The advertisement calls of three South American poison frogs (Amphibia: Anura: Dendrobatidae), with comments on their taxonomy and distribution

The advertisement calls of three species of dendrobatid frogs from Bolivia and Peru are described. For each species we present a characteristic audiospectogram and oscillogram. We also provide numerical information about the spectral and temporal features of the calls. Our recordings of these species are compared with previously described calls of the same species from other locations. Comparisons between the calls of three different populations of Colostethus from Peru and Bolivia support their conspecificity. Characteristics of the call of a Peruvian population of Epipedobates differ from those of E. hahneli, suggesting that further taxonomic research is needed. The distribution of the genus Colostethus and Epipedobates in Bolivia is reassessed.     

Advertisement calls of Neotropical poison frogs (Amphibia: Dendrobatidae) of the genera Colostethus,Dendrobates and Epipedobates,with notes on dendrobatid call classification

The advertisement calls of the following Neotropical poison frog species (Dendrobatidae) are described: Colostethus brunneus, Dendrobates imitator yurimaguensis, D. leucomelas and two populations referable to Epipedobates boulengeri. Oscillograms, audiospectrograms and measurements of vocalizations are provided. Advertisement calls of C. brunneus are similar to possible related species, while D. leucomelas vocalizations deviate from suggested phylogenetic relatives. Advertisement calls of D. imitator yurimaguensis do not differ from those of D. i. imitator ; the validity of the former is doubted. Bioacoustics provide evidence that E. boulengeri could probably comprise a complex of at least two species. Five formerly suggested call types are re-defined using measurable characters. As far as possible, the 71 dendrobatid frog species for which advertisement calls have been described are allocated.     

Natural history of Phyllomedusa megacephala (Miranda-Ribeiro, 1926) (Anura: Hylidae) in southeastern Brazil,with descriptions of its breeding biology and male territorial behaviour

The breeding biology and male territorial behaviour of the large-headed leaf-frog (Phyllomedusa megacephala) were studied in three temporary altitudinal streams located in the Cerrado biome of southeastern Brazil, during three consecutive years (2007–2009). Phyllomedusa megacephala showed significant sexual dimorphism, with females being bigger and heavier than males. Acoustic and physical interactions between males defending or not defending territories including amplectant and non-amplectant males, patrolling behaviour by males without established territories, and triple amplexus were observed. Neither males nor females were observed using visual cues when searching for mates. We found that males that were present at breeding sites in previous years bred more successfully and maintained territory better.     

Development and demography of Phasmahyla jandaia (Bokermann and Sazima, 1978) (Anura,Hylidae) tadpoles in an Atlantic Forest site,southeastern Brazil

Mortality rates are often high during the anuran tadpole stage, making demographic parameters in this phase of their life cycle important to the understanding of population demography. Nevertheless, information on mortality rates or population size is lacking for most Brazilian anurans. Herein we report on the demographic parameters of Phasmahyla jandaia (Hylidae) during the larval stage, including number of individuals through time, mortality rates and time of recruitment. Tadpole recruitment occurred year‐round, although froglet recruitment to the terrestrial habitat was restricted to the warm, rainy season. This trend seems to result in high plasticity of the tadpole developmental period. Mortality rates decreased with advancing tadpole stage, totalling 77% during the whole aquatic phase. Survivorship can be regarded as intermediate compared with other anurans for which data are available, and is in accordance with a high investment in egg size and the low number of eggs laid by P. jandaia.     

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.     

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.     

Vocalization and territorial behaviour of Phyllomedusa nordestina Caramaschi, 2006 (Anura: Hylidae) from southern Bahia,Brazil

Territoriality is common among amphibians with a prolonged breeding season and can be expressed through the defence of territories with vocalizations and aggressive interactions. The present study aims to describe the territorial behaviour of male Phyllomedusa nordestina, test whether the physical characteristics of males influence the results of disputes, and describe the vocalizations of the species. The study was conducted at temporary and permanent ponds located in the Ecological Reserve Michelin, Igrapiúna, Bahia, Brazil. Male P. nordestina defended territories and showed aggressive behaviour, consisting of vocal disputes, chasing and physical fighting. Winners were not bigger, heavier, or in better condition than the losers. The victory may be associated with the vocalization activity. Three types of vocalizations were recorded: the advertisement call, composed of one or two multipulsed notes, and two types of territorial calls. We also report on male patrolling behaviour and habitat use.     

