Herpetologists' League

Guilds of Anuran Larvae: Relationships among Developmental Modes, Morphologies, and

Habitats
Author(s): Ronald Altig and Gail F. Johnston
Reviewed work(s):
Source: Herpetological Monographs, Vol. 3 (1989), pp. 81-109
Published by: Herpetologists' League
Stable URL: http://www.jstor.org/stable/1466987 .
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HerpetologicalMonographs,3, 1989, 81-109
? 1989 by The Herpetologists'League, Inc.

GUILDS OF ANURAN LARVAE: RELATIONSHIPS

AMONG DEVELOPMENTAL MODES,
MORPHOLOGIES, AND HABITATS
RONALD ALTIG AND GAIL F. JOHNSTON1
Department of Biological Sciences, Mississippi State University,
Drawer GY, Mississippi State, MS 39762, USA

ABSTRACT: Anurans show a distinct dichotomy among the sources of energy used during larval
growth and development, endotrophy and exotrophy. This distinction allows more exact definitions
of direct development, ovoviviparity, viviparity, and related terms. Endotrophic larvae, whether
as a non-hatched embryo or a free-swimming, non-feeding tadpole, gain immediate developmental
nutrition solely from parental sources, most frequently from the yolk allotted to each egg during
vitellogenesis. Exotrophic larvae are always free-swimming, feeding tadpoles and orally consume
numerous sources of energy not derived from a parent.
The morphology of exotrophic tadpoles is surveyed with an emphasis on oral structures. Spec-
ulative scenarios and hypotheses concerning the functions of the various morphologies and the
relationship of trophic structures to the ecology of the tadpoles are offered.
Larval morphology and behavior permit the recognition of six developmental guilds of endo-
trophic larvae and 18 ecomorphological guilds of exotrophic larvae; these guilds are fully charac-
terized.

Key words: Salientia; Tadpoles; Energetics; Development; Morphology; Ecology; Guilds

"Larval adaptive radiation and convergent ad- vergent evolution of large-mouthedstream

