Description of a New Reproductive Mode in Leptodactylus (Anura, Leptodactylidae), with a Review of the Reproductive Specialization Toward Terrestriality in the Genus

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U'/Jeia,2002(4), pp, 1128-1133

Description of a New Reproductive Mode in Leptodactylus (Anura, Leptodactylidae), with a Review of the Reproductive Specialization toward Terrestriality in the Genus

CYNTHIA P. DE A. PRADO,MASAO UETANABARO,AND Ctuo F. B. HADDAD

The genus Leptodactylusprovides an example among anurans in which there is an evident tendency toward terrestrial reproduction. Herein we describe a new reproductive mode for the frog Leptodactyluspodicipinus, a member of the "melanonotus" group. This new reproductive mode represents one of the intermediate steps from the most aquatic to the most terrestrial modes reported in the genus. Three reproductive modes were previously recognized for the genus Leptodactylus.However, based on our data, and on several studies on Leptodactylusspecies that have been published since the last reviews, we propose a new classification, with the addition of two modes for the genus.

T HE concept of reproductive mode in am- demonstrated by species of the "fuscus" and phibians was defined by Salthe (1969) and "marmaratus" groups. Heyer (1974) placed the Sallie and Duellman (1973) as being a combi- "marmaratus" species group in the genus Aden- nation of traits that includes oviposition site, omera.Species in the "fuscus" group have foam ovum and clutch characteristics, rate and dura- nests that are placed on land in subterranean tion of development, stage and size of hatch- chambers constructed by males; exotrophic lar- ling, and type of parental care, if any. For an- vae in advanced stages are released through urans, Duellman (1985) and Duellman and floods or rain into lentic or lotic water bodies. Trueb (1986) recognized 29 modes of repro- Frogs in the genus Adenomeraalso deposit foam duction, although in recent studies on ecology nests in subterranean chambers, and in most and natural history new reproductive modes species,tadpoles develop inside these chambers have been described (e.g., Haddad and Hodl, and are endotrophic, that is, entire develop- 1997; Haddad and Pombaljr., 1998; Haddad mental energy is obtained from vitellogenic yolk and Sawaya,2000). Amphibians exhibit a great (Heyer; I969J. More recemly.. DeJa R;.a (1~95} diversity of reproductive modes, especially in described another reproductive mode for the the New World tropics, including a clear trend genus Adenomera,which corresponds to the same reproductive mode of the L. fuscusgroup. toward terrestriality (Duellman, 1985), that is, In the present paper, we report a new repro- reproduction becoming gradually independent ductive mode in a leptodactylid frog, Leptodac- of water bodies. tylus podiciPinus,a member of the "melanonotus" Members of the family Leptodactylidae exhib- group, in the Pantanal, southwestern Brazil. -it several reproductive modes ranging from Based in this new reproductive mode, and on aquatic to terrestrial breeding, with many inter- data published after Heyer's (1969) review, we mediate forms depositing eggs embedded in update the reproductive modes exhibited by the foam nests (Heyer, 1969). Species of Leptodacty- species of Leptodactylusand propose a new clas- ius and of the related genus Adenomeraare an sification of modes for the genus. example in which a tendency toward terrestriality is evident (Heyer, 1969; Duellman, 1985). Heyer (1969) proposed that Leptodactylusspe- MATERIALS AND METHODS cies belonging to the "ocellatus" and "melanon- The study was conducted in the southern Pan- otus" groups have the most primitive reproduc- tanal, municipality of Corumba, State of Mato tive modes. Species of both groups deposit eggs Grosso do SuI, southwestern Brazil (19°34'S, in foam nests on top of the water and tadpoles 5TOO'W). The Pantanal is a floodplain, with an are exotrophic, feeding and developing in wa- area of approximately 140,000 km2 and an ele- ter. According to Heyer's (1969) review, species vation between 75 and 200 m above sea level, in the "pentadactylus" group show the first step delimited mostly by the Paraguay river in the to a more terrestrial life (Heyer, 1969), with west and Brazilian uplands in the east (see Por, foam nests deposited in depressions or burrows 1995). The region is characterized by a seasonal at the edges or close to water and producing climate ("Aw" type in Koppen's classification), exotrophic tadpoles. More specialized modes with a rainy summer from October to April and

