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 Leptodactylus provides an example among anurans in which there is anevident tendency toward terrestrial reproduction. Herein we describe a new repro-ductive mode for the frog Leptodactylus podicipinus, a member of the "melanonotus"group. This new reproductive mode represents one of the intermediate steps fromthe most aquatic to the most terrestrial modes reported in the genus. Three repro-ductive modes were previously recognized for the genus Leptodactylus. However,based on our data, and on several studies on Leptodactylus species that have beenpublished since the last reviews, we propose a new classification, with the additionof two modes for the genus.

are

demonstrated by species of the "fuscus" and"marmaratus" groups. Heyer (1974) placed the"marmaratus" species group in the genus Aden-omera. Species in the "fuscus" group have foamnests that are placed on land in subterraneanchambers constructed by males; exotrophic lar-vae in advanced stages are released throughfloods or rain into lentic or lotic water bodies.Frogs in the genus Adenomera also deposit foamnests in subterranean chambers, and in mostspecies, tadpoles develop inside these chambersand are endotrophic, that is, entire develop-mental energy is obtained from vitellogenic yolk(Heyer; I969J. More recemly.. DeJa R;.a (1~95}described another reproductive mode for thegenus Adenomera, which corresponds to thesame reproductive mode of the L. fuscus group.

In the present paper, we report a new repro-ductive mode in a leptodactylid frog, Leptodac-tylus podiciPinus, a member of the "melanonotus"group, in the Pantanal, southwestern Brazil.Based in this new reproductive mode, and ondata published after Heyer's (1969) review, weupdate the reproductive modes exhibited by thespecies of Leptodactylus and propose a new clas-sification of modes for the genus.

T HE concept of reproductive mode in am-phibians was defined by Salthe (1969) and

Sallie and Duellman (1973) as being a combi-nation of traits that includes oviposition site,ovum and clutch characteristics, rate and dura-tion of development, stage and size of hatch-ling, and type of parental care, if any. For an-urans, Duellman (1985) and Duellman andTrueb (1986) recognized 29 modes of repro-duction, although in recent studies on ecologyand natural history new reproductive modeshave been described (e.g., Haddad and Hodl,1997; Haddad and Pombaljr., 1998; Haddadand Sawaya, 2000). Amphibians exhibit a greatdiversity of reproductive modes, especially inthe New World tropics, including a clear trendtoward terrestriality (Duellman, 1985), that is,reproduction becoming gradually independentof water bodies.

Members of the family Leptodactylidae exhib--it several reproductive modes ranging fromaquatic to terrestrial breeding, with many inter-mediate forms depositing eggs embedded infoam nests (Heyer, 1969). Species of Leptodacty-ius and of the related genus Adenomera are anexample in which a tendency toward terrestri-ality is evident (Heyer, 1969; Duellman, 1985).Heyer (1969) proposed that Leptodactylus spe-cies belonging to the "ocellatus" and "melanon-otus" groups have the most primitive reproduc-tive modes. Species of both groups deposit eggsin foam nests on top of the water and tadpolesare exotrophic, feeding and developing in wa-ter. According to Heyer's (1969) review, speciesin the "pentadactylus" group show the first stepto a more terrestrial life (Heyer, 1969), withfoam nests deposited in depressions or burrowsat the edges or close to water and producingexotrophic tadpoles. More specialized modes

MATERIALS AND METHODS

The study was conducted in the southern Pan-tanal, municipality of Corumba, State of MatoGrosso do SuI, southwestern Brazil (19°34'S,5TOO'W). The Pantanal is a floodplain, with anarea of approximately 140,000 km2 and an ele-vation between 75 and 200 m above sea level,delimited mostly by the Paraguay river in thewest and Brazilian uplands in the east (see Por,1995). The region is characterized by a seasonalclimate ("Aw" type in Koppen's classification),with a rainy summer from October to April and

@ 2002 by the American Society of Ichthyologist, and Herpetologists

PRADO ET Ai .REPRODUCTIVE MODE IN LEPTODACTYLUS

1129

a dry winter from May to September. Annualfloods occur in the Pantanal, and at the studysite, 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, galleryforests, and grassland fields.

