Reproductive ecology and behaviour of a species of Adenomera (Anura,Leptodactylinae) with endotrophic tadpoles: Systematic implications

The species of the Leptodactylus fuscus group and those of the genus Adenomera lay their eggs in underground chambers. According to current systematic arrangement of these genera, this behaviour is convergent. Here we describe reproduction, courtship, tadpole morphology, calls, chamber structure, and populational phenology of an Adenomera species, and compare some of these features with those of other species of the genus and with species of Leptodactylus of the fuscus and pentadactylus groups. We tested the tadpoles of the Adenomera sp. and those of Leptodactylus labyrinthicus (pentadactylus group) for their foam‐making abilities. There was sexual dimorphism in size; males averaged 22.0?mm and females 24.3?mm in snout–vent length. Males called from late September to late February; calling often began about 2–3?h before sunset. Males called exclusively in open (non‐forest) areas. Egg clutches were found around male calling sites. Males excavated spherical chambers which had a direct entrance. During mating, the male led the female towards a previously excavated chamber. Territorial interactions (aggressive calls and fights) occurred when an intruder male approached a calling male. Late‐stage tadpoles and newly metamorphosed juveniles were found within underground chambers. Clutch size averaged 10.6; eggs averaged 3.7?mm in diameter and were cream coloured. Tadpoles had horny beaks, but no labial tooth; spiracle was present. All tested groups of tadpoles generated foam within 10?h. As we report for Adenomera sp., the males of Leptodactylus species of the fuscus group lead the female to a previously excavated chamber. Tadpole foam‐making behaviour was reported in Leptodactylus of the fuscus group and was previously unknown for any species of Adenomera or for Leptodactylus of the pentadactylus group. The way in which the tadpoles of Adenomera sp., Leptodactylus spp. (of the fuscus group) and L. labyrinthicus made foam was quite similar. The foam‐making behaviour of the studied tadpoles may act to avoid compaction of the tadpoles at the bottom of the basin or underground chamber, avoiding overcrowding and increasing respiratory and excretory efficiency. As presently recognized, the phylogenetic position of Adenomera suggests that reproductive major behavioural features are convergent with some Leptodactylus species. Alternatively, our data point to close phylogenetic relationships between Adenomera and Leptodactylus of the fuscus and pentadactylus groups, reinforcing the paraphyletic nature of the genus Leptodactylus.     

Metazoan endoparasites of 18 anuran species from the mesophytic semideciduous Atlantic Forest in southern Brazil

Brazil has the richest anuran biodiversity in the world and many species have not yet been studied for parasites. One hundred and forty frogs belonging to 18 species (Rhinella schneideri, Dendropsophus aff. minutus, Dendropsophus nanus, Hypsiboas albopunctatus, Hypsiboas punctatus, Hypsiboas raniceps, Phyllomedusa tetraploidea, Pseudis platensis, Scinax fuscovarius, Trachycephalus typhonius, Leptodactylus chaquensis, Leptodactylus fuscus, Leptodactylus aff. latrans, Leptodactylus mystacinus, Leptodactylus podicipinus, Physalaemus cuvieri, Physalaemus nattereri and Elachistocleis bicolor) collected in aquatic habitats in forest remnants and surrounding agricultural landscapes in southern Brazil were examined for endoparasites. Twenty-four species of endoparasites were identified among 21 adult and three larval individuals: one species of Monogenea, Polystoma lopezromani; eight species of Digenea, Catadiscus marinholutzi, Catadiscus propinquus, Choledocystus simulans, Gordoderina sp., Neohaematoloechus neivai, Rauschiella lenti, Rauschiella linguatula, Rauschiella repandum; one species of Cestoda, Ophiotaenia sp.; one species of Acanthocephala, Centrorhyncus sp.; 12 species of Nematoda, Aplectana sp., Aplectana travassosi, Cosmocerca podicipinus, Raillietnema sp., Schrankiana formolusa, Falcaustra mascula, Oxyascaris oxyascaris, Ochoterenella digiticauda, Physaloptera sp., Brevimulticecum sp., Rhabdias sp., Parapharyngodon hylidae; and one species of Annelida, Dero (Allodero) lutzi. The endoparasite fauna found is constituted by generalist species. Two new records of occurrence in Brazil and 33 new host records are reported.     

