Zootaxa 370: 18 (2003) ISSN 1175-5326 (print edition)

www.mapress.com/zootaxa/
Copyright 2003 Magnolia Press
ZOOTAXA 370
ISSN 1175-5334 (online edition)

The tadpole of Physalaemus fuscomaculatus (Anura: Leptodactyl-

idae), with a description of internal oral morphology1

FAUSTO NOMURA2, DENISE DE CERQUEIRA ROSSA-FERES3 & VITOR HUGO

MENDONA DO PRADO4
1 This work was supported by the State of So Paulo Research Foundation (FAPESP), within the BIOTA/
FAPESP The Biodiversity Virtual Institute Program (http://www.biota.org.br)
2 Programa de Ps Graduao em Biologia Animal, UNESP, Campus de So Jos do Rio Preto,SP 15054-
000, email: fausto_nomura@yahoo.com.br
3 Departamento de Zoologia e Botnica, UNESP, Campus de So Jos do Rio Preto, SP 15054-000, Brazil;
denise@dzb.ibilce.unesp.br
4 Curso de Cincias Biolgicas, UNESP, Campus de So Jos do Rio Preto, SP 15040-000

Abstract

The external morphology and internal oral features of Physalaemus fuscomaculatus (Steindachner,
1864) tadpoles are described and compared with other species in the Physalalemus biligonigerus
group (Lynch, 1970). Tadpoles of P. fuscomaculatus have a morphology similar to other species
within this group and closely resemble those of P. santafecinus Barrio, 1965 and P. biligonigerus
(Cope, 1861). The tadpole of P. fuscomaculatus differs from those of the biligonigerus group by the
following characters: i) proportionally shorter tail compared to total length, ii) presence of two nar-
row ventral gaps on marginal papillae of the oral disc; iii) upper jaw sheath M- shaped; iv) presence
of two lingual papillae; v) two to three prepocket papillae, and vi) three to five pustulations anterior
to each buccal pocket. This is the first record of Physalaemus fuscomaculatus in southeastern Bra-
zil.

Key words. Physalaemus fuscomaculatus, tadpole, oral morphology, new record, distribution, Lep-
todactylidae, Anura

Introduction

Approximately three quarters of the 4,400 known species of anurans have a tadpole phase
at some stage of development (McDiarmid & Altig, 1999). For the majority of these spe-
cies, tadpoles are present in aquatic habitats for longer periods than breeding adults and are
often more easily collected (Altig & McDiarmid, 1999a). Consequently, larval sampling is

Accepted: 25 November 2003; published: 28 November 2003 1

ZOOTAXA a quick and efficient method of assessing local anuran biodiversity, but requires proper
370 identification of this phase of the anuran life-cycle (Altig & McDiarmid, 1999a). Unfortu-
nately, tadpole descriptions are available only for a third of anuran species; reference col-
lections, larval keys, and documentation of interspecifc variations are lacking (McDiarmid
& Altig, 1999; Altig & McDiarmid, 1999a). There is a particular need for descriptions of
tropical tadpoles. Furthermore, for the majority of species where the tadpole are known,
only external morphology has been described. Buccopharyngeal structures which have
taxonomic significance are rarely examined (McDiarmid & Altig, 1999).
Physalaemus fuscomaculatus (Steindachner, 1864) is a small-sized species (40.62
1.77 mm, n= 7) that occurs in Mato Grosso (Brazil), and the lowlands of adjacent Para-
guay and Bolivia (Frost, 2002). Its biology and ecology are little known. According to
Lynch (1970) and Frost (2002), Physalaemus fuscomaculatus, P. biligonigerus (Cope,
1861), P. nattereri (Steindachner, 1863), and P. santafecinus Barrio, 1965 comprise the
Physalaemus biligonigerus group. Tadpoles of the latter three species have been described
by Fernandez and Fernandez (1921), Vizotto (1967), and Perotti and Cspedez (1999),
respectively. Here we describe the tadpole of P. fuscomaculatus, present data on its exter-
nal morphology and internal oral features, and compare it with other tadpoles in biligoni-
gerus group.