Observations on Leptodactylus podiciPinus weremade at ponds and flooded areas near the Basede Estudos do PantanalfUniversidade Federalde Mato Grosso do SuI (57°00'W, 19°34'S). Datareported here were collected between January1998 and March 1999, and from January toApril 2001. Diameter and depth of the depres-sions where males called were measured with ameasuring tape to the nearest 0.1 cm. Callingmales were captured and toe clipped accordingto Waichman (1992) between 23 March and 08April 2001. Snout-vent length (SVL) was mea-sured in the field to the nearest 0.1 mm with acaliper. Then, individuals were released at theircapture point. Calling sites were also marked.Clutches were collected and immediately pre-served in 10% formalin; number of eggs perclutch was determined and egg diameter mea-sured with an ocular micrometer in a Zeiss ste-reomicroscope (:t 0.1 mm). The terminologyused to describe larval nourishment follows Thi-baudeau and Altig (1999).

RESULTS

Basin description.-Basins of L. podiciPinus wereobserved at the edges of permanent ponds andflooded areas, among grass clumps or aquaticplants. Each depression was approximately cir-cular, with a mean diameter of 61.0 mm :!: 4.5SD (range = 50-70, n = 16). Water inside thedepressions, which permeated from the adja-cent water bodies, averaged 31.0 mm :!: 4.5 SDof depth (range = 24-40, n = 16). In general,males called from the interior of the basins withtheir bodies partially submerged (Fig. 1). Call-ing males were difficult to see because basinswere well covered by the marginal vegetation,fallen leaves or dead vegetation, which func-tioned as a roof. In 24 basins that we observed,all were covered by vegetation and males calledbeside

the basin in two cases; the remaining 22males were inside the depressions. Mean dis-tance to the nearest occupied basin was 2.5 m:!: 2.1 SD (range = 0.6-8.4, n = 12). As waterlevel decreased, new nests were constructed fol-lowing the water line at the edges of the waterbodies, and the older ones were abandoned.

Fig. 1. (A) Dorsal and (B) lateral views of a maleof Leptodactylus podiciPinus calling inside an excavatedbasin (Corumba, Mato Grosso do Sui, South Pantanal,Brazil). (B) Note that leaves function as a roof for thebasin.. Drawn from photographs.

sured. Five marked males were recaptured fromone to three times on successive nights duringa 15-day study period. Mean SVL of recapturedmales (33.8 mm :!: 0.8 SD, range = 32.7-34.5,n = 5) was larger (t = 4.41, P = 0.001) thanthose that were not recaptured (31.0 mm :!: 1.0SD, range = 30.0-32.4, n = 4). Two males wererecaptured three times at the same sites, al-

Behavior of males.-Nine vocalizing males thatwere inside their basins were marked and mea-

1130 COPEIA, 2002, NO.4

though they had moved to new basins near theoriginal ones as the water level decreased. Twoother males were recaptured; one of them,marked on 29 March 2001, was recaptured sixdays later calling in a new basin 4.5 m from theoriginal site, and the second male was recap-tured six days later approximately 10 m fromthe original site. One male was recaptured twiceinside the same basin. Three other males cap-tured calling inside their depressions weremarked at night in March 1999. These maleswere

recaptured resting inside the depressionsthe next morning.

Clutches and female parental care.-Foam nests ofL. podiciPinuswere observed inside basins inJan-uary 1998, September 1998, and January 1999.The eggs were pigmented, with a mean diame-ter of 1.1 mm :!: 0.05 SD (range = 1.0-1.2, n =21 eggs from two clutches), and mean numberof eggs per clutch was 2102.5 :!: 442.1 SD (range= 1750-2953, n = 6 clutches). The foam nestswere covered by dead vegetation and mean wa-ter depth inside the basins was 26.3 mm :!: 3.2SD (range = 24-30, n = 3). Oviposition wasobserved once inside a basin covered by aquaticvegetation in April 2001.

