Zootaxa,Redescription of the tadpoles of three ...

Zootaxa 1638: 1–20 (2007) www.mapress.com / zootaxa/

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Redescription of the tadpoles of three species of frogs from Uruguay (Amphibia: Anura: Leiuperidae and Leptodactylidae), with notes on natural history CLAUDIO BORTEIRO1 & FRANCISCO KOLENC2 1

Río de Janeiro 4058, Montevideo 12800, Uruguay. E-mail: [email protected] Universidad de la República, Montevideo, Uruguay. Universidad Católica del Uruguay, Montevideo, Uruguay. E-mail: [email protected]

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Abstract In this work the tadpoles of the neotropical frogs Leptodactylus latinasus, Physalaemus biligonigerus and Physalaemus riograndensis are redescribed. Relevant features of L. latinasus tadpoles are a medial vent tube, labial tooth row formula (LTRF) 2(2)/3(1), and oral disc with a single row of marginal papillae interrupted by a dorsal gap, similarly to other species within the L. fuscus species group. Tadpoles of P. riograndensis have a medial vent tube, LTRF 2(2)/2(1), oral disc with single row of marginal papillae, interrupted by a dorsal gap and usually two ventrolateral gaps. The tadpole of P. biligonigerus has a dextral vent tube, the oral disc presents a single row of marginal papillae (sometimes double ventrally) with dorsal gap, and LTRF 2(2)/2(1). Although considered relevant for the taxonomy of Physalaemus, character variation of larval external morphology is incongruous with the phenetic species group arrangements proposed up to date. A reproductive mode previously unreported for P. riograndensis and P. henselii was observed: foam nests in the humid ground outside ponds. We also report the display of deimatic behavior in L. latinasus, L. ocellatus, P. henselii, and P. biligonigerus, in the last case with exhibition of the eye-like inguinal glands. Key words: Leptodactylus latinasus, Physalaemus biligonigerus, Physalaemus riograndensis, larval morphology, distribution, defensive behavior, reproductive mode

Introduction The knowledge of tadpole morphology is a valuable tool for different biological studies, i.e., taxonomic, ecological, biogeographic and faunistic inventories (Altig & McDiarmid 1999; Haas 2003; Frost et al. 2006; Rossa-Feres & Nomura 2006). The external morphology of the tadpoles of some well known neotropical frogs was described early in the 20th century in pioneer works (i.e., Budgett 1899; Fernández & Fernández 1921; Fernández 1927) which were sometimes reproduced in more recent monographs (Cei 1980), and are still the source of information about these species. Despite being very valuable, these early descriptions were based on a single or few individuals not taking into account intraspecific variation, usually without morphometrics and complete illustrations, thus limiting interspecific comparisons with more recent works. An example is the tadpole of the common and widespread South-American frog Leptodactylus latinasus Jiménez de la Espada (Leptodactylidae, L. fuscus group, Fig. 1 A) which was studied by Fernández and Fernández (1921) on material from Buenos Aires Province, Argentina (as L. prognathus Boulenger). These authors provide a general description of external morphology along with an illustration of the oral disc. In a recent review of the tadpoles of the L. fuscus group (Langone & de Sá 2005), those of two other species were redescribed, showing important intraspecific variation when compared with previous descriptions, but the work of Fernández and Fernández (1921) remained as the sole source of information about L. latinasus. Recently, Vera Candioti et al.

Accepted by M. Vences: 8 Oct. 2007; published: 14 Nov. 2007

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(2007), while describing the tadpole of another species of the L. fuscus group, noticed some differences between the samples of L. latinasus available to them and the data provided by Fernández and Fernández (1921); we observed the same features in samples from the type locality of the species (Montevideo, Uruguay). A similar case is that of the tadpole of Physalaemus biligonigerus (Cope) (Leiuperidae, Fig. 1 B), which was also described by Fernández and Fernández (1921) (as Paludicola fuscomaculata Steindachner) based on specimens collected in Santa Fe Province, Argentina. This early work, or its later reproduction by Cei (1980), was used for comparative purposes in recent descriptions of Physalaemus tadpoles (Alcalde et al. 2006; Both et al. 2006). A different case is that of P. riograndensis Milstead (Fig. 1 C, D), a still little known Leiuperidae, whose tadpole was recently described by Prigioni and García (2002) based on a single specimen from La Coronilla, Department of Rocha, Uruguay. The analysis of additional samples from Uruguay revealed significant variation in some character states regarding those reported by Prigioni and García (2002) mainly in the oral disc configuration; this is worth noticing due to the informative value of those structures in species recognition within Physalaemus (Alcalde et al. 2006; Kolenc et al. 2006). The purpose of this work is to redescribe the tadpoles of Leptodactylus latinasus, Physalaemus biligonigerus and P. riograndensis from Uruguay; in the former case from the type locality, Montevideo. We also provide some observations on natural history and geographic distribution of these and some allied taxa in Uruguay.

Material and methods Specimens used in this work were fixed in formalin (10%) and are stored at the Batrachians Collection of the Vertebrates Zoology Department (ZVCB) of the Faculty of Sciences, Universidad de la República, Montevideo, Uruguay. Tadpole descriptions are based on the following specimens: 10 tadpoles of Leptodactylus latinasus at stages 34–35, collected in a temporary pond on 26 December 2005 by C. Borteiro in the surroundings of Estadio Luis Tróccoli, Villa del Cerro, Department of Montevideo, Uruguay, 34º51.985’S, 56º15.116’W, 12 m above sea level (a.s.l.) (ZVCB 15186); six tadpoles of Physalaemus biligonigerus at stages 34–36, collected in a semi permanent pond on 4 March 2007 by C. Borteiro, F. Kolenc, M. Tedros and C. Prigioni in the surroundings of Quebrada de los Cuervos, Department of Treinta y Tres, Uruguay, 32º57.868’S, 54º27.254’W, 185 m a.s.l. (ZVCB 15192, ZVCB 15191); and 10 tadpoles of P. riograndensis at stages 31–36, collected in a temporary pond on 10 January 2003 by C. Borteiro, F. Kolenc and M. Tedros, at Cooperativa Azucarera del Litoral Norte del Uruguay (CALNU), Department of Artigas, Uruguay, 30º19.857’S, 57º37.226’W, 65 m a.s.l. (ZVCB 15196). Species identity of tadpole samples was confirmed with some individuals reared through metamorphosis (L. latinasus ZVCB 15188, P. biligonigerus ZVCB 15194, P. riograndensis ZVCB 15199), and with adults from the same site (L. latinasus ZVCB 15189, P. riograndensis ZVCB 15201). Drawings were made using a stereoscopic microscope Nikon SMZ–10 with a camera lucida. Morphological terminology follows that of Altig and McDiarmid (1999). Tadpole developmental stages follow the staging Gosner table (1960). Lateral line system nomenclature follows that of Lannoo (1987). The oral disc was stained with a 1% methyl blue solution for proper visualization of the marginal papillae. Twenty morphometric variables were registered for tadpoles from all visited localities, seven of them according to Altig and McDiarmid (1999): total length (TL), body length (BL), tail length (TAL), tail fin height (FH), internarial distance (IN, measured between the external edges of narial apertures), interorbital distance (IOD, measured between the external edges of pupils), tail musculature width (TMW). The remaining measurements were recorded as follows (according to Lavilla & Scrocchi 1986): body maximum width (BMW), body width at nostrils (BWN), body width at eye level (BWE), body maximum height (BMH), rostro-spiracular distance (RSD, measured horizontally from tip of the snout to the posterior edge of the tube), fronto-nasal distance (FN, from the tip of the snout to the anterior edge of nostrils), eye-nostril distance (END, from the posterior

