Neotropical Poison Frogs Research Articles

Phylogenomic Reconstruction of the Neotropical Poison Frogs (Dendrobatidae) and Their Conservation

The evolutionary history of the Dendrobatidae, the charismatic Neotropical poison frog family, remains in flux, even after a half-century of intensive research. Understanding the evolutionary relationships between dendrobatid genera and the larger-order groups within Dendrobatidae is critical for making accurate assessments of all aspects of their biology and evolution. In this study, we provide the first phylogenomic reconstruction of Dendrobatidae with genome-wide nuclear markers known as ultraconserved elements. We performed sequence capture on 61 samples representing 33 species across 13 of the 16 dendrobatid genera, aiming for a broadly representative taxon sample. We compare topologies generated using maximum likelihood and coalescent methods and estimate divergence times using Bayesian methods. We find most of our dendrobatid tree to be consistent with previously published results based on mitochondrial and low-count nuclear data, with notable exceptions regarding the placement of Hyloxalinae and certain genera within Dendrobatinae. We also characterize how the evolutionary history and geographic distributions of the 285 poison frog species impact their conservation status. We hope that our phylogeny will serve as a backbone for future evolutionary studies and that our characterizations of conservation status inform conservation practices while highlighting taxa in need of further study.

Oviposition and father presence reduce clutch cannibalism by female poison frogs

BackgroundThe consumption of conspecific young by adult individuals is a common phenomenon across various animal taxa. Possible adaptive benefits of such behaviour include the acquisition of nutrients, decreased competition for one’s own offspring, and/or increased mating opportunities. Clutch cannibalism has occasionally been observed in several species of Neotropical poison frogs, but the circumstances under which this behaviour occurs has rarely been investigated experimentally. Recent experiments with the poison frog Allobates femoralis have shown that males indiscriminately transport all clutches located inside their own territory to bodies of water, but become highly cannibalistic when taking over a new territory. Females are able to indirectly discriminate between their own and foreign clutches by location and take over transport duties of their own clutches only in the absence of the father. Cannibalism by A. femoralis females has not been previously observed. We thus asked if, and under which circumstances, cannibalism of unrelated clutches by female A. femoralis would occur, by manipulating the presence of the clutch’s father, the female’s own reproductive state, and the female’s familiarity with the environment.ResultsFemales clearly cannibalize foreign clutches. Cannibalism was most pronounced when the female had not recently produced her own clutch and the father of the foreign clutch was absent. The female’s familiarity with the area had no significant influence on the likelihood of cannibalism to occur.ConclusionsOur data indicate that both previous oviposition and the father’s presence reduce cannibalistic behaviour in A. femoralis females. Cannibalistic females may gain nutritional benefits or enhanced inclusive fitness by preying on other females’ offspring. The finding that the father’s presence at the clutch site/territory was sufficient to reduce cannibalism by females suggests a prominent role of male territoriality for the evolution of male parental care.

Poison frogs, defensive alkaloids, and sleepless mice: critique of a toxicity bioassay

In studies of defensive allomones, appropriate methods of presenting chemicals and measuring their deterrent effects on consumers are essential for understanding the contributions that chemicals make to the survivorship of potential prey. However, unnatural chemical presentations and/or ambiguous bioassay responses occasionally have left open questions on some allelochemical effects. This discussion critiques a toxicity bioassay of Neotropical poison frogs (Dendrobatidae), a group whose skins are known to possess a diverse array of bioactive alkaloids. The problematic bioassay entails injecting laboratory mice with the skin extracts of frogs and monitoring the time taken for mice to fall back to sleep to estimate extract toxicity, where longer latencies of sleep onset were claimed to reflect greater toxicity. Dendrobatids do not invasively deliver skin alkaloids to offenders, hence the method of injecting mice with skin extracts does not correspond to the frogs’ natural defense mechanisms. Neither does the injection of frog extracts permit gastrointestinal deactivation or clearance mechanisms that may reduce the bioavailability of toxins. Whether or not increased sleep latencies induced by injected skin extracts reflect toxicity, irritability or other effects, the ultimate protective value for frogs of prolonging the wakefulness of mice (or relevant predators) is unclear. Defensible bioassays entail both modes of chemical delivery consistent with those by which would-be predators normally encounter chemicals and quantified measures of responses by predators that detract from their success.