Females of L. podicipinus attending tadpoleswere observed (n = 14), generally, in the mar-gin of ponds or flooded areas, where waterdepth was about 5 cm. Females remained closeto the tadpole schools. When tadpoles were dis-turbed, almost all females were aggressive, es-pecially those with hatchlings, jumping andknocking with their heads against observers'hands. They also performed pumping move-ments (sensu Wells and Bard, 1988), after whichthey usually dived and emerged at short dis-tances, being followed by the tadpoles. Femaleswere observed attending tadpoles at differentdevelopmental stages. For six foam nests ex-amined, we did not observe females attendingthe eggs, although we suggest that they do be-cause females attended tadpoles.

DISCUSSION

Reproductive mode in Leptodactylus podicipinus.-Leptodactylus podiciPinus occurs in open forma-tions of P~raguay, Argentina, and Bolivia, andthe Amazon basin, central Brazil through thesoutheast and south of that country (Heyer,1994). The reproductive biology of this species,like that of many tropical species, is poorlyknown (Vizotto, 1967; Rossa-Feres and Jim,1994). Recent studies report the existence of fe-male parental care of eggs and tadpoles (Pradoet al., 2000; Martins, 2001), but the exact de-

scription of calling and oviposition sites arelacking. An exception is a study conducted byMartins (1996) in which he reported the occur-rence of males of L. podiciPinus calling from ba-sins at the edges of water bodies in the State ofSao Paulo, Brazil. We observed the same situa-tion for this species in the Pantanal.

We did not observe the construction of thebasins, but Martins (1996) observed males con-structing basins with their snouts and suggestedthat males could use either natural or construct-ed depressions. Female parental care of tad-poles was observed at our study site, but wefailed

to observe females attending eggs. Nev-ertheless, Martins (1996, 2001) observed fe-males attending eggs and tadpoles. Based onthis information, our observations on the be-havior of males, and the uniform dimensions ofthe depressions we have measured, we considerthat L. podiciPinus exhibits a new reproductivemode, which can be summarized as follows: pig-mented eggs and early larval stages in foamnests, which are deposited in water-filled basinsconstructed by the males adjacent to water; ex-otrophic tadpoles in ponds; females performparental care, attending eggs and tadpoles.

Among the reproductive modes exhibited byanurans, the generalized mode of aquatic eggsand tadpoles is considered to be primitive(Duellman, 1985). The evolution of specializedmodes, with eggs deposited in protected sites orout of water, have been considered to be adap-tations against aquatic predators (Magnussonand Hero, 1991; Haddad and Sawaya, 2000).The

reproductive mode of L. podicipinus couldhave evolved in response to predation pressureon eggs, embryos, and even adults (e.g., callingmales, amplexed pairs during oviposition, andfemales

attending eggs). Although females of L.podiciPinus attend nests and tadpoles until meta-

morphosis (Prado et al., 2000; Martins, 2001;present study), the deposition of foam nests in-side vegetation-covered basins may provide ad-ditional protection for the eggs and embryos.Adult males were observed inside leaf-coveredbasins during the day. Visual predators, likewading

birds, were observed preying upon oth-er anuran species (Leptodactylus chaquensis andPseudis paradoxa) during the day at the study site(CPAP, pers. obs.). It seems that the basinscould also function as shelter sites for L. podi-cipinus males, avoiding or diminishing preda-tion risk.

Studies on other species of the "melanonotus"group show no evidence of basin constructionby males (e.g., L. teptodactyloides: Heyer and Bel-lin, 1973, reported as L. wagneri; either L. tepto-dactyloides or L. wagneri: Duellman, 1978; L. val-

PRADO ET AL.-REPRODUCTIVE MODE IN LEPTODACTYLUS

131~

"-

",'~~,'

Fig. 2. Schematic representation of sequentialsteps of the reproductive modes in the genus Lepta-dactylus, from the most aquatic to the most terrestrial.(1) Eggs in foam nest on top of water; tadpoles inlentic water, (2) eggs in foam nest in depressions closeto water; tadpoles in lentic water, (3) eggs in foamnest in water-filled basins excavated by males; tadpolesin lentic water, (4) eggs in foam nest in subterraneanchambers constructed by males; tadpoles in lentic wa-ter, (5) eggs in foam nest in burrows; larval develop-ment in the foam nest inside the burrows. New stepsproposed for the genus Leptodactylus since Heyer(1969) are (3) and (5).

idus: Downie, 1996). Nevertheless, Downie(1996) pointed out that clutches of L. validus inTrinidad were always found at the edges ofsmall ponds, usually well covered by dead veg-etation. It is possible that the reproductivemode described here for L. podiciPinus occursin other species of the "melanonotus" group, butmore detailed studies on their reproductive be-havior are necessary.