Material and Methods

Physalaemus fuscomaculatus tadpoles were collected with a dipnet along unshaded edges
of a temporary pond (210440S; 493223W) in Nova Itapirema, So Paulo State, Bra-
zil, on 18/December/1989, 21 and 29/November/1994, and 20/December/1994. Analyses
of the external morphology, tadpole drawings, and photographs were based on tadpoles in
stages 3638 (Gosner, 1960). Morphological characters follow Altig and Johnston (1986;
1989), Johnston and Altig (1986), and McDiarmid and Altig (1999). Measurements were
made with an ocular micrometer at 16.0 x magnification, except for the total length, which
was measured with a caliper. For observations of the marginal papillae, the oral disc was
stained with a 1% methylene blue solution. Mouth parts were mounted on temporary slides
with Hoyers medium (Jeppson et al. 1975). Three tadpoles in stages 3738 were dis-
sected; the internal oral structures were stained with a 1% methylene blue solution and
observed under 40.0 x. The buccopharyngeal terminology follows Wassersug (1976). The
analyses of Physalaemus biligonigerus, P. nattereri and P. santafecinus tadpoles were
based on original descriptions, reinterpreted according to McDiarmid and Altig (1999).
Forty-three Physalaemus fuscomaculatus tadpoles in stages 30-40 (Gosner, 1960) are
deposited in the DZSJRP Collection, Department of Zoology and Botany, Universidade
Estadual Paulista, So Paulo State, Brazil (DZSJRP L-15A, L-116A, L-117B, L-120A and
L-120B).

2 2003 Magnolia Press NOMURA ET AL.

Description of the tadpole of Physalalemus fuscomaculatus ZOOTAXA

370
Measurements (mm). Mean and standard deviation (range) of 10 specimens at Gosner
(1960) developmental stage 38: total length 23.321.37 (22.025.59); body length 11.36
0.66 (10.0812.16); tail length 11.961.29 (10.5813.61); maximum body height 4.73
0.28 (4.165.12); maximum body width 5.950.27 (5.446.40); eye diameter 1.420.034
(1.361.44); nostril diameter 0.440.076 (0.320.56); interorbital distance 1.27 0.096
(1.121.44); internarial distance 0.82 0.039 (0.800.88); nostril snout distance 0.75
0.086 (0.640.88); eyesnout distance 1.760.18 (1.442.08); maximum dorsal fin height
2.140.23 (1.602.40); maximum ventral fin height 0.920.11 (0.801.09); maximum tail
muscle width 1.800.038 (0.830.93); maximum tail muscle height 2.500.11 (2.40
2.72).
External morphology. Body ovoid in dorsal view and globular/depressed in lateral
view (Fig. 1A and 1B). Snout rounded in dorsal and lateral view. Eyes relatively small,
dorsal, dorsolaterally directed. Nostrils large, rounded, with dorsally directed aperture.
Spiracle sinistral, long and narrow with free distal edge. Centripetal wall of the spiracle
tube fused to body wall, spiracular opening directed posterodorsally, on the middle third of
the body. Vent tube long, medial, attached to the ventral fin, with dextrally directed open-
ing.

FIGURE 1. Physalaemus fuscumaculatus tadpole at stage 35 (Gosner, 1960), (A) Dorsal view, (B)
Lateral view (scale = 10 mm).

Oral disc ventral (Fig. 2A), laterally emarginated. Marginal papillae in single row usu-
ally with a wide dorsal gap and two narrow ventral gaps. Ventral papillae number 8 to 18
(13.452.44, n = 33), and are in a single row (23.7%), alternate row (65.8%) or mixed of
both (10.5%); only 10% of 43 analyzed tadpoles examined lacked ventral gaps in the mar-
ginal papillae; one to five submarginal papillae, larger than marginal papillae, in unequal

PHYSALAEMUS TADPOLE 2003 Magnolia Press 3

ZOOTAXA number on each side of oral disc. Papillae long, conical, simple, with convex extremity.
370 Tooth row formula 2(2)/2(1); A-1 and A-2 rows subequal in length, P-2 slightly shorter
than P-1; A-2 and P-1 rows interrupted medially by a gap approximately three to four
labial teeth wide; tooth density 52/mm in A-1 row. Labial teeth dark, curved slightly
toward the oral opening, with five to seven cusps with slightly divergent tips (Fig. 2B and
2C). Jaw sheaths heavy, darkly pigmented; upper sheath M-shaped and the lower V-
shaped; upper jaw sheath with 40 serrations/mm on the edge, individual serration triangu-
lar, broad-based with equal sides.