Mating behaviour,territoriality and natural history notes of Phyllomedusa ayeaye Lutz, 1966 (Hylidae: Phyllomedusinae) in south-eastern Brazil

The mating (male courtship, amplexus and oviposition) and male territorial behaviours of Phyllomedusa ayeaye are described from a high-altitude site in the state of Minas Gerais, south-eastern Brazil. Information related to male breeding success and territoriality, as well as egg clutch parameters, is provided, together with qualitative information regarding tadpole phenology and juvenile recruitment. In addition, estimations of sexual dimorphism and numbers of marked individuals are available through capture-mark-recapture sampling. Females bred with males within spatially clustered oviposition sites (broadleaf plants). In some cases, the amplectant couple actively searched for the oviposition site. Males defended territories from other males, employing both acoustic and physical interactions. Some males successfully maintained their calling sites over successive nights, and others seemed to switch among nearby sites during successive nights and tried to disrupt ongoing ovipositions. No significant relationship was found between physical attributes (snout vent length or body mass) of males with breeding success. Also, no influence of the number of nights a male was active in chorus and its breeding success was detected. Therefore, it is proposed that the mating system in P. ayeaye may be opportunistic. Additional information related to reproduction (egg clutch parameters and breeding behaviours) is also discussed for other species of the Phyllomedusa hypochondrialis group and compared with the results of the present study.     

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.     

Reproductive behaviour and development dynamics of Odontophrynus cordobae (Anura,Cycloramphidae)

We provide detailed information on breeding sites, release call, satellite behaviour, courtship, and embryonic and larval development of Odontophrynus cordobae. Field observations were carried out during two breeding seasons (2004–2005 and 2008–2009). Clutches were raised in captivity (artificial ponds) to analyse the development of embryos and tadpoles. Breeding sites were represented by streams and their backwaters, as well as temporary and permanent ponds of varying sizes. Operational sex ratio was male-biased varying between 0.154 and 0.25. Acoustic activity started about 8–10 pm and ended between 2 and 4 am the next day. Distance among calling males was approximately three metres. Male satellite behaviour was observed. Amplexus attempts among males were common. Release calls were structurally similar although shorter than advertisement calls. Courtship and formation of amplexus were documented.     

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.     

Field and laboratory observations on reproductive aspects of Pseudopaludicola ameghini (Cope, 1887) (Leptodactylidae: Leiuperinae)

ABSTRACT

The genus Pseudopaludicola includes small-sized anurans, widely distributed throughout South America. Twenty-three out of the 25 species occur in Brazil. Although described more than a century ago, from mid-southern Mato Grosso state, central Brazil, Pseudopaludicola ameghini is poorly known. Here we describe the characteristics of reproductive site, amplexus, egg-laying behaviour, eggs and tadpoles of P. ameghini based on specimens and observations performed in the vicinities of the type locality. Pairs of P. ameghini reproduce in shallow and slow groundwater established on hydromorphic terrains, in open environments amidst the Brazilian Cerrado savanna. Reproductive activity occurred between 17:00 and 21:00 h at two sites studied from December 2013 to April 2014. Amplexus is axillary. Eggs are spherical, with a mean diameter of 5.1 mm (yolk plus jelly envelope). Oviposition occurs in shallow sites at a depth of nearly 2.0 cm. Females deposit their eggs one at a time, directly onto sediment at the bottom of waterbodies or attached to submerged vegetation. The tadpole body is oval in dorsal view and globular/depressed in lateral view; eyes are large and dorsally positioned. Nares are large, round, with a small apophysis on marginal rim, dorsally positioned, near the eyes. The spiracle is short, with posterodorsal opening. The oral disc is anteroventral, emarginated laterally, with one dorsal and two ventral gaps; the tooth row formula is 2(2)/2(1), and the upper jaw sheath is ‘arc’ shaped. Pseudopaludicola ameghini has a unique behaviour of oviposition among members of the genus. The differences in reproductive pattern and larval characteristics of P. mystacalis and P. ameghini reinforce the taxonomic validity of the latter, questioned until recently.     

Breeding biology of Ameerega braccata (Steindachner, 1864) (Anura: Dendrobatidae) in the Cerrado of Brazil

Reproductive aspects of Ameerega braccata, a Cerrado endemic species of Dendrobatidae, were studied in the surroundings of the type locality of the species, Chapada dos Guimarães, mid-southern Mato Grosso State, Brazil. We found that males call mainly early in the morning and in the late afternoon. During courtship, the female approaches a calling male and tactile and visual communication occurs. Males call continuously while guiding females to the oviposition site, which may be situated as far as 24 m (in a straight line) from the initial encounter site. Spawn are deposited over fallen leaves on the soil surface or in burrows. Female snout–vent length and body mass did not explain the variation in ovary mass, or the variation in the number and size of post-vitellogenic oocytes. The results reported here for A. braccata might help to understand trends in the evolution of dendrobatids in open Cerrado environments.     