On the natural history of the South American pepper frog,Leptodactylus labyrinthicus (Spix, 1824) (Anura: Leptodactylidae)

Some species of Leptodactylus of the L. pentadactylus group lay their eggs outside water but the tadpoles need to reach water to complete the larval phase; other species complete development in terrestrial nests. Here we present details of the reproduction of L. labyrinthicus in south‐eastern Brazil. The proportion of tadpoles and trophic eggs in aged egg clutches was determined, as well as the growth of the tadpoles while in the nest. The gut contents of tadpoles that were in egg clutches of frogs were analysed. Adult males did not differ from females in size and had hypertrophied forearms and an enlarged spine on the thumb. Reproduction was initiated with the first rains of August/September and extended to mid‐January. Calling and spawning occurred at permanent or temporary water bodies. The foam nests were built in excavated basins outside of, but close to the water. The male determined the place of the basin construction; after amplexus, the female completed the excavation. The amplexus was axillary. One female spent the day after spawning in the foam. The eggs were pale grey, the yolk averaging 2.3?mm in diameter. The mean number of eggs was 2101 per egg clutch. The number of tadpoles in individual nests varied between 0.05% and 11.40% in relation to the total laid eggs. The tadpoles entered water when rains flooded the basin. The tadpoles grew to 12 times the weight of an individual egg while in the nest; no nesting tadpole was beyond stage 25. The longest time we followed tadpoles in a nest was 25 days. Tadpoles were found preying upon eggs of three other frog species and upon conspecific eggs. Males fought by grasping each other in a belly‐to‐belly position; the powerful arms and the thumb spines represent weapons. Even though males can reach maturity in the season following birth, small size would prevent them from establishing their own territory. All the species of the L. pentadactylus group may build their foam nests within excavated basins. The basins may protect the eggs and embryos from cannibalistic tadpoles and may have an anti‐desiccation effect. In order to produce trophic eggs, the female may delay laying additional unfertilized eggs until after the male has abandoned the foam nest. Anuran eggs represent an important food item for tadpoles after they leave the nest.     

On the natural history of Leptodactylus syphax with comments on the evolution of reproductive features in the L. pentadactylus species group (Anura,Leptodactylidae)

We describe the reproduction of Leptodactylus syphax from Brazil and attempt to trace the evolution of reproductive traits within the L. pentadactylus species group. We quantified the proportion of eggs/embryos from fresh nests. We test whether L. labyrinthicus and L. syphax tadpoles can prey on eggs from heterospecific foam nests. Egg clutches were found outside the water at the edges of rocky/seasonal streams, usually within excavated basins. Males beat the foam with their legs moving from side to side. Clutches do not have trophic eggs, since most of their eggs develop into tadpoles. Tadpoles cling on rocks in current/shallow waters. Only L. labyrinthicus tadpoles could prey on eggs from heterospecific foam nests. If the L. pentadactylus group is monophyletic, excavated basins and foam‐beating in lateral motions may be possible synapomorphies of this group. However, large adults, carnivorous tadpoles and trophic eggs appear to be associated synapomorphies of a less inclusive group.     

Aspects of the natural history of Leptodactylus knudseni Heyer, 1972 (Anura: Leptodactylidae) in a pristine forest in Central Amazonia,Brazil, with comments on ontogenetic variation of its tadpoles

The Leptodactylus pentadactylus species group is comprised of medium to large species of Neotropical frogs. Leptodactylus knudseni, a member of this species group, has a wide distribution throughout the Amazon Basin. Herein we describe aspects of the reproductive biology of L. knudseni and provide notes about the ontogenetic variation of its tadpoles based on a population in a non-flooded forest near Manaus, Amazonian Brazil. Amplectant pairs of L. knudseni lay foam nests in excavated basins on the edge of temporary ponds located on clay soil and at least 50 m from a stream. The tadpole development happens initially in the foam nests with access to the pond after the rain flooding the basins. Studied clutches lacked trophic eggs and tadpoles did not produce foam. Ontogenetic variations in L. knudseni tadpoles are related to size, teeth formulae and body colour. The use of excavated basins for the deposition of foam nests has been reported in several species of the L. pentadactylus group. The absence of trophic eggs and production of foam by the tadpoles differ from other species of the L. pentadactylus group. The tadpole morphology is similar to that described for other species of the group.     