Poison frog tadpoles seek parental transportation to escape their cannibalistic siblings

AbstractParental care is a limited resource which in many species is acquired by the offspring through begging behaviours and often causes competition between siblings. The Neotropical poison frog Ranitomeya variabilis provides a very specific form of parental care: because its tadpoles are cannibalistic males usually separate them from their siblings after hatching by transporting them singly to small water bodies. However, in some cases parents do not transport their tadpoles but let them all hatch into the same pool. Here, we investigate if abandoned tadpoles of R. variabilis actively seek parental care in form of transportation. We conducted experiments where tadpoles of the same clutch were presented with con‐ and heterospecific frogs, and both moving and non‐moving frog models. Our results revealed that abandoned tadpoles actively approached all frogs and sometimes even climbed onto their backs. We suggest that this tadpole behaviour may function to allow tadpoles to escape sibling competition and cannibalism. Being the first (and possibly the only one) to leave the shared pool should give a tadpole a high survival advantage over its brood‐mates. We further found that tadpoles did not approach artificial models, suggesting that these where either not natural enough or that tadpoles do not recognize frogs by visual or tactile cues but might use chemical or multiple stimuli. The latter is also the case in related egg‐feeding species where tadpoles beg for food. We therefore discuss our results in relation to potential begging behaviours, as well as fixed action patterns and parent–offspring conflict, being potential questions opening up for future examinations regarding our findings.

Male and Female Home Range Behavior in the Neotropical Poison FrogAmeerega trivittata(Anura, Dendrobatidae) Over Two Consecutive Years

Abstract. Neotropical poison frogs (Dendrobatidae) display complex social behaviors. We studied home range behavior in Ameerega trivittata in the rainy season of two consecutive years at Panguana, Peru. Minimum convex polygon (MCP) and Kernel methods were employed. For the first time in the genus Ameerega, we found that females also occupied home ranges. Home range size in both sexes varied greatly and overlap was commonly found between and between sexes. Only a few specimens (both sexes) were rediscovered in the second rainy season, but always within the home range of the previous year. This finding suggests strong site fidelity but also a high seasonal turnover, which could be an indication of dispersal propensity. Maintenance and size of home ranges in males might be linked to individual fitness and the monopolization of resources (i.e., habitat structures) related to mating. Female home range behavior remains to be explained.

The palatability of Neotropical poison frogs in predator‐prey systems: do alkaloids make the difference?

AbstractNeotropical poison frogs sequester alkaloid‐based chemical defenses from their diet, which seem to repel invertebrate predators after contact. In this study, we tested the reaction of predatory ants toward skin secretions of captive‐bred poison frogs without alkaloids. Although the secretions had a smell and taste similar to those of wild‐caught frogs, the ants did not avoid them, but actually preferred them. We infer that amphibian secretions are attractive to invertebrate predators (probably due to palatable nutritive components), but that this attraction is overridden when unpalatable alkaloids are present.

Brood-partitioning behaviour in unpredictable environments: hedging the bets?

Spreading reproduction across time or space can optimize fitness by minimizing the risks for offspring survival in varying and unpredictable environments. Poison frogs (Dendrobatidae) are characterized by complex spatial and reproductive behaviour, such as territoriality, prolonged courtship and parental care. The partitioning of larvae from terrestrial clutches across several water bodies is mainly known from species with carnivorous tadpoles that allocate their tadpoles in very small pools, where limited food availability is accompanied by an increased risk of cannibalism. However, little is known about the deposition behaviour of non-carnivorous species that use medium-sized to large pools. In the present study, we investigated whether the Neotropical poison frog Allobates femoralis exhibits brood-partitioning behaviour when males transport tadpoles 3 weeks after oviposition. We sampled 30 artificial water bodies for tadpoles, which we genotyped at seven highly polymorphic microsatellite loci. Based on the reconstructed pedigree, we show that A. femoralis males distribute larvae of single and of successive clutches across several water bodies. The number of pools used was significantly associated with the number of clutches per male. Ninety-three percent of the males that were assigned to more than one clutch spread their tadpoles across several water bodies. Given the highly variable and unpredictable biotic and abiotic conditions in tropical rainforest, at the spatial scale of the study species’ behaviour, we interpret this behaviour as bet-hedging to improve offspring survival.

