Stream-breeding Frogs Research Articles

Chytrid infections exhibit historical spread and contemporary seasonality in a declining stream-breeding frog.

Species with extensive geographical ranges pose special challenges to assessing drivers of wildlife disease, necessitating collaborative and large-scale analyses. The imperilled foothill yellow-legged frog (Rana boylii) inhabits a wide geographical range and variable conditions in rivers of California and Oregon (USA), and is considered threatened by the pathogen Batrachochytrium dendrobatidis (Bd). To assess drivers of Bd infections over time and space, we compiled over 2000 datapoints from R. boylii museum specimens (collected 1897-2005) and field samples (2005-2021) spanning 9° of latitude. We observed a south-to-north spread of Bd detections beginning in the 1940s and increase in prevalence from the 1940s to 1970s, coinciding with extirpation from southern latitudes. We detected eight high-prevalence geographical clusters through time that span the species' geographical range. Field-sampled male R. boylii exhibited the highest prevalence, and juveniles sampled in autumn exhibited the highest loads. Bd infection risk was highest in lower elevation rain-dominated watersheds, and with cool temperatures and low stream-flow conditions at the end of the dry season. Through a holistic assessment of relationships between infection risk, geographical context and time, we identify the locations and time periods where Bd mitigation and monitoring will be critical for conservation of this imperilled species.

The tadpoles of five Megophrys Horned frogs (Amphibia: Megophryidae) from the Hoang Lien Range, Vietnam.

Frogs in the genus Megophrys are an Asian radiation of stream-breeding frogs. The tadpoles of many Megophrys species are undescribed; those that are described are often dubiously allocated to species by association with post metamorphic specimens at collection sites and without supportive molecular data. We provide detailed descriptions of the larvae of five species of Megophrys from the Hoang Lien Range in northwest Vietnam: Megophrys fansipanensis, M. gigantica, M. hoanglienensis, M. jingdongensis and M. maosonensis. Tadpoles from different subgenera differ from each other via a combination of patternation in life, oral disc shape and tail morphology but given the small sample size, and limited number of species it is unlikely that these differences can be applied more widely to delineate subgenera. Morphological differences between tadpoles from species within the subgenus Panophrys were insufficient to clearly delineate all species. The ability to identify tadpoles is likely to advance our understanding of the frog fauna in mainland southeast Asia.

Title: Recruitment is key to understanding amphibian’s different population-level responses to chytrid fungus infection

Understanding why related species have differing population-level responses to threats can be key to identifying conservation options for declining populations. However, this is difficult when multiple threats are implicated. Chytrid fungus (Batrachochytrium dendrobatidis: Bd) is implicated in at least 500 amphibian population declines globally, although few tangible options exist to mitigate pathogen impacts. Other threatening processes also invariably operate on most amphibians. Non-native fish, for example, can contribute to amphibian declines and may exacerbate Bd impacts. We disentangled the impacts of Bd and non-native fish upon two stream breeding frog species with differing conservation statuses to reveal vital rates that are crucial for species persistence. Litoria spenceri are threatened and historically occurred at elevations between 300–1100m asl in southeastern Australia. Litoria lesueurii are non-threatened and sympatric with L. spenceri at some sites. Using mark-recapture derived demographic rates known to correlate with climate and elevation, discrete-time deterministic population models were constructed for each species at high, moderate and low elevation sites, and multiple management scenarios. Our study reveals that age to maturation, clutch size and egg-year 1 survival influenced interspecific and intraspecific population-level responses of the two frogs to Bd impacts. Importantly, our results highlight that an amphibian population’s capacity to counteract Bd-mediated adult mortality is clearly constrained by other threats and environment interactions that moderate species recruitment. Furthermore, understanding limits to recruitment may help identify Bd mitigation strategies. In our study, disease mitigation may be best achieved at some sites by enhancing recruitment through non-native fish management.