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edge of nares to the anterior edge of eyes), nostril major axis (N), eye diameter (E), extra nasal distance (EN, distance between external edges of nares), intraocular distance (IO, distance between interior edges of eyes), oral disc width (OD), and dorsal gap length (DG). Measurements were made to the nearest 0.1 mm using a microscope with a scaled objective except for TL, which was measured with a caliper. We studied additional and comparative material listed in Appendix 1, including 15 nests of Physalaemus riograndensis which were measured at field with calipers and then fixed in 10% formalin.

FIGURE 1. A. Leptodactylus latinasus (male) from type locality, Montevideo, Uruguay, February 2007. ZVCB 15189 (Photo: C. Borteiro). B. Physalaemus biligonigerus (male), Bañado de los Oliveras, Treinta y Tres, Uruguay, January 2006. ZVCB 15195 (Photo: A. Sosa). C. Physalaemus riograndensis (male), Valizas, Rocha, Uruguay, 11 March 2007 (Photo: F. Kolenc). D. Foam nest construction in P. riograndensis, Departamento Candelaria, Misiones, Argentina, October 2006 (Photo: D. Baldo).

Results Description of tadpoles Leptodactylus latinasus Tadpole external morphology. The tadpoles of Leptodactylus latinasus (Fig. 2 A, B) belong to the benthic ecomorphological guild (section II: A: 1) of McDiarmid and Altig (1999) as revised from Altig and Johnston (1989). Tadpoles at stages 34–36 are about 23.1 ± 2.0 mm of total length, and they have a depressed body

REDESCRIPTION OF THREE TADPOLES FROM URUGUAY

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FIGURE 2. The tadpole of Leptodactylus latinasus, stage 34, ZVCB 15186. A. Lateral view. B. Dorsal view. C. Oral disc. Scale bars = 5 mm (A, B), and = 1 mm (C).

(BMH/BMW = 0.75 ± 0.13). The body length is about 40% of total length (BL/TL = 0.40 ± 0.02), body shape is ovoid in dorsal view and the maximum width is placed at the beginning of the spiracular tube. In lateral view, the ventral contour of the body is slightly convex. The snout is slightly truncated in dorsal and lateral views. The nostrils are oval; they are dorsolaterally positioned (EN/BWE = 0.74 ± 0.02), closer to the tip of the snout than to the eyes (FN/END = 0.63 ± 0.10), more visible laterally than dorsally and its opening is laterodorsally directed. The eyes are large (E/BWE = 0.47 ± 0.02) and dorsolateral (IOD/BWE = 0.65 ± 0.19), not visible from ventral view. Pineal organ and lateral line system were not visible. The spiracle is single, lateral, sinistral, short, with its inner wall entirely fused to the body, and it is placed at the middle of the body length (RSD/BL = 0.56 ± 0.02), posterodorsally directed; its opening is oval, with a small elevated rim, being its diameter slightly smaller than the tube diameter, and is visible only laterally. The intestinal assa was usu-


BORTEIRO & KOLENC

ally observed approximately at the center of the abdominal ventral surface, but in two exemplars was left sided. The vent tube is medial, and in one specimen it opened to the left due to a fold in the origin of the ventral fin. The tail is large (TAL/TL = 0.60 ± 0.02), and both fins are slightly higher than the body height (FH/ BMH = 1.19 ± 0.47). The dorsal fin originates at the body-tail junction and it has a regularly curved, convex free margin. The ventral fin originates from the longitudinal axis of the posterior wall of the vent tube and its free margin is convex. The tail axis is straight, and the tail smoothly stretches towards the tip, ending rounded. The tail musculature almost reaches the tail end. The oral disc (Fig. 2 C) is anteroventral, medium sized (OD/ BMW = 0.37 ± 0.03), lacks lateral constrictions (not emarginated) and has a large dorsal gap (DG/OD = 0.62 ± 0.02). Marginal papillae are usually arranged in a single row on both sides of the dorsal gap, in a double row in sub angular regions, and in a single or double row in the ventral portion of the oral disc. Papillae are simple, longer than wide, subconical, with rounded tip. Submarginal papillae are absent. The upper jaw sheath is widely arch-shaped, and the lower jaw sheath is V-shaped. Both jaw sheaths are well developed, finely serrated and heavily pigmented on their distal halves. Labial tooth row formula is 2(2)/3(1), the gap present in A2 is wide but that of P1 is very narrow. The length of P3 is about a half to two thirds the length of other tooth rows. Measurements are shown in Table 1. TABLE 1. Measurements (in millimeters) of tadpoles of Leptodactylus latinasus, Physalaemus riograndensis and Physalaemus biligonigerus from Uruguay (mean ± standard deviation, range given in parentheses); see measurement explanation in the text. Variable

L. latinasus (Montevideo, n = 10, stages 31–36)

P. riograndensis (Artigas, n = 10, stages 31–36)

P. biligonigerus (Treintay Tres, n = 6, stages 34–36)

TL

23.1 ± 2.0 (19.6–26.4)

14.7 ± 1.0 (12.8–15.9)

23.6 ± 1.3 (21.4–25.0)

BL

9.1 ± 0.7 (7.8–10.0)

5.8 ± 0.4 (5.0–6.3)

10.2 ± 0.7 (9.4–11.2)

TAL

13.9 ± 1.5 (11.8–16.7)

8.9 ± 0.7 (7.8–10.0)

16.9 ± 1.1 (15.2–18.0)

BMW

5.4 ± 0.4 (4.4–5.9)

4.0 ± 0.2 (3.7 –4.2)

7.2 ± 0.5 (6.5–7.9)

BWE

2.3 ± 0.1(2.1–2.5)

3.2 ± 0.2 (2.9–3.5)

5.5 ± 0.4 (5.0–6.0)

BWN

5.1 ± 0.7 (4–6.2)

2.1 ± 0.1 (1.9–2.3)

3.8 ± 0.3 (3.4–4.3)

BMH

4.1 ± 0.9 (1.8–4.9)

2.9 ± 0.2 (2.6–3.1)

5.7 ± 0.3 (5.3–6.2)

FH

4.5 ± 0.4 (4.0–5.0)

3.2 ± 0.2 (2.9–3.6)

5.9 ± 0.4 (5.5–6.3)

RSD

5.1 ± 0.4 (4.4–5.4)

3.8 ± 0.3 (3.3–4.2)

6.6 ± 0.7 (5.8–7.7)