Breeding behaviour of Bokermannohyla nanuzae (Anura: Hylidae) at an Atlantic Forest site in southeastern Brazil

We studied the breeding activities of Bokermannohyla nanuzae at an Atlantic Forest site in southeastern Brazil from August 2010 to April 2012. We described courtship behaviour, acoustic parameters of calls, egg clutch features and the egg-laying site, and characterized the reproductive mode. We recorded calling males and gravid females almost year-round, except for a few months in the dry season. We observed the interaction of five male–female pairs that exhibited stereotyped behavioural sequences including visual and tactile signals. We identified three different types of calls that we considered as the advertisement call and two types of courtship calls. Egg clutches were placed in rocky crevices with water or in streamside puddles, among rocks, that would be likely to be flooded as stream water level raises, which characterizes a reproductive mode different from the one previously recognized for this species. The breeding biology of B. nanuzae is complex, with elaborate courtship behaviour and signalling.     

Target-enriched DNA sequencing from historical type material enables a partial revision of the Madagascar giant stream frogs (genus Mantidactylus)

ABSTRACT

The subgenus Mantidactylus is a group of frogs endemic to Madagascar, including the largest anuran species on the island. Although these frogs are common and widely distributed, their taxonomy remains unclear. Two species are currently recognised, M. grandidieri and M. guttulatus, with another available name, Rana pigra, considered to be a synonym of M. grandidieri. However, molecular studies have suggested the presence of several cryptic species within the group. Additionally, due to the lack of prominent morphological features, allocating the available names to evolutionary lineages has proven challenging. In the present study, we take a first step towards solving these problems by using fragments of the 16S mitochondrial gene and RAG1 nuclear gene from all over the range of the subgenus to describe its genetic diversity. We also use a newly designed target enrichment laboratory protocol to sequence three mitochondrial fragments from five name-holding museum specimens (as old as 120 years) in order to determine to which lineages the existing names should be applied. The study of the 16S mitochondrial gene revealed 7 geographically separated lineages, distinct enough to be considered candidate species. Out of the five museum specimens analysed, four successfully yielded DNA sequences and could be attributed to one of the aforementioned lineages. Therefore, the name Mantidactylus grandidieri should be applied to the populations from North-Eastern Madagascar, while M. guttulatus refers to populations from inland localities along the Eastern coast of the island. On the other hand, the holotype of Rana pigra did not yield enough genetic material to allow definitive identification. While our data were not sufficient to assess the status of the four lineages distributed along the Eastern coast, the populations from North-Western Madagascar were highly distinct on both the mitochondrial and nuclear markers. We thus describe them as a new species, M. radaka sp. nov.

http://www.zoobank.org/urn:lsid:zoobank.org:pub:1EDDAF0D-FE37-490A-B09E-E136A0C5CB35     

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.     

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.     

Spawning behaviour of Engystomops pustulatus (Anura: Leptodactylidae)

Foam nests have evolved independently in several amphibian groups as an adaptive response to prevent predation and desiccation in dry environments. Nests are normally laid on ponds, or in underground galleries, humid forest leaf litter or terrestrial bromeliads. They are built when males or females beat a foam precursor associated with the egg masses extruded by the female. The spawning process requires the synchronic actions of the mating pair to obtain a hemispheric nest that protects the offspring. Herein, we describe the spawning behaviour of Engystomops pustulatus based on videos from 13 nesting couples from the lowlands of western Ecuador. Three variables were measured as indicators of male effort: duration of mixing events, duration of resting periods, and number of kicks per mixing event. We consider that not only male physical effort but also female behaviour influences nest structure. We suggest that nest building requires prolonged and intense physical activity by the male as well as the female’s steady position during spawning and female’s oviposition site selection. Nest building has two phases. In the first phase, the duration of resting periods, the duration of mixing events, and the number of kicks increase and are highly variable. During the second phase the three variables stabilise until the end. The volume of the nest increased mainly during the second phase. In four nesting events we observed kicking movements by the female. To our knowledge, this is the first time that female kicking has been observed in leptodactylid frogs. The function of this behaviour is unknown but our observations suggest that it may be triggered by insufficient male effort. Traditionally, female mate choice in Engystomops has been explained under models of indirect benefits exclusively. We argue that the prolonged male activity during nesting could influence female fitness directly. This will allow the operation of sexual selection via direct benefits.     

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.