Reproductive Cycle, Size and Age at Sexual Maturity, and Sexual Dimorphism in the Stream-Breeding Frog Crossodactylus schmidti (Hylodidae)

A reproductive strategy includes physiological, morphological, behavioral traits dependent on exogenous and endogenous regulators, including size/age at maturity, temporal variation in gametogenic cycles, and size-fecundity relationships. Sexual differences in reproductive investment, territoriality and resource use may result in sexual dimorphism on body size and other morphological traits. These life-history components are key for understanding the selective forces underlying male and female reproductive strategies in a population. We investigated the reproductive biology of the stream-breeding frog Crossodactylus schmidti through the histological analysis of testes, ovaries, and bone samples. Mature males and females and free-swimming tadpoles occurred in all months, though the monthly proportion of mature females was variable. Free spermatozoa, sperm bundles, and germ cell cysts in several stages occurred in testes of all except two males, whilst ovaries of most females presented all follicle stages, indicating continuous gametogenesis in both sexes. There was no significant seasonal variation in snout–vent length (SVL), body mass (BM) or in the gonadosomatic index for neither sex, further indicating a continuous pattern of reproduction. Minimum SVL and age at sexual maturity was 22.14 mm and 2 a, respectively, in males, and 21.78 mm and 3 a, respectively, in females; both sexes reached up to six years of longevity. Gonad mass increased with BM in both sexes, though this effect was much stronger in females. After controlling for age, females were significantly larger than males in SVL, BM, and MW (mouth width): the larger female body size suggests selection for increased fecundity, whereas the larger MW possibly favors the consumption of large, energetically important prey for sustaining the continuous egg production. Finally, there was a positive correlation between female SVL and number of thumb spines, but the number of thumb spines did not differ between the sexes; we briefly discuss a possible role of thumb spines in the courtship of C. schmidti based on field observations.

Seasonal, annual and decadal change in tadpole populations in tropical Australian streams

Abstract Declines due to fungal disease (chytridiomycosis) have affected many stream-dwelling frog species, especially in the tropics, leading to reduced abundance and diversity of their tadpoles. Studies in the Australian Wet Tropics have demonstrated that some frog species have declined or disappeared, while others have persisted. To assess the occurrence of stream-breeding frogs, we monitored tadpole populations of five frog species in Wet Tropics streams in the early 1990s (uplands, before chytridomycosis emergence), and in 2011-2013 (uplands and lowlands, after chytridiomycosis emergence), and investigated environmental factors that might influence tadpole abundance. Riffle-dwelling tadpoles of two frog species disappeared from the upland stream site during the 1990s, reflecting reported losses of adult populations. Tadpoles of one upland pool species initially declined but had recovered by 2011-2013. Samples from the lowlands in 2011 to 2013 indicated no similar loss. Chytridiomycosis was the likely cause of changes in tadpole abundances between the two survey periods, given its known occurrence and documented effects on adult frogs in these systems; however, we did not measure its prevalence in this study. Tadpole populations fluctuated seasonally, with abundances highest in spring and summer, reflecting the timing of frog reproduction. The most important biophysical influence on the assemblages that we measured was current velocity. Tadpole peak abundances suggest that they make a substantial contribution at the consumer level of food webs, and that their loss has altered food webs substantially in upland streams.

Molecular phylogeny and diversification of Malagasy bright-eyed tree frogs (Mantellidae: Boophis)

We investigate the molecular phylogeny of Boophis, a group of arboreal frogs from the Malagasy-Comoroan family Mantellidae. Based on newly acquired DNA sequences of five mitochondrial and five nuclear markers (7444 base pairs), we infer a phylogeny of Boophis with complete species-level taxon sampling. We reconstruct the phylogeny using Bayesian inference and maximum likelihood and estimate divergence dates for the major clades of the genus. The phylogenetic analyses together support the monophyly of the two subgenera (Sahona and Boophis), and provide strong support for most previously identified species groups, except that the B. ulftunni group is nested within the B. majori group. We also erect a new species group related to the B. mandraka group, the B. blommersae group, composed of small-sized, brown stream-breeding frogs previously included within the B. majori group. Finally, we use the resulting phylogeny to illustrate striking examples of repeated evolution of coloration and ventral transparency and address the biogeographic history and broad pattern of species diversification in the genus. Ancestral area reconstructions provide evidence that Boophis diversified within the Eastern highland forests of Madagascar, and we suggest that adaptation to these highland areas was important in their diversification.

