Oophaga Pumilio Research Articles

Thermal niche variation among individuals of the poison frog, Oophaga pumilio, in forest and converted habitats

AbstractThe conversion of natural habitats to human land uses often increases local temperatures, creating novel thermal environments for species. The variable responses of ectotherms to habitat conversion, where some species decline while others persist, can partly be explained by variation among species in their thermal niches. However, few studies have examined thermal niche variation within species and across forest‐land use ecotones, information that could provide clues about the capacity of species to adapt to changing temperatures. Here, we quantify individual‐level variation in thermal traits of the tropical poison frog, Oophaga pumilio, in thermally contrasting habitats. Specifically, we examined local environmental temperatures, field body temperatures (Tb), preferred body temperatures (Tpref), critical thermal maxima (CTmax), and thermal safety margins (TSM) of individuals from warm, converted habitats and cool forests. We found that frogs from converted habitats exhibited greater mean Tb and Tpref than those from forests. In contrast, CTmax and TSM did not differ significantly between habitats. However, CTmax did increase moderately with increasing Tb, suggesting that changes in CTmax may be driven by microscale temperature exposure within habitats rather than by mean habitat conditions. Although O. pumilio exhibited moderate divergence in Tpref, CTmax appears to be less labile between habitats, possibly due to the ability of frogs in converted habitats to maintain their Tb below air temperatures that reach or exceed CTmax. Selective pressures on thermal tolerances may increase, however, with the loss of buffering microhabitats and increased frequency of extreme temperatures expected under future habitat degradation and climate warming.Abstract in Spanish is available with online material.

Assessing the role of habitat and species interactions in the population decline and detection bias of Neotropical leaf litter frogs in and around La Selva Biological Station, Costa Rica

Worldwide, amphibian populations have been declining rapidly. This decline can be attributed to many factors including climate change, pesticide exposure, and emerging infectious diseases, among other important factors, but few studies have examined the influence of species interactions. In this study, we examined how habitat factors and co-occurring avian and mammalian species, as well as humans, exert direct and indirect effects on Neotropical amphibian population dynamics. We further examined how these habitat and species interactions could affect our ability to reliably detect amphibian presence to robustly estimate population trends. We conducted amphibian visual encounter surveys at 26 randomly selected sites in the La Selva Biological Station, in northeastern Costa Rica, as well as 26 sites across five additional forest fragments in the region. Furthermore, we used camera traps to collect data on avian and mammalian communities and human visitation at those amphibian survey plots. From these data, we were able to estimate species occupancy probabilities for leaf litter frogs across sites and their relationships to habitat and interspecific species interaction covariates. We also conducted an experiment with plastic model frogs to estimate detection probabilities when a population is known to occur at a site with certainty. Our results suggested that strawberry poison dart frog (Oophagapumilio) occupancy was positively related to secondary forest and their detection was negatively related to increasing air temperatures at the times of the surveys. Leaf litter frog occupancy was negatively related to core La Selva sites and human detections at sites, yet their detection was positively related to human trail presence, which might be related to reduced leaf litter cover due to heavy trampling. Our experimental surveys suggested that Neotropical leaf litter frog communities are difficult to detect when present and future studies should explicitly account for this detection bias to effectively monitor population trends.

Experimental evidence for maternal provisioning of alkaloid defenses in a dendrobatid frog

Dendrobatid frogs sequester alkaloid defenses from dietary arthropods. Here, we provide experimental evidence that mother strawberry poison frogs (Oophaga pumilio) provision alkaloids to tadpoles. Captive-raised females were fed the synthetic alkaloid decahydroquinoline (DHQ), which we subsequently quantified in their skin, eggs, and developing tadpoles. DHQ quantity was positively associated with tadpole mass/development, suggesting high sequestration rates by tadpoles. These data confirm that tadpoles obtain nutrition and alkaloids by feeding exclusively on maternally provisioned eggs.

