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New Species ofPhysalaemus Fitzinger, 1826 from Southern

Bahia, Brazil (Anura, Leptodactylidae)

Author(s) :Carlos Alberto Gonalves Cruz and Bruno V. S. Pimenta

Source: Journal of Herpetology, 38(4):480-486. 2004.

Published By: The Society for the Study of Amphibians and Reptiles

DOI:

URL: http://www.bioone.org/doi/full/10.1670/214-02A

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Reproduction and Sexual Size Dimorphism in the Lacertid LizardPedioplanis burchelli (Sauria: Lacertidae) in South Africa

W. T. NKOSI,1 N. J. L. HEIDEMAN,1,2 AND J. H. VAN WYK3

1Department of Zoology and Entomology, University of the Free State (Qwaqwa Campus),Private Bag X13, Phuthadithjaba 9866, South Africa

3Department of Zoology, University of Stellenbosch, Private Bag Matieland,Stellenbosch, South Africa

ABSTRACT.Pedioplanis burchelli is a small oviparous lacertid lizard that inhabits rocky montane areas inthe highveld grassland biome of South Africa. We studied its reproductive cycle by monthly monitoring ofgravimetric, morphometric, and histological changes of the reproductive system of males and femalesthroughout 1999. Reproduction took place in spring/summer, and gonadal activity of males and females waswell synchronized and prenuptial. Photoperiod was the best predictor of seasonal fluctuations in testes massand rainfall in the case of ovarian seasonality. Neither vitellogenic follicle count nor oviducal egg count were

correlated with snoutvent length. Sexual size dimorphism with respect to certain body parts is explainedeither in terms of sexual selection, differential growth, or intraspecific food niche segregation. The absence ofa significant difference in incidence in damaged tails between males and females may be indicative of similarlevels of predation pressure.

Lizard species diversity in Southern Africaranks among the highest in the world, with anendemicity of more than 92% (Bauer, 1999).However, life history is larger unstudied in mostspecies, even entire families (for example, theLacertidae). The Lacertidae comprises nine gen-

era of which Pedioplanis comprises 11 species,nine of which are endemic to South Africa(Branch, 1998). Apart from a detailed study oftwo Namib Desert lacertid species belonging tothe genus Meroles (Louw and Holm, 1972; Gold-

berg and Robinson, 1979), existing knowledge ofsouthern African lacertid reproductive biology isanecdotal and based mostly on brief comments intaxonomic works such as De Waal (1978) andBranch (1998). This study is the first detailedaccount of reproduction in a South Africanlacertid lizard. Pedioplanis burchelli is insectivo-rous and cryptically colored and inhabits rockymontane areas in highveld grassland biomewhere individuals take shelter mainly under flatsandstone rock slabs (Branch, 1998). The aims ofthe present study were to describe the reproduc-tive cycle of males and females and how theycorrelate with each other and with certainenvironmental variables. In addition, sexual sizedimorphism was investigated and the incidenceof damaged tails used as possible indicator ofpredation pressure experienced by males andfemales.

MATERIALS AND METHODS

Study Area and Climate.The study area wassituated in the highveld grassland biome ofSouth Africa, in the Phuthadithjaba area of thenortheastern Free State Province between 288299Slatitude and 288499E longitude, at an altitude of

1850 m above sea level. Rain falls mainly insummer and varies from 250 to 500 mm per year(Rutherford and Westfall, 1986). Weather data for1998 and 1999 (Fig. 1) were obtained fromBethlehem (about 75 km northwest of the studyarea), the nearest weather station.

Collecting and Laboratory Procedure.A mini-mum of six adult males (only three in April) andfemales were collected around the middle of eachmonth from January through December 1999.Lizards were killed by freezing within 48 h ofcapture, mass recorded to the nearest 0.1 g, and

snoutvent (SVL) measured to the nearest 0.1 mm.In males, testes and ductuli epididymides wereexcised, mass recorded to the nearest 0.01 g, fixedand stored in Bouins solution. Testis length wasmeasured to the nearest 0.1 mm. In females,ovaries and oviducts were removed and massrecorded to the nearest 0.01 g. The diameter of thefour largest ovarian follicles was measured to thenearest 0.1 mm, and their developmental stagesdescribed following the criteria of Van Wyk (1984).Appearance of vitellogenic follicles, corpora lutea,and oviducal eggs was recorded. Oviducal eggswere counted to estimate clutch size.

The reproductive cycle was studied by observ-ing gravimetric, morphometric, and histologicalchanges (males only) of gonads and accessoryducts throughout the year for each sex. Histo-

2 Corresponding Author. E-mail: [email protected]

Journal of Herpetology, Vol. 38, No. 4, pp. 473480, 2004Copyright 2004 Society for the Study of Amphibians and Reptiles

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logical sections were made using the method

described by Prophet et al. (1994), which in-volved staining sections with Harriss haematox-ylin and eosin. Sections were taken at 8lm andthe diameter of five randomly selected cross-sections of the seminiferous tubules measuredper testis to the nearest 1 lm using a microscopegraticule. In the case of the epididymus, changesin the height of its epithelium were measuredand the presence of spermatozoa in its lumenrecorded.

Staging of spermatogenic activity followed theclassification system of Licht (1967), whichcomprises the following stages: Stage 1, seminif-

erous tubules involuted with only spermatogo-nia; epididymus atrophic and empty; Stage 2,seminiferous tubules with primary spermato-cytes; epididymus atrophic and empty; Stage 3,secondary spermatocytes and early spermatidspresent; epididymus atrophic and empty; Stage4, transforming spermatids with a few sperma-tozoa; epididymus atrophic and empty (butothers with few spermatozoa); Stage 5, sperma-tozoa abundant with maximum spermiogenesis;epididymus hypertrophied and many sper-matozoa; Stage 6, spermatozoa abundant but

spermatocytes and spermatids greatly reduced;epididymus atrophic and empty; Stage 7, semi-niferous tubules involuted with only spermato-gonia; epididymus hypertrophied and empty.