FIGURE 2. Physalaemus fuscumaculatus tadpole (A) Oral disc (scale = 1 mm), (B) Lateral view
of a tooth of the A-2 row (scale = 100 m), (C) Ventral view of apical region of a tooth (scale = 20
m).

Caudal muscle heavy, higher than dorsal fin along the anterior third of the tail. Dorsal
fin moderate, with the same height of caudal musculature at the plane of tail-body junc-
tion, weakly convex, originating on the posterior third of the body; ventral fin low, nearly
parallel to tail muscle; tip narrowly rounded.
Coloration. In formalin, body brown, with dark spots forming a semicircular arch
around the internal margins of nostrils. Ventrally transparent. Caudal muscle light brown,
with dark brown dots with irregular distribution. A midlateral blood vessel, similar to a
thin dark stripe, lying on proximal fifth of the tail. Fins transparent, with slight reticulation
formed by blood vessels and with some dark brown marks, on dorsal and ventral fin edges.
In life, coloration very similar to that of preserved tadpoles, with the body, tail, and sickle-
shaped marks near the nostrils darker brown.
Internal oral features. Buccal floor triangular (Fig. 3A), about 20% wider than long;
oral aperture about 20% of buccal floor width; four infralabial papillae, the lateral pair
large, and the medial ones small, all papillae with pustulated margins. Two simple, conical,
lingual papillae, with rounded apices; buccal floor arena triangular, with four to six papil-
lae on each side, majority conical, with acute apices or with a slight projections; a bifur-
cate papilla, with acute apices, lateral to each buccal pocket and 30 to 40 pustulations

4 2003 Magnolia Press NOMURA ET AL.

randomly distributed within buccal floor arena; two to three short, conical papillae and ZOOTAXA

three to five prepocket pustulations; buccal pockets perforated, wider than long, tran- 370
versely oriented on middle region of buccal floor; free velar surface, about 20% of buccal
floor length, with three pustulations on each side. Glottis distinct, open, fully exposed.

FIGURE 3. Physalaemus fuscomaculatus tadpole (A) floor and (B) roof of buccopharyngeal cavity
(scale = 1 mm).

PHYSALAEMUS TADPOLE 2003 Magnolia Press 5

ZOOTAXA Buccal roof triangular (Fig. 3B), same shape as floor, broad posteriorly; prenarial
370 arena with two semicircular arches of pustulations separated by a moderate notch,
arranged in a V-shaped pattern, with vertex oriented posteriorly; nares elliptical, posi-
tioned at about 25% of the distance from oral disc to esophagus, in 25 orientation from
transverse plane; internarial distance about 50% of long axis of naris; narial-valve projec-
tion indistinct; anterior narial wall pustulate; posterior narial wall flap-like and twice as
wide as high; postnarial arena triangular and narrow with four papillae, one anteromedial
pair tall and conical, with pustulate anterior margin and the posterolateral pair short and
conical; median ridge semicircular, with pustulate free surface; lateral-ridge papillae claw-
shaped, with pustulate anterior margins; buccal roof arena narrow elongate rectangle;
bounded by three or four papillae on each side, all papillae conical, with truncate or acute
apices, distributed parallel to longitudinal plane; about 5060 pustulations randomly dis-
tributed; glandular zone conspicuous; dorsal velum long, interrupted on midline with
smooth free margin.
Habitat. In the northwestern region of So Paulo State, Brazil, males of Physalaemus
fuscomaculatus were observed calling during the early rainy season (October to Decem-
ber), in temporary, rain-filled ponds in pasture areas. In this region, males were not
detected every year, but are very abundant in those years they appear (Rossa-Feres, 1997).
Tadpoles were found along unshaded shallow (13.710.9 cm deep, n = 16) pond edges,
mostly in areas without vegetation.
These tadpoles are preponderantly nocturnal, benthonic, and have cryptic coloration.
They do not constitute aggregates and react quickly to predators, swimming a short dis-
tance and then stopping (personal observation). This set of characteristics is found in tad-
poles of other Physalaemus Fitzinger, 1826 species (e.g. P. pustulosus, Heyer et al. 1975;
P. nattereri, personal observation). The swimming behavior by rapid bursts is an efficient
means of avoiding invertebrate predators (Hoff et al. 1999; Azevedo-Ramos et al. 1992;
Heyer et al. 1975), which are abundant in temporary ponds (Buskirk, 1988; Pearman,
1995). Foam nests of Physalaemus fuscomaculatus were observed inside the ponds on the
water surface, anchored on emergent vegetation in the shallows; the foam nests had a
mean diameter of 10.56 cm2.56 SD (range = 714, n = 18 clutches) and 2036.67 479.62
eggs (range = 17402590, n = 3 clutches), with a mean diameter of 1.5 mm0.12 SD
(range = 1.321.82, n = 14 eggs).