Multiple sexual signals: calls over colors for mate attraction in an aposematic, color-diverse poison frog

Sexual signals indicate species identity and mate quality, and their importance for mate attraction is largely recognized. Recently, research in animal communication has started to integrate multiple signal modalities and evaluate their interactions. However, mate choice experiments across animal taxa have been limited to laboratory conditions, and assessments of multiple sexual signals under field conditions are still lacking. We take advantage of the divergence in visual and acoustic signals among populations of the Neotropical poison frog Oophaga pumilio to evaluate the importance of male advertisement calls and color patterns in female mate selection. Previous mate choice experiments in this species suggested color-assortative female mate preferences across many populations. Nevertheless, acoustic signals are crucial for sexual selection in frogs, and males of O. pumilio use advertisement calls to attract females. We hypothesize that both advertisement calls and coloration affects female mate selection in O.pumilio. To test this hypothesis we tested 452 receptive females from six populations in Costa Rica and Panama in their natural home ranges for preferences regarding local vs. non-local advertisement calls and color patterns. Overall, the calls overrode the effect of coloration, whereby most females preferred local over non-local calls. We found a tendency to prefer brighter (but not necessarily local) males in two populations. Furthermore the strength of preferences varied geographically, and thus might be involved in prezygotic isolation among populations. The stronger effect of calls on mate attraction is associated with acoustic divergence between genetic groups in the species, while colour pattern diversity is mostly located within one genetic group, i.e. not linked to large-scale population structure. Finally our data highlights the importance to consider an array of signal modalities in multiple wild populations in studies of behavioral isolation.

Feeding or avoiding? Facultative egg feeding in a Peruvian poison frog (Ranitomeya variabilis)

The choice of breeding resources can be very important for the reproductive success and accordingly the fitness of an individual. Often, however, advantageous breeding sites also include disadvantageous characteristics. Neotropical poison frogs (Dendrobatidae), for example, use phytotelmata for the deposition of their tadpoles. The exploitation of these small pools is advantageous as it lowers the risk of predation, but it is also costly because of limited resource availability. Several species evolved regular provision with unfertilized trophic eggs to compensate for the resource limitations for their tadpoles. Fertilized eggs in contrast are usually deposited outside of the phytotelmata in both egg-feeding and non-feeding species, to avoid consumption by cannibalistic conspecific tadpoles. The Peruvian species Ranitomeya variabilis is an exception: clutches are deposited within the phytotelmata. Several studies show a strong avoidance for egg deposition within phytotelmata already containing a tadpole. Here the hypothesis is tested that this avoidance behavior is mainly directed towards unrelated offspring, while R. variabilis is less concerned and therefore shows less avoidance when faced with its own offspring. Therefore, two setups were compared, one in which frogs had to face newly erected phytotelmata containing cues of non-familiar tadpoles and one where phytotelmata remained at the same place, so frogs could deposit and recognize their own tadpoles. While non-familiar tadpoles were completely avoided for egg deposition, phytotelmata with familiar tadpoles received several clutches, suggesting a form of parental care in R. variabilis that exceeds the transportation of tadpoles and might be a step towards egg feeding.

A danger foreseen is a danger avoided: how chemical cues of different tadpoles influence parental decisions of a Neotropical poison frog

The protection of offspring against predators and competitors is especially important in organisms using spatially separated breeding resources, impeding the offspring's chances to escape. One example of such isolated reproductive resources are phytotelmata (small water bodies in plant axils), exploited by the Neotropical poison frog Ranitomeya variabilis (Dendrobatidae) for both clutch and tadpole deposition. Because poison frog tadpoles are often cannibalistic, parents tend to avoid deposition with conspecifics. Previous studies have shown that this avoidance is based on chemical cues produced by conspecific tadpoles. Further, cues produced by phylogenetically less-related tadpoles (Bufonidae) were avoided for clutch but not tadpole depositions. We analyzed how the different responses to tadpole cues are triggered. We tested the reactions of parental R. variabilis to tadpole cues of species differing in two aspects: whether or not they are dendrobatids, and whether or not they reproduce in phytotelmata. We found that for clutch deposition, tadpole cues were always avoided, i.e., all tadpoles were treated by the frogs as if they pose a danger to the eggs. However, responses varied for tadpole depositions: while dendrobatid larvae living in phytotelmata were avoided, those breeding in streams were not. Non-poison frog tadpoles were ignored when associated with habitat other than phytotelmata, but they were preferred when living in phytotelmata. This suggests that both phylogeny and tadpole habitat are important triggers for the decisions made by R. variabilis. Only tadpoles using the same breeding resources are considered as relevant for the frog's own larvae (i.e., as a potential danger or food resource), while further decisions are related to evolutionary relationship.