aptation have produced an abundance of mod-
ifications for pond life, stream life, arboreal life,
terrestrial life (direct development), for surface
feeding, and for predatory habits, and other
specializations of less obvious ecological signif-
icance" [G. L. Orton, 1957].
ORTON(1953) recognized four morpho-
logical types of tadpoles based largely on
spiracularand external oral morphologies.
Starrett(1973) provided names for Orton's
types and added a diversity of morpho-
logical information to the framework of
the four basic types. Orton's types, Star-
rett's names and the included families are
as follows: Type I (xenoanura),pipids and
rhinophrynids;Type II (scoptanura), mi-
crohylids; Type III (lemnanura), asca-
phids and discoglossids; and Type IV
(acosmanura), all other families. In ad-
dition, Orton (1953) illustrated major
adaptive groups of tadpoles; six types
(i.e., arboreal, surface-feeding, direct
development, mountain stream, nektonic,
and carnivorous) were "derived" from a
generalized pond form. Examples of con-
PRESENT ADDRESS: Department of Biology, Den-
ison University, Granville, OH 43023, USA.
81
tadpoles and tadpoles with upturned
mouths each from several families were
illustrated. Informal concepts of ecomor-
phological kinds of tadpole morphologies
have arisen from these categorizations.
Heyer et al. (1990), Liu (1940), and van
Dijk (1972) applied these ideas to the tad-
poles of specific geographic regions, and
Inger (1986) recognized five feeding types
among Bornean tadpoles that correspond
reasonably well with ecomorphological
types. A scheme that includes all known
tadpole diversity and provides more exact
boundaries and definitions of the various
groups has not been attempted. With de-
scriptive data now available on the tad-
poles of almost 1000 species (update of
Altig and Johnston, 1986), the diversity of
tadpoles seems reasonablywell known, al-
though new morphologies continue to ap-
pear (e.g., Dubois, 1986). A classification
of all known tadpole types would 1) pro-
vide a better understanding of the taxo-
nomic and ecological diversity of tadpoles
with more precise conceptual images of
types or adaptive peaks, i.e., guilds and 2)
identify pertinent areas for further study.
As recognized by Orton (1957), any clas-
82
82 HERPETOLOGICAL
HERPETOLOGICAL MONOGRAPHS
MONOGRAPHS
sification of ecomorphological kinds of
tadpoles must reflect the fact that the
scheme is actually a continuum.
The paper is divided into three sections.
The first part addresses the interactions
among developmental energy and devel-
opmental pattern. Secondly, in support of
the second comment above, we survey
morphological diversity of oral and body
configurationsand propose many hypoth-
eses and speculative scenariosto stimulate
investigations of the interactions between
functional morphology and ecology. A dis-
cussion of the interaction of oral structures
and tadpole ecology follows. Lastly, six de-
velopmental guilds of endotrophic larvae
and 18 ecomorphological guilds of exo-
trophic larvae are described. Tadpole ter-
minology of Altig (1970) and staging by
Gosner (1960) are followed throughout.
DEVELOPMENTAL ENERGY,
PATTERNS, AND SITES
Classically stated, anuran breeding bi-
ology includes an aquatic, non-reproduc-
tive, energy-gathering larval stage that
eventually metamorphosesinto a frog. En-
ergy for early development is derived from
enzymatic degradationof yolk supplied by
the mother. Developmental regimens
through hatching are surprisingly conser-
vative among species. After yolk exhaus-
tion, the free-swimming, feeding tadpole
orally consumes numerous other kinds of
nutrientsthat usually are not derived from
a parent. Conversely, developmental pat-
terns and breeding biologies of many taxa
diverge from this standard in numerous
ways. For example, feeding may not oc-
cur, even when a tadpole morphotype ex-
ists.
We suggest that the source of develop-
mental energy is the ultimate discrimi-
natorbetween the typical patternand those
that diverge from it, regardlessof all other
developmental or biological (e.g., female
size, breeding mode, clutch size, etc.) fac-
tors of anuran breeding. Developmental
patternsthat diverge from the norm imply
some degree of escape from 1) the reliance
on free water and 2) a feeding tadpole as
dictated by the standard breeding mode.
To accomplish such a shift, an alteration
[No.
[No. 3
in the available developmental energy
supplied by the mother must exist (Elin-
son, 1987; Raff, 1987), because oral con-
sumption of nutrients is usually omitted.
By recognizing a dichotomy rooted at the
point of divergence of the two types of
embryonic energy sources, 1) develop-
mental patterns are partitioned into two
groups and 2) developmental modes not
involving a feeding tadpole become more
precisely defined. The following terms ap-
ply equally well to all orders of amphib-
ians.
Endotrophic larvae, regardless of any
other factor(s)of the reproductive process,
obtain immediate developmental nu-
trients only from parentally derived
sources. The first grade includes the vast
majority of species in which only yolk al-
lotted to a given egg during vitellogenesis
is available. The second grade includes a
few cases in which vitellogenic yolk from
the mother is eventually supplemented by
non-yolk, oviducal (e.g., some Nectophry-
noides) or pseudo-oviducal (e.g., paternal
vocal sac secretions from male Rhinoder-
ma) materialsfor oral consumptionwithin
the parent's body. Embryological devel-
opment ranging from entirely typical to
highly modified results in a free-swim-
ming, non-feeding tadpole of various sorts
or an embryonic froglet. Regardless, all
endotrophic juveniles first enter the tro-
phic environment outside the parent as
miniature replicas of their parents. Con-
cepts of oviparity, ovoviviparity, and vi-
viparity do not change, and this develop-
mental-energetic categorization does not
imply that all developmental patterns di-
vergent from normal development are
monophyletic.
Alternately, for some variable period
during development, exotrophic larvae
orally consume a number of kinds of nu-
trients that are rarely derived from a par-
ent. A feeding-tadpole morphotype always
occurs. A few cases that appear as excep-
tions are classified as exotrophic, because
even if parental yolk is involved, it is ex-
traneous to the vitellogenic yolk allotted
for the initial development of a given em-
bryo and never while the embryo or tad-
pole is intimately associated with a par-
1989]
1989] HERPETOLOGICAL MONOGRAPHS
ent's body. For example, some dendrobatid
females purposelysupply unfertilized eggs
to a specific tadpole (Weygoldt, 1980).
Cannibalism of siblings or eating of non-
sibling but homospecific or heterospecific
eggs or embryos is common in arboreal
tadpoles (Lannoo et al., 1987). Tadpoles of
Bufo periglenes (Crump, 1989) and prob-
ably Bufo haematiticus (R. W. Mc-
Diarmid, personal communication) devel-
op in a typical manner from large eggs for
Bufo and facultatively alternate between
endotrophy and exotrophy depending on
the availability of food.
The physical environments of endo-
trophic larvae are varied, although consid-
erably less so than those of exotrophs.Mor-
phologicalvariationof the few endotrophic
tadpoles is low relative to exotrophic tad-
poles. Details of embryology are poorly
known for most endotrophs(see Townsend
and Stewart, 1985, for an exception), and
the development of hemiphractine hylids
is unique. Developmental patterns may be
similar among certain of the highly mod-
ified endotrophic groups. Six develop-
mental guilds of endotrophs (Appendix)
are based on the site of development, sex
of the associated parent when pertinent,
type of association with a parent, degree
of lossof the tadpole morphotype,and post-
hatching activities of early larvae. Eigh-
teen ecomorphological guilds of exotrophs
(Appendix) are based on morphological,
anatomical, and behavioral features that
reflect adaptations to specific but varied
environments.
SURVEY OF TADPOLE MORPHOLOGY
Oral and Buccal Structures
Oral disc orientation.-The orientation
of the oral disc reflects ecological differ-
ences. Qualitative terms (e.g., ventral, an-
teroventral,subterminal,and terminal) are
used commonly to describe the variations.
Figure 1 presents a means of measuring
oral disc orientation. The longitudinal axis
of the tadpole is described as the extended
line connecting the tip of the tail and the
point where the axis of the tail myotomes
contacts the body. Because of morpholog-
ical variations, no other two points de-
83
FIG. 1.-Proposed method to quantify the angular
orientation of the oral disc of anuran tadpoles relative
to a defined longitudinal body axis. Two extremes,
ventral (acute angle A) and upturned (obtuse angle
B) mouths, are shown; angles for other mouths would
fall between these two values. See text for further
explanation.
scribe consistently the body axis, and this
method demands that the entire specimen
be straight. Secondly, the plane of the oral
disc is described by a line connecting the
junction of the base of the lower labium
with the body (or similar point, as in mi-
crohylids)and a similarpoint dorsally.This
line is extended until it contacts the lon-
gitudinal axis, and the angle between de-
scribes mouth position. Species with ex-
tremely ventral mouths may produce an
angle of 0? (lines parallel), those with ter-
minal mouths would be at 90?, and those
with upturned mouths would be greater
than 90?. Pertinent points for this mea-
surement can be quickly located with a
camera lucida without drawing the tad-
pole. When the plane of the mouth is not
easily determined, as with some micro-
hylids and pipids, the orientation of the
oral structuresmay be difficult to evaluate.
Oral disc papillae.-Configurations of
marginal papillae are commonly used in
the identification of tadpoles and strongly
influenced our designation of guilds, par-
ticularly of stream tadpoles. Distributions
of marginal oral disc papillae fall into five
groups:absent, dorsal gap only (taxonom-
ically and ecologically common), dorsal
and ventral gaps (predominate in bufo-
nids, few ranids, rhacophorids, and hy-
lids), ventral gap only (uncommon), and
no gaps (= complete). At least some species
of Cardioglossa have papillae around the
entire "lower labium" so that some pa-
pillae stand in front of the recessed jaw
sheaths. Within the above groups, there
are large variationsin the number, shape,
and size of papillae. Most categories are
scattered throughout a diverse taxonomic
and ecological range of tadpoles, whereas
84
84 HERPETOLOGICALMONOGRAPHS
E an object in flowing water. We suggest that
D ,,
C
B 0 I
x
a.
B
I A
o
FASTER CURRENT ? with numerous formulae larger than 2/3
FIG. 2.-Diagrammatic relationship between tad-
pole oral complexity and occupation of water of in-
creasing velocity: (A) lotic-benthic among others, la-
bial tooth row formula (LTRF) 2/3, few, large
marginal papillae with anterior gap; (B) clasping,
marginal papillae largely unchanged, LTRF > 2/3;
(C) adherent, many small, closely spaced marginal
papillae complete around oral disc, LTRF usually
2/3; (D) suctorial, marginal papillae as in (C), LTRF
> 2/3-17/21; (E) gastromyzophorous, mouth parts
as in (C) or (D) and belly modified as a sucker, sucker
surface papillate and some with rugose keratinized
areas. In (B), (C), and (D), the shown row numbers
are not indicative of specific formulae; see text for
additional discussion.
complete marginal papillae are more lim-
ited: stream inhabitants of several families,
some species with inverted funnel-mouths
(= umbelliform; Fig. 8B), and some species
that are totally or partially carnivorous
(Fig. 8F) that may inhabit tree holes and
other small bodies of water. Those with
umbelliform mouths that feed at the sur-
face of the water may use the complete,
but sparse, papillary row as a crude filter
for water entering the small pool within
the oral disc.
In those tadpoles that adhere to sub-
strates via their mouths, the particular mi-
crohabitat that the tadpoles occupy ob-
viously reflects the degree to which a
particular disc configuration affords adhe-
sion. In species with incomplete marginal
papillae (Fig. 8A), the upper labium is ab-
sent for the width of the papillary gap, so
that complete marginal papillae also de-
mands a complete upper labium. Small,
closely packed papillae may allow better
adhesion to the irregularities of substrates
and perhaps lie within the thin layer of
still water (boundary layer) surrounding
[No.
[No. 3
the following series of morphological
changes allows a progressive occupation of
faster water: relatively few marginal pa-
pillae with an anterior gap and a labial
tooth row formula (LTRF) of 2/3 - pa-
pillae similar with increased number of
tooth rows in various formulae -, many
small marginal papillae in a complete se-
ries and often in multiple rows with a
LTRF of about 2/3 - papillae similar and
up to at least 17/21 -- papillae as before,
LTRF 2/3 or greater, and belly modified
into a sucker (= gastromyzophorous). This
scheme does not imply that the changes
occurred in a linear fashion as shown in
Fig. 2.
Without knowing more about the func-
tions of the papillae (e.g., chemosensory,
tactile, flow and water content monitors,
modification of mouth shape during feed-
ing, substrate manipulation), comments
concerning the functional differences of
lesser patterns of variation [number/dis-
tance, size (extremely long posterior pa-
pillae in some Hemisus and Phrynobatra-
chus), and shape] cannot be made. Van
Dijk (1981) believed that the ventral gap
common in bufonid tadpoles acted as a
"wier-like flow controlling structure," and
Gradwell (1975a) believed that these gaps
gave needed flexibility to the disc for feed-
ing and attaching to irregular objects.
Configurations of submarginal papillae
seem less correlated with habitats. Large
numbers of small, closely spaced papillae
occur in lentic-nektonic forms (some North
American Hyla) and many rheophilous
forms. Lotic forms other than clasping
types often have submarginal papillae in
a row(s) distal to A-1 (cannot occur in
species without complete marginal pa-
pillae) and below the last posterior row
(particularly hylids). Bufonid and ranid
tadpoles have few submarginal papillae re-
gardless of habitat.
Labial teeth.-Other than characteriza-
tion (e.g., Altig, 1973; Altig and Pace, 1974;
Faier, 1972; Gosner, 1959; Heron-Royer
and van Bambeke, 1889; Nicholls, 1937)
and explanations of formation (Deunff and
Beaumont, 1959; Luckenbill, 1964; Tachi-
1989] HERPETOLOGICALMONOGRAPHS
bana, 1978), little can be said concerning
the diversityof tooth forms. Mertens(1960)
and Nachtigall (1974) discuss morpholo-
gies of tadpole mouths and other structures
that serve analogous functions. Our un-
published data and those of Faier (1972),
Gosner(1959), and othersreveal only weak
ecological or taxonomic correlations.
Functional differences are largely un-
known. Suggested functions of labial teeth
include rasping material from a substrate
(Savage, 1952), cellular piercing (Savage,
1952), holding food (Luckenbill, 1965),
trapping food (Tyler, 1963), and substrate
attachment (Altig and Brodie, 1972; Grad-
well, 1975a). Acting as a broom or current
generator to sweep material toward the
mouth, breaking up mucilagenous layers,
sieving particles, and combing strandsinto
alignment for easier cutting could be
added. Even so, these functions would not
appear to require the large diversity of
shapes, sizes, and cusping patternsthat ex-
ist.
Cusps commonly occur on the terminal
and lateral surfaces of tooth heads where
they act only when a tooth is inserted into
a substrate or the row folds backwards.
Assuming the points of the cusps are the
primary working surfaces, the points of
some medially flexed cusps would seem
never to contact the surface (e.g., Heleo-
phryne). There are interspecific and row
differences in the degree of interdigitation
of replacement teeth (Fig. 3C), although
the degree of interdigitation and the num-
ber of replacement teeth (usually 2-3)
seemingly show no ecological or taxonom-
ic correlations. Lotic tadpoles commonly
have smaller teeth arranged more densely
than lentic forms, although it is not clear
which part(s) of the tooth are reduced
(Gosner,1959). These differences likely re-
flect physical characteristics of the foods
eaten and the substratesto which the tad-
poles attach. Intraspecific row differences
in tooth density are most commonly less
than 10 teeth/mm. A Litoria or Nycti-
mystes from New Guinea with tooth den-
sities of 88, 33, 56, 85, and 140 teeth/mm
in rows A-1 through P-3 is exceptional.
Tooth density in the distal posterior rows
of Ascaphus tadpoles is much higher than
85
other rows and the teeth are much smaller
and probably a different form. Different
lengths of adjacent teeth (e.g., Bragg and
Hayes, 1963) are probable misinterpreta-
tions of where transparentsoft tissue of the
tooth ridge stops. Retention of a tooth seat-
ed upon the presently erupting tooth caus-
es some teeth to appear longer than others.
Retention of just the basal sheath of an old
tooth on a newly erupted tooth sometimes
presents an unexpected shape. We know
of no case where adjacent teeth are grossly
different in size, although size and cusp
complexity generally reduce gradually as
one moves laterally within a row.
Two cases will illustratemany pertinent
traits. Amolops larutensis (ranid) has a
suctorial,gastromyzophoroustadpole with
complete marginal papillae. The tadpoles
attach to rocks in fast flowing, often tur-
bulent, water. The head of a tooth from
the medial part of A-1 (stage 25; 10 mm
TL) is ca. 8.4 Am wide with ca. 1.1 ,/m
between teeth; about 96% of the row is
teeth and 4% is space. With 16 cusps per
tooth and 115 teeth/mm, over 1800 work-
ing points/mm occur. If all cusps of all
rows are implanted, the large surface sure-
ly provides an efficient tool for food re-
moval and a strong anchor for position
maintenance. In suctorial species, the oral
disc obviously cannot flex during jaw op-
erations, so the teeth cannot rasp in the
same manner as non-suctorial tadpoles;
much of the substrateremoval may be via
the serrationson the jaw sheaths.
The lentic-nektonic, "rasping"tadpole
of Rana heckscheri illustratesthe opposite
extreme. Teeth are spikes so that width
depends on where the tooth is measured,
intertoothdistance is 1.5,m, tooth density
39/mm, number of working surfaces/mm
is 39 (no cusps), 29% of the row is teeth
and 71%is space. Drawing an analogyfrom
mechanical abrasives, tools for working
hard materials have many small, closely
spaced surfaces, pressure applied to the
tool is high, and the removal per stroke is
small (metal file analog). Tips of non-
cusped teeth (few points/distance) of sim-
ilar dimensions to cusps of cusped teeth
(more points/distance) may perform quite
different functions. Conversely, tools for
86 HERPETOLOGICALMONOGRAPHS
workingsoft materialshave relatively few,
larger, widely spaced surfaces, work with
less pressure, and remove more material
per stroke (wood rasp analog). Tool sta-
bility, angle of attack, stroke rate, and the
ability of the abrasive to remain clean re-
late to shape, size, and longevity of the
working surface. Wear and turnover rates
of labial teeth are not known (see Kuang
and Kollros,1976 for data on jaw sheaths).
We have observed wear only in darkly
pigmented teeth. Because darkly pig-
mented structures are typically stronger
than lightly pigmented ones, we suggest
that darkly pigmented teeth are retained
longer and thus exhibit wear, whereas
lightly pigmented teeth are simply re-
placed.
In summary,one could predict that tad-
poles of R. heckscheri forage on thicker,
less dense substratesand remove a larger
amount per feeding stroke than tadpoles
of Amolops. Large numbers of small,
closely spaced, cusped teeth apparently
supply a useful tool for harvesting thin,
perhaps tough layers of organics attached
to rocks in fast flowing water. Thicker
growths of less tensile strength common to
lentic periphyton suggest different har-
vesting mechanics. A Rana-type of tooth
arrangement may either "pick" diatoms
or "comb" fibrillar periphyton into par-
allel arrays for easier cutting by the jaw
sheaths.
Labialtooth shape surelyaffectsthe style
and length of substrate contact and the
pressureneeded to keep the tooth implant-
ed or in properalignment. It would appear
that strongly curved teeth (e.g., Fig. 3B;
Bufo in Altig, 1973) contact the substrate
for a short distance before labial disc flex-
ure rotatesthe cusps off the substrate.Such
teeth may be used primarilyto pry objects,
such as diatom frustules, off a substrate.
Adhesion of diatoms may equal 2.9-4800
(x = 634; n = 8 species) nanoNewtons
(Harper, 1977);Drum and Hopkins (1966)
found it difficult to pipette diatoms be-
cause they adhered firmly to glass. With-
out knowing the mechanics of the entire
feeding mechanism (Gradwell,1968,1970,
1971, 1973, 1975b; Gradwell and Pasztor,
1968) of a tadpole, we cannot judge wheth-
[No. 3
[No.
er such adhesive abilities pose a removal
problem for tadpoles, but the thinness of
the cells or cell layers provides some pro-
tection from ranid tadpoles with relatively
straight, non-cusped teeth (Fig. 3A; Dick-
man, 1968).
Labial teeth may break up the relatively
strong sheets of diatom mucilage at the
soil-water interface (Holland et al., 1974).
The flocculent nature of bottom debris in
temporaryponds is partiallycaused by this
mucilage layer being disrupted by such
organisms as tadpoles. Tadpoles of Bufo
and Scaphiopus that appear to be filled
only with soil are likely feeding on this
soil-mucilage-diatom mixture plus parti-
cle attached bacteria (Bowen, 1980; Test
and McCann, 1976).
Labial tooth rows and tooth ridges.-
The number and arrangement of tooth
rows are common traits used in identifi-
cation; intraspecificvariation in row num-
ber is known (e.g., Bragg and Bragg, 1959;
Hampton and Volpe, 1963; Potthoff and
Lynch, 1986) but is relatively uncommon
in most taxa. Inter-row spacing and tooth
ridge topography seemingly reflect eco-
logical specializations. Inter-row spacing
and tooth size are reduced distally on at
least the lower labium in species with large
numbers of tooth rows. This reduces the
potential of the oral disc becoming im-
mense and provides an increase in contacts
per area as distance from the mouth in-
creases. The musculature of oral discs is
probablynot well developed distally to the
mouth in most species. Tooth ridges with
biserial tooth rows (e.g., ascaphids, disco-
glossids) may represent an alternate solu-
tion to increasingthe total number of tooth
rows.Tadpolesof Bombina orientalis have
all rows presentand uniserialat about stage
26, so the anlagenof the second serieseither
are not presently differentiated or tooth
production in the second series is delayed.
It is not known if the production of two
tooth rows/tooth ridge represents fusion
of tooth ridges, fission of developmental
anlage, or the production of two cell lines
from one mitotic zone. Transitory ap-
pearance of tooth ridges indicative of the
second series in each row in Bombina does
not occur. We have seen a few specimens
 1989] HERPETOLOGICAL MONOGRAPHS 87

