Spatial and temporal patterns of phenotypic variation in a Neotropical frog

Aim Studies of the spatial and temporal patterns of phenotypic diversity help to elucidate the fine‐scale evolutionary and ecological mechanisms underlying geographical differentiation. The red‐eyed tree frog, Agalychnis callidryas, is a widespread Neotropical frog that exhibits a broad range of polymorphism of coloration and flank‐stripe pattern. The goal of this study was two‐fold: first, to investigate the stability of polymorphisms over a 38‐year period; and second, to evaluate biogeographical hypotheses of diversification between lower Central American populations through quantification of phenotypic diversity on a fine geographical scale. Location This study was conducted at 12 sites across four biogeographical regions in Costa Rica and Panama. Methods We quantified colour, categorized flank‐stripe pattern from digital photos taken during field sampling, and measured body size for each individual. We compared the regional frequency of each flank‐stripe pattern in 2005 with the frequency distribution from a previous study of the same sites in 1967 using logistic regression analyses. We determined the geographical signal of leg coloration by employing linear discriminant function analyses to generate a classification matrix based on covariance similarities, and by comparison of the average hue values within and between regions. Results We found a temporal shift in the frequency of flank‐stripe patterns in three of four regions over 38 years. Based on measures of leg coloration, the frequency distribution of flank‐stripe patterns and body size, we conclude that A. callidryas populations are easily distinguishable at a regional scale. Main conclusions Agalychnis callidryas exhibits regional differentiation in all phenotypic traits measured in this study, supporting the role of three major biogeographical barriers to gene exchange. We found evidence of a putative contact zone between polytypic regions in Costa Rica. In addition, we report temporal instability of the relative frequency of stripe patterns located on the flanks. The ecological and evolutionary mechanisms that may underlie this variation include sexual selection and avoidance of predators.     

Context-dependent reproductive site choice in a Neotropical frog

In organisms whose offspring develop in discrete habitat patchessuch as pools, studies have frequently shown that adults avoidsites based on a single risk factor facing offspring. However,natural reproductive sites often vary in multiple risk factorsin both space and time. In this study, I used choice tests amongfield mesocosms to determine whether adults of a Neotropicalanuran, Edalorhina perezi, select the safest pools for offspringbased on two biotic risks of different magnitude: insect predatorsand conspecific competitors. I also investigated whether adultsite-choice was context dependent (i.e., whether it varied bysex or by season or whether it was based on local pool quality).I found that both sexes avoided pools containing predatory insects,but only females significantly avoided those containing conspecifictadpoles. When offered two risky options, both sexes favoredpools with competitors over those with predators. Site-choicebehavior also varied depending on the temporal and spatial context.Female sensitivity to insect predators decreased late in theseason. In addition, both sexes exhibited dampened reproductiveactivity when only risky sites were available locally. Thisstudy emphasizes that social and environmental factors simultaneouslyimpact reproductive site choice. Whether a site is acceptedultimately depends not only on the assessment of mortality risksto offspring but also on the sex and spatiotemporal contextof the decision maker.     

Environmental drivers of anuran calling phenology in a seasonal Neotropical ecosystem

Temporal variation represents an important component in understanding the structure of ecological communities and species coexistence. We examined calling phenology of an assemblage of anurans in the Gran Chaco ecoregion of Bolivia by deploying automated recording devices to document nocturnally vocalizing amphibians nightly at seven ponds from 20 January 2011 until 31 October 2011. Using logistic regression, we modelled the relationships between temperature, rainfall and photoperiod with calling activity. There was a distinct seasonal effect with calling activity concentrated in the rainy season with no species detected during the dry season from June until the end of October. Calling activity was positively and significantly correlated with photoperiod in 9 of the 10 species analyzed, but there were distinct species‐specific relationships associated with rainfall and temperature. All of these species utilize ephemeral ponds as breeding sites, which can account for their reliance on rainfall as an important driver in calling activity. Two prolonged breeders exhibited similar seasonal breeding patterns across the rainy season, but differed in their response to daily abiotic factors, which might be attributed to the constraints imposed by their reproductive mode. Explosive breeders needed several days of rain to elicit calling. Two pairs of congeners had distinct species‐specific relationships between their calling activity and abiotic factors, even though the congeners shared the same reproductive mode, suggesting that the reproductive modes vary in the constraints imposed on calling activity. The patterns observed suggest that calling phenology of tropical anurans is determined by the interaction of exogenous factors (i.e. climatic variables) and endogenous factors (i.e. reproductive modes).     

