Personality traits differentially affect components of reproductive success in a Neotropical poison frog.

Individual reproductive success has several components, including the acquisition of mating partners, offspring production, and offspring survival until adulthood. While the effects of certain personality traits-such as boldness or aggressiveness-on single components of reproductive success are well studied, we know little about the composite and multifaceted effects behavioural traits can have on all the aspects of reproductive success. Behavioural traits positively linked to one component of reproductive success might not be beneficial for other components, and these effects may differ between sexes. We investigated the influence of boldness, aggressiveness, and exploration on the number of mating partners, mating events, and offspring surviving until adulthood in males and females of the Neotropical poison frog Allobates femoralis. Behavioural traits had different-even opposite-effects on distinct components of reproductive success in both males and females. For example, males who displayed high levels of aggressiveness and exploration (or low levels of aggressiveness and exploration) managed to attract high number of mating partners, while males with low levels of boldness, low levels of aggressiveness, and high levels of exploration had the most offspring surviving until adulthood. Our results therefore suggest correlational selection favouring particular combinations of behavioural traits.

Naive poison frog tadpoles use bi-modal cues to avoid insect predators but not heterospecific predatory tadpoles.

For animals to survive until reproduction, it is crucial that juveniles successfully detect potential predators and respond with appropriate behavior. The recognition of cues originating from predators can be innate or learned. Cues of various modalities might be used alone or in multi-modal combinations to detect and distinguish predators but studies investigating multi-modal integration in predator avoidance are scarce. Here, we used wild, naive tadpoles of the Neotropical poison frog Allobates femoralis ( Boulenger, 1884) to test their reaction to cues with two modalities from two different sympatrically occurring potential predators: heterospecific predatory Dendrobates tinctorius tadpoles and dragonfly larvae. We presented A. femoralis tadpoles with olfactory or visual cues, or a combination of the two, and compared their reaction to a water control in a between-individual design. In our trials, A. femoralis tadpoles reacted to multi-modal stimuli (a combination of visual and chemical information) originating from dragonfly larvae with avoidance but showed no reaction to uni-modal cues or cues from heterospecific tadpoles. In addition, visual cues from conspecifics increased swimming activity while cues from predators had no effect on tadpole activity. Our results show that A. femoralis tadpoles can innately recognize some predators and probably need both visual and chemical information to effectively avoid them. This is the first study looking at anti-predator behavior in poison frog tadpoles. We discuss how parental care might influence the expression of predator avoidance responses in tadpoles.

Experience shapes accuracy in territorial decision-making in a poison frog.

The trade-off between speed and accuracy affects many behavioural processes like predator avoidance, foraging and nest-site selection, but little is known about this trade-off relative to territorial behaviour. Some poison frogs are highly territorial and fiercely repel calling male intruders. However, attacks need to be conducted cautiously, as they are energetically costly and bear the risk of own injury or accidentally targeting the wrong individual. In this study, we investigated the speed-accuracy trade-off in the context of male territoriality during the breeding season in the brilliant-thighed poison frog, Allobates femoralis. In our experiment, we presented the call of an invisible 'threatening' intruder together with a visible 'non-threatening' intruder, using acoustic playback and a frog model, respectively. Contrary to our prediction, neither reaction time nor approach speed of the tested frogs determined the likelihood of erroneous attacks. However, younger individuals were more likely to attack the non-threatening model than older ones, suggesting that experience plays an essential role in identifying and distinguishing rivalling individuals in a territorial context.

Hierarchical decision-making balances current and future reproductive success.

Parental decisions in animals are often context-dependent and shaped by fitness trade-offs between parents and offspring. For example, the selection of breeding habitats can considerably impact the fitness of both offspring and parents, and therefore, parents should carefully weigh the costs and benefits of available options for their current and future reproductive success. Here, we show that resource-use preferences are shaped by a trade-off between parental effort and offspring safety in a tadpole-transporting frog. In a large-scale in situ experiment, we investigated decision strategies across an entire population of poison frogs that distribute their tadpoles across multiple water bodies. Pool use followed a dynamic and sequential selection process, and transportation became more efficient over time. Our results point to a complex suite of environmental variables that are considered during offspring deposition, which necessitates a highly dynamic and flexible decision-making process in tadpole-transporting frogs.

Low reproductive skew despite high male-biased operational sex ratio in a glass frog with paternal care.