I
V,
A

406
. A- .
.

FIG. 3.-Scanning electron micrographs of labial teeth and an example of a feeding mark: (A) short-cusped,
relatively straight tooth of Megaelosia goeldi, x440; (B) strongly curved, long-cusped teeth in single row/
tooth ridge of Hyla biobeba, x710; (C) emergent tooth (upper left) and replacement teeth in Leptodactylus
chaguensis, x550; (D) lateral view of non-cusped, short-sheathed tooth of Scaphiopus bombifrons, tooth
head broadly spatulate in face view, x1720; (E) negative cast of two feeding marks made by a tadpole of
Rana utricularia in an agar-based food penetrated by the jaw sheaths (upper jaw sheath entered rather
shallowly at left, lower jaw sheath entered steeply at right; lower sheath skipped once before actual entry
on left mark); (F) cusped teeth in two rows/tooth ridge in Bombina orientalis, x510.
88 HERPETOLOGICAL MONOGRAPHS
FIG. 4.-Schematic longitudinal section of the low-
er labia of (A) lotic-suctorial and (B) lentic-nektonic
tadpoles showing the topography and shapes of tooth
ridges and associated structures.
of ranid and rhacophorid tadpoles nor-
mally with uniserial tooth rows that have
biserial tooth rows. Thibaudeau and Altig
(1988) showed a close spatial-temporal de-
velopmental relationshipbetween rows A-
1 and P-2, and tooth row use indicates
these two rows are likely of prime impor-
tance in some lentic species (G. F. John-
ston, unpublished data). Accessory tooth
rowsof some ranids(e.g., Webb and Korky,
1977) and pelobatids are not parallel with
the main tooth rows and are situated lat-
eral to the jaw sheaths. Their functions
appear unassociatedwith the suspected di-
rection of action of either labium.
Lentic tadpoles have high, distally
rounded tooth ridges that often are widest
near the apex and separatedby wide, deep
inter-row valleys situated about equidis-
tant between rows (Fig. 4B; Noble, 1931).
Such arrangementsafford high flexibility,
small forces against a substrate, and little
retardationof the entire row folding back-
wards during use. If rasping is the ex-
pected action, efficiency of removal would
seem to be low. Teeth are inflexible but
rows are flexible. Lotic forms show pro-
[No. 33
[No.
gressive changes with occupation of faster
water. Tooth ridges become broad-based
pyramids with flattened apices as viewed
in cross-section.Inter-row valleys are shal-
low, slit-like, and immediately posteriorto
the preceding row so that the plane of the
oral disc appearsalmost uniform (Fig. 4B).
Extended front bases of the teeth (e.g.,
Ascaphus, Altig and Pace, 1974) extend
into the inter-row tissue to form strong
attachmentsfor both teeth and rows. Rows
have little flexibility and cannot fall back-
wards. These arrangements aid active
gripping by the upper and lower rows that
face and act in opposite directions.
Shapes of tooth rows suggest potential
actions and functions. Rows are typically
arched away from the mouth, with lower
rowscommonly straighterthan upper rows.
This shape remains during use (Johnston,
1982). Regardlessof the arch of a row, each
tooth is set parallel with the longitudinal
axis of the tadpole. Without this configu-
ration,either the row would have to change
orientation during a strike or only medial
teeth would face the substrate squarely.
Because the row is arched, at least the lat-
eral sections skid even though each tooth
does not. This action should provide ad-
ditional abrasion and plow material to-
ward the mouth.
Lastly, tooth row lengths relative to oral
disc dimensions and the positions of rows
on the disc are considered. Suctorial tad-
poles use their mouths for position main-
tenance, and long rows, particularly ad-
jacent to the edges of the oral disc, would
seem important. This is typical, however
Hyla uranochroa (Fig. 8H), H. rufioculis,
and part of the genus Ptychohyla (Fig. 261
in Duellman, 1970) have all short rows
situated adjacent to the jaw sheaths. Large
lateral and posteriorzones lack teeth. The
large oraldisc with weakly developed tooth
rows and jaw sheaths of at least some tad-
poles of Taudactylus (Watsonand Martin,
1973) is similar. Oral discs of lotic species
are less resilient than those of lentic forms,
but how are these toothless areas held
againstthe substrate?We suspectthat these
forms inhabit a zone different from those
species that have rows nearly equal to the
oral disc width and closer to the edges. As
199
1989] MONOGRAPHS
HERPETOLOGICALMONOGRAPHS
HERPETOLOGICAL
expected,lowertoothrowsof lotic species
are typically long, whereas lentic forms
may have a distalmostrow as shortas 5%
of the lengthof the proximalmost
posterior
row.
Tooth row formula diversity and row
homology.-We categorizetoothrowfor-
mulaeas balanced(equalnumberof rows
on upperand lowerlabia),negativelyim-
balanced(morerowson lowerlabium),or
positivelyimbalanced(morerows on up-
per labium).A tabulationis alwayspoten-
tially biasedby the speciesincluded,but
of 627 speciesexcludingspecieswith 0/0
(Table 1), imbalancedmaximawere +7
and -11, and 88% of the species were
between+2 and -2. Untilmoreis known
aboutthefunctionalaspectsof varioustooth
row formulae,the significanceof this ba-
sicallyunimodaldistributioncannotbe ad-
dressed, but interestingquestions arise.
What are the functionaldifferencesbe-
tween negatively (4/15) and positively
(10/3) imbalancedformulae?Whatis the
significanceof the sequencesbetween -2
and +4 wherethe mostcommonformulae
areusuallyformedby increasingthe upper
labialrowsby 1 while keepingthe lower
labiumat 3 (i.e., 1/3 through7/3). Does
the relative rarity of highly imbalanced
formulaeimply specificfunctionsor mi-
crohabitats?What is the relationshipbe-
tweenthe sametotalrownumberandbal-
ancevalue(e.g.,9/9 vs.4/14)?Theformula
2/3 at BV -1 occursin taxa from many
habitatsand in 51%of the taxa sampled.
Total rows ranged from 1-38 in 49 row
configurationswithout considering row
gaps, and at least 124 formulaeoccur if
rowgapsareincluded(AltigandJohnston,
1986).
The sequenceof tooth row appearance
is known within a narrowrange of taxa,
guilds,and tooth row formulae,and pat-
ternsof metamorphicatrophyarelesswell
understood.Evenso, thesedatalikelypro-
vide the best evaluationsof toothrow ho-
mology,i.e., which rows in a formulaof
17/21 equalthe rowsin a formulaof 2/3.
The ontogeneticsequenceof row appear-
ance for Bufo valliceps (Limbaughand
Volpe, 1957), Rana pipiens (Nicholls,
1937), Bufo arenarum (de Lopez and
89
89
Echeverria, 1984), and Hyla chrysoscelis
and Rana utricularia (Thibaudeauand Al-
tig, 1988) [all pond forms with 2/3 rows]
appears to be A-i, P-2, P-l, A-2, P-3
(sequentialformulae = 1/0, 1/1, 1/2, 2/2,
2/3). The timing and developmental to-
pography of A-1 and P-2 are closely
linked, and these rows may appear simul-
taneously or slightly reversed in time. Lit-
erature data on partial developmental se-
ries suggest that this pattern is common in
species with 2/3 rows and for the appear-
ance of the first five rows in species with
more than five rows. These five rows in a
2/3 configuration appearing in the above
order are designated the prime rows or
formula. Adding subsequent rows alter-
nately on each labium seems to be a com-
mon occurrence, but discordance of stage
and tooth row appearance, especially in
species with formulae much larger than
2/3, is common. Species with many tooth
rows do not attain the eventual comple-
ment of rows until later in ontogeny and
retain teeth into later stages at metamor-
phosis compared to species with 2/3 rows,
and this phenomenon is accentuated in
stream forms that use their mouths for po-
sition maintenance.
Evaluation of whether ontogenetic gain
mimics phylogenetic additions of rows is
difficult, because 1) the ontogeny and de-
velopmental controls of median row gaps
are not understood (e.g., Dutta and Mo-
hanty-Hejmadi, 1984; Michalowski, 1966)
and 2) data are available for so few species
with more than 2/3 rows. We hypothesize
that there are four basic patterns (Fig. 5)
of tooth row additions to the prime for-
mula. Less common patterns of row ad-
ditions (or losses) involve combinations or
parts (one labium) of these patterns. Two
contrasting examples will illustrate.
Ranids and pelobatids include many
stream forms with many tooth rows and
incomplete marginal papillae. We suggest
that these tadpoles do not use the mouth
extensivelyfor attachmentto substratesand
have more jaw mobility, larger gapes, and
different actions for substrate removal
compared with suctorial forms. Gaps in
rows are progressively wider towards the
large,stronglyarchedjaw sheaths,and rows
90 HERPETOLOGICAL
HERPETOLOGICALMONOGRAPHS
MONOGRAPHS [No.
[No. 33

TABLE 1.-Number of species (n = 627) that occurs at each labial tooth row formula (LTRF) and balance
value (BV); see text for further discussion.