Communication in a noisy environment: short-term acoustic adjustments and the underlying acoustic niche of a Neotropical stream-breeding frog

Acoustically active animals may show long- and short-term adaptations in acoustic traits for coping with ambient noise. Given the key role of calls in anurans’ life history, long- and short-term adaptations are expected in species inhabiting noisy habitats. However, to disentangle such adaptations is a difficult task, incipiently addressed for Neotropical frogs. We investigated if males of a stream-breeding frog (Crossodactylus schmidti) adjust call traits according to the background noise, and if the signal-to-noise ratio (SNR) varies between call harmonics and along call notes. We measured sound pressure levels of calls and noise in the field and used a fine-scale acoustic analysis to describe the signal and noise structure and test for noise-related call adjustments. The multi-note harmonic call of C. schmidti greatly varied in the spectral structure, including a trend for increasing note amplitude along the call, a wide frequency bandwidth of the 2nd harmonic, a minor call frequency modulation due to a trend for increasing note frequency within the same harmonic, and a major call frequency modulation due to the variable location of the dominant harmonic along the call. Calls had significantly higher frequencies than the noise at the range of the 1st and the 2nd call harmonics, and significantly louder sound pressure than the noise at the range of all harmonics. Males emitted the majority of call notes showing positive SNR, and though males also emitted some notes with negative SNR, when a given harmonic was negative the other harmonics in the same note did not tend to be SNR-negative. Our results indicate that male C. schmidti show short-term acoustic adjustments that make the advertisement call effective for coping with the interference of the stream-generated noise. We suggest that the call spectral plasticity serves for coping with temporary changes in the background noise, whilst we also discuss the possibility that the redundant, harmonic-structured call may have evolved to diminish masking interference on the acoustic signal by the background noise. This is the first study to uncouple noise-related acoustic adjustments and putative long-term acoustic adaptations for a Hylodidae, providing insights on behavioral plasticity and signal evolution of stream-breeding frogs.

Calling Activity of a Stream-Breeding Frog from the Austral Neotropics: Temporal Patterns of Activity and the Role of Environmental Factors

Abstract: Animal activity patterns can be influenced by selection pressures from local environmental conditions that might fluctuate at different temporal scales. Although studies with frog species and local populations can suggest how variation of environmental factors affects activity patterns, this topic has received little coverage for Neotropical diurnal frogs that inhabit streams, particularly for subtropical species. We described the temporal patterns of calling activity of Schmidt's Spinythumb Frogs (Crossodactylus schmidti) in southern Brazil and investigated the role of environmental factors on this activity. We recorded local environmental variables and monitored calling activity from October 2011 to September 2012, by counting the number of calling males and the number of emitted calls at hourly intervals throughout the day. Male frogs engaged in calling activity year-round, despite the local climatic seasonality. There was no seasonality in the number of calling males or in the number of cal...

Rediscovery of the Critically Endangered Streamside Frog, Craugastor Taurus (Craugastoridae), in Costa Rica

In 1987 the amphibian decline crisis reached its apex in Costa Rica when at least 17 species experienced population crashes and subsequently went undetected for decades. The amphibian declines in Costa Rica were relatively well documented and came to exemplify the current global amphibian decline crisis. The Mesoamerica endemic frog clade, the Craugastor punctariolus species group, is one of most severely affected anuran clades, experiencing a loss of 26 out of 33 species throughout Mesoamerica. Eight species of C. punctariolus group frogs occur in Costa Rica, and all declined following the 1987 die-off; despite intensive surveys over the last 14 years, most remain undetected. To date, only one species in this group, the stream-breeding frog C. ranoides, in known to have a stable population, and only in the Santa Elena Peninsula. Here we document the rediscovery of another species, the South Pacific streamside frog C. taurus, in southeastern Costa Rica, representing the first sighting after fifteen years of searching. We discovered two previously unknown populations in Punta Banco, the driest section within the historical range, in an area representing only 4% of the historical distribution. Our findings add to the short but growing list of recently rediscovered amphibian species in Costa Rica and provide encouraging news in an otherwise discouraging situation for amphibian conservation. Additional research and monitoring are urgently needed to develop long-term management plans for this and other Critically Endangered species

Extremely low prevalence of Batrachochytrium dendrobatidis in frog populations from neotropical dry forest of Costa Rica supports the existence of a climatic refuge from disease.