FN

0.6 ± 0.1 (0.5–0.8)

0.4 ± 0.1 (0.4–0.5)

1.0 ± 0.2 (0.7–1.4)

END

0.9 ± 0.1 (0.9–1.0)

0.4 ± 0.0 (0.4–0.5)

0.8 ± 0.1 (0.7–0.9)

N

0.2 ± 0.0 (0.2–0.3)

0.3 ± 0.0 (0.3–0.4)

0.3 ± 0.0 (0.2–0.3)

E

1.0 ± 0.1 (0.9–1.2)

0.9 ± 0.1 (0.6–1.0)

1.5 ± 0.1 (1.3–1.6)

EN

1.7 ± 0.1 (1.6–1.8)

1.1 ± 0.1 (1.1–1.3)

1.5 ± 0.1 (1.4–1.5)

IN

1.2 ± 0.1 (1.1–1.4)

0.6 ± 0.1 (0.5–0.7)

1.0 ± 0.2 (0.9–1.4)

IOD

1.5 ± 0.4 (1.0–2.4)

2.1 ± 0.1 (1.9–2.3)

3.4 ± 0.4 (2.9–4.0)

TMW

1.7 ± 0.1 (1.5–2.0)

1.1 ± 0.1 (0.9–1.2)

2.0 ± 0.1 (1.9–2.2)

IO

0.8 ± 0.3 (0.7–1.7)

0.9 ± 0.1 (0.9–1.0)

1.5 ± 0.1 (1.3–1.6)

OD

2.0 ± 0.1 (1.9–2.2)

1.2 ± 0.1 (1.1–1.4)

2.0 ± 0.2 (1.8–2.3)

DG

1.3 ± 0.1 (1.0–1.4)

0.8 ± 0.1 (0.8–1.0)

1.3 ± 0.1 (1.2–1.5)

Tadpole in vivo coloration. The body is brown dorsally and laterally with greenish shines, with a light fine reticulated black pattern visible with magnification. The ventral surface of the body is yellowish with scarce dark pigmentation, and greenish and golden shines. Caudal musculature is brown, also with greenish shines



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and ventral irregular yellowish areas in the first half. Both fins are irregularly pigmented with dark blotches, which are less intense in the anterior part of the ventral fin. The iris is light yellow. Tadpole coloration in preservative. The body and caudal musculature coloration turns light brown. The ventral surface of the body has a less intense coloration and unpigmented areas in the gular region and in the centre of the abdomen. The coloration of both fins lightens and the small dark blotches of melanophores are more numerous along the upper half of the dorsal fin. The myomers become more evident in the two distal thirds of the tail. Tadpole morphological variation: Lot ZVCB 15187, three tadpoles at stage 40, papillation and LTRF present the same characteristics as in lot ZVCB 15186.

Physalaemus biligonigerus Tadpole external morphology. The tadpoles of Physalaemus biligonigerus (Fig. 3 A, B) belong to the benthic ecomorphological guild (section II: A: 1) of McDiarmid and Altig (1999) as revised from Altig and Johnston (1989). At stages 34–36 they are about 23.6 ± 1.3 mm of total length, and they have a depressed body (BMH/ BMW = 0.79 ± 0.03). The body length is about 40% of total length (BL/TL = 0.43 ± 0.02), body shape is ovoid in dorsal view and the maximum width is placed at the middle of the body. In lateral view, the ventral contour is slightly convex in the gular region and convex in the branchial and abdominal regions. The snout is slightly rounded in dorsal view, and truncated in lateral view. The nostrils are rounded and placed in a depression; they are dorsolaterally positioned (EN/BWE = 0.28 ± 0.02), closer to the eyes than to the tip of the snout (FN/END = 1.24 ± 0.41), more visible dorsally than laterally. Their openings are anterodorsally directed and present a slightly elevated marginal rim. The eyes are large (E/BWE = 0.28 ± 0.01) and dorsal (IOD/BWE = 0.63 ± 0.03), dorsolaterally oriented and not visible from ventral view. Pineal organ is not visible. The spiracle is single, lateral, sinistral, short, posterodorsally directed and placed in the second third of the body (RSD/BL = 0.64 ± 0.04), with its inner wall fused to it except for the distal end; its opening is rounded or oval, placed approximately at the body midline, being its diameter smaller than the tube diameter, and it is visible laterally and dorsally. The intestinal assa was observed approximately at the center of the abdominal ventral surface or slightly displaced to the left. The vent tube is dextral; it starts at midline but runs on the right side of the longitudinal axis, and is attached to a fold of the ventral fin. A weakly noticeable transversal skin fold separates the vent tube from the abdominal skin. The tail is large (TAL/TL = 0.72 ± 0.02), and both fins are slightly higher than the body height (FH/BMH = 1.04 ± 0.06). The dorsal fin originates on the body-tail junction or slightly anteriorly to it, and has a regularly curved, convex free margin. It is somewhat higher than the ventral fin, which originates from the longitudinal axis of the posterior wall of the vent tube, and presents a smoothly convex free margin, almost flat. The tail axis is straight, and the tail smoothly stretches towards the tip in its last third, ending acutely rounded. The tail musculature almost reaches the tail end, and myomeres are more visible in the distal half. Neuromasts of the angular, anterior oral, supraorbital, infraorbital, dorsal, middle and ventral lines are weakly visible. The middle line extends over the tail musculature for a short run, and the dorsal one over the first third of the dorsal fin. The oral disc (Fig. 3 C) is anteroventral, small (OD/BMW = 0.27 ± 0.02), emarginated, and has a large dorsal gap (DG/OD = 0.66 ± 0.02). Marginal papillae are arranged in a single row on both sides of the dorsal gap and angular region; they are in single (sometimes alternate) and/or double row in the ventral region. Papillae are simple, longer than wide, subconical, with rounded tip. Submarginal papillae are absent. The upper jaw sheath is convex in the middle, near trapezoid, and the lower jaw sheath is U-shaped. Both jaw sheaths are finely serrated and pigmented distally for about 1/3 of their widths. Labial tooth row formula is 2(2)/2(1), P2 is slightly shorter than P1, the gap in A2 is evident but that of P1 is very narrow. In one specimen, A2, P1 and P2 were fragmented because of developmental alterations, and in another one (ZVCB 15192), several teeth of P1 and P2 were lost and the lower jaw sheath was unpigmented. Measurements are shown in Table 1.


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FIGURE 3. The tadpole of Physalaemus biligonigerus, stage 34, ZVCB 15191. A. Lateral view. B. Dorsal view. C. Oral disc. Scale bars = 5 mm (A, B), and = 1 mm (C).