Number of species
BV LTRF 0 10 20 30 320

Negative imbalance
-11 4/15 XX
-10 4/14 X
-6 3/9 X
-5 8/13 X
-4 3/7 XX
-4 7/11 X
-3 1/4 X
-3 2/5 XXXXXXXXX
-3 4/7 XX
-3 6/9 XXX
-3 8/10 X
-3 17/21 X
-2 1/3 XXXXXXXXXXXXXXXXXXXXXXXXXXXXX
-2 2/4 XXXXXXXXXXXXX
-2 3/5 XXXXX
-2 4/6 XXX
-2 7/9 X
-2 8/10 X
-1 0/1 XXXXXXXXX
-1 1/2 XXXXXXXXXXXXXXXXXXXXXXXX
-1 2/3 XXXXXXXXXXXXXXXXXXXXXXXXXXXXXXXXXXXXXX XXXXXXXX
-1 3/4 XXXXX
-1 4/5 XXXXXX
-1 5/6 X
-1 6/7 XXX
-1 7/8 XX
Balance
0 1/1 XXXXXX
0 2/2 XXXXXXXXXXXXXXXXXXXXXXXXXX
0 3/3 XXXXXXXXXXXXXXXXXXXXXXXXX
0 4/4 XXXXXXXXXXX
0 5/5 XXXXXX
0 6/6 XXXXXXX
0 7/7 XXX
0 8/8 X
0 9/9 X
Positive imbalance
+1 1/0 XXX
+1 2/1 X
+1 3/2 X
+1 4/3 XXXXXXXXXXXXXXXXXXXXXXXXXXXXXX
+1 5/4 XXXXXXX
+1 7/6 XXXXX
+2 5/3 XXXXXXXXXXXXXXXXXXXXXX
+2 6/4 XXXX
+3 6/3 XXXXXXXXXXXXX
+3 7/4 X
+3 9/6 X
+4 7/3 XXXXX
+5 8/3 X
+7 10/3 X
1989]
1989] HERPETOLOGICAL MONOGRAPHS
appear to be added proximally on both
labia after the formula of 2/3 is attained
as above. Therefore, the upper prime rows
retain early ontogenetic designations,
whereas lower prime rows become at least
numerically more distal (Type E, Fig. 5).
Conversely, in stream-dwelling sucto-
rial forms (e.g., Ascaphus, many Hyla, He-
leophryne), only the row adjacent to each
jaw sheath is commonly broken. Rows ap-
pear to be added distally on both labia
(Type C, Fig. 5) so that A-1 (= A-i') of
a young tadpole becomes A-5 of a species
with six eventual upper rows, whereas P-
1', 2', and 3' retain original designations.
In species that add rows distally on the
lower labium and proximally on the upper
labium, prime rows would retain original
designationsregardlessof the eventual for-
mula (Type B, Fig. 5). Such variations in
the patternsof row additions preclude any
numbering system that will preserve the
same designation for homologous rows of
all formulae throughout ontogeny.
Metamorphicoral atrophy appearshap-
hazardous,but the general pattern follows
the reverse of ontogenetic gain (Takahama
et al., 1988; Thibaudeau and Altig, 1988).
P-3 appears last and is lost first in meta-
morphic B. valliceps (Limbaugh and
Volpe, 1957). Hillis and de Sa (1988) sug-
gested that the presence of three lower
tooth rows in Rana sierramadrensis was a
reversal from the typical four rows in the
R. palmipes group; since P-1 is broken as
expected, it was presumably P-4 that was
lost. Tadpoles of Hyla crucifer have few
teeth in P-3, and up to 50%of the tadpoles
may normally have a formula of 2/2 (Gos-
ner and Black, 1957); when P-3 is absent,
the tooth ridge of P-3 may or may not be
present, and the ventromedial gap in the
marginal papillae that is normally present
may or may not be present in 2/2 indi-
viduals (personal observation). P-3 is the
first row lost in those that have it. We
suggest that phylogenetic loss of tooth rows
may occur in reverse order of the onto-
genetic gain of the prime formula, that is,
in the order of metamorphic atrophy. If
so, certain formulae should not exist. Of
124 species (from Altig and Johnston,1986)
91
B c
0 % D 0
A
D 0
0 % % 0
FIG. 5.-Schematic tadpole tooth row formulas in-
dicating proposed means of phylogenetic increase and
decrease of tooth rows from the suggested prime for-
mula of 2/3. Heavy lines = prime rows, light lines =
additions, circle = jaw sheaths.
with fewer than 2/3 rows, 88 (71%)species
fit the expected sequence of 2/3, 2/2 (loss
of P-3), 1/2 (loss of A-2), 1/1 (loss of P-
1), and 1/0 (loss of P-2) or, based on the
similar reversal between A-1 and P-2
above, 0/1 (loss of A-i). Formulae such as
0/2 (n = 1), 2/1 (1), and 1/3 (34; mostly
ranids and hyperoliids) indicate alternate
but generally uncommon patterns.
Few data are available on the genetics
of tooth row configurations (Michalowski,
1966), because 1) few studies involve
species with different formulae or config-
urations of the same formula, 2) people
have not collected these data from hybrids
that are available, and 3) few data are
available beyond the ratheruninformative
F1 generation. Hybrids with tooth for-
mulae of 2/4 from crosses of Rana cas-
cadae (3/4) x R. pretiosa (2/3; Haertel
and Storm, 1970) imply different genetic
or developmental controls for the two la-
bia. The observations of Grillitsch and
Grillitsch (1989) concerning more fre-
quent abnormalities in the lower, distal
rows may suggest decreased develop-
mental control distally.
Systematistshave included tadpole data
in their analysesto varying degrees (Gran-
dison, 1981; Griffiths and de Carvalho,
1965; Inger, 1967; Kluge and Farris, 1969;
92 HERPETOLOGICALMONOGRAPHS
HERPETOLOGICAL MONOGRAPHS
FIG. 6.-Schematic drawings of jaw sheaths. Buc-
cal faces of flattened upper sheaths (stipple = lightly
keratinized; cutting surface downward) of (A) Hyla
femoralis and (B) Rana utricularia showing keratini-
zation patterns presumed to indicate different inter-
actions between upper and lower jaw sheaths; (C)
front surfaces of both broken sheaths composed of
large units in Amolops sp.; (D) front surface of the
upper sheath of Plectrohyla matudai with hypertro-
phied serrations (drawn from Duellman, 1970); (E)
front surfaces of both cuspate sheaths of the carniv-
orous tadpole of Rana tigerina (drawn from Kirti-
singhe, 1957); (F) front surfaces of both sheaths of
Hyla pictipes showing typical cutting surface and
M-shaped accessory working surface on the outer face
of the upper sheath (drawn from Duellman, 1970).
Sokol, 1975). Lynch (1971) regarded a for-
mula of 3/3 or greater (associated with
other traits that form a mosiac of traits
common to stream versus pond tadpoles)
as primitive within leptodactylids. Larger
tooth formulae within the conservative ar-
ray of tooth row formulae in hyperoliids
belonged to the more primitive genera
based primarily on analyses of adult traits
(Drewes, 1984). Non-cusped teeth have
been considered primitive (Noble, 1931)
or derived (Gosner, 1959). Detailed inter-
specific developmental data should allow
judgements of character polarity so that
data on oral structures could be used more
effectively in systematics. Without the on-
togenetic data, one cannot differentiate
between identical formulae derived by dif-
ferent developmental patterns. Accessory
rows in some ranids (Webb and Korky,
1977) and pelobatids, keratinized areas ad-
jacent to the lower jaw sheaths in some
ranids and hyperoliids, and the keratinized
patch in the roof of the buccal cavity in
some Scaphiopus (Spea) also need atten-
tion.
Jaw sheaths.-Jaw sheaths form by fu-
[No.
[No. 33
sion of cellular arrays (Luckenbill, 1964,
1965) that resemble labial teeth, and large
sections of the sheaths are shed similarly
to individual teeth. At metamorphosis, en-
tire sheaths often disengage from the jaw
cartilages as intact units. Jaw serrations are
not cusped. Young tadpoles of Heleo-
phryne (Visser, 1985) and all sizes of Oto-
phryne (Wassersug and Pyburn, 1987) ap-
pear to have hypertrophied jaw serrations
without a common sheath at their bases.
Because jaw serrations usually slant more
posteriorly as one moves laterally along
either sheath, jaw occlusion may provide
a different action laterally than medially.
In most cases, the lower jaw passes inside
the upper, but the jaws are quite mobile
so that the sheaths may sometimes meet
in a chiseling action. Keratinization of the
oral face of the upper sheath (Fig. 6A, B;
Johnston and Altig, 1986) shows various
patterns that may reflect the kind of con-
tact between the two sheaths. Enlarged
serrations, perhaps analogs of mammalian
canines (Fig. 6D), occur on parts of the
upper jaw sheaths of lentic-benthic tad-
poles of Leptopelis and suctorial Plectro-
hyla. Some carnivores have protrusions on
either the upper and/or lower sheaths, and
the upper protrusion is often complemen-
tary to a notch in the lower jaw sheath
without enlargement of serrations (e.g.,
Fig. 6E; Ceratophrys, Scaphiopus).
Serration density, shape, and length plus
a number of sheath dimensions, curva-
tures, and shapes that have not been mea-
sured likely reflect substrate characteristics
that can be manipulated most effectively.
Assuming that jaw mechanics are similar,
tadpoles of Hyla gratiosa, H. regilla, and
Rana utricularia with wide, thick, robust
sheaths with curved front surfaces must be
able to feed on resources unavailable to
species with narrow, thin sheaths with flat-
ter surfaces (e.g., Bufo spp., R. catesbei-
ana). Johnston (1982) showed that tad-
poles of Rana utricularia consistently could
penetrate and remove pieces from an
agar-based food that tadpoles of Bufo
woodhousei of the same size could not pen-
etrate. Several physical and biological fac-
tors (e.g., substrate thickness, consistency,
1989]
19891 H T C
HERPETOLOGICALMONOGRAPHS
conformity, and position; water depth;
suitabilityof food; hunger) likely influence
jaw actions, and lotic species seem to ex-
hibit the most profound morphological
modifications. The analogies between la-
bial teeth and abrasives apply here, and
lotic tadoles can be placed in a continuum
from those with finely spaced, narrow-
based sharp serrationsto those with broad-
ly spaced,wide-basedblunt serrations.Fine
serrationsseem to occur in species where
the oral disc-substrate space may not be
severely restricted. Tadpoles may adjust
the orientation and action of the sheaths
to accommodate one of several actions
when in water with different flow rates.
In extreme suctorial species, the sheaths
may not occlude, as they appear to be ro-
tated to a more "mouth open" position so
that the bluntly serrated edges probably
act in a scouring or scratching motion
nearly perpendicular to the substrate.As-
caphus tadpoles representanother solution
to action in a restricted space; the huge,
flat upper sheath lies almost parallel with
the substrate and acts at an acute angle.
Some suctorial forms have jaw sheaths di-
vided into lateral sections separated by a
medial, non-keratinized area (e.g., some
Amolops, Ansonia, and pelodryadinine
hylids) or sheaths are absent (e.g., most
Heleophryne); the functions of these kinds
of sheaths relative to typical forms are not
known. Broken sheaths are often com-
posed of fewer large cellular columns
(Luckenbill, 1965) where each column ap-
pears to produce a serration [8/mm in
Amolops sp. (Fig. 6C) versus 30-80/mm
in more typical sheaths] with square tips.
Substrate removal during oral hitching
(Altig and Brodie, 1972) or ratcheting
would seem essential in these cases.
Many lotic species have a perpendicular
shelf of variable extent projectingfrom the
medial buccal curvature of the upper
sheath slightly orad of the occlusive sur-
face (Fig. 209 in Duellman, 1970; Hyla
sumichrasti, H. smaragdina). The shelf
presumably acts as an anti-warping strut
to the arch and prevents the lower jaw
from passing far beyond the face of the
upper sheath or prevents the sheath from
93
being implanted too deeply into a sub-
strate. Tadpoles of Hyla tica and H. pic-
tipes (Fig. 6F; Fig. 136 in Duellman, 1970)
appear to have two working surfaces on
the upper sheath. The serrated edge may
be used in slower water when the disc-
substrate space is not severely restricted.
A roughened area on the front surface of
the sheathis probablyused when the sheath
is nearly parallel with the substrateduring
oralhitching in fasterwater when the disc-
substratespace is restricted. M-shaped up-
per sheaths of some lotic forms probably
add strength,retardwarping, and increase
working surface length without increasing
jaw length in species having short gapes.
Within a crowded space, the serrationsof
such a sheath may remain free of debris
more effectively than a straight surface
and plow material toward the mouth.
Correlationsbetween feeding activities,
morphology,and substratesformulated for
larval aquatic insects (e.g., chewer, shred-
der, scraper; Cummins and Klug, 1979)
and snails (Breureand Gittenberger, 1982;
Steneck and Watling, 1982) have never
been recognized for tadpoles. We propose
tentative functional designations for the
actions of jaw sheaths, while suggestions
for the actions of labial tooth rows would
be premature. The unique large upper
sheath of Ascaphus tadpoles surely attacks
at a small angle and thus shaves thin sub-
stratesattached to stones in flowing water.
The sheath moves by protraction-retrac-
tion cycles of the anterior end of the body
(oral hitching of Altig and Brodie, 1972).
The small lower sheath probably has no
feeding function. Many tadpoles remove
filamentousor projectingmaterial (bite) or
extract a portion (gouge, scoop) of periph-
yton from submerged surfaces. Tadpoles
with only jaw sheaths (e.g., Fig. 8E, Hyla
microcephala and leucophyllata groups)
are limited to these types of feeding,
whereas many other tadpoles with labial
teeth may commonly feed in this manner.
In any case, sheaths contact surfaces at
variable but large attack angles and then
rotate towards each other (Fig. 3E). The
sheathsmay not necessarilyocclude (lower
orad of upper); material may be ripped
94 HERPETOLOGICALMONOGRAPHS [No. 33
[No.

