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.     

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.     

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.     

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.     

‘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.     

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.     

Reproductive ecology of the glass frog Espadarana prosoblepon (Anura: Centrolenidae) in an urban forest of the Central Andes of Colombia

Population and reproductive behaviour aspects of the glass frog Espadarana prosoblepon are well known for populations from Central America, but similar information is lacking for populations from South America. We recorded the reproductive ecology of a population of the glass frog E. prosoblepon in the city of Armenia, Central Andes of Colombia. With weekly surveys with mark-recapture between December 2013 and November 2015, we monitored activity patterns and evaluated if the probability of males mating is associated to their body size or to chorus tenure (i.e. the number of nights a same individual is calling for attracting a mate). In addition, upon observing an amplexus, we recorded the behaviour of the individuals until oviposition and noted characteristics of egg clutch. We recorded 47 males and 32 females, nine amplexus events, eight ovipositions, and 21 egg clutches (35.4 ± 4.79 eggs per clutch, N = 29). Activity of males and females and the number of egg clutches were positively correlated to rainfall. Mating success of males was not associated to their body size, but it was positively associated to longer chorus tenure; clutches from large females had a higher number of eggs than clutches from small females. Oviposition occurred on average 3.76 ± 1.74 hours after we first observed the amplexus, occurring 93.1% of the time in fronds of Selaginella geniculata at an average height of 1.58 ± 0.44 m. After the oviposition, the male left the site, while the female remained between 30 and 45 min, partially covering the eggs. The reproductive behaviour of E. prosoblepon did not vary widely between a population in Costa Rica and our population in time to oviposition, and mating success of males associated to chorus tenure; however, in our study population we recorded a larger clutch size and the preference for S. geniculata fronds as oviposition substrate.     

Natural history of the Lined Seedeater Sporophila lineola (Aves: Thraupidae) in southeastern Brazil

The Lined Seedeater (Sporophila lineola) is a migratory species that inhabits a variety of open habitats in South America. We studied the breeding biology and territorial behaviour of a colour-banded population of the species in the Universidade Federal de Viçosa, Campus Florestal (1–19,8808ºS, –44,4136ºW), during two breeding seasons (2014/2015 and 2015/2016), which spans from December to April. We monitored 74 nests of this species. The nest is a low cup supported between a fork. Nests are mainly built with grass stems and rootlets, with spider-web used to hold the material together and to bind the nest to its supporting plant. Females are solely responsible for nest building and incubation, which is synchronic, and also for feeding nestlings to a large extent. Males are responsible for defending the territory, which corresponds to a small portion of the home range restricted to the nest environs, and also feed the nestlings. Mean clutch size is two eggs (78% of nests monitored), with clutches of three (20.3%) and four (1.7%) eggs also observed. Eggs are whitish, covered with dark brown blotches and spots to a variable extent. Mean incubation period, considered as the period between the onset of incubation and hatching of the first egg, is 11 days. Nestling period, considered as the period between hatching of the first egg and fledging of the last young, is 10 days. During the first breeding season, the simple percentage of successful nests was 34.1%, while the Mayfield success was 29.8%, with slightly higher values observed during the second breeding season, with 39.4% and 35.7%, respectively. We recorded, for the first time, three cases of polygamy in the species. We also recorded breeding site fidelity for the first time in the species, with males returning to the same territory owned in a previous breeding season.     

On the life-habits and developmental stages of Nidomyia cana Papp (Diptera,Borboropsidae)

Eggs, second and third instar larvae of the enigmatic species Nidomyia cana, which was discovered most recently from the nests of raptorial birds in southern Hungary, are described. Both egg and larvae show peculiarities among the so-called heleomyzoid flies. Larvae were found in wet vegetable material (mostly pieces of poplar bark) of a buzzard nest and their shape is of a saprophagous type. Females are macro-oviparous, with a maximum of 15 to 17 eggs laid in one batch. Adults live mostly on the surface the of the nest, they copulate there, and they find shelter in the nest itself. No direct contact with adults or nestlings within the nest was observed. It is suggested that overwintering occurs as pupae (pharate adults) underground, beneath the nest. However, if N. cana lives exclusively in the nests of raptors, adults would have difficulties in finding a new nest, and it is probable that they are transferred to new nests attached to the birds.     

