova are
released. As eggs are extruded, the male
catches them in a ?basket? formed by his hind
feet, presumably fertilizes and moves them
dorsally onto his back, and then pushes them
into the foam with his hind legs (e.g.,
Physalaemus ephippifer, Ho?dl, 1990). In those
species studied, eggs are released in several
bouts and scattered throughout the mass of
foam, and trophic eggs are sometimes de-
posited in foam nests (Prado et al., 2005). In
arboreal cases the outer portion of the foam
dries to a crust (Fig. 5C; Coe, 1974). Bossuyt
and Milinkovitch (2000) suggested that arbo-
real foam nests of Asian Polypedates spp. could
be an initial step toward direct development on
land or trees (see Altig and Crother, 2006).
Actions of hatchlings and enzymes eventually
degrade the inner portion of the foam, and the
hatchlings stream out into the water or drop
into the water in arboreal species of Chiro-
mantis spp. and Polypedates spp. (Rhacophor-
idae; Liu, 1950; Coe, 1975).
2007] HERPETOLOGICAL MONOGRAPHS 19
Brizzi et al. (2003), Duellman and Trueb
(1986) and Ho?dl (1990) discussed variations in
foam nests and provided pertinent citations.
The ?foam? in nests of the hylid frog Scinax cf.
rizibilis was white, fragile, and full of large air
bubbles (Haddad et al., 1990); these authors
were able to produce foam by manually
beating the mucus present in the spawn of
Scinax heimalis, a close relative of S. rizibilis,
although a foam nest is not known in this
species. Perhaps foam can be formed from the
jelly of any species that has watery jelly if
parental behaviors were modified. Haddad
and Ho?dl (1997) pointed out that the foam
nests of S. rizibilis seem intermediate be-
tween a typical foam nest and the bubble nest
of Chiasmocleis leucosticta (see below), and
commented further that Scinax foam is pro-
duced by ??a few leaps of the female on the
eggs and jelly.?? If true, we predict the absence
of ?foam glands? in these species of Scinax.
Small groups of tadpoles of Leptodactylus
fuscus and related species can produce froth
from skin secretions and active wiggling well
after the original foam nest has disappeared
(Caldwell and Lopez, 1989; Downie and
Smith, 2003). The larval froth is clear with
larger bubbles than the white foam produced
by adults and allows larvae to survive for
longer periods out of water. The results of this
behavior appear adaptive, but whether the
actions are part of the tadpole?s behavioral
repertoire or byproducts of wiggling and air
gulping in a mucin-rich and probably oxygen-
poor environment is not known.
Bubble nests.?Bubble nests resemble foam
nests, but differ in having relatively few, large
bubbles. The resulting nest is typically flat to
dome-shaped in aquatic or subterranean sites.
The bubbles are formed in two different ways.
Some female limnodynastids (Tyler and Da-
vies, 1979; Williams and Tyler, 1994), with
flanges on some fingers, place their hands
successively above the water and then paddle
down and back to propel bubbles along their
bellies; the bubbles float upwards under the
surface film of oviposited eggs (Fig. 5A). This
may be another case in which escape or
stabilization maneuvers have been co-opted
for breeding functions. In contrast, pairs of
Chiasmocleis leucosticta (Microhylidae) de-
posit a surface film typical of most aquatic-
breeding microhylids. After oviposition is
complete, either the amplectant pair or the
male alone swims below the floating eggs and
expels air bubbles from the nostrils (Haddad
and Ho?dl, 1997). Presumably, eggs in bubble
nests develop faster in the better oxygenated
surface water and derive additional respirato-
ry benefit from the bubbles themselves.
Linear Arrangements
There are four morphological types of
linear arrangements.
Bar.?A bar is a short, linear arrangement
of eggs formed when the outer jelly layers of
adjacent eggs adhere to each other. A bar is
reminiscent of a short string of bufonid eggs,
but without the outer tube(s); several bars can
attach to each other at a common point to
form a rosette (Wright and Wright, 1949:plate
6). Whether a bar is real or a temporary
happenstance of single eggs remains unclear.
The outer tubes enclosing the eggs of Bufo
debilis and B. quercicus (Volpe and Dobie,
1959) are so diaphanous that they may not be
noticed, and these strings may look as if they
are arranged in a bar. The single eggs of Bufo
punctatus sometimes temporarily cohere to
form a bar or small groups of eggs one tier
thick (Stebbins, 1951; Miller and Stebbins,
1964:fig. 107).
String.?Strings (Fig. 3I?L) consist of a sin-
gle or double series of ova aligned linearly
inside either a uni- or bilayered jelly tube;
how the one or two tubes are formed around
a linear group of eggs is not known. An entire
clutch usually is laid as one, continuous, and
usually lengthy cord. The outer tube collects
silt but usually does not stick to itself;
uncommonly it is so diaphanous as to be
nearly invisible, and it is variably fragile
(Sweet, 1993; notably more fragile in Bufo
californicus than in B. boreas). One or
commonly two strings are extruded simulta-
neously, and an unknown tensile quality of the
jelly often causes the strings to lie initially in
a loose spiral. Slight constrictions between
successive ova may cause the outer surface of
the tube to appear scalloped (e.g., Bufo
cognatus, Bragg, 1936, 1950), and partitions
form by the juxtaposition of jelly layers
surrounding successive ova (Fig. 3L). Move-
ment of the amplectant adults during ovipo-
20 HERPETOLOGICAL MONOGRAPHS [No. 21
sition causes the string to be wound around
stems and leaves of aquatic plants or haphaz-
ardly about the bottom of the breeding site.
Rosary.?A rosary (Fig. 3H) is a string of
usually large and widely-separated ova in
which the jelly between successive eggs is
distinctly constricted and sometimes twisted;
whether the jelly is twisted during or after
oviposition is not clear. All components of the
tube appear to be continuous, but each ovum
may also have its own associated layers. A
rosary commonly becomes twisted upon itself
and may appear as a clump in terrestrially
breeding species (e.g., caecilians). The com-
mon inclusion of large ova is a striking feature
of this clutch form whether it occurs in
caecilians, salamanders that breed aquatically
(e.g., cryptobranchids), semiterrestrially (e.g.,
amphiumids), or terrestrially (e.g., various
plethodontines), or frogs (e.g., leiopelmatids,
alytids, some scaphiopodids).
Strand.?A strand (Fig. 3M; Pelobates) is
a large diameter tube with flimsy, sometimes
indistinct walls that contain multiple rows of
eggs that may meld together to form what
appears to be a mass. The rows of ova are not
arranged in lines as orderly as those in strings.
Strands typically are wound around aquatic
vegetation, often from bottom to top, or short
strands may be attached to vegetation or to
the bottom.
EVOLUTION OF CLUTCH STRUCTURE
Selective Factors
Amphibian eggs are rather fragile structures
that are subject to a variety of selective factors
in both the physical and biological environ-
ments in which they develop. Primary among
these are the abiotic factors of moisture,
temperature, and oxygen and the biological
factor of predation (e.g., Holomuzski, 1995;
Magnusson and Hero, 1991; Malone, 2006;
Mills et al., 2001; Woods, 1999). We contend
that the complex interaction among these
ecological factors and their temporal and
spatial patterns in those habitats in which
amphibians evolved have resulted in the
clutch structures characteristic of amphibians.
For purposes of this discussion, we assume
that the ancestral amphibian laid single eggs
(Mamay et al., 1998) in an aquatic environ-
ment. One can imagine that the dispersion of
eggs (highly clumped to widely scattered)
would pose different challenges for egg-eating
predators and, depending on the types of
predators and their ability to locate and
consume eggs, might favor the evolution of
different ovipositional modes. One set of
conditions might select for dispersed eggs
(e.g., single eggs scattered over a large area),
whereas another would favor groups of eggs
placed in areas that were difficult to locate.
At the same time, differences in moisture
availability (ephemeral puddles versus perma-
nent ponds), temperature (shallow and ex-
posed versus deep and shaded pools; temper-
ate versus tropical habitats; lowland versus
montane environments), and oxygen concen-
tration (surface versus bottom) would have
been important environmental variables that
may have favored one type of egg or
ovipositional mode over another. While these
environmental factors are easy to measure
today, their evolutionary impacts are more
difficult to demonstrate. Nevertheless we
suggest that predation on single eggs by
bottom feeding organisms (e.g., fish, other
amphibians, crustaceans, insects, leeches) had
a major selective impact on the placement of
eggs in ancestral environments. One solution
to the predation problem would be to hide
eggs beneath structures (e.g., under rocks in
streams) which would generally decrease, if
not eliminate, exposure to some bottom
feeding predators. Other solutions might
involve placement of eggs on aquatic vegeta-
tion above the bottom or into the surface film.
Such shifts could potentially facilitate de-
velopment by exposing eggs to higher oxygen
concentrations and warmer temperatures
(e.g., surface film) that result in faster de-
velopment and thereby a temporal escape
from predation. Avoidance of predators and
exposure to better developmental conditions
could also serve as the primary selective
factors resulting in shifts from one aquatic
ovipositional mode to another. Placing the
eggs completely out of the water on over-
hanging leaves or in burrows adjacent to the
stream or pond would eliminate exposure to
all aquatic predators. Such shifts would,
however, expose eggs to a different suite of
environmental problems (e.g., desiccation,
2007] HERPETOLOGICAL MONOGRAPHS 21
terrestrial predators) and favor the evolution
of elaborate behavioral traits (e.g., froth nests,
egg guarding, tadpole transport) and direct
development. The latter mode is often ac-
companied by changes in the outer jelly layers
and parental attendance.