Population declines and extinctions of numerous species of amphibians, especially stream-breeding frogs, have been linked to the emerging infectious disease chytridiomycosis, caused by the chytrid fungus, Batrachochytrium dendrobatidis. In Central America, most of the 34 species of the Craugastor punctariolus species group have disappeared in recent years in high- and low-elevation rainforests. Distribution models for B. dendrobatidis and the continuous presence of the extirpated stream-dwelling species, Craugastor ranoides, in the driest site of Costa Rica (Santa Elena Peninsula), suggest that environmental conditions might restrict the growth and development of B. dendrobatidis, existing as a refuge from chytridiomycosis-driven extinction. We conducted field surveys to detect and quantify the pathogen using Real-time PCR in samples from 15 species of frogs in two locations of tropical dry forest. In Santa Elena Peninsula, we swabbed 310 frogs, and only one sample of the species, C. ranoides, tested positive for B. dendrobatidis (prevalence <0.1%). In Santa Rosa Station, we swabbed 100 frogs, and nine samples from three species tested positive (prevalence = 9.0%). We failed to detect signs of chytridiomycosis in any of the 410 sampled frogs, and low quantities of genetic equivalents (between 0 and 1073) were obtained from the ten positive samples. The difference in the prevalence between locations might be due not only to the hotter and drier conditions of Santa Elena Peninsula but also to the different compositions of species in both locations. Our results suggest that B. dendrobatidis is at the edge of its distribution in these dry and hot environments of tropical dry forest. This study supports the existence of climatic refuges from chytridiomycosis and highlights the importance of tropical dry forest conservation for amphibians in the face of epidemic disease.

The importance of thermal conditions to recruitment success in stream-breeding frog populations distributed across a productivity gradient

Predicting the vulnerability of species to environmental change requires integrating observations of individual ecophysiological and behavioral responses with community level constraints. To assess the response of stream-breeding frogs (Rana boylii) to thermal stressors, such as cold water released from the depths of upstream reservoirs or warm water that results from climate change, we combined field manipulations with population censuses and environmental correlations. These frogs migrate between shaded tributaries and open canopy mainstem channels to oviposit where algal food is abundant for tadpoles. Within this context of spatial variation in aquatic primary productivity, we evaluated whether tadpole thermoregulatory behavior is a useful indicator of survival to metamorphosis and adult distribution. In a thermal gradient, tadpoles selected temperatures between 16.5–22.2°C (mean, 19.60±0.6°C). We reared tadpoles in streams colder, warmer, or close to thermal preference. Temperature effects were mediated through algal quantity and quality. Mortality increased with increasing deviation from preferred temperatures, but the effects were ameliorated when tadpole diet was supplemented with algae (Cladophora glomerata with epiphytic nitrogen-rich diatoms, Epithemia spp.) harvested from sun-lit channels. Distribution of frogs in free-flowing and dammed reaches within a northern California watershed was in equilibrium with tadpole thermal preference. Populations were dense (⩾125 breeding females/km) where July water temperatures averaged 17.5–19°C in 2010, a relatively cool summer. Below 16°C, frogs were sparse with open canopy and absent under closed canopy. Integration of thermoregulatory behavior with ecological context can thus be useful to forecast recruitment when the thermal regimes of rivers are altered by anthropogenic factors.

Population Recovery following Decline in an Endangered Stream-Breeding Frog (Mixophyes fleayi) from Subtropical Australia

Amphibians have undergone dramatic declines and extinctions worldwide. Prominent among these have been the stream-breeding frogs in the rainforests of eastern Australia. The amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd) has been postulated as the primary cause of these declines. We conducted a capture-mark-recapture study over a 7-year period on the endangered Fleay’s barred frog (Mixophyes fleayi) at two independent streams (30 km apart) in order to assess the stability of these populations. This species had undergone a severe decline across its narrow geographic range. Mark-recapture modelling showed that the number of individuals increased 3–10 fold along stream transects over this period. Frog detection probabilities were frequently above 50% but declined as the populations increased. Adult survival was important to overall population persistence in light of low recruitment events, suggesting that longevity may be a key factor in this recovery. One male and female were present in the capture record for >6 years. This study provides an unambiguous example of population recovery in the presence of Bd.