Female parental care of eggs and tadpoles inspecies of the "ocellatus" and "melanonotus"groups (e.g., Wells and Bard, 1988; Prado et al.,2000; Martins, 2001) reinforces Heyer's (1969)proposition that members of both groups are themost closely related of the four Leptodactylusgroups he identified. However, the reproductivemode of L. podiciPinus, a member of the "melan-onotus" group, represents a specialization possi-bly derived from the primitive mode present inspecies of the "ocellatus" group and some speciesof the "melanonotus" group, representing onestep toward terrestrial reproduction in the genus.

Reproductive modes in the genus Leptodactylus.-Heyer (1969) proposed four reproductive stagesfor the species groups of the genus Leptodactylus,including the species of Adenomera. Several stud-ies on Leptodactylus species have been publishedsince, resulting in new information regardingtheir reproductive biology (e.g., Rodriguez andDuellman, 1994; Davis et al., 2000; Eterovickand Sazima, 2000). An interesting group con-cerning reproduction within the genus Lepta-dactylus is the "pentadactylus" group, which hasat least two reproductive modes. The first modeis the deposition of foam nests in water-filleddepressions at the edges of water bodies; sub-sequent to flooding, exotrophic tadpoles devel-op in water (e.g., L. knudseni: Hero and Galatti,1990; Rodriguez and Duellman, 1994; L. labyrin-thicus: Agostinho, 1994; CFBH, pers. obs.).Whether these depressions are natural or con-structed remains unclear. The ultimate special-ization in the "pentadactylus" group is the totalterrestrial reproductive mode described for L.fallax (Davis et al., 2000). In this species foamnests are placed in burrows in the ground, andtadpoles develop inside the nests, but some de-tails on reproduction and larval developmentneed to be clarified. Also in this species it is notclear whether the cavities used are natural orconstructed (Davis et al., 2000). Although Les-cure and Letellier (1983) reported that tadpolesof L. fallax develop to metamorphosis inside thenest by metabolizing vitelline reserves, Davis etal. (2000) described tadpoles without yolk sacs.If tadpoles develop only on their yolk, this re-productive mode could be considered compa-

rable to the mode described for some speciesof Adenomera (Heyer, 1969; De la Riva, 1995).

Leptodactylus pentadactylus apparently has tworeproductive modes: (1) deposition of foamnests in open depressions ("potholes"); subse-quent to flooding, exotrophic tadpoles developin water (Breder, 1946), as in other species ofthe group mentioned above; (2) a reproductivemode similar to that described for L. fallax(Hero and Galatti, 1990; Rodriguez and Duell-man, 1994), that is, a foam nest inside burrowsin the ground and development of larvae insidethe nest. Muedeking and Heyer (1976) ob-served nests of L. pentadactylus in Panama de-posited in apparently excavated potholes, andat a distance from water bodies. These authorsalso registered the coexistence of larvae andeggs in the same nests, and noted that some ofthe larvae had yolk-colored guts, which was in-terpreted to indicate ingestion of eggs by thelarvae. As suggested by Muedeking and Heyer(1976), possibly the normal pattern for L. pen-tadactylus is the release of tadpoles in waterthrough floods of potholes, as observed byBreder (1946). Nevertheless, in unfavorableconditions of rain, larvae could remain in thenest feeding on eggs up to metamorphosis(Muedeking and Heyer, 1976). The latter situ-ation was observed by Hero and Galatti (1990)in Central Amazonia, although they did notmention how larvae were nourished. It is pos-sible that the alternative modes present in L.pentadactylus

are partially associated with feed-ing diversity exhibited by the larvae, which canfeed on algae, foam (Vinton, 1951), other tad-poles (Heyer et aI., 1975), and eggs (Muedekingand Heyer, 1976). Also, the presence of a foam

1132 COPEIA, 2002, NO.4

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

Reproductive mode Examples

Species of the L. oceUatus (e.g., L. bolivianus, L. cha-quensis, L. ocellatus) and L. melanonotus groups(e.g., L. leptodactyloides, L. validus).