Tadpole coloration in preservative. The body is light brown dorsally, slightly darker at the midline, but more markedly darker in the abdominal region. Irregular small blotches of melanophores are present in the dorsal region of the snout and laterally in the branchial regions. The ventral surface is almost unpigmented, and allows visualization of the viscera. The caudal musculature is yellowish-brown with small dark areas dorsally that can come into sight as transverse bands; laterally an irregular reticulated pattern is present, with REDESCRIPTION OF THREE TADPOLES FROM URUGUAY


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more extended light areas in the first third. The dorsal fin is irregularly and slightly pigmented, with a lower density of melanophores in the middle. The ventral fin is scarcely pigmented, mainly along a narrow band parallel to the margin of the two last thirds of the tail. Tadpole morphological variation: Lot ZVCB 15193, three tadpoles at stage 40, one of them exhibits a labial tooth row formula 2(2)/2; in another one, A2, P1 and P2 are fragmented because of developmental alterations, a single submarginal papillae with a few labial teeth is present, and the intestinal assa was on the left side of the abdominal ventral surface.

Physalaemus riograndensis Tadpole external morphology. The tadpoles of Physalaemus riograndensis (Fig. 4 A, B) belong to the benthic ecomorphological guild (section II: A: 1) of McDiarmid and Altig (1999) as revised from Altig and Johnston (1989). At stages 31–36 they are about 14.7 ± 1.02 mm of total length, and they have a depressed body (BMH/ BMW = 0.73 ± 0.03). The body length is about 40% of total length (BL/TL = 0.39 ± 0.01), body shape is ovoid or oval in dorsal view and the maximum width is placed just behind the cephalic region. In lateral view, the ventral contour of the body is slightly convex, near flat. The snout is rounded in dorsal and lateral views. The nostrils are rounded; they are dorsolaterally positioned (EN/BWE = 0.35 ± 0.02), at mid distance between the tip of the snout and the eyes (FN/END = 1.09 ± 0.18), more visible dorsally than laterally. The opening is anterodorsally directed and presents a slightly elevated and unpigmented rim, with a small, elevated and pigmented fleshy projection in the medial margin. The eyes are large (E/BWE = 0.26 ± 0.03) and dorsolateral (IOD/BWE = 0.65 ± 0.02), not visible from ventral view. Pineal organ and lateral line system were not observed. The spiracle is single, lateral, sinistral, short, posterodorsally directed and placed in the second third of the body (RSD/BL = 0.67 ± 0.03), with its inner wall fused to it except for its very distal end; its opening is oval, placed just behind body midline, being its diameter slightly smaller than the tube diameter, and it is visible laterally, sometimes dorsally. The intestinal assa was observed approximately at the center of the abdominal ventral surface. The vent tube is medial; in one specimen it opened to the left and in another one it opened to the right due to a fold in the origin of the ventral fin; it is separated from the abdominal skin by a weak fold interrupted at the midline. The tail is large (TAL/TL = 0.61 ± 0.01), and both fins are slightly higher than the body height (FH/BMH = 1.08 ± 0.08). The dorsal fin originates slightly anteriorly to the body-tail junction and it has a regularly curved, convex free margin, and is somewhat higher than the ventral fin. The ventral fin originates from the longitudinal axis of the posterior wall of the vent tube and its free margin is smoothly convex. The tail axis is straight, and the tail smoothly stretches towards the tip, ending rounded. The tail musculature almost reaches the tail end. The oral disc (Fig. 4 C) is anteroventral, small (OD/BMW = 0.29 ± 0.02), emarginated, and has a large dorsal gap (DG/OD = 0.71 ± 0.07). Marginal papillae are arranged in a single row, alternate in subangular regions. Two ventrolateral gaps were present in all but one example, one at each side of the oral disc, usually separated by few marginal papillae (2–10). Papillae are simple, longer than wide, subconical, with rounded tip. Submarginal papillae are absent. The upper jaw sheath is widely arch-shaped, and the lower jaw sheath is V-shaped. Both jaw sheaths are finely serrated and pigmented distally for about 1/ 5 to 1/4 of their widths. Labial tooth row formula is 2(2)/2(1), the gap in A2 is evident but that of P1 is very narrow, and P2 is about 2/3 the length of the other rows. Measurements are shown in Table 1. Tadpole coloration in preservative. The body and caudal musculature are brownish dorsally, with small darker spots along the dorsal midline which are more or less defined. Laterally, the body and tail musculature pigmentation become more irregular, especially below the body midline. The ventral surface of the body presents scarce marginal pigmentation, mainly in the gular and branchial regions. The centre of the abdomen is almost unpigmented and internal organs are visible. Both fins are scarcely pigmented, with small and sparse groups of melanophores.


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Tadpole morphological variation: Lot ZVCB 15198, papillation and LTRF with the same characteristics as lot 15196. Tadpoles of Lot ZVCB 15197 has the same LTRF but three examples have a double row of marginal papillae in infraangular regions, one of them also exhibits double row of papillae in mental region and two submarginal papillae, another one has no ventrolateral gaps; two examples have the vent tube left sided.

FIGURE 4. The tadpole of Physalaemus riograndensis, stage 34, ZVCB 15196. A. Lateral view. B. Dorsal view. C. Oral disc. Scale bars = 5 mm (A, B), and = 1 mm (C).

Natural history observations The tadpoles of Leptodactylus latinasus were captured in a temporary, shallow and muddy pond in an urban area in the outskirts of Montevideo. Tadpoles of other species were not found in that place, although Rhinella REDESCRIPTION OF THREE TADPOLES FROM URUGUAY


