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Redescription of Physalaemus Spiniger (Anura: Leptodactylidae) and Description of Two New Reproductive Modes

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Redescription of Physalaemus Spiniger (Anura: Leptodactylidae) and Description of Two New Reproductive Modes RATTLESNAKE HARVEST IN FLORIDA 557 Histories,and Influenceon Mankind,2nd ed. Univ. TIMMERMAN, W. W. 1995. Home range, habitat use, CaliforniaPress, Berkeley. and behavior of the eastern diamondbackrattle- NEILL, W. T. 1961. Giant rattlesnakes-past and pres- snake (Crotalus adamanteus) on the Ordway Pre- ent. FloridaWildl. 15:10-13. serve. Bull. FloridaMus. Nat. Hist. 38:127-158. SNYDER, B. 1949. Diamondbacksand dollarbills. Flor- TINKLE,D. W. 1962.Reproductive potential and cycles ida Wildl. 3:3-5, 16, 19. in female Crotalusatrox from northwesternTexas. TELFORD, S. R., JR. 1952. A herpetological survey in Copeia 1962:306-313. the vicinity of LakeShipp, Polk County,Florida. Q. J. FloridaAcad. Sci. 15:175-185. Accepted:5 August 1998. Journalof Herpetology,Vol. 32, No. 4, pp. 557-565, 1998 Copyright1998 Societyfor the Study of Amphibiansand Reptiles Redescription of Physalaemus spiniger (Anura: Leptodactylidae) and Description of Two New Reproductive Modes CELIO E B. HADDAD13 AND JOSE P. POMBAL, JR.2 'Museum of VertebrateZoology, University of California,Berkeley, California 94720, USA, and 2Departamentode Vertebrados,Museu Nacional, Quinta da Boa Vista, 20940-040 Rio de Janeiro,Rio de Janeiro,Brasil ABSTRACT.-We redescribe Physalaemus spiniger and describe its tadpole and its reproductive modes. This species has the following three alternative reproductive modes: (1) foam nest on pond and feeding tadpoles in pond (the typical mode for the genus Physalaemus); (2) foam nest on humid places on the forest floor near a pond, and feeding tadpoles in pond; (3) foam nest on water accumulated on the axils of terrestrial bromeliads and feeding tadpoles in pond. These last two modes were not included in the reviews of repro- ductive modes in anurans. The vocalizations of P?spiniger are described and compared with the vocalizations of P nanus, a sibling species. Miranda-Ribeiro (1926) described Engysto- bal and Madureira, 1997): P bokermanniCardoso mops spinigera from Iguape, Sao Paulo State, and Haddad, P caete Pombal and Madureira, P southeastern Brazil, attributing the specific crombiei Heyer and Wolf, P maculiventris (A. name to Boulenger because the specimens were Lutz), P moreirae (Miranda-Ribeiro), P nanus so identified in the collection of the Museu Pau- (Boulenger), P obtectus Bokermann, P olfersii lista (currently Museu de Zoologia da Univer- (Lichtenstein and Martens), P signifer (Girard), sidade de Sao Paulo). However, Boulenger never and P spiniger (Miranda-Ribeiro). In recent years described Engystomops (=Physalaemus) spinigera we collected and observed specimens of P spi- and accordingly the short account by Miranda- niger at several localities in southern and south- Ribeiro (1926) serves as the original description. eastern Brazil. Herein, we redescribe this species The specific name Engystomopsspinigera was ap- and its tadpole. The vocalizations are described parently forgotten and ignored by subsequent and compared with the vocalizations of P nanus, authors (e.g., Cochran, 1955; Bokermann, 1966a; a sibling species. Also, we provide information Lynch, 1970; Frost, 1985; Heyer and Wolf, 1989; on reproduction, including two new reproduc- Duellman, 1993). Lynch (1970) recognized four tive modes for anurans. in the Physalaemus:P bili- species groups genus MATERIALS AND METHODS gonigerus group, P cuvieri group, P pustulosus group, and P signifer group; P deimaticus and P Specimens used in the description or exam- rupestris are not presently allocated to any spe- ined for comparisons are deposited in AL-MN cies group (Sazima and Caramaschi, 1986; Car- (Adolpho Lutz collection, deposited in Museu amaschi et al., 1991). Ten species are presently Nacional, Rio de Janeiro, RJ,Brasil), CFBH (Celio allocated to the Physalaemussignifer group (Pom- F B. Haddad collection, deposited in Departa- mento de Zoologia, Universidade Estadual Pau- lista, Rio Claro, SP, Brasil), MNRJ (Museu Na- 3Present Address: Departamento de Zoologia, cional, Rio de Janeiro, RJ, Brasil), MZUSP (Mu- UniversidadeEstadual Paulista,13506-900 Rio Claro, seu de Zoologia da Universidade de Sao Paulo, Sao Paulo,Brasil, E-mail: [email protected] Sao Paulo, SP, Brasil), WCAB (Werner C.A. Bok- 558 C. F. B. HADDAD AND J. P. POMBAL, JR. ;, s. Wj *e- ,<w I4 * a.. 0 VI FIG. 1. Physalaemusspiniger, an adult male in life from Ilha do Cardoso,Canan6ia, SP, Brazil. ermann collection, deposited in Museu de Zoo- RESULTS logia da Universidade de Sao Paulo, Sao Paulo, and with other ZUEC de Hist6ria Diagnosis Comparison Species.