Nursery crowding does not influence offspring, but might influence parental, fitness in a phytotelm-breeding frog

One way parents shape the fitness prospects of their offspring is by providing a nursery. When parents divide a brood across several nurseries, they must assess not only the costs and benefits of multiple nurseries, but also the optimal proportion of the brood to deposit in each. Here, we explored the factors shaping these decisions in the strawberry poison frog (Oophaga pumilio), a species that typically, but not always, deposits its offspring singly in small phytotelmata. By monitoring occupancy and tadpole success in an artificial phytotelm array used by a free-living population, we tested for preferences for nursery size and height, asked whether multi-tadpole deposition was non-random with respect to these factors, and assessed the fitness consequences of these decisions. Parents were equally likely to use all types of artificial phytotelmata, but multi-tadpole depositions occurred almost exclusively in large nurseries. The probability that a tadpole would complete metamorphosis was unrelated to the physical characteristics of the rearing site, and individual tadpole survival was equivalent regardless of whether the nursery held one, two, or three tadpoles. Multi-tadpole nurseries were more likely, therefore, to have one occupant surviving to independence (metamorphosis). Although tadpoles are usually deposited alone, O. pumilio mothers may benefit from the insurance function played by additional tadpoles in a nursery. While most animals that care for their young provide a single nursery for their entire brood, a few separate and rear each brood member in an individual nursery. In such cases, parents must decide not only which nurseries to use, but also how many young they should deposit into each. Here, we explore the factors shaping these decisions in the strawberry poison frog (Oophaga pumilio), a species that typically, but not always, rears its young individually in small water-filled leaf axils. While O. pumiliodo not appear to choose nurseries based on size, parents were more likely to deposit multiple tadpoles into larger nurseries. Additionally, because the number of tadpoles in a nursery did not influence likelihood of metamorphic success for each individual, nurseries that contained multiple tadpoles were more likely to produce at least one offspring that completed metamorphosis. These results highlight the fitness effects of plasticity in reproductive strategies, and the possibility of divergent parent and offspring fitness optima.

Mate Choice versus Mate Preference: Inferences about Color-Assortative Mating Differ between Field and Lab Assays of Poison Frog Behavior.

Codivergence of mating traits and mate preferences can lead to behavioral isolation among lineages in early stages of speciation. However, mate preferences limit gene flow only when expressed as mate choice, and numerous factors might be more important than preferences in nature. In the extremely color polytypic strawberry poison frog (Oophaga pumilio), female mate preferences have codiverged with color in most allopatric populations tested. Whether these lab-assayed preferences predict mating (gene flow) in the wild remains unclear. We observed courting pairs in a natural contact zone between red and blue lineages until oviposition or courtship termination. We found color-assortative mating in a disturbed habitat with high population density but not in a secondary forest with lower density. Our results suggest color-assortative O. pumilio mate choice in the wild but also mating patterns that do not match those predicted by lab-assayed preferences.

Differential responses to forest edges among populations of Oophaga pumilio (Anura: Dendrobatidae) from Panama

Differential responses to forest edges among populations of Oophaga pumilio (Anura: Dendrobatidae) from Panama. As habitat fragmentation increasingly becomes a prevalent feature in tropical systems, investigating how such novel features affect the distribution of species is of vital importance for understanding species’ ecology and conservation concerns. Species that show interpopulation variation in features that may affect their ecology (i.e., coloration) should be of high priority for elucidating the effects fragmentation may have. It is possible that these features unique to certain populations could promote or constrain the population’s ability to adapt to change. I investigated nine populations of the Strawberry Poison Frog (Oophaga pumilio) throughout the Bocas del Toro archipelago in Panama. By running transects from forest edge into interior forest, I assessed both population density and individual distance from forest edge for each population. One population was signifcantly denser than six of the other eight populations. Three populations showed increased numbers farther from forest edges while six populations showed no variation. This research highlights how reactions to habitat fragmentation may be population specifc, possibly linked to physical traits of individuals within the population. This research suggests that high interpopulation variation should be taken into account when examining species’ reactions to environmental perturbations.

Behavioural preference for low levels of UV-B radiation in two neotropical frog species from Costa Rica

Abstract:Tropical frogs experience damaging effects from exposure to UV-B radiation, and some diurnally active, conspicuous species exhibit avoidance behaviours to high levels of UV-B. To determine if similar behaviours are present in other diurnal frogs, we experimentally compared UV-B avoidance in two common species of neotropical diurnal frogs –Oophaga pumilio, an aposematic poison frog andCraugastor bransfordii, a cryptic leaf-litter frog – in response to different levels of UV-B. Wild-caught frogs were tested in experimental arenas fitted with filters that permitted two different levels of UV-B (low: 14% vs. high: 84% UV-B). Both species spent significantly more time under the low UV-B filter, suggesting that behavioural preferences for lower levels of UV-B are common to different diurnal species. Furthermore, maleO. pumiliosignificantly preferred lower levels of UV-B, whereas females did not exhibit a preference for lower UV-B, which may suggest differences in UV-B exposure or sensitivity and/or alternative mechanism(s) to avoid UV-B between sexes. Although limited in scope, the findings of our study suggest that UV-B avoidance may be a behavioural adaptation common to all diurnal frogs.