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arenarum (Hensel), Physalaemus gracilis (Boulenger) and Hypsiboas pulchellus (Duméril and Bibron) are present in the surrounding areas. However, tadpoles of L. latinasus and L. ocellatus (Linnaeus) were observed in the same pond during the following breeding season (January 2007). In the Department of Artigas, northwestern Uruguay, breeding males of L. latinasus were present in great numbers in other types of anthropized habitats: flooded rice and sugar cane crops (ZVCB 15190). The tadpoles of Physalaemus biligonigerus were collected in an artificial pond by the road in a hilly area, along with tadpoles of Scinax granulatus (Peters), S. uruguayus (Schmidt), Pseudopaludicola falcipes (Hensel) and Odontophrynus americanus (Duméril and Bibron). The tadpoles of Physalaemus riograndensis from CALNU, Department of Artigas, were captured in a temporary pond within an agriculture area, next to flooded sugar cane crops. At this site, calling males, nests, and tadpoles (ZVCB 15204) were observed in sugar cane crops flooded by irrigation. Adult specimens were also collected on the shoreline of agriculture impoundments used for irrigation of rice at a near locality (ZVCB 15208). In the Departments of Treinta y Tres and Artigas, this species was found to inhabit marshes satellite to rivers and streams, and in flooded plains of the Merín Lake and Uruguay River drainages, in eastern and northern Uruguay respectively (ZVCB 15206, 15207, 15209, 15211). Breeding specimens were also captured in sandy temporary ponds and marshes of coastal plains, very close to the Atlantic Ocean in Barra de Valizas and La Coronilla, Department of Rocha, southeastern Uruguay (ZVCB 15210, 15212). The nests of P. riograndensis (Fig. 5 A) were found in small and shallow water bodies in natural grasslands and in flooded sugar cane crops of anthropized areas (ZVCB 15202, 15203). They are small, major and minor axes are about 40.5 ± 6.7 and 34.5 ± 5.7 mm respectively (ZVCB 15202, 15203, n = 11) and most of them were found floating inside the ponds (12/15, 80%), anchored or not to the emergent vegetation. Three nests were found on the ground, between the vegetation outside the ponds, at a distance of 2.5, 3.5 and 33.5 cm from the water edge. The eggs of P. riograndensis are moderately pigmented (greyish) and mean number of eggs per nest was 225 ± 121 (range 106–546, n = 15, ZVCB 15200, 15202, 15203, 15205). Calling sites in P. riograndensis are located in relatively open areas of ponds, and males vocalize during day and night. Foam nests on humid ground outside the ponds were also repeatedly observed by the authors in another small species of Physalaemus, P. henselii (Peters) at Barra de Valizas, Department of Rocha (Fig. 5 B). Most frequently, the nests of this species were found floating on ponds, hidden at the base of dense mats of vegetation (mostly Cyperaceae and Poaceae) or even under a thick vegetal stratum mainly composed by dead material which almost completely covered the shallow ponds (Fig. 5 C). Males of P. henselii usually vocalized hidden inside vegetation mats being very difficult to locate, and in several occasions they were observed calling just next to a foam nest. Males of this species vocalize mainly at night but can be heard also during day. The display of deimatic behavior was observed and documented in Leptodactylus latinasus, Physalaemus biligonigerus, and also in the allied species L. ocellatus and P. henselii. An adult male of L. latinasus was found under a small rock in a hilly area of Sierra de las Ánimas, Department of Maldonado, Uruguay (34º44’S, 55º19’W, 411 m a.s.l., 11 September 2005). As we lifted the rock, it immediately arched the dorsum, while keeping the head downwards (Fig. 5 D). Similar behavior was observed in an adult L. ocellatus at San José de Mayo, Department of San José, Uruguay (34º20’S, 56º42’W, on 5 November 2006); when attempted to be captured, it elevated the posterior part of the body and kept still for several minutes until finally escaped (Fig. 5 E). The defensive posture of P. biligonigerus was documented while handling a captive adult male that was collected at Bañado de los Oliveras, Department of Treinta y Tres (ZVCB 15195) and also consisted of puffing up the body and arching the dorsum, but in this case with a notorious exhibition of the bright black spots of the inguinal glands (Fig. 5 F). The defensive display of P. henselii (Peters) (ZVCB 15213) was observed in a female at Barra de Valizas, Department of Rocha and similarly consisted on elevation of the pelvic region while keeping the head on the ground (Fig. 5 G). When capturing it, it remained immobile feigning being dead (Fig. 5 H).


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Discussion Leptodactylus latinasus belongs to the L. fuscus species group, which is composed of 25 species; larval external morphology has been described in most of them (see Vera Candioti et al. 2007 and references therein). The tadpoles of L. latinasus collected at its type locality are similar to those described by Fernández and Fernández (1921) from Argentina, but differ in the labial tooth row formula (LTRF). We observed only the LTRF arrangement 2(2)/3(1), as also did Vera Candioti et al. (2007), while Fernández and Fernández (1921) reported a LTRF 2(2)/3. Larval external morphology of Leptodactylus latinasus is very similar to that of other species within the L. fuscus group: tadpoles are cryptically colored, the oral disc has a single row of marginal papillae, sometimes double in the ventral region, and LTRF is usually 2(2)/3 or 2(2)/3(1) (Langone & de Sá 2005; Bilate et al. 2006; Prado & d’Heursel 2006; Vera Candioti et al. 2007, and references therein). Tooth rows P2 and P3 may appear fragmented in L. gracilis (Duméril & Bibron) and L. mystacinus (Burmeister) by non-medial gaps with missing teeth (Langone & de Sá 2005). Larval morphology in the Leptodactylus fuscus group was reviewed by Langone and de Sá (2005), who suggested that external larval character variation of Leptodactylus do not fit in with the species group arrangements currently considered for this genus. Conversely, Prado and d’Heursel (2006) summarized the available information about Leptodactylus larvae finding that it could be phylogenetically informative. They observed that apart from some exceptions and interpopulational differences, morphological and behavioral character variation between species generally coincide with the currently recognized phenetic groups proposed by Heyer (1969): the L. fuscus, L. melanonotus, L. ocellatus, and L. pentadactylus species groups. The tadpoles of the L. melanonotus species group are darkly colored, with double row of ventral marginal papillae, and LTRF usually 2(2)/3 (L. melanonotus [Hallowell] and L. silvanimbus McCranie, Wilson & Porras; and also 2/ 3 in L. podicipinus [Cope], Prado & d’Heursel 2006). Tadpoles of the L. ocellatus group (L. ocellatus and L. chaquensis Cei) have a 2/3 formula, a double row of ventral marginal papillae, are also darkly colored, and, as in the L. melanonotus group, they form noticeable and coordinated schools (Cei 1980; Vaz-Ferreira & Gehrau 1986; Wells & Bard 1988; Prado et al. 2000; Prado & d’Heursel 2006). Tadpoles of the L. pentadactylus group are cryptically colored, have a single row of marginal papillae (double in L. syphax Bokermann; Eterovick & Sazima 2000), and LTRF 2(2)/3(1) (Prado & d’Heursel 2006) except for L. labyrinthicus (Spix) in which is 1/2(1) (Rossa-Feres & Nomura 2006) or 1/3(1) (Vizotto 1967, fide Prado & d’Heursel 2006). In addition, larvae of some Leptodactylus species exhibit morphological features that can be related to habitat and feeding habits (i.e., semi terrestrial larvae and trophic egg eating tadpoles: Heyer pers. comm., in Prado & d’Heursel 2006), resultig morphotypes that do not always agree with phylogenetic structure. The presence of the lateral line system in tadpoles of the Leptodactylus fuscus group was reported in L. albilabris (Günther), L. cunicularis Sazima and Bokermann, L. elenae Heyer, L. fuscus (Schneider), L. longirostris Boulenger, L. marambaie Izecksohn, L. mystaceus (Spix), L. notoaktites Heyer, L. mystacinus, and L. poecilochilus (Cope) and might have been unnoticed in other species descriptions (Langone & de Sá 2005; Prado & d’Heursel 2006; de Sá et al. 2007). Langone and de Sá (2005) mentioned that these structures were not visible in specimens of L. gracilis from Atlántida, Department of Canelones, Uruguay. However, in tadpoles of L. gracilis we examined (from Laguna de Rocha and from Playa del Barco, Parque Nacional de Santa Teresa, Department of Rocha, Uruguay; ZVCB 15214, 15216), neuromasts of the angular, anterior oral, infraorbital, supraorbital, posterior supraorbital, ventral, dorsal and middle lines were evident, showing that these structures may be more or less visible in different populations of this species. The tadpoles of Leptodactylus latinasus we studied were found in artificial water bodies of anthropized and highly modified areas. The presence of L. latinasus in synanthropic habitats of urban areas and their surroundings is fairly common in Uruguay, as noticed by Fernández and Fernández (1921) almost a century ago for La Plata, Argentina. Leptodactylus latinasus and Physalaemus gracilis in Uruguay are commonly found