The value of remnant trees in pastures for a neotropical poison frog

Abstract:Conversion of natural habitats to anthropogenic land uses is a primary cause of amphibian declines in species-rich tropical regions. However, agricultural lands are frequently used by a subset of forest-associated species, and the habitat value of a given land use is likely modified by the presence and characteristics of remnant trees. Here we used mark–recapture methods to examine abundances and movement probability of the poison frog, Oophaga pumilio, at individual trees in forest-fragment edges and adjacent pastures in north-eastern Costa Rica. One hundred and forty-seven trees were surveyed at three replicate sites that each included a forest fragment and adjacent pasture. Trees were sampled at distances of ≤30 m into forest and ≤150 m into pastures for Oophaga pumilio, and local environmental characteristics were measured at each tree. We also measured indices of physical condition (size and endurance) of frogs captured in forest edges and in nearby pastures. Analyses of 167 marked individuals showed no difference in per-tree abundances or sex ratios between pasture and forest edges. We found significant interactions between habitat type and leaf-litter cover, tree dbh and number of logs, indicating greater influence of local variables on abundances in pastures. Movement among trees was infrequent and not predicted by sex, size, habitat type or environmental variables. While results of endurance tests did not differ for individuals from the two habitats, frogs captured in pastures were, on average, larger than frogs captured in forest edges. These data indicate that remnant trees are important habitat features for O. pumilio in pastures and corroborate research in other systems that suggests that large relictual trees should be retained to maximize the potential for altered landscapes to provide habitat for native species.

The evolution of parental care, aposematism and color diversity in Neotropical poison frogs

This Special Issue demonstrates the breadth of evolutionary ecology research occurring on Neotropical poison frogs (Dendrobatidae). It also draws attention to the incredible diversity of the poison frogs themselves (phenotypic, behavioral and taxonomic diversity) and this group's potential for research programs focusing on speciation, the evolution of toxicity, color pattern diversity, Mullerian and Batesian mimicry, sexual selection, mating systems and parental care. This Special Issue focused on two key research foci in the field of evolutionary ecology: (1) Understanding the interplay between ecology and the evolution of parental care and (2) Elucidating the ecological factors contributing to the evolution of toxicity, aposematism and color pattern diversity. In this paper, I summarize the major findings of studies presented in this Special Issue. Understanding the interplay between ecology and the evolution of parental care Parent poison frogs transport and subsequently deposit their tadpoles in pools of water. The evolutionary transition from terrestrial to smaller arboreal phytotelmata for tadpole deposition is thought to be driven by a reduction in competition and predation associated with smaller tadpole nurseries. This transition is considered a key evolutionary innovation, allowing access to relatively unexploited resources and facilitating the evolution of many novel breeding strategies. To date, there are only a few empirical examples in dendrobatids to support this hypothesis (Weygoldt 1980; Caldwell 1997; Brown et al. 2010). Field experimentation by McKeon and Summers (2013) present a more complete picture of the interactions between the natural history of Allobates femoralis and the tadpole predators present. Their results suggest that pool size, the presence of predatory insects and inter- actions between predators (and indirect effects on tadpoles) influence larval deposition in A. femoralis. Previous research on Ranitomeya species, a genus distantly related to Allobates, has demonstrated that adults also assess multiple aspects of reproductive resources to

Neotropical poison frogs: evolution’s guide to parenting, fashion and communication in a dynamic world