Neural correlates of frog calling

Summary A tissue bath incorporating a screen for support of the specimen and an air-lift pump to circulate saline across the screen was designed to provide maximum exposure of isolated frog brainstems ofRana pipiens pipiens to oxygenated saline (Fig. 1). Normal neural correlates of electrically-evoked mating calling were recorded from the region of the pretrigeminal nucleus and the laryngeal nerve in the isolated brainstem (Fig. 3A) and isolated hemi-brainstem (Fig. 2) of the Northern leopard frog. Conspicuous slow-wave activity in the region of the pretrigeminal nucleus supports the possibility that this may be an important integrative area for calling. It appears that the pretrigeminal region is not able, independently, to generate the pulses of the vocal phase of calling. Synchronizing and reinforcing inter-connections between the calling mechanisms of the two sides were identified. The data are summarized in a revised model of mating calling (Fig. 7).This work was supported by NINDS grant NS-06673. The electronic equipment was set up and maintained by Mr. Wayne R. Hudson. I am grateful to Dr. William Van Meter for suggesting the Sylgard for the pinning block and to Dr. Patricia Gallagher for suggesting the saline solution of Phillis and Tebcis.     

Near-synchronous calling in the hip-pocket frog Assa darlingtoni

Sustained perfect synchrony of signal production by animals is unrealistic, but even near-synchronous signalling is extremely rare. Near-synchronous signalling has been documented in some orthopteran insects and fireflies, and one kind of frog. This study provides observations and analyses of sustained bouts of impressive near-synchronous calling by a terrestrial breeding frog from Australia, the hip-pocket frog (Assa darlingtoni). Males called in scattered clusters of several individuals from the rainforest floor of northern New South Wales. In eight of nine pairs of semi-isolated males, there was sustained near-synchronous calling in bouts consisting of 16–20 calls and lasting 5–10 min. There was extensive overlap of the pulsed calls, and calls of a lagging male began overlapping that of a leading male after 2–5 pulses of a leader’s call note. In five pairs, one male’s calls were usually in the leading position; in three pairs, leadership frequently switched between males. In the latter interactions, males frequently skipped a call and produced its next call or calls in the leading position. This tactic has been interpreted as sexual competition between neighbours in orthopterans, but further research is required to rule out possible alternative hypotheses.     

Acoustic interference limits call detection in a Neotropical frog Hyla ebraccata

Problems1999 The Association for the Study of Animal Behaviourassociated with communication in noisy environments include detection, discrimination, and localization of appropriate signals. I investigated the effects of broadband background noise on call detection by female Copyright 1999 The Association for the Study of Animal Behaviour.     

A continental assessment of diurnality in frog calling behaviour

Acoustic signalling is evolutionarily important, influencing sexual selection and serving as a premating isolation mechanism. There is a strong evolutionary basis for acoustic signalling to occur nocturnally across many terrestrial vertebrate groups including mammals, reptiles and amphibians. Within some of these groups, there is a general assumption that ‘most taxa are nocturnal’ in their acoustic signalling, and this is a particularly strongly held view for most frogs. Here we challenge this well-accepted notion by quantifying diurnal calling behaviour in Australian frogs, leveraging a continental-wide citizen science dataset. Of 196 species present in the citizen science dataset, 140 (71%) were recorded at least once during the day. Of the most commonly observed species (i.e. species with at least 150 calls recorded in the database), there were surprisingly high rates of diurnal calling: 14 species had >25% of their calls recorded during the day. We also found that the relative rate of diurnal calling in frogs showed a strong phylogenetic signal, suggesting that the plasticity in calling behaviour as it relates to time of the day is strongly evolutionarily conserved. Our results highlight a suite of ecological and evolutionary questions that are worthy of further investigation.     