Evolution of Ovipositional Modes
Observations of actual oviposition are un-
common, and hypotheses about the evolution
of ovipositional modes are almost completely
lacking. Primitive fishes (i.e., some lungfishes,
gars, paddlefish, and sturgeon) either scatter
single eggs on the bottom or among vegeta-
tion, and a few reports of eggs of primitive
amphibians exist. Mamay et al. (1998) de-
scribed groups of eggs assumed to be those of
a dissorophoid temnospondyl (Lower Perm-
ian, Wichita Group, Leonardian Series; Baylor
County, Texas). Based on terminology pre-
sented in this paper, those eggs were likely
oviposited as grouped singles or clumps. The
diameters of the ova and eggs (,0.5 mm) are
comparable to those of small, extant frogs. A
vitelline membrane and one jelly layer also
appears around each ovum. Witzmann and
Pfretzschner (2003) discussed the ontogeny,
morphology, and biology of an animal that
may have been similar to one that developed
from those eggs. S?pinar (1972) reported
ovarian or abdominal eggs (up to 0.6 mm
diameter) in Palaeobatrachus from the Ter-
tiary of central Europe but provided no
information on egg or clutch structure. With
no evidence to the contrary, we consider
single eggs as an appropriate starting point for
discussing the evolution of amphibian ovi-
position modes. Based on observations of
oviposition in a few species of temperate
Rana, Aronson (1943) posited that a surface
film type of oviposition likely was derived
from some sort of a submerged egg group
oviposition. Given the behavioral coordination
required of both parents to produce a film, we
agree.
The known diversity of ovipositional modes
in amphibians is not high, and with few
exceptions (e.g., sacs in hynobiid salaman-
ders), modes that appear structurally similar
are scattered throughout the Order. That is,
there seem to be relatively few ways to
package a series of spheres, and no clear
patterns of relationships between ovipositional
mode and systematic position are known.
These observations suggest that the evolution-
ary transition from one mode to another is not
a difficult matter, and that the resulting
morphological diversity likely is a consequence
of shifts in three aspects of amphibian biology:
changes in oviductal function, changes in
ovipositional behavior of the parents, and
postovipositional changes in the jelly layers
(e.g., formation of capsular chamber; also see
Lindsay and Hedrick, 2004). Variations in the
morphological and physiological components
of the female reproductive tract provide the
material on which selection can operate and
likely involve shifts (Table 2) in the following
components: timing of reproduction, rate and
synchrony of ovum maturation, frequency of
ovulation within and among clutches, rate of
egg passage down the oviduct, and changes in
the number, position, and function of various
secretory sections of the oviduct. Any changes
in the reproductive biology of females must
also be accompanied by concomitant changes
in the physiology and behavior of males, and
both are subject to natural selection from
TABLE 2.?Changes in egg and clutch morphology that
may represent evolutionary modifications during the
processes of egg production and deposition. Oviductal
processes 5 physiological and chemical changes in
secretory sites and their products that affect the ova as
they pass down the oviduct. Ovipositional modifications 5
morphological changes to eggs and clutches effected by
behavioral changes of parents at the time of egg
deposition. Postovipositional changes 5 changes in the
physical structure and chemical composition of the jelly.
Oviductal Processes
Increase or decrease in the number of jelly layers/zones
Change in stickiness so eggs are coherent or adherent
Shift from single eggs to string
Shift from single eggs to rosary
Change in hydrophobicity of outer jellies
Change in hygroscopic capacity of jelly components
Ovipositional Processes
Shift from single eggs to clump
Shift from single eggs to surface film
Shift from egg mass to surface film
Shift from single eggs to array
Shift from single eggs to cluster
Shift from single eggs to froth nests
Postovipositional Processes
Development of a capsular chamber
Shift from clump to a mass
Shift from string to strand
22 HERPETOLOGICAL MONOGRAPHS [No. 21
abiotic and biotic components of the habitats
in which amphibians breed.
A. Kupfer (personal communication) noted
that 1?2 h may pass between successive
expulsion events of the few eggs in a rosary
clutch of Ichthyophis cf. kohtaoensis. An
interaction between the rates of ovulation and
jelly formation likely explains this slow rate of
oviposition. It also seems likely that the rate of
jelly formation is the primary controlling factor
in most cases, although in the narrow confines
of the vermiform body of a caecilian, the
ovulation rate of the rather large eggs may also
be constrained. In contrast, the ovipositional
periods (time between first to last egg) of an
hour or less in North American Hyla and Rana
indicate that all eggs have been ovulated and
jellies produced before oviposition begins. An
intermediate situation may occur in Bufo that
lay long strings of eggs. In these species the
clutch is laid over several hours with periodic
expulsions of sections of the string; this pattern
suggests that jelly formation and perhaps even
ovulation have not been completed prior to the
start of oviposition. These responses may be
a result of large clutch sizes that cannot be
accommodated within the oviducts. Different
reproductive strategies associated with the
timing of ovulation relative to amplexus in
frogs is another issue. If ovulation is stimulated
by amplexus, as apparently occurs in some
species of Hyla, the amplectant pair must wait
some period for ovulation and jelly formation
to occur before depositing eggs (Scarliata and
Murphy, 2003; RA, personal observations). In
contrast, ovulation and formation of jelly layers
have already occurred at some point prior to
amplexus in female Pseudacris crucifer (Oplin-
ger, 1966) and Acris spp. (RA, personal
observation), as females of these species begin
to lay shortly after entering amplexus and
females ready to oviposit can hardly be handled
without eggs being extruded.
In summary, the reproductive patterns
characteristic of living amphibians are prod-
ucts of a variety of selective regimes encoun-
tered during the course of their evolution. The
diversity of modes reflects a long, complex
evolutionary history and the morphological,
physiological, and behavioral changes that
have been refined by various ecological and
energetic constraints (e.g., see Broomhall,
2004; Byrne et al., 2003; Kaplan, 1989;
Lu?ddecke, 2002; Ogielska and Kotusz, 2004;
Parichy and Kaplan, 1992, 1995; Seymour et
al., 2000; Semlitsch and Gibbons, 1990; Smith
et al., 2005). The eggs of Hyla chrysoscelis laid
late in the season often accumulate gas
bubbles released from bottom sediments and
suffer total mortality by daybreak presumably
from high temperatures and low oxygen
concentrations (RA, personal observation),
even though they are laid as a film. A review
and synthesis of the timing and influences of
factors such as the environment, adult mor-
phology, endocrinology, behavior, phylogeny,
and adult condition (i.e., all factors included in
the definitions of breeding mode) that mod-
ulate vitellogenesis, ovulation, jelly formation,
and breeding across taxa would provide
additional information useful in understand-
ing the evolution of these modes.
Changes in Oviductal Function
Changes in oviductal function across
lineages likely are manifest in structural
changes in the jelly layers and in clutch
morphology (e.g., singles to strings; singles to
sac; clump to mass; and perhaps strand-string-
rosary transitions). Strings versus rosaries
likely exemplify the influences of changes in
ovulatory and oviductal functions (i.e., string:
many small ova ovulated rapidly and passing
quickly in succession down the oviduct;
rosary: few, larger eggs ovulated less frequent-
ly and passing more slowly). The suspended,
pendant eggs of some plethodontids could be
derived from another mode if the few, large,
infrequently ovulated eggs that typically form
a rosary, were oviposited singly. These ideas
would demand that secretory sequences of
certain oviductal regions be modulated (e.g.,
continuous production of the outer jelly tube
in bufonids; intermittent production in pen-
dant eggs noted here). We presume that all
areas of the egg surface are competent to form
a pedicel at least for some short period
immediately after oviposition.
Changes in Adult Behavior
Courtship behaviors differ appreciably be-
tween species with internal (most salaman-
ders) versus external (most frogs) fertilization
and those that deposit eggs in terrestrial
2007] HERPETOLOGICAL MONOGRAPHS 23
versus aquatic habitats (Duellman and Trueb,
1986). It seems likely that many changes in
ovipositional mode are a result of changes in
the behavior of adults, especially in frogs (see
Ho?dl, 1990) where the presence of both
parents could influence ovipositional beha-
viors. The different roles that males and
females play during oviposition have been
described in detail for only a few species (e.g.,
Miller, 1909: Bufo americanus; Aronson, 1943:
Rana clamitans and R. catesbeiana; Aronson,
1944: B. americanus, B. fowleri, and B.
terrestris; Aronson and Noble, 1945; Noble
and Aronson, 1942: R. pipiens; Gosner and
Rossman, 1959: Pseudacris triseriata; Ho?dl,
1992: Pleurodema diplolistris; and Williams
and Tyler, 1994: Limnodynastes tasmanien-
sis). Male hynobiids sometimes pull the egg
sacs from the female but this behavior does
not modify the ovipositional mode. The
parents, especially in those species with
external fertilization, often engage in elabo-
rate and coordinated behavior (e.g., frogs that
build froth nests). In frogs, the position and
behavior of the male relative to the female
during external fertilization of eggs is espe-
cially variable. Knowing if and how the
activities of each partner influence clutch
structure, the timing of ovulation relative to
oviposition, the patterns of oviposition (e.g.,
partial or entire clutch extruded/bout), and
the co-ordination of behavioral signals be-
tween sexes would be valuable adjuncts to
understanding frog breeding biology, as would
insights into the presumed selective advan-
tages of the various modes of oviposition (e.g.,
Moore, 1940). Future consideration of data on
clutch structure from different lineages, ex-
amination of phylogenetic influences (e.g.,
Gomes and de Carvalho, 1995 and citations
therein), and an understanding of the evolu-
tion of complicated behaviors and how such
behaviors might influence clutch structure
surely will improve the resolution of our
preliminary ideas relative to the evolution of
clutch structure within Amphibia.