BACKGROUND: Reproductive skew, the uneven distribution of reproductive success among individuals, is a common feature of many animal populations. Several scenarios have been proposed to favour either high or low levels of reproductive skew. Particularly a male-biased operational sex ratio and the asynchronous arrival of females is expected to cause high variation in reproductive success among males. Recently it has been suggested that the type of benefits provided by males (fixed vs. dilutable) could also strongly impact individual mating patterns, and thereby affecting reproductive skew. We tested this hypothesis in Hyalinobatrachium valerioi, a Neotropical glass frog with prolonged breeding and paternal care. RESULTS: We monitored and genetically sampled a natural population in southwestern Costa Rica during the breeding season in 2012 and performed parentage analysis of adult frogs and tadpoles to investigate individual mating frequencies, possible mating preferences, and estimate reproductive skew in males and females. We identified a polygamous mating system, where high proportions of males (69 %) and females (94 %) reproduced successfully. The variance in male mating success could largely be attributed to differences in time spent calling at the reproductive site, but not to body size or relatedness. Female H. valerioi were not choosy and mated indiscriminately with available males. CONCLUSIONS: Our findings support the hypothesis that dilutable male benefits - such as parental care - can favour female polyandry and maintain low levels of reproductive skew among males within a population, even in the presence of direct male-male competition and a highly male-biased operational sex ratio. We hypothesize that low male reproductive skew might be a general characteristic in prolonged breeders with paternal care.

Homing trajectories and initial orientation in a Neotropical territorial frog, Allobates femoralis (Dendrobatidae).

INTRODUCTION: The ability to relocate home or breeding sites after experimental removal has been observed in several amphibians and the sensory basis of this behavior has been studied in some temperate-region species. However, the actual return trajectories have rarely been quantified in these studies and it remains unknown how different cues guide the homing behavior. Dendrobatidae (dart-poison frogs) exhibit some of the most complex spatial behaviors among amphibians, such as territoriality and tadpole transport. Recent data showed that Allobates femoralis, a frog with paternal tadpole transport, successfully returns to the home territories after experimental translocations of up to 400 m. In the present study, we used harmonic direction finding to obtain homing trajectories. Additionally, we quantified the initial orientation of individuals, translocated 10 m to 105 m, in an arena assay. RESULTS: Tracking experiments revealed that homing trajectories are characterized by long periods of immobility (up to several days) and short periods (several hours) of rapid movement, closely fitting a straight line towards the home territory. In the arena assay, the frogs showed significant homeward orientation for translocation distances of 35 m to 70 m but not for longer and shorter distances. CONCLUSIONS: Our results describe a very accurate homing behavior in male A. femoralis. The straightness of trajectories and initial homeward orientation suggest integration of learned landmarks providing a map position for translocated individuals. Future research should focus on the role of learning in homing behavior and the exact nature of cues being used.

Poison frogs rely on experience to find the way home in the rainforest.

Among vertebrates, comparable spatial learning abilities have been found in birds, mammals, turtles and fishes, but virtually nothing is known about such abilities in amphibians. Overall, amphibians are the most sedentary vertebrates, but poison frogs (Dendrobatidae) routinely shuttle tadpoles from terrestrial territories to dispersed aquatic deposition sites. We hypothesize that dendrobatid frogs rely on learning for flexible navigation. We tested the role of experience with the local cues for poison frog way-finding by (i) experimentally displacing territorial males of Allobates femoralis over several hundred metres, (ii) using a harmonic direction finder with miniature transponders to track these small frogs, and (iii) using a natural river barrier to separate the translocated frogs from any familiar landmarks. We found that homeward orientation was disrupted by the translocation to the unfamiliar area but frogs translocated over similar distances in their local area showed significant homeward orientation and returned to their territories via a direct path. We suggest that poison frogs rely on spatial learning for way-finding in their local area.

Odor cues rather than personality affect tadpole deposition in a neotropical poison frog.

Animals constantly need to evaluate available external and internal information to make appropriate decisions. Identifying, assessing, and acting on relevant cues in contexts such as mate choice, intra-sexual competition, and parental care is particularly important for optimizing individual reproductive success. Several factors can influence decision-making, such as external environmental cues and the animal's own internal state, yet, we have limited knowledge on how animals integrate available information. Here, we used an entire island population (57 males, 53 females, and 1,109 tadpoles) of the neotropical brilliant-thighed poison frog Allobates femoralis to investigate how 2 factors (olfactory cues and personality traits) influence the ability of males to find and use new resources for tadpole deposition. We experimentally manipulated the location of tadpole deposition sites and their associated olfactory cues, and repeatedly measured exploration and boldness in adult males. We further reconstructed tadpole deposition choices via inferred parent-offspring relationships of adult frogs and tadpoles deposited in our experimental pools using molecular parentage analysis. We found that the discovery and use of new rearing sites were heavily influenced by olfactory cues; however, we did not find an effect of the measured behavioral traits on resource discovery and use. We conclude that in highly dynamic environments such as tropical rainforests, reliable external cues likely take priority over personality traits, helping individuals to discover and make use of reproductive resources.