Ovarian activity was staged according to theclassification of Van Wyk (1984) which is as fol-lows: (1) Nonreproductive stage, Only hydratedovarian follicles (diameter: 1.8 mm); nooviducal eggs or corpora lutea (MarchAugust);(2) Early vitellogenic stage, Early vitellogenicfollicles (diameter: from 1.82.0 mm); no ovidu-cal eggs or corpora lutea (SeptemberOctober);(3) Preovulatory stage (I), Late vitellogenicfollicles (diameter: from 2.12.9 mm); no ovidu-cal eggs or corpora lutea (October); (4) Post-ovulatory stage (I), Hydrated ovarian follicles(diameter: 1.8 mm); oviducal eggs or corpora

lutea present (November) but not in (January);(5) Late postovulatory (II), Early vitellogenicfollicles (diameter: from 1.82.0 mm); oviducaleggs or corpora lutea present (November); (6)Preovulatory period (II), Late vitellogenic fol-licles (diameter: from 3.06.2 mm); no oviducal

eggs or corpora lutea (NovemberDecember); (7)Postovulatory (III), Hydrated ovarian follicles(diameter: 2.0 mm); no oviducal eggs butcorpora lutea present (December).

The following body dimensions were alsocompared between the sexes: SVL, TL (usingspecimens showing no signs of tail damage orregeneration), head length (HDL), width (HDW),and height (HDH), as well as forelimb (FL) andhindlimb length (HL). All measurements weretaken with a digital sliding vernier caliper tothe nearest 0.1 mm. HDL was measured from the

posterior edge of the ear opening to the tip of thesnout, whereas HDW and HDH were measuredat an imaginary plane running vertically throughthe center of the ear openings. FL and HLcomprised the respective combined lengths ofthe upper and lower limb elements, hand/footand longest digit. The female:male ratio (FMR) ofFitch (1981) was used to calculate the degree ofdimorphism. The entire sample was examinedfor damaged tails and signs of regeneration forcomparison between males and females. Speci-mens with freshly damaged tails were notconsidered to ensure that ones with capture

injuries were not included in the analyses.Data Analysis.All means are given as6 1 SE.

Data were tested for normality using the Kolmo-gorov-Smirnov test and for homogeneity ofvariances using Bartletts test (Sokal and Rohlf,1981) prior to analyses. Data on epididymusmass, epithelium height and diameter as well asovarian mass, oviducal mass and follicle di-ameter did not meet assumptions of normality.Kruskal-Wallis nonparametric analysis of vari-ance was therefore used to test for significantseasonal variation in those parameters, followed

by Dunns nonparametric multiple comparisonstest for ranked data (Heath, 1995). The number ofgroups compared (k) using the latter test waseight, giving a test statistic, Q, of 3.124 at P 0.05. Covariation between reproductive parame-ters and environmental factors was analyzedusing Spearmans rank correlation analyses andstepwise multiple regression analyses withmonthly testis mass and ovarian mass as de-pendent variables and the climatic factors (max-imum and minimum ambient temperature,photoperiod, and rainfall) as independent varia-

bles. In the case of the morphometric compar-isons, all variables were log-transformed beforeregression analysis, and ANCOVA were carriedout. Least-squares regression analysis of log-transformed variables against log total body

FIG. 1. Mean maximum and minimum ambienttemperature, photoperiod, and rainfall for 1998 and1999 recorded at Bethlehem.

474 W. T. NKOSI ET AL.

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length (TBL, SVL TL) or logSVL was used todetermine their scaling in cases where SSDexisted. ANCOVA was used to compare theslopes of regression equations, which served asindicators of growth rate in the two sexes. TheMann-Whitney U-test was used to compare the

incidence of broken tails between males andfemales. Differences between sets of data wereconsidered significant at P 0.05. All thestatistical analyses were carried out using thesoftware package STATISTICA 5.1 (StatSoft Inc.).

RESULTS

Spermatogenesis and the Testicular Cycle.Inmales, mean SVL was 53.4 6 3.3 mm (range:45.661.5 mm; N 5 75); SVL of the smallestreproductively mature specimen was 45.6 mm.All testes appeared quiescent from February

through August (late summer through latewinter; Table 1, Stages 1 and 2). Although thefirst sign of testicular recrudescence (Stage 3) wasseen in a specimen from July, it was only inspecimens from August that testicular recrudes-cence was most prevalent. The first specimenwith testes showing full spermatogenesis (sper-miogenesis, Stage 5) appeared in September(spring). From October through January (earlythrough late summer), the testes of most speci-mens showed maximum spermatogenic activity(Stage 5). The testes of one specimen fromNovember, however, showed declining sper-

matogenesis (Stage 6) whereas that of anotherwas already quiescent (Stage 7). By January, thetestes of more than half the specimens werequiescent (Stages 1 and 7).

Significant monthly variation was found intestis mass and length as well as in meanseminiferous tubule diameter (testis mass:ANOVA: F7;67 5 21.5, P , 0.001; testis length:

F7;67 5 20.7, P , 0.001; seminiferous tubulediameter, F7;67 5 21.4, P , 0.001; Fig. 2B). Allthree variables peaked in October (Stage 5) andwere then significantly greater than those of all

the other months except September (LSD: P,

0.05). Among the rest of the months, the variablesdid not differ significantly (LSD: P . 0.05), andthey were at their lowest between January andMarch (Stage 1).

Epididymus diameter and mass, and epithe-lium height varied significantly among themonths (diameter, H5 33.9, P , 0.01; mass, H5 29.4, P , 0.001; epithelium height, H5 31.5,P , 0.001). In October (Stage 6), all threevariables were significantly higher than those ofthe other months (Dunn: P, 0.05). The rest of themonths showed no significant differences (Dunn:P. 0.05). Epididymus diameter was at its lowestin August (Stages 2 and 3), epithelium height in

January through March (Stage 1), and mass inJune through August (Stages 2 and 3).