Aquatic eggs are fertilised by multiple males not engaged in amplexus in a stream-breeding frog

In anuran amphibians, multiple males amplexing a single female to fertilise her eggs has been found for less than 25 species, whereas matings without amplexus are known for less than five species. Here we provide a new example of simultaneous polyandry with multiple males not engaged in amplexus, in Feirana taihangnicus, a stream-dwelling, explosive breeder endemic to central China. Laboratory experiments showed that when one female was kept with one male in a vessel with elevated, flat stones, the female stood on her head with her swollen cloaca against the undersurface of the stone substrate to lay eggs (clutch size ranged from 371 to 533, n=7 females). Then, 10–102min after oviposition began, the male stood on his head and released sperm over the eggs distributed as a single layer on the stone surfaces. It took about 3h for the female to finish oviposition and for the male to finish fertilisation. On average, 96% of eggs were fertilised. In natural oviposition habitats, stream sections with slow flowing, we observed that 1 up to 15 males (8.7±6.6, n=6 cases), none in amplexus, participated in fertilising the eggs deposited by a single female. Evolutionary implications of this unusual reproductive strategy remain to be explored.

Survival and Abundance in Males of the Glass FrogEspadarana(Centrolene)prosobleponin Central Panama

While many amphibian species around the world are experiencing catastrophic declines, we have little understanding of the population dynamics of the majority of species. Estimating demographic parameters can help us understand the spatial and temporal dynamics of healthy populations, assess how populations may be impacted by threats, and interpret the recovery of diminished populations. Capture–mark–recapture (CMR) techniques represent a powerful approach for estimating such vital rates, but they have been used rarely in studies of tropical amphibians. We use 5 yr of mark–recapture data (2000–2004) to estimate survival probabilities and abundances of the stream-breeding frog species Espadarana (Centrolene) prosoblepon prior to the arrival of Batrachochytrium dendrobatidis, the amphibian chytrid fungus. We estimated these parameters for male E. prosoblepon on four streams (Cascada, Guabal, Loop, and Silenciosa) in Parque Nacional Omar Torríjos in central Panama. Across all streams and years, mean annual survival probability was 0.46 (0.41–0.52, 95% CI). Abundance varied among streams, with larger population sizes on Loop (78 ± 12 SE) and Cascada (64 ± 4) and smaller population sizes on Guabal (28 ± 3) and Silenciosa (30 ± 2), but showed little difference among years. Streams with different abundances had similar survival rates, and we suggest that availability of overhanging vegetation—used for oviposition and male territories—limits population size. These are the first survival and abundance estimates that exist for this species. They provide a critical baseline for comparison to other healthy populations and for evaluating recovery in sites infected with the amphibian chytrid fungus.

Movement patterns and habitat use of rainforest stream frogs in northern Queensland, Australia: implications for extinction vulnerability

Amphibians are one of the most highly threatened groups of animals, but their effective conservation is hampered by a paucity of basic ecological knowledge, particularly for tropical stream-breeding species, in which declines have been most common and severe. We examined the movement patterns and habitat use of three stream-breeding frog species at five sites in northern Queensland, Australia. Movement and habitat use differed significantly among species. Litoria lesueuri moved more frequently and greater distances than did our other study species, and was often located away from streams, moving between intact rainforest and highly disturbed environments. Litoria genimaculata moved less frequently and shorter distances and was more restricted to stream environments compared with L. lesueuri, but was often located in the canopy. L. genimaculata occasionally moved large distances along and between streams, but was never located outside of intact rainforest. Litoria nannotis moved almost as frequently as the other species, but remained in streams during the day, did not move large distances along or between streams, and was always located within intact rainforest. Because of its sedentary behaviour, narrow habitat tolerance and affinity for stream environments, L. nannotis may be more vulnerable to extinction in human-modified landscapes compared with L. lesueuri and L. genimaculata.