11

FIGURE 5. A. Nest of Physalaemus riograndensis, Barra de Valizas, Rocha, Uruguay, 11 March 2007. B. Nest of Physalaemus henselii between the vegetation, on the humid ground next to a pond, Barra de Valizas, Rocha, Uruguay, 1 May 2007. C. Nest of P. henselii hidden under aerial vegetation cover (mainly Poaceae and Cyperaceae) in a shallow pond of flooded grassland, Pueblo Madera, Rivera, Uruguay, 18 June 2006. A large amount of dead vegetation (right side of the photograph) was moved apart to make the water surface and nest visible. D. Defensive display in Leptodactylus latinasus, Sierra de las Ánimas, Maldonado, Uruguay, 11 September 2005. ZVCB 15954. E. Defensive display in Leptodactylus ocellatus, San José, Uruguay, 5 November 2006. F. Physalaemus biligonigerus. Deimatic behavior, same specimen as in Figure 1 B. G. Defensive display in P. henselii, Barra de Valizas, Rocha, Uruguay, 3 June 2007. ZVCB 15213. H. Death feigning by the same specimen. All photos: F. Kolenc, except 5F: A. Sosa.


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together in anthropized habitats. These species seem to be plastic enough to survive and breed in urban areas, especially if pluvial drainages are scarcely or not paved at all. Most features of the tadpoles of Physalaemus riograndensis described herein are in agreement with those of Prigioni and García (2002), but these authors reported a continuous single row of marginal papillae only interrupted by a dorsal gap. In addition to the dorsal gap, we observed that the row of marginal papillae is most frequently discontinued by two small ventrolateral gaps (9 out of 10 tadpoles). The continuous single row observed by Prigioni and García (2002) seems to be an alternative state of a polymorphic character, present with low frequency in this species (10% in the studied sample), similar to what was observed in P. marmoratus Reinhardt and Lütken (Nomura et al. 2003; as P. fuscomaculatus). The general aspect, the small total length, the presence of ventrolateral gaps, and the presence of two posterior rows of labial teeth make the tadpoles of P. riograndensis most similar to those of P. centralis Bokermann (P. cuvieri group; Rossa-Feres & Jim 1993), but the ventrolateral gaps are wider and P1 row is continuous in the latter [LTRF 2(2)/2]. Another species with ventrolateral gaps, combined with a dorsal gap and a LTRF 2(2)/2(1) is P. marmoratus of the P. albifrons species group (sensu Nascimento et al. 2005), but their tadpoles have a relatively wider body (Nomura et al. 2003). As mentioned by Kolenc et al. (2006), the ventrolateral gaps combined with both ventral and dorsal gaps are seen in P. albonotatus (Steindachner) (Perotti 1997; Kehr et al. 2004), P. cuqui Lobo (Perotti 1997) and P. cuvieri Fitzinger (Heyer et al. 1990; Rossa-Feres & Nomura 2006), of the P. cuvieri species group. This combination is also present in the tadpoles of another Leiuperidae, Pseudopaludicola falcipes (Hensel) (pers. obs.). Physalaemus riograndensis was considered part of the P. cuvieri species group by Lynch (1970), and was recently assigned to the P. henselii species group by Nascimento et al. (2005) along with P. henselii and P. fernandezae. Oral characters in this group are variable: P. fernandezae and P. henselii differ from P. riograndensis by having a LTRF 2(2)/3(1) and a medial ventral gap instead of ventrolateral ones (Alcalde et al. 2006; Kolenc et al. 2006), so larval morphology does not support the inclusion of P. riograndensis in the P. henselii group. The external morphology of Physalaemus biligonigerus tadpoles we studied, from Treinta y Tres, Uruguay, is similar to that described by Fernández and Fernández (1921) (as Paludicola fuscomaculata). These authors mentioned that tadpoles of P. biligonigerus have a single row of oral marginal papillae (single and/or double in our sample), and a LRTF 2(2)/2. From their illustration it can be seen that P1 is smoothly bent anteriorly in the middle. We observed this arrangement in only one specimen (11%), being the most common LRTF 2(2)/2(1) with a very narrow gap in P1. The tadpoles of the cryptic species P. santafecinus Barrio, and those of P. marmoratus (both belonging to the P. albifrons species group sensu Nascimento et al. 2005) are very similar to that of P. biligonigerus and also have a LTRF 2(2)/2(1), with a narrow gap in P1; they differ in having submarginal papillae at the commissural region, and also ventrolateral gaps in the latter (Perotti & Céspedez 1999; Nomura et al. 2003). Zaracho et al. (2003), while studying early larval development in P. biligonigerus, found that P1 tooth row develops as two ridges with labial teeth which fuse at the body midline after stage 25, leaving a notch in the midline. Maybe a variable extent in the fusion of both ridges, due to genetic or environmental influences, could account for the different configurations of this tooth row observed by different authors. Another interesting feature observed in the illustrations of Zaracho et al. (2003) is that the marginal row of papillae develops in this species with two ventrolateral gaps, at least until stage 25. These gaps are lost in later stages in P. biligonigerus, in which a continuous row is present in the lower lip, but the permanence or not of these gaps in advanced stages may account for the variability of this character in the related species P. marmoratus (Nomura et al. 2003). Further studies on early larval development of these and other species are needed to test this hypothesis. The variable configuration of marginal papillae gaps within Physalaemus (for a review see Alcalde et al. 2006 and Kolenc et al. 2006; and references therein), highlights the importance of developmental studies for proper inclusion of this information in phylogenetic analyses. Meanwhile, it is interesting to note that most species of Physalaemus share the presumably plesiomorphic character states of P3 present and approximately as long as the other tooth rows, and a continuous row of mar-