Oogenesis, the Follicular Cycle and Fecundity.In females, mean SVL was 54.16 3.8 mm (range:45.262.9 mm; N 5 91) and the size of thesmallest sexually mature specimen was 45.2 mm.The ovaries were inactive, with only clear(hydrated) follicles, from March through August(Stage 1). From September (Stage 2) to December(Stage 6) yellowish follicles and signs of ovula-tion (corpora lutea and oviducal eggs) wereevident. Ovarian and oviducal mass and folliclediameter (Fig. 2B) all varied significantly among

the months (ovarian mass, H5 26.9, P , 0.001;oviducal mass, H 5 27.3, P , 0.001; folliclediameter, H 5 26.7, P , 0.01). Ovarian andoviducal mass peaked in October and were thensignificantly greater than that of the othermonths (Dunn: P , 0.05). Follicle diameterpeaked in December and was significantlygreater than that of the other months (Dunn:P , 0.05) all of which did not differ significantlyfrom each other (Dunn: P . 0.05).

Vitellogenic follicles were first observed inSeptember (spring), numbered 47 in 78 females

(mean: 5.56

1.3) and their number was notcorrelated with SVL (rs 5 0.005, P . 0.05).Oviducal eggs were found simultaneously in

both oviducts and were present from Novemberthrough February. Clutch size ranged from 46eggs per female (mean: 4.5 6 1.4) and was alsonot correlated with SVL (rs 50.01, P . 0.05). InNovember, a female with both oviducal eggs andvitellogenic follicles was found, suggesting thatat least some females produced two clutches perreproductive season.

Climatic Correlates.Significant negative corre-lations were found between ambient temperatureand testis mass (rs 5 0.30, P , 0.01). Stepwisemultiple regression analysis showed that photo-period was the best predictor of seasonal varia-tion in testis mass (testis mass5 2.22 photoperiod

TABLE 1. Seasonal changes in spermatogenic activ-ity in Pedioplanis burchelli males according to theclassification system of Licht (1967).

Spermatogenic stages with number oflizards in each stage

Month N 1 2 3 4 5 6 7 JAN 6 3 2 1FEB 6 6MAR 6 6APR 3 3MAY 7 7

JUN 7 7 JUL 7 6 1AUG 8 4 4SEP 7 3 3 1OCT 6 6NOV 6 4 1 1DEC 6 6

REPRODUCTION IN THE SOUTH AFRICAN LACERTID PEDIOPLANIS BURCHELLI 475

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FIG. 2. Seasonal variation in testis mass, testis length and seminiferous tubule diameter in male Pedioplanisburchelli (A); seasonal variation in ovarian and oviducal mass, and follicle diameter in female P. burchelli (B). Thenumbers above the standard error bars indicate sample size which was the same for all three variables in each sex.


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1.4 maximum ambient temperature, rs 5 0.85,P , 0.001). Ovarian mass was positively andsignificantly correlated with ambient temper-ature, photoperiod and rainfall (ambient temper-ature: rs 5 0.34, P , 0.01; photoperiod: rs 5 0.47,P , 0.001; rainfall: rs5 0.53, P , 0.001). Stepwisemultiple regression analysis showed that rainfallwas the best predictor of seasonal variation inovarian mass (ovarian mass 5 0.89 rainfall1.14maximum ambient temperature, rs 5 0.53, P ,0.001).

Sexual Size Dimorphism and Damaged TailIncidence.The FMR of SVL was 1.01: femaleswere slightly (1%) larger than males. ANCOVA

with sex as factor and logTBL as covariate never-theless showed that SVL in females was signifi-cantly greater than that of equal sized males. Inthe case of TL the FMR was 0.87: TL of males was13% longer than females. Relative TL of maleswasalso shown to be significantly greater than that offemales using ANCOVAwith logSVL as covariate(Fig. 3A, Table 2). ANCOVA with logSVL ascovariate also showed that in all the head and

limb dimensions compared males were signifi-cantly greater than females (Figs. 3B, C, Table 2).The mean absolute tail lengths of males andfemales differed significantly as did the slope ofthe relationship between TL and SVL (heteroge-neous slopes) and the mean asymptotic taillengths (lizards with an SVL larger than 58 mm;Student t-test, N5 6, t 53.52, 10 df, P , 0.05).

Of the sample of 77 males, 31.2% had tailsshowing signs of damage and/or regenerationwhile in the sample of 91 females; the figurewas 30.8%. A Mann-Whitney U-test showed that

these differences were not significant (U5

65,P . 0.05).

DISCUSSION

Reproduction was seasonal in P. burchelli withmale and female cycles well synchronized.Although testicular recrudescence commencedearlier (late winter) than ovarian recrudescence(spring) both reached peak activity in summer,presumably the mating period, a pattern charac-teristic of prenuptial lizard species from thetemperate region (Fitch, 1970). Clutch sizeranged from 46 eggs with at least some femalesproducing more than one clutch per reproductiveseason. The pattern of reproduction in P. burchelliwas similar to that described for the Namib

FIG. 3. Log-transformed body and head dimensionsregressed against logTBL and logSVL in male (solidlines and triangles) and female (broken lines andsquares) Pedioplanis burchelli; SVL and TL (A); HDH,

HDL, and HDW (B); FL and HL (C).

TABLE 2. The table shows the regression slopes andregression coefficients of the log-transformed SVL, TL,and head and limb measurements of male and femalePedioplanis burchelli. r is the regression coefficient, F-ratios and P-values refer to results of male versusfemale comparisons using ANCOVA, with logSVL as

covariate (except in the case of logSVL which useslogTBL as covariate). The numbers in parenthesesdenotes sample size in the case of the head and limbmeasurements; M denotes males and F females.

