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.     

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.     

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.     

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.     

The strangest tadpole: the oophagous,tree-hole dwelling tadpole of Rhacophorus vampyrus (Anura: Rhacophoridae) from Vietnam

The tadpole of the vampire flying frog Rhacophorus vampyrus from Vietnam is one of the strangest tadpoles known. These tadpoles develop from non-pigmented eggs suspended in a foam nest placed on the wall of a tree hole. The elongate, depressed body resembles that of some phytotelmon-breeding frogs, but the mouthparts bear little resemblance to any other tadpole: upper labium reduced to one large papilla-like structure on each side, upper jaw sheath with a few huge, widely spaced, hook-shaped serrations that face backwards into the buccal cavity, lower jaw sheath absent, sinistral spiracle visible only ventrally, and two large, forward facing, keratinized hooks accompanied laterally by two similar sized fleshy papillae on the margin of the reduced lower labium. All evidence suggests that the tadpoles are oophagous and that the mother returns to deposit trophic eggs.     

Asymmetric larval competition between two species of neotropical foam‐nesting frogs: Leptodactylus fuscus and Engystomops pustulosus

Larval competition was investigated in foam‐nesting frogs with contrasting breeding strategies. Leptodactylus fuscus nests in burrows with moderate numbers of large eggs, mainly on dry nights; Engystomops pustulosus makes floating nests with large numbers of small eggs, mainly on wet nights. Both use the same temporary pools in open habitat over an extended breeding season. Larval growth to metamorphosis was assessed in a semi‐natural experiment and in the laboratory. Tanks contained either single species or equal numbers of both species. Inter‐specific competition was asymmetric; L. fuscus survived as well as or better in competition with E. pustulosus than in intra‐specific competition. Leptodactylus fuscus attained larger sizes with E. pustulosus present. In interspecific competition E. pustulosus showed worse survival and grew slower and to a smaller size. Outdoors, both species tolerated water temperatures that often rose to 42°C and reached metamorphosis in very short times: 14 days after oviposition in L. fuscus and 17 days in E. pustulosus.     

Reproductive aspects of Leptodactytus hylaedactylus (Anura: Leptodactylidae), a member of the Leptodactylus marmoratus species group,with a description of tadpoles and calls

In this paper we describe some aspects of the reproductive biology of Leptodactylus hylaedactylus from open areas of Central Amazonia, Brazil. We describe the calling site, reproductive season, daily pattern of calling activity, chamber structure, vocalizations and tadpole morphology. Males of Leptodactylus hylaedactylus called amidst grasses and bushes in open and urban areas, throughout the year, and a greater number of males were heard in the period from 16:00 to 20:00 h. The eggs are deposited in underground chambers, which are spherical or elliptical. Larval development occurs inside the chambers. Two types of vocalizations were detected, the advertisement and the territorial call. The advertisement call of the species studied herein differs from other calls described for L. hylaedactylus from other localities of Brazil, but is very similar to that described from Peru. Tadpole morphology is similar to that described from individuals in French Guiana.     

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.     

Reproduction,phenology and mortality sources of a species of Physalaemus (Anura: Leptodactylidae)

Physalaemus cf. fuscomaculatus is a foam-nesting frog of seasonally dry environments of south-eastern Brazil. We report on the reproduction and other natural history features of this species. Population parameters were based on trapped specimens. The advertisement call is described. The calling and spawning season is coincident with the rainy period. Calling and spawning were performed in ponds. Most of the adults were trapped in October and the juveniles during wetter months and the beginning of the dry season. At the end of the reproductive season, the median size of adults lowered. Egg clutches averaged 2350 eggs, each egg being about 1.4?mm in diameter. Males were more abundant than females in traps. Communal foam nests were frequent, involving up to 40 individual nests. Tadpoles entered the water within about 40?h. Maggots (Diptera) infested egg clutches; water bugs and mammals preyed upon adults. In this region, the dry/cold season may be so difficult for survival that early maturation at small size would be advantageous. The male-biased sample may be related to the greater motility of males. The rapid abandonment of the foam by the tadpoles and communal nesting may help to reduce predation by maggots. Skin toxins were not effective in deterring predation upon adults. The call of P. cf. fuscomaculatus differs from that of other species in the biligonigerus group and can help to define the specific status of the studied population.     