from position after only a partial cut by well with macro- and microhabitats, al-
the jaw sheaths. Understanding feeding though hydrodynamic data to verify their
modes between these two extremes must functions are lacking. Although many of
await additional examination of the ac- the generalities formulated for fish loco-
tions of both jaw sheaths and labial teeth. motion apply, body form and lack of lat-
Multiple mastication (chewing) of mo- eral fins on tadpoles must impart specific
lariform surfaces does not apply. Cuspate modifications on their locomotion. Tad-
sheaths of some carnivorous species may poles that live in flowing water may be
allow more efficient cutting of animal tis- strongly depressed (pelodryadininehylids,
sues, and hypertrophied serrations may Heleophryne) or bluntly rounded ante-
pierce or penetrate viscous or dense sub- riorly (Fig. 7M; Ascaphus, many Hyla);
stratesmore effectively than a uniform se- these shapes likely reflect the influences of
ries of serrations. The actions of an in- drag, but analyses are lacking. Other de-
creased number of tooth rows or increased pressed tadpoles include various lentic-
tooth densities in some rows adjacent to benthic (perhaps for shadow reduction)
the jaw sheathsin stream species may sub- forms, burrowers(Fig. 70), lentic-nekton-
stitute for jaw actions (Tyler, 1963). Rheo-ic forms that either remain motionless
philous tadpoles sometimes appear to feed much of the time (microhylids, Xenopus)
repeatedly in the same area rather than or swim most of the time (Rhinophrynus),
moving to a slightly different area at each and variousarborealtypes that live in con-
feeding strokeas is often the case with non-fined spaces. Cylindrical (inactive swim-
suctorialtadpoles.For those with few, blunt mers) and compressedbodies (more active
sheath serrations, such activity would swimmers) are limited to lentic-nektonic
seemingly scour the substrate.Those with forms. Hoff and Wassersug (1985, 1986),
numerous, fine serrations may produce a Nishikawa and Wassersug (1989), Was-
scratching action, especially if they move sersug (in press), and Wassersugand Hoff
between each feeding cycle. (1985) address numerous factors concern-
Buccopharyngeal structures. -The ing tail kinematics and morphology of
feeding mechanism of a tadpole has sev- swimming tadpoles.
eral interacting phases. Materialdislodged Tail fins range from almost absent in
by the mouth parts or suspended in the semiterrestrialforms to immense sizes in
water must be moved into the buccal cav- some lentic-nektonic forms. Stream tad-
ity by the buccal pump. What arrives in poles can be characterized (comparisons
the buccal cavity is selectively captured for lentic tadpoles in parentheses) as fol-
by the gill filters. An array of buccal pa- lows: low, relatively stiff fins roughly par-
pillae (Viertel, 1982; Wassersug, 1980) allel with the tail muscle (higher, more
probably monitors and maneuvers (Inger, flexible fins, often with considerable arch
1986) materialwithin the incoming stream. in silhouette), neither fin extends onto the
Although the filter system is well under- body (dorsal fin commonly does; ventral
stood (Seale, 1982; Seale and Wassersug, fin rarely, e.g., Xenopus, some Rhacopho-
1979; Viertel, 1984a,b, 1985, 1987), the rus, Ololygon, and Phyllomedusa), tail tip
data include too few species to allow rounded (typically pointed, often atten-
uate as a flagellum), and tail muscle mas-
grouping tadpoles by filtering abilities. In-
ger (1986) recognized five feeding types sive in all dimensions (much less massive
among 16 species of Borneantadpoles, and at same or larger total length). Variations
most types could be associated with mor- of fin area/muscle volume, body shape,
phological specializations that were func- and center of gravity probably reflect the
tionally related to the particles ingested. different attitudes in the water (attached
to substratevs. horizontalin water column
Body Forms and Habitats vs. head up or down), swimming styles
Body shapes and eye positions.-Body (positionmaintenance vs. cruise vs. sprint;
and tail shapes and eye positions correlate braking vs. coasting stop; highly maneu-
1989] HERPETOLOGICALMONOGRAPHS
verable vs. not so; fast vs. slow), and swim-
ming mechanics (strokes/time, stroke am-
plitude).
The tail terminus of taxa within several
lentic guilds that inhabit the water column
is attenuated, often non-pigmented, and
may move independently of the remain-
der of the tail. This attenuate portion is
called a flagellum because it is a locomotor
device, a function not necessarily implied
in filament, etc. Fins of tadpoles that have
a flagellum vary from very tall (e.g., some
Hyla, Ololygon, and Rhacophorus) to low
and parallelwith the tail muscle (e.g., Hyla
leucophyllata group) to reduced (e.g.,
Xenopus, some phyllomedusine hylids).
The high, sail-like anteriorpart of the dor-
sal fin followed by a greatly reduced por-
tion in the lentic-benthic tadpoles of Oc-
cidozyga is unique.
Size, position, orientation, lenticular
protrusion,and bulge of the eye above the
surface changes as one moves from lentic-
nektonic (large, bulging, lateral, oriented
perpendicular) through lentic-benthic
(smaller, slightly bulging, dorsolateral to
dorsal, oriented mostly horizontally) to
stream inhabitants (smaller, dorsal, non-
bulging eyes) to lotic burrowers(very small,
non-bulging eyes that are distinctly para-
sagittal).
Spiracles, vent tubes, neuromast topog-
raphy, and nares.-Even though varia-
tions of these structures aid identification
(Altig, 1970; Johnston and Altig, 1986;
Lannoo, 1985), ecological correlationsare
rare. Starrett (1973) correlated spiracle
configurations and modes of feeding and
swimming. She pointed out that dual lat-
eral, single midventral, or parasagittalspi-
raclesoften occur in midwaterforms, many
of which are suspension feeders. Flows
from these types of spiracles may not dis-
rupt the stability of the tadpole as the flow
from a sinistral spiracle may, or at least
not disturbfood items in the water column.
We have observed tadpoles of Gastro-
phryne moving via the midventral spirac-
ular jet as Starrett (1973) speculated. A
suggestion for the function of long spirac-
ular tubes that are free from the body (e.g.,
Amolops, Acris, Cardioglossa) has been
95
made only for the extremely long tube in
Otophryne (Wassersugand Pyburn, 1987).
Johnstonand Altig (1986) recognized a
number of character states for vent con-
figurations other than dextral versus me-
dial, but functional, developmental, or
ecological correlationsare not known. Ob-
servationof neuromast often requires spe-
cific procedures (Lannoo, 1985), and data
on these structuresare uncommonly used
(e.g., Boulenger, 1891; Scott and Jennings,
1985; Shelton, 1970). Many lotic forms in
several families have an enlarged neuro-
mast ventrolaterally on the body just an-
terior to the tail. The morphology of the
external nares varies in a number of ways
(aperturerimmed, variously papillate, tu-
bular; aperture shape; position relative to
the surrounding surface and orientation;
Channing, 1984;Johnstonand Altig, 1986),
but no ecological correlationsare known.
Future Studies
Creative use of myography (e.g., Liem,
1980), high-speed cinematography, high-
speed x-ray cinematography,electrophysi-
ology (e.g., sensory capabilities of oral and
buccal papillae), and physiographicequip-
ment (e.g., Gradwell, 1971) on intact and
manipulated individuals (i.e., selective re-
moval of oral papillae, tooth rows, etc.) will
answer many questions concerning the
functions of various oral structures and
configurations. Many descriptive projects
concerning development (e.g., Thibau-
deau and Altig, 1988), comparative anat-
omy and mechanics of the chondrocra-
nium (e.g., de Jongh, 1968) and oral
apparatus (Johnston, 1982), and creative
analysesof intra- and interspecific oral ap-
paratusvariation (e.g., labial teeth and jaw
sheaths) would be helpful. Mendelian and
developmental/biochemical studies of the
genetics of various structures would be
valuable, especially in the light that none
of the oral disc structureshas adult deriv-
atives. The temporal-spatial distributions
of tadpoles within and among communi-
ties remain poorly known, particularly of
stream forms, and the enormous realm of
feeding ecology, including what the tad-
pole eats and the qualities (e.g., abun-
96 HERPETOLOGICAL
HERPETOLOGICAL MONOGRAPHS
MONOGRAPHS (No.
[No. 33