Few groups of amphibians invoke such an abiding fascination as the Neotropical poison frogs (Dendrobatidae). For many people, these tiny, often brightly-colored frogs serve as ambassadors to the Neotropical rainforests. For some, they may conjure up images of Choco Indians clothed in loin cloths, armed with blowgun darts coated in highly toxic alkaloids secreted by poison frogs, hunting in misty rainforests. Though slightly romanticized, these caricatures get to the core of why these frogs have been the focus of over 350 scientific studies: poison frogs are toxic and many alert predators of their toxicity through bright warning coloration (aposematism). The evolutionary history of Neotropical poison frogs (Dendrobatidae) is the result of a dynamic interaction between ecology and evolution—their evolutionary ecology. Each species’ history was shaped by their local ecology (i.e., toxicity and abundance of prey, population structures and sizes, predation, larval and adult competition) and varying intensities of natural and sexual selection (including sexual conflict). Each diverging lineage, constrained by their own genetic inheritance and phylogenetic inertia, traveled a unique path that led to the astonishing diversity we observe today. This Special Issue of Evolutionary Ecology summarizes multiple avenues of research related to the Second Symposium on ‘‘Poison Frog Ecology, Evolution and Behavior’’ at the 7th World Congress of Herpetology. This issue focuses on two key research foci in evolutionary ecology: (1) Understanding the interplay between the ecology and the evolution of parental care and (2) Elucidating the ecological factors contributing to the evolution of toxicity, aposematism and color pattern diversity.

The power of the seasons: rainfall triggers parental care in poison frogs

The quality of breeding sites is of great importance for the reproductive success and accordingly the fitness of many animal species. Hence, individuals should decide carefully where to rear their offspring. Often parents have to account for multiple characteristics of habitat quality at once, which in turn might change over time. Specimens confronted with such variability may evolve the ability to display context-dependant decision plasticity. Anuran amphibians breeding in ephemeral pools largely face two risks for their offspring: desiccation and predation. The Neotropical poison frog Ranitomeya variabilis deposits both eggs and tadpoles in phytotelmata. These small tadpole nurseries lower the risk of offspring predation. However, because most poison frog tadpoles are cannibalistic, even these pools need to be surveyed for predators, and parents tend to avoid deposition with conspecifics. We tested if this avoidance behaviour does change in parental R. variabilis depending on seasonal circumstances. Over several months we provided the frogs the option to deposit their eggs or tadpoles in pools that did and did not contain chemical cues of cannibalistic conspecifics, respectively. During the rainy season, frogs strongly avoided conspecific cues for both eggs and tadpoles. Anyway, with the change to the dry season, parental preferences changed such that parent frogs were more likely to deposit tadpoles (but not eggs) in pools containing cues of conspecific tadpoles. We suggest that R. variabilis, a species that typically isolates its cannibalistic offspring, has evolved a plastic feeding behaviour with regard to the risk of phytotelmata desiccation. We interpret that parents provide older tadpoles with younger ‘trophic’ tadpoles in order to accelerate their development and save them from impending desiccation.

Contact toxicities of anuran skin alkaloids against the fire ant (Solenopsis invicta)

Nearly 500 alkaloids, representing over 20 structural classes, have been identified from the skin of neotropical poison frogs (Dendrobatidae). These cutaneous compounds, which are derived from arthropod prey of the frogs, generally are believed to deter predators. We tested the red imported fire ant (Solenopsis invicta) for toxicosis following contact with 20 alkaloids (12 structural classes) identified from dendrobatids or other anurans. Individual ants forced to contact the dried residues of 13 compounds exhibited convulsions and/or reduced ambulation. We estimated the cutaneous concentrations of several compounds based on their reported recoveries from skin extracts of free-ranging frogs and our measurements of the skin surface areas of museum specimens. Pumiliotoxin 251D exhibited contact toxicity below its estimated cutaneous concentration in the Ecuadorian frog, Epipedobates anthonyi, an observation consistent with the hypothesized role of this compound in anuran chemical defense. Our results and those of a previous study of mosquitoes indicate that some anuran skin compounds function defensively as contact toxins against arthropods, permeating their exoskeleton.