- SP, Brazil), (Museu Natural, A to the Physalaemus Universidade Estadual de species belonging signifer Campinas, Campinas, (sensu 1970), characterized (1) Additional examined are group Lynch, by SP, Brasil). specimens small size (males 17.1-21.3 mm SVL, females listed in 1. Appendix 20.6-22.0 mm SVL); (2) canthus rostralis dis- Abbreviations used in the measurements of tinct; (3) dorsal skin texture smooth to rugose; the adults are SVL HL (snout-vent length), (4) belly orange in life; (5) structure of the ad- (head length), HW (head width), ED (eye di- vertisement call. THL TBL ameter), (thigh length), (tibia length), Physalaemus spiniger is distinguished from P and FL All measurements are ex- (foot length). caete, P moreirae,P obtectus, and P olfersii by its in millimeters. The measurements of pressed smaller size (combined SVL of males ranging the adults follow Duellman (1970) and Cei 22.5-34.5 mm; Bokermann, 1966b; Heyer, 1985; (1980). Measured adult specimens were fixed in Heyer and Wolf, 1989; Heyer et al., 1990; Pombal 10% formalin and maintained in 70% ethyl al- and Madureira, 1997). By its larger size and dis- cohol. Eggs and tadpoles were fixed and main- tinct advertisement call, P spiniger differs from tained in 5% formalin. For measurements we P bokermanni(P bokermannimales with 15.3-17.0 used an ocular micrometer in a Zeiss stereo- mm SVL; see Cardoso and Haddad, 1985). Phys- microscope, except that SVL was measured with alaemus spiniger differs from P signifer by calipers. Drawings of the adult and tadpole smoother dorsal skin (more rugose in P signifer), were made using a Zeiss stereomicroscope with larger black spot on the inguinal glands, and a drawing tube. Vocalizations were recorded us- smaller mean length (P signifer males with SVL ing a Nagra E tape recorder with a Sennheiser = 20.1-22.4, x = 21.7, SD = 0.7, N = 20). Phys- ME 80 microphone at a tape speed of 19 cm/s. alaemus spiniger differs from P crombiei by the The sonagrams were produced by a Macintosh orange belly (pinkish in P crombiei;Heyer and computer coupled to the MacRecorded Sound Wolf, 1989) and distinct advertisement call (see System 2.0.5, using 8 bit resolution, 22 kHz sam- below and Heyer and Wolf, 1989). Physalaemus pling frequency, and FFT with 256 points. spiniger differs from P maculiventris by wider REDESCRIPTION AND REPRODUCTION OF PHYSALAEMUS SPINIGER 559 I \ci B A, t/ C D FIG.2. Physalaemusspiniger, CFBH 0307. (A) Dorsal and (B) lateral views of head; ventral views of (C) hand and (D) foot (scales = 3.0 mm). head and snout, and by posterior belly light col- chest; vocal slits present in males; choanae ored (boldly dark and light mottled in P macu- small, nearly round; tongue narrow, long; vo- liventris). Preserved specimens of P nanus and P merine teeth absent; maxillary teeth not visible, spiniger are indistinguishable; however, they but discernible by probe. Arms slender, fore- have different advertisement calls (see below). arms moderately robust in males (in females Description of Adults.-Body slender (Fig. 1); slender); fingers short; brown nuptial pad on head wider than long; snout rounded and pro- thumb in males; subarticular tubercles single, truding in dorsal and lateral views (Fig. 2A, B); protruding and rounded; outer metacarpal tu- nostril slightly protuberant, directed laterally; bercle large to small, rounded (81% of speci- canthus rostralis distinct; loreal region concave; mens) or ovoid (19% of specimens); inner met- eye slightly protuberant; tympanum indistinct acarpal tubercle large to medium, nearly ellip- to weakly distinct; distinct supratympanic fold tical, sometimes rounded; supernumerary tu- from tympanum to shoulder; narrow dorsolat- bercles small; finger tips not expanded; finger eral fold extending from posterior corer of eye lengths I = IV (or rarely IV < I) < II < III (Fig. to inguinal region; males with subgular vocal 2C). Legs moderately robust; tibia longer than sac, expanded externally, extending to border of thigh; foot with an inner metatarsal tubercle 560 C. F. B. HADDAD AND J. P. POMBAL, JR. TABLE1. Measurements (in mm) of males and fe- 4- males of Physalaemusspiniger. -2 A N Males (N = 28) Females(N = 4) x SD Range x SD Range B 2 SVL 18.8 1.0 17.1-21.3 21.1 0.6 20.6-22.0 z e HL 5.2 0.4 4.0-5.8 5.9 0.3 5.7-6.5 HW 5.9 0.3 5.2-6.5 6.3 0.1 6.2-6.5 ED 2.1 0.2 1.8-2.6 2.3 0.3 2.0-2.7 THL 8.6 0.3 8.1-9.3 9.5 0.4 9.1-10.0 Lo2 TBL 9.3 0.4 8.5-10.5 10.2 0.3 9.9-10.7 FL 9.1 0.4 8.2-10.0 10.2 0.2 9.9-10.4 TIME 0.2 s the arrow marks sometimes with a fine light ^^j^Uilgl,^ D border, in some specimens dorsal marks not ev- ident; a white line on the dorsolateral fold (sometimes absent); flanks below the dorsolat- eral fold, black; forearm light brown or gray, with a dark brown transverse bar; elbow dark IIIIII. E brown; thigh, tibia, and foot light brown, brown or gray, similar to the color of the dorsum; thigh and tibia with a dark brown transverse bar; two " MTT black bars on the upperparts of thigh and tibia; TIME , anal dark; cream or chest and 0.2 s region belly gray; throat gray or dark brown.
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