Sodium ion channel alkaloid resistance does not vary with toxicity in aposematic Dendrobates poison frogs: An examination of correlated trait evolution.

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.

Spatial patterns of the frog Oophaga pumilio in a plantation system are consistent with conspecific attraction.

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 homogenous Theobroma cacao plantation, 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 migrant O. pumilio by 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 resident O. pumilio is 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.

Sequestered Alkaloid Defenses in the Dendrobatid Poison Frog Oophaga pumilio Provide Variable Protection from Microbial Pathogens.

Most amphibians produce their own defensive chemicals; however, poison frogs sequester their alkaloid-based defenses from dietary arthropods. Alkaloids function as a defense against predators, and certain types appear to inhibit microbial growth. Alkaloid defenses vary considerably among populations of poison frogs, reflecting geographic differences in availability of dietary arthropods. Consequently, environmentally driven differences in frog defenses may have significant implications regarding their protection against pathogens. While natural alkaloid mixtures in dendrobatid poison frogs have recently been shown to inhibit growth of non-pathogenic microbes, no studies have examined the effectiveness of alkaloids against microbes that infect these frogs. Herein, we examined how alkaloid defenses in the dendrobatid poison frog, Oophaga pumilio, affect growth of the known anuran pathogens Aeromonas hydrophila and Klebsiella pneumoniae. Frogs were collected from five locations throughout Costa Rica that are known to vary in their alkaloid profiles. Alkaloids were isolated from individual skins, and extracts were assayed against both pathogens. Microbe subcultures were inoculated with extracted alkaloids to create dose-response curves. Subsequent spectrophotometry and cell counting assays were used to assess growth inhibition. GC-MS was used to characterize and quantify alkaloids in frog extracts, and our results suggest that variation in alkaloid defenses lead to differences in inhibition of these pathogens. The present study provides the first evidence that alkaloid variation in a dendrobatid poison frog is associated with differences in inhibition of anuran pathogens, and offers further support that alkaloid defenses in poison frogs confer protection against both pathogens and predators.

Male-male aggression is unlikely to stabilize a poison frog polymorphism.

Phenotypic polymorphism is common in animals, and the maintenance of multiple phenotypes in a population requires forces that act against homogenizing drift and selection. Male-male competition can contribute to the stability of a polymorphism when males compete primarily with males of the same phenotype. In and around a contact zone between red and blue lineages of the poison frog Oophaga pumilio, we used simulated territorial intrusions to test the nonexclusive predictions that males would direct more aggression towards males of (i) their own phenotype and/or (ii) the phenotype that is most common in their population. Males in the monomorphic red and blue populations that flank the contact zone were more aggressive towards simulated intruders that matched the local coloration. However, males in the two polymorphic populations biased aggression towards neither their own colour nor the colour most common in their population. In sympatry, the rarer colour morph gains no advantage via reduced male-male aggression from territorial males in these O.pumilio populations, and so male aggression seems unlikely to stabilize colour polymorphism on its own. More broadly, these results suggest that the potential for divergent male aggression biases to maintain phenotypic diversity depends on the mechanism(s) that generate the biases and the degree to which these mechanisms persist in sympatry.

Empirical evidence for multiple costs of begging in poison frog tadpoles

In recent decades, theoretical and empirical work has investigated the relative roles of costs and benefits in inhibiting excessive displays of begging to parents. Whether costs are important in maintaining reliability of offspring signals is still debated, in part because empirical evidence for costs is conflicting. Nearly 90% of empirical studies have focused on birds. Costs may differ between birds and other animal groups, but more information is needed about non-avian systems. In this study, we tested for evidence of costs of begging in an anuran, Oophaga pumilio, in which tadpoles vibrate vigorously against mother frogs to solicit nutritive eggs. First, we tested whether a realistic manipulation of begging effort affected tadpole growth over two weeks, and found evidence for such physiological costs. Second, we tested whether the presence of a natural predator would alter begging behavior. Tadpoles begged when hungry, but begged significantly less when both hungry and viewing a spider, suggesting that they have evolved to reduce potential costs of predation risk when begging. Thus, we demonstrate the first example of costs via both physiological expenditure and predation risk in a non-avian species. Unlike most birds which rear offspring in clutches, O. pumilio mothers rear tadpoles in individual sites, suggesting that in the absence of sibling effects, multiple costs of begging work concomitantly to prevent the expression and evolution of excessive or indiscriminate signaling. Future studies of begging from a comparative perspective will continue to augment our understanding of the mechanisms behind the evolution of parent-offspring communication.