Tadpole transport logistics in a Neotropical poison frog: indications for strategic planning and adaptive plasticity in anuran parental care

IntroductionIndividuals should aim to adjust their parental behaviours in order to maximize the success of their offspring but minimize associated costs. Plasticity in parental care is well documented from various bird, mammal and fish species, whereas amphibians were traditionally assumed as being highly instinct-bound. Therefore, little is known about ‘higher’ cognitive abilities of amphibians, such as strategic planning and behavioural flexibility. Dendrobatid frogs have evolved a remarkable diversity of parental behaviours. The most noticeable of these behaviours is tadpole transport, which is obligatory in almost all species. Nonetheless, there is limited knowledge about spatial and temporal patterns of tadpole transport and the possible existence of behavioural plasticity on the individual level. In this study, we investigated correlates of tadpole transport behaviour in a natural population of the dendrobatid frog Allobates femoralis during five years.ResultsTadpole transport was predominantly observed during morning hours. Although tadpoles were carried almost exclusively by males (N = 119), we also observed ten females performing this task. The parentage analysis revealed that in all cases females transported their own offspring. In contrast, four tadpole-carrying males were not the genetic fathers of the larvae they were transporting. The average clutch size of 20 eggs and our observation of an average of 8 tadpoles on the back of transporting individuals indicate that frogs do not carry entire clutches at once, and/or that they distribute their larvae across several water bodies. Contrary to the predictions from a hypothetical random search for deposition sites, the number of transported tadpoles was higher in males that travelled over longer distances.ConclusionsOur results suggest a strong selective pressure on males to shift the time invested in tadpole transport to periods of low intra-specific competition. The number of tadpoles on the back of the males significantly correlated with displacement distance from the respective home territories, indicating a strategic non-random tadpole transport rather than random search for suitable tadpole deposition sites during tadpole transport. The observation of females who occasionally transported larvae supports the prevalence of adaptive plasticity in parental behaviours even in a species with a rather low level of parental care.

Synthesis of Alkaloid (−)-205B via Stereoselective Reductive Cross-Coupling and Intramolecular [3+2] Cycloaddition

An asymmetric synthesis of alkaloid (-)-205B, a tricyclic member of the architecturally diverse family of natural products isolated from the skin of neotropical poison frogs, is described that proceeds through two recently developed stereoselective synthetic methods: (1) Ti-mediated allylic alcohol-imine reductive cross-coupling and (2) intramolecular [3+2] cycloaddition of a glyoxylate-based homoallylic nitrone. The utility of this latter cycloaddition process for the assembly of the stereochemically dense piperidine core of 205B is noteworthy, as this method enables direct [3+2] cycloaddition of an intermediate homoallylic (E)-nitrone via a pathway that is stereochemically unscathed by competitive [3,3]-sigmatropic rearrangement processes. Overall, the synthesis is asymmetric, concise, and highly stereoselective-features which point to the potential future utility of these chemical methods in natural product synthesis and medicinal chemistry.

An endogenous bile acid and dietary sucrose from skin secretions of alkaloid-sequestering poison frogs.

The skins of Madagascar poison frogs (Mantella) and certain Neotropical poison frogs (Epipedobates, Dendrobates) secrete the new bile acid tauromantellic acid (1), which was found in both wild-caught and captive-born frogs. This is the first molecule of endogenous origin detected in skin secretions from these taxa. Sucrose was also detected in secretions from wild-caught Mantella but not in captive-born frogs, suggesting a dietary origin.

A taxonomic revision of the Neotropical poison frog genus Ranitomeya (Amphibia: Dendrobatidae)