Interspecific variation in the phenology of advertisement calling in a temperate Australian frog community

Spatial and temporal partitioning of resources underlies the coexistence of species with similar niches. In communities of frogs and toads, the phenology of advertisement calling provides insights into temporal partitioning of reproductive effort and its implications for community dynamics. This study assessed the phenology of advertisement calling in an anuran community from Melbourne, in southern Australia. We collated data from 1432 surveys of 253 sites and used logistic regression to quantify seasonality in the nightly probability of calling and the influence of meteorological variables on this probability for six species of frogs. We found limited overlap in the predicted seasonal peaks of calling among these species. Those shown to have overlapping calling peaks are unlikely to be in direct competition, due to differences in larval ecology (Crinia signifera and Litoria ewingii) or differences in calling behavior and acoustics (Limnodynastes dumerilii and Litoria raniformis). In contrast, closely related and ecologically similar species (Crinia signfera and Crinia parinsignifera; Litoria ewingii and Litoria verreauxii) appear to have staggered seasonal peaks of calling. In combination with interspecific variation in the meteorological correlates of calling, these results may be indicative of temporal partitioning of reproductive activity to facilitate coexistence, as has been reported for tropical and temperate anurans from other parts of the globe.     

Neural correlates of frog calling. Masculinization by androgens

Neural correlates of mating calling can be recorded from isolated brainstems of male, Northern leopard frogs after the circuits for this behavior have been triggered by electrical stimulation of the preoptic area. Correlates can be evoked reliably and by a stimulus of low amplitude. However, such correlates can be evoked only rarely from female brainstems, and then only by a much larger stimulus. The sensitivity to triggering in female brainstems can be masculinized by previous treatment of the intact frog with testosterone propionate or dihydrotestosterone, but not by estradiol benzoate. This suggests that the action of the androgens is direct and does not require aromatization to estrogens. Comparisons with other studies suggest that the androgen effect may be mainly on posterior parts of the calling circuits (i.e., call pattern generator or motoneurons), rather than on the preoptic area trigger of the generator.     

“Reverse” sexual dichromatism in a Neotropical frog

Sexual dichromatism is widespread among animals, but examples of “reverse” sexual dichromatism, in which females are more brightly colored than males, are extremely rare. We discovered a unique case of reverse sexual dichromatism in the golden rocket frog (Anomaloglossus beebei), a diurnal Neotropical frog. Females are bright “golden” in color, and males are drab tan with brown pigmentation that darkens when they are calling. Here, we document this color variation with calibrated digital photography and further show that there is no evidence for sex‐specific habitat matching; both sexes live in the same well‐lit habitat on green bromeliad leaves. Our results suggest that color variation in this species is an intraspecific signal and provide an important exception to the general expectation that males are more visually conspicuous in species with conventional sex roles.     

Background noise from a natural chorus alters female discrimination of male calls in a Neotropical frog

Many animals communicate in environments with high levels of background noise. Although it is a fundamental prediction of signal detection theory that noise should reduce both detection and discrimination of signals, little is known about these effects in animal communication. Female treefrogs, Hyla ebraccata, in Costa Rica choose mates in large noisy multispecies choruses. We tested gravid females for preferences between computer-synthesized calls with carrier frequencies of 3240 and 2960 Hz (values near the mode and the fifth percentile of the population, respectively) in four levels of background noise from a natural chorus. In the absence of noise (signal/noise ratio >25 dB), females preferred the lower frequency. With moderate signal/noise ratios (6 and 9 dB), they did not discriminate between these frequencies. With low signal/noise ratios (3 dB), females preferred the frequency near the mode for the population. Similar experiments had previously demonstrated that females can detect the presence of a male's calls with signal/noise ratios of 3 dB or greater. Thus moderate levels of natural background sound reduced a female's ability to discriminate between males' calls even when she could detect them. In high levels of background sound, females abandoned discrimination for low-frequency calls and reverted to the task of detecting signals with modal properties for the population. These results justify recent theoretical analyses of the importance of receivers' errors in the evolution of communication.     

Disentangling composite colour patterns in a poison frog species

A phylogenetic approach was performed to infer whether variation in conspicuous colour-patterns of a poison frog (Dendrobatidae: Dendrobates tinctorius ) has evolved neutrally or under selection. Colour and pattern were split into components that were separately analysed and subsequently re-grouped via principal component analysis. This revealed four different 'displayed' factors on the dorsal and lateral views versus one 'concealed' factor on the ventral view. Based on the assumption that current patterns of trait variation contain information about the evolutionary history of the phenotype, we correlated these trait components to a neutrally evolving gene fragment (cytochrome b ). The concealed factor was significantly correlated with the marker fragment, which identified it as having evolved under genetic drift. Noncorrelation of all displayed factors with the marker may indicate the evolution of colour patterns on dorsum and flanks under selection. In our example, colour pattern should therefore be regarded as a multicomponent signal system.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 93 , 433–444.