Discussion

Three characters of the oral disc vary within the studied sample of P. fuscomaculatus tad-
poles: the presence of two narrow ventral gaps in the marginal papillae, the number and
distribution of ventral papillae, and the number and distribution of submarginal papillae.
Although intraspecific variations are poorly documented, the morphology of closely
related species often is remarkably consistent (Altig & McDiarmid, 1999b). The function
of gaps in the marginal papillae is not known but, according to Altig and McDiarmid
(1999b), occurs in phylogenetically related taxa.

6 2003 Magnolia Press NOMURA ET AL.

 Tadpoles of P. fuscomaculatus closely resemble those of P. santafecinus and P. bili- ZOOTAXA

gonigerus; they are short (total length) and have only two posterior rows of labial teeth. 370
These features distinguish them from P. nattereri. The tadpoles of P. fuscomaculatus differ
from those of P. santafecinus and P. biligonigerus by the: i) shorter tail (proportion tail
length/total length), ii) presence of two narrow ventral gaps on marginal papillae of oral
disc, and iii) a M- shaped upper jaw sheath.
Within Physalaemus, the internal oral features are known for five species: Physalae-
mus petersi and P. pustulosus (Wassersug & Heyer, 1988), P. nattereri (Spirandelli-Cruz,
1991), P. santafecinus and P. biligonigerus (Perotti & Cspedez, 1999). As with the exter-
nal morphology, the internal oral features of P. fuscomaculatus closely resemble those of
P. santafecinus tadpoles, mostly in terms of the number of pustulations on buccal floor; the
presence of two semicircular arches of pustulations separated by a moderate notch, and
arranged in a V-shaped pattern in the prenarial arena; the presence of two postnarial papil-
lae, with the anteromedial pair large and tall and the posterolateral pair small; the semicir-
cular shape of medium ridge; and the lateral-ridge papillae claw-shaped. Physalaemus
fuscomaculatus tadpoles differ from those of other species of this genus by the presence of
two lingual papillae, two to three prepocket papillae, and three to five pustulations anterior
to each buccal pocket.
The external morphology and internal oral features of Physalaemus fuscomaculatus
are similar to the other species of the Physalaemus biligonigerus group: body shape; fin
shape and height; color pattern; triangular shape of the buccal floor, wider than long; pres-
ence of four infralabial papillae with irregular margins, one pair anteromedial and one pos-
terolateral; nares positioned at about 25% of the distance from oral disc to esophagus, with
pustulate anterior wall and wide, flap-like posterior wall; and conspicuous glandular zone.
These findings suggest that larval characteristics have taxonomic importance. More-
over, the set of morphological characteristics which characterize tadpoles of Physalaemus
biligonigerus group are probably also related to habitat and microhabitat, since P. fusco-
maculatus tadpoles were found in similar kinds of ponds and microhabitats as those
described for P. biligonigerus, P. santafecinus and P. nattereri (Vizotto, 1967; Perotti &
Cspedez, 1999). Detailed studies of diet and feeding behaviors of these tadpoles are
needed in order to understand the function of and variation in buccopharyngeal features.
This is the first record of Physalaemus fuscomaculatus in southeastern Brazil, and rep-
resents an outlier population from the known distribution of Physalaemus fuscomaculatus.
Presumably other populations occur between the previously known range and this new
locality.

Acknowledgements
We thank A.B. Cady (Miami University, Ohio, USA) for critical review of the manuscript and help-
ful suggestions; F.A. Hernandes for the computer hardware assistance. Research support was pro-
vided by Fundao de Amparo Pesquisa do Estado de So PauloFAPESP: grants 01/07944-7
(D.C.R.F.) and 02/05426-1 (V.H.M.P.), and by Coordenao de Aperfeioamento de Pessoal de
Nvel SuperiorCAPES grant 3300415-3 (F.N.).

PHYSALAEMUS TADPOLE 2003 Magnolia Press 7

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