Reproductive behaviour of the glass frog Hyalinobatrachium cappellei (Anura: Centrolenidae) in the Southern Amazon

Frog species of the Centrolenidae family exhibit a high variation in reproductive behaviours. Herein we describe the reproductive, ecological, acoustic and behavioural features of Hyalinobatrachium cappellei in Southern Amazon. Two hypotheses were also evaluated: (1) are ecological characteristics of the reproductive site related to male size and quantity of eggs and clutches? And (2) do males with one or more existing clutches at reproductive sites accumulate more new clutches than those males initially without them? This study was conducted at two streams, with sampling at 1 km each in Southern Amazon. Species reproduction occurred during the wet season and was considered prolonged breeding. Although male vocalization occurred on both the upper and underside of leaves, clutches were most often deposited on the underside of leaves. Males emitted a courtship call upon female approach. The process of female approach until oviposition lasted approximately eight hours. After oviposition, females left the breeding site while males remained near the clutch, covering it with the belly in ventral brooding behaviour. Thus, egg attendance is reported for the first time for this species. No intraspecific or interspecific aggressive behaviour was recorded. There was no relationship between habitat characteristics of the reproductive sites and male size, number of eggs and clutches. However, after 10 days of monitoring, we found evidences that parental males had a higher number of clutches than those males initially without clutches. Similar to other glass frog species, the behavioural characteristics of H. cappellei make this species an excellent model to use in evaluating the cost-effectiveness of parental care and the importance of egg attendance for offspring survival. Therefore, these data contribute towards a better understanding of the complex phylogenetic and biogeographic relationships between centrolenid lineages.     

Structural comparisons of isomorphic breeding nests between closely allied spiders Cheiracanthium japonicum and Cheiracanthium lascivum (Araneae: Eutichuridae)

Closely allied spider species Cheiracanthium japonicum and Cheiracanthium lascivum make a closed breeding nest for egg laying and parental care. The nest provides the internal climatic stability required for suitable development of eggs and the physical durability required for protection against intruders. Although the breeding nests of these two spiders are quite similar in structure and appearance, their climatic stability and physical durability seem to be empirically different. Such physical features of the nests of these two spiders were compared based on a balance between the inner and outer air temperature and humidity of the nest as well as on the amount and size of spider silks lining the nest. In addition, the female’s relative energy allocation to egg production versus nest construction was examined based on the number or weight of eggs versus the climatic stability and physical durability of the nest. According to the results, the stability of temperature and humidity was maintained better in the breeding nest of C. japonicum than in that of C. lascivum. Furthermore, the nest of C. japonicum was more strongly constructed, with a greater volume and size of silks, than that of C. lascivum. On the other hand, the number or weight of eggs in relation to the female’s body weight in C. japonicum was smaller than that in C. lascivum. These results suggested that the reproductive effort towards nest construction for the purpose of egg and juvenile care in C. japonicum was larger than that in C. lascivum. In contrast, the effort towards egg production in C. japonicum was smaller than that in C. lascivum. Consequently, it is likely that the structural differences in breeding nests between these two spiders are responsible for the discrepancies in the female’s relative energy allocation to nest construction.     

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.     

Oviposition site preference and reproductive ecology of Teratohyla midas (Anura: Centrolenidae) in the Colombian Amazon