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.-C:~~~~~~~~t
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'.9.,-. - . ~ ~ ~~~ ~ ~ ~ ~ abnm?iA.~~.
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FIG. 7.-Representative body forms of tadpoles in various guilds: (A) lentic-benthic to lotic-clasping, Rana
palmipes; (B) lotic-neustonic, Megophrys montana; (C) lentic-nektonic, Type 1, Ololygon nebulosa; (D)
lotic-suctorial, Type 1, Hyla rivularis; (E) lotic-gastromyzophorous, Atelopus ignescens, (F) lotic-neustonic,
19891
1989] HERPETOLOGICAL MONOGRAPHS 97

dance, distribution, nutrient value, phys-
ical properties) of the prey items, is a
notable void.
RELATIONSHIPS OF LARVAL
MORPHOLOGY AND ECOLOGY
The naturalfeeding ecology (e.g., when,
where, how, and what, including changes
induced by environmental factors, ontog-
eny, and coinhabitants) of no tadpole is
well known. Studiesof larval insects, snails,
and microcrustaceans are well ahead of
studies in the feeding mechanics and ecol-
ogy of tadpoles. Our goal should be to un-
derstand how the morphology, behavior,
and physiology of tadpoles influence their
ecology and community structure.
Tadpoleseat large quantitiesof food and
have short gut clearance times (Altig and
McDearman, 1975), non-acidic gut pH
(Thrall, 1972), and a long gut with weak
peristalsisand no featuresother than length
to increase surface area (Savage, 1952,
1955; Wilcznska, 1981). At least on arti-
ficial diets, conversion efficiencies are high
(Culley and Sotiaridis, 1983). High den-
sities of numerous species of various mor-
phological types are commonly syntopic:
15 species in one brook in Madagascar
(Blommers-Schlosser and Blommers,1984);
16 lentic tadpoles in Ecuador (Berger,
1985); 11 species of calling males in south-
ern Mississippi(personalobservations).We
assume that the means by which tadpoles
partition food resources include the me-
chanics of oral structures.Three pertinent
questions arise: 1) What do tadpoles eat?
2) How does oral morphology relate to
feeding methodology? 3) How does feed-
ing methodology influence resource par-
titioning and therefore community struc-
ture?
The first question might be cast better
as "what do tadpoles digest?" The appar-
ent material that a tadpole swallows may
not be the primary material that is di-
gested. The following are available com-
monly as food: free and attached algae plus
their extracellular products; higher plant
tissue and plant products alive or degrad-
ed; zooplankton, periphyton, and auf-
wuchs; particulate organic debris plus at-
tached bacteria and meiofauna; and
polypeptide chains and amino acids
throughout the system including the sur-
face film (Goldacre, 1949). Live material
from higher plants and some algae prob-
ably are ingested to obtain the attached
periphyton, as much of this material is pro-
tected by thick cell walls and remains vi-
able during gut passage. Other than bro-
ken cells, proportionately little of the
material is digested, although some nu-
trients probably can be removed from in-
tact cells. Organic debris is likely ingested
to obtain the resident meiofauna, bacteria,
and molecular fragments. We know al-
most nothing about energetic, physiolog-
ical, or behavioral cost-benefit character-
istics associated with the "prey."
Studies of gut contents sometimes in-
dicate interspecific and site differences in
diet of tadpoles (Belova, 1964; Bugayski,
1930; Diaz-Paniagua,1985; Farlowe, 1928;
Gosner, 1959; Hendricks, 1973; Heyer,
1974; Inger, 1986; Jenssen, 1967; Osborne
and Maclahan, 1985; Sin and Gavrila,
1977) and often suggest non-selective
(composition,spatial, or temporal; see Ca-
rothersand Jaksic, 1984) feeding and per-
haps uniform or random distribution of
food items. We have little idea how diet
affects morphology (Meyer, 1987), life his-
tory features (Anderson and Cummins,
1979; Hota and Dash, 1986), and rather
little on how diet affects physiology (e.g.,
Culley and Sotiaridis,1983; Marshallet al.,
1980; Steinwascher and Travis, 1983).

Colostethus nubicola; (G) lotic-semiterrestrial, Thoropa petropolitana; (H) lotic-benthic, Leptopelis hyloides;
(I) lentic-arboreal, Type 3, Hyla bromeliacia; (J) lentic-suspension feeder, Type 2, Gastrophryne carolinensis;
(K) lentic-macrophagous, Type 2, Hyla microcephala; (L) lentic-macrophagous, Type 1, Occidozyga lima;
(M) lotic-adherent, Type 1, Hyla lindae; (N) lentic-adherent, Type 2, Hyla uranochroa; (0) lotic-fossorial,
Type 1, Centrolenella griffithsi; (P) lentic-arboreal, Type 2, Anotheca spinosa; (Q) lentic-carnivorous, Type
1, Ceratophrys cornuta; (R) lentic-arboreal, Type 5, Stephapaedes anotis. Original drawings by Linda Trueb;
reproduced courtesy of McGraw-Hill Publishing Co. from Duellman and Trueb, Biology of Amphibians.
98 HERPETOLOGICALMONOGRAPHS [No. 3
[No.

A E

I
1' 11'1l 1
"~l~lui'11i 1111
111l1
1k~111111111
1IIIp-IIIM,i
"'LLI'r
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11h '
I,S'IIIII

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Aq
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r i
o,
i?
i'

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:
il IAIA I

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9

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1989]
1989] HERPETOLOGICAL MONOGRAPHS 99

Three important data sets are small or of tadpoles,2) thesedifferencescrosstaxo-

lacking: temporal-spatial distribution of
tadpoles under the influence of a number
of variables (e.g., Alford, 1986; Alford and
Crump, 1982; Diaz-Paniagua, 1988;
Mitchell, 1983), microdistribution, abun-
dance, availability, and nutrient value of
food items; and detailed comparative food
habits of tadpoles at one site and time. As
normally done, gut content analyses may
be largely non-productivebecause the ma-
terial digested cannot be identified and
measured easily; Bogdan and Gilbert
(1987), Caron (1983), Caswell et al. (1973),
Coats and Heinbokel (1982), Coleman
(1980), Feller (1984), Fleming and Couch-
lan (1978), and Rau and Anderson (1981)
offer alternative but often labor-intensive
methods. Diatoms are the only easily
quantified objects in the gut that are likely
purposelyingested and digested. Available
information implies efficient feeding and
digestion of abundant, nutritious, and
probably widespread food. Stringent par-
titioning of food sourceshas not been dem-
onstrated. Perhaps the circumstances (i.e.,
non-reproductive, temporary inhabitants
that feed low on a short food chain with
abundant types and amounts of food) do
not demand stringent or continuous re-
source partitioning.
There are few data (e.g., Gosner, 1959;
Johnston, 1982; Kenny, 1969) concerning
the second question-how do oral mor-
phologies relate to feeding methodology?
The relative utility of labial teeth and jaw
sheathsin different ecological types of tad-
poles is not yet clear. Only Johnston(1982)
has made interspecific and ontogenetic
comparisonsinvolving a substratethat can
be penetrated by the oral structures.Only
general statements can be made: 1) there
are consistent differences in oral mor-
phology relative to major ecological types
nomic lines, but within certain bounds
generalideas of feeding functionscan be
suggestedfrom oral morphology,and 3)
within a major ecomorphologicaltype
thereare othermoresubtledifferencesre-
lating to oral function.It shouldbe kept
in mind that the functionsof the gill fil-
tering systemdeterminewhat eventually
arrivesin the gutfordigestion(Seale,1982;
Sealeand Beckvar,1980;Sealeand Was-
sersug,1979;Sealeet al., 1975;Wassersug,
1984).
Primarilybecausewe cannotanswerthe
secondquestionsufficientlywell, the third
question-how feedingmethodsinfluence
resourcepartitioningand thereforecom-
munity structure-cannot be answered.
We suggest reasonswhy present infor-
mationhas not revealedconcordantideas
on tadpole trophic relationships.Either
tadpolesshowmorphological oraldiversity
withouttrophicspecializationsor we have
not recognizedthe detailsof trophicdif-
ferences.Thisdoes not imply that all tad-
poles are euryphagous,but oral features
thatsuggestfeedingdifferencesmay have
been selectedfor by that raredemandfor
actual resource partitioning. The real
questionmay concernwhat a tadpolecan
do when resourcesare limited, not what
it doesroutinely(i.e.,"competitivecrunch"
of Wiens,1977,as comparedin Grossman
et al., 1982).
At the trophiclevel at which tadpoles
presumablyfeed, food scarcityor unavail-
ability is probablyuncommon.Structure
allows function but does not necessarily
predict it. High morphologicaldiversity
suggestshigh niche diversity.The diverse,
specialized morphologyof tadpoles ac-
commodatesthese ideas,but the circular-
ity is obvious:the observeddiversityof
structures,the presumedcommonalityof