For example, surface films usually are
oviposited by the pair making temporary
forward dips to place the vents of both
individuals above the water surface, and
gametes of both sexes are released onto the
water surface. This behavior may have arisen
as an aborted surface dive initiated primarily
by the female and perhaps mediated by the
male. Wright?s (1914) description of oviposi-
tion and fertilization in Hyla versicolor seems
untenable; he stated that ??? fertilization took
place beneath the surface of the water??? and
??After each fertilization, the female would
raise her vent above the water and lay 18 to 25
eggs.?? Fertilization surely had to accompany
the release of the eggs. The oviposition of
Microhyla sp. was closely observed during
a frenzy of many pairs ovipositing at daybreak
in southern Vietnam (R. Altig, personal
observation). Pairs repeatedly made oviposi-
tional dips without moving, and a single,
conglomerate film of eggs accumulated di-
rectly behind each pair. One frightened
female made a presumed escape dive in
a similar manner and angle as an ovipositional
dip; at that point, some fluid, presumably
semen but it could have been urine, escaped
the vent of the male. Without knowing what or
if signals were being passed between the
partners to coordinate oviposition and fertil-
ization, one could interpret this observation as
the male mistaking the escape movement for
the next ovipositional dip. An analogous
argument for the ovipositional initiation and
completion of the loop-and-roll movement off
the bottom in Pipa pipa (Rabb, 1973; Rabb
and Rabb, 1960) could be made. Perhaps the
process is initiated by the female (i.e., the
loop, perhaps an aborted trip to the surface to
breath) but modified or guided (i.e., the roll,
attempting to intercept her progress) by the
male. Detailed observations and analyses of
other species are needed to clarify the origins
of these behaviors. The question concerning
the influences of males on ovipositing females
remains open.
Another example of how ovipositional
behavior influences clutch structure involves
the egg rafts produced by some hylid frogs
(e.g., Hyla chrysoscelis) that oviposit their
clutches in multiple rafts. These packets likely
are homologous to those parts of a clutch
deposited as separate masses by other hylids
(e.g., Pseudacris spp.). Stated otherwise, the
surface rafts of some Hyla would form a mass
if the eggs were oviposited underwater, and
eggs of Pseudacris that normally are laid as
a mass likely would produce a film if
24 HERPETOLOGICAL MONOGRAPHS [No. 21
oviposited onto the water surface. If an
amplectant pair that lays a clump or mass
moves sufficiently during oviposition, then
a group could be distributed as singles, as in P.
crucifer.
Building of froth nests is accomplished by
some amazing behaviors by the parent frogs.
Ho?dl (1990) presented a detailed description
of the formation of a foam nest in Physalae-
mus ephippifer. Some movements of the pair
are similar to those of other frogs and may
have been derived from the two-legged frog
kick commonly used for swimming (Abour-
achid and Green, 1999), stabilization, or
escape. The froth beating movements of the
male, on the other hand, seem different and
may have been associated with vent cleaning
or some other activity that facilitates fertiliza-
tion (basket formation, Miller, 1909). In some
ways the hind limb movements of males are
reminiscent of the peculiar ?wiping? behavior
of some phyllomedusine hylids (e.g., Blaylock
et al., 1976) and likely are derived from the
generalized cleaning and grooming behaviors
used by most frogs to remove debris or shed
skin. The limb churning is not rapid, but
sufficient air is mixed with the oviductal
secretions from the ?foam gland? to form
a surprisingly dense foam that is sometimes
voluminous. Similar behaviors have been
reported for nest construction in arboreal
rhacophorids but in these species the females
do most of the construction (Liu, 1950; Coe,
1975). Bubble nests are less organized struc-
tures than foam nests and are generated by
arm movements of the amplectant female
(limnodynastids) or bubble blowing by the
pair (microhylids). In bubble nests, egg jellies
typically remain visible (i.e., jelly not very
foamy) and adherent, and the whole clutch
floats on the surface (Fig. 5A).
Examples from North American Amphibians
Two examples from North American frogs
illustrate patterns of evolutionary shifts be-
tween ovipositional modes. For this discus-
sion, we distinguish three major groups of
North American ranids: (1) seven species of
?wood frogs? (R. sylvatica plus R. boylii group;
Hillis and Wilcox, 2005; Frost et al., 2006)
which have eggs with 2?3 jelly layers and
oviposit clumps (Wright and Wright, 1949),
(2) 13 species in the R. pipiens complex,
which have 2 jelly layers and oviposit clumps,
and (3) seven species of the R. catesbeiana
group, which have eggs with 1?2 jelly layers
and oviposit clumps (Rana septentrionalis,
a boreal species, and R. virgatipes, a south-
eastern Coastal Plain inhabitant) or surface
films (5 species). A simplified hypothesis
illustrates the distribution of clutch structures
on a cladogram (Fig. 6A; modified from Wolf,
1996:fig. 23). Species that oviposit clumps
include members of the R. pipiens group,
?wood frogs,? and two species of the R.
catesbeiana group. The remainder of the R.
catesbeiana group oviposits films. The pre-
viously proposed origin of a floating surface
arrangement from a submerged group seems
to be supported (see Evolution of Oviposi-
tional Modes and Aronson, 1943).
Another scheme (Fig. 6B; modified from
Cocroft and Ryan, 1995:fig. 2) for North
American hylids shows a different pattern.
Some hylids (e.g., Hyla chrysoscelis) oviposit
surface films while others (e.g., Pseudacris
spp.) deposit masses attached to vegetation or
FIG. 6.?Two cladograms showing the distributions of
oviposition modes in groups of (A) ranids (modified from
Wolf, 1996:fig. 23) and (B) hylids (modified from Cocroft
and Ryan, 1995:fig. 2).
2007] HERPETOLOGICAL MONOGRAPHS 25
scattered singles (e.g., P. crucifer). P. crucifer
lies among other mass-producing taxa. This
case is likely an example of adult behavior
modifying ovipositional mode. If amplectant
P. crucifer did not move as much during
oviposition, they would likely produce masses.
Patterns such as these suggest that certain
ovipositional modes are relatively labile and
easily changed by the behavior of amplectant
adults.
CONCLUDING COMMENTS
In summary, we have identified 14 ovipo-
sitional patterns within the Amphibia. These
modes reflect egg morphology, breeding
ecology, and postovipositional events, biotic
and abiotic conditions (i.e., ovipositional site),
and parental behavior (i.e., actions of males
and females during oviposition and fertiliza-
tion). We argue that the appearance of some
of these patterns is best understood from
a phylogenetic perspective but that others
may more closely reflect ecological influences
(e.g., Moore, 1940). More information on
ovipositional behavior is needed, as are
experimentally-based evaluations of the pre-
sumed ecological benefits of the various
modes. For example, when the temperature
is high, films seemingly are most effective
because they place the eggs in the most highly
oxygenated water at the surface; likewise,
because of their structure and position below
the surface, masses and clumps presumably
avoid freezing in cold weather. We suspect
that certain modes and their described varia-
tions are not always advantageous, and strat-
egies that are successful in one situation may
fail in another (margins of a species range;
modified or fragmented habitats; regional
changes in climate).
Clearly, information about amphibians
eggs, accounts of egg laying behavior, and
basic descriptions of the resulting clutch
morphology are limited, even for most of the
common members of the North American
fauna. We believe that considerable research
on descriptive natural history is needed. We
especially encourage colleagues to extend our
treatment across groups and into different
faunas. We are convinced that more detailed
examinations of ovipositional behaviors and
clutch structures will lead to the description of
additional ovipositional modes and the expan-
sion of our organizational framework. We are
aware that thorough examination of the details
of oviposition in some modes may show that
some of our interpretations are incorrect and
that some modes may better be treated as
a subsets of another. The extreme trans-
parency of egg jellies and the multiple
reflections from the jellies and water surfaces
present challenges to those studying eggs.
Nevertheless, we encourage field biologists to
collect and properly preserve identified
groups of amphibian eggs, recognizing that
appropriate fixatives are not generally avail-
able. The standard fixative of 10% buffered
formalin is clearly inadequate as it seldom
maintains the integrity of egg jellies over time.