@ 2002 by the American Society of Ichthyologist, and Herpetologists are PRADO ET Ai .REPRODUCTIVE MODE IN LEPTODACTYLUS

a dry winter from May to September. Annual floods occur in the Pantanal, and at the study site, along the Miranda river, floodings are com- mon from January to April. The "cerrado" (sa- vanna-like vegetation) predominates in the area, with patches of semideciduous forests, gallery forests, and grassland fields. Observations on LeptodactyluspodiciPinus were made at ponds and flooded areas near the Base de Estudos do PantanalfUniversidade Federal de Mato Grosso do SuI (57°00'W, 19°34'S). Data reported here were collected between January 1998 and March 1999, and from January to April 2001. Diameter and depth of the depressions where males called were measured with a measuring tape to the nearest 0.1 cm. Calling males were captured and toe clipped according to Waichman (1992) between 23 March and 08 April 2001. Snout-vent length (SVL) was measured in the field to the nearest 0.1 mm with a caliper. Then, individuals were released at their capture point. Calling sites were also marked. Clutches were collected and immediately pre- served in 10% formalin; number of eggs per clutch was determined and egg diameter measured with an ocular micrometer in a Zeiss ste- reomicroscope (:t 0.1 mm). The terminology used to describe larval nourishment follows Thi- baudeau and Altig (1999).

RESULTS Basin description.-Basins of L. podiciPinuswere observed at the edges of permanent ponds and flooded areas, among grass clumps or aquatic plants. Each depression was approximately cir- cular, with a mean diameter of 61.0 mm :!: 4.5 SD (range = 50-70, n = 16). Water inside the depressions, which permeated from the adjacent water bodies, averaged 31.0 mm :!: 4.5 SD of depth (range = 24-40, n = 16). In general, males called from the interior of the basins with their bodies partially submerged (Fig. 1). Call- ing males were difficult to see because basins Fig. 1. (A) Dorsal and (B) lateral views of a male were well covered by the marginal vegetation, of LeptodactyluspodiciPinus calling inside an excavated fallen leaves or dead vegetation, which func- basin (Corumba, Mato Grosso do Sui, South Pantanal, tioned as a roof. In 24 basins that we observed, Brazil). (B) Note that leaves function as a roof for the all were covered by vegetation and males calledbesidebasin.. Drawn from photographs. the basin in two cases; the remaining 22 males were inside the depressions. Mean distance to the nearest occupied basin was 2.5 m sured. Five marked males were recaptured from :!: 2.1 SD (range = 0.6-8.4, n = 12). As water one to three times on successivenights during level decreased, new nests were constructed fol- a 15-day study period. Mean SVL of recaptured lowing the water line at the edges of the water males (33.8 mm :!: 0.8 SD, range = 32.7-34.5, bodies, and the older ones were abandoned. n = 5) was larger (t = 4.41, P = 0.001) than those that were not recaptured (31.0 mm :!: 1.0 Behavior of males.-Nine vocalizing males thatwereSD, range = 30.0-32.4, n = 4). Two males were inside their basins were marked and mea- recaptured three times at the same sites, al-