First record of the genus Leptodactylus (Anura: Leptodactylidae) in Cuba: Leptodactylus fragilis,a biological invasion?

The Neotropical genus Leptodactylus is currently represented by three species in the West Indies (Leptodactylus albilabris, Leptodactylus fallax and Leptodactylus validus). Based on morphological, acoustic and molecular evidence, we document the presence of a fourth species in the Caribbean region, Leptodactylus fragilis (Brocchi, 1877). The species was found at two localities in western Cuba, and molecular data suggest a northern South American origin, possibly Venezuela, for these populations. We discuss the potential invasive status of L. fragilis, based on its known distribution, relative abundance, behaviour and possible impacts on native species of Cuban amphibians.     

Habitat,egg‐laying behaviour,eggs and tadpoles of four sympatric species of Pseudopaludicola (Anura,Leiuperidae)

In contrast to most leiuperid frogs, Pseudopaludicola falcipes does not lay eggs in foam nests; this could represent a reversion to the primitive state. We found that in four other Pseudopaludicola species, eggs were also not embedded in foam nests and had a well‐defined outermost jelly layer. The females also constantly moved or dived and males lacked vigorous “wiping/kicking” leg motions while eggs were being laid, features that make foam nesting difficult. The tadpoles of three species have two gaps in the marginal papillae along the lower labium and two posterior rows of labial teeth; the tadpoles of one species had three gaps and three rows, a pattern resembling that of some Physalaemus (Leiuperidae) species. Our data on tadpole morphology and reproductive behaviour do not allow us to rule out the paraphyletic nature of Physalaemus in relation to Pseudopaludicola but they provide some support against the “foam‐loss hypothesis” in Pseudopaludicola.     

Prolonged parental behaviour by males of Limnonectes palavanensis (Boulenger 1894), a frog with possible sex-role reversal

ABSTRACT

In sex-role-reversed systems, males carry out all parental care duties, forgoing further mating opportunities. Cases of complete sex-role reversal have not been reported in anurans. We describe the parental care behaviour of the leaf-litter frog Limnonectes palavanensis, a Bornean endemic with egg-guarding and tadpole transport, possibly the first anuran with sex-role reversal. In this study, we tested one of the predictions of the sex-role reversal hypothesis: males invest more in parental care than females do, and this prevents them from quickly acquiring additional mates. We observed egg-guarding behaviour in captivity to determine the length and intensity of parental care. Also, we describe the tadpole climbing and tadpole transport behaviour. We found that males perform all of the parental duties, remaining with the clutch until hatching. They do not call during this time, nor do they care for more than one clutch at a time. Observations of tadpole transport in the field indicate that all tadpoles in the clutch are retrieved at once. The behaviour of males during tadpole retrieval suggests that they stimulate synchronous hatching. Together, these results indicate that the male parental expenditure in this species is high, resulting in lost mating opportunities. The prolonged male-only parental care behaviour of this species satisfies an important criterion for the occurrence of sex-role reversal.     

Goliath frogs build nests for spawning – the reason for their gigantism?

ABSTRACT

In contrast to its popularity, astonishingly few facts have become known about the biology of the Goliath Frog, Conraua goliath. We herein report the so far unknown construction of nests as spawning sites by this species. On the Mpoula River, Littoral District, West Cameroon we identified 19 nests along a 400 m section. Nests could be classified into three types. Type 1 constitutes rock pools that were cleared by the frogs from detritus and leaf-litter; type 2 constitutes existing washouts at the riverbanks that were cleared from leaf-litter and/or expanded, and type 3 were depressions dug by the frogs into gravel riverbanks. The cleaning and digging activities of the frogs included removal of small to larger items, ranging from sand and leaves to larger stones. In all nest types eggs and tadpoles of C. goliath were detected. All nest types were used for egg deposition several times, and could comprise up to three distinct cohorts of tadpoles. Nests seemed to be clustered. Camera trapping revealed that nests are guarded by adult frogs at night. The breeding nests may allow the frogs to deposit their eggs away from the torrent rivers, and potential egg and tadpole predators. As nest construction, at least in some cases, requires the removal of large and heavy items, we hypothesize that this can only be achieved by decent sized frogs, possibly explaining the unique size of the species.     