Measurement

MaleN5 53

(75)

FemaleN5 63

(91) r M; F F P

SVL 0.60 0.42 0.71; 0.43 12.1 0.001TL 0.90 0.40 0.53; 0.17 31.2 0.0001HDL 0.90 0.60 0.76; 0.63 103.7 0.0001HDH 1.10 0.70 0.42; 0.62 38.2 0.0001HDW 0.90 0.80 0.62; 0.81 77.9 0.0001

FL 0.80 0.50 0.49; 0.48 45.9 0.0001HL 0.60 0.40 0.28; 0.40 41.8 0.0001


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Desert lacertid Meroles cuneirostris by Goldbergand Robinson (1979). That species produces 14eggs per reproductive season and may also laya second clutch. A second Namib Desert lacertid,

Meroles anchietae, however, exhibits continuousreproductive activity, that is, a typical tropical

cycle, with spermatogenic regression occurringonly briefly in autumn and females producing 24 clutches annually (Goldberg and Robinson,1979). The latter authors ascribed this continuousreproductive pattern in M. anchietae to a contin-uous supply of food resources. This species isomnivorous, supplementing its winter diet withwindblown seeds when insect food is scarce.However, M. cuneirostris is strictly insectivorousand, thus, suffers a food resource scarcity duringwinter. When compared to other species in itsgeographic area the reproductive cycle of P.

burchelli corresponds to that reported for Mabuyacapensis by Flemming (1994) but differs from thatreported for Cordylus giganteus by van Wyk(1991, 1995) and Pseudocordylus melanotus mela-notus by Flemming (1993a,b). In the latter twospecies, spermatogenesis is postnuptial and re-productive activity of males and females asyn-chronous. These differences in reproductivecycles shown by species from the same geo-graphic area support the suggestion of reproduc-tive conservatism among lizards put forward by

James and Shine (1985) and Van Wyk (1998).The negative correlation between testis mass

and ambient temperature was unexpected be-cause increasing ambient temperature has tradi-tionally been implicated as one of the majorfactors regulating testicular activity in reptiles(Duvall et al., 1982; Licht 1984). In contrast tomales, ovarian mass in females was positivelycorrelated with all three environmental variablesas was expected. That rainfall was the bestpredictor of ovarian mass fluctuations in femalesmay be related to the higher energy demands ofegg production, as food resource (insects) quan-tity and quality are usually dependent on rainfall.

A number of studies have in fact reporteda positive relationship between precipitationand insect productivity (Parker and Pianka,1975; Ferguson et al., 1990). The commencing ofvitellogenic activity in autumn in the insectivo-rous Pseudocordylus capensis coincident with in-creasing rainfall (Van Wyk and Mouton, 1998) isconsistent with the suggestion of high energydemands of egg production. Van Wyk (1991)found that female C. giganteus would deferreproduction if energy reserves were not ade-quate, whereas female Sceloporus virgatus pro-visioned with abundant moisture-rich foodproduced greater clutch masses and more eggsper clutch than nonprovisioned females of similar

body size (Abell, 1999). There are neverthelesscases where the correlation between reproduction

in females and rainfall was found to be negative(e.g., in Cordylus polyzonus polyzonus in the FreeState; Van Wyk, 1989); thus, the suggestionsadvanced above may not always hold. For P.burchelli, a further advantage of reproducingduring the rainfall season (summer) is that the

arrival of its hatchlings coincides with the periodof high insect availability. The lack of a correlation

between follicle number and clutch size and SVLin P. burchelli may simply reflect a narrow sizerange of females. A similar situation found inPodacris milensis led Adamopolou and Valakos(2000) to argue that it was possibly indicative ofegg volume and size having reached an evolu-tionary optimum. Clutch size and egg volumealso showed no increase with increasing bodysize in Acanthodactylus scutellatus (Frankenbergand Werner, 1992).

The significantly longer SVL of femaleP. burchelli compared to equal sized males isprobably an adaptation for increasing fecundity,several studies having reported a positive re-lationship between increasing female body sizeand clutch size in lizards (e.g., Flemming and vanWyk, 1992; Heideman, 1994). The significantlylonger tail of males, however, may simply beattributed to a longer tail base to accommodatethe pair of hemipenes as suggested by theMorphological Constraint hypothesis of King(1989). However, when applying the latterhypothesis to lacertid lizards, Barbadillo and

Bauwens (1997) found support for it in only oneof nine species studied. The possibility that itmay have evolved as a result of higher predationpressure seems unlikely because of the similarityin broken tail incidence between the sexes.However, if the relatively longer limbs of malesafford them greater running speed than femalestheir presumed greater success at outrunningpredators may offset higher predation pressureresulting in a similar incidence of broken tails tofemales. Avery et al. (1987), for example, foundthat running speed in Lacerta vivipara increased as

stride length and stride rate increased; stridelength being a function of limb length (Hilde-brand, 1982). These suggestions requirefollow-upstudies in P. burchelli.

Relatively larger head dimensions (width,length, and height) in males compared to femalesmay have several explanations. It could be theresult of sexual selection, if aggressive male-maleencounters take place during reproduction (Re-aney and Whiting, 2002) or if females preferen-tially mate with larger headed males (Vitt andCooper, 1985). It may also be diet related withmales consuming larger prey than females (in-traspecific food niche divergence), thereby relax-ing intersexual competition (Shine, 1989; Shine etal., 1996). However, in the absence of informationon aspects such as the mating system and diet,


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current data cannot address the latter twosuggestions. The relatively larger head in malescould also be the result of a faster growth ratecompared to females, the general view being thatfemales allocate relatively more energy to re-production after reaching sexual maturity than to

somatic characters such as head size.