Fine scale gene flow and individual movements among subpopulations of Centrolene prosoblepon (Anura: Centrolenidae)

Dispersal capabilities determine and maintain local gene flow, and this has implications for population persistence and/or recolonization following environmental perturbations (natural or anthropogenic), disease outbreaks, or other demographic collapses. To predict recolonization and understand dispersal capacity in a stream-breeding frog, we examined individual movement patterns and gene flow among four subpopulations of the Neotropical glassfrog, Centrolene prosoblepon, at a mid-elevation cloud forest site at El Copé, Panama. We measured male movement directly during a two year mark-recapture study, and indirectly with gene flow estimates from mitochondrial DNA sequences (mtDNA). Individuals of this species showed strong site fidelity: over two years, male frogs in all four headwater streams moved very little (mean = 2.33 m; mode = 0 m). Nine individuals changed streams within one or two years, moving 675-1,108 m. For those males moving more than 10 m, movement was biased upstream (p < 0.001). Using mtDNA ND1 gene sequences, we quantified gene flow within and among headwater streams at two spatial scales: among headwater streams within two adjacent watersheds (2.5 km2) and among streams within a longitudinal gradient covering 5.0 km2. We found high gene flow among headwater streams (phi(ST) = 0.007, p = 0.325) but gene flow was more limited across greater distances (phi(CT) = 0.322, p = 0.065), even within the same drainage network. Lowland populations of C. prosoblepon potentially act as an important source of colonists for upland populations in this watershed.

Habitat use by stream-breeding frogs in south-east Sulawesi, with some preliminary observations on community organization

The habitat associations of stream-breeding frogs were examined along a series of stream transects on Buton Island in south-east Sulawesi, Indonesia. Of the eight frog species located along streams, four were observed breeding in stream habitats. We examined spatial habitat partitioning among these species. Three of the four species were found to be associated with a non-random selection of the available perch sites. Strong partitioning between species in habitat associations was found; partitioning of the available habitat space was primarily associated with differences in proximity to stream features, and in the height of perch sites. General observations indicated that oviposition sites of most species were associated with the microhabitats in which the adult frogs were found. All four stream-breeding species appear to have synchronous breeding phenologies and the spatial relationships of these species within the habitat space appear to reflect partitioning of calling sites and oviposition sites. The stream-breeding frog community in this region of Sulawesi has much lower species richness and less specialized habitat use compared with other tropical stream-breeding frog communities in the region.

Female Size-specific Clutch Parameters of Two Closely Related Stream-breeding Frogs, Rana sakuraii and R. tagoi tagoi: Female Size-independent and Size-dependent Egg Sizes

Female Size-specific Clutch Parameters of Two Closely Related Stream-breeding Frogs, Rana sakuraii and R. tagoi tagoi: Female Size-independent and Size-dependent Egg Sizes

Distribution, habitat requirements and conservation of the cascade treefrog ( Litoria pearsoniana, Anura: Hylidae)

Thirty-three species of Australian frogs have apparently declined in abundance since the late 1970s, some perhaps to extinction. The cascade treefrog Litoria pearsoniana, a stream-breeding frog from the forests of sub-tropical eastern Australia, was listed as an endangered species in Queensland following reports of population declines between 1978 and 1984. However, these reports were based on limited field data. I conducted a stratified survey across the geographic and environmental range of L. pearsoniana to determine its current distribution, abundance and habitat requirements. I detected L. pearsoniana in all major areas of mesic forest within its historical range, and at 29 of 65 sites surveyed. Statistical habitat modelling demonstrated that L. pearsoniana was most likely to occur at large streams with mesic midstorey vegetation, as indicated by the presence of palms. Abundance of the species, conditional on presence at a site, increased with increasing stream size. Litoria pearsoniana appears to have recovered from earlier population declines. However, suitability of habitat for the species in extensive areas of public forest may be threatened by cattle grazing, and the associated practices of tree clearing and frequent burning.

Description of the Tadpole of a Stream Breeding Frog, Rana curtipes

Anuran larvae exhibit diverse and ecologically correlated morphological variations (Duellman and Trueb, 1986; Jennings and Scott, 1993; Kaiser and Altig, 1994; de Sa et al., 1997; Lavilla et al., 1997; Santos et al., 1998). The mountain range called in Southern India harbors over 100 species of anurans representing 14 genera (Daniels, 1997a,b,c). However, descriptions of larval morphology of anurans from the Indian subcontinent are scanty (Hiragond and Saidapur, 1999). The larvae of Rana curtipes live in streams and are among the largest anuran tadpoles found in the Western Ghats (Daniels, 1997b) and are poorly described (Rao, 1914; Sekar, 1990). Here we