FIG. 8.-Representative oral discs of tadpoles in various guilds: (A) lotic-clasping, Rana palmipes; (B)
lotic-neustonic, Megophrys montana; (C) lotic-adherent, Hyla rivularis; (D) lotic-gastromyzophorous, Ateo
lopus ignescens; (E) lentic-macrophagous, Hyla microcephala; (F) lentic-carnivorous, Ceratophrys cornuta;
(G) lotic-suctorial, Hyla lindae; (H) lotic-adherent, Type 2, Hyla uranochroa. Original drawings by Linda
Trueb; reproduced courtesy of McGraw-Hill Publishing Co. from Duellman and Trueb, Biology of Am-
phibians.
100
100 HERPETOLOGICALMONOGRAPHS
functions, and the availability of food ap-
pear contradictory. Dietary specializations
can be coupled with generalized mor-
phologies (Greene, 1982), but perhaps tad-
poles couple dietary generalization with
morphological specialization. Liem (1980)
supplied pertinent comparative data on
cichlid fishes. Species classified as algal eat-
ers were more specialized morphologically
but had a relatively wide range of func-
tional activities; pursuit hunters had a more
generalized morphology coupled with a
restricted functional repertoire. Such data
emphasize the danger of predicting func-
tion and ecological latitude solely from
morphology.
We predict that most tadpoles can feed
in a variety of probably minutely different
ways on a number of resources, but all
tadpoles do not have equal capabilities.
Variations in keratinized oral features may
function selectively only on those occasions
when food limitations demand partition-
ing. Also, many differences (e.g., number
and arrangement of cusps on labial teeth)
may have arisen through fixation of var-
ious contingencies of polygenic inheri-
tance (e.g., linkage, pleiotropy, position ef-
fect), while selection was for an
unidentified factor(s) or heterochronic
changes in development. The cellular basis
for pattern formation must be resolved be-
fore an understanding of some traits will
be understood. Crosses of species with dif-
ferent tooth row formulae carried through
several generations would suggest mech-
anisms of genetic control. Proper analyses
of variation (e.g., Palmer and Strobeck,
1986) may allow ranking of the relative
importance of features without knowing
their actual functions. The functional sig-
nificance of the numerous configurations
of tadpole vent tubes (Johnston and Altig,
1986) and microdermatoglyphics of snake
scales judged to be of taxonomic but not
ecological significance (Price, 1982) may
be analogous cases (see Gans, 1976).
Data on various facets of tadpole ecol-
ogy, environmental effects, and metabolic
functions are available (e.g., Alford, 1986;
Alford and Crump, 1982; Berven, 1982a,b;
Black, 1976; Breden and Kelly, 1982;
Brockelman, 1969; Brodie and Formano-
wicz, 1983; Calef, 1973; Cecil and Just,
[No.
[No. 3
1979; Collins, 1979; Crump, 1981, 1983,
1984; DeBenedictus, 1974; Dupre and Pe-
tranka, 1985; Freda and Dunson, 1985;
Gatten et al., 1984; Herreid and Kinney,
1966; Heyer, 1973, 1974; Hota and Dash,
1986; Inger et al., 1986; Licht, 1974; Ling
et al., 1986; Loschenkohl, 1986; Morin,
1981, 1983; Noland and Ultsch, 1981;
Odendaal and Bull, 1983; Odendaal and
Nias, 1982; Seale, 1980; Semlitsch and
Caldwell, 1982; Smith, 1983; Smith-Gill
and Gill, 1978; Steinwascher, 1978; Travis,
1981, 1983a,b; Wassersug and Murphy,
1987; Wassersug and Seibert, 1975; Weig-
mann, 1982; Wilbur, 1972; Wilbur et al.,
1983; Wiltshire and Bull, 1977; Wood-
ward, 1982a,b, 1983). Laboratory data on
competition for food (e.g., Steinwascher,
1979a,b; Travis, 1980a,b; Wilbur, 1982)
reveal competitive interactions that cause
profound effects, but design constraints
disallow many factors (e.g., space, time,
alternate food sources) that may reduce or
eliminate these effects in the field. It would
seem that factors associated with the feed-
ing niches of at least representative tadpole
morphotypes must be unveiled before de-
tailed descriptions of communities of tad-
poles can be made.
Spatial segregation suggested by body,
fin, and eye configurations, especially when
coupled with diel and seasonal differences,
may be a prime mechanism to allow par-
titioning of food resources that are difficult
to partition directly (Toft, 1985). The de-
gree of interspecific or ontogenetic differ-
ences in feeding ecology may be less than
or at least not concordant with the differ-
ences in magnitude of the more easily seen
morphological traits. We must retreat to
autecology (Greene, 1986), functional
anatomy, digestive physiology, and closely
controlled studies of many facets of field
ecology before feeding ecology can be used
in community definitions of tadpoles to
any accurate degree. Functional mor-
phology of oral features to complement the
data on gill filter systems and detection of
the subtle differences in resource parti-
tioning are the most pertinent and prob-
ably the most difficult data to obtain.
Acknowledgments. -We graciously acknowledge
Linda Trueb, William E. Duellman, and McGraw-
1989]
1989] HERPETOLOGICAL MONOGRAPHS
Hill Publishing Company for allowing us to reprint
figures appearing originally in Biology of Amphib-
ians (1986). D. G. Thibaudeau prepared the other
figures. A. Channing, M. L. Crump, R. W. Mc-
Diarmid, and R. J. Wassersug were the latest in a
long series of persons to substantially improve this
constantly evolving manuscript; we thank them and
all the others for numerous comments and sugges-
tions. Specimens were examined at the California
Academy of Sciences, Field Museum of Natural His-
tory (R. M. Louer Fund Award to GFJ), United States
National Museum of Natural History (Smithsonian
Visiting Student Research Appointment to GFJ), and
the University of Michigan Museum of Zoology; we
thank the respective curators for their assistance.
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dophryne bibroni and P. semimarmorata (Anura:
Leptodactylidae). Australia J. Zool. 25:449-454.
WOODWARD, B. D. 1982a. Tadpole competition in
a desert anuran community. Oecologia 54:96-100.
.1982b. Tadpole interactions in the Chi-
huahuan Desert at two experimental densities.
Southw. Nat. 27:119-121.
[No. 3
1983. Tadpole size and predation in the
Chihuahuan Desert. Southw. Nat. 28:470-471.
Accepted: 25 October 1988
Associate Editor: Raymond D. Semlitsch
APPENDIX
Developmental Guilds of
Endotrophic Anurans
"Live-bearing" is a confusing term. We restrict its
use to situations where a froglet is birthed from the
oviducts, i.e., viviparous or ovoviviparous. To avoid
a new term for males that carry eggs and embryos,
gravid is extended to either parent in the next four
guilds associated with eggs or larvae. Guild names
are in boldface, and taxonomic listings are not always
exhaustive.
1. Viviparous: Froglet birthed from oviducts; nu-
trition provided by maternal oviducal materials
after yolk exhaustion; placenta not required
(Wake, 1982); fertilization internal; develop-
ment highly modified; fetus applies to advanced
unborns-Nectophrynoides occidentalis only.
2. Ovoviviparous: Froglet birthed from oviducts;
no extra-ova nutrition whether confined within
egg membranes or not; fertilization internal;
development highly modified-Eleutherodac-
tylus jasperi, Nectophrynoides tornieri, N. vi-
viparus only.
3. Paraviviparous: Froglet hatched from egg cap-
sules at eventual site of deposition-in the stom-
ach (Rheobatrachus), in the dorsal skin (Pipa
pipa), on the dorsal skin (some hemiphractine
hylids), or within a complete (Gastrotheca part)
or partial (Flectonotus) dorsal pouch; larva may
exhibit partial tadpole morphotype during de-
velopment; female parent always involved.
4. Exoviviparous: Froglet not "birthed" from site
of egg deposition as hatched embryo, 1) moves
of own accord into dorsal pouch with inguinal
port (Assa) or onto parent's dorsum (Leiopelma
archeyi, L. hamiltoni, Sooglossus sechellensis)
or 2) is swallowed into the vocal sac (Rhino-
derma sp.); male parent usually involved. Be-
cause 1) parental action involved, 2) a tadpole
morphotype exists, and 3) a complex paternal-
larval nutritional relationship is involved (Goi-
coechea et al., 1986), at least R. darwinii may
have to be removed from this guild.
5. Direct Developer: Froglet hatched from egg
capsules of deposited eggs not intimately asso-
ciated with parent's body; reports of meroblasty
(de Villiers, 1929; Warren, 1922) warrant in-
vestigation; tail greatly reduced or enlarged and
vascularized; small gills present or not; spiracle
absent; oral structures of exotrophic tadpoles
absent-Arthroleptis, Australopapuan micro-
hylids, Eleutherodactylus (most), Hylacto-
phryne, Myobatrachus, Oreophrynella, Platy-
mantis, Sooglossus gardneri, Syrrhophus,
Tomodactylus, and others.
6. Nidicolous: Egg or larva seldom intimately as-
19891
199 HERPEOLOGIAL MONOGRAPHS
HERPETOLOGICALMOOGRAPS
sociated with parent's body; eggs often small
and numerous; normal embryology results in
free-living, non-feeding tadpole, continuum
from those having morphologicaltraits of exo-
trophic tadpoles to those that have fins, oral
apparatus, pigment and/or spiracle variously
reduced to absent; tadpole remains in or near
nest site until metamorphosis-Adenomera,
Anodontohyla, Craspedoglossa, Eupsophus,
Leiopelma hochstetteri, probably Mertenso-
phryne, Nectophrynoides malcolmi, Para-
cophyla, Pelophryne, Philoria, Phrynodon,
Platypelis, Plethodontohyla, Rana (few),
Synapturanus, Vanzolinius, Zachaenus.
EcomorphologicalGuilds of
Exotrophic Anurans
Guild names are in boldface and noted by Arabic
numerals;taxonomic listings are not always exhaus-
tive. SectionI coverslotic forms,and section II covers
lentic forms.
Section I. Tadpoles inhabit flowing water
systems-streams, rivers, creeks, seeps,
rivulets;lotic is a generic term.
A. Tadpolesinhabitflowingportionsof the system;
rheophilous(= rhyacophilous)is a generalterm;
eyes small, non-bulging, and dorsal; oral disc
usually large, pendant, and ventral;tail muscle
often massive;fins low, terminate at tail-body
junction or posteriorly,often in rounded tip.
1. Clasping:Marginalpapillae with anteriorgap;
tooth rows 5 (= 2/3) up to at least 8/8 but often
with more anterior rows than posterior rows;
eyes not as small as in following groups;inhabit
slow water; position maintenance by oral disc
minor-Boophis (part),Natalobatrachus,Rana
pustulosa and palmipes groups (Figs. 7A, 8A)
2. Adherent: Complete marginalpapillae numer-
ous, small,and closely packed, often in multiple
rows;LTRF (= labial tooth row formula) com-
monly 2/3; inhabit faster water than Clasping
tadpoles; position maintenance via oral disc B.
common to continuous; submarginal papillae
often large and in rows above A-1 and below
last lower row; torrent tadpole is a collective
term for this and next two guilds.
2a. Type 1: Belly flattened, body bluntly rounded
anteriorly-Hyla (many), Plectrohyla (all),
Ptychohyla (part;Fig. 8G).
2b. Type 2: Similar to above, but more slender;
tooth rows sometimes reduced to absent but
never long;large areasof oraldisc withouttooth
rows;jaw sheaths not robust-Hyla rufioculis,
H. uranochroa (Figs. 7N, 8H), Mantidactylus