Odor cues rather than personality affect tadpole deposition in a neotropical poison frog.

Animals constantly need to evaluate available external and internal information to make appropriate decisions. Identifying, assessing, and acting on relevant cues in contexts such as mate choice, intra-sexual competition, and parental care is particularly important for optimizing individual reproductive success. Several factors can influence decision-making, such as external environmental cues and the animal's own internal state, yet, we have limited knowledge on how animals integrate available information. Here, we used an entire island population (57 males, 53 females, and 1,109 tadpoles) of the neotropical brilliant-thighed poison frog Allobates femoralis to investigate how 2 factors (olfactory cues and personality traits) influence the ability of males to find and use new resources for tadpole deposition. We experimentally manipulated the location of tadpole deposition sites and their associated olfactory cues, and repeatedly measured exploration and boldness in adult males. We further reconstructed tadpole deposition choices via inferred parent-offspring relationships of adult frogs and tadpoles deposited in our experimental pools using molecular parentage analysis. We found that the discovery and use of new rearing sites were heavily influenced by olfactory cues; however, we did not find an effect of the measured behavioral traits on resource discovery and use. We conclude that in highly dynamic environments such as tropical rainforests, reliable external cues likely take priority over personality traits, helping individuals to discover and make use of reproductive resources.

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

INTRODUCTION: Individuals 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. RESULTS: Tadpole 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. CONCLUSIONS: Our 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.

Characterization of seven new polymorphic microsatellite loci in the brilliant-thighed poison frog Allobates femoralis (Dendrobatidae), and their cross-species utility in three other dendrobatid species.

Here we document the development of seven novel polymorphic microsatellite markers for the brilliant-thighed poison frog Allobates femoralis (Dendrobatidae). We found between six and 27 alleles per locus in 100 individuals (50 males, 50 females) from the field site 'Saut Pararé', French Guiana, with an average observed heterozygosity of 0.79. One locus (Afem23) deviated significantly from Hardy-Weinberg equilibrium. We did not find any evidence for linkage disequilibrium among the new loci, or to seven of the already described markers for A. femoralis. We also report cross-species amplification of some of the markers in three other dendrobatid species (A. talamancae, Dendrobates tinctorius and Oophaga pumilio).

Regardless of personality, males show similar levels of plasticity in territory defense in a Neotropical poison frog.

Animal personality traits are sometimes linked to an individual's degree of plasticity, with certain personality types being more plastic than others. In territorial species, consistently high levels of aggression might increase the risk of harmful fights, while consistently low aggression might lead to the loss of a territory. Consequently, reacting plastically with an appropriate territorial response should be beneficial to avoid these risks. An integrative investigation of both personality traits and plasticity can help us better understand the dynamics of aggressive interactions during male-male competition. Here, we used a free-ranging Neotropical poison frog population to investigate the role of plasticity in male territorial aggression towards intruders. We conducted repeated standardized territorial intrusion experiments mimicking frogs of different body sizes via playback calls with different peak frequencies. We found individual repeatability for the latency to reach and approach a simulated intruder and observed that both aggressive and less aggressive males decreased their level of aggression towards big intruders. However, our results do not support a correlation between personality and plasticity in the context of male territory defense during the breeding season. We discuss how such a correlation between personality and plasticity might be conditional on the costs and benefits across contexts.

Mate choice in a promiscuous poison frog.

In many animal species, members of one sex, most often females, exhibit a strong preference for mating partners with particular traits or resources. However, when females sequentially mate with multiple partners, strategies underlying female choice are not very well understood. Particularly, little is known if under such sequential polyandry females mate truly randomly, or if they actively try to spread mating events across multiple partners. In the present study, we used the highly promiscuous poison frog Allobates femoralis to investigate whether promiscuity could result from a preference for novel mates. Furthermore, we examined the importance of call characteristics for mate choice. We conducted mate choice experiments in a laboratory setup, by presenting females with recent mating partners or novel males. We recorded call characteristics of both males and the time females spent close to each male. In our trials, females preferred previous mating partners over novel males and also males with shorter advertisement calls. Results from previous studies on A. femoralis suggest that females in our trials recognized previous partners based on individual call characteristics. While mating decisions in the wild and in the laboratory might differ, our study provides first evidence for female mate choice in a poison frog with sequential polyandry.

Repeatable Territorial Aggression in a Neotropical Poison Frog.