Streck Tissue Fixative (STF) suggested as an
egg preservative by McDiarmid and Altig
(1999, Chapter 2) is no longer produced; we
are testing other nonaldehyde fixatives, and
new methods of preserving eggs and clutches
should be found. In addition, a relatively
simple method of sectioning eggs that keeps
the jelly layers intact would be helpful.
Amphibian biologists need to determine if
consistent and predictable patterns linking
ovum characteristics, habitat features, ovipo-
sitional modes, and deposition sites exist, and
if so, how they vary geographically and
taxonomically. The concept of reproductive
mode (e.g., Crump, 1974; Haddad and
Sawaya, 2000) attempts to distinguish some
of these patterns, but we suggest that the
undue attention given to features of deposi-
tion site and to egg number and size has
masked any phylogenetic signal that may be
revealed by the details of egg and clutch
structure. After improved observational tech-
niques have been devised and ovipositional
modes have been refined and described more
completely, a comprehensive and coordinated
research effort focused on the structure of egg
jellies and clutches should be undertaken. We
believe that the incorporation of egg and
clutch morphology into phylogenetic and
ecological analyses is long overdue and
anticipate the myriad positive contributions
that such information will make to our
understanding of amphibian diversity.
Acknowledgments.?Ideas, comments, and literature
provided by K. De Queiroz, J. Faivovich, T. Grant, H.
26 HERPETOLOGICAL MONOGRAPHS [No. 21
Greven, C. Prado, S. Salthe, D. Sever, M. Wake, M.
Wilkinson, and K. Zamudio sharpened our thinking and
improved this presentation. M. S. Foster and W. R. Heyer
critically read the entire manuscript and offered many
valuable comments and recommendations. R. Brandon, R.
C. Drewes, E. Griffith, and S. E. Trauth supplied
specimens or photographs, and P. Ustach provided the
drawing of Pelobates eggs. Persons at Chase Studio,
Cedarcreek, Missouri and Z. Roek kindly provided
citations on fossil eggs.
LITERATURE CITED
ABOURACHID, A., AND D. M. GREEN. 1999. Origins of the
frog-kick? Alternate-leg swimming in the primitive
frogs, families Leiopelmatidae and Ascaphidae. Journal
of Herpetology 33:657?663.
AL-ANZI, B., AND D. E. CHANDLER. 1998. A sperm
chemoattractant is released from Xenopus egg jelly
during spawning. Developmental Biology 198:366?375.
ALCALA, A. C., AND W. C. BROWN. 1956. Early life history
of two Philippine frogs with notes on deposition of eggs.
Herpetologica 12:241?246.
ALTIG, R. 1972. Notes on the larvae and premetamorphic
tadpoles of four Hyla and three Rana with notes on
tadpole color patterns. Journal of the Elisha Mitchell
Scientific Society 88:113?119.
ALTIG, R., AND B. I. CROTHER. 2006. The evolution of three
deviations from the biphasic anuran life cycle: alter-
natives to selection. Herpetological Review 37:321?325.
ALTIG, R., AND G. F. JOHNSTON. 1989. Guilds of anuran
larvae: relationships among developmental modes,
morphologies and habitats. Herpetological Mono-
graphs (3):81?109.
AMIET, J.?L. 1974. La ponte et la larve d?Opistothylax
immaculatus (Boulenger)(Amphibien Anoure). Annales
de la Faculte? Sciences du Cameroun 17:121?130.
AMIET, J.?L. 1981. Ecologie, e?thologie et de?veloppement
de Phrynodon sandersoni Parker, 1939 (Amphibia,
Anura, Ranidae). Amphibia-Reptilia 2:1?13.
ANDERSON, M. J., A. S. DIXSON, AND A. F. DIXSON. 2006.
Mammalian sperm and oviducts are sexually selected:
evidence for co-evolution. Journal of Zoology 270:
682?686.
ANGEL, F. 1947. Vie et moeurs des amphibiens. Payot,
Paris, France.
ANSTIS, M. 2002. Tadpoles of south-eastern Australia. A
guide with keys. New Holland Publishers, Pty. Ltd.,
Sydney, Australia.
ARNOLD, E. N., AND J. A. BURTON. 1978. A field guide to
the reptiles and amphibians of Britain and Europe.
Collins, London, U.K. 272 pages and 40 plates.
ARONSON, L. R. 1943. The sexual behavior of Anura 5.
Oviposition in the green frog, Rana clamitans, and the
bull frog, Rana catesbeiana. American Museum Novi-
tates (1224):1?6.
ARONSON, L. R. 1944. The sexual behavior of Anura 6. The
mating pattern of Bufo americanus, Bufo fowleri, and
Bufo terrestris. American Museum Novitates
(1250):1?15.
ARONSON, L. R., AND G. K. NOBLE. 1945. The sexual
behavior of Anura. 2. Neural mechanisms controlling
mating in the male leopard frog, Rana pipiens. Bulletin
of the American Museum of Natural History 86:85?139.
BACHMANN, M. D., R. G. CARLTON, J. M. BURKHOLDER, AND
R. G. WETZEL. 1986. Symbiosis between salamander
eggs and green algae: microelectrode measurements
inside eggs demonstrate effect of photosynthesis on
oxygen concentration. Canadian Journal of Zoology
64:1586?1588.
BAGNARA, J. T., L. IELA, F. MORRISETT, AND R. K. RASTOGI.
1986. Reproduction in the Mexican Leaf Frog (Pachy-
medusa dacnicolor). I. Behavioral and morphological
aspects. Occasional Papers of the Museum of Natural
History, The University of Kansas 121:1?31.
BALAKRISHNA, T. A., K. R. GUNDAPPA, AND K. SHAKUNTALA.
1983. Observations on the eggs and embryos of
Ichthyophis malabarensis (Taylor) (Apoda: Amphibia).
Current Science 52:990?991.
BARBIERI, F. D., AND E. J. DEL PINO. 1970. Jelly coats and
diffusible factor in anuran fertilization. Archives de
Biologie 86:311?321.
BARRIO, A. 1965. Cloricia fisiologica en batracios anuros.
Physis 25:137?142.
BERNARDO, J. 1996. The particular maternal effect of
propagule size, especially egg size: patterns, models,
quality of evidence and interpretations. American
Zoologist 36:216?236.
BHADURI, J. 1932. Observations on the urogenital system
of the tree-frogs of the genus Rhacophorus Kuhl, with
remarks on their breeding habits. Anatomischer Anzei-
ger 74:336?343.
BISHOP, S. C. 1943. Handbook of salamanders. The
Salamanders of the United States, of Canada, and of
Lower California. Comstock Publishing Company,
Ithaca, New York, U.S.A. [Reprinted 1994, Comstock
Classic Handbooks, Comstock Publishing Associates
Cornell University Press].
BLAUSTEIN, A. R., P. D. HOFFMAN, D. G. HOKIT, J. M.
KIESECKER, S. C. WALLS, AND J. B. HAYS. 1994. UV
repair and resistance to solar UV-B in amphibian eggs:
a link to population declines? Proceedings of the
National Academy of Sciences, U.S.A. 91:1791?1795.
BLAYLOCK, L. A., R. RUIBAL, AND K. PLATT-ALOIA. 1976.
Skin structure and wiping behavior of phyllomedusine
frogs. Copeia 1976:282?295.
BONNELL, B. S., AND D. E. CHANDLER. 1998. Egg jelly
layers of Xenopus laevis are unique in ultrastructure
and sugar distribution. Molecular and Reproductive
Development 44:212?220.
BOSSUYT, F., AND M. C. MILINKOVITCH. 2000. Convergent
adaptive radiations in Madagascan and Asian ranid
frogs reveal covariation between larval and adult traits.
Proceedings of the National Academy of Science,
U.S.A. 97:6585?6590.
BRAGG, A. N. 1936. Notes on the breeding habits, eggs,
and embryos of Bufo cognatus with a description of the
tadpole. Copeia 1:14?20.
BRAGG, A. N. 1940. Observations on the ecology and
natural history of Anura. V. The process of hatching in
several species. Proceedings of the Oklahoma Academy
of Science 20:71?74.
BRAGG, A. N. 1950. The identification of Salientia in
Oklahoma. Pp. 9?29. In A. N. Bragg, A. O. Weese, H. A.
Dundee, H. T. Fisher, A. Richards, and C. B. Clark
(Eds.), Researches on the Amphibia of Oklahoma. The
University of Oklahoma Biological Survey. University of
Oklahoma Press, Norman, Oklahoma, U.S.A.
2007] HERPETOLOGICAL MONOGRAPHS 27
BRAGG, A. N. 1964. Lens action by jelly of frog?s eggs.
Proceedings of the Oklahoma Academy of Science
44:23.
BRECKENRIDGE, W. R., AND G. I. S. DE SILVA. 1973. The
egg case of Ichthyophis glutinosus (Amphibia, Gymno-
phiona). Proceedings of the Ceylon Association for the
Advancement of Science 29:107.
BRECKENRIDGE, W. R., AND S. JAYASINGHE. 1979. Observa-
tions on the eggs and larvae of Ichthyophis glutinosus.
Ceylon Journal of Science (Biol. Sci.) 13:187?202, 2
plates.
BRECKENRIDGE, W. R., S. NATHANAEL, AND L. PEREIRA.
1987. Some aspects of the biology and development of
Ichthyophis glutinosus (Amphibia: Gymnophiona).
