Concept: Poison dart frog
BACKGROUND: Females have often been shown to exhibit preferences for certain male traits. However, little is known about behavioural rules females use when searching for mates in their natural habitat. We investigated mate sampling tactics and related costs in the territorial strawberry poison frog (Oophaga pumilio) possessing a lek-like mating system, where both sequential and simultaneous sampling might occur. We continuously monitored the sampling pattern and behaviour of females during the complete period between two successive matings. RESULTS: We found no evidence that females compared males by visiting them. Instead females mated with the closest calling male irrespective of his acoustic and physical traits, and territory size. Playback experiments in the natural home ranges of receptive females revealed that tested females preferred the nearest speaker and did not discriminate between low and high call rates or dominant frequencies. CONCLUSIONS: Our results suggest that females of O. pumilio prefer the closest calling male in the studied population. We hypothesize that the sampling tactic in this population is affected by 1) a strongly female biased sex ratio and 2) a low variance in traits of available males due to strong male-male competition, preventing low quality males from defending a territory and mating.
Understanding the external stimuli and natural contexts that elicit complex behaviors, such as parental care, is key in linking behavioral mechanisms to their real-life function. Poison frogs provide obligate parental care by shuttling their tadpoles from terrestrial clutches to aquatic nurseries, but little is known about the proximate mechanisms that control these behaviors. In this study, we used Allobates femoralis, a poison frog with predominantly male parental care, to investigate whether tadpole transport can be induced in both sexes by transferring unrelated tadpoles to the backs of adults in the field. Specifically, we asked if the presence of tadpoles on an adult’s back can override the decision-making rules preceding tadpole pick-up and induce the recall of spatial memory necessary for finding tadpole deposition sites. We used telemetry to facilitate accurate tracking of individual frogs and spatial analyses to compare movement trajectories. All tested individuals transported their foster-tadpoles to water pools outside their home area. Contrary to our expectation, we found no sex difference in the likelihood to transport nor in the spatial accuracy of finding tadpole deposition sites. We reveal that a stereotypical cascade of parental behaviors that naturally involves sex-specific offspring recognition strategies and the use of spatial memory can be manipulated by experimental placement of unrelated tadpoles on adult frogs. As individuals remained inside their home area when only the jelly from tadpole-containing clutches was brushed on the back, we speculate that tactile rather than chemical stimuli are triggering these parental behaviors.
Animals relying on uncertain, ephemeral and patchy resources have to regularly update their information about profitable sites. For many tropical amphibians, widespread, scattered breeding pools constitute such fluctuating resources. Among tropical amphibians, poison frogs (Dendrobatidae) exhibit some of the most complex spatial and parental behaviors-including territoriality and tadpole transport from terrestrial clutches to ephemeral aquatic deposition sites. Recent studies have revealed that poison frogs rely on spatial memory to successfully navigate through their environment. This raises the question of when and how these frogs gain information about the area and suitable reproductive resources. To investigate the spatial patterns of pool use and to reveal potential explorative behavior, we used telemetry to follow males of the territorial dendrobatid frog Allobates femoralis during tadpole transport and subsequent homing. To elicit exploration, we reduced resource availability experimentally by simulating desiccated deposition sites. We found that tadpole transport is strongly directed towards known deposition sites and that frogs take similar direct paths when returning to their home territory. Frogs move faster during tadpole transport than when homing after the deposition, which probably reflects different risks and costs during these two movement phases. We found no evidence for exploration, neither during transport nor homing, and independent of the availability of deposition sites. We suggest that prospecting during tadpole transport is too risky for the transported offspring as well as for the transporting male. Relying on spatial memory of multiple previously discovered pools appears to be the predominant and successful strategy for the exploitation of reproductive resources in A. femoralis. Our study provides for the first time a detailed description of poison frog movement patterns during tadpole transport and corroborates recent findings on the significance of spatial memory in poison frogs. When these frogs explore and discover new reproductive resources remains unknown.