ABSTRACT

The family Centrolenidae (Glass frogs) includes 157 species of anurans with a Neotropical distribution. Although glass frogs have been the subject of several studies encompassing various aspects of their biology, natural history data on their reproductive ecology is still scarce. One of the important aspects of reproductive ecology is the oviposition site since it can impact the reproductive success of a species. Herein, we provide detailed information on the reproductive ecology of a population of Teratohyla midas from the Colombian Amazon foothills and test whether this species shows a preference on substrate and height of oviposition site. We monitored a population using capture-mark-recapture of individuals identified by a photograph of their unique pattern of dorsal yellow spots. Wild-ID Software was used to corroborate if the dorsal pattern was different between individuals. Additionally, we monitored the presence of egg clutches, amplexus and oviposition behaviour. We observed 110 males and 5 females of T. midas, seen at an average height of 3.1 m ± 2.9 (0–17.8 m) from the ground. Likewise, we recorded the amplexus behaviour of two pairs for approximately 150 min. Once the oviposition happened, the male retreated, and the female covered the egg clutches for approximately 60 min. We observed 25 egg clutches with 60% being deposited in leaves of Selaginella sp and found at an average height of 2.9 ± 1.7 m (1.1–7.0 m). Thus, the selection of oviposition site was not random but mostly specific to one type of substrate. Furthermore, there was an overlap of the re-sampled median height distributions of active individuals and clutches, which suggests that oviposition does not occur at a preferred height within the vertical distribution of individuals. The information presented here is the first detailed record of reproductive ecology for this species and we hope to provide a basis to improve our knowledge on the biology of this species and other glass frogs.     

Reproductive ecology of a Tibetan frog Nanorana parkeri (Anura: Ranidae)

Endemic to the Tibetan Plateau, Nanorana parkeri figures among the highest altitude amphibians in the world. The present work, which was conducted in an alpine marsh at 4300 m altitude, is the first report of the species’ reproductive ecology. The breeding season, as indicated by the presence of amplectant pairs and fresh eggs in ponds, lasted from early Mary to early July. The ratios of adult male to female were 1.3 in hibernation ponds and 2.3 in spawning ones. Males were smaller than females. Amplexus was typically axillary (81.7%), with a few exceptional amplexus in which a male clasped another male or object rather than gravid females. Scramble competition occurred in 6.8% of the normal amplexus located. The body sizes of amplexed couples correlated positively. Deposited eggs were attached to submerged plants solitarily (60.5%) or in small clusters (39.5%), and the scattered arrangement of individual eggs could be a strategy to ensure embryonic development in oxygen-poor environments. Clutch size averaged 189 [standard deviation (SD) = 64], and correlated positively with female body size; egg size averaged 2.18 mm (SD = 0.10), independent of female body size; both traits within a clutch were negatively related with each other even controlling for female body size. Relatively few and large eggs laid by the Tibetan frogs, compared with those by lowland aquatic-spawning anuran species, should be adaptive to the harsh high-altitude conditions. Larvae hatched from eggs after 16.4 days on average (SD = 5.8). Froglets emerged between late July and early August, but some tadpoles were present in winter. These findings may help to understand the evolution of amphibians in extreme environments and to protect these remote species.     

Reproductive biology and strategies of nine meloid beetles from Central Europe (Coleoptera: Meloidae)

The reproductive biology of meloid species from Central Europe is investigated by means of laboratory breeding experiments. They show that the total reproductive potential of meloids, with up to 40,000 eggs, largely exceeds prior data. Furthermore, the number of laid eggs strongly relates to the way by which the triungulins find their host. Clutch size correlates significantly with the size of the beetle, while egg size is independent of this. Both clutch size and egg size decrease with each oviposition. For some species, reproductive data are used to demonstrate how they have adapted to their habitat and to point out existing trade‐offs. Based on the obtained results and on an evaluation of the relevant literature, three types of reproductive strategy can be distinguished within the meloids: (1) very high reproductive rates of open field species with phoretic larvae; (2) average reproductive rates of forest populations of species with phoretic larvae and of species the larvae of which search the nests of their hosts actively; and (3) small to average reproductive rates of those species depositing their clutches in the immediate proximity of their hosts' 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.     

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.     

Reproductive biology of the endangered wattled curassow (Crax globulosa; Galliformes: Cracidae) in the Juruá River Basin,Western Brazilian Amazonia

The reproductive biology of Crax globulosa is virtually unknown, this knowledge comprised of only a few anecdotal notes. We found nine nests of Crax globulosa in the middle section of the Juruá River, western Brazilian Amazon, during the dry season. Nests averaged 22.5 m from water and 13.3 m above the ground. We observed two nest types: five made of twigs, leaves and vines, and four within a bromeliad. All nests contained two eggs, but six (67%) were subsequently predated. A female tagged with a transmitter nested twice during the same breeding season. A chick was monitored together with its parents for > 10 months. In addition to hunting and habitat loss, nest predation could be another threat to this endangered species.