Mating status correlates with dorsal brightness in some but not all poison frog populations.

Sexual signals are important for intraspecific communication and mate selection, but their evolution may be driven by both natural and sexual selection, and stochastic processes. Strawberry poison frogs (Oophaga pumilio) show strong color divergence among populations, but coloration also varies among individuals of the same population. The importance of coloration for female mate choice has been studied intensely, and sexual selection seems to affect color divergence in strawberry poison frogs. However, the effect of coloration on mating success under field conditions has received very little attention. Furthermore, few studies examined how phenotypic variation among individuals of the same color morph affects mate selection under natural conditions. We measured the spectral reflectance of courting and noncourting individuals and their background substrates in three geographically separated populations. In one population (Sarapiquí, Costa Rica), we found that naturally occurring courting pairs of males and females had significantly brighter dorsal coloration than individual males and females not engaged in courtship interactions. Our field observations suggest that, in the wild, females prefer brighter males while the reason for the higher courtship activity of brighter females remains unclear. Overall our results imply that brightness differences among individuals of the same color morph may actually affect reproductive success in some populations of strawberry poison frogs.

Complete Genome Sequence of Frog virus 3 , Isolated from a Strawberry Poison Frog ( Oophaga pumilio ) Imported from Nicaragua into the Netherlands

ABSTRACTFrog virus 3 was isolated from a strawberry poison frog (Oophaga pumilio) imported from Nicaragua via Germany to the Netherlands, and its complete genome sequence was determined. Frog virus 3 isolate Op/2015/Netherlands/UU3150324001 is 107,183 bp long and has a nucleotide similarity of 98.26% to the reference Frog virus 3 isolate.

The effects of background coloration and dark spots on the risk of predation in poison frog models

Protective coloration is a well-known predator avoidance strategy in prey species. Aposematic species often display a contrasting color pattern consisting of dark spots of different shapes and sizes on a bright background coloration. Both elements, background color and spots are expected to serve different purposes. While the ecological function of the bright coloration has been addressed in many studies, the question of whether the interaction with differently sized spots influences predator behavior has received less attention by researchers. In a lowland rain forest in Costa Rica we used 2700 clay models that imitated the polytypic strawberry poison frog (Oophaga pumilio) as a proxy for an aposematic prey species. We manipulated the dorsal color pattern by using a local and a non-local aposematic and a non-local cryptic background color and combined them with black spots increasing in size (none, small, medium, large). The major objective was to test if spot size alters the survival rate of differently colored models. Background coloration and spot size were significant predictors of being attacked. However, the interaction between both effects was not. During five trials predators avoided the non-local aposematic color morph and did not discriminate between local aposematic and non-local cryptic models. Spot size and attack rate were negatively linear correlated which suggests that predator selection promotes the evolution of dark spots. We further conclude that spot size matters in a contrasting color pattern and plays an important role in predator avoidance.

Tadpole begging reveals high quality

Parents can benefit from allocating limited resources nonrandomly among offspring, and offspring solicitation (i.e. begging) is often hypothesized to evolve because it contains information valuable to choosy parents. We tested the predictions of three 'honest begging' hypotheses - Signal of Need, Signal of Quality and Signal of Hunger - in the tadpoles of a terrestrial frog (Oophaga pumilio). In this frog, mothers provision tadpoles with trophic eggs, and when mothers visit, tadpoles perform a putative begging signal by stiffening their bodies and vibrating rapidly. We assessed the information content of intense tadpole begging with an experimental manipulation of tadpole condition (need/quality) and food deprivation (hunger). This experiment revealed patterns consistent with the Signal of Quality hypothesis and directly counter to predictions of Signal of Need and Signal of Hunger. Begging effort and performance were higher in more developed and higher condition tadpoles and declined with food deprivation. Free-living mothers were unlikely to feed tadpoles of a nonbegging species experimentally cross-fostered with their own, and allocated larger meals to more developed tadpoles and those that vibrated at higher speed. Mother O.pumilio favour their high-quality young, and because their concurrent offspring are reared in separate nurseries, must do so by making active allocation decisions. Our results suggest that these maternal choices are based at least in part on offspring signals, indicating that offspring solicitation can evolve to signal high quality.