1129 1130 COPEIA, 2002, NO.4

though they had moved to new basins near the scription of calling and oviposition sites are original ones as the water level decreased. Two lacking. An exception is a study conducted by other males were recaptured; one of them, Martins (1996) in which he reported the occur- marked on 29 March 2001, was recaptured six rence of males of L. podiciPinuscalling from ba- days later calling in a new basin 4.5 m from the sins at the edges of water bodies in the State of original site, and the second male was recap- Sao Paulo, Brazil. We observed the same situa- tured six days later approximately 10 m from tion for this species in the Pantanal. the original site. One male was recaptured twice We did not observe the construction of the inside the same basin. Three other males cap- basins, but Martins (1996) observed males con- tured calling inside their depressions were structing basins with their snouts and suggested marked at night in March 1999. These maleswerethat males could use either natural or construct- recaptured resting inside the depressions ed depressions. Female parental care of tad- the next morning. poles was observed at our study site, but wefailed to observe females attending eggs. Nev- Clutchesand femaleparental care.-Foam nests of ertheless, Martins (1996, 2001) observed fe- L. podiciPinuswere observed inside basins inJan- males attending eggs and tadpoles. Based on uary 1998, September 1998, and January 1999. this information, our observations on the be- The eggs were pigmented, with a mean diame- havior of males, and the uniform dimensions of ter of 1.1 mm :!: 0.05 SD (range = 1.0-1.2, n = the depressions we have measured, we consider 21 eggs from two clutches), and mean number that L. podiciPinusexhibits a new reproductive of eggs per clutch was 2102.5 :!: 442.1 SD (range mode, which can be summarized as follows: pig- = 1750-2953, n = 6 clutches). The foam nests mented eggs and early larval stages in foam were covered by dead vegetation and mean wa- nests, which are deposited in water-filled basins ter depth inside the basins was 26.3 mm :!: 3.2 constructed by the males adjacent to water; ex- SD (range = 24-30, n = 3). Oviposition was otrophic tadpoles in ponds; females perform observed once inside a basin covered by aquatic parental care, attending eggs and tadpoles. vegetation in April 2001. Among the reproductive modes exhibited by Females of L. podicipinus attending tadpoles anurans, the generalized mode of aquatic eggs were observed (n = 14), generally, in the mar- and tadpoles is considered to be primitive gin of ponds or flooded areas, where water (Duellman, 1985). The evolution of specialized depth was about 5 cm. Females remained close modes, with eggs deposited in protected sites or to the tadpole schools. When tadpoles were dis- out of water, have been considered to be adap- turbed, almost all females were aggressive, es- tations against aquatic predators (Magnusson pecially those with hatchlings, jumping and and Hero, 1991; Haddad and Sawaya,2000).The knocking with their heads against observers' reproductive mode of L. podicipinus could hands. They also performed pumping move- have evolved in response to predation pressure ments (sensuWells and Bard, 1988), after which on eggs, embryos, and even adults (e.g., calling they usually dived and emerged at short dis- males, amplexed pairs during oviposition, andfemales tances, being followed by the tadpoles. Females attending eggs). Although females of L.podiciPinus were observed attending tadpoles at different attend nests and tadpoles until meta- developmental stages. For six foam nests ex- morphosis (Prado et al., 2000; Martins, 2001; amined, we did not observe females attending present study), the deposition of foam nests in- the eggs, although we suggest that they do be- side vegetation-covered basins may provide ad- cause females attended tadpoles. ditional protection for the eggs and embryos. Adult males were observed inside leaf-covered basins during the day. Visual predators, likewading DISCUSSION birds, were observed preying upon oth- Reproductivemode in Leptodactyluspodicipinus.- er anuran species (Leptodactyluschaquensis and LeptodactyluspodiciPinus occurs in open forma- Pseudisparadoxa) during the day at the study site tions of P~raguay, Argentina, and Bolivia, and (CPAP, pers. obs.). It seems that the basins the Amazon basin, central Brazil through the could also function as shelter sites for L. podi- southeast and south of that country (Heyer, cipinus males, avoiding or diminishing preda- 1994). The reproductive biology of this species, tion risk. like that of many tropical species, is poorly Studies on other species of the "melanonotus" known (Vizotto, 1967; Rossa-Feres and Jim, group show no evidence of basin construction 1994). Recent studies report the existence of fe- by males (e.g., L. teptodactyloides:Heyer and Bel- male parental care of eggs and tadpoles (Prado lin, 1973, reported as L. wagneri;either L. tepto- et al., 2000; Martins, 2001), but the exact de- dactyloidesor L. wagneri: Duellman, 1978; L. val- PRADO ET AL.-REPRODUCTIVE MODE IN LEPTODACTYLUS