Journal of Zoology (London) 211:437?499.
BRIZZI, R., G. DELFINO, AND S. JANTRA. 2003. An overview
of breeding glands. Chapter 6, Pp. 253?317. In B. G. M.
Jamieson (Ed.), Reproductive Biology and Phylogeny of
Anura. Science Publishers, Inc., Enfield, New Hamp-
shire, U.S.A.
BROOMHALL, S. D. 2004. Egg temperature modifies
predator avoidance and the effects of the insecticide
endosulfan on tadpoles of an Australian frog. Journal of
Applied Ecology 41:105?113.
BYRNE, P. G., L. W. SIMMONS, AND J. D. ROBERTS. 2003.
Sperm competition and the evolution of gamete
morphology in frogs. Proceedings of the Royal Society
of London 270B:2079?2086.
CALDWELL, J. P., AND P. T. LOPEZ. 1989. Foam generating
behavior in tadpoles of Leptodactylus mystaceus.
Copeia 1989:498?502.
CAROTENUTO, C. C. 2001. Following passage through the
oviduct, the coelomic envelope of Discoglossus pictus
(Amphibia) acquires fertilizability upon reorganization,
conversion of gp42 to gp40, extensive glycosylation, and
formation of a specific layer. Molecular and Reproduc-
tive Development 58:318?329.
CARROLL, E. J. JR., AND J. L. HEDRICK. 1974. Hatching in
the toad Xenopus laevis: morphological events and
evidence for a hatching enzyme. Developmental Bi-
ology 38:1?13.
CARROLL, E. J. JR., S. H. WEI, G. M. NAGEL, AND R.
RUIBAL. 1991. Structure and macromolecular composi-
tion of the egg and embryo jelly coats of the anuran
Lepidobatrachus laevis. Development, Growth, and
Differentiation 33:37?43.
CEI, J. M. 1980. Amphibians of Argentina. Monitore
zoologico italiano (N.S.) Monograph 2, i?xii + 609 p.
CHIVERS, D. P., J. M. KIESECKER, A. MARCO, J. DEVITO,
M. T. ANDERSON, AND A. R. BLAUSTEIN. 2001. Predator-
induced life history changes in amphibians: egg pre-
dation induces hatching. Oikos 92:135?142.
COCROFT, R. B., AND M. J. RYAN. 1995. Patterns of
advertisement call evolution in toads and chorus frogs.
Animal Behaviour 49:283?303.
COE, M. 1974. Observations on the ecology and breeding
biology of the genus Chiromantis (Amphibia: Rhaco-
phoridae). Journal of Zoology (London) 172:13?34.
COHEN, C. S., AND R. R. STRATHMANN. 1996. Embryos at
the edge of tolerance: effects of environment and
structure of egg masses on supply of oxygen to embryos.
Biological Bulletin 190:8?15.
COOK, M. I., S. R. BEISSINGER, G. A. TORANZOS, AND W. J.
ARENDT. 2005. Incubation reduces microbial growth on
eggshells and the opportunity for trans-shell infection.
Ecology Letters 8:532?537.
CORKRAN, C. C., AND C. THOMS. 1996. Amphibians of
Oregon, Washington and British Colombia. A field
identification guide. Lone Pine Publishing, Vancouver,
British Columbia, Canada.
CORNMAN, I., AND N. GRIER. 1941. Refraction of light by
amphibian egg jelly. Copeia 1941:180.
CRUMP, M. L. 1974. Reproductive strategies in a tropical
anuran community. University of Kansas Museum of
Natural History, Miscellaneous Publications (61):1?68.
DANIEL, J. F. 1937. The living egg-cell of Triturus torosus.
Cytologia 1937:641?643.
DOWNIE, J. R., AND J. SMITH. 2003. Survival of larval
Leptodactylus fuscus (Anura: Leptodactylidae) out of
water: developmental differences and interspecific
comparisons. Journal of Herpetology 37:107?115.
DREWES, R. C., AND R. ALTIG. 1996. Anuran egg predation
and heterocannibalism in a breeding community of
East African frogs. Tropical Zoology 9:333?347.
DUELLMAN, W. E., AND L. TRUEB. 1986. Biology of
amphibians. McGraw-Hill Publishing Company, New
York, New York, U.S.A.
DUNSON, W. A., AND J. CONNELL. 1982. Specific inhibition
of hatching in amphibian embryos by low pH. Journal
of Herpetology 16:314?316.
EXBRAYAT, J.-M. 2006. Fertilization and embryonic de-
velopment. Chapter 12, Pp. 359?386. In J.-M. Exbrayat
(Ed.), Reproductive Biology and Phylogeny of Gymno-
phiona (Caecilians). Science Publishers, Inc., Enfield,
New Hampshire, U.S.A.
EXBRAYAT, J.-M., AND M. DELSOL. 1988. Oviparite? et
de?veloppement intra-ute?rin chez les gymnophiones.
Bulletin de la Societe Herpetologique de France
45:27?36.
FAIVOVICH, J., C. F. B. HADDAD, P. C. A. GARCIA, D. R.
FROST, J. A. CAMPBELL, AND W. C. WHEELER. 2005.
Systematic review of the frog family Hylidae, with
special reference to Hylinae: phylogenetic analysis and
taxonomic revision. Bulletin of the American Museum
of Natural History 294:1?240.
FALCHUK, K. H., J. M. CONTIN, T. S. DZIEDZIC, Z. FENG,
T. C. FRENCH, G. J. HEFFRON, AND M. MONTORZI. 2002.
A role for biliverdin IXa in dorsal axis development of
Xenopus laevis embryos. Proceedings of the National
Academy of Sciences of the United States of America
99:251?256.
FROST, D. R., T. GRANT, J. FAIVOVICH, R. H. BAIN, A. HASS,
C. F. B. HADDAD, R. O. DE SA?, A. CHANNING, M.
WILKINSON, S. C. DONNELLAN, C. J. RAXWORTHY, J. A.
CAMPBELL, B. L. BLOTTO, P. MOLER, R. C. DREWES, R. A.
NUSSBAUM, J. D. LYNCH, D. A. GREEN, AND W. C.
WHEELER. 2006. The amphibian tree of life. Bulletin of
the American Museum of Natural History 297:1?370.
FUKUYAMA, K. 1991. Spawning behaviour and male mating
tactics of a foam-nesting treefrog, Rhacophorus schle-
gelii. Animal Behaviour 42:193?199.
FUNK, W. C., G. FLETCHER-LAZO, F. NOGALES-SORNOSA, AND
D. ALMEIDA-REINOSO. 2004. First description of a clutch
and nest site for the genus Caecilia (Gymnophiona:
Caeciliidae). Herpetological Review 35:128?130.
GANS, C. 1961. The first record of egg laying in the
caecilian Siphonops paulensis Boettger. Copeia 1961:
490?491.
28 HERPETOLOGICAL MONOGRAPHS [No. 21
GERTON, G. L., AND J. L. HEDRICK. 1986. The vitelline
envelope to fertilization envelope conversion in eggs of
Xenopus laevis. Developmental Biology 116:1?7.
GIARETTA, A. A., AND K. G. FACURE. 2004. Reproductive
ecology and behavior of Thoropa miliaris (Spix, 1824)
(Anura, Leptodactylidae, Telmatobiinae). Biota Neo-
tropica 4:1?10.
GLAW, F., AND M. VENCES. 1992. A fieldguide to the
amphibians and reptiles of Madagascar. Moos-Druck,
Leverkusen, Germany.
GO?LDI, E. A. 1899. Ueber die Entwicklung von Siphonops
annulatus. Zoologische Jahrbu?cher 12:170?173, plate 9.
GOLLMANN, B., AND G. GOLLMANN. 1993. Hatching
dynamics of larvae of the Australian smooth froglets,
Geocrinia laevis and Geocrinia victoriana (Amphibia,
Anura, Myobatrachidae). Zoologische Anzeiger 229:
191?199.
GOMES, U. L., AND M. R. DE CARVALHO. 1995. Egg
capsules of Schroederichthys tenuis and Scyliorhinus
haeckelii (Chondrichthyes, Scyliorhinidae). Copeia
1995:232?236.
GOMEZ-MESTRE, U., J. C. TOUCHON, AND K. M. WARKEN-
TIN. 2006. Amphibian embryos and parental defenses
and a larval predator reduces egg mortality from water
mold. Ecology 87:2570?2581.
GOPURENKO, D., R. N. WILLIAMS, C. R. MCCORMICK, AND
J. A. DEWOODY. 2006. Insights into the mating habits of
the tiger salamander (Ambystoma tigrinum tigrinum) as
revealed by genetic parentage analyses. Molecular
Ecology 15:1917?1928.
GORZULA, S. 1977. Foam nesting in leptodactylids:
a possible function. British Journal of Herpetology
5:657?659.
GOSNER, K. L. 1960. A simplified table for staging anuran
embryos and larvae with notes on identification.
Herpetologica 16:183?190.
GOSNER, K. L., AND D. A. ROSSMAN. 1959. Observations on
the reproductive cycle of the swamp chorus frog,
Pseudacris nigrita. Copeia 1959:263?266.
