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.

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.

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.

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.

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.

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.

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.

Relying on known or exploring for new? Movement patterns and reproductive resource use in a tadpole-transporting frog.

Animals relying on uncertain, ephemeral and patchy resources have to regularly update their information about profitable sites. For many tropical amphibians, widespread, scattered breeding pools constitute such fluctuating resources. Among tropical amphibians, poison frogs (Dendrobatidae) exhibit some of the most complex spatial and parental behaviors-including territoriality and tadpole transport from terrestrial clutches to ephemeral aquatic deposition sites. Recent studies have revealed that poison frogs rely on spatial memory to successfully navigate through their environment. This raises the question of when and how these frogs gain information about the area and suitable reproductive resources. To investigate the spatial patterns of pool use and to reveal potential explorative behavior, we used telemetry to follow males of the territorial dendrobatid frog Allobates femoralis during tadpole transport and subsequent homing. To elicit exploration, we reduced resource availability experimentally by simulating desiccated deposition sites. We found that tadpole transport is strongly directed towards known deposition sites and that frogs take similar direct paths when returning to their home territory. Frogs move faster during tadpole transport than when homing after the deposition, which probably reflects different risks and costs during these two movement phases. We found no evidence for exploration, neither during transport nor homing, and independent of the availability of deposition sites. We suggest that prospecting during tadpole transport is too risky for the transported offspring as well as for the transporting male. Relying on spatial memory of multiple previously discovered pools appears to be the predominant and successful strategy for the exploitation of reproductive resources in A. femoralis. Our study provides for the first time a detailed description of poison frog movement patterns during tadpole transport and corroborates recent findings on the significance of spatial memory in poison frogs. When these frogs explore and discover new reproductive resources remains unknown.

Acoustic ranging in poison frogs-it is not about signal amplitude alone.

ABSTRACT: Acoustic ranging allows identifying the distance of a sound source and mediates inter-individual spacing and aggression in territorial species. Birds and mammals are known to use more complex cues than only sound pressure level (SPL), which can be influenced by the signaller and signal transmission in non-predictable ways and thus is not reliable by itself. For frogs, only SPL is currently known to mediate inter-individual distances, but we hypothesise that the strong territoriality of Dendrobatids could make the use of complex cues for ranging highly beneficial for this family. Therefore, we tested the ranging abilities of territorial males of Allobates femoralis (Dendrobatidae, Aromobatinae) in playback trials, using amplitude-normalized signals that were naturally degraded over distance, and synthetic signals that were masked with different levels of noise. Frogs responded significantly less to signals recorded from larger distances, regardless of SPL and signal-to-noise ratio (SNR), but showed no differential response to natural minimum and maximum SNRs across the typical communication range in wild populations. This indicates that frogs used signal amplitude and SNR only as ancillary cues when assessing the distance of sound sources and relied instead mainly on more complex cues, such as spectral degradation or reverberation. We suggest that this ability mediates territorial spacing and mate choice in A. femoralis. Good ranging abilities might also play a role in the remarkable orientation performance of this species, probably by enabling the establishment of a mental acoustic map of the habitat. SIGNIFICANCE STATEMENT: Acoustic ranging allows the distance of vocalizing competitors and mates to be identified. While birds and mammals are known to use complex cues such as temporal degradation, frequency-dependent attenuation and reverberation for ranging, previous research indicated that frogs rely only on signal amplitude (sound pressure level) to assess the distance of other callers. The present study shows for the first time that also poison frogs can make use of more complex cues, an ability which is likely to be highly beneficial in their territorial social organization and probably can also be used for orientation.

Adopt, ignore, or kill? Male poison frogs adjust parental decisions according to their territorial status.

Systematic infanticide of unrelated young has been reported in several animal taxa. Particular attention has been given to carnivores and primates, where infanticide is a sexually selected strategy of males to gain increased access to female mating partners. Cannibals must ensure avoiding their own offspring and targeting only unrelated young. Therefore, decision rules are needed to mediate parental and cannibalistic behaviour. Here we show experimentally that male poison frogs adjust their parental responses - care or infanticide - towards unrelated clutches according to their territorial status. Male frogs followed the simple rule 'care for any clutch' inside their territory, but immediately switched to cannibalism when establishing a new territory. This demonstrates that simple cognitive rules can mediate complex behaviours such as parental care, and that care and cannibalism are antagonistically linked. Non-parental infanticide is mediated by territorial cues and presumably serves to prevent misdirected care in this poison frog. Our results thus prompt a re-consideration of evolutionary and causal aspects of parental decision making, by suggesting that selective infanticide of unrelated young may generally become adaptive when the risks and costs of misdirected care are high.

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.

Behavioural Type Affects Space Use in a Wild Population of Crows (Corvus corone).

While personality-dependent dispersal is well studied, local space use has received surprisingly little attention in this context, despite the multiple consequences on survival and fitness. Regarding the coping style of individuals, recent studies on personality-dependent space use within a habitat indicate that 'proactive' individuals are wider ranging than 'reactive' ones. However, such studies are still scarce and cover limited taxonomic diversity, and thus, more research is needed to explore whether this pattern generalises across species. We examined the link between coping style and space use in a population of crows (Corvus corone) freely inhabiting the urban zoo of Vienna, Austria. We used a binary docility rating (struggle during handling vs. no struggle) and a tonic immobility test to quantify individual coping style. Individual space use was quantified as the number of different sites at which each crow was observed, and we controlled for different number of sightings per individual by creating a space use index. Only the binary docility rating showed repeatability over time, and significantly predicted space use. In contrast to previous studies, we found that reactive crows (no struggle during handling) showed wider ranging space use within the study site than proactive individuals (who struggled during handling). The discrepancy from previous results suggests that the relationship between behavioural type and space use may vary between species, potentially reflecting differences in socioecology.

Sex-specific offspring discrimination reflects respective risks and costs of misdirected care in a poison frog.

The ability to differentiate between one's own and foreign offspring ensