JOURNAL OF MORPHOLOGY 238:109–141 (1998)

Correlations of Cranial Morphology, Ecology, and Evolution

in Australian Suctorial Tadpoles of the Genera Litoria and
Nyctimystes (Amphibia: Anura: Hylidae: Pelodryadinae)
ALEXANDER HAAS1* AND STEPHEN J. RICHARDS2
1Institut
für Spezielle Zoologie und Evolutionsbiologie, Friedrich-Schiller-
Universität Jena, D-07743 Jena, Germany
2Cooperative Research Centre for Tropical Rainforest Ecology and

Management, and Department of Zoology and Tropical Ecology, James

Cook University, Townsville, QLD 4811, Australia

ABSTRACT Suctorial anuran larvae are highly specialized for living in

fast-flowing waters, using their oral disks as adhesive organs to attach to the
substrate. The cranial musculoskeletal structure of suctorial larvae of Litoria
nannotis, L. rheocola, and Nyctimystes dayi (Hylidae: Pelodryadinae) were
compared with congenerics with pond-type larvae (L. caerulea, L. genimacu-
lata, L. xanthomera). Data from two other neobatrachian species with sucto-
rial larvae (Boophis sp., Hyla armata) as well as published descriptions were
taken into account. Suctorial tadpoles evolved several times independently in
the Neobatrachia and share various features, irrespective of their phyloge-
netic position. These include the following. Cornua trabeculae are expanded
anteriorly and sometimes fused. The lower jaws are robust. The greatest
width of the skull is at the level of the jaw articulation. The upper jaw
cartilages are partially or fully fused. The palatoquadrate is robust and
connected to the skull by a wide commissura quadratocranialis anterior,
processus oticus, processus basalis (in some species), and processus ascendens
(vestigial or absent in some species). A processus ventralis quadrati provides
an extended area of origin for the m. orbitohyoideus. The m. rectus abdominis
inserts far anterior and acts on the cranium. The insertion of the epaxial
musculature is shifted anteriorly to the anterior parts of the otic capsule. The
mm. diaphragmatobranchialis and rectus cervicis cross at their origins. The
origin of the m. levator mandibulae anterior has shifted posteriorly. The
branchial basket is relatively small and the ceratohyal area is large. Multiple
convergent evolution of these features suggests that they may be causally
associated with the suctorial mode of larval life. Aside from these characters,
however, the suctorial and pond-type neobatrachian species are remarkably
similar in their jaw musculature and hyobranchial musculoskeletal composi-
tion. In some features, Ascaphus truei differs significantly from the neobatra-
chian suctorial species, indicating the influence of the historically distant
separation of the two taxa. A novel modification of the upper jaw abduction
mechanism has evolved in L. nannotis, L. rheocola, and N. dayi. It involves an
adrostral cartilage as a pushing-rod element. This mechanism and unique
structural similarities of the cartilago labialis superior gives support to the
preliminary assumption that the nannotis species group is more closely
related to the suctorial Nyctimystes dayi than it is to other Litoria species with

Contract grant sponsor: Deutsche Forschungsgemeinschaft; Contract grant number: Ha 2323/2–1.

*Correspondence to: Alexander Haas, Institut für Spezielle Zoologie und Evolutionsbiologie, Friedrich-Schiller-Universität Jena,
Erbertstr. 1, D-07743 Jena, Germany.
E-mail: b5haal@rz.uni-jena.de

r 1998 WILEY-LISS, INC.

110 A. HAAS AND S.J. RICHARDS

pond-type larvae. Suctorial larvae presumably were present in the most

recent common ancestor of the Litoria nannotis group and Nyctimystes dayi.
J. Morphol. 238:109–141, 1998. r 1998 Wiley-Liss, Inc.
KEY WORDS: Amphibia; Anura; Hylidae; Pelodryadinae; Litoria; Nyctimystes; Hyla; Boophis;
cranial morphology; musculature; suctorial larvae; functional morphology; phylogeny

Most frog species have a biphasic life cycle
in which aquatic larvae metamorphose into
froglets. Selective pressures in the larval
and adult stages are quite independent, so
ecological and morphological evolution in the
two life stages is largely uncoupled. A broad
diversity of modes of life and body shapes
have evolved in both tadpoles and frogs,
sometimes convergently in several lineages.
Correlations of tadpole habitat choice and
feeding with body shape, features of the oral
disk, and buccal cavity are often obvious and
have been used to define ‘‘ecomorphological
types’’ (Orton, ‘53; Duellman and Trueb, ‘86;
Altig and Johnston, ‘89). These types are, of
course, to some extent arbitrary delimita-
tions of a continuum. The so-called rheophi-
lous suctorial-type tadpoles (Altig and Johns-
ton, ‘89) live in fast-flowing streams or rivers,
cascades, or at the bases of waterfalls. Their
bodies are dorsoventrally flattened, the tail
is strongly muscular, and the tail fin is low
and often restricted to the posterior half of
the tail. The rostral region is conspicuously
expanded and bears a large ventral suctorial
oral disk (Altig and Johnston, ‘89; Richards,
‘92), with which the tadpoles attach them-
selves to the substrate.
The literature on the interrelationships of
larval ecology and larval morphology fo-
cuses mainly on external features, i.e., body
shape, oral disk features, or epithelial struc-
tures of the feeding apparatus (e.g., Orton,
‘53; Wassersug and Rosenberg, ‘79; Wasser-
sug, ‘80; Wassersug and Duellman, ‘84;
Duellman and Trueb, ‘86; Viertel, ‘87; Wass-
ersug and Heyer, ‘88; Altig and Johnston,
‘89). A few studies have considered correla-
tions of the skeletal structure with ecology
(Pusey, ‘43; Wassersug and Hoff, ‘79; Ruibal
and Thomas, ‘88). Anatomical features of
torrent-dwelling tadpoles were described in
detail by Pusey (‘43)(Ascaphus truei), Ra-
maswami (‘44)(Heleophryne purcelli,
H. regis, and a ‘‘cystignathid’’ tadpole), van
Eeden (‘51)(Ascaphus truei), and van der
Westhuizen (‘61)(Heleophryne purcelli).
However, the intention of each of these inves-
tigators was primarily to address either
questions of homology or the process of meta-
morphic changes. Thus, although the cra-
nial anatomy of some species of torrent-
dwelling suctorial tadpoles has been
described, there is no comparative analysis
of the significance of the cranial features in
suctorial larvae in general.
In this paper, we investigate correlations
of suctorial habits with features of cranial
musculoskeletal structure of suctorial lar-
vae. To distinguish confidently derived fea-
tures correlated with habits from persisting
plesiomorphic features, a sample of closely
related species was chosen from the genera
Litoria and Nyctimystes. Larvae of some spe-
cies live in fast streams and others live in
slow-moving or stagnant aquatic habitats.
Litoria and Nyctimystes are included in the
endemic Australopapuan hylid subfamily
Pelodryadinae (Frost, ‘85; Duellman and
Trueb, ‘86) and are more closely related to
each other than to any of the other three
subgroups of the Hylidae, i.e., Phyllomedusi-
nae, Hylinae, and Hemiphractinae (Tyler,
‘71; Tyler and Davies, ‘78; Duellman and
Trueb, ‘86; Hutchinson and Maxson, ‘87). In
this phylogenetic context, one would expect
species to resemble one another morphologi-
cally as a result of their recent common
ancestry. Therefore, structural differences
between closely related species with distinct
habits may be interpreted to reflect features
related to habits and ecology.
We examined six Australian pelodryadine
species occupying a range of aquatic habi-
tats. Litoria caerulea occurs predominantly
in large temporary ponds and small ephem-
eral pools in monsoon savanna habitats
across northern Australia. Litoria xan-
thomera larvae live in temporary rainforest
pools and in rock holes adjacent to but sepa-
rate from rainforest streams. Litoria geni-
maculata occurs in rainforest streams, but
is restricted to slow-flowing areas of these
streams. These three species have typical
pond-type larvae. Although predominantly
benthic, they spend a considerable propor-
tion of their time swimming in the water
column. The three remaining species (L. nan-
notis, L. rheocola, and Nyctimystes dayi) oc-
cur in sympatry with L. genimaculata in
 CRANIAL MORPHOLOGY OF SUCTORIAL TADPOLES 111

rainforest streams but have suctorial larvae

and are restricted largely to fast-flowing,
rocky sections and highly oxygenated pools
at the base of waterfalls. They graze on
algae on exposed rocks in riffles and tor-
rents, adhering almost continuously to rocks
with their suctorial mouths to avoid being
dislodged by the current. When not grazing,
these species seek shelter by moving be-
tween or under rocks, and do not appear to
use the water column at all. Both L. nanno-
tis and L. rheocola belong to the L. nannotis
species group of Tyler and Davies (‘78). Exter-
nal features of suctorial tadpoles of the
L. nannotis group and N. dayi have been
described earlier (Davies and Richards, ‘90;
Richards, ‘92). Larvae of Hyla armata (Hyli-
dae: Hylinae) and one unidentified species of
the genus Boophis (Ranoidea: Rhacophori-
dae) were compared with the pelodryadine
sample. A close phylogenetic relationship of
the latter two species to the pelodryadines
can be excluded (Duellman and Trueb, ‘86;
Ford and Cannatella, ‘93). The same applies
to Ascaphus truei (Ascaphidae), Heleophryne
purcelli, and H. natalensis, for which data
are considered from the literature (Pusey,
‘43; Ramaswami, ‘44; van Eeden, ‘51; van
der Westhuizen, ‘61; Reiss, ‘97; Haas, ‘97).
The phylogenetic framework for the species
considered is depicted in Figure 1.
In the following comparative study on the
musculoskeletal structure of the larval cra-
nium, we will assess whether suctorial hab-
its correlate with specific structural features
of the closely related pelodryadine larvae,
and if there are differences and/or similari-
ties with suctorial larvae in distantly re-
lated taxa. Within this context of close and
distant relationships, we will try to differen-
tiate convergently evolved versus phyloge-
netically informative characters and discuss
their significance for phylogenetic hypoth-
eses concerning the evolution of suctorial
tadpoles in pelodryadine frogs.
MATERIALS AND METHODS
The Appendix summarizes species, num-
bers of specimens, stages, types of prepara-
tion, and localities. S.J.R. collected all larval
materials, except specimens of Litoria caeru-
lea that were obtained from a captive breed-
ing group (N. Meyer). The staging table of
Gosner (‘60) was applied to all specimens,
although using it for the torrent-dwelling
species is somewhat misleading. The se-
quence of larval differentiation and metamor-
phic events in torrent-dwelling larvae devi-
Fig. 1. Hypothetical phylogenetic relationships of
the Anura. Adopted and simplified from Ford and Canna-
tella (‘93) and modified according to Haas (‘97). Bold, the
groups sampled. Suctorial tadpoles evolved multiple
times in the Anura. Aside from the sampled taxa, sucto-
rial tadpoles have been reported for the Bufonidae and
the Ranidae (Orton, ‘53; Mertens, ‘60; Altig and Johns-
ton, ‘89; Inger, ‘92).
ates from that generally known for pond-
type larvae (Davies and Richards, ‘90;
Nodzenski and Inger, ‘90).
Larvae were fixed in neutral-buffered for-
malin (4–10%). The larvae were used for
either serial sectioning (n ⫽11), clearing and
staining (n ⫽31), or manual dissection
(n ⫽12) preparations. All three sources of
information were used for each species. For
serial sectioning, specimens were embedded
in paraffin, sectioned at 10 µm, and stained
with Azan trichrome (Romeis, ‘89). Clearing
and double staining followed the protocol of
Dingerkus and Uhler (‘77). Specimens for
manual dissection were prepared by apply-
ing only the first staining step (Alcian blue)
of the Dingerkus and Uhler protocol. As Al-
cian blue binds specifically to acid gly-
cosaminoglycans in the extracellular matrix
of hyaline cartilage, this staining yields good
contrast between dark blue cartilaginous
structures and unstained, white muscles.
Dissections were done under an Olympus
SZH stereomicroscope using sharp watch-
maker‘s forceps. After dissection, the clear-
ing and staining protocol was resumed.
Drawings from cleared specimens were
made with a Zeiss SV 11 stereomicroscope
112 A. HAAS AND S.J. RICHARDS
equipped with a camera lucida. Final finish
was done either with an airbrush technique
and/or digitally with Adobe Photoshopt 3.0
software. Three-dimensional reconstructions
were made from serially sectioned speci-
mens on a Silicon Graphics Indigo2 Ex-
tremey computer, using Alias Studioy 7.5
software (Haas and Fischer ‘97).
For morphometry, cleared and stained
specimens were photographed electronically
with a JVC KY-F55 video camera mounted
on a Zeiss SV11 stereomicroscope. The cam-
era was connected to an Apple Power Macin-
toshy 8500 computer. Frame capturing was
done with Avid Videoshopt 3.0 software.
Measurements were taken from electronic
measurements with NIH Image 1.61 soft-
ware. We recorded several measurements
from cleared and stained hyobranchial skel-
eton to quantify observable shape differ-
ences. The planum hypobranchiale was ori-
ented parallel to the camera plane. Because
some measurements depend on the orienta-
tion of the specimen, each specimen was
reoriented twice, so that three different pho-
tographs of the same specimen could be mea-
sured. Both sides of the body were mea-
sured. The package Morphometrika (by J.A.
Walker; http://192.107.185.24/Morphometrics.
html) was used to perform a landmark-
based, geometric comparison (Thin Plate
Spline; Bookstein, ‘91) of two species.
Skeletal terminology follows that of Haas
(‘95, ‘96a, ‘97) and, with a few exceptions,
conforms to that of Sokol (‘81). The classifica-
tion of Edgeworth (‘35) is adopted for man-
dibular arch musculature, modified accord-
ing to the suggested terminology of Schlosser
and Roth (‘95). The recently proposed nomen-
clature of Haas (‘97) was applied for hyobran-
chial musculature. The expression ‘‘flexible
cartilage’’ is used to describe a type of carti-
lage found in various intracartilage, i.e., syn-
chondrotic, articulations of the tadpole skull
(Gaupp, 1894; de Jongh, ‘68; Gradwell, ‘72a),
for example, the pars reuniens. It is contigu-
ous with hyaline cartilage but differs from it
in having smaller cells and in the extent and
composition of the extracellular matrix. Its
acid staining reaction with Alcian blue is
weak or absent in cleared and stained speci-
mens.
RESULTS
The general external and oral disk mor-
phologies of four species occupying a range
of habitat types in north Queensland rainfor-
ests are illustrated in Figure 2. The two
suctorial species, Litoria nannotis and Nycti-
mystes dayi, are characterized by a dorsoven-
trally flattened body, thick tail muscle, tail
fin originating posterior to the tail-body junc-
tion, undivided tooth rows (2/3), and a large,
ventrally located oral disc with an uninter-
rupted outer row of oral papillae. Litoria
genimaculata and L. xanthomera, which live
in slow-flowing stretches of streams and in
temporary rainforest pools respectively, have
external features typical of pond-dwelling
pelodryadine hylid tadpoles. These include a
small, anteroventrally located oral disk, di-
vided tooth rows (2(2)/3(1)), and a dorsomedi-
ally interrupted outer row of oral papillae.
Apart from the differences in the musculo-
skeletal structure of the head that will be
described below, we found delayed lung de-
velopment in the pelodryadine suctorial spe-
cies studied. Litoria nannotis (stage 39) and
Nyctimystes dayi (stage 37) have lung and
laryngeal anlagen but the opening of the
glottis has not yet perforated in these larval
stages. Even the advanced stage 41 larva of
L. rheocola has still no discernible glottis
opening, although the lung sacks were in a
more advanced stage than that of the
L. nannotis specimen. Boophis sp. (stage 37)
and Hyla armata (stage 36) larvae differ
from the pelodryadine suctorial larvae in
having relatively large lungs and an open
glottis orifices. We assume that their lungs
are functional and used throughout larval
life.
A full description of skeletal and muscular
features of the head is given for Litoria geni-
maculata. Other species are described only
in those features that differ from L. geni-
maculata.
Anatomy of Litoria genimaculata
Neurocranium and first visceral arch (Figs.
3, 4)
The cartilago labialis superior is com-
posed of a pars alaris (lateral wing) and a
pars corporis (frontal bar). The distal ends of
the partes corpores fuse medially. The pars
alaris is a smooth triangular plate that bears
a lateral process near its articulation with
the cornu trabeculae. It is synchondrotically
connected proximally (but not distally) with
the pars corporis. The articulation of the
upper jaw with the cornua trabeculae is
mainly by the pars alaris. Viewed ventrally,
the partes of the cartilago labialis superior
form a simple arch (Fig. 4b). An adrostral
chondrification is absent. The cornua tra-
beculae are the anterior extensions of the
 CRANIAL MORPHOLOGY OF SUCTORIAL TADPOLES
Fig. 2. Litoria nannotis, Nyctimystes dayi, L. xan-
thomera, and L. genimaculata. Oral disks and body
shapes in comparisons. Two suctorial (above) and two
pond-type pelodryadine larvae (below). Note the ventral
trabeculae cranii of the cranial floor. These
relatively slender, diverging bars possess a
lateral process near their proximal base and
articulate distally with the cartilagines labia-
les superiores.
The cartilago meckeli has a sigmoid shape
and is transversely oriented. It bears a dor-
somedial, ventromedial, and retroarticular
process. The medial part of its anterior face
forms a shallow fossa for articulation with
the cartilago labialis inferior. The carti-
lagines labiales inferiores form a U-shaped
arch in anterior view. They are connected
medially by a synchondrotic symphysis. The
cartilago meckeli and cartilago labialis infe-
rior are connected by the commissura intra-
mandibularis and the ligamentum intraman-
dibularis. The ligamentum lies parallel and
anterior to the commissura.
The roof of the braincase is incomplete
and formed by the tectum synoticum and the
taeniae tecti transversalis, medialis, and
marginalis. Fenestrae parietales are pres-
ent at least until stage 41. The septum nasi
and the taeniae ethmoidales develop well
before metamorphosis. The crista parotica is
almost absent except for a small but distinct
processus posterolateralis that is well devel-
113
position of the large oral sucker, the broad snout, the
dorsoventrally compressed body, and reduced tail fin in
suctorial larvae.
oped in stages 36 and beyond. The cartilago
orbitalis is high even from as early as stages
30 on. The foramen trochleare is located
dorsal and posterior to the center of the
foramen opticum.
The processus muscularis quadrati rises
from the lateral margin of the palatoquad-
rate and ends with a blunt apex. The proces-
sus ethmoidalis is shorter than wide. The
processus pseudopterygoideus is a small pro-
tuberance in some specimens and absent in
others. There is no commissura quadratoor-
bitalis (i.e., a confluence between the tip of
the processus muscularis and the proximal
base of the commissura quadratocranialis
anterior), but a ligamentum tectum is found
in the equivalent position (Fig. 4). The larval
processus basalis between the palatoquad-
rate and otic capsule is absent in this
species, but the larval processus oticus is
present. The arcus subocularis of the palato-
quadrate is without prominent lateral projec-
tions. In cross section the arcus is oriented
horizontally. The suspensorium is intermedi-
ate (sensu Sokol, ‘81) in the position of its
attachment to the neurocranium. The maxi-
mum width of the neurocranium and palato-
 Fig. 3. Litoria genimaculata (KU 224671, stage 31),
Nyctimystes dayi (KU 224697, stage 30), L. xanthomera
(KU 224695, stage 37), and L. nannotis (KU 224678,
stage 25). Dorsal view of neurocranium and first visceral
arch. Litoria genimaculata and L. xanthomera (left)
have pond-type larvae; Nyctimystes dayi and L. nanno-
tis (right) have suctorial larvae. Drawings from cleared
and stained specimens. Note the anteriorly expanded
skulls, massive jaws, large adrostral cartilages, and
broad commissura quadratocranialis anterior of the suc-
torial larvae. ad, adrostral; aso, arcus subocularis qua-
drati; ca, capsula auditiva; cli, cartilago labialis inferior;
cls, cartilago labialis superior; cm, cartilago meckeli; co,
cartilago orbitalis; coc, condylus occipitalis; cqc, commis-
sura quadratocranialis anterior; ct, cornu trabeculae;
ex, exoccipital; fbc, fenestra basicranialis; fca, foramen
caroticum; fcp, foramen craniopalatinum; fj, foramen
jugulare; foc, foramen oculomotorium; fol, foramen olfac-
torium; fop, foramen opticum; fp, frontoparietal; fso,
fenestra subocularis; lon, lamina orbitonasalis; pa, pars
alaris of cartilago labialis superior; pac, processus acces-
sorius; pao, processus antorbitalis; paq, processus ascen-
dens quadrati; pc, pars corporis of cartilago labialis
superior; pe, processus ethmoidalis; plt, processus latera-
lis trabeculae; pm, processus muscularis; pot, processus
oticus; pp, processus pseudopterygoideus; ppl, processus
posterolateralis; pq, palatoquadrate; ps, parasphenoid;
sn, septum nasi; te, taenia ethmoidalis; ts, tectum synoti-
cum; ttm, taenia tecti medialis; ttmg, taenia tecti margin-
alis; ttt, taenia tecti transversalis.
 CRANIAL MORPHOLOGY OF SUCTORIAL TADPOLES
quadrate is at the level of the processus
ascendens.
Hyobranchial skeleton (Fig. 5)
The basihyale (⫽ copula anterior) is pres-
ent and embedded in the ligamentum inter-
hyoideum that spans the processus anteri-
ores of the ceratohyal. The ceratohyalia
articulate synchondrotically by the flexible
cartilage of the pars reuniens. The medial
part of the ceratohyal forms a horizontal
plate. It possesses a well-developed proces-
sus anterior, anterolateralis, and posterior.
Flexible cartilage connects the basibran-
chiale (⫽ copula posterior) to the pars reu-
niens anteriorly and the plana hypobranchia-
les posteriorly. The basibranchiale is short
and does not separate the plana hypobran-
chiales (i.e., the plana hypobranchiales meet
in the median plane). The basibranchiale
bears a processus urobranchialis posteroven-
trally. The ceratobranchiale I has a proces-
sus anterior branchialis. The ceratobran-
chiale I is broadly fused to the anterior part
of the planum hypobranchiale. The proximal
ends of the ceratobranchialia II and IV are
synchondrotically connected to the planum
hypobranchiale. All four ceratobranchialia
are bridged distally by commissurae termi-
nales. Proximal connections between the
ceratobranchialia, i.e. commissurae proxi-
males, are lacking. The proximal end of cera-
tobranchiale III closely approaches the pla-
num hypobranchiale, but does not fuse to it.
Ceratobranchialia II and III each have a
processus branchialis ventrally. The cerato-
branchialia bear rakerlike projections along
the gill slits (inconspicuous or absent in
young, but well developed in full grown lar-
vae). The spicula I–IV are present and long.
They originate as slender rods from the
proximal ends of the ceratobranchialia and
extend into the velum ventrale.
Musculature
The cranial musculature of Litoria geni-
maculata is summarized in Table 1. Gradwell
(‘72b) used electromyography to study the
function of the largest most accessible cra-
nial muscles of Rana catesbeiana larvae.
Although the function of the other cranial
muscles remains to some extent uncertain
and speculative, we include some informa-
tion about their suggested function in
Table 1.
The m. rectus abdominis and the epaxial
musculature do not belong to the cranial
musculature but need to be considered here
115
too, as will be obvious below. The m. rectus
abdominis of Litoria genimaculata is re-
stricted to the wall of the pleuroperitoneal
cavity. It does not reach beyond the origin of
the m. rectus cervicis anteriorly; rather, the
latter muscle can be considered an anterior
extension of the m. rectus abdominis. The
epaxial muscles along the dorsolateral sides
of the vertebral column insert on the poste-
rior cupula and wall of the canalis semicircu-
laris posterior of the otic capsule. The ramus
mandibularis (V) crosses between the mm.
levator mandibulae externus and subexter-
nus.
Features in which the other species differ
from Litoria genimaculata
Litoria caerulea
The differences from Litoria genimaculata
are few and subtle. The tectum parietale is
present in advanced stages (ⱖ38). It is the
result of a complete fusion of all tectal tae-
niae to form a closed roof anterior to tectum
synoticum, i.e., without fenestrae parietales.
The processus pseudopterygoideus is longer
than wide. The crista parotica and its proces-
sus posterolateralis are well developed. The
proximal ends of ceratobrachialia II and III
touch the planum hypobranchiale but do not
fuse to it. The rakerlike projections of the
ceratobranchialia are more conspicuous. The
commissura proximalis II is present; in some
individuals a vestigial commissura proxima-
lis III is present as well. The m. subarcualis
rectus II–IV extends to ceratobranchiale I.
Litoria xanthomera (Figs. 3, 5, 7)
Litoria xanthomera is most similar to
L. caerulea and differs slightly from L. geni-
maculata. The processus pseudopterygoi-
deus is approximately as long as wide. The
ceratobranchialia II and III are proximally
bridged by the commissura proximalis II.
The proximal ends of ceratobrachialia II and
III touch the planum hypobranchiale but do
not fuse to it. Rakerlike projections are more
conspicuous along the ceratobranchialia than
in L. genimaculata. In some individuals, the
m. subarcualis rectus II–IV reaches to cera-
tobranchiale I with a few fibers.
Litoria nannotis and L. rheocola
(Figs. 3, 5, 7–9, 11)
Both species are very similar and differ
from L. genimaculata in many features. The
partes corpores of the cartilago labialis supe-
rior are broadly fused into a large plate. The
 le cli pc
lms
lcq
mlmps ct
mlmpp pa
mlmal cm
mlmse
pq
mlme
lt pe
moh
pm
a cc

1 mm
pc cli msm
pa mmls
cm lcq
pra
msa

pq

b moh

mgh mim
cqc mmli mqa mha
fol
sn lt
pm
moh
cqc
mlmps
ct mlme

mlmse
mlmpp
mlmaa
msa
cm mha
pa lcq mlmal
cls
c pc cli
msm
mim

Figure 4
 CRANIAL MORPHOLOGY OF SUCTORIAL TADPOLES
Fig. 4. Litoria genimaculata (KU 224676, stage 37).
Three-dimensional reconstruction of the rostral region
in dorsal (a), ventral (b), and frontal (c,d) views. Liga-
ments and musculature were reconstructed on only one
side of the body. The fiber bundles of the m. mandibulola-
bialis have been cut. The muscular and skeletal composi-
tion, geometry, and structural interrelationships de-
picted here for L. genimaculata are typical for many
pond-type, neobatrachian tadpoles. cc, cavum cranii; cli,
cartilago labialis inferior; cls, cartilago labialis superior;
cm, cartilago meckeli; cqc, commissura quadratocrania-
lis anterior; ct, cornu trabeculae; fol, foramen olfacto-
rium; lcq, ligamentum cornuquadratum; le, ligamentum
ethmoidale; lms, ligamentum mandibulosuprarostrale;
lt, ligamentum tectum; mgh, m. geniohyoideus; mha, m.
lateral part of the pars corporis plate char-
acteristically curves posteriorly and lies
parallel to the pars alaris (concentric ar-
rangement). Thus, posterior ends of the kera-
tinized jaw sheath are also located medial to
the pars alaris. The pars alaris is fused with
the lateral part of the pars corporis plate by
a posterior and a anterior confluence (Fig.
9a). A ligament connects the ventral side of
the distal cornu trabeculae to the dorsal
margin of the pars corporis. The cornua tra-
beculae are extremely wide anteriorly and
117
hyoangularis; mim, m. intermandibularis; mlmaa, m.
levator mandibulae anterior articularis; mlmal, m. leva-
tor mandibulae anterior lateralis; mlme, m. levator man-
dibulae externus; mlmpp, m. levator mandibulae poste-
rior profundus; mlmps, m. levator mandibulae posterior
superficialis; mlmse, m. levator mandibulae subexter-
nus; mmli, mandibulolabialis inferior; mmls, m. man-
dibulolabialis superior; moh, m. orbitohyoideus; mqa, m.
quadratoangularis; msa, m. suspensorioangularis; msm,
m. submentalis; pa, pars alaris of cartilago labialis supe-
rior; pc, pars corporis of cartilago labialis superior; pe,
processus ethmoidalis; pm, processus muscularis; pq,
palatoquadrate; pra, processus retroarticularis; sn, sep-
tum nasi.
have a wide transversely oriented synchon-
drotic articulation with the cartilagines la-
biales superiores. The adrostral cartilage is
large, and without cartilaginous connections
to other elements. The anteroventral tip of
the adrostral cartilage is connected to the
lateral face of the cartilago labialis superior
(pars alaris) by collagen fiber-rich tissue.
The posterodorsal tip of the adrostral carti-
lage is attached to the processus dorsomedia-
lis of the cartilago meckeli by dense collagen
fibers.
Figure 5
 CRANIAL MORPHOLOGY OF SUCTORIAL TADPOLES
The cartilago meckeli is large and stout.
The maximum width of the chondrocranium
is at the level of the anterior base of the
processus muscularis. The arcus subocu-
laris is inclined; its lateral margin is below
the level of the medial margin in cross sec-
tion. The apex of the processus muscularis
bears a medial projection. A conspicuous pro-
cessus ventralis projects from the anterolat-
eral base of the processus muscularis (less
pronounced in early than in late larval
stages). The processus pseudopterygoideus
is absent and the commissura quadratocra-
nialis anterior is very broad. The posterior
palatoquadrate is fused to the floor of the
otic capsule forming larval processus basalis
in Litoria nannotis; it is close to the floor of
the otic capsule but not fused to it in
L. rheocola (serially sectioned specimen; Fig.
11). The basihyale is lacking in our speci-
mens of L. nannotis, but present in L. rheo-
cola.
The ramus mandibularis (V) crosses the
m. levator mandibulae externus dorsally. The
m. levator mandibulae anterior lateralis in-
serts in connective tissue close to the dorsal
end of the adrostral cartilage. Some fibers of
the m. levator mandibulae posterior origi-
nate from the lateral wall of the braincase
anterior to the attachment of the processus
ascendens. The epaxial musculature inserts
on the anterior third of the otic capsule. The
m. rectus cervicis crosses the m. diaphragma-
tobranchialis dorsally near its origin. The
m. rectus abdominis extends far anteriorly
beyond the origin of the m. rectus cervicis.
Thus the m. rectus abdominis underlies the
branchial basket up to the level of the gill
slit between ceratobranchiale I and II. The
Fig. 5. Litoria genimaculata, Nyctimystes dayi,
L. xanthomera, and L. nannotis. Larval hyobranchial
skeleton drawn from cleared and stained specimens in
dorsal view. Species with suctorial larvae right (N. dayi,
KU 224697, stage 30; L. nannotis; KU 224678, stage 25),
pond-type larvae left (L. genimaculata, KU 224671, stage
31; L. xanthomera, KU 224694, stage 37). It is obvious
that the suctorial species have relatively small bran-
chial baskets and large ceratohyal areas (see also Fig.
13). Presence of well-developed spicula, a short basibran-
chial element, and plana hypobranchiales that meet in
the midline are common features of neobatrachian lar-
vae. bb, basibranchiale; bh, basihyale; con, condylus
articularis; cb, ceratobranchiale; cte, commissura termi-
nalis; pab, processus anterior branchialis; pah, proces-
sus anterior hyalis; pal, processus anterolateralis; pl,
processus lateralis of ceratohyal; plh, planum hypobran-
chiale; pph, processus posterior hyalis; pr, pars reu-
niens; sp, spiculum.
119
muscle inserts in a tissue sheath rich in
collagen fibers that stretches between the
ceratohyal and the oral sucker and connects
to the palatoquadrate.
Nyctimystes dayi (Figs. 3, 5, 7)
There are marked differences to Litoria
genimaculata. In Nyctimystes dayi, the
partes corpores of the cartilago labialis supe-
rior are fused and form a broad plate. The
lateral part of the pars corporis plate charac-
teristically curves posteriorly and lies paral-
lel to the pars alaris (concentric arrange-
ment). Thus, the posterior ends of the
keratinized jaw sheath are located medial to
the pars alaris. The pars alaris is broadly
fused to the pars corporis plate; a ventral
sulcus (for the jaw sheath) indicates the
position of the border between the fused
elements. The cornu trabeculae has a wide
transverse synchondrotic articulation of flex-
ible cartilage with the cartilago labialis supe-
rior. A large adrostral cartilage is present. It
is attached to the posterior end of the carti-
lago labialis superior (pars alaris) by a rod of
flexible cartilage.
The cartilago meckeli is robust and has an
accessory process projecting from its ante-
rior face. This process presumably guides
the movement of the adrostral cartilage dur-
ing jaw rotations. The cornua trabeculae are
extremely wide anteriorly and fused medi-
ally along most of their length.
The maximum width of the chondrocra-
nium is at the level of the anterior base of
the processus muscularis. The arcus subocu-
laris is inclined in cross section; its lateral
margin lies below the level of the medial
margin. A conspicuous processus ventralis
projects from the anterolateral base of the
processus muscularis. There is no processus
pseudopterygoideus. The commissura quad-
ratocranialis anterior is very broad. The
palatoquadrate forms a larval processus ba-
salis with the otic capsule.
The basihyale is lacking. The proximal
ends of ceratobranchiale II and III are fused
to the planum hypobranchiale. The commis-
sura proximalis II is present. Parts of the
m. levator mandibulae posterior originate
from the cartilago orbitalis anterior to the
attachment of the processus ascendens. The
ramus mandibularis (V) crosses ventral to
the m. levator mandibulae subexternus. The
m. levator mandibulae anterior originates
from posterior parts of the planum basale,
some fibers even attaching to the ventral
side of vertebra I. The m. subarcualis II–IV
120 A. HAAS AND S.J. RICHARDS
Fig. 6. Litoria genimaculata (KU 224676, stage 37).
Three-dimensional reconstruction of the rostral region
with mandibular musculature in camera view (virtual
lens with 50-mm focal length). The view from a dorsolat-
eral position clearly shows the spatial interrelationships
of the jaw adductor muscles. Note the thin m. levator
mandibulae anterior lateralis and the typical crossing
orientation of the m. levator mandibulae externus. Both
muscles are absent in larvae of some anurans (Haas,
‘96a). Their function is unclear. Note also the ligamen-
tous connection (lms) between the cartilago meckeli and
the pars alaris of the cartilago labialis superior. The
ligamentum mandibulosuprarostrale couples both carti-
lages mechanically. It pulls down the posterior tip of the
upper jaw when the cartilago meckeli rotates ventrad
inserts on ceratobranchiale I. The epaxial
musculature reaches anteriorly onto the an-
terior third of the otic capsule. The m. rectus
cervicis reaches the processus branchialis
III on only one side of the body with less
than six fibers in the serially sectioned speci-
men. In the manually dissected specimen,
no attachment of this muscle to the proces-
sus branchialis III was found. The m. rectus
cervicis crosses the m. diaphragmatobran-
chialis ventrally near its origin. The m. rec-
tus abdominis extends far anteriorly beyond
the origin of the m. rectus cervicis. The m.
rectus abdominis underlies the branchial
basket up to the level of the posterior end of
the processus lateralis hyalis. The muscle
inserts in a tissue sheath rich in collagen
fibers that spans between ceratohyale and
oral sucker and that has connections to the
palatoquadrate.
(abduction). The fiber bundles of the m. mandibulolabia-
lis have been cut. cli, cartilago labialis inferior; cm,
cartilago meckeli; ct, cornu trabeculae; lcq, ligamentum
cornuquadratum; le, ligamentum ethmoidale; lms, liga-
mentum mandibulosuprarostrale; mha, m. hyoangula-
ris; mlmaa, m. levator mandibulae anterior articularis;
mlmal, m. levator mandibulae anterior lateralis; mlme,
m. levator mandibulae externus; mlmpp, m. levator
mandibulae posterior profundus; mlmps, m. levator man-
dibulae posterior superficialis; mlmse, m. levator man-
dibulae subexternus; mmli, mandibulolabialis inferior;
mmls, m. mandibulolabialis superior; mqa, m. quadra-
toangularis; msa, m. suspensorioangularis; pa, pars
alaris of cartilago labialis superior; pm, processus mus-
cularis; pq, palatoquadrate.
Hyla armata
The partes corpores and alares are fully
fused and form a broad plate. The cornua
trabeculae are broadly extended anteriorly
and fused medially along their entire length.
A wide transverse synchondrotic articula-
tion of flexible cartilage exists between the
cornu trabeculae and the cartilago labialis
superior. The lower jaw is robust. A well-
developed processus ventralis quadrati is
present, but the processus pseudopterygoi-
deus is absent. The commissura quadrato-
cranialis anterior is very broad. There is
approximately the same width of the chon-
drocranium at the level of the anterior base
of the processus muscularis and the level of
the arcus subocularis. The tectum parietale
is present; i.e., the fenestrae parietales are
closed. The nervus trochlearis leaves the-
 CRANIAL MORPHOLOGY OF SUCTORIAL TADPOLES 121
TABLE 1. Larval cranial musculature of Litoria genimaculata1
Muscle Origin Insertion Comment
n. trigeminus (c.n. V)
m. submentalis Posteroventral side of carti- Median raphe Function unknown in
lago labialis inferior larvae; m. intermandibu-
laris anterior of Edge-
worth (’35)
m. intermandibularis Ventral side of cartilago Median raphe Broad, flat U-shaped band
meckeli of fibers, probably lifting
the floor of the anterior
buccal cavity; m. inter-
mandibularis posterior of
Edgeworth (’35)
m. levator mandibulae Ventral side of processus With long tendon on lateral Lower jaw adductor
anterior ascendens and anterior face of cartilago meckeli
cupula of otic capsule,
extending with few fibers
on anteriormost lateral
margin of planum basale
m. levator mandibulae Base of medial side of pro- Dorsolateral face of carti- Lower jaw adductor
anterior articularis cessus muscularis lago meckeli
m. levator mandibulae Anterolateral corner of pars Connective tissue sur- Very thin, cylindrical
anterior lateralis articularis quadrati rounding processus pos- bundle of fibers with
terodorsalis of pars alaris unknown function;
(cartilago labialis supe- absence in larval stages
rior) of some anuran taxa
(Haas, ’96a) may be the
primitive condition
m. levator mandibulae Anterior part of medial side Joining tendon of m. Thin muscle of unknown
externus of processus muscularis levator mandibulae pro- function; absent in some
quadrati fundus superficialis and anuran taxa (Haas, ’96a)
inserting on processus
dorsomedialis of cartilago
meckeli
m. levator mandibulae Anterior part of medial side Posteroventral margin of Upper jaw adductor
subexternus of processus muscularis pars alaris (cartilago
quadrati labialis superior) by a
common tendon with m.
levator mandibulae pos-
terior profundus
m. levator mandibulae Posterior part of palato- Processus dorsomedialis of Lower jaw adductor
posterior superficialis quadrate and processus cartilago meckeli
ascendens
m. levator mandibulae Posterior part of palato- Posteroventral margin of Upper jaw adductor
posterior profundus quadrate pars alaris (cartilago
labialis superior)
m. mandibulolabialis Ventromedial aspect of car- Two major streams (infe- Acting on base of kera-
tilago meckeli rior and superior) of loose todont rows and on orien-
fiber bundles invading tation of keratodonts
lower oral disk and lat- (Carr and Altig, ’91;
eral parts of upper oral Taylor et al., ’96); absent
disk, respectively in Ascaphus truei
n. facialis (c.n. VII)
m. interhyoideus Ventral margin of pro- Median raphe Elevates buccal floor;
cessus lateralis hyalis antagonistic to the m.
orbitohyoideus in the
buccal pump mechanism
m. interhyoideus poste- Soft tissue of operculum Soft tissue of operculum Layer of very loose fibers
rior immediately ventral to
the cavum peribran-
chiale and with more or
less transverse orienta-
tion, possibly able to
compress the cavum
(auxiliary force pump);
muscle missing in some
anuran species (Haas,
’96a, ’97); m. constrictor
colli of Edgeworth (’35)
122 A. HAAS AND S.J. RICHARDS

TABLE 1. (continued)
Muscle Origin Insertion Comment
m. hyoangularis Ceratohyal lateral to con- Processus retroarticularis Jaw abductor (normal
dylus articularis of cartilago meckeli inspiration cycle); absent
in Ascaphus and Disco-
glossus
m. quadratoangularis Ventral surface of the pala- Processus retroarticularis Jaw abductor (normal
toquadrate anterior to of cartilago meckeli inspiration cycle)
ceratohyal articulation
m. suspensorioangularis Lateral side of processus Processus retroarticularis Jaw abductor (hyperinspi-
muscularis, along its pos- of cartilago meckeli ration); flat, fan-shaped
terior margin muscle lying medial to
the m. suspensoriohyoi-
deus and m. orbitohyoi-
deus
m. orbitohyoideus Lateral side of processus Lateral face of processus Major muscle powering the
muscularis lateralis hyalis downward movement of
the buccal floor in the
buccal pump mechanism
(Gradwell, ’72b; Wass-
ersug and Hoff, ’79);
antagonist to the m.
interhyoideus
m. suspensoriohyoideus Lateral side of processus Tip of processus lateralis Flat, fan-shaped muscle
muscularis, along its pos- hyalis, medial to m. orbi- lying medial to the m.
terior margin tohyoideus orbitohyoideus and lat-
eral to m. suspensorioan-
gularis; function uncer-
tain.
n. glossopharyngeus (c.n.
IX)
m. constrictor branchialis Absent Absent Among anurans, this
I muscle is exclusively
known from Ascaphus
truei, Alytes, Bombina,
and Discoglossus frogs
(Haas, ’97); function
uncertain
m. levator arcuum bran- Lateral margin of arcus Distal ceratobranchiale I Broad, thin ribbon of fibers;
chialium I subocularis quadrati lifting the branchial
arch, thus, compressing
the branchial chamber
and pressing water into
the peribranchial cavity
m. subarcualis rectus I Lateral base of processus Dorsal bundle of fibers Links ceratohyal to bran-
posterior hyalis inserting on proximal chial basket; assists
part of ceratobranchiale, anteromediad movement
two ventral bundles of branchial basket
inserting on proximal during buccal floor eleva-
ceratobranchialia II and tion
III, respectively
n. vagus (c.n. X)
m. constrictor branchialis Processus branchialis II Commissura terminalis I Muscle in the soft tissue of
II the branchial septum,
regulates water flow
through the gill slit
m. constrictor branchialis Processus branchialis II Commissura terminalis II (See m. constrictor bran-
III chialis II)
m. constrictor branchialis Proximal ceratobranchiale Commissura terminalis III (See m. constrictor bran-
IV III chialis II)
m. diaphragmatobran- Wall of peritoneal cavity Dorsal extension of distal Antagonistic to the m.
chialis ceratobranchiale III levator arcuum branchi-
alium, lowering the bran-
chial basket
m. levator arcuum bran- Processus oticus Commissura terminalis I (See m. levator arcuum
chialium II branchialium I)

Muscle
m. levator arcuum bran-
chialium III
m. levator arcuum bran-
chialium IV
m. subarcualis obliquus
II
m. subarcualis obliquus
IV
m. subarcualis rectus
II–IV
m. tympanopharyngeus
m. dilatator laryngis
m. constrictor laryngis
n. hypoglossus (s.n. II)
m. geniohyoideus
m. rectus cervicis
c.n., cranial nerve; s.n., spinal nerve.
1Muscles were grouped according to their innervation, following the scheme of Schlosser and Roth (’95). The terminology of Edgeworth
(’35) was modified as suggested by Schlosser and Roth (’95) and Haas (’97). Some comments on function are provided, although there is
a dearth of information on muscular activation patterns (electromyography) in tadpoles. The most comprehensive experimental work
has been done by Gradwell (’68, ’72). His functional suggestions are adopted herein. The function of some muscles is speculative and
may change depending on synchronous activation of other muscles.
CRANIAL MORPHOLOGY OF SUCTORIAL TADPOLES 123
TABLE 1. (continued)
Origin Insertion Comment
Lateral capsula auditiva Commissura terminalis II (See m. levator arcuum
(wall of canalis semicir- branchialium I)
cularis lateralis and
neighboring connective
tissue)
Posterolateral capsula Commissura terminalis III (See m. levator arcuum
auditiva (wall of canalis and ceratobranchiale IV, branchialium I)
semicircularis lateralis) fibers extending into
posterior to m. levator septum branchiale IV,
arcuum branchialium III and pharyngeal tissue
medial to ceratobran-
chiale IV
Fan-shaped origin from Processus urobranchialis Moves proximal ceratobra-
both processus bran- chialia anteromesiad
chiales II and III during buccal floor eleva-
tion; m. transversus ven-
tralis II of Edgeworth
(’35)
Absent Absent Exclusively known for
Ascaphus truei
Ventromedial face of cera- Processus branchialis II Fibers of muscle reaching
tobranchiale IV ceratobranchiale I on one
side of the body in one
individual of Litoria geni-
maculata; function
uncertain but see m.
subarc. rectus I
Absent Absent In Litoria genimaculata, no
bundle of fibers is clearly
separate from m. lev. arc.
branch. IV
Connective tissue below Cartilago arytaenoidea Fibers run from posterolat-
otic capsule and lateral eral to anteromedial in
to esophagus ventral view; opener of
the glottis
Connective tissue pos- Connective tissue antero- Muscle forming a loop
terodorsal to cartilago ventral to cartilago ary- around the cartilago ary-
arytaenoidea taenoidea taenoidea; closes glottis
orifice
Ventral side of planum Ventral face of medial part Having insertion and origin
hypobranchiale of cartilago labialis infe-on two highly moveable
rior elements may cause pro-
found changes in func-
tion depending on syn-
chronous activity of other
muscles; it possibly has a
role in the jaw opening
mechanism (hyperinspi-
ration)
Wall of peritoneal cavity Mainly on processus bran- Lowering and retracting
medial to m. diaphrag- chialis III, but some the branchial basket
matobranchialis fibers attaching to medial during buccal floor
side of proximal cerato- depression
branchiale IV and con-
nective tissue between
ceratobranchialia III and
IV
Figure 7
 CRANIAL MORPHOLOGY OF SUCTORIAL TADPOLES
cavum cranii through the foramen opticum.
The tip of the processus posterior hyalis
underlies the anterolateral part of the pla-
num hypobranchiale and is attached to it by
a ligament and a synchondrotic connection.
The commissura proximalis II is absent, but
III is present. The ceratobranchialia II–IV
do not fuse to the planum hypobranchiale
(syndesmotic connection). The origin of the
m. levator mandibulae posterior superficia-
lis extends medially to the very base of the
processus ascendens. Fibers of the dorsal
part of the m. mandibulolabialis invade the
dorsal lip far medially. The ramus mandibu-
laris (V) crosses dorsal to the mm. levator
mandibulae externus and subexternus. The
insertion of the epaxial musculature spreads
to the anterior third of the otic capsule. The
m. rectus abdominis extends anteriorly be-
yond the origin of the m. rectus cervicis and
underlies the branchial basket up to the
level of the posterior end of the processus
lateralis hyalis. The muscle inserts in a tis-
sue sheath rich in collagen fibers that
stretches between the ceratohyale and the
oral sucker.
Boophis sp. (Fig. 10)
The Boophis specimens combine the most
deviating features compared with L. geni-
maculata. The partes corpores and alares
are fully fused and form a broad plate. The
posterior process of the pars alaris is con-
Fig. 7. Schematic representations of the larval hyo-
branchial structures (skeleton left, skeleton plus muscles
right for each species) of four pelodryadine species. Ven-
tral views of the right body side. Species with pond-type
larvae are grouped to the left (Litoria genimaculata,
L. xanthomera), species with suctorial larvae to the
right (Nyctimystes dayi, L. nannotis). Muscles are repre-
sented by black lines; cartilages are drawn in gray. Only
topologic relations are depicted. Size differences, propor-
tions, and muscle diameters are neglected. The m. inter-
hyoideus posterior is not shown, because it is a diffuse
layer of fibers in the operculum underlying the bran-
chial basket. Note that despite their very different hab-
its and behavior, suctorial tadpoles differ consistently
from pond-type larvae in only one subtle feature in
hyobranchial musculoskeletal topology: m. rectus cervi-
cis and m. diaphragmatobranchialis cross at their ori-
gins. In general, high conservatism of the patterns are
evident. bb, basibranchiale; cb, ceratobranchiale; ch,
ceratohyal; cp, commissura proximalis; cte, commissura
terminalis; mcbr, m. constrictor branchialis; mdbr, m.
diaphragmatobranchialis; mgh, m. geniohyoideus; mih,
m. interhyoideus; mlab, m. levator arcuum branchi-
alium; mrc, m. rectus cervicis; msao, m. subarcualis
obliquus; msar, m. subarcualis rectus; plh, planum hypo-
branchiale; pbr, processus branchialis; pr, pars reu-
niens.
125
spicuously extended dorsally. The plate of
the cartilago labialis superior possesses ven-
trolateral projections that support the lat-
eral parts of the keratinized jaw sheath. The
cartilago labialis inferior is wide and has a
flat anterior edge. The cornua trabeculae
are very wide anteriorly and are fused medi-
ally for approximately one-third to one-half
their length.
A processus ventralis quadrati is present
but small. The anterolateral corner of palato-
quadrate extends conspicuously anteriorly.
The processus pseudopterygoideus is lack-
ing. The chondrocranium has approximately
the same width at the level of the anterior
base of the processus muscularis and the
level of the arcus subocularis. The palato-
quadrate is connected to the otic capsule
floor by dense collagen fibers (ligamentum
oticum). A larval processus basalis is not
formed. The commissura quadratocranialis
anterior is very broad. The processus oticus
has a small but distinct posterolateral protu-
berance. The processus ascendens is thin
and, in the cleared and stained specimen,
does not attach to the pila antotica on one
side of the body.
The development of the septum nasi is
delayed and this structure is lacking in the
two large specimens studied. The taeniae
tecti transversalis is absent and the taenia
tecti medialis vestigial. The sidewalls of the
braincase are largely membranous (even at
stage 37), but a dorsal taenia tecti margin-
alis is present. The foramen opticum is large
and the nervus trochlearis leaves the cavum
cranii through the foramen opticum.
The commissurae proximales are lacking.
The ceratobranchialia II and III are con-
nected to the planum hypobranchiale by liga-
ments; the ceratobranchiale IV, however, is
fused to the planum. Spiculum I is absent,
but spicula II–IV are present. Spiculum III
is separate from ceratobranchiale III and
originates instead from the lateral margin of
the planum hypobranchiale. Lateral projec-
tions (rakers) of ceratobranchialia II–IV are
tiny or missing. A filter epithelium on the
branchial arches is absent.
The m. levator mandibulae anterior latera-
lis is absent. The ramus mandibularis (V)
crosses ventral to the m. levator mandibulae
subexternus. The origin of the m. levator
mandibulae anterior covers parts of the pla-
num basale, parasphenoid, and floor of the
otic capsule; some fibers originate as far
Figure 8
 CRANIAL MORPHOLOGY OF SUCTORIAL TADPOLES
posteriorly as the occipital region. Boophis
sp. is the only species in the sample that
possesses a m. tympanopharyngeus. It origi-
nates immediately medial to the m. levator
arcuum branchialium IV, diverges from the
latter medially, and closely approaches its
counterpart anterior to the glottis (not to be
confused with the m. dilatator laryngis that
is posterior to it). Both mm. tympanopharyn-
gei are connected by a sheath of dense colla-
gen fibers. These muscles are surprisingly
well developed and composed of 8–10 layers
of thick fibers in cross section.
The epaxial musculature extends anteri-
orly up to the anterior third of the otic cap-
sule. The m. rectus abdominis attaches far
anteriorly beyond the origin of the m. rectus
cervicis. The m. rectus abdominis underlies
the branchial basket to the level of the poste-
rior end of the processus lateralis hyalis.
The muscle inserts in the tissue sheath rich
in collagen fibers that stretches between the
ceratohyale and the oral sucker and that has
connections to the palatoquadrate.
Morphometry
Figure 12 shows the 17 landmarks that
we used to define and record areas and angles
of the hyobranchial skeleton. Partial areas
were transformed to relative values by divid-
ing each by total area to make size-indepen-
dent comparisons among taxa. Mean values
of measurements are given in Table 2. The
relative branchial area is consistently
Fig. 8. Litoria nannotis (KU 224681, stage 26/27).
Three-dimensional reconstruction of the rostral region
in dorsal (a), ventral (b), and frontal (c) views. Note the
anteriorly broadened cornu trabeculae, the large adros-
tral cartilage, and the robust cartilago meckeli of this
suctorial larva. The reconstruction was done because
details of the jaws could not be described precisely in
cleared and stained preparations. The configuration of
the cartilago labialis superior is shared with L. rheocola
and Nyctimystes dayi and is unique and the most com-
plex in shape within the Anura. The pars corporis forms
a broad plate. Its lateral part extends substantially
posteriorly, medial to the pars alaris. The keratinized
jaw sheath (not shown) is supported by the pars corporis
plate. There is a clear gap between pars corporis and
pars alaris in L. nannotis and L. rheocola. This gap has
almost disappeared in N. dayi owing to more extensive
fusion of the parts. ad, adrostral; cc, cavum cranii; cli,
cartilago labialis inferior; cls, cartilago labialis superior;
cm, cartilago meckeli; ct, cornu trabeculae; fol, foramen
olfactorium; pa, pars alaris of cartilago labialis superior;
pao, processus antorbitalis; pc, pars corporis of cartilago
labialis superior; pm, processus muscularis; pq, palato-
quadrate; pra, processus retroarticularis; ps, parasphe-
noid; pta, planum trabeculare anticum; pv, processus
ventralis; sn, septum nasi.
127
smaller and the relative ceratohyal area is
larger in suctorial larvae than in nonsucto-
rial larvae. Among the suctorial larvae, the
values for Litoria rheocola are closest to the
nonsuctorial sample and those of Nyctimy-
stes dayi most different from them.
DISCUSSION
Structure of the cranium
and its musculature
The anteriorly expanded chondrocranium
is the internal structural support of the ex-
panded rostral region. In most suctorial lar-
vae, the greatest width of the neurocranium
plus first visceral arch is at the level of the
jaw articulation, whereas in pond-type lar-
vae the maximum width is at the level of the
posterior palatoquadrate (Sokol, ‘81; Fab-
rezi and Lavilla, ‘92; Haas, ‘95, ‘96a).
Heleophryne spp. and Boophis sp. larvae dif-
fer from the pelodryadine suctorial larvae in
that their palatoquadrate is as broad poste-
riorly as anteriorly, and the width of the
skull is about the same at the jaw articula-
tion and the posterior part of the palatoquad-
rate (van der Westhuizen, ‘61). The cornua
trabeculae of neobatrachian suctorial larvae
are expanded distally (Figs. 3, 8, 10). In
some of the species they are fused medially
along most or all of their length (e.g.,
Heleophryne spp., Hyla armata, and Nycti-
mystes dayi). The cornua do not reach the
anterior tip of the animal; gelatinous (in
preserved specimens) mesenchyme and lym-
phatic canals fill the most anterior snout
parts and may facilitate an intimate sucker–
substrate contact (Gradwell, ‘73). A different
constructional design of the rostral region
can be found in Ascaphus truei; the cornua
are short, not expanded significantly, and
bent ventrally (Pusey, ‘43).
The configurations of the cartilagines la-
biales superiores (partes alares and cor-
pores) of Litoria caerulea, L. xanthomera,
and L. genimaculata (Fig. 4b–c) resemble
those of other hylid species that have pond-
type larvae (de Sá, ‘88; Fabrezi and Lavilla,
‘92; Haas, ‘96a). The cartilago labialis supe-
rior consists of two lateral wings (partes
alares) that proximally touch or are conflu-
ent with two slender, medial bars (partes
corpores). The latter are fused distally in the
species of Litoria. This structural pattern
has also been described in dendrobatid spe-
cies (Haas, ‘95), Rhinoderma (Lavilla, ‘87),
telmatobiine leptodactylids (Fabrezi and
Lavilla, ‘93), and bufonids (Sedra, ‘50; Haas,
‘96a). Because the configuration of the carti-
Figure 9
 CRANIAL MORPHOLOGY OF SUCTORIAL TADPOLES
lago labialis superior found in nonsuctorial
species of Litoria is widespread in hylid frogs
outside the Pelodryadinae, it can be as-
sumed that this feature is plesiomorphic in
the Australian species studied. The modifica-
tion of the upper jaw cartilages in suctorial
larval L. nannotis, L. rheocola, and N. dayi,
however, is strikingly different from that of
the other species of Litoria examined (Figs.
8b–c, 9), and might be derived from the
plesiomorphic condition. In all three species,
the partes corpores are broadly fused and
form a transverse plate that curves back-
ward laterally. This lateral part of the pars
corporis is approximately parallel to the pars
alaris (Fig. 8b). A deep gap between the pars
alaris and the pars corporis plate is retained
in L. nannotis and L. rheocola and the ele-
ments are only connected by an anterior and
a posterior confluence (Fig. 9a). In N. dayi,
the elements are broadly fused; thus, the
gap is reduced to a ventral sulcus. In all
three suctorial species, the keratinized jaw
sheath is solely supported by the pars cor-
poris.
The lower jaw of the suctorial tadpoles
examined does not deviate in structure from
that of other neobatrachian species (Sedra,
‘50; de Jongh, ‘68; Sokol, ‘81; de Sá, ‘88;
Haas, ‘95; Haas, ‘96a,b). The cartilago meck-
Fig. 9. Litoria nannotis (KU 224681, stage 26/27).
Three-dimensional reconstruction of the rostral region.
a: Camera view (virtual 50 mm lens) of the isolated jaw
cartilages. Three-dimensional scale bar, paramedial
plane with rostral and dorsal orientation arrows. It is
the most complex jaw apparatus known for tadpoles.
The view shows the two fusions (thick arrows) between
the pars alaris and pars corporis (also found in L. rheo-
cola, but completely fused along that line in Nyctimystes
dayi). b,c: Lateral views of the complete reconstruction.
An inverse kinematics model, involving five joints (b,
lines and circles), was applied to the reconstructed geom-
etry of the jaw cartilages to simulate the jaw-opening
mechanism. The abduction of the jaws is driven by the
outward rotation of the cartilago meckeli (b, right ar-
row). The adrostral cartilage is attached to both the
cartilago meckeli and the pars alaris (cartilago labialis
superior) by ligaments (not visible). The proximal adros-
tral follows the cartilago meckeli rotation and acts as a
pushing-rod on the upper jaw, which is opened indi-
rectly, i.e., without an abductor muscle inserting on it.
There are no mechanical conflicts in this model; how-
ever, the exact extent of upper jaw abduction in living
animals is not yet known. ad, adrostral; cim, commis-
sura intramandibularis; cli, cartilago labialis inferior;
cm, cartilago meckeli; ct, cornu trabeculae; fa, facies
articularis; fol, foramen olfactorium; pa, pars alaris of
cartilago labialis superior; pc, pars corporis of cartilago
labialis superior; plt, processus lateralis trabeculae; pm,
processus muscularis; pra, processus retroarticularis;
sn, septum nasi.
129
eli has a complex shape and is transversely
oriented (Figs. 8, 9). In suctorial pelodrya-
dines the cartilages of the lower jaw are
massive, robust structures. Nyctimystes dayi
differs from the other pelodryadine species
in that its cartilago meckeli forms a distinct
processus accessorius (Fig. 3) that seems to
prevent lateral movements of the adrostral
cartilage during jaw opening and closing.
Some derived neotropical hylid taxa de-
velop the anterior braincase walls and the
septum nasi late in their larval life or just at
metamorphosis (Haas, ‘96a ). This was also
found in the rhacophorid Boophis sp., but
not in the Australian hylid taxa studied. In
all stages examined, and independent of size,
a well-developed septum nasi and well-
developed lateral walls of the braincase (car-
tilago orbitalis) are present in pelodryadine
larvae. The cartilaginous roof of the brain-
case is composed of the tectum synoticum,
taenia tecti transversalis, and taenia tecti
medialis in larval stages close to metamor-
phosis. At least in L. caerulea, the fenestrae
parietales between the taeniae disappear
before metamorphosis, and a closed roof (tec-
tum parietale) is formed anterior to, and
confluent with, the tectum synoticum. We
could not examine metamorphic stages of
the other Australian species and hence do
not know if a tectum parietale forms later in
ontogeny. The tectum parietale was de-
scribed for a variety species of the hylid
subgroups Hylinae and Hemiphractinae
(Haas, ‘96a). The presence of the tectum
parietale presumably is plesiomorphic in the
Hylidae. It is present in Hyla armata. Exten-
sive tectal chondrifications and closed roofs
also were reported for representatives of the
‘‘Leptodactylidae’’ (Reinbach, ‘39; Wild, ‘97).
The parietal tectal cartilages are partly ab-
sent or vestigial in Heleophryne spp. and
Boophis sp.
The palatoquadrates of the pelodryadine
species consistently lack a commissura
quadrato-orbitalis. This commissura was
described for species of the genus Bufo (Bu-
fonidae), Caudiverbera (‘‘Leptodactylidae’’),
Gastrotheca (Hylidae), Leptodactylus (‘‘Lep-
todactylidae’’), Pleurodema (‘‘Leptodactyli-
dae’’), and Pelodytes (Pelodytidae) (Rein-
bach, ‘39; Barry, ‘56; Sokol, ‘81; Haas, ‘96a).
The functional significance of having a com-
missura quadrato-orbitalis instead of a liga-
mentum tectum is unclear.
One of the most characteristic features of
the palatoquadrate in suctorial tadpoles is
130 A. HAAS AND S.J. RICHARDS
Fig. 10. Boophis sp. KU 224700. a: Chondrocranium,
dorsal view. b: Ventral view. c: Hyobranchial skeleton,
dorsal view. Drawn from a cleared and stained speci-
men. Spicula II and III did not stain with Alcian blue in
this preparation, but could be seen and drawn with
adequate background. Spiculum I is absent. Boophis sp.
is a rather typical suctorial tadpole in its greatly ex-
panded rostral region. However, the cartilagines meck-
eli are rather moderate in size, the cartilagines labialis
the broad commissura quadratocranialis an-
terior (Figs. 3, 10)(van der Westhuizen, ‘61:
figs. 6, 7). The extension of the commissura
reduces the size of the fenestra subocularis
which is much smaller than that of pond-
type larvae. The suctorial tadpoles of
Heleophryne and Ascaphus truei differ from
the other suctorial tadpoles in this study in
having a low processus muscularis quadrati.
The presence of a larval processus oticus
was reported for some representatives of the
Hylinae and Phyllomedusinae (Fabrezi and
Lavilla, ‘92; Haas, ‘96a; de Sá and Hines,
‘97); however, it is absent in Anotheca spi-
nosa, Flectonotus goeldii, Hyla lanciformis,
inferior are broad and flat in cross section, and the
branchial basket is small and shallow with laterally
oriented ceratobranchialia. These features together with
evidences from musculature, pharynx, and gut suggest
that Boophis sp. might be a macrophagous larvae, spe-
cialized in feeding on water insects. The combination of
suctorial habits and insectivory has not been reported
before. See Figures 3 and 5 for abbreviations.
and six species of Gastrotheca (de Sá, ‘88;
Haas, ‘96a,b). The absence of the processus
was suggested to be the plesiomorphic condi-
tion among hylids (Haas, ‘96a). Ascaphus
truei, Heleophryne purcelli, H. natalensis,
and all species in this study have a larval
processus oticus. In Litoria nannotis (Fig.
11) and Nyctimystes dayi there is an addi-
tional connection of the palatoquadrate with
the otic capsule: the larval processus basa-
lis. It is a fusion of the palatoquadrate with
the floor of the otic capsule, medial and
ventral to the larval otic process (Fig. 11).
The processus oticus and processus basalis
enclose the vena capitis lateralis. A larval
 CRANIAL MORPHOLOGY OF SUCTORIAL TADPOLES
Fig. 11. Litoria nannotis (KU 224681, stage 26/27,
section 28/5/3) and L. rheocola (KU 224690, stage 41,
section 16/2/5). Cross section through the otic capsule
showing the posterior connections of the palatoquadrate
with the otic capsule. In L. nannotis, the palatoquadrate
has two synchondroses: the larval processus oticus (pot)
and the larval processus basalis (pbas). Both connec-
tions enclose a canal for the vena capitis lateralis. The
ramus hyomandibularis (VII) does not run through that
canal. In L. rheocola a larval processus oticus is present,
and the palatoquadrate connects to the floor of the otic
processus basalis was described for Asca-
phus truei and Heleophryne larvae (Pusey,
‘43; Ramaswami, ‘44: ⫽pseudobasal process;
van Eeden, ‘51; van der Westhuizen, ‘61;
Reiss, ‘97). In both taxa, the ramus hyoman-
dibularis (VII) and vena capitis lateralis run
laterad, dorsal to the process. The nerves of
L. nannotis and N. dayi, in contrast, extend
anterior and ventral to the larval processus
oticus. The topological relationships of nerve,
otic capsule, and palatoquadrate are similar
in L. rheocola (Fig. 11), Hyla armata, and
Boophis sp.; however, in these species the
connection of the palatoquadrate to the otic
capsule is by dense collagen fibers only. Al-
though not all suctorial species have a proces-
sus basalis, the information available indi-
cates that the occurrence of a larval
processus basalis is restricted to larvae with
suctorial habits.
We found few differences between sucto-
rial and pond-type pelodryadine tadpoles in
the mandibular arch musculature (nervus
trigeminus innervated). Each species exam-
ined has the same sets of muscles, that differ
only in proportional size and shifts in the
areas of origin. In suctorial species, for ex-
ample, the m. levator mandibulae posterior
superficialis has an expanded origin along
the processus ascendens and some fibers
originate from the side wall of the braincase.
131
capsule by collagen fiber-rich connective tissue (lot).
Larval processus basales have only been reported for
stream-dwelling, suctorial tadpoles. Note the anterior
insertion of the epaxial musculature (em). csl, canalis
semicircularis lateralis; em, epaxial musculature; fac,
foramen acusticum; fp, frontoparietale; lot, ligamentum
oticum; mlmps, m. levator mandibulae posterior superfi-
cialis; nc, notochord; pb, planum basale; pbas, processus
basalis; pot, processus oticus; pq, palatoquadrate; ps,
parasphenoid; th, thymus; ts, tectum synoticum; utr,
utriculus; vcl, vena capitis lateralis.
The most striking feature of Nyctimystes
dayi musculature is the extreme posterior
shift of the m. levator mandibulae anterior,
a feature shared with Boophis sp. in our
sample. In N. dayi, fibers of this muscle
extend beyond the planum basale and reach
the ventral side of the first vertebra.
All pelodryadine species have a m. levator
mandibulae anterior lateralis, a thin muscle
(few fibers of small diameter) that is easily
overlooked, both in serial sections and
manual dissections (Fig. 6). It occurs in Pelo-
bates fuscus (Luther, ‘14; ⫽ adductor man-
dibulae posterior lateralis), various hylids
(Haas, ‘96a), and presumably in Discoglos-
sus pictus (Pusey, ‘43; contradicting evi-
dence in Schlosser and Roth, ‘95). Its phylo-
genetic and functional significance is
unknown. Likewise, this applies to the
m. levator mandibulae externus. This flat
muscle consists of only a few loose fibers
that have a fan-shaped origin from the inner
side of the anterior margin of the processus
muscularis. (Fig. 6). The ramus mandibu-
laris (V) crosses the m. levator mandibulae
externus dorsally in Litoria nannotis and
L. rheocola, but ventrally in L. caerulea,
L. xanthomera, and L. genimaculata. The
nerve crosses both the m. levator mandibu-
lae externus and subexternus ventrally in
132 A. HAAS AND S.J. RICHARDS

Fig. 12. Measurements taken from the hyobranchial
skeleton. Both body sides were measured for each ani-
mal. CH ⫹ HB is equivalent with the buccal floor area of
tadpoles. CH, ceratohyal area; HB, area of hypobran-
chial elements; BB, branchial basket area; ␣ orientation
of ceratohyal (1,17) to median plane; ␤, orientation of
second gill slit (7,15) to median plane; 1, anterior margin
of pars reuniens; 2, tip of processus anterior; 3, tip of
processus anterolateralis; 4, condylus of ceratohyal; 5,
most lateral point (internal) of branchial basket; 6, most
posterior point of gill slit I; 7, most posterior point of gill
slit II; 8, most posterior point of gill slit III; 9, base of
spiculum IV; 10, most posterior point of planum hypo-
branchiale junction; 11, most posterior point of basibran-
chiale; 12, lateral point of basibranchiale/planum hypo-
branchiale junction; 13, tip of processus posterior; 14,
base of spiculum III; 15, base of spiculum II; 16, base of
spiculum I; 17, lateral tip of processus lateralis.

N. dayi and Boophis sp. The m. levator man- ‘96a). The nerve is dorsal to the m. levator
dibulae externus is crossed by the ramus mandibulae externus in Hyla armata,
mandibularis ventrally in Bufo japonica H. arborea, H. cinerea, Scinax rubra, Phyllo-
(Takisawa et al., ‘52) and B. bufo (Haas, bates bicolor, and Leptodactylus pentadac-

TABLE 2. Measurements taken from the hyobranchial apparatus1

Relative Relative Relative Branchial
ceratohyal hypobranchial branch. basket Ceratohyal basket
Lever arm area CH/(CH ⫹ area HB/(CH ⫹ area BB/(CH ⫹ orientation orientation
Species ratio AB/AC HB ⫹ BB) (%) HB ⫹ BB) (%) HB ⫹ BB) (%) (␣) (␤)
Litoria caerulea 33 0.36 24.1 14.4 61.8 74.7 32.9
Litoria genimaculata 39 0.37 27.8 17.0 55.8 77.8 34.9
Litoria. xanthomera 37 0.32 23.7 15.5 61.0 70.7 32.1
Litoria. nannotis 252 0.37 34.3 18.2 48.5 72.1 35.1
Litoria. rheocola 372 0.38 28.0 19.0 53.2 74.5 38.6
Nyctimystes dayi 302 0.30 38.0 19.8 42.4 62.1 36.5
Ascaphus truei 392 0.30 — — 58.8 67.7 45.2
Boophis sp. 252 0.36 39.0 21.7 40.4 64.1 50.8
Heleophryne natalensis2 0.50 — — — — —
1Each specimen was measured after reorientation on three pictures. Both body sides were measured. Thus, numbers in the table are
mean values of six measurements per individual. For definition of measurements, see Figure 12. Relative ceratohyal and hypobran-
chial area were not determined for Ascaphus truei because the required landmarks are not applicable for Ascaphus truei. Only lever
arm ratio was available for Heleophryne natalensis from the literature (Wassersug and Hoff, ’79). Hyla armata could not be measured
because of the poor quality of the cleared-and-stained specimen. The numbers following species names indicate Gosner stages.
2Suctorial larvae.
 CRANIAL MORPHOLOGY OF SUCTORIAL TADPOLES
tylus, but penetrates the m. levator mandibu-
lae subexternus in species of Gastrotheca,
Anotheca, Agalychnis, and Phyllomedusa
(Haas, ‘96a). The muscle is absent in six
species of Gastrotheca (Haas, ‘96a) but is
known for representatives of various neoba-
trachian groups: species of Hyla, Scinax,
Phyllobates, Leptodactylus, and Bufo (Luther,
‘14 ⫽adductor mandibulae externus dorsa-
lis; Takisawa et al., ‘52; Haas, ‘96a). A corre-
lation of ecology and presence/absence of
this muscle is not evident from the available
data.
The structures of the hyobranchial skel-
eton and musculature (Fig. 7) of the species
examined conform with the general findings
for taxa of the clade Neobatrachia ⫹ Peloba-
toidea (Schulze, 1892; de Jongh, ‘68; Star-
rett, ‘73; Haas, ‘97). The commissura proxi-
malis I is missing, but the commissura
proximalis II is retained in some of the spe-
cies. The basihyale is present in some spe-
cies, but missing in others. There is interspe-
cific variation in the proximal connections of
ceratobranchiale II and III in pelodryadine
frogs. The m. constrictor branchialis I is
missing and the m. subarcualis rectus I is
composed of three main bundles of fibers. A
musculoskeletal topology that is obviously
correlated with the mode of life is not evi-
dent.
In the neobatrachian species examined,
there is little variation in the spatial arrange-
ment of the hyobranchial muscles inner-
vated by cranial nerves VII, IX, X, and XII
(Fig. 7). Their topology does not deviate sub-
stantially from the general neobatrachian
pattern. The m. subarcualis rectus II–IV
inserts anteriorly on ceratobranchiale I in
some species and on ceratobranchiale II in
others. The site of anterior insertion varies
intraspecifically in Litoria genimaculata and
L. xanthomera, suggesting that it is not a
phylogenetically or functionally informative
character within the pelodryadine sample
examined. The m. diaphragmatobranchialis
originates from a more medial position in
most suctorial larvae than in pond-type lar-
vae. It crosses the origin of the m. rectus
cervicis in Litoria nannotis, L. rheocola,
N. dayi, and Boophis sp. (Fig. 7). Although
the neobatrachian species studied share
similar hyobranchial muscle arrangements,
there are marked, phylogenetically informa-
tive differences in their pattern compared
with that of Ascaphus truei detailed in Pu-
sey (‘43) and Haas (‘97).
133
Suctorial and pond-type larvae clearly dif-
fer in the anterior insertion of the m. rectus
abdominis. In pond-type tadpoles, this
muscle is restricted to the wall of the pleuro-
peritoneal cavity, and usually terminates an-
teriorly at the origin of the m. rectus cervicis
(Schulze, 1892; Gradwell, ‘72a; Sokol, ‘75:
fig. 5; Carr and Altig, ‘92). The m. rectus
abdominis of suctorial pelodryadine species
(and also Boophis sp. and Hyla armata) ex-
tends anteriorly, beyond and ventral to the
origin of the m. rectus cervicis; it underlies
part of the branchial basket and inserts in a
sheath of collagen-rich tissue.
To demonstrate the shape differences be-
tween suctorial and pond-type larvae we
compared Nyctimystes dayi with Litoria xan-
thomera using the Thin Plate Spline tech-
nique (Bookstein, ‘91). The comparison is
based on the same 17 landmarks that were
used for area measurement (Fig. 12) and 12
landmarks of the chondrocranium (Fig. 13).
Landmark coordinates of L. xanthomera
were targeted on N. dayi geometry, and vice
versa. The meshes over the chondrocrania
indicate that shape differences between the
two species are restricted to anterior, preor-
bital parts of the skulls. The orbital and
postorbital regions of the neurocranium are
of similar shape and show only subtle differ-
ences. The meshes over the hyobranchial
skeleton visualize the relatively small bran-
chial basket area, large ceratohyal area, and
more inclined ceratohyal position in the suc-
torial N. dayi compared with the pond-type
L. xanthomera.
It is evident that the neobatrachian sucto-
rial tadpoles that we examined share vari-
ous features, irrespective of the taxonomic
group they represent (Tab. 3). These charac-
ters seem to have evolved independently
multiple times in the Neobatrachia, in our
sample at least four times (i.e., Boophis,
Heleophryne, Hyla armata, and Litoria/
Nyctimystes). We conclude that these fea-
tures are causally linked to highly special-
ized suctorial habits. They include (Table 3):
1. The cornua trabeculae are very wide an-
teriorly and fused along most of their
length in some taxa.
2. The lower jaws are robust.
3. The components the cartilago labialis su-
perior are robust and partially or fully
fused.
4. The maximum width of the skull (with-
out branchial basket) is at the jaw articu-
lation.
134 A. HAAS AND S.J. RICHARDS
Fig. 13. Thin-plate-spline shape comparison of Lito-
ria xanthomera (pond-type) and Nyctimystes dayi (sucto-
rial). To demonstrate correspondence between calcu-
lated mesh and structures, the video images of the
objects were digitally processed (cleaned, reduced in
contrast, resized) and positioned below meshes. Neuro-
cranium above, hypobranchial skeleton below; both in
dorsal views. Note that the structures branching off
along the ceratobranchialia in N. dayi are largely soft
tissue and not cartilaginous structures (see Fig. 5). The
landmark-based meshes visualize that the brain cavity,
orbital and otic region of the skulls are quite similar in
shape in suctorial and pond-type larvae, while the ros-
tral regions are strikingly different. The shape of the
5. The palatoquadrate is robust and strongly
attached to the neurocranium by broad
commissura quadratocranialis anterior,
larval processus oticus, processus ascen-
dens, and larval processus basalis (liga-
mentum oticum in L. rheocola, Boophis
hyobranchial apparatus in the suctorial N. dayi can be
derived fom the shape in L. xanthomera largely by
compression of the branchial basket and a backward
rotation of the lateral ceratohyal processus. 1, medial
posterior margin of tectum synoticum; 2, posterior mar-
gin of septum nasi; 3, medial, distal angle of cornu
trabeculae; 4, lateral, distal angle of cornu trabeculae; 5,
lateral angle of pars articularis quadrati; 6, medial
angle of pars articularis quadrati; 7, processus ethmoida-
lis; 8, apex of processus muscularis; 9, anteriormost
point of fenestra subocularis; 10, most anterior point of
cupula anterior (capsula auditiva); 11, processus oticus;
12, most posterior point of cupula posterior (capsula
auditiva).
sp, H. armata); some taxa exhibit a re-
duced processus ascendens (absent in
Heleophryne, thin in Boophis sp.).
6. The palatoquadrate bears a processus
ventralis at the anterolateral base of the
processus muscularis.
 CRANIAL MORPHOLOGY OF SUCTORIAL TADPOLES
TABLE 3. Shared features of neobatrachian suctorial
Suctorial neobatrachians
Cornua trabeculae extremely wide anteriorly, some-
times fused along most of their length
Robust lower jaws
Robust but movable upper jaw with fused components;
species differ in the extent of fusion.
Greatest width of skull at the level of jaw articulation
Robust palatoquadrate, strongly attached to neurocra-
nium by a broad commissura quadratocranialis ante-
rior, processus oticus, processus ascendens (vestigial
or absent in some species), and processus basalis
(present in some species); (jaw articulation anterior
to eye)
Processus ventralis quadrati present
Far anterior insertion of m. rectus abdominis (connec-
tive tissue sheath attached to palatoquadrate and
oral sucker)
Insertion of epaxial musculature extended anteriorly
m. diaphragmatobranchialis and m. rectus cervicis
cross at their origins
Origin of the m. levator mandibulae anterior shifted
posteriorly
Small branchial basket and large ceratohyal area
1The characters listed evolved convergently several times in neobatrachian species with suctorial tadpoles and correlate with this
specific mode of life. Ascaphus truei, however, differs in some of these features, likely reflecting the long separate history of the two
groups (Fig. 1). For a more general comparison of Ascaphus with neobatrachian larvae, see Pusey (’43) and Haas (’97).
7. A modified m. rectus abdominis insertion
allows the muscle to act on the palato-
quadrate and posterior base of oral disk.
8. The epaxial musculature extends to the
anterior parts of the otic capsule.
9. The branchial basket area is relatively
small, and the ceratohyal area relatively
large.
10. The m. diaphragmatobranchialis and
m. rectus cervicis cross at their origins
(not crossing but very close to each other
in H. armata).
11. The origin of the m. levator mandibulae
anterior extends far posteriorly on the
planum basale and/or floor of the otic
capsule (most extremely in Nyctimystes
dayi and Boophis sp.).
It is evident that most of these characters
involve positional shifts or changes in propor-
tions, rather than structural novelties. Con-
dition 7 can be identified as a novel func-
tional feature, but even this feature is a
result of modification in suctorial larvae of a
muscle well-known in pond-type tadpoles.
Aside from the characters just listed and
despite their distinct life habits, strikingly
different body shapes, and modified oral disk
function, suctorial and pond-type pelodrya-
dine tadpoles have remarkably similar man-
dibular and hyobranchial musculature. The
135
larvae1
Ascaphus truei
Cornua not significantly expanded, short, bent ven-
trally
Very large cartilago meckeli, but small and slender car-
tilago labialis inferior
Medial part of upper jaw (pars corporis) fused to cornu
trabeculae, lateral wings (partes alaris) not fused to
medial part
Greatest width of skull at the level of jaw articulation
Robust palatoquadrate, strongly attached to neurocra-
nium by a broad commissura quadratocranialis ante-
rior, processus oticus, processus ascendens, and pro-
cessus basalis; (jaw articulation more posterior than
in neobatrachians, at level of optic nerve)
Absent
Far anterior insertion of m. rectus abdominis (tendon
to cartilago meckeli)
Insertion of epaxial musculature extended anteriorly
Origins of these muscles clearly separate
m. levator mandibulae anterior absent
Small branchial basket and large ceratohyal area
same muscles are found in all six species,
and differences are few and subtle. The mus-
culoskeletal hyobranchial topology is largely
congruent with the pattern found in other
neobatrachian taxa, irrespective of life hab-
its. This pattern is widespread and probably
plesiomorphic within the Neobatrachia.
Variations found in the course of the ramus
mandibularis (V), and absence/presence of
the mm. levator mandibulae externus and
lateralis seem independent of life-style, and
might be phylogenetically informative. For
example, the course of the nerve in Litoria
nannotis and L. rheocola might be a derived
feature of the nannotis-species group.
Ascaphus truei shares some features (4–9)
with neobatrachian suctorial larvae, but dif-
fers significantly in others (Table 3), e.g., the
cornua trabeculae are short and not ex-
panded distally, the cartilago labialis infe-
rior is thin, the upper jaw is probably not
abducted during feeding, and the hyobran-
chial skeleton and musculature have differ-
ent topologies and compositions (Pusey, ‘43;
Haas, ‘97). Similar life habits but alterna-
tive constructional designs of cranial struc-
tures suggest that a long separate history of
Ascaphus truei and neobatrachians might
account for these differences.
136 A. HAAS AND S.J. RICHARDS
Functional Morphology
Gradwell (‘71, ‘73) and Taylor and Altig
(‘95) discussed the functional morphology of
oral suction and oral disk kinematics in
rheophilous suctorial tadpoles. Gradwell (‘71)
cited older literature on various aspects of
the biology of stream-living tadpoles.
Gradwell (‘75) studied suction and gill
breathing in rheophilous adherent tadpoles
including some species of Litoria. In sucto-
rial tadpoles, the oral disk is used to adhere
almost permanently to the substrate (rocks)
in fast-flowing streams. The larvae move
over the substrate by extension and retrac-
tions cycles (‘‘hitching’’ action) of the oral
disk and the jaws while maintaining contact
to the substrate. Feeding and locomotor
movements probably involve the same pat-
tern of disk extension (Taylor and Altig, ‘95).
The action of the jaws scrapes organic mate-
rial off the rock surface seemingly without
detachment of the disk from the substrate.
How exactly the food suspension thus cre-
ated in the disk–substrate cavity is subse-
quently flushed into the pharynx remains
unclear. It has been suggested that reduced
suction pressure during feeding probably al-
lows rhythmic water exchange between the
disk–substrate and internal oral cavity syn-
chronous with buccal pump action (Gradwell,
‘71). Loosening of the disk–substrate seal
during a short phase of the feeding cycle
might allow oral inflow and transport of the
food suspension to the pharynx (Gradwell,
‘75).
Gradwell (‘71, ‘75) measured negative pres-
sures in living larvae attached to the sub-
strate by their oral disks. We observed that
deeply anaesthetized and relaxed Litoria
nannotis and Nyctimystes dayi still stick to
the substrate and resist removal. Detached,
anaesthetized tadpoles will immediately ad-
here to a fingertip that is pressed against
their sucker. This finding suggests that once
attachment to the substrate has been estab-
lished by negative pressure generated in the
buccal pump (Gradwell, ‘71), it can largely
be maintained passively by the physical
properties (seal, elasticity, recoil) of the disk
itself without muscular action. An oral valve
seals off the disk–substrate cavity from the
internal oral cavity and seems to be essen-
tial for maintaining sucker engagement
(Gradwell, ‘71). The flat body and wedge
shaped snout may help to press the animal
onto the substrate in the strong currents
that these animals prefer. In Ascaphus truei
and some rheophilous, adherent-type tad-
poles of the genus Litoria, a respiratory wa-
ter current entering through the nostrils is
maintained during sucker engagement (Al-
tig and Brodie, ‘72; Gradwell, ‘71, ‘75) and
allows gill breathing in attached animals.
A large adrostral cartilage is developed in
suctorial pelodryadine species. Nyctimystes
dayi differs from Litoria nannotis and
L. rheocola in that the adrostral cartilage is
flexibly and synchondrotically connected to
the pars alaris, whereas it is connected by
ligaments in L. nannotis and L. rheocola.
The adrostral cartilage has been described
in a number of neobatrachian species
(Schulze 1892; Sokol, ‘81, Haas, ‘95, ‘96a),
but no hypothesis about its function has
been proposed in the literature.On the basis
of its connections to the cartilago meckeli
and cartilago labialis superior, and the geom-
etry of the jaws, the following functional
scenario is proposed.
In anuran larvae, the upper jaw is opened
indirectly (de Jongh, ‘68:fig. 15; Gradwell,
‘72b:fig. 2). As the cartilago meckeli rotates
to depress the lower jaw, the posterior tip of
the cartilago labialis superior is pulled down
by the ligamentum mandibulosuprarostrale.
There is no abductor muscle inserting di-
rectly on the cartilago labialis superior. This
mechanism could only work efficiently if the
posterior tip of the cartilago labialis supe-
rior were located near or above of the proces-
sus dorsomedialis (cartilago meckeli) in the
resting position (adduction) of the jaws (Figs.
4c, 6). In suctorial pelodryadines, the geom-
etry of the jaws is such that the processus
dorsomedialis of the cartilago meckeli lies
far dorsal to the posterior tip of the cartilago
labialis superior (pars alaris) (Fig. 9b). The
ligamentum mandibulosuprarostrale con-
nects to the adrostral and pulls the adrostral
with the cartilago meckeli during lower jaw
abduction. The adrostral cartilage acts as a
pushing rod that transmits the force to the
pars alaris and rotates the pars alaris out-
ward. The pars alaris and adrostral carti-
lage are coupled by ligaments. Another liga-
ment connects the ventral side of the end of
the cornu trabeculae with the dorsal margin
of the cartilago labialis superior (pars cor-
poris), thereby possibly preventing overex-
tension of the upper jaw when it is abducted.
According to this functional scenario a five-
joint model was applied to the three-dimen-
sionally reconstructed geometry of a Litoria
nannotis larva. The inverse kinematics func-
 CRANIAL MORPHOLOGY OF SUCTORIAL TADPOLES
tions of the Alias Studio software facilitate
computer simulation of the hypothesized
pushing-rod function of the adrostral carti-
lage during jaw opening on the computer
(Fig. 9b–c). The simulation may differ from
real movements in the degree of rotation of
the upper jaw, but demonstrates that there
are no mechanical conflicts in the functional
scenario.
Larvae of the genus Heleophryne have a
large adrostral cartilage in the same posi-
tion as L. nannotis, but no information is
available about its connections to neighbor-
ing elements. The geometry of the rostral
skull in Heleophryne spp. (van der Westhui-
zen, ‘61:fig. 8), however, suggest that a simi-
lar opening mechanism has evolved conver-
gently in these species. Heleophryne spp.
have an additional, submeckelian cartilage
of unknown function in the jaw apparatus.
In Ascaphus, a ligamentum mandibulosupra-
rostrale and adrostral are absent and the
cartilago labialis superior is broadly fused to
the cornua trabeculae (Pusey, ‘43; van Ee-
den, ‘51; Reiss, ‘97). The anatomical features
suggest that larvae of Ascaphus do not ab-
duct their upper jaws in connection with
rotation of the lower jaw (Gradwell, ‘71). In
Hyla armata, there might be yet another
opening mechanism; the processus dorsome-
dialis of the cartilago meckeli is laterally
expanded and lies posterior and dorsal to
the posterior tip of the cartilago labialis su-
perior. Inferred from its position this process
might push down the tip of and rotate the
cartilago labialis superior by direct contact
during lower jaw abduction.
In anurans, a larval processus basalis has
so far only been described in stream-dwell-
ing larvae. The processus basalis may addi-
tionally stabilize the palatoquadrate and
may be part of the force transmission chain
from the anterior adhesive organ to the
trunk. When the animal uses its oral disk to
cling to rocks in the current, some force will
be transmitted to the postcranial parts of
the body via the mandibular musculature
and the palatoquadrate. This functional in-
terpretation raises the question as to
whether the larval processus basalis of Asca-
phus is plesiomorphic for anurans and ho-
mologous to the processus basalis of sala-
manders (Reiss, ‘97), or a de novo larval
(caenogenic) character correlated with
stream-dwelling habits. In Heleophryne (van
der Westhuizen, ‘61), the processus ascen-
dens is missing and in Boophis sp. it is thin.
137
In both species, the processus oticus and the
basal connection (ligamentum oticum in Bo-
ophis, processus basalis in Heleophryne)
seem to be replace the processus ascendens
in its mechanic function.
The processus ventralis (van der Westhui-
zen, ‘61) is a common feature of the palato-
quadrate in the suctorial tadpoles studied. It
is located laterally, at the anterior base of
the processus muscularis (Fig. 3). The pro-
cess is connected ventrally to a collagen fiber-
rich sheet of connective tissue into which the
m. rectus abdominis inserts posteriorly. Al-
though not measured directly, it is likely
that forces of the m. rectus abdominis act on
this process. This topology suggests that the
m. rectus abdominis can pull the body to-
ward the substrate once the oral sucker has
been attached to the ground. A similar func-
tion was suggested originally by Gradwell
(‘73) for Ascaphus truei, in which the
m. rectus abdominis attaches via a long ten-
don to the cartilago meckeli. The epaxial
musculature reaches more anteriorly in suc-
torial larvae than in pond-type larvae. It
probably acts antagonistically to the m. rec-
tus abdominis and extends the head. Thus,
the epaxial musculature might assist the
detachment of the oral sucker. Abdominal
and epaxial musculature are surprisingly
similar in the fossorial, nonsuctorial micro-
hylid Otophryne robusta. Wassersug and Py-
burn (‘87) suggested that in this species far
anteriorly reaching abdominal and epaxial
musculature are used to extend and bend
the head during burrowing into sand. This
could also be a second function of these
muscles in suctorial larvae, as we observed
burrowing abilities in some suctorial pelo-
dryadine larvae (Richards, ’92).
The origin of the m. orbitohyoideus of suc-
torial tadpoles extends onto the processus
ventralis quadrati. Its fibers form a broad
fan extending over an angle of up to 90°
(Litoria nannotis), at least twice the angle
that anterior and posterior fibers form in
pond-type larvae, and reminiscent of a pin-
nate muscle. Wassersug and Hoff (‘79) and
Satel and Wassersug (‘81) described param-
eters (muscle diameter, muscle length, cera-
tohyal geometry) of the buccal pump struc-
tures in relation to the ecology of tadpoles.
According to their geometric analysis, the
fan-shaped m. orbitohyoideus in combina-
tion with a moderate to long ceratohyal lever
arm (Table 2) in suctorial larvae provides
great muscular force and high mechanical
138 A. HAAS AND S.J. RICHARDS
advantage. There is limited excursion of the
buccal floor, but high negative pressures can
be generated in the buccal cavity.
Our sample for hyobranchial measure-
ments was small (Table 2). Wassersug and
Hoff (‘79) studied a much larger sample of
tadpoles of diverse ecologies and discovered,
for example, no correlation of lever arm ratio
with intraspecific or interspecific size differ-
ences. Although their study revealed gen-
eral correlations of lever arm ratio and lar-
val ecology, both their values and ours for
suctorial tadpoles range from 0.29 to 0.50.
This indicates that a suctorial lifestyle can
be realized with a broad range of ceratohyal
geometries. Within the pelodryadine sam-
ple, the relative branchial basket area is
smaller, the relative hypobranchial area
larger, the relative ceratohyal area larger,
and the ceratohyal angle (␣) smaller in suc-
torial larvae than in pond-type larvae (Ta-
ble 2). These differences are consistent in
the sample, but the absolute differences be-
tween the two groups are small. Among the
suctorial pelodryadine larvae, Nyctimystes
dayi has the most extreme area values, but
Boophis sp. has an even smaller branchial
basket area, and larger ceratohyal and hypo-
branchial areas. Furthermore, Boophis sp.
has the most laterad orientation of the cera-
tobranchialia. We found complete ephemero-
pteran larvae in the gut of Boophis sp., no-
ticed longitudinal plicae in the anterior gut
region, and observed vestigial filter epithe-
lia. These observations, the unusual geom-
etry of the hyobranchial skeleton, and the
wide, anteriorly flat cartilago meckeli sug-
gest that Boophis sp. is a suctorial macropha-
gous larvae specialized in feeding on water
insects. The unusually well-developed
m. tympanopharyngeus in this species is
able to constrict the esophageal funnel and
might help to swallow large food items.
Noble (‘29) pointed out the phenomenon
that functional lungs are present in some
but vestigial in other suctorial larvae. This
is in accord with our observations. Lungs
seem to become functional only during meta-
morphosis in pelodryadine species with suc-
torial larvae. While the advantage of de-
layed lung development seems evident in a
fast-flowing habitat (reduced buoyancy), it
is not clear why stream-dwelling larvae of
some species (Boophis sp., Hyla armata) still
have lungs.
Evolution of suctorial larvae
in the Pelodryadinae
If the Pelodryadinae is monophyletic
(Tyler, ‘71; Tyler and Davies, ‘78; Hutchin-
son and Maxson, ‘87), alternative hypoth-
eses can be advanced to explain the evolu-
tion of suctorial tadpoles in the Litoria
nannotis group and Nyctimystes. The first
assumes that the suctorial tadpoles evolved
in both groups independently and that their
similarities, therefore, are convergent. Tyler
(‘82), without further elaboration, suggested
that the Australian Litoria nannotis group
acquired suctorial adaptations indepen-
dently from the New Guinean pelodryadine
species. This scenario was supported by
Hutchinson and Maxson (‘87), who indicated
that the Litoria nannotis group is most
closely related to Australian stream-dwell-
ing frogs in the Litoria citropa group, which
do not have suctorial larvae, whereas New
Guinean suctorial Litoria and Nyctimystes
might be derived from ancestors of the Aus-
tralian Litoria freycineti assemblage (nonsuc-
torial larvae). The foregoing morphological
comparisons between pelodryadines and the
distantly related neobatrachian taxa Bo-
ophis sp., Hyla armata, and Heleophryne
spp. demonstrate that suctorial life habits
correlate with certain larval cranial features
across several neobatrachian groups. This
might cast doubts on the utility of these
larval characters in the resolution of histori-
cal relationships of the nannotis group and
Nyctimystes. It would be in accord with the
current taxonomic arrangement, which
places the species in question in two genera
distinguished by characters of adults (e.g.,
pupil shape, palpebrum, ornamentation)
(Tyler and Davies, ‘78, ‘79; Cogger, ‘92).
In the second hypothesis, the nannotis
species group would be more closely related
to Nyctimystes dayi than to the other species
groups of Litoria represented in our study. It
would follow that the suctorial tadpole was
already present in the most recent common
ancestor of both.
The suctorial pelodryadine species exam-
ined share many features that distinguish
them from pond-type pelodryadine larvae
(Table 3). Although most of these characters
are homoplastic within the Neobatrachia,
they probably are valid unique, shared-
derived characters within the Pelodryadi-
nae. If one eliminates all characters that are
homoplastic within the Neobatrachia from
discussion, i.e., all those also present in Asca-
 CRANIAL MORPHOLOGY OF SUCTORIAL TADPOLES
phus truei, Heleophryne, Boophis sp. or Hyla
armata, there remain characters uniting the
nannotis species group and Nyctimystes dayi.
The configuration of the cartilago labialis
superior, in which the pars corporis is fused
to a broad plate, the lateral parts of it curv-
ing posteriorly and lying medial to the pars
alaris, is unique among all described anuran
tadpoles. This distinct configuration of the
cartilage of the upper jaw occurs in combina-
tion with a novel upper jaw-opening mecha-
nism involving the adrostral cartilage as a
pushing-rod element. All pond-type pelodrya-
dines examined, in contrast, lack an adros-
tral cartilage. As inferred from data in the
literature, only Heleophryne species might
have evolved a similar mechanism conver-
gently. Although a larval processus basalis
is present in A. truei and Heleophryne spp,
Litoria nannotis and N. dayi differ from them
in having the ramus hyomandibularis (VII)
running anterior and ventral to the proces-
sus basalis; pond-type pelodryadines lack
the process. The inclination of the arcus
subocularis in cross section (lateral edge ven-
tral to medial edge) in N. dayi, L. rheocola,
and L. nannotis is unique within the species
examined herein. Comparing the suctorial
pelodryadine larvae with respect to the pond-
type larvae, N. dayi is more derived than
L. nannotis and L. rheocola in having more
extensive fusions in the cartilago labialis
superior and cornua trabeculae, a processus
accessorius on the cartilago meckeli, a rela-
tive larger ceratohyal area, a relative smaller
branchial basket area, more posteriorly in-
clined ceratohyalia, and a smaller lever arm
ratio.
Suctorial larvae, similar appearance of
adults, deposition of large unpigmented eggs,
and the geographic distributions of taxa
(northern Queensland) suggest that the nan-
notis group and Nyctimystes dayi may repre-
sent a natural group. If this were true, ei-
ther the genus Litoria or Nyctimystes would
be paraphyletic. The nannotis group would
be more closely related to N. dayi than to
species of Litoria with pond-type larvae; also,