GREVEN, H. 2002. The urodele oviduct and its secretions
in and after G. von Wahlert?s doctoral thesis ??Eileiter,
Laich und Kloake der Salamandriden.?? Bonner Zoolo-
gische Monographien 50:25?61.
GREVEN, H. 2003. Oviduct and egg-jelly. Pp. 151?181. In
David M. Sever (Ed.), Reproductive Biology and
Phylogeny of Urodela. Science Publishers, Inc., En-
field, New Hampshire, U.S.A.
HADDAD, C. F. B., AND W. HO?DL. 1997. New reproductive
mode in anurans: bubble nest in Chiasmocleis leucos-
ticta (Microhylidae). Copeia 1997:585?588.
HADDAD, C. F. B., J. P. POMBAL, JR., AND M. GORDO. 1990.
Foam nesting in a hylid frog (Amphibia, Anura). Journal
of Herpetology 24:225?226.
HADDAD, C. F. B., AND C. P. A. PRADO. 2005. Reproductive
modes in frogs and their unexpected diversity in the
Atlantic forest of Brazil. BioScience 55:207?217.
HADDAD, C. F. B., AND R. J. SAWAYA. 2000. Reproductive
modes of Atlantic hylid frogs: a general overview and
the description of a new mode. Biotropica 32:862?871.
HAMMEN, C. S. 1962. Carbon dioxide assimilation in the
symbiosis of the salamander Ambystoma maculatum
and the alga Oophila amblystomatis. Life Sciences
10:527?532.
HARDY, D. M., AND J. L. HEDRICK. 1992. Oviductin.
Purification and properties of the oviductal protease
that processes the molecular weight 43 000 glyroprotein
of the Xenopus laevis egg envelope. Biochemistry
31:4466?4472.
HARDY, J. D. JR. 1984. Frogs, egg teeth, and evolution:
preliminary comments on egg teeth in the genus
Eleutherodactylus. Bulletin of the Maryland Herpeto-
logical Society 20:1?11.
HARDY, L. M., AND M. C. LUCAS. 1991. A crystalline
protein is responsible for dimorphic egg jellies in the
Spotted Salamander, Ambystoma maculatum (Shaw)
(Caudata: Ambystomatidae). Comparative Biochemis-
try and Physiology 100A:653?660.
HASSINGER, D. D. 1970. Notes on the thermal properties
of frog eggs. Herpetologica 26:49?51.
HASUMI, M. 1996. Time required for ovulation, egg sac
formation, and ventral glad secretion in the salamander
Hynobius nigrescens. Herpetologica 52:605?611.
HEDRICK, J. L., AND C. KATAGIRI. 1988. Bufo japonicus
japonicus and Xenopus laevis laevis egg jellies contain
structurally related antigens and cortical granule lectin
ligands. Journal of Experimental Zoology 245:78?85.
HEYER, W. R. 1969. The adaptive ecology of the species
groups of the genus Leptodactylus (Amphibia, Lepto-
dactylidae). Evolution 23:421?428.
HEYER, W. R., AND A. S. RAND. 1977. Foam nest
construction in the leptodactylid frogs Leptodactylus
pentadactylus and Physalaemus pustulosus (Amphibia,
Anura, Leptodactylidae). Journal of Herpetology 11:
225?228.
HILLIS, D. M., AND T. P. WILCOX. 2005. Phylogeny of the
New World true frogs (Rana). Molecular Phylogenetics
and Evolution 34:299?314.
HIMSTEDT, W. 1996. Die Blindwu?hlen. Die Neue Brehm-
Bu?cherei; Bd. 630. Westarp Wissenschaften, Magde-
burg.
HO?DL, W. 1986. Foam nest construction in South
American leptodactylid frogs. Pp. 565?569. In Z. Roc?ek
(Ed.), Studies in Herpetology. Charles University,
Prague, Czechoslovakia.
HO?DL, W. 1990. An analysis of foam nest construction in
the neotropical frog Physalaemus ephippifer (Lepto-
dactylidae). Copeia 1990:547?554.
HO?DL, W. 1992. Reproductive behaviour in the neotrop-
ical foam-nesting frog Pleurodema diplolistris (Lepto-
dactylidae). Amphibia-Reptilia 13:263?274.
HOLOMUZSKI, J. R. 1995. Oviposition sites and fish-
deterrent mechanisms of two stream anurans. Copeia
1995:607?613.
HOYT, D. L. 1960. Mating behavior and eggs of the Plains
Spadefoot. Herpetologica 16:199?201.
HUNTER, T., AND S. VOGEL. 1986. Spinning embryos
enhance diffusion through gelatinous egg masses.
Journal of Experimental Marine Biology and Ecology
96:303?308.
ITOH, T., S. KAMIMURA, A. WATANABE, AND K. ONITAKE.
2002. Egg-jelly structure promotes efficiency of internal
fertilization in the newt, Cynops pyrrhogaster. Journal
of Experimental Zoology 292:314?322.
JOHNSTON, G. R., AND S. J. RICHARDS. 1993. Observations
on the breeding biology of a microhylid frog (genus
Oreophryne) from New Guinea. Transactions of the
Royal Society of Australia 117:105?107.
2007] HERPETOLOGICAL MONOGRAPHS 29
JONES, D. A. 1967. Green pigmentation in neotropical
frogs. Ph.D. Dissertation, University of Florida, Gai-
nesville, Florida, U.S.A.
KABISCH, K., H.-J. HERRMAN, P. KLOSSEK, H. LUPPA, AND K.
BRAUER. 1998. Foam gland and chemical analysis of
the foam of Polypedates leucomystax (Gravenhorst
1829)(Anura: Rhacophoridae). Russian Journal of
Herpetology 5:10?14.
KAPLAN, R. H. 1989. Ovum size plasticity and maternal
effects on the early development of the frog, Bombina
orientalis, in a field population in Korea. Functional
Ecology 3:597?604.
KOMOROSKI, M. J., AND J. D. CONGDON. 2001. Scaling of
nonpolar lipids with ovum size in the mole salamander,
Ambystoma talpoideum. Journal of Herpetology
35:517?521.
KOMOROSKI, M. J., R. D. NAGLE, AND J. D. CONGDON. 1998.
Relationships of lipids to ovum size in amphibians.
Physiological Zoology 71:633?641.
KUBICKI, B. 2005. Glass frogs of Costa Rica (Family
Centrolenidae). Costa Rican Amphibian Research
Center field laminate series, plates 1?4. [www.
cramphibian.com].
KUPFER, A., J. NABHITABHATA, AND W. HIMSTEDT. 2004.
Reproductive ecology of female caecilian amphibians
(genus Ichthyophis): a baseline study. Biological
Journal of the Linnean Society 83:207?217.
LARABELL, C. A., AND D. E. CHANDLER. 2005. Quick-
freeze, deep-etch, rotary-shadow views of the extracel-
lular matrix and cortical cytoskeleton of Xenopus laevis
eggs. Journal of Electron Microscopy Technique
13:228?243.
LI, J.-C. 1934. Studies of the ??rain frog?? Kaloula borealis.
I. The adaptive features of the early embryo. Peking
Natural History Bulletin 9:57?70, 1 plate.
LIMA, A. P., D. E. A. SANCHEZ, AND J. R. D. SOUZA. 2007. A
new Amazonian species of the frog genus Colostethus
(Dendrobatidae) that lays its eggs on undersides of
leaves. Copeia 2007:114?122.
LINDSAY, L. L., AND J. L. HEDRICK. 2004. Proteolysis of
Xenopus laevis egg envelope ZPA triggers envelope
hardening. Biochemical and Biophysical Research
Communications 324:648?654.
LITTLEJOHN, M. J. 1963. The breeding biology of the Baw
Baw frog Philoria frosti Spencer. Proceedings of the
Linnean Society of New South Wales 88:273?276.
LIU, C.-C. 1950. Amphibians of western China. Fieldiana:
Zoology Memoirs 2:1?400, 10 plates.
LIVEZEY, R. L., AND A. H. WRIGHT. 1947. A synoptic key to
the salientian eggs of the United States. The American
Midland Naturalist 37:179?222.
LU?DDECKE, H. 2002. Variation and trade-off in reproduc-
tive output of the Andean frog Hyla labialis. Oecologia
130:403?410.
LUTZ, B. 1944. Observao?es so?bre batra?quios com desen-
volvimento direto; a eclosa?o Eleutherodactylus parvus
Girard. Boletim do Museu Nacional, Rio de Janeiro,
Zoologia (15):1?7.
MAES, E., Y. PLANCKE, F. DELPLACE, AND G. STRECKER.
1995. Primary structure of acidic oligosaccharide-
alditols derived from the jelly coat of Ambystoma
tigrinum. European Journal of Biochemistry 230:
146?156.
MAGNUSSON, W. E., AND J. M. HERO. 1991. Predation and
the evolution of complex oviposition behaviour in
Amazon rainforest frogs. Oecologia 86:310?318.
MALONE, J. H. 2006. Ecology of the basin construction
reproductive mode in Smilisca sordida (Anura: Hyli-
dae). Journal of Herpetology 40:230?239.
MAMAY, S. H., R. W. HOOK, AND N. HOTTON, III. 1998.