Predation on eggs of Schneider’s dwarf caiman,Paleosuchus trigonatus (Schneider, 1807), by armadillos and other predators

Nests of Schneider’s dwarf caiman, Paleosuchus trigonatus, were located in the forests around three streams that drain into the Xingu River, Brazilian Amazonia, in October 2014. Camera traps were installed at the edge of four nests to document predators and female parental care. At two nests, females unsuccessfully defended their nests against one or more giant armadillos, Priodontes maximus, and nine-banded armadillos, Dasypus novemcinctus. Both armadillo species responded to the attack by fleeing and returning on the opposite side of the nest by going around the tree under which the nest was located. Giant armadillos have never before been recorded consuming caiman eggs and their diet has been described as consisting mostly of ants and termites. Another species of armadillo, Cabassous unicinctus, was also registered digging into a nest and probably consuming eggs, though it is generally considered to be primarily insectivorous. A tayra (Eira barbara), lizard (Tupinambis teguixin) and coati (Nasua nasua) were also registered taking eggs from nests during the day, but we obtained no registers of nest defence by caimans during the day. The three nests were attacked after 60 days of incubation, when the eggs were well developed.     

Home range behaviour in male and female poison frogs in Amazonian Peru (Dendrobatidae: Ranitomeya reticulata)

The poison frog Ranitomeya reticulata was studied for 3 months while mark–recapture surveys were performed. Ranitomeya species deposit terrestrial clutches and carry tadpoles to phytotelmata with few taxa performing biparental brood care including larval feeding. Home range size and spatial affinity to phytotelmata in the genus are linked to mating systems. In R. reticulata, individual home range size and overlap were similar in both sexes, indicating equal levels of site fidelity. Although territory defence was never observed, strong intrasexual intolerance within individuals' core areas was found. The large intersexual home range overlap for breeding pairs indicated that mate fidelity occurs. Individuals' home ranges were not overlapping, suggesting that R. reticulata lacks pair-bonding or strongly cooperative behaviour in parental duties. The number of ground bromeliads containing phytotelmata and home range size of males were positively correlated. Our findings suggest that females do not perform egg-feeding and male-only parental care is likely.     

‘On the rocks’: reproductive biology of the endemic toad Xanthophryne (Anura: Bufonidae) from the Western Ghats,India

Xanthophryne is a toad genus endemic to the northern Western Ghats of India, with two extant sister species – Xanthophryne koynayensis and Xanthophryne tigerina. Both species are local endemics and endangered. We studied reproductive biology of these toads and found that they are specialized to the lateritic rocky outcrops at mid-elevations in high rainfall areas. Xanthophryne toads have sporadic, multiple spawning bouts lasting 2–4 days during early monsoon. In this explosive breeding behaviour, we observed male toads to engage in ‘pelvic thrusts’, a unique and novel behaviour among anurans. Females oviposit in shallow pools in depressions of lateritic boulders where their tadpoles metamorphose. These ephemeral rocky pools have limited resources and they desiccate rapidly with a break in the rains. To mitigate the stochastic risk of desiccation and subsequent large-scale egg/tadpole mortality, females may disperse their reproductive investment spatially and temporally in multiple clutches, and tadpoles metamorphose rapidly. Here, we describe the amplexus, spawning and male advertisement call, and provide a comparative account of the life history traits of the two Xanthophryne species. These toads face numerous threats and are in need of urgent conservation action. These toads, seemingly well adapted to the isolated rocky outcrops, offer an excellent opportunity to understand endemism, mating systems, anuran ecology and behaviour.     