Ineffectiveness of Call Surveys for Estimating Population Size in a Widespread Neotropical Frog,Oophaga pumilio

Abstract Call surveys offer a valuable method to monitor anuran populations attributable to their temporal breeding habits and close association with water. Many temperate locations have adopted citizen science programs to monitor local anuran populations using call surveys and road transects. These surveys, however, are not commonly conducted in the tropics. I tested use of call surveys for estimating population density of a small terrestrial poison frog, Oophaga pumilio, in six different populations in Bocas del Toro, Panama. By conducting three-minute call surveys, and searching for all individual frogs in a 10 m radius of the survey point, I directly compared the number of calling males to the observed number of frogs in a given area. I found call density to be a poor predictor of population density. Despite there being differences in population densities, the lack of a relationship between the number of calls and population density highlights the limited use for call surveys for terrestrial, territor...

Variable Alkaloid Defenses in the Dendrobatid Poison Frog Oophaga pumilio are Perceived as Differences in Palatability to Arthropods.

Conspicuously colored dendrobatid frogs sequester alkaloid defenses from dietary arthropods, resulting in considerable alkaloid variation among populations; however, little is known about how variation is perceived as a defense against predators. Previous studies have found variable alkaloids in the dendrobatid Oophaga pumilio to be associated with differences in toxicity to laboratory mice, suggesting variable defenses are important. Arthropods are natural predators that use chemoreception to detect prey, including frogs, and may therefore perceive variation in alkaloid profiles as differences in palatability. The goal of the present study is to determine how arthropods respond to variable alkaloid defenses in O. pumilio. Frog alkaloids were sampled from individual O. pumilio from ten geographic locations throughout the Bocas del Toro region of Panama and the Caribbean coast of Costa Rica. Alkaloid extracts were used in feeding bioassays with the vinegar fly Drosophila melanogaster and the ant Ectatomma ruidum. Both species of arthropods fed significantly less on frog alkaloid extracts when compared to controls, and differences in alkaloid palatability were observed among frog populations, as well as between sexes and life stages within a population. Differences in alkaloid quantity, richness, and type were the main predictors of arthropod palatability. Our findings also represent the first direct evidence of a palatability spectrum in a vertebrate that sequesters chemical defenses from dietary sources. Further, the presence of a palatability spectrum suggests that variable alkaloid defenses in O. pumilio are ecologically relevant and play an important role in natural predator-prey interactions, particularly with respect to arthropod predators.

Escape behaviour of aposematic (Oophaga pumilio) and cryptic (Craugastor sp.) frogs in response to simulated predator approach

Abstract:Crypsis and aposematism are common antipredator strategies that can each be coupled with behaviours that maximize predator deterrence or avoidance. Cryptic animals employ camouflage to conceal themselves within their environment and generally rely on immobility to avoid detection by predators. Alternatively, aposematic animals tend to rely on an association between conspicuous colouration and secondary defence to deter potential predators, and tend to exhibit slow movements in response to predators. The goal of the present study was to determine how cryptic Craugastor sp. and aposematic Oophaga pumilio respond to simulated human and bird model predators. Oophaga pumilio responded more often with movement to both the human (17/22) and bird (9/25) predators than Craugastor sp. (human: 2/21; bird: 0/21). The increased movement resulted in a greater average flight initiation distance, latency to move, and distance fled in O. pumilio. These findings suggest that cryptic Craugastor sp. rely on immobility to avoid detection, whereas aposematic O. pumilio utilize movement, possibly as a mechanism to increase the visibility of their warning signals to potential predators. Furthermore, O. pumilio exhibited greater movement in response to humans, suggesting that they actively avoid trampling by large threats, rather than considering them predators.

Developmental morphology of granular skin glands in pre-metamorphic egg-eating poison frogs

Parents in many taxa, including insects, molluscs, fish, snakes, and amphibians provision chemical defences, such as peptides, steroids, or alkaloids to their offspring to reduce the risk of predation. In most cases, those defences are transferred to offspring in the egg and gradually diminish throughout the larval period. Adult poison frogs sequester alkaloid-based defences from arthropod prey in granular skin glands. In at least one poison frog, Oophaga pumilio, mother frogs intermittently feed tadpoles until metamorphosis with nutritive eggs containing those alkaloid-based defences. However, alkaloids are not detected in tadpoles until they reach the middle stages of larval development. Here, we investigate the histology of a developmental series of O. pumilio tadpoles to determine whether their ontogenetic alkaloid profile coincides with granular gland development. Our findings suggest that alkaloid sequestration in tadpoles is delineated by the differentiation of rudimentary granular skin glands in epithelial tissue. The timing of differentiation of granular glands in this species coincides with other anurans. Thus, provisioning of chemical defences to offspring is likely constrained by developmental timing of derived structures that can effectively store those toxic or noxious compounds.