Complex phenotypes typically have a correspondingly multifaceted genetic component. However, the genotype-phenotype association between chemical defense and resistance is often simple: genetic changes in the binding site of a toxin alter how it affects its target. Some toxic organisms, such as poison frogs (Anura: Dendrobatidae), have defensive alkaloids that disrupt the function of ion channels, proteins that are crucial for nerve and muscle activity. Using protein-docking models, we predict that three major classes of poison frog alkaloids (histrionicotoxins, pumiliotoxins, and batrachotoxins) bind to similar sites in the highly conserved inner pore of the muscle voltage-gated sodium channel, Nav1.4. We predict that poison frogs are somewhat resistant to these compounds because they have six types of amino acid replacements in the Nav1.4 inner pore that are absent in all other frogs except for a distantly-related alkaloid-defended frog from Madagascar, Mantella aurantiaca. Additional protein-docking models and comparative phylogenetics support the role of these replacements in alkaloid resistance. Taking into account the four independent origins of chemical defense in Dendrobatidae, phylogenetic patterns of the amino acid replacements suggest that (1) alkaloid resistance evolved independently at least seven times in these frogs, (2) variation in resistance-conferring replacements is likely a result of differences in alkaloid exposure across species, and (3) functional constraint shapes the evolution of the Nav1.4 inner pore. Our study is the first to demonstrate the genetic basis of autoresistance in frogs with alkaloid defenses.
Natural selection is widely noted to drive divergence of phenotypic traits. Predation pressure can facilitate morphological divergence, for example the evolution of both cryptic and conspicuous coloration in animals. In this context Dendrobatid frogs have been used to study evolutionary forces inducing diversity in protective coloration. The polytypic strawberry poison frog (Oophaga pumilio) shows strong divergence in aposematic coloration among populations. To investigate whether predation pressure is important for color divergence among populations of O. pumilio we selected four mainland populations and two island populations from Costa Rica and Panama. Spectrometric measurements of body coloration were used to calculate color and brightness contrasts of frogs as an indicator of conspicuousness for the visual systems of several potential predators (avian, crab and snake) and a conspecific observer. Additionally, we conducted experiments using clay model frogs of different coloration to investigate whether the local coloration of frogs is better protected than non-local color morphs, and if predator communities vary among populations. Overall predation risk differed strongly among populations and interestingly was higher on the two island populations. Imprints on clay models indicated that birds are the main predators while attacks of other predators were rare. Furthermore, clay models of local coloration were equally likely to be attacked as those of non-local coloration. Overall conspicuousness (and brightness contrast) of local frogs was positively correlated with attack rates by birds across populations. Together with results from earlier studies we conclude that conspicuousness honestly indicates toxicity to avian predators. The different coloration patterns among populations of strawberry poison frogs in combination with behavior and toxicity might integrate into equally efficient anti-predator strategies depending on local predation and other ecological factors.
Spatial heterogeneity in the strength or agents of selection can lead to geographic variation in ecologically important phenotypes. Many dendrobatid frogs sequester alkaloid toxins from their diets and often exhibit fixed mutations at NaV1.4, a voltage-gated sodium ion channel associated with alkaloid toxin resistance. Yet previous studies have noted an absence of resistance mutations in individuals from several species known to sequester alkaloid toxins, suggesting possible intraspecific variation for alkaloid resistance in these species. Toxicity and alkaloid profiles vary substantially between populations in several poison frog species (genus Dendrobates) and are correlated with variation in a suite of related traits such as aposematic coloration. If resistance mutations are costly, due to alterations of channel gating properties, we expect that low toxicity populations will have reduced frequencies and potentially even the loss of resistance alleles. Here, we examine whether intraspecific variation in toxicity in three dendrobatid frogs is associated with intraspecific variation in alleles conferring toxin resistance. Specifically, we examine two species that display marked variation in toxicity throughout their native ranges (Dendrobates pumilio and D. granuliferus) and one species with reduced toxicity in its introduced range (D. auratus). However, we find no evidence for population-level variation in alkaloid resistance at NaV1.4. In fact, contrary to previous studies, we found that alkaloid resistance alleles were not absent in any populations of these species. All three species exhibit fixed alkaloid resistance mutations throughout their ranges, suggesting that these mutations are maintained even when alkaloid sequestration is substantially reduced.
Most animals move in dense habitats where distant landmarks are limited, but how they find their way around remains poorly understood. Poison frogs inhabit the rainforest understory where they shuttle tadpoles from small territories to widespread pools. Recent studies revealed their excellent spatial memory and the ability to home back from several hundred meters. It remains unclear if this homing ability is restricted to the areas that had been previously explored or if it allows the frogs to navigate from areas outside their direct experience. Here we used radio-tracking to study the navigational performance of three-striped poison frog translocated outside the area of their routine movements (200 - 800 m). Translocated frogs returned to their home territory via a direct path from all distances and with little difference in orientation accuracy, suggesting a flexible map-like navigation mechanism. These findings challenge our current understanding of mechanisms and the sensory basis of amphibian orientation.