Reproductive biology of Scinax fuscomarginatus (Anura,Hylidae) in south‐eastern Brazil

The present study describes the reproductive biology of Scinax fuscomarginatus in a remnant of Cerrado in south‐eastern Brazil. Observations were made between September 2002 and March 2004 at Estação Ecológica de Itirapina, State of São Paulo, south‐eastern Brazil. Breeding activities occurred in lentic and temporary bodies of water during the rainy season. Scinax fuscomarginatus exhibited a prolonged breeding pattern and a lek mating system. Males were smaller than females and defended individual calling areas through acoustic and physical interactions. Resident males consistently won encounters, but did not differ in size or mass from intruder males. Satellite behaviour was observed, but no female or amplected pair interception was registered. Scinax fuscomarginatus exhibited low operational sex ratios and the general reproductive mode in which eggs are laid in the water and tadpoles are aquatic. Amplexus was axillary and the eggs were deposited at the bottom of temporary ponds. Details on oocytes, egg masses, and eggs are included.     

Breeding biology of the rapids frog Limnomedusa macroglossa (Anura: Cycloramphidae) in southern Brazil

Limnomedusa is a monotypic genus that occurs in association with rocky outcrops and stream beds. Based on observational and mark–recapture fieldwork from 2005 to 2008, we report the breeding biology of Limnomedusa macroglossa in southern Brazil. The reproductive season lasted from late August to early February. Tadpoles were recorded from early September to late February. A clear pattern of emergence/recruitment was observed in juveniles. The occurrence of reproductive activities was clearly related to the longest photoperiods, when the highest temperatures occur. Males called from rocky or concrete substrates, mostly under rocks. Amplexus was axillary and the operational sex ratio was nearly even. Spawn occurred in lentic water bodies but tadpoles also completed their development in slow‐flowing water. Although using similar habitats for reproduction, L. macroglossa reached lower levels of specialization toward terrestriality than did the cycloramphids Cycloramphus and Thoropa. We classify L. macroglossa as a breeding habitat specialist that would be threatened by river damming.     

Helminth biodiversity of Costa Rican Anurans (Amphibia: Anura)

One hundred and sixty-three frogs representing 21 species collected in Costa Rica were examined for helminths. Those found were: one species of Digenea (Mesocoelium monas), one species of Cestoda (Cylindrotaenia americana), 15 species of Nematoda, 11 species represented by gravid individuals (Aplectana hylambatis, Aplectana incerta, Aplectana itzocanensis, Capillaria recondita, Cosmocerca parva, Cosmocerca podicipinus, Falcaustra costaricae, Hedruris heyeri, Oswaldocruzia costaricensis, Oswaldocruzia nicaraguensis, Rhabdias savagei) and four species represented by larvae (Physaloptera sp., Porrocaecum sp., Spirocamallanus sp., Ascarididae gen. sp.) and three species of Acanthocephala, one species represented by gravid individuals (Anuracanthorhynchus lutzi) and two species by cystacanths (Centrorhynchidae gen. sp. and Oligacanthorhynchidae gen. sp.). Mean helminth diversity (number of helminth species) per frog species was 2.4 ± 0.3 SE, range: 1–6. Forty-nine new host records are reported. Costa Rican frogs are infected by generalist helminths, which infect other species of frogs from Central and South America.     

Spatial and temporal organization in three syntopic species of the Scinax ruber group (Anura: Hylidae) in the Atlantic rainforest,southeastern Brazil

Coexistence of anuran species might lead to acoustic interference among communications, especially where species are closely related. This problem might be minimized through resource partitioning. To test this idea, we analysed calling with respect to temporal and physical space usage in three syntopic, closely related species (Scinax cuspidatus, Scinax aff. hayii and Scinax aff. x-signatus) in a temporary pond in the Atlantic rainforest. The chorus attendance of each species resulted from a different combination of factors in the rainy season. Although there was some temporal overlap of daily activity among species, peak activity time differed, particularly between the two species whose calls were most similar. Although all three species tend to aggregate in open microhabitats, their coexistence is apparently facilitated by differential use of vertical strata and organization of calling sites near the sites of conspecifics. Together, these factors apparently reduce acoustic interference among heterospecific calls.