femoralis, Ptychohyla (part), Taudactylus.
3. Suctorial: Complete marginal papillae small,
numerous,and usually in multiple rows;LTRF
> 2/3-17/21; inhabit faster water than Ad-
herent or Clasping tadpoles; position mainte-
nance via oral disc continuous;submarginalpa-
pillae often more numerous and not arranged
as for adherent species; fleshy flap underlies
hindleg anlagen in some (e.g., Ascaphus, He-
leophryne). Once more is known about mouth
107
10
part functions, this group will surely be divided
further: total number of tooth rows, row ar-
rangement (more on anterior labium, more on
posterior labium, equal; one versus several rows
broken medially adjacent to jaw sheaths), many
variations in jaw sheath configurations and body
shape.
3a. Type 1: Belly flattened, snout rounded in lateral
view-Ascaphus, Bufo penangensis, Conraua,
Hyla (many),Petropedetes,Scutiger(may have
narrow anterior gap in marginal papillae typ-
ical of pelobatids), Trichobatrachus (Fig. 7D).
3b. Type 2: Anterior end of body markedly de-
pressed-Heleophryne, some peladryadinine
hylids.
4. Gastromyzophorous: Belly sucker present,
sucker cup papillate and/or with keratinized
patches; complete marginal papillae or poorly
developed posteriorly; fins low, dorsal fin often
terminates posterior to body; LTRF upwards
from 2/3; inhabit fastest, often turbulent water;
position maintenance by oral disc/belly sucker
continuous-Amolops, Atelopus (Figs. 7E, 8D).
5. Psammonic: Long spiracular tube free from
depressed body; hypertrophied jaw serrations
lack basal sheath; labial teeth absent; "oral disc"
greatly reduced; eyes dorsal-Otophryne ro-
busta (Pyburn, 1975; Wassersug and Pyburn,
1987).
6. Semiterrestrial: Semiterrestrial (Duellman and
Trueb, 1986) seems more appropriate than sub-
aerial (Wassersug and Heyer, 1983). May in-
volve two groups-Leptodactylus versus oth-
ers. Inhabit wet rock faces and rivulets, spend
time out of water; low tail fins on attenuate tail
often restricted to posterior third of tail; mouth
ventral with incomplete marginal papillae and
5 tooth rows; eyes often large and protrudent;
belly flattened; hindlegs often develop early-
Cycloramphus (part), Leptodactylus rugosus,
Nannophrys ceylonensis, Rana beddomei,
Thoropa, Werneria (part) (Fig. 7G).
Tadpoles inhabit microhabitats of non-flowing
portions (backwaters, burrows, eddies, pools) of
lotic systems, habitats similar in many respects
to lentic systems; tadpoles resemble lentic forms.
7. Benthic: See lentic-benthic tadpoles, II.12-
Colostethusinguinalis, Hyla arenicolor,H. ca-
daverina, Leptopelis sp. (Fig. 7H), Rana an-
golensis, R. fuscigula, Strongylopusgrayii (Fig.
7A).
8. Fossorial: Vermiform burrowers with de-
pressed body; eyes dorsal; low fins on long tail.
8a. Type 1: LTRF 2/3, oral disc small; marginal
papillae incomplete anteriorly; eyes small, not
bulging, and notedly parasagittal; often red be-
cause of skin vascularity; stated that tadpoles
live among rocks of stream bottoms, but more
commonly buried within leaf mats in still-water
areas-Centrolene, Centrolenella (Fig. 70).
8b. Type 2: Tooth rows reduced to absent; often
found among interstices of small stones; mouth
structure suggests suctorial forms, but body-tail
configurations and behavior suggest placement
here-Leptobrachium (part).
 108 108 HERPETOLOGICAL MONOGRAPHS
HERPETOLOGICAL MONOGRAPHS
9. Nektonic: Syn: pelagic (= open water). This and
the analogous lentic guild (II.15) form mor-
phological continuum-lotic-nektonic forms
have higher fins and more lateral eyes than llg.
lotic-benthic forms but never have fins as high
or eyes as lateral as most lentic-nektonic forms-
Hyla miotympanum, Strongylopus fasciatus.
10. Neustonic: Enlarged oral disc directed dorsally 12.
(= umbelliform); eyes usually lateral, tail long
with low fins. Once development and function
of the oral configurations are known, this guild
may require division: presence/absence of ker- 12a.
atinized mouth parts, oral disc form and func-
tion, and feeding ecology (see 11.16-) Colo-
stethus nubicola, Mantidactylus oviparus,
Megophrys montana, Phyllomedusa guttata, 12b.
P. jandaia (Fig. 7B).
Section II. Tadpoles inhabit non-flowing
systems-bromeliads, lakes, ponds, puddles,
tree holes; lentic is a generic term. 13.
11. Arboreal: As used by Lannoo et al. (1987) plus
all isolated pockets of water, elevated or not
13a.
(tree holes, terrestrial and arboreal bromeliads,
holes in logs, stumps, and bamboo, leaf axils,
fallen leaves, large snail shells, etc.); syn: phy-
totelmonous. Largely adopted from Lannoo et
al. (1987).
1 la.
Type 1: Elongate with attenuate body; tail: body
ratio >2; LTRF 1/1 or less; highly reduced gill
filters and filaments; musculoskeletal special-
izations for macrophagy; reduced pigment; in
areas with low productivity-bromeliads and
leaf axils; all may be obligatory oophagous-
Dendrobates (part), Hoplophryne, Osteopilus
brunneus, Philautus (part).
1 b. Type 2: Shorter with stout body; tail: body ratio
<2; LTRF <2/2; reduced gill filters and fila-
13b.
ments; reduced pigment; carnivorous and mac-
rophagous-Anotheca spinosa, Hyla zeteki (Fig.
7P).
llc.
Type 3: Elongate with attenuate body; tail: body
ratio >1.7; LTRF >2/3; minimal reduction of 13c.
internal oral features; no musculoskeletal spe-
cializations for macrophagy. Once functions of
tooth row configurations are known, this group
may be divided-those that increase the LTRF
above 2/3 by adding posterior rows and those 14.
that add anterior rows-Hyla bromeliacia, H.
dendroscarta, Mantidactylus (part), Phyllo-
dytes (Fig. 71). 14a.
lid. Type 4: Short with stout body; tail:body ratio
<2; LTRF >2/3, some increase in anterior rows; 14b.
gill filters and filaments normal to greater than
normal; darkly pigmented-Acanthixalus,
Nyctixalus, Theloderma.
lie. Type 5: Raised fleshy ring of unknown function
on head encompasses eyes and nares; otherwise
resemble lentic-benthic forms (II.12)-Mer- 15.
tensophryne (morphologically belongs here, but
probably nidicolous, see above), Stephopaedes
(Fig. 7R).
llf. Type 6: Inhabit humid microhabitat on and
under bark of trees, feed on organic detritus 15a.
with jaw sheaths and labial teeth; large hindlegs
[No.
[No. 3~~~~~~~~~~
3
develop early; long tail with no fins; hides among
organic debris in tree holes-Indirana gundia
(Dubois, 1986).
Type 7: Closely resembles most other phyllo-
medusine hylids (II.18) but with complete mar-
ginal oral disc papillae-Agalychnis calcarifer,
Phyllomedusa fimbriata.
Benthic: Body depressed to globular-depressed;
oral disc ventral to anteroventral; eyes dorsal;
low fins do not extend beyond tail-body junc-
tion; LTRF often 2/3.
Type 1: Littoral, shallow, often weedy shoreline
or shallow areas-Acris, Alytes, Bufo (most),
Colostethus (part), Dendrobates (part), Smilis-
ca (part).
Type 2: Profundal (= bottom without emergent
vegetation or at least deeper); may move from
littoral to profundal areas for thermoregula-
tion-Bufo (part), Ptychadena, Rana (many).
Carnivore: Configurations of body, tail, and eyes
usually similar to lentic-benthic forms (11.12),
although mouth often terminal.
Type 1: Keratinized jaw sheaths present, often
cuspate; tooth rows absent to >2/3; carnivory
in all individuals (Ceratophrys, Lechriodus,
perhaps Hyla marmorata) or only some indi-
viduals at some sites in some years (Scaphiopus
part); cannibalism may be included; prey may
be engulfed by one individual (Ceratophrys)
or rasped apart (alive or dead) by a group (Hyla
marmorata); jaw musculature often hypertro-
phied; body often widest anteriorly except in
hylids; most are active swimmers in the water
column; carnivorous/oophagous arboreal forms
placed in the arboreal guild because of adap-
tations for living in small bodies of water (Fig.
7Q).
Type 2: LTRF 0/0, isolated jaw serrations with-
out a base; huge mouth without an oral disc;
body depressed; macrophagous-Lepidobatra-
chus.
Type 3: No keratinized mouth parts, soft mouth
parts reduced and protrusible; inhabit water
column, eyes lateral; macrophagous on small
crustaceans, etc.-Hymenochirus, Pipa carval-
hoi.
Macrophagous: LTRF 0/0 or 0/1; jaw sheaths
present; terminal oral disc small to absent, with
or without a few marginal papillae.
Type 1: Benthic, body depressed; eyes dorsal-
Occidozyga (Fig. 7L), probably Cardioglossa.
Type 2: Nektonic, body cylindrical to depressed
in cross-section; eyes lateral; tail flagellum and
cryptic coloration common; float motionless and
horizontally in water column, often among
vegetation-Afrixalus, Hyla leucophyllata, mi-
crocephala, and parviceps groups (Figs. 7K, 8E).
Nektonic: Body compressed; tail flagellum
common; fins commonly high and may extend
anteriorly to level of bulging, lateral eyes; tail
muscle not massive; feed by rasping surfaces
with anteroventral mouth.
Type 1: LTRF commonly 2/3-Hyla (many),
Ololygon (most), Smilisca (part) (Fig. 7C).
1989] HERPETOLOGICALMONOGRAPHS
15b. Type 2: LTRF greater than 2/3-Phrynohyas,
Trachycephalus.
16. Neustonic: Similar to II.12 but oral disc in-
verted (= umbelliform) like lotic-neustonic
(I.B.10)-Microhyla achatina (Figs. 7F, 8B).
17. Suspension Feeder: Keratinized mouth parts
absent; tail flagellum common; inhabit the water
column; body usually strongly depressed, eyes
lateral; low fins similar in size or ventral larger.
17a. Type 1: Often lightly pigmented without bold
patterns; barbels present, no other prominent
oral features around terminal, horizontal, slit-
like mouth; includes only Orton (1953) Type I
tadpoles-Rhinophrynus, Silurana, Xenopus.
17b. Type 2: Almost nonpigmented and transparent
other than eyes and gut to heavily pigmented;
oral disc derivatives variously shaped but sel-
dom prominent around terminal mouth; bar-
bels absent; often small; sometimes locomote by
current from midventral spiracle-Chiasmo-
cleis, Ctenophryne, Gastrophryne, Nelsono-
phryne, Hypopachus, Microhyla (part), Phry-
nomerus (Fig. 7J).
18. Suspension-Rasper: Keratinized jaw sheaths and
labial teeth (usually 2/3) with anterior gap in
109
109
marginal papillae; eyes lateral; tail flagellum
present to lesser or greater degree; often sus-
pended in midwater, often head-up; ventral fin
may be considerably higher than dorsal fin,
which stops near tail-body junction; schooling
reported-Agalychnis (most), Kassina, Pachy-
medusa, Phyllomedusa (most).
Comments.-Behavioral variations sometimes
suggest moving a taxon to another guild. For example,
the normally benthic tadpoles of Bufo and Rana
sometimes swim within the water column, whereas
many nektonic species of Hyla spend considerable
time on the bottom when in shallow water. Tadpoles
of Kassina may be carnivorous at times (van Dijk,
1972). We suggest that such variations be noted but
that each taxon be placed in the one guild to which
it most commonly conforms.
Other guilds and types will surely be recognized.
The large genus Hyperolius with similar mouth parts
could not be categorized because of insufficient data.
Tadpoles of Scarthyla ostinodactyla and the Ololy-
gon rostrata group have unique oral configurations
that may warrant a separate lentic group.