Poison frogs sequester chemical defenses from arthropod prey, although the details of how arthropod diversity contributes to variation in poison frog toxins remains unclear. We characterized skin alkaloid profiles in the Little Devil poison frog, Oophaga sylvatica (Dendrobatidae), across three populations in northwestern Ecuador. Using gas chromatography/mass spectrometry, we identified histrionicotoxins, 3,5- and 5,8-disubstituted indolizidines, decahydroquinolines, and lehmizidines as the primary alkaloid toxins in these O. sylvatica populations. Frog skin alkaloid composition varied along a geographical gradient following population distribution in a principal component analysis. We also characterized diversity in arthropods isolated from frog stomach contents and confirmed that O. sylvatica specialize on ants and mites. To test the hypothesis that poison frog toxin variability reflects species and chemical diversity in arthropod prey, we (1) used sequencing of cytochrome oxidase 1 to identify individual prey specimens, and (2) used liquid chromatography/mass spectrometry to chemically profile consumed ants and mites. We identified 45 ants and 9 mites in frog stomachs, including several undescribed species. We also showed that chemical profiles of consumed ants and mites cluster by frog population, suggesting different frog populations have access to chemically distinct prey. Finally, by comparing chemical profiles of frog skin and isolated prey items, we traced the arthropod source of four poison frog alkaloids, including 3,5- and 5,8-disubstituted indolizidines and a lehmizidine alkaloid. Together, the data show that toxin variability in O. sylvatica reflects chemical diversity in arthropod prey.
Ambient ultraviolet-B radiation can harm amphibian eggs, larvae and adults. However, some amphibians avoid UV-B radiation when given the opportunity. The strawberry poison dart frog, Oophaga pumilio, is diurnal and males vocalize throughout the day in light gaps under forest canopies that expose them to solar radiation. Previous studies have demonstrated that males calling from high perches are more successful at mating than those at lower perches. We investigated whether frogs at higher perches receive more ultraviolet-B than those calling from lower perches. We also investigated whether frogs on perches receiving relatively low ultraviolet-B levels maintained their positions for longer compared to individuals calling from perches receiving higher levels of ultraviolet-B. Finally, since it has been hypothesized that some animals utilize levels of UV-A as a visual cue to avoid UV-B damage, we artificially elevated ultraviolet-A levels to examine whether males exposed to artificially elevated ultraviolet-A abandoned their perches sooner compared to males exposed to visible light. We found that frogs called from perches receiving low ultraviolet-B regardless of perch height, and that frogs maintain their positions longer on perches receiving low ultraviolet-B compared to perches receiving even slightly higher ultraviolet-B levels. Exposing the frogs to artificially elevated levels of ultraviolet-A radiation caused males to move off of their perches faster than when they were exposed to a control light source. These experiments suggest that ultraviolet radiation plays an important role in frog behavior related to perch selection, even in rainforests where much of the solar radiation is shielded by the forest canopy.
The conspecific attraction hypothesis predicts that individuals are attracted to conspecifics because conspecifics may be cues to quality habitat and/or colonists may benefit from living in aggregations. Poison frogs (Dendrobatidae) are aposematic, territorial, and visually oriented-three characteristics which make dendrobatids an appropriate model to test for conspecific attraction. In this study, we tested this hypothesis using an extensive mark-recapture dataset of the strawberry poison frog (Oophaga pumilio) from La Selva Biological Station, Costa Rica. Data were collected from replicate populations in a relatively homogenousTheobroma cacaoplantation, which provided a unique opportunity to test how conspecifics influence the spatial ecology of migrants in a controlled habitat with homogenous structure. We predicted that (1) individuals entering a population would aggregate with resident adults, (2) migrants would share sites with residents at a greater frequency than expected by chance, and (3) migrant home ranges would have shorter nearest-neighbor distances (NND) to residents than expected by chance. The results were consistent with these three predictions: Relative to random simulations, we observed significant aggregation, home-range overlap, and NND distribution functions in four, five, and six, respectively, of the six migrant-resident groups analyzed. Conspecific attraction may benefit migrantO. pumilioby providing cues to suitable home sites and/or increasing the potential for social interactions with conspecifics; if true, these benefits should outweigh the negative effects of other factors associated with aggregation. The observed aggregation between migrant and residentO. pumiliois consistent with conspecific attraction in dendrobatid frogs, and our study provides rare support from a field setting that conspecific attraction may be a relevant mechanism for models of anuran spatial ecology.