N. dayi could be more closely related to the
L. nannotis group than to New Guinea Nyc-
timystes. Suctorial tadpoles might have
evolved once in the most recent common
ancestor of all suctorial pelodryadines or
twice in the Australian (L. nannotis group ⫹
N. dayi) and the New Guinea (montane Lito-
ria ⫹ Nyctimystes) suctorial species. It is not
possible to resolve this systematic issue based
139
on the limited data presented herein. However,
it is obvious that larval morphological evidence
may not be congruent with current taxonomic
arrangements.
ACKNOWLEDGMENTS
We gratefully acknowledge critical com-
ments of L. Trueb and L. Olsson on an early
draft of the manuscript. Further helpful criti-
cism and suggestions of two reviewers im-
proved the manuscript in many ways. We
are indebted to R. McDiarmid (Smithsonian
Institution), N. Meyer, and R. Altig for kindly
providing specimens and literature. E.
Gretscher contributed her skills in doing
serial sections of specimens. Figure 2 was
produced by B. Scott. We thank the National
Institute of Health and Jeffrey A. Walker for
distributing relevant software as freeware.
Research by S.J.R. was conducted under per-
mits issued by the Queensland Department
of Environment, and Queensland DPI For-
estry.
LITERATURE CITED
Altig, R. and E.D. Brodie (1972) Laboratory behavior of
Ascaphus truei tadpoles. J. Herpetol. 6:21–24.
Altig, R., and F. Johnston (1989) Guilds of anuran lar-
vae: Relationships among developmental modes, mor-
phologies, and habitat. Herpetol. Monogr. 3:81–109.
Barry, T.H. (1956) The ontogenesis of the sound-conduct-
ing apparatus of Bufo angusticeps. Morphol. Jb. 97:
477–544.
Bookstein, F.L. (1991) Morphometric Tools for Land-
mark Data. New York: Cambridge University Press.
Carr, K.M. and R. Altig 1991. Oral disc muscles of
anuran tadpoles. J. Morphol 208:271–277.
Carr, K.M., and R. Altig (1992) Configuration of the
rectus abdominis muscle of anuran tadpoles. J. Mor-
phol. 214:351–356.
Cogger, H.G. (1992) Reptiles and Amphibians of Austra-
lia. 5th Ed. Ithaca, NY: Cornell University Press.
Davies, M., and S.J. Richards (1990) Developmental
biology of the Australian hylid frog Nyctimystes dayi
(Günther). Trans. R. Soc. S. Aust. 114:207–211.
de Jongh, H.J. (1968) Functional morphology of the jaw
apparatus of larval and metamorphosing Rana tempo-
raria. Neth. J. Zool. 18:1–103.
de Sá, R.O. (1988) Chondrocranium and ossification se-
quence of Hyla lanciformis. J. Morphol. 195:345–355.
de Sá, R.O., and E. Hines (1997) Anatomical characteris-
tics of phyllomedusine tadpoles. In Z. Roček and S.
Hart (eds.): Abstract Volume of the Third World Con-
gress of Herpetology, Prague, p. 52.
Dingerkus, G., and D.L. Uhler (1977) Enzyme clearing
of Alcian blue stained whole small vertebrates for
demonstration of cartilage. Stain Tech. 52:229–232.
Duellman, W.E., and L. Trueb (1986) Biology of the
Amphibians. New York: McGraw-Hill.
Edgeworth, F.H. (1935) The Cranial Muscles of Verte-
brates. London: Cambridge University Press.
Fabrezi, M., and E.O. Lavilla (1992) Estructura del
condrocraneo y esceleto hı́obranquial en larvas de
algunos hı́lidos neotropicales (Anura: Hylidae). Acta
Zool. Lilloana 41:155–164.
140 A. HAAS AND S.J. RICHARDS
Fabrezi, M., and E.O. Lavilla (1993) Anatomia del con-
drocraneo en larvas de tres especies de Telmatobius
del grupo meridional (Anura: Leptodactylidae). Phy-
sis (Buenos Aires) 48 Sec.B:39–46.
Ford, L.S., and D.C. Cannatella (1993) The major clades
of frogs. Herpetol. Monogr. 7:94–117.
Frost, D.R. (ed.) (1985) Amphibian Species of the World.
A Taxonomic and Geographical Reference. Lawrence,
KS: Allen Press.
Gaupp, E. (1894) Beitraege zur Morphologie des Schae-
dels. II. Das Hyo-Branchial-Skelet der Anuren und
seine Umwandlung. Morphol. Arb. 3:389–437.
Gosner, K.L. (1960) A simplified table for staging anuran
embryos and larvae with notes on identification. Her-
petologica 16:183–190.
Gradwell, N. (1968) The jaw and hyoidean mechanism of
the bullfrog tadpole during aqueous ventilation. Can.
J. Zool. 46:1041–1052.
Gradwell, N (1971) Ascaphus tadpole: Experiments on
the suction and gill irrigation mechanism. Can. J.
Zool. 49:307–332.
Gradwell, N. (1972a) Gill irrigation in Rana catesbei-
ana. Part I. On the anatomical basis. Can. J. Zool.
50:481–499.
Gradwell, N. (1972b) Gill irrigation in Rana catesbei-
ana. Part II. On the musculoskeletal mechanism. Can.
J. Zool. 50:501–521.
Gradwell, N. (1973) On the functional morphology of
suction and gill irrigation in the tadpole of Ascaphus,
and notes on hibernation. Herpetologica 29:84–93.
Gradwell, N. (1975) Experiments on oral suction and gill
breathing in five species of Australian tadpole (Anura:
Hylidae and Leptodactylidae). J. Zool. Lond. 177:81–98.
Haas, A. (1995) Cranial features of dendrobatid tadpoles
(Amphibia: Anura: Dendrobatidae). J. Morphol. 224:
241–264.
Haas, A. (1996a) Das larvale Cranium von Gastrotheca
riobambae und seine Metamorphose (Amphibia, Anura,
Hylidae). Verh. Naturwiss. Ver. Hamburg 36:33–162.
Haas, A. (1996b) Non-feeding and feeding tadpoles in
hemiphractine frogs: Larval head morphology, heter-
ochrony, and systematics of Flectonotus goeldii (Am-
phibia: Anura: Hylidae). J. Zool. Syst. Evol. Res. 34:
163–171.
Haas, A. (1997) The larval hyobranchial apparatus of
discoglossoid frogs: Its structure and bearing on the
systematics of the Anura (Amphibia: Anura). J. Zool.
Syst. Evol. Res. 53:179–197.
Haas, A., and M.S. Fischer (1997) Three-dimensional
reconstruction of histological sections using modern
product-design software. Anat. Rec. 249:510–516.
Hutchinson, M.N., and L.R. Maxson (1987) Phylogenetic
relationships among Australian tree frogs (Anura: Hy-
lidae: Pelodryadinae): An immunological approach.
Austr. J. Zool. 35:61–74.
Inger, R. F. (1992) Variation of apomorphic characters in
stream-dwelling tadpoles of the bufonid genus Ansonia
(Amphibia: Anura). Zool. J. Linn. Soc. 105:225–237.
Lavilla, E.O. (1987) La larva de Rhinoderma darwinii
Dumeril & Bibron (Anura: Rhinodermatidae). Acta
Zool. Lilloana 39:81–88.
Luther, A. (1914) Über die vom N. trigeminus versorgte
Muskulatur der Amphibien, mit einem vergleichen-
den Ausblick über den Adductor mandibulae der Gna-
thostomen, und einem Beitrag zum Verständnis der
Organisation der Anurenlarven. Acta Soc. Sci. fenn.
44:1–151.
Mertens, R. (1960) Die Larven der Amphibien und ihre
evolutive Bedeutung. Zool. Anz. 164:337–358.
Noble, G.K. (1929) The adaptive modifications of the arbo-
real tadpoles of Hoplophryne and the torrent tadpole of
Staurois. Bull. Am. Mus. Nat. Hist. 58:291–334.
Nodzenski, E., and R.F. Inger (1990) Uncoupling of
related structural changes in metamorphosing torrent-
dwelling tadpoles. Copeia 1990:1047–1054.
Orton, G.L. (1953) The systematics of vertebrate larvae.
Syst. Zool. 2:63–75.
Pusey, H.K. (1943) On the head of the liopelmid frog,
Ascaphus truei. I. The chondrocranium, jaws, arches,
and muscles of a partly-grown larva. Q. J. Microsc.
Sci. 84:105–185.
Ramaswami, L.S. (1944) The chondrocranium of two torrent-
dwelling anuran tadpoles. J. Morphol. 74:347–374.
Reinbach, W. (1939) Untersuchungen ueber die Entwick-
lung des Kopfskeletts von Calyptocephalus gayi (mit
einem Anhang ueber das Os supratemporale der an-
uren Amphibien). Jena Z. Naturw. 72:211–362.
Reiss, J.O. (1997) Early development of chondrocranium
in the tailed frog Ascaphus truei (Amphibia: Anura):
Implications for anuran palatoquadrate homologies.
J. Morphol. 231:63–100.
Richards, S.J. (1992) The tadpole of the Australian frog
Litoria nyakalensis (Anura, Hylidae), and a key to the
torrent tadpoles of northern Queensland. Alytes 10:99–
103.
Romeis, B. (1989) Mikroskopische Technik. P. Böck (ed.).
München: Urban & Schwarzenberg. 697 pp.
Ruibal, R., and E. Thomas (1988) The obligate carnivo-
rous larvae of the frog, Lepidobatrachus laevis (Lepto-
dactylidae). Copeia 1988:591–604.
Satel, S. L. and R. Wassersug (1981) On the relative
sizes of the buccal floor depressor and elevator muscu-
lature in tadpoles. Copeia 1981:129–137.
Schlosser, G. and G. Roth (1995) Distribution of cranial
and rostral nerves in tadpoles of the frog Discoglossus
pictus (Discoglossidae). J. Morphol. 226:189–212.
Schulze, F.E. (1892) Über die inneren Kiemen der Ba-
trachierlarven. II.Mittheilung. Skelet, Muskulatur,
Blutgefä␤e, Filterapparat, respiratorische Anhänge
und Athmungsbewegungen erwachsener Larven von
Pelobates fuscus. Abh. königl. preuss. Akad. Wiss.
1892:1–66.
Sedra, S.N. (1950) The metamorphosis of the jaws and
their muscles in the toad, Bufo regularis, correlated
with the changes in the animal‘s feeding habits. Proc.
Zool. Soc. Lond. 120:405–449.
Sokol, O.M. (1975) The phylogeny of anuran larvae: A
new look. Copeia 1975:1–23.
Sokol, O.M. (1981) The larval chondrocranium of
Pelodytes punctatus, with a review of tadpole chondro-
crania. J. Morphol. 169:161–183.
Starrett, P.H. (1973) Evolutionary patterns in larval
morphology. In J.L. Vial (ed.): Evolutionary Biology of
the Anurans. Columbia, MO: University of Missouri
Press, pp. 251–272.
Takisawa, A., Y. Ohara, and K. Kano (1952) Die Kau-
muskulatur der Anuren (Bufo vulgaris japonicus) wae-
hrend der Metamorphose. Okaji. Folia Anat. Jpn. 24:
1–28.
Taylor, C.L., and R. Altig (1995) Oral disc kinematics of
four rheophilous anuran tadpoles. Herpetol. Nat. Hist.
3:101–106.
Taylor, C.L., Altig, R., and C.R. Boyle (1996) Oral disc
kinematics of four lentic anuran tadpoles. Herpetol.
Nat. Hist. 4:49–56.
Tyler, M.J. (1971) The phylogenetic significance of vocal
sac structure in hylid frogs. Univ. Kans.Publ. Mus.
Nat. Hist. 19:319–360.
Tyler, M.J. (1982) The hylid frog genus Litoria Tschudi:
An overview. Proc. NZ Herpetol. Symp., Occ. Publ.
2:103–112.
 CRANIAL MORPHOLOGY OF SUCTORIAL TADPOLES
Tyler, M.J., and M. Davies (1978) Phylogenetic relation-
ships of Australian hyline and Neotropical phyllome-
dusine frogs of the family Hylidae. Herpetologica 34:
219–224.
Tyler, M.J., and M. Davies (1979) Redefinition and evolu-
tionary origin of the Australopapuan hylid frog genus
Nyctimystes Stejneger. Aust. J. Zool. 27:755–772.
van der Westhuizen, C.M. (1961) The development of the
chondrocranium of Heleophryne purcelli Sclater with spe-
cial reference to the palatoquadrate and sound-conduct-
ing apparatus. Acta Zool. (Stockh.) 42:1–72.
van Eeden, J.A. (1951) The development of the chondro-
cranium of Ascaphus truei with special references to
the relations of the palatoquadrate to the neurocra-
nium. Acta Zool., Stockh. 32:41–176.
Viertel, B. (1987) The filter apparatus of Xenopus laevis,
Bombina variegata and Bufo calamita (Amphibia,
Anura). A comparison of different larval types. Zool.
Jb. Anat. 115:425–452.
Wassersug, R.J. (1980) Internal oral features of larvae
from eight anuran families: Functional, systematic,
evolutionary, and ecological considerations. Misc. Publ.
Mus. Nat. Hist. Univ. Kans. 68:1–146.
Wassersug, R.J., and W.E. Duellman (1984) Oral struc-
tures and their development in egg brooding hylid frog
embryos and larvae: Evolutionary and ecological impli-
cations. J. Morphol. 182:1–37.
Wassersug, R., and W.R. Heyer (1988) A survey of inter-
nal oral features of leptodactylid larvae. Smithson.
Contrib. Zool. 457:1–99.
Wassersug, R.J., and K. Hoff (1979) A comparative study
of the buccal pumping mechanism of tadpoles. Biol. J.
Linn. Soc. 12:225–259.
Wassersug, R., and W. F. Pyburn (1987) The biology of
the Pe-ret’ Toad, Otophryne robusta (Microhylidae),
with special consideration of its fossorial larva and
systematic relationships. 91:137–169.
Wassersug, R., and K. Rosenberg (1979) Surface anatomy
of branchial food traps of tadpoles: A comparative
study. J. Morphol. 159:393–426.
Wild, E.R. (1997) Description of the adult skeleton and
developmental osteology of the hyperossified horned
frog, Ceratophrys cornuta (Anura: Leptodactylidae). J.
Morphol. 232:169–206.
APPENDIX
Species, specimens (collection numbers),
stages, kinds of preparation; localities.
Litoria caerulea (White, 1790). KU 224662,
stage 31, dissection/cleared; KU 224663,
stage 32, dissection/cleared; KU 224664,
stage 33, cleared; KU 224665, stage 38,
cleared; KU 224666, stage 39, cleared; KU
224667, stage 40, serial sections; all speci-
mens from captive breeding group of un-
known geographic origin.
Litoria genimaculata (Horst, 1883). KU
224668, stage 27, dissection/cleared; KU
224669, stage 29, dissection/cleared; KU
224670, stage 28, cleared; KU 224671, stage
31, cleared; KU 224672, stage 36, cleared;
KU 224673, stage 39, cleared; KU 224674,
stage 40, cleared; KU 224675, stage 41,
141
cleared; KU 224676, stage 37, serial sec-
tions; KU 224677, stage 41, serial sections;
all specimens from rainforest stream pool,
Birthday Creek, Mt. Spec State Forest, 800
m, 7 km NW Paluma, Queensland, Australia
(146°10’E, 18°59’S).
Litoria nannotis (Andersson, 1916). KU
224678, stage 25, cleared; KU 224679, stage
25, dissection/cleared; KU 224680, stage 25,
dissection/cleared; KU 224681, stage 26/27,
serial sections; KU 224682, stage 27, cleared;
KU 224683, stage 29, cleared; KU 224684,
stage 39, serial sections; all specimens from
riffle in rainforest stream, tributary of Tully
River, 100 m, 50 km by road NW of Tully,
Queensland, Australia (145°38’E, 17o46’S).
Litoria rheocola Liem, 1974. KU 224685,
stage 26, dissection/cleared; KU 224686,
stage 27, cleared; KU 224687, stage 28, se-
rial sections; KU 224688, stage 37, cleared;
KU 224689, stage 39, cleared; KU 224690,
stage 41, serial sections; all specimens from
riffle in rainforest stream, tributary of Tully
River, 100 m, 50 mm by road NW of Tully,
Queensland, Australia (145°38’E, 17°46’S).
Litoria xanthomera Davies, McDonald and
Adams, 1986. KU 224691, stage 28, serial
sections; KU 224692 stage 28, dissection/
cleared; KU 224693, stage 34, cleared; KU
224694, stage 37, dissection/cleared; KU
224695, stage 31, cleared; all specimens from
pool on rainforest floor, Mt. Spec State For-
est, 800 m, 7 km NW of Paluma, Queens-
land, Australia (146°10’E, 18°59’S).
Nyctimystes dayi (Günther, 1897). KU
224696, stage 25 (32 mm), dissection/cleared;
KU 224697, stage 30, cleared; KU 224698,
stage 37, cleared; KU 224699, stage 37, se-
rial sections; all specimens from riffle in
rainforest stream, tributary of Tully River,
100 m, 50 km by road NW of Tully, Queens-
land, Australia (145°38’E, 17°46’S).
Hyla armata Boulenger, 1902. USMN
346276 (both): #1, stage 26 (54 mm), dissec-
tion/cleared; #2, stage 36, serial sections;
Peru, Cuzco, Paucartambo, 68 km (by road)
NE Puente Union on Rı́o Tachila (⫽ Bosque
de las Nubes, Km 150 on Paucartambo-
Atalaya Road), 1,700 m, at base of waterfall.
Boophis sp: KU 224700, stage 25 (49 mm),
dissection/cleared; KU 224701, stage 37, se-
rial sections, Madagascar, Fiarnarotsoa,
Ranomafana National Park, 6 km NE of
Ranomafana (R. Altig field notes #12103).