Helminths of 13 species of microhylid frogs (Anura: Microhylidae) from Papua New Guinea

In an attempt to better document the invertebrate biodiversity of the threatened fauna of Papua New Guinea (PNG), 208 microhylid frogs representing 13 species collected in 2009 and 2010 in PNG were examined for endoparasitic helminths. This study found mature individuals of one species of Digenea (Opisthioglyphe cophixali), adults of two species of Cestoda (Nematotaenia hylae, Cylindrotaenia sp.) and cysticerci of an unidentified cestode species; adults of nine species of Nematoda (Aplectana krausi, Bakeria bakeri, Cosmocerca novaeguineae, Cosmocercella phrynomantisi, Falcaustra papuensis, Icosiella papuensis, Ochtoterenella papuensis, Parathelandros allisoni, Parathelandros andersoni), and one species of Acanthocephala (cystacanths in the family Centrorhynchidae). There was a high degree of endemism among the helminth species infecting the microhylids, with 83% of the species known only from PNG. Yet the helminth fauna infecting Papuan microhylids are generalists with direct life cycles (no intermediate host) that also infect other anuran species. We thus conclude infection is more dependent upon habitat conditions than diet. Twenty-nine new host records are reported.     

Helminths of 26 species of microhylid frogs (Anura: Microhylidae) from Papua New Guinea

Five hundred and sixty microhylid frogs representing 26 species collected from 2002 to 2005 in Papua New Guinea were examined for helminths. Found were three species of Digenea, two species of Cestoda, nineteen species of Nematoda, and two species of Acanthocephala. One hundred and eleven new host records were recorded. Nematodes comprised 73% (19/26) of the species present and 95% (10,581/11,107) of the individuals present. Seventeen of the 26 (65%) helminth species found are currently known only from Papua New Guinea.     

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.     

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.     

Preliminary report on the genetic structure of Glyphoglossus molossus (Anura: Microhylidae) from the Khorat Plateau,north-eastern Thailand

Glyphoglossus molossus, is one of the most economically important amphibians in the Khorat Plateau, north-eastern Thailand. It is categorised as a near-threatened species by IUCN due to over-exploitation. Here, we examined the genetic structure of G. molossus using partial mitochondrial cytochrome-b gene sequences from specimens collected at 11 localities. The sequence analysis revealed the presence of 15 haplotypes, 5 of which are shared by 2 or more populations, and 10 haplotypes that are confined to a single population. The relatively low haplotype (h) and nucleotide (π) diversities suggest that the Phu Phan Mountain Range is not high enough to act as an effective dispersal barrier between the Sakon Nakhon and Khorat Basins. However, AMOVA and phylogenetic analyses based on Maximum likelihood (ML) and Bayesian inference (BI) strongly supported the presence of two genetically divergent clades, Sakon Nakhon Basin and the northern part of the Khorat Basin (clade A) and the southern part of the Khorat Basin (clade B). These two lineages are separated by substantial geographical distance, which has putatively resulted in a reduction of gene flow. Further studies, with more extensive genetic sampling, especially from throughout the species range will aid in better interpreting our results.     

Reproductive site selection in the leaf-frog Phyllomedusa azurea Cope, 1862 (Anura: Hylidae) in altered areas of the Brazilian Cerrado

The selection of reproductive sites by anurans may be associated with each species’ behavioural restrictions, reproductive modes, morphology and physiology. We investigated the use of reproductive sites by Phyllomedusa azurea in an area of Cerrado, Central-Western Brazil, which has been modified by agricultural and cattle ranching. Reproductive activity was studied during the peak of the rainy season in two consecutive years. No correlation was found between male body size and position of the calling site, and calling sites did not vary among ponds. Conversely, the height and distance from the water margin where clutches were found varied among ponds. Phyllomedusa azurea used mainly Brachiaria sp. and Brachiaria humidicola grasses as calling sites and the grass Brachiaria sp. and the shrub Melochia villosa (Malvaceae) as oviposition sites. Calling males used the vegetation according to its availability; however, individuals seemed to exhibit significant preferences regarding the type of vegetation used for oviposition.     

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.     

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.     

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.     

Breeding behaviour of the Omei tree frog Rhacophorus omeimontis (Anura: Rachophoridae) in a subtropical montane region

Breeding behaviour of the Omei tree frog, Rhacophorus omeimontis, was studied during the egg-laying period (mid-April to late June) in south-west China. The operational sex ratio of the breeding population was male-biased at 3.0?±?0.8 (mean?±?SD) on a nightly basis in Pond A and 4.3?±?1.1 in Pond B. Pairs with a male clasping a female occurred in ponds first; the amplectant pairs moved to a neighbouring plant and then released foam in leaves 14–370 cm above the pond's water surface. Immediately, other males came to join the pair, forming an amplexing group of 2 to 7 males (for all 45 breeding units observed). Among the males no direct physical competition for possession of the females was observed. Females produced foam which surrounded the subsequently-laid eggs. The whole process of oviposition lasted 45–65 minutes. After ovipositing, males left the female, the female folded and lined neighbouring leaves with more foam produced to surround the eggs further. This process took 15–45 minutes. The numbers of eggs in a clutch ranged from 457 to 837 and eggs were between 2.9 and 3.4 mm in diameter; those two measures were negatively correlated with each other. Eggs hatched after 12–17 days; the larval period lasted 63–78 days. Fertilization success was positively related to the number of males participating in matings.     

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.     

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.     

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.     

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.     

Basking behaviour in two sympatric herbivorous lizards (Liolaemidae: Phymaturus) from the Payunia volcanic region of Argentina

We studied several aspects of the thermal biology of two coexisting saxicolous species of the genus Phymaturus (Liolaemidae) at the Payunia, a volcanic region in Argentina where harsh conditions prevail. We marked individuals in grids and assessed the environmental conditions when the individuals showed their maximum activity (i.e. when more than 50% of marked individuals were active), the time spent basking, and the postural behaviour in relation to different cloudiness conditions. We found that temperatures recorded when the species exhibit their peaks of activity were higher for Phymaturus payuniae, the smaller species, during the summer at one of the three studied sites. Phymaturus roigorum exhibited the longest basking periods, but during these longer periods cloudy conditions prevailed. Both species adopted a head-up posture when conditions were sunny and a head-down posture when under cloudy conditions. This is the first contribution where thermal aspects of two sympatric species of Phymaturus are evaluated.     

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.     

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.     

A new species of Phrynobatrachus (Amphibia: Anura: Phrynobatrachidae) from the Northern Mountains of Tanzania

ABSTRACT

Using integrative approaches, a new large-bodied species of Phrynobatrachus is described from a series of 48 specimens from the montane forests of the West Usambara and North Pare Mountains of Tanzania. The most distinguishing morphological feature separating Phrynobatrachus ambanguluensis sp. nov from similar species is the markedly overhanging and pointed upper jaw and snout. Mitochondrial 16S rRNA indicates that the new species differs from all other species with published sequence data by a minimum distance of 4.75% and is sister to P. krefftii, with which it has been confused in the past. The new species is known from two forest reserves and is of high conservation concern given these areas are highly impacted by anthropogenic change.

http://www.zoobank.org/urn:lsid:zoobank.org:pub:E0C82A87-47A5-426B-978D-96D27FA7A3B7     

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.     

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.