Intra-specific aggressive interactions play a prominent role in the life of many animals. While studies have found evidence for repeatability in boldness, activity, and exploration in amphibians, we know relatively little about consistent among-individual variation in aggressiveness, despite its importance for male-male competition and territoriality. Amphibians, and Neotropical poison frogs (Dendrobatidae) in particular, are highly suitable for investigating among-individual variation in aggressiveness, as most species exhibit strong territoriality in at least one of the sexes. In the present study, we aimed to fill this gap in knowledge, by investigating within- and between-individual variation in territorial aggression in a semi-natural population of the Neotropical poison frog Allobates femoralis (Dendrobatidae) in French Guiana. We conducted repeated, standardized behavioral tests to assess if the level of territorial aggression is consistent within and different between individuals. Further, we tested a possible link between body size and level of territorial aggression. We found moderate repeatability in territorial aggressiveness, but no link to age and/or body size. In conclusion, our study represents the first documentation of repeatable aggressive behavior in a territorial context in amphibians.

Exploring links between personality traits and their social and non-social environments in wild poison frogs.

An animal's behavioral phenotype comprises several traits, which are hierarchically structured in functional units. This is manifested in measured behaviors often being correlated, partly reflecting the need of a coordinated functional response. Unfortunately, we still have limited understanding whether consistent differences in animal behaviors are due to underlying physiological constraints or a result of plastic adaptation to their current environment. Therefore, characterizing the spatial distribution of behaviors can provide important insights into causes and consequences of behavioral variation. In the present study, we quantified behaviors in a wild, free-ranging population of the Neotropical frog Allobates femoralis. We investigated how these behaviors were linked to the frogs' natural and social environment and quantified the extent to which these behaviors consistently differed among individuals (i.e., animal personality). We assessed levels of aggressiveness, exploration, and boldness by measuring several underlying behaviors expressed in a set of experimental assays, and found evidence for consistent among-individual differences along these axes. Contrary to our expectation, there was no relationship between individual behaviors and their natural environment, but we found a plastic response of males to changes in female density, which might reflect how individuals cope with their socio-ecological environment. Significance statement: How are behavioral phenotypes distributed across space? Here, we studied an entire free-ranging population of poison frogs, and investigated if the personality traits aggressiveness, exploration, and boldness are linked to the frogs' natural or social environment. We found that behavioral traits were non-randomly distributed across the population, suggesting that the spatial arrangement of behavioral traits reflects how individuals cope with their complex natural and social environment.

Contrasting parental roles shape sex differences in poison frog space use but not navigational performance.

Sex differences in vertebrate spatial abilities are typically interpreted under the adaptive specialization hypothesis, which posits that male reproductive success is linked to larger home ranges and better navigational skills. The androgen spillover hypothesis counters that enhanced male spatial performance may be a byproduct of higher androgen levels. Animal groups that include species where females are expected to outperform males based on life-history traits are key for disentangling these hypotheses. We investigated the association between sex differences in reproductive strategies, spatial behavior, and androgen levels in three species of poison frogs. We tracked individuals in natural environments to show that contrasting parental sex roles shape sex differences in space use, where the sex performing parental duties shows wider-ranging movements. We then translocated frogs from their home areas to test their navigational performance and found that the caring sex outperformed the non-caring sex only in one out of three species. In addition, males across species displayed more explorative behavior than females and androgen levels correlated with explorative behavior and homing accuracy. Overall, we reveal that poison frog reproductive strategies shape movement patterns but not necessarily navigational performance. Together this work suggests that prevailing adaptive hypotheses provide an incomplete explanation of sex differences in spatial abilities.

Strong male/male competition allows for nonchoosy females: high levels of polygynandry in a territorial frog with paternal care.

Our knowledge about genetic mating systems and the underlying causes for and consequences of variation in reproductive success has substantially improved in recent years. When linked to longitudinal population studies, cross-generational pedigrees across wild populations can help answer a wide suite of questions in ecology and evolutionary biology. We used microsatellite markers and exhaustive sampling of two successive adult generations to obtain population-wide estimates of individual reproductive output of males and females in a natural population of the Neotropical frog Allobates femoralis (Aromobatidae), a pan-Amazonian species that features prolonged iteroparous breeding, male territoriality and male parental care. Parentage analysis revealed a polygynandrous mating system in which high proportions of males (35.5%) and females (56.0%) produced progeny that survived until adulthood. Despite contrasting reproductive strategies, successfully reproducing males and females had similar numbers of mating partners that sired the adult progeny (both sexes: median 2; range 1-6); the numbers of their offspring that reached adulthood were also similar (both sexes: median 2; range 1-8). Measures of reproductive skew indicate selection on males only for their opportunity to breed. Reproductive success was significantly higher in territorial than in nonterritorial males, but unrelated to territory size in males or to body size in both sexes. We hypothesize that female polyandry in this species has evolved because of enhanced offspring survival when paternal care is allocated to multiple partners.