Acknowledgments.We gratefully acknowledgeL. Mashinini for assistance in collecting thespecimens for this study and thank the Universityof the Free State (Qwaqwa campus) for logisticalsupport. Research funds received by NJLH fromthe South African National Research Foundationhelped to defray expenses. Constructive sugges-tions by two anonymous reviewers greatlyimproved the quality of the manuscript.

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RUTHERFORD, M. C., AND R. H. WESTFALL. 1986. Biomesof Southern Africaan objective categorization.

Memoirs of the Botanical Survey of South Africa54:198.SHINE, R. 1989. Ecological causes for the evolution of

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SHINE, R., P. S. HARLOW, W. R. BRANCH, AND J. K. WEBB.1996. Life on the lowest branch: sexual dimor-phism, diet and reproductive biology of an AfricanTwig Snake, Thelotornis capensis (Serpentes, Colu-

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VAN WYK, J. H., AND P. LE F. N. MOUTON. 1998.

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Accepted: 9 July 2004.

Journal of Herpetology, Vol. 38, No. 4, pp. 480486, 2004Copyright 2004 Society for the Study of Amphibians and Reptiles

New Species of Physalaemus Fitzinger, 1826 fromSouthern Bahia, Brazil (Anura, Leptodactylidae)

CARLOS ALBERTO GONCALVES CRUZ1 AND BRUNO V. S. PIMENTA2

Departamento de Vertebrados, Museu Nacional, Universidade Federal do Rio de Janeiro, Quinta da Boa Vista,20940-040 Rio de Janeiro, R J, Brazil

ABSTRACT.A new species of Physalaemus belonging to the Physalaemus cuvieri species group is describedfrom southern Bahia, Brazil. It inhabits the borders of Atlantic Rain Forest fragments, natural forest clearings,and cacao plantations. The new species is characterized by its medium size, robust body, warty skin, presenceof inguinal glands, one pair of dorsal tubercles on the sacral region, and an interorbital black transversal stripegenerally covering a pair of tubercles.

RESUMEN.Uma nova especie de Physalaemus pertencente ao grupo de Physalaemus cuvieri, e descrita dosul da Bahia, Brasil. A especie e encontrada nas bordas de fragmentos de Mata Atlantica, clareiras naturais e

plantac~

oes de cacau. A especie nova e caracterizada pelo seu tamanho medio, corpo robusto, pele verrucosa epresenca de glandulas inguinais, de um par de tuberculos dorsais na regiao sacral e de uma faixa pretatransversal na regiao interorbital, geralmente cobrindo um par de tuberculos.

The Neotropical frog genus Physalaemus Fit-zinger, 1826, currently contains 41 valid species(Frost, 2002; Caramaschi et al., 2003). Lynch(1970) recognized and diagnosed four speciesgroups in the genus: Physalaemus biligonigerusgroup, Physalaemus pustulosus group, Physalae-mus signifer group, and Physalaemus cuvieri

group. Two species, Physalaemus deimaticus andPhysalaemus rupestris, are not assigned to any ofthese species groups (Sazima and Caramaschi,1986; Caramaschi et al., 1991). The Physalaemuscuvieri group is the most diverse, including 20species distributed throughout South America(Frost, 2002). The P. cuvieri group is characterized

by small to moderate size (1439 mm SVL),slender to stocky build, smooth to warty skin,first finger not longer than the second, presenceof an inner tarsal tubercle, presence of small,

1 Corresponding Author. E-mail: [email protected]

2 E-mail: [email protected]


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noncompressed metatarsal tubercles (exceptPhysalaemus albifrons), absence or presence ofsmall inguinal glands (large in Physalaemusaguirrei), absence of parotoid glands, and pres-ence of maxillary and premaxillary teeth (Lynch,1970). In the coastal region of eastern Brazil, this

group is represented by eight species: Physalae-mus aguirrei, Physalaemus albifrons, Physalaemusbarrioi, Physalaemus cicada, Physalaemus cuvieri,Physalaemus jordanensis, Physalaemus kroyeri, andPhysalaemus soaresi (Frost, 2002). Feio et al. (1999)pointed out that P. aguirrei, Physalaemus maximus,Physalaemus olfersii, and P. soaresi should composea new species group, but they lacked supportingevidence.

Recent surveys in the Atlantic Rain Forest ofsouthern Bahia, Brazil, resulted in the collectionof a new species of this group. Herein, we present

the description of this new species, the sonogramof the advertisement call, and some notes onnatural history and distribution.

MATERIALS AND METHODS

Comparisons with the new species were re-stricted to the forms of the P. cuvieri groupinhabiting the eastern coastal region of Brazil, as

based on the authors examination of specimensand on information given by Izecksohn (1965),Bokermann (1966a,b, 1967), Lynch (1970), andHeyer et al. (1990). Specimens used in thedescription or examined for comparisons are

deposited in EI (Eugenio Izecksohn collection,deposited in Universidade Federal Rural do Riode Janeiro, Seropedica, RJ, Brazil), MCN (Museude Ciencias Naturais PUC Minas, Belo Hori-zonte, MG, Brazil), MNRJ (Museu Nacional, Riode Janeiro, RJ, Brazil), and MZUSP (Museu deZoologia, Universidade de Sao Paulo, SP, Brazil).Specimens examined are listed in Appendix 1.

Abbreviations used in the measurements ofspecimens are SVL (snoutvent length), HL(head length), HW (head width), ED (eye di-ameter), TD (tympanum diameter), UEW (upper

eyelid width), IOD (interorbital distance), IND(internostril distance), END (eyenostril dis-tance), THL (thigh length), TBL (tibia length),and FL (foot length, including tarsus). Allmeasurements are in millimeters, and SVL, HL,HW, THL, TBL, and FL were measured withcalipers, whereas the other measurements weremade with an ocular micrometer. Specimenswere sexed by the presence or absence of vocalsac.