idus: Downie, 1996). Nevertheless, Downie (1996) pointed out that clutches of L. validus in Trinidad were always found at the edges of small ponds, usually well covered by dead vegetation. It is possible that the reproductive "- mode described here for L. podiciPinus occurs ",' in other species of the "melanonotus" group, but ~~,' more detailed studies on their reproductive behavior are necessary. Fig. 2. Schematic representation of sequential steps of the reproductive modes in the genus Lepta- Female parental care of eggs and tadpoles in dactylus,from the most aquatic to the most terrestrial. species of the "ocellatus" and "melanonotus" (1) Eggs in foam nest on top of water; tadpoles in groups (e.g., Wells and Bard, 1988; Prado et al., lentic water, (2) eggs in foam nest in depressions close 2000; Martins, 2001) reinforces Heyer's (1969) to water; tadpoles in lentic water, (3) eggs in foam proposition that members of both groups are the nest in water-filled basins excavated by males; tadpoles most closely related of the four Leptodactylus in lentic water, (4) eggs in foam nest in subterranean groups he identified. However, the reproductive chambers constructed by males; tadpoles in lentic wa- mode of L. podiciPinus,a member of the "melan- ter, (5) eggs in foam nest in burrows; larval develop- onotus" group, represents a specialization possi- ment in the foam nest inside the burrows. New steps proposed for the genus Leptodactylussince Heyer bly derived from the primitive mode present in (1969) are (3) and (5). species of the "ocellatus" group and some species of the "melanonotus" group, representing one step toward terrestrial reproduction in the genus. rable to the mode described for some species of Adenomera(Heyer, 1969; De la Riva, 1995). Reproductivemodes in the genus Leptodactylus.- Leptodactyluspentadactylus apparently has two Heyer (1969) proposed four reproductive stages reproductive modes: (1) deposition of foam for the speciesgroups of the genus Leptodactylus, nests in open depressions ("potholes"); subse- including the species of Adenomera.Several stud- quent to flooding, exotrophic tadpoles develop ies on Leptodactylusspecies have been published in water (Breder, 1946), as in other species of since, resulting in new information regarding the group mentioned above; (2) a reproductive their reproductive biology (e.g., Rodriguez and mode similar to that described for L. fallax Duellman, 1994; Davis et al., 2000; Eterovick (Hero and Galatti, 1990; Rodriguez and Duell- and Sazima, 2000). An interesting group con- man, 1994), that is, a foam nest inside burrows cerning reproduction within the genus Lepta- in the ground and development of larvae inside dactylusis the "pentadactylus" group, which has the nest. Muedeking and Heyer (1976) ob- at least two reproductive modes. The first mode served nests of L. pentadactylusin Panama de- is the deposition of foam nests in water-filled posited in apparently excavated potholes, and depressions at the edges of water bodies; sub- at a distance from water bodies. These authors sequent to flooding, exotrophic tadpoles devel- also registered the coexistence of larvae and op in water (e.g., L. knudseni:Hero and Galatti, eggs in the same nests, and noted that some of 1990; Rodriguez and Duellman, 1994; L. labyrin- the larvae had yolk-colored guts, which was in- thicus: Agostinho, 1994; CFBH, pers. obs.). terpreted to indicate ingestion of eggs by the Whether these depressions are natural or con- larvae. As suggested by Muedeking and Heyer structed remains unclear. The ultimate special- (1976), possibly the normal pattern for L. pen- ization in the "pentadactylus" group is the total tadactylus is the release of tadpoles in water terrestrial reproductive mode described for L. through floods of potholes, as observed by fallax (Davis et al., 2000). In this species foam Breder (1946). Nevertheless, in unfavorable nests are placed in burrows in the ground, and conditions of rain, larvae could remain in the tadpoles develop inside the nests, but some de- nest feeding on eggs up to metamorphosis tails on reproduction and larval development (Muedeking and Heyer, 1976). The latter situ- need to be clarified. Also in this species it is not ation was observed by Hero and Galatti (1990) clear whether the cavities used are natural or in Central Amazonia, although they did not constructed (Davis et al., 2000). Although Les- mention how larvae were nourished. It is pos- cure and Letellier (1983) reported that tadpoles sible that the alternative modes present in L.pentadactylus of L. fallax develop to metamorphosis inside the are partially associated with feed- nest by metabolizing vitelline reserves, Davis et ing diversity exhibited by the larvae, which can al. (2000) described tadpoles without yolk sacs. feed on algae, foam (Vinton, 1951), other tad- If tadpoles develop only on their yolk, this re- poles (Heyer et aI., 1975), and eggs (Muedeking productive mode could be considered compa- and Heyer, 1976). Also, the presence of a foam

~131 1132 COPEIA, 2002, NO.4

TABLE 1. DIVERSITY OF REPRODUGnVE MODES IN LEPTODACfYLID FROGS OF THE GENUS Leptodactylus, FROM THE MOST AQUATIC TO THE MOST TERRESTRIAL.In bold, the new steps proposed since Heyer (1969).