Reproductive behavior drives female space use in a sedentary Neotropical frog.

Longer-range movements of anuran amphibians such as mass migrations and habitat invasion have received a lot of attention, but fine-scale spatial behavior remains largely understudied. This gap is especially striking for species that show long-term site fidelity and display their whole behavioral repertoire in a small area. Studying fine-scale movement with conventional capture-mark-recapture techniques is difficult in inconspicuous amphibians: individuals are hard to find, repeated captures might affect their behavior and the number of data points is too low to allow a detailed interpretation of individual space use and time budgeting. In this study, we overcame these limitations by equipping females of the Brilliant-Thighed Poison Frog (Allobates femoralis) with a tag allowing frequent monitoring of their location and behavior. Neotropical poison frogs are well known for their complex behavior and diverse reproductive and parental care strategies. Although the ecology and behavior of the polygamous leaf-litter frog Allobates femoralis is well studied, little is known about the fine-scale space use of the non-territorial females who do not engage in acoustic and visual displays. We tracked 17 females for 6 to 17 days using a harmonic direction finder to provide the first precise analysis of female space use in this species. Females moved on average 1 m per hour and the fastest movement, over 20 m per hour, was related to a subsequent mating event. Traveled distances and activity patterns on days of courtship and mating differed considerably from days without reproduction. Frogs moved more on days with lower temperature and more precipitation, but mating seemed to be the main trigger for female movement. We observed 21 courtships of 12 tagged females. For seven females, we observed two consecutive mating events. Estimated home ranges after 14 days varied considerably between individuals and courtship and mating associated space use made up for ∼30% of the home range. Allobates femoralis females spent large parts of their time in one to three small centers of use. Females did not adjust their time or space use to the density of males in their surroundings and did not show wide-ranging exploratory behavior. Our study demonstrates how tracking combined with detailed behavioral observations can reveal the patterns and drivers of fine-scale spatial behavior in sedentary species.

Counting crows: population structure and group size variation in an urban population of crows.

Social complexity arises from the formation of social relationships like social bonds and dominance hierarchies. In turn, these aspects may be affected by the degree of fission-fusion dynamics, i.e., changes in group size and composition over time. Whilst fission-fusion dynamics has been studied in mammals, birds have received comparably little attention, despite some species having equally complex social lives. Here, we investigated the influence of environmental factors on aspects of fission-fusion dynamics in a free-ranging population of carrion and hooded crows (Corvus corone ssp.) in the urban zoo of Vienna, Austria over a 1-year period. We investigated 1) the size and 2) spatio-temporal structure of the local flock, and 3) environmental influences on local flock and subgroup size. The local flock size varied considerably over the year, with fewest birds being present during the breeding season. The spatio-temporal structure of the local flock showed 4 distinct presence categories, of which the proportions changed significantly throughout the year. Environmental effects on both local flock and subgroup size were time of day, season, temperature, and weather, with additional pronounced effects of the structure of the surroundings and age class on subgroup size. Our findings show environmental influences on party size at the local flock and subgroup level, as well as indications of structured party composition in respect to the 4 presence categories. These results suggest that environmental factors have significant effects on fission-fusion dynamics in free-ranging crows, thereby influencing social complexity.

The role of temporal call structure in species recognition of male Allobates talamancae (Cope, 1875): (Anura: Dendrobatidae).

Acoustic species recognition in anurans depends on spectral and temporal characteristics of the advertisement call. The recognition space of a species is shaped by the likelihood of heterospecific acoustic interference. The dendrobatid frogs Allobates talamancae (Cope, 1875) and Silverstoneia flotator (Dunn, 1931) occur syntopically in south-west Costa Rica. A previous study showed that these two species avoid acoustic interference by spectral stratification. In this study, the role of the temporal call structure in the advertisement call of A. talamancae was analyzed, in particular the internote-interval duration in providing species specific temporal cues. In playback trials, artificial advertisement calls with internote-intervals deviating up to ± 90 % from the population mean internote-interval were broadcast to vocally active territorial males. The phonotactic reactions of the males indicated that, unlike in closely related species, internote-interval duration is not a call property essential for species recognition in A. talamancae. However, temporal call structure may be used for species recognition when the likelihood of heterospecific interference is high. Also, the close-encounter courtship call of male A. talamancae is described.