13

ginal papillae in the lower lip. In the P. albifrons group P3 is lost and ventrolateral gaps appear in P. marmoratus. In the P. cuvieri group sensu Lynch (1970), P3 is lost in two species, both of them have ventrolateral gaps (P. centralis and P. riograndensis). In three species (P. albonotatus, P. cuqui and P. cuvieri, all of them in the P. cuvieri group sensu stricto, Nascimento et al. 2005) a ventral gap appears in addition to the ventrolateral gaps, and P3 is present as a short row, as long as the ventral gap in the marginal papillae. Another two species (P. fernandezae and P. henselii) also show this configuration, but without the ventrolateral gaps. It is possible that the ventrolateral and the ventral gaps follow different developmental pathways, and that the P3 row present in the species with a ventral gap could not be homologous with that present in the other species, being derived from the marginal row of papillae. There seem to be evidence about tooth ridges and papillae developmental relationship (Altig 2006), and the development of labial teeth on papillae, as observed in many species, also supports this idea (see Altig & McDiarmid 1999 for general information; Langone 1989; Alcalde et al. 2006, and this work for cases in Physalaemus species). In the three species of the Physalaemus albifrons species group from which tadpoles are known, the vent tube configuration is dextral, a character state that is shared by P. albonotatus, P. cuqui and P. cuvieri (P. cuvieri group; Heyer et al. 1990; Perotti 1997; Kehr et al. 2004), P. soaresi Izecksohn (P. olfersii group; Weber et al. 2005), P. lisei Braun and Braun, P. gracilis (P. gracilis group; Langone 1989; Both et al. 2006), and by P. maculiventris Lutz and P. signifer Girard (P. signifer group; Bokermann 1963; Weber & Carvalho e Silva 2001). In the other Physalaemus species studied up to date, the vent tube configuration is medial. Available data about external larval morphology in Physalaemus do not allow a definition of the phenetic species groups proposed either by Lynch (1970) or more recently by Nascimento et al. (2005). Conversely, Alcalde et al. (2006) found that larval characters from buccopharyngeal and chondrocranial morphology could help to improve the diagnosis of those groups proposed early by Lynch (1970). Clearly, a phylogenetic analysis of the genus including larval characters is needed. The biology of Physalaemus riograndensis is poorly known, data about its natural history is limited to some observations on distribution and advertisement call made by Barrio (1965), who mentioned that foam nests of this species are about 3–4 cm diameter. Nests in the field can be distinguished from those of syntopic P. biligonigerus, as they are bigger in the latter (Fernández & Fernández 1921; Zaracho et al. 2004; pers. obs.). Additionally, eggs of P. riograndensis are more pigmented than those of P. biligonigerus, which are whitish (Fernández & Fernández 1921; Barrio 1965; Cei 1980; pers. obs.). Nest size of P. riograndensis is similar to that of P. henselii and P. fernandezae; these species are sympatric at some places in southern Uruguay, but the latter two breed in autumn and winter, whereas P. riograndensis breeding season extends from January to March, in the austral summer (Barrio 1964; 1965; Maneyro et al. in press). The finding of foam nests of Physalaemus riograndensis and P. henselii on humid ground around the ponds where the tadpoles later develop was unreported to date. Terrestrial nest location was observed in other Physalaemus species as an alternative to nests floating inside the ponds, which is the generalized reproductive mode for the genus (Haddad & Pombal 1998). These reproductive modalities are related to rainfall unpredictability and to the presence of a foam nest that protects the eggs from desiccation, and it is probable that when rainfall releases larvae from the nests they enter the pond with a temporal advantage over larvae of another anuran species reproducing at the pond (Haddad & Pombal 1998). Two remarkable reproductive characteristics of P. henselii that were also not described to date are nest construction hidden under the emergent vegetation cover of ponds, and males calling next to a foam nest. We do not know whether the nest found next to a calling male was made by the male itself, but we consider it very likely, due to the high frequency of this finding and because calling site fidelity of reproductive males was previously observed for another species of this genus, P. fischeri (Boulenger) (as P. enesefae Heatwole, Solano & Heatwole; Tárano 2001). Additionally, calling site fidelity and calling males next to nests hidden in vegetation mats are also exhibited by P. fernandezae (R. Cajade pers. comm.), a close relative of P. henselii according to adult and larval morphological traits, and also in regard to its reproductive ecology (Barrio 1964; Cei 1980; Alcalde et al. 2006; Kolenc et al. 2006;


BORTEIRO & KOLENC

Maneyro et al. in press). Interestingly, the construction of floating nests hidden under a thick vegetation cover in shallow ponds was not reported for Neotropical anurans (for review see Haddad & Prado 2005). This reproductive modality in P. henselii is probably transitional between the reproductive modes exhibited by this species of foam nest floating on pond and foam nest on the humid floor (modes 11 and 28 respectively of Haddad & Prado 2005).

FIGURE 6. Geographic distribution of Physalaemus riograndensis in Uruguay. Circles correspond to previously known localities according to Núñez et al. (2004) and González et al. (1998), squares are new localities reported in the present work: CALNU 1, Boris Misena Establishment 2, Los Espinillos Establishment 3, Bañado de los Oliveras 4, Ciudad de Treinta y Tres 5, and Barra de Valizas 6. Shaded areas indicate altitudes between 100-200 m and above 200 m a.s.l. (light grey and grey respectively).

Until recently, Physalaemus riograndensis was known in Uruguay only in a few localities (Prigioni & Langone 1983). Núñez et al. (2004) presented new ones and suggested that this species is associated to hilly environments (“hilly ecosystems”). Some localities presented by Núñez et al. (2004) are indeed in hilly environments or surrounded by them (i.e., those at Rivera Department). However, the geographic pattern of most REDESCRIPTION OF THREE TADPOLES FROM URUGUAY


15

localities rather corresponds to lowland landscapes of the Uruguay and Tacuarembó River basins, of the Merín Lake basin, and the Atlantic coastal plains (Fig. 6). The landscape matrix at most of these localities and in the new localities reported here for the Departments of Artigas and Treinta y Tres (northwestern and central-eastern Uruguay respectively) is characterized by natural grasslands associated to fluvial plains and coastal habitats (Evia & Gudynas 2000). We observed that P. riograndensis in this kind of environments inhabits small water bodies as small temporary ponds, flooded grasslands and shallow marshes usually satellite to small creeks, streams or rivers, in agreement with previous works from Uruguay (Prigioni & Langone 1983; González et al. 1998; González & Gambarotta 2001). Colonization and breeding in artificial habitats such as flooded crops and impoundments was not previously reported for this species. The defensive display reported here for Leptodactylus latinasus and L. ocellatus is one of several common behaviors described for anurans to avoid predators, generically called predator encounter behavior (Duellman & Trueb 1986). In the specious genus Leptodactylus, predator encounter behavior has been documented just in a few species: L. labyrinthicus, L. laticeps Boulenger, L. pentadactylus (Laurenti) (L. pentadactylus group), L. ocellatus (L. ocellatus group), and in L. mystacinus (L. fuscus group). It was reported that L. labyrinthicus usually remain motionless or escape in reaction to human approach, but some individuals adopt a defensive posture consisting of body lifting from the ground and the display of the bright reddish inguinal coloration (Toledo et al. 2004). Although not described in detail, pictures of this kind of encounter behavior in the colorful L. laticeps are widespread in the literature (Cei 1980; Laurent 1986; Heyer & Scott 2006; Jansen et al. 2006). The reddish and contrasting coloration of this species, in addition to the aggressive posture may serve to the predator as an indication of noxiousness (Duellman & Trueb 1986). Quite similar defensive posture is exhibited by L. pentadactylus when faced to potential predators: it notoriously puff up the body elevating the pelvic region while keeping the head downwards, also with a noisy air exhalation (Villa 1969). A repertoire of aggressive behavior was reported by Brattstrom and Yarnell (1968) for L. melanonotus during male-male interactions, which includes the elevation of the pelvic region (“back-raised display”). Rezende de Carvalho (2005) reported that L. mystacinus is also capable of displaying similar defensive posture. Although being a rather common species, references to the defensive display of L. ocellatus are scarce. Vaz-Ferreira and Gehrau (1975) mentioned that females attending their nests occasionally adopt a passive defensive display consisting of inflating and elevating the body. Hudson (1895) describes the attack of an anuran whose characteristics correspond to an adult exemplar of L. ocellatus: “…it sprang straight at my hand, and, catching two of my fingers round with its fore legs, administered a hung so sudden and violent as to cause an acute sensation of pain…”. This kind of aggressive behavior in L. ocellatus against potential predators (struggling and biting the attacker) is exhibited by both sexes, but mainly by females while protecting their nests or school of tadpoles (Vaz-Ferreira & Gehrau 1975). The adults of Leptodactylus species whose defensive postures have been previously observed are medium to large-sized, being our observations on L. latinasus the first report for a small species. The exhibition of the defensive posture elevating posterior parts of the body in Leptodactylus species which are not brilliantly colored, as L. ocellatus, L. latinasus and L. mystacinus, suggests that this behavior may be phylogenetically conserved. The defensive behavior reported here for Physalaemus biligonigerus and P. henselii, with exhibition of the black spots on inguinal glands in the former, had not been previously documented for these species. A short comment about its presence in P. biligonigerus was made by Achaval and Olmos (1997). The exhibition of inguinal glands as part of defensive display is also known for P. deimaticus Sazima and Caramaschi, and Eupemphix nattereri Steindachner (Sazima & Caramaschi 1986), and was also documented in frogs of the genus Pleurodema (Cei 1962; Cei 1980; Vaz-Ferreira 1984; Martins 1989). The deimatic posture of P. henselii in figure 10 is not as evident as that observed in those Physalaemus species with noticeable inguinal glands, and is quite similar to the “exibição de pouca intensidade, sem orientação particular” (low intensity exhibition, without any particular orientation) described for E. nattereri (Sazima & Caramaschi 1986). The death feigning behavior observed in P. henselii is the first record for a species of this genus, as far as we are aware.