Reproductivemode Examples 1. Eggs and early larval stages in foam nest on Species of the L. oceUatus(e.g., L. bolivianus,L. cha- top of the water; exotrophic tadpoles in quensis,L. ocellatus)and L. melanonotusgroups lentic water. (e.g., L. leptodactyloides,L. validus). 2. Eggs and early larval stages in foam nest in Some species of the L. pentadactylusgroup (e.g., L. water-filled depressions close to water; sub- knudseni,L. laiJyrinthicus,L. pentadactylus). sequent to flooding, exotrophic tadpoles in lentic water. 3. Eggs and early larval stagesin foam nest in One species of the L. melanonotusgroup (L. podicipi- water-filled basins constructed by males; nus). exotrophic tadpoles in lentic water. 4. Eggs and early larval stages in foam nest in L. fuscus group (e.g.. L. cunicularius,L. elenae,L. fur- subterranean chambers constructed by narius, L. fuscus,L. jolyi, L. mystaceus,L. notoakti- males; subsequent to flooding, exotrophic its). tadpoles in lentic or lotic water. 5. Eggs in foam nest in burrows, either close or Somespecies of dIe L. pentadactylusgroup (e.g.,L. far from water; larval development in the fallax, L. pentadactylus). foam nest inside the burrows".

'It remains unclear whether tadpoles of L. fallax develop only on their vitelline reserves, or whether they have another nutrition source (see text for references).

nest provides protection from desiccation to ACKNOWLEDGMENTS tadpoles, as previously mentioned by Heyer (1969). Alternatively, the occurrence of these We thank M. A. Donnelly, R. P. Bastos, andW. different reproductive modes could indicate the R. Heyer for critically reading the manu- existence of more than one species (W. R. Hey- script and for the valuable suggestions that er, pers. comm.). helped us to improve the text,J. R. Somera for Oophagous tadpoles are also known for other the drawing, and E. A. Pedroso, E. Pereira, E. species of the "pentadactylus" group. Tadpoles Q. Gomes, and P. Landgref Filho for field assis- of L. knudsenifeed on conspecific eggs placed tance. This study was made possible by the lo- later in the same pond (CFBH, pers. obs.). gistical support of Base de Estudos do Pantanal/ Agostinho (1994) verified that a mean of 90% Universidade Federal de Mato Grosso do SuI. C. of eggs present in foam nests of L. labynnthicus P. A. Prado and M. Uetanabaro acknowledge were not fertilized and were consumed by the CNPq for financial support (proc. 521746/97- tadpoles, which could survive in the nest for al- 3/NV). C. P. A. Prado acknowledges CNPq for most 30 days before being carried to water by a graduate fellowship (procs. 351228/97-7, rain. Female deposition of eggs that are not fer- 140397/2000-0). C. F. B. Haddad acknowledges tilized, but instead, supply nourishment for tad- CNPq and FAPESPfor financial support. poles can occur in other species of the "pentadactylus" group and could explain larval nutri- LITERATURE CITED tion in L. fallax. The reproductive mode of L. podiciPinus is AGOSTINHO, C. A. 1994. Characterization of Leptodac- tylus labyrinthicus (Spix, 1824) population, and eval- one of the transitional steps from aquatic to ter- uation of its performance in captivity. Unpubl. restrial breeding within the genus (Fig. 2). In Ph.D. diss., Universidade Federal de Silo Carlos, this case, males construct water-filled basins at Silo Carlos, Silo Paulo, Brasil (In Portuguese). the edges of ponds, which are covered by leaves BREDERJR., C. M. 1946. Amphibians and reptiles of or dead vegetation. Exotrophic tadpoles hatch the Rio Chucunaque drainage, Darien, Panama, in these nests and develop in water. In Table 1, with notes on their life histories and habits. Bull. we summarized the reproductive modes known Am. Mus. Nat. Rist. 86:375-436. for the genus Leptodactylus.Analysis of all avail- DAVIS, S. L., R. B. DAVIS, A. JAMES, AND B. C. P. TALIN. able information reveals that the pathway to ter- 2000. Reproductive behavior and larval development of Leptodactylus fallax in Dominica, West In- restrial reproduction in the genus Leptodactylus dies. Rerpetol. Rev. 31:217-220. is complex, with many intermediate steps, sim- DE LA RIVA, 1.1995. A new reproductive mode for the ilar to the one described in our study, remain- genus Adenomera (Amphibia: Anura: Leptodactyli- ing to be discovered. dae): taxonomic implications for certain Bolivian PRADO ET AL.-REPRODUCTIVE MODE IN IEFTODACTYLUS 1133