Amphibian eggs from the Lower Permian of north-
central Texas. Journal of Vertebrate Paleontology
18:80?84.
MARQUIS, O., A. MILLERY, S. GUITTONNEAU, AND C. MIAUD.
2006. Toxicity of PAHs and jelly protection of eggs in
the common frog Rana temporaria. Amphibia-Reptilia
27:472?475.
MARSH, D. M., AND B. J. BORRELL. 2001. Flexible
oviposition strategies in Tu?ngara frogs and their
implications for tadpole spatial distributions. Oikos
93:101?109.
MARINETTI, G. V., AND J. T. BAGNARA. 1983. Yolk pigments
of the Mexican leaf frog. Science 219 (4587):985?987.
MCDIARMID, R. W., AND R. ALTIG (Eds.). 1999. Tadpoles.
The Biology of Anuran Larvae. University of Chicago
Press, Chicago, Illinois, U.S.A. xvi + 444 pp.
MCDIARMID, R. W., AND R. D. WORTHINGTON. 1970.
Concerning the reproductive habits of tropical pletho-
dontid salamanders. Herpetologica 26:57?70.
MCLAUGHLIN, E. W., AND A. A. HUMPHRIES, JR. 1978. The
jelly envelopes and fertilization of eggs of the newt,
Notophthalmus viridescens. Journal of Morphology
158:73?90.
MENIN, M., AND A. A. GIARETTA. 2003. Predation on foam
nests of leptodactyline frogs (Anura: Leptodactylidae)
by larvae of Beckeriella niger (Diptera: Ephydridae).
Journal of Zoology 261:239?243.
MILLER, A. H., AND R. C. STEBBINS. 1964. The lives of
desert animals in Joshua Tree National Monument.
University of California Press, Berkeley and Los
Angeles, California, U.S.A.
MILLER, N. 1909. The American toad (Bufo lentiginosus
americanus, LeConte). The American Naturalist 43:
641?668, 730?744.
MILLS, N. E., M. C. BARNHART, AND R. D. SEMLITCH. 2001.
Effects of hypoxia on egg capsule conductance in
Ambystoma (Class Amphibia, Order Caudata). Journal
of Experimental Biology 204:3747?3753.
MONTERO, I., S. REICHLE, AND A. KUPFER. 2005. Observa-
tions on the reproductive ecology of Siphonops
paulensis Boettger, 1892 (Gymnophiona: Caeciliidae)
in Bolivia. Salamandra 41:91?94.
MOOI, R. D. 1990. Egg surface morphology of pseudo-
chromoids (Perciformes, Percoidea), with comments on
its phylogenetic implications. Copeia 1990:455?475.
MOORE, J. A. 1940. Adaptive differences in the egg
membranes of frogs. The American Naturalist 74:
89?93.
NOBLE, G. K. 1926. The hatching process of Alytes,
Eleutherodactylus and other amphibians. American
Museum Novitates (229):1?7.
NOBLE, G. K. 1927. The value of life history data in the
study of the evolution of the Amphibia. Annals of the
New York Academy of Sciences 30:31?128, plate 14.
NOBLE, G. K., AND L. R. ARONSON. 1942. The sexual
behavior of Anura. 1. The normal mating pattern of
30 HERPETOLOGICAL MONOGRAPHS [No. 21
Rana pipiens. Bulletin of the American Museum of
Natural History 80:127?142, plates 15 and 16.
NORRIS, K. M., AND C. A. HOSIE. 2005. A quantified
ethogram for oviposition in Triturus newts: description
and comparison of T. helveticus and T. vulgaris.
Ethology 111:357?366.
NUSSBAUM, R. A. 1969. Nests and eggs of the Pacific Giant
Salamander, Dicamptodon ensatus (Eschscholtz). Her-
petologica 25:257?262.
OGIELSKA, M., AND A. KOTUSZ. 2004. Pattern and rate of
ovary differentiation with reference to somatic de-
velopment in anuran amphibians. Journal of Morphol-
ogy 259:41?54.
OPLINGER, C. S. 1966. Sex ratio, reproductive cycles, and
time of ovulation in Hyla crucifer crucifer Wied.
Herpetologica 22:276?283.
ORIZAOLA, G., AND F. BRAN?A. 2003. Oviposition behaviour
and vulnerability of eggs to predation in four newt species
(genus Triturus). Herpetological Journal 13:121?124.
PAINE, T. 2005. Cover photo ? Eggs of Aneides lugubris.
Herpetological Review 36:1.
PARICHY, D. M., AND R. H. KAPLAN. 1992. Maternal effects
on offspring growth and development depend on
environmental quality in the frog Bombina orientalis.
Oecologia 91:579?586.
PARICHY, D. M., AND R. H. KAPLAN. 1995. Maternal
investment and developmental plasticity: functional
consequences for locomotor performance on hatchling
frog larvae. Functional Ecology 9:606?617.
PETRANKA, J. W., J. J. JUST, AND E. C. CRAWFORD. 1982.
Hatching of amphibian embryos; the physiological
trigger. Science 217:257?259.
PFINGSTEN, R. A., AND F. L. DOWNS (Eds.). 1989.
Salamanders of Ohio. Bulletin of the Ohio Biological
Survey 7 (2):i?xx, 1?315, 29 plates.
POMBAL, J. P., JR., AND C. F. B. HADDAD. 2005. Estrate?gias
e modos reproductivos de anuros (Amphibia) em uma
poa permanente na Serra de Paranapiacaba, Sudeste do
Brasil. Pape?is Avulsos de Zoologia 45:201?213.
PRADO, C. P. A., L. F. TOLEDO, J. ZINA, AND C. F. B.
HADDAD. 2005. Trophic eggs in the foam nests of
Leptodactylus labyrinthicus (Anura, Leptodactylidae):
an experimental approach. Herpetological Journal
15:279?284.
PYBURN, W. F. 1963. Observations on the life history of the
treefrog, Phyllomedusa callidryas (Cope). The Texas
Journal of Science 15:155?170.
PYBURN, W. F. 1967. Breeding and larval development of
the hylid frog Phrynohyas spilomma in southern
Veracruz, Mexico. Herpetologica 23:184?194.
PYBURN, W. F. 1970. Breeding behavior of the leaf-frogs
Phyllomedusa callidryas and Phyllomedusa dacnicolor
in Mexico. Copeia 1970:209?218.
PYBURN, W. F. 1971. Nests and breeding behavior of
Phyllomedusa hypochondrialis in Colombia. Journal of
Herpetology 5:49?52.
RABB, G. B. 1973. Evolutionary aspects of the reproduc-
tive behavior of frogs. Pp. 213?227. In J. L. Vial (Ed.),
Evolutionary Biology of the Anurans: Contemporary
Research on Major Problems. University of Missouri
Press, Columbia, Missouri, U.S.A.
RABB, G. B., AND M. S. RABB. 1960. On the mating and
egg-laying behavior of the Surinam Toad, Pipa pipa.
Copeia 1960:271?276.
REGESTER, K. J., K. R. LIPS, AND M. R. WHILES. 2005. Energy
flow and subsidies associated with the complex life cycle
of ambystomatid salamanders in ponds and adjacent
forest in southern Illinois. Oecologia 147:303?314.
REGESTER, K. J., AND M. R. WHILES. 2006. Decomposition
rates of salamander (Ambystoma maculatum) life stages
and associated energy and nutrient fluxes in ponds and
adjacent forest in southern Illinois. Copeia 2006:
640?649.
RUTH, B. C., W. A. DUNSON, C. L. ROWE, AND S. B.
HEDGES. 1993. A molecular and functional evaluation of
the egg mass color polymorphism of the spotted
salamander, Ambystoma maculatum. Journal of Herpe-
tology 27:306?314.
RYAN, M. J. 1985. The Tu?ngara Frog. A study in sexual
selection and communication. University of Chicago
Press, Chicago, Illinois, U.S.A.
SAITO, H. 2001. Blue biliprotein as an effective factor for
cryptic colouration in Rhodinia fugax larvae. Journal of
Insect Physiology 47:205?212.
SALTHE, S. N. 1963. The egg capsules in the Amphibia.
Journal of Morphology 113:161?171.
SALTHE, S. N., AND W. E. DUELLMAN. 1973. Quantitative
constraints associated with reproductive mode in
anurans. Pp. 229?249. In J. L. Vial (Ed.), Evolutionary
Biology of the Anurans: Contemporary Research on
Major Problems. University of Missouri Press, Colum-
bia, Missouri, U.S.A.
SAMMOURI, R., S. RENOUS, J. M. EXBRAYAT, AND J. LESCURE.
1990. De?veloppement embryonnaire de Typhlonectes
compressicaudus (Amphibia, Gymnophiona). Annales
Sciences Naturelles Zoologie, Paris, Ser. 13, 11:135?163.
SANDERSON, I. T. 1937. Animal Treasure. Viking Press,
New York. 325 p.
SARASIN, P., AND F. SARASIN. 1980?90. Zur Entwicklungs-
geschichte und Anatomie der Ceylonesischen Blind-
wu?hle Ichthyophis glutinosus (Epicrium glutinosum
Aut.). Zweiter Band, Heft 1?4, 263 pages, 24 plates. In
Ergebnisse Naturwissenschaftlicher Forschungen auf
Ceylon in den Jahren 1884?1886. C. W. Kreidel?s
Verlag, Wiesbaden.