Reproductive features of three maternal-caring species of Leptodactylus (Anura: Leptodactylidae) with a report on alloparental care in frogs

We describe aspects of the reproduction of three shoaling/maternal-caring Leptodactylus species (Leptodactylus aff. latrans, Leptodactylus podicipinus and Leptodactylus aff. leptodactyloides), pointing to the relevance of the female to tadpoles and describe a case of alloparental care in frogs. Females of the three species connected water bodies by digging channels to their tadpoles. Leptodactylus aff. latrans females often expelled predatory snakes and conspecific males that approached shoals to prey upon tadpoles. In water bodies containing predatory teleosts, tadpoles of L. aff. latrans only reached metamorphosis in the presence of guardian females. Channel digging can provide tadpoles with access to new feeding grounds and prevent predation and desiccation. We found brood mixing and alloparental care between L. aff. latrans and L. podicipinus which, as in some Teleostei, may be regarded as the result of identification mistakes.     

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.     

Camera traps capture images of predators of Caiman crocodilus yacare eggs (Reptilia: Crocodylia) in Brazil’s Pantanal wetlands

Camera traps were set up in forest nests in 2009, 2010 and 2012 to capture images of possible predators eating eggs of the Pantanal caiman, Caiman crocodilus yacare. We monitored 57 caiman nests; 42 nests were opened and the eggs were counted (mean = 25 eggs/nest, SD = 4.3). Females were present and captured at 38 of those nests. The remaining 15 nests were used as controls, and we did not capture the females or open the egg cavities of these nests. Most of the nests had the eggs eaten by predators, in both the disturbed group (38 nests) and the control group (13 nests). The main predators were carnivorous mammals, such as crab-eating foxes (Cerdocyon thous), coatis (Nasua nasua) and tayras (Eira barbara), although feral pigs (Sus scrofa) and armadillos (Dasypus novemcinctus) were also photographed eating caiman eggs. The lizard Salvator merianae was photographed eating eggs of two nests.     

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.     

Breeding biology of Phyllomedusa azurea Cope, 1862 and P. sauvagii Boulenger, 1882 (Anura) from the Cerrado,Central Brazil

Phyllomedusa azurea and P. sauvagii are treefrogs from seasonal dry environments of Central Brazil. We report on reproductive and other natural history features of these species. The study was carried out in Serra da Bodoquena, Mato Grosso do Sul, Brazil. The reproductive period was determined by the presence of vocalizing males, amplectant pair or presence of tadpoles. The reproductive effort was measured as the ratio of gonad mass in relation to body mass (BM). The reproduction of both species was correlated with the rainy season. Female P. sauvagii produced more eggs and their eggs were larger than those of P. azurea. Both species showed sexual dimorphism in relation to the snout–vent length (SVL) and BM. The mating behaviour of both species was similar. Males in both species showed similar reproductive efforts, but females of P. azurea invested more in gonads compared to the males of P. sauvagii. Phyllomedusa azurea showed a significant relation between SVL versus number of the mature eggs (NME), and P. sauvagii between SVL versus NME and BM versus ovarian mass.     

Tadpole deposition behaviour in male stream frogs Mannophryne trinitatis (Anura: Dendrobatidae)

Male Mannophryne trinitatis transport their larvae on their backs to predator‐free pools and deposit them there. The experiments reported here investigated M. trinitatis male deposition behaviour in containers placed near a heavily fish‐populated stream at Mount Saint Benedict, northern Trinidad. Choice of deposition site was not related to height above or distance from the stream. The low mean number of tadpoles deposited in each container in the field and in a laboratory experiment indicated that most males tended not to deposit complete clutches in single pools. Deposition experiments in the laboratory with a choice of different‐sized containers showed that deposition was pool size dependent, with more tadpoles deposited in larger containers. Deposition behaviour when given a choice of containers with leaf litter (a source of food and shelter) and with no leaf litter showed no significant preference. Tadpoles grown in different water volumes with different food sources revealed that tadpole growth was best in larger water volumes containing leaf litter. Regular tadpole inspections at a pool in the field established that most tadpoles present were the result of downstream movement.     

Asynchronous reproduction in three species of crocodilians in south-eastern Amazonia

We studied reproduction of three species of crocodilians, Paleosuchus trigonatus, Caiman crocodilus and Melanosuchus niger, in the Xingu River, near the Belo Monte hydroelectric dam. The periods of laying and hatching of eggs were estimated for each nest before (2013–2014) and after (2016–2017) the river was dammed and the reservoir was formed. Nesting of the three species occurred between August and December, but was largely asynchronous; nest construction peaked in September for P. trigonatus, October for M. niger and November for C. crocodilus. Reservoir filling had little effect on the laying period of any of the species. Nests of P. trigonatus and M. niger were always within 0–12 m of the bank, whereas nests of C. crocodilus, which nests later in the season when flooding is more likely, were up to 100 m from the nearest water body. There was no relationship between distance from water and the number of eggs in nests, suggesting that larger and presumably more experienced females do not lay at different distances from the bank in any of the species.     

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.