Vocalizations were recorded with a Sony DATTCD-D8 digital tape recorder with a SennheiserK6/ME66 microphone set. Sonograms were pro-duced by the software Avisoft-SASLab Light forWindows, version 3.74, using 16 bit resolution, 22kHz sampling frequency, FFT with 256 points,FlatTop window, 50% overlap, and 100% frame.

Physalaemus erikae sp. n.Figures 12

Holotype.MNRJ 30349, adult male (Fig. 1),collected at Fazenda Vista Bela (168369S,398559W), Municipality of Guaratinga, State ofBahia, Brazil, by B. V. S. Pimenta, R. T. Moura, A.Paglia, and R. V. Lopes on 14 September, 2000.

Paratypes.MNRJ 28981, adult female, collected by B. V. S. Pimenta on 13 March 2001, MNRJ28982, adult female, collected by B. V. S. Pimentaon 21 June 2001, MNRJ 28983, adult male,

collected by B. V. S. Pimenta on 12 July 2001,and MNRJ 28985, adult female, collected by B. V.S. Pimenta on 20 March 2002, at ReservaParticular do Patrimonio Natural (RPPN) Esta-cao Veracruz (168239S, 398109W), Municipality ofPorto Seguro, State of Bahia, Brazil; MNRJ 28984,adult female, collected by R. V. Lopes onNovember, 2001 at Fazenda Princesa do Pajau(178109S, 398509W), Municipality of Itamaraju,State of Bahia, Brazil; MNRJ 3002829, MNRJ30348, three adult females, collected by B. V. S.Pimenta and R. V. Lopes on 18 July 2000, MNRJ30347, MCN 219899, MCN 2203, four adultfemales, collected by B. V. S. Pimenta and P. H. C.Cordeiro on 30 April 2000, at RPPN Serra doTeimoso (158099S, 398319W), Municipality of

Jussari, State of Bahia, Brazil; MNRJ 3034346,

FIG. 1. Physalaemus erikae sp. n., holotype (MNRJ30349), dorsal view.

NEW SPECIES OF PHYSALAEMUS 481

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two adult males and two adult females, collectedon 12 and 14 September 2000, at the same localityof the holotype.

Diagnosis.A species belonging to the P.cuvieri group, characterized by (1) medium size

(males 21.626.6 mm SVL, females 19.227.1 mmSVL); (2) body robust; (3) tympanum weaklydistinct; (4) presence of inguinal glands; (5)dorsal skin texture warty or with longitudinalridges; (6) presence of one pair of dorsal tubercles

FIG. 2. Physalaemus erikae sp. n., holotype (MNRJ 30349). (A) Dorsal and (B) lateral views of head (scale 5 5mm); ventral views of (C) hand and (D) foot (scale 5 1 mm).

482 C. A. G. CRUZ AND B. V. S. PIMENTA

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on the sacral region; (7) presence of an in-terorbital black transversal stripe, generallycovering a pair of tubercles; and (8) presence ofa dorso-lateral dermal fold beginning at theposterior corner of the eye, ending near theinguinal region.

Physalaemus erikae has a smaller size (SVL formales 21.626.6 mm) than P. albifrons, P. barrioi, P.cuvieri, and P. kroyeri (combined SVL for males25.935.0 mm), warty skin (with longitudinalglandular lines in P. albifrons and P. barrioi, smoothor finely granular in P. cuvieri), and presence ofinguinal glands (absent in these species). Phys-alaemus erikae is distinguished from P. aguirrei,P. cicada, P. jordanensis, and P. soaresi by its stocky

build and warty skin (smooth in P. aguirrei,P. cicada, and P. soaresi; with longitudinal glandu-lar lines in P. jordanensis). By its weakly distinct

tympanum, P. erikae differs from P. barrioi,P. cicada, and P. cuvieri, which have indistincttympanums. Physalaemus erikae is distinguishedfrom P. aguirrei, P. barrioi, P. cicada, P. jordanensis,and P. soaresi by the absence of a black or dark-

brown stripe covering the loreal region and flanksand differs from P. jordanensis and P. barrioi by thelack of pigmentation on inguinal glands.

Description of Holotype.Body robust; headwider than long; snout rounded in dorsal andlateral views (Fig. 2AB); nostrils ovoid, non-protuberant, directed laterally; canthus rostralisdistinct, straight; loreal region concave; eyes

slightly protuberant; tympanum weakly distinct;supratympanic fold from posterior corner of eyeto shoulder (Fig. 2B); a weakly marked dorsolat-eral fold beginning at posterior corner of eye,immediately above the supratympanic fold,ending near inguinal region; vocal sac subgular,large, expanded externally; choanae large, nearlyround; tongue narrow, long; maxillary and pre-maxillary teeth visible under magnification.Arms slender, upper-arms shorter and moder-ately more robust than forearms; fingers slender,long; finger lengths I , II ffi IV , III; brown

nuptial asperities on thumbs; subarticular tu-bercles single, round; outer metacarpal tuberclemedium, ovoid; inner metacarpal tubercle large,ovoid; few small supranumerary tubercles;fingers tip not expanded (Fig. 2C). Legs moder-ately robust; tibia longer than thigh; sum of tibiaand thigh lengths smaller than SVL; presence ofa discrete tarsal fold; toes slender, long, toelengths I , II , V , III , IV; subarticulartubercles single, conical, protrunding; foot withan elliptical inner metatarsal tubercle, small;outer metatarsal tubercle small, conical, pro-trunding; few supranumerary tubercles, small;toes tip not expanded (Fig. 2D); tarsal tubercle onthe distal third, round. Inguinal glands small, notpigmented; dorsal surfaces warty with scattered,weakly developed, short ridges; presence of one

conspicuous pair of dorsal black tubercles on thesacral region, and another pair between the eyes.Undersurfaces smooth, except for the thighs,which are finely areolate.