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Acknowledgments Authors are grateful to Cooperativa Azucarera del Litoral Norte Uruguayo (CALNU), Intendencia Municipal de Treinta y Tres, J. E. García, M. Pallas, G. Duarte and J. Valbuena for their hospitality during field-work. DINARA-MGAP provided logistic support. M. Tedros, C. Prigioni, A. Sosa, and M. Letamendía participated of the field work and the former two collected tadpoles with us. J. E. García gently provided a specimen of Physalaemus riograndensis from La Coronilla, and D. Baldo the photograph of nest construction in P. riograndensis. A. Sosa kindly gave us the photographs of P. biligonigerus and shared his observations on deimatic behavior of this species. R. Cajade kindly shared with us his observations and comments on reproductive behavior of P. fernandezae. D. Baldo, C. Both, D. Ferraro, T. Gomes dos Santos, J. Langone, L. F. Toledo, R. Rezende de Carvalho, F. Vera Candioti and V. Zaracho shared bibliography, and I. Costas assisted in manuscript preparation. The comments made by M. Vences and an anonymous reviewer improved the final version of this work. This work was done under División Fauna-MGAP permits Nos. 1043/01, 417/03 and 195/06.

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Appendix 1 Additional and comparative specimens studied from Uruguay. Acronym ZVCB: Batrachians Collection of the Vertebrates Zoology Department (ZVCB), Faculty of Sciences, Universidad de la República, Montevideo, Uruguay. Leptodactylus gracilis. Two tadpoles, surroundings of Laguna de Rocha, Department of Rocha, Uruguay (34º38’S, 54º12’W, 54 m a.s.l.), 10 March 2007, C. Borteiro and F. Kolenc: ZVCB 15216; two tadpoles, Playa del Barco, Parque Nacional de Santa Teresa, Department of Rocha, 17 January 2006, FK: ZVCB 15214 (species identity confirmed by a juvenile reared in the laboratory: ZVCB 15215). Leptodactylus latinasus. Three tadpoles stage 40, surroundings of Estadio Luis Tróccoli, Villa del Cerro, Department of Montevideo, Uruguay (34º51.985’S, 56º15.116’W, 12 m a.s.l.), 26 December 2005, CB: ZVCB 15187; adult male, Los Espinillos Establishment, Bella Unión, Department of Artigas (30º28’S, 57º39’W, 49 m a.s.l.), 9 January 2003, CB, FK, M. Tedros, F. Gutiérrez: ZVCB 15190; adult male, Cerro de las Ánimas, Sierra de las Ánimas, Department of Maldonado (34º44’S, 55º19’W, 411 m a.s.l.), 11 September 2005, CB, FK: ZVCB 15954. Physalaemus biligonigerus. Three tadpoles stage 40, surroundings of Quebrada de los Cuervos, Department of Treinta y Tres, Uruguay (32º57.868’S, 54º27.254’W, 185 m a.s.l.), 4 March 2007, CB, FK, MT, C. Prigioni: ZVCB 15193; adult male, Bañado de los Oliveras, Department of Treinta y Tres (33º11’S, 54º27’W, 29 m a.s.l.), 9 January 2006, CP and A. Sosa: ZVCB 15195). Physalaemus henselii. Adult female, Barra de Valizas, Department of Rocha (34º20’S, 53º48’ W 2 m a.s.l.), 4 June 2007, CB, FK, CP: ZVCB 15213. Physalaemus riograndensis. Two tadpoles stages 39 and 40, Cooperativa Azucarera del Litoral Norte del Uruguay (CALNU), Department of Artigas, Uruguay (30º19.857’S, 57º37.226’W, 65 m a.s.l.), 10 January 2003, CB, FK, MT: ZVCB ZVCB 15198; five tadpoles stages 33-38, same locality, 15 January 2003, CB, FK, MT: ZVCB 15197; 5 nests, same locality, 15 January 2003, CB, MT, M. Letamendía: ZVCB 15202; 6 nests, same locality, 15 January 2003, CB, MT, M. Letamendía: ZVCB 15203; one tadpole, same locality, 10 January 2001, CB, FK, MT, FG: ZVCB 15204; three nests, Bañado de los Oliveras, Department of Treinta y Tres (33º11’S, 4º27’W, 43 m a.s.l.), 14 March 2005, CB, MT, CP: ZVCB 15200; one nest, same locality and date: ZVCB 15205, obtained from an amplectant couple: female ZVCB 15206 and male ZVCB 15207; adult, Boris Misena Establishment, Bella Unión, Department of Artigas (30º24’S, 57º37’W, 68 m a.s.l.), 10 January 2003, CB, FK: ZVCB 15208; adult male, Los Espinillos Establishment, Bella Unión, Department of Artigas (30º28’S, 57º39’W, 49 m a.s.l.), 12 January 2001, FK: ZVCB 15209; adult male, Barra de Valizas, Department of Rocha (34º20’S, 53º48’W, 10 m a.s.l.), 10 February 2007, CB: ZVCB 15212; adult male, La Coronilla, Department of Rocha (33º53’S, 53º30’W, 22 m a.s.l.), 11 February 2006, J. E. García: ZVCB 15210; adult male, Ciudad de Treinta y Tres, Department of Treinta y Tres (33º14’S, 54º22’W, 39 m a.s.l.), 6 January 2002, CB, CP: ZVCB 15211.


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