and Paraguayan populations. Stud. Neotrop. Fauna Parental care behaviour in Leptodactylus Environ. 30:15-29.DOWNIE,]. podicipinus (Cope, 1862) (Anura, Leptodactylidae). R. 1996. A new example of female parental Herpetol.J.11:29-32. behaviour in Leptodactylusvalidus, a frog of the lep- MUEDEKING, M. H., AND W. R. HEWR. 1976. Descrip- todactylid "melanonotus" speciesgroup. Herpetol.]. tions of eggs and reproductive patterns of Leptodac- 6:32-34. tylus pentadactylus (Amphibia: Leptodactylidae). DUELLMAN,W. E. 1978. The biology of an Equatorial Herpetologica 32:137-139. herpetofauna in Amazonian Ecuador. Univ. Kans. POR, F. D. 1995. The Pantanal of Mato Grosso (Bra- Nat. Hist. Mus., Misc. Publ. 65:1-352.-.1985. zil): world's largest wetlands, p. 1-122. In: Mono- Reproductive modes in anuran amphib- graphiae Biologicae. H. J. Dumont and M. J. A. ians: phylogenetic significance of adaptive strate- Werger (eds.). Vol. 73. Kluwer Academic Publish- gies. South Mr.]. 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An alphanumeric code for toe -, ANDM. S. BELLIN. 1973. Ecological notes on clipping amphibians and reptiles. Herpeto!. Rev. five sympatric Leptodactylus(Amphibia, Leptodactyl- 23:19-21. idae) from Ecuador. Herpetologica 29:66-72. WELLS, K. D., AND K. M. BARD. 1988. Parental behavior --, R. W. McDIARMID,AND D. L. WEIGMANN.1975. of an aquatic-breeding tropical frog, Leptodactylus Tadpoles, predation and pond habitats in the trop- bolivianus.J. Herpetol. 22:361-364. ics. Biotropica 7:100-111. LESCURE,].,AND F. LETEu.IER.1983. Reproduction en (CPAP, CFBH) DEPARTAMENTO DE ZOOLOGIA, captivite de Leptodactylusfallax Muller, 1926 (Am- INS"I1TUTO DE BIOCIENCIAS, UNIVERSIDADE Es- phibia, Leptodactylidae). Rev. Fr. Aquariol. 10:61- TADUAL PAUUSTA, CAIXA POSTAL 199, 13506- 64. 900, RIo CLARO, SAO PAULO, BRAZIL; AND MAGNUSSON,W. E., AND].-M. HERO. 1991. Predation (MU) DEPARTAMENTO DE BIOLOGIAjCCBS, and the evolution of complex oviposition behaviour UNIVERSIDADE FEDERAL DE MATO GROSSO DO in Amazon rainforest frogs. Oecologia 86:310-318. SUL, CAIXA POSTAL 549, 79070-900, CAMPo MARTINS,I. A. 1996. Reproductive biology of Leptodac- GRANDE, MATO GROSSO DO SOL, BRAZIL. E- tylus podiciPinus (Cope, 1862) (Anura, Leptodactyl- idae) in the northwest region of the State of Sao mail: (CPAP) [email protected]. Send reprint Paulo. Unpubl. master's thesis, Universidade Estad- requests to CPAP. Submitted: 2 December ual Paulista, Botucatu, Sao Paulo, Brasil (In Portu- 2001. Accepted: 13 May 2002. Section editor: guese). C. Guyer.

-.2001.