SATO, T. 1992. Reproductive behavior in the Japanese
salamander Hynobius retardatus. Japanese Journal of
Herpetology 14:184?190.
SCARLIATA, J. K., AND C. G. MURPHY. 2003. Timing of
oviposition by female barking treefrogs (Hyla gratiosa).
Journal of Herpetology 37:580?582.
SCHLU?TER, A. 1990. Reproduction and tadpole of Eda-
lorhina perezi (Amphibia, Leptodactylidae). Studies on
Neotropical Fauna and Environment 25:49?56.
SCHLU?TER, A. 2005. Amphibian an einem Stillgewa?sser in
Peru. Edition Chimaira, Frankfurt am Main. 347 p.
SCHLU?TER, A., AND A. W. SALAS. 1991. Reproduction,
tadpoles, and ecological aspects of three syntopic
microhylid species from Peru (Amphibia: Microhyli-
dae). Stuttgarter Beitra?ge zur Naturkunde, Ser. A,
(458):1?17.
SCHWALM, P. A., P. H. STARRETT, AND R. W. MCDIARMID.
1977. Infrared reflectance in leaf-sitting neotropical
frogs. Science 196:1225?1227.
SEMLITSCH, R. D., AND J. W. GIBBONS. 1990. Effects of egg
size on success of larval salamanders in complex aquatic
environments. Ecology 71:1789?1795.
2007] HERPETOLOGICAL MONOGRAPHS 31
SESHACHAR, B. R. 1942. The eggs and embryos of
Gegeneophis carnosus (Bedd.). Current Science
11:439?441.
SESHACHAR, B. R., J. A. BALAKRISHNA, K. SHAKUNTALA, AND
K. R. GUNDAPPA. 1982. Some unique features of egg
laying and reproduction in Ichthyophis malabarensis
(Taylor)(Apoda: Amphibia). Current Science 51:32?34.
SEYMOUR, R. S., J. D. ROBERTS, N. J. MITCHELL, AND A. J.
BLAYLOCK. 2000. Influence of environmental oxygen on
development and hatching of aquatic eggs of the
Australian frog, Crinia georgiana. Physiological and
Biochemical Zoology 73:501?507.
SHAVER, J. R. 1966. Immunobiological studies of the jelly-
coats of anuran eggs. American Zoologist 6:75?87.
SHEPARD, D. B., AND J. P. CALDWELL. 2005. From foam to
free-living: Ecology of larval Leptodactylus labyrinthi-
cus. Copeia 2005:803?811.
SHIVERS, C. A., AND J. M. JAMES. 1970. Morphology and
histochemistry of the oviduct and egg-jelly layers in the
frog, Rana pipiens. Anatomical Record 166:541?555.
SMITH, M. A., M. BERRILL, AND C. KAPRON. 2002.
Photolyase activity of the embryo and the ultraviolet
absorbance of embryo jelly for several Ontario amphib-
ian species. Canadian Journal of Zoology 80:1109?1116.
SMITH, M. J., M. M. DREW, M. PEEBLES, AND K. SUMMERS.
2005. Predator cues during the egg stage affect larval
development in the gray treefrog, Hyla versicolor
(Anura: Hylidae). Copeia 2005:169?173.
S?PINAR, Z. V. 1972. Tertiary frogs from central Europe.
Academia Publishing House of the Czechoslovak
Academy of Sciences, Prague. 286 pages, 184 plates.
STEBBINS, R. C. 1951. Amphibians of western North
America. University of California Press, Berkeley and
Los Angeles, California, U.S.A.
STEBBINS, R. C. 2003. A field guide to western reptiles and
amphibians. 3rd ed. Houghton Mifflin Co., Boston,
Massachusetts & New York, New York, U.S.A.
STEINKE, J. H., AND D. G. BENSON, JR. 1970. The structure
and polysaccharide cytochemistry of the jelly envelopes
of the egg of the frog, Rana pipiens. Journal of
Morphology 130:57?66.
STIASSNY, M. L. J., AND J. MEZEY. 1993. Egg attachment
systems in the family Cichlidae (Perciformes: Labroi-
dei), with some comments on their significance for
phylogenetic studies. American Museum Novitates,
(3058):1?11.
STRATHMANN, R. R., AND C. CHAFFEE. 1984. Constraints on
egg masses. II. Effects of spacing, size, and number of
eggs on ventilation of masses of embryos in jelly,
adherent groups, or thin-walled capsules. Journal of
Experimental Marine Biology and Ecology 84:85?93.
SUMMERS, K., C. S. MCKEON, H. HEYING, J. HALL, AND W.
PATRICK. 2007. Social and environmental influences on egg
size evolution in frogs. Journal of Zoology 271:225?232.
SWEET, S. 1993. Second report on the biology and status of
the Arroyo Toad (Bufo microscaphus californicus on the
Los Padres National Forest of southern California.
Contract report to USDA, Forest Service, Los Padres
National Forest, Goleta, California, U.S.A.
TAKAMUNE, K., L. LINDSAY, J. L. HEDRICK, AND C. KATAGIRI.
1987. Comparative studies of Bufo and Xenopus laevis
vitelline coat molecular transformations induced by
homologous and heterologous oviducal pars recta pro-
teases. Journal of Experimental Zoology 244:145?150.
TAYLOR, E. H. 1922. Additions to the herpetological fauna
of the Philippine Islands, II. Philippine Journal of
Science 21 (3):257?303, plates 1?4.
THUMM, K., AND M. MAHONY. 2002. Hatching dynamics
and bet-hedging in a temperate frog, Pseudophryne
australis (Anura: Myobatrachidae). Amphibia-Reptilia
23:433?444.
TOUCHON, J. C., I. GOMEZ-MESTRE, AND K. M. WARKENTIN.
2006. Hatching plasticity in two temperate anurans:
responses to a pathogen and predation cues. Canadian
Journal of Zoology 84:556?563.
TYLER, M. J., AND M. DAVIES. 1979. Foam nest construc-
tion by Australian leptodactylid frogs (Amphibia, Anura,
Leptodactylidae). Journal of Herpetology 13:509?510.
URCH, U. A., AND J. L. HEDRICK. 1981. The hatching
enzyme from Xenopus laevis: limited proteolysis of the
fertilization membrane. Journal of Supramolecular
Structure and Cellular Biochemistry 15:111?117.
VOLPE, E. P., AND J. L. DOBIE. 1959. The larva of the oak
toad, Bufo quercicus Holbrook. Tulane Studies in
Zoology 7:145?152.
WAGER, V. A. 1965. Frogs of South Africa. Their fascinating
life stories. Delta Books, Craighall, South Africa.
WARD, D., AND O. J. SEXTON. 1981. Anti-predator role of
salamander egg membranes. Copeia 1981:724?726.
WAKE, M. H., AND R. DICKIE. 1998. Oviduct structure and
function and reproductive modes in amphibians.
Journal of Experimental Zoology 282:477?506.
WARKENTIN, K. M. 1995. Adaptive plasticity in hatching age:
a response to predation risk trade-offs. Proceedings of the
National Academy of Science, U.S.A. 92:3507?3510.
WEBB, R. G. 1971. Egg deposition of the Mexican Smilisca,
Smilisca baudinii. Journal of Herpetology 5:185?187.
WILLIAMS, C. R., AND M. J. TYLER. 1994. Spawn deposition
behavior in Australian frogs (Limnodynastes tasmanien-
sis Gu?nther) that fail to produce foam nests. Herpeto-
logical Natural History 2:111?113.
WITZMANN, F., AND H.-U. PFRETZSCHNER. 2003. Larval
ontogeny of Micromelerpeton credneri (Temnospon-
dyli, Dissorophoidea). Journal of Vertebrate Paleontol-
ogy 23:750?768.
WOLF, A. J. 1996. Systematics of the Rana catesbeiana
species group and the phylogenetic informativeness of
anuran vocalizations. Ph.D. Dissertation, University of
Michigan, Ann Arbor, Michigan, U.S.A.
WOODS, H. A. 1999. Egg-mass size and cell size: effects of
temperature on oxygen distribution. American Zoolo-
gist 39:244?252.
WRIGHT, A. H. 1914. North American Anura. Life-
histories of the Anura of Ithaca, New York. Carnegie
Institution of Washington (197):i?vii + 98 p.
WRIGHT, A. H., AND A. A. WRIGHT. 1924. A key to the eggs
of the Salientia east of the Mississippi River. The
American Naturalist 58:375?381.
WRIGHT, A. H., AND A. A. WRIGHT. 1949. Handbook of
frogs and toads of the United States and Canada.
Comstock Publishing Company, Ithaca, New York,
U.S.A. [Reprinted 1995, Comstock Classic Handbooks,
Comstock Publishing Associates, Cornell University
Press Associates, Ithaca, New York, U.S.A.]
YUREWICZ, E. C., G. OLIPHANT, AND J. L. HEDRICK. 1975.
The macromolecular composition of Xenopus laevis egg
jelly coat. Biochemistry 14:3101?3107.
32 HERPETOLOGICAL MONOGRAPHS [No. 21