The Neotropical poison frog genus Ranitomeya is revised, resulting in one new genus, one new species, five synonymies and one species classified as nomen dubium. We present an expanded molecular phylogeny that contains 235 terminals, 104 of which are new to this study. Notable additions to this phylogeny include seven of the 12 species in the minuta group, 15 Ranitomeya amazonica, 20 R. lamasi, two R. sirensis, 30 R. ventrimaculata and seven R. uakarii. Previous researchers have long recognized two distinct, reciprocally monophyletic species groups contained within Ranitomeya, sensu Grant et al. 2006: the ventrimaculata group, which is distributed throughout much of the Amazon, and the minuta group of the northern Andes and Central America. We restrict Ranitomeya to the former group and erect a new genus, Andinobates Twomey, Brown, Amézquita & Mejía-Vargas gen. nov., for members of the minuta group. Other major taxonomic results of the current revision include the following: (i) A new species, Ranitomeya toraro Brown, Caldwell, Twomey, Melo-Sampaio & Souza sp. nov., is described from western Brazil. This species has long been referred to as R. ventrimaculata but new morphological and phylogenetic data place it sister to R. defleri. (ii) Examination of the holotype of R. ventrimaculata revealed that this specimen is in fact a member of what is currently referred to as R. duellmani, therefore, Dendrobates duellmani Schulte 1999 is considered herein a junior synonym of D. ventrimaculatus Shreve 1935 (= R. ventrimaculata). (iii) For the frogs that were being called R. ventrimaculata prior to this revision, the oldest available and therefore applicable name is R. variabilis. Whereas previous definitions of R. variabilis were restricted to spotted highland frogs near Tarapoto, Peru, our data suggest that this color morph is conspecific with lowland striped counterparts. Therefore, the definition of R. variabilis is greatly expanded to include most frogs which were (prior to this revision) referred to as R. ventrimaculata. (iv) Phylogenetic and bioacoustic evidence support the retention of R. amazonica as a valid species related to R. variabilis as defined in this paper. Based on phylogenetic data, R. amazonica appears to be distributed throughout much of the lower Amazon, as far east as French Guiana and the Amazon Delta and as far west as Iquitos, Peru. (v) Behavioral and morphological data, as well as phylogenetic data which includes topotypic material of R. sirensis and numerous samples of R. lamasi, suggest that the names sirensis, lamasi and biolat are applicable to a single, widespread species that displays considerable morphological variation throughout its range. The oldest available name for this group is sirensis Aichinger; therefore, we expand the definition of R. sirensis. (vi) Ranitomeya ignea and R. intermedia, elevated to the species status in a previous revision, are placed as junior synonyms of R. reticulata and R. imitator, respectively. (vii) Ranitomeya rubrocephala is designated as nomen dubium. In addition to taxonomic changes, this revision includes the following: (i) Explicit definitions of species groups that are consistent with our proposed taxonomy. (ii) A comprehensive dichotomous key for identification of ‘small’ aposematic poison frogs of South and Central America. (iii) Detailed distribution maps of all Ranitomeya species, including unpublished localities for most species. In some cases, these records result in substantial range extensions (e.g., R. uakarii, R. fantastica). (iv) Tadpole descriptions for R. amazonica, R. flavovittata, R. imitator, R. toraro sp. nov., R. uakarii and R. variabilis; plus a summary of tadpole morphological data for Andinobates and Ranitomeya species. (v) A summary of call data on most members of Andinobates and Ranitomeya, including call data of several species that have not been published before. (vi) A discussion on the continued impacts of the pet trade on poison frogs (vii) A discussion on several cases of potential Müllerian mimicry within the genus Ranitomeya. We also give opinions regarding the current debate on recent taxonomic changes and the use of the name Ranitomeya.

The smell of success: choice of larval rearing sites by means of chemical cues in a Peruvian poison frog

Parental care is a common strategy among vertebrates to ensure successful reproduction. Anuran amphibians have evolved a remarkable diversity of reproductive methods including advanced levels of parental care. Among the most derived strategies are those of the Neotropical poison frogs (Dendrobatidae). These amphibians exhibit a wide array of behavioural traits such as egg guarding, larval transport by parental frogs and larval feeding with trophic (unfertilized) eggs. Ranitomeya variabilis from the upper Amazon basin in Peru deposits both eggs and tadpoles in phytotelmata. The exploitation of these small pools is advantageous as it lowers the risk of predation, but it is more costly because of limited resource availability. Additionally, poison frog larvae are often cannibalistic, so the identification and avoidance of conspecifics represents an adaptive behaviour for these amphibians. While studies have shown that poison frogs actively avoid depositing with conspecifics, the mechanism for assessing pool quality remains unknown. In field experiments, we found that parental R. variabilis frogs used chemical cues to recognize the presence of tadpoles in phytotelmata. Furthermore, they distinguished between cannibalistic and noncannibalistic tadpoles, a behaviour that supports the survival of their own offspring.