Color in Preservative of Holotype.The generalpattern is brown with small black blotches on

dorsum and an interorbital black transversalstripe, covering a pair of tubercles. Dorsalsurfaces of arms are light brown with a transverse

black blotch; legs are light brown with dark brown transverse stripes and small black gran-ules. Flanks are grayish-brown. Ventral surfaceshave a cream background with chest and part ofthe belly gray marbled. Hands and feet aregrayish-brown. Gular and cloacal regions are

black. Measurements of Holotype.SVL 24.8; HL 7.2;

HW 8.8; ED 2.6; TD 1.0; UEW 1.9; IOD 1.8; IND

1.7; END 2.7; THL 10.9; TBL 12.3; FL 13.9.Variation.In some specimens, the dorsolat-eral dermal fold is more evident. Arms in femalesare slender and the inner metacarpal tubercle issmaller than in males. Some specimens havea higher number of small supranumerary tu-

bercles on hands. Instead of a warty skin withdiscrete, short ridges, females MCN 21982199,MNRJ 28982, and MNRJ 30348, and male MNRJ30344 posses a pair of well-developed longitudi-nal ridges from upper eyelids to sacral region andanother short pair between the eyes, and many

longitudinal rows of small granules. A fewspecimens posses a less evident interorbital blacktransversal stripe or it is absent. Tarsal fold is notpresent in some specimens. Coloration patternvaries substantially among specimens. Gularregion is cream with light-brown small blotchesin females. Specimens MNRJ 3034430345 havea cream and light-brown general color pattern.Some specimens present a white or light-brownline on the urostylum. Females MNRJ 30347 andMCN 21982199 have yellowish-brown flanks,and female MNRJ 28982 has a white vertebralline from snout to vent, interrupting the inter-orbital black transversal stripe. Variations onmeasurements are in Table 1.

Vocalization.On 25 October 2001, two male P.erikae calling alternately were recorded emittingcalls with one note consisting of eight harmonics

between approximately 0.34 and 4.8 kHz, withdescendent frequency modulation (Fig. 3A). Themean duration of the call was 0.56 sec (SD5 0.01,range 5 0.530.57, N5 16 vocalizations of twomales), and the mean intercall interval (definedhere as the time from the end of one call to the

beginning of the next call) was 13.42 sec (SD 5

8.87, range 5 4.8535.92, N5 16 vocalizations oftwo males). The fundamental harmonic wasabout 0.34 and 0.78 kHz; dominant frequencywas 3.22 kHz, corresponding to the seventh


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harmonic. The eighth harmonic ranged from 3.24.8 kHz.

Physalaemus erikae call has a shorter durationthan the calls of P. barrioi (1.21.4 sec; Boker-mann, 1967), P. jordanensis (1.41.6 sec;Bokermann, 1967) and P. kroyeri (0.70.9 sec;Bokermann, 1966b), a higher dominant frequency

range than the calls of P. aguirrei (2.03.0 kHz;Bokermann, 1966a), P. albifrons (1.02.0 kHz;Bokermann, 1966b), P. cicada (2.03.0 kHz; Boker-mann, 1966b), and P. cuvieri (0.580.8 kHz;Heyer et al., 1990). Information on the call ofP. soaresi is not available.

Habitat and Distribution.Specimens ofP. erikaewere found in temporary ponds in cow pasturesat the borders of Atlantic Rain Forest remnants,natural clearings inside the forest, and cacaoplantations. Males call from the edges of ponds

or floating on shallow water. Females were foundnear ponds or dwelling on forest floor litter.Males also call during the day after heavy rains.This species was also registered by vocalization,with no specimens captured, at Fazenda Taquara(158589S, 398229W), Municipality of Belmonte,Fazenda Palmeira (158569S, 398389W), Municipal-ity of Itapebi, Mata Cara Branca (168179S,398259W), Municipality of Santa Cruz de Cabra-lia, and Fazenda Alcoprado (178179S, 398409W),Municipality of Teixeira de Freitas. All theselocalities are also situated in southern Bahia,Brazil (Fig. 4). It is also expected to occur in

northeastern Minas Gerais and northern EspritoSanto, because of the proximity and similarity ofvegetation types between south Bahia and theseregions.

Etymology.The specific epithet erikae hon-ors the second authors wife, Erika Costa Elias, ingratitude for her friendship and assistance.

DISCUSSION

The P. cuvieri species group, as proposed byLynch (1970), shows a wide diversity of formsand life histories. The validity of this group asa natural group was questioned by Feio et al.(1999) when they suggested that P. aguirrei, P.maximus, P. olfersii, and P. soaresi could compose

FIG. 3. (A) Sonogram, (B) oscilogram, and (C)power spectrum of the advertisement call of Physalae-mus erikae sp. n.; recorded at RPPN Estacao Veracruz,Porto Seguro, Bahia, Brazil, on 25 October 2001, 2100 h.Air temperature 5 24.48C. Specimen not collected.

TABLE 1. Mean (x), standard deviation (SD), and range of the measurements (in millimeters) of males andfemales of Physalaemus erikae sp. n.

Males (N5 5) Females (N5 13)

x SD Range x SD Range

SVL 23.7 2.1 21.626.6 23.1 2.3 19.227.1HL 7.0 0.8 6.07.8 6.9 0.7 5.77.7HW 7.6 1.0 6.88.8 7.4 0.8 6.08.3ED 2.4 0.1 2.22.6 2.4 0.2 2.02.9TD 1.0 0 1.01.0 0.9 0.2 0.61.2UEW 2.0 0.1 1.92.2 2.0 0.2 1.62.3IOD 2.4 0.3 2.02.7 2.5 0.3 2.03.0IND 1.7 0.1 1.61.8 1.7 0.1 1.61.8END 1.7 0.2 1.31.8 1.7 0.2 1.41.9THL 10.2 0.8 9.210.9 9.9 0.9 7.911.2TBL 11.7 0.9 10.412.7 11.6 1.0 9.112.8FL 12.7 1.0 11.313.9 12.7 0.8 10.713.6


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a separate species group, because of morpholog-ical similarities and the habit of reproducing onforested areas. It is possible that as the knowledgeof the relationships between the Physalaemusspecies grows other groups will be proposed.