Some species of the L. pentadactylus group (e.g., L.knudseni, L. laiJyrinthicus, L. pentadactylus).

One species of the L. melanonotus group (L. podicipi-nus).

L. fuscus group (e.g.. L. cunicularius, L. elenae, L. fur-narius, L. fuscus, L. jolyi, L. mystaceus, L. notoakti-its).

1. Eggs and early larval stages in foam nest ontop of the water; exotrophic tadpoles inlentic water.

2. Eggs and early larval stages in foam nest inwater-filled depressions close to water; sub-sequent to flooding, exotrophic tadpoles inlentic water.

3. Eggs and early larval stages in foam nest inwater-filled basins constructed by males;exotrophic tadpoles in lentic water.

4. Eggs and early larval stages in foam nest insubterranean chambers constructed bymales; subsequent to flooding, exotrophictadpoles in lentic or lotic water.

5. Eggs in foam nest in burrows, either close orfar from water; larval development in thefoam nest inside the burrows".

Some species of dIe L. pentadactylus group (e.g., L.fallax, L. pentadactylus).

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

ACKNOWLEDGMENTS

We thank M. A. Donnelly, R. P. Bastos, andW. R. Heyer for critically reading the manu-

script and for the valuable suggestions thathelped us to improve the text,J. R. Somera forthe drawing, and E. A. Pedroso, E. Pereira, E.Q. Gomes, and P. Landgref Filho for field assis-tance. This study was made possible by the lo-gistical support of Base de Estudos do Pantanal/Universidade Federal de Mato Grosso do SuI. C.P. A. Prado and M. Uetanabaro acknowledgeCNPq for financial support (proc. 521746/97-3/NV). C. P. A. Prado acknowledges CNPq fora graduate fellowship (procs. 351228/97-7,140397/2000-0). C. F. B. Haddad acknowledgesCNPq and FAPESP for financial support.

nest provides protection from desiccation totadpoles, as previously mentioned by Heyer(1969). Alternatively, the occurrence of thesedifferent reproductive modes could indicate theexistence of more than one species (W. R. Hey-er, pers. comm.).

Oophagous tadpoles are also known for otherspecies of the "pentadactylus" group. Tadpolesof L. knudseni feed on conspecific eggs placedlater in the same pond (CFBH, pers. obs.).Agostinho (1994) verified that a mean of 90%of eggs present in foam nests of L. labynnthicuswere not fertilized and were consumed by thetadpoles, which could survive in the nest for al-most 30 days before being carried to water byrain. Female deposition of eggs that are not fer-tilized, but instead, supply nourishment for tad-poles can occur in other species of the "penta-dactylus" group and could explain larval nutri-tion in L. fallax.

The reproductive mode of L. podiciPinus isone of the transitional steps from aquatic to ter-restrial breeding within the genus (Fig. 2). Inthis case, males construct water-filled basins atthe edges of ponds, which are covered by leavesor dead vegetation. Exotrophic tadpoles hatchin these nests and develop in water. In Table 1,we summarized the reproductive modes knownfor the genus Leptodactylus. Analysis of all avail-able information reveals that the pathway to ter-restrial reproduction in the genus Leptodactylusis complex, with many intermediate steps, sim-ilar to the one described in our study, remain-ing to be discovered.

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(CPAP, CFBH) DEPARTAMENTO DE ZOOLOGIA,

INS"I1TUTO DE BIOCIENCIAS, UNIVERSIDADE Es-

TADUAL PAUUSTA, CAIXA POSTAL 199, 13506-

900, RIo CLARO, SAO PAULO, BRAZIL; AND

(MU) DEPARTAMENTO DE BIOLOGIAjCCBS,

UNIVERSIDADE FEDERAL DE MATO GROSSO DO

SUL, CAIXA POSTAL 549, 79070-900, CAMPo

GRANDE, MATO GROSSO DO SOL, BRAZIL. E-

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