The discovery of a new species of Physalaemusoccurring over a relatively broad area demon-

strates the current poor knowledge about taxon-omy and composition of species in large regionsof the Atlantic Rain Forest in Brazil. The lastspecies of the P. cuvieri group described fromBrazil was P. lisei, which occurs in the AtlanticRain Forest of southern Brazil (Braun and Braun,1977). Because of the high level of anthropogenicpressure that the Atlantic Rain Forest experien-ces, field studies on distribution and compositionof herpetological communities are vital. Thesestudies might reveal other new species andidentify centers of endemism, population fluctu-ations, and other important data regarding thetaxonomy, conservation, and management oflowland tropical forest anurans.

Acknowledgments.D. L. Silvano made possi-

ble the collection of specimens in Bahia. Wethank L. B. Nascimento and U. Caramaschi forcomments on the manuscript; L. B. Nascimentoalso contributed with valuable suggestions andinformation; P. H. C. Cordeiro, R. T. Moura, A.Paglia, and R. V. Lopes for field assistance; P. R.Nascimento for the drawings; the owners of the

localities visited for the permission and supportto collect in their areas; Conselho Nacional deDesenvolvimento Cientfico e Tecnologico(CNPq) for the grants and financial support.This study is a result of the subproject Ecolog-ical Approaches and Economic Instruments forthe Establishment of the Discovery Corridor:a Strategy to Revert Forest Fragmentation of theAtlantic Forest at Southern Bahia, supported bythe Project on the Conservation and SustainableUse of the Brazilian Biological Diversity/Brazil-ian Ministry of the Enviroment (PROBIO/MMA), Center for Applied Biodiversity Sci-ence/Conservation International (CABS/CI),The World Bank, and coordinated by the In-stitute for Social and Enviromental Studies ofSouthern Bahia (IESB).

FIG. 4. Distribution ofPhysalaemus erikae sp. n. (dots) in southern Bahia, Brazil.


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LITERATURE CITED

BOKERMANN, W. C. A. 1966a. Dos nuevas especies dePhysalaemus de Espiritu Santo, Brasil Physis 26:193202.

. 1966b. Notas sobre tres especies de Physalae-mus de Maracas, Bahia (Amphibia, Leptodactyli-

dae). Revista Brasileira de Biologia 26:253259.. 1967. Tres novas especies de Physalaemus dosudeste brasileiro (Amphibia, Leptodactylidae).Revista Brasileira de Biologia 27:135143.

BRAUN, P. C., AND C. A. S. BRAUN. 1977. Nova especie dePhysalaemus do Rio Grande do Sul (Anura, Lep-todactylidae). Revista Brasileira de Biologia 37:86771.

CARAMASCHI, U., L. C. CARCERELLI, AND R. N. FEIO. 1991.A new species of Physalaemus (Anura: Leptodacty-lidae) from Minas Gerais, southeastern Brazil.Herpetologica 47:148151.

CARAMASCHI, U., R. N. FEIO, AND A. S. GUIMARAES-NETO.2003. A new, brightly colored species of Physalae-

mus (Anura: Leptodactylidae) from Minas Gerais,southeastern Brazil. Herpetologica 59:519524.

FEIO, R. N., J. P. POMBAL JR., AND U. CARAMASCHI. 1999.New Physalaemus (Anura: Leptodactylidae) fromthe Atlantic Forest of Minas Gerais, Brazil. Copeia1999:141145.

FROST, D. R. 2002. Amphibian Species of the World: anonline reference. V2.21 (15 July 2002). Electronicdatabase available at ,http://research.amnh.org/herpetology/amphibia/index.html..

HEYER, W. R., A. S. RAND, C. A. G. CRUZ, O. L. PEIXOTO,AND C. E. NELSON. 1990. Frogs of Boraceia. Arquivosde Zoologia 31:231410.

IZECKSOHN, E. 1965. Uma nova especie de PhysalaemusFitzinger, do Estado do Rio de Janeiro (Amphibia,Anura). Revista Brasileira de Biologia 25:165168.

LYNCH, J. D. 1970. Systematic of the Americanleptodactylid frog genera Engystomops, Eupemphix,and Physalaemus. Copeia 1970:488496.

SAZIMA, I. , AND U. CARAMASCHI. 1986. Descric ao

de Physalaemus deimaticus, sp. n., e observac~oessobre comportamento deimatico em P. nattereri(Steindn.)Anura, Leptodactylidae. Revista deBiologia 13:91101.

Accepted: 9 July 2004.

APPENDIX 1

Specimens Examined

Physalaemus aguirrei: MNRJ 2093820943 (Conceicaoda Barra, ES). Physalaemus albifrons: MNRJ 2406224063

(Brejo Santo, CE). Physalaemus barrioi: MZUSP 84821,MZUSP 84823, MZUSP 8428526, MZUSP 8482829(topotypes, Sao Jose do Barreiro, SP). Physalaemuscicada: EI 6152 (paratopotype, Maracas, BA); MNRJ28552, MNRJ 26040 (Brejo Santo, CE). Physalaemuscuvieri: MNRJ 66016615 (Fortaleza, CE). Physalaemus

jordanensis: ZUEC 44794480, ZUEC 6257-6258 (Pocosde Caldas, MG) Physalaemus kroyeri: MZUSP 9651596518, MZUSP 96522, MZUSP 96527, MZUSP 9654496545, MZUSP 96472, MZUSP 96478, MZUSP 96483,MZUSP 96485, MZUSP 96487, MZUSP 96490, MZUSP96493, MZUSP 96501 (Maracas, BA). Physalaemussoaresi: EI 17821783 (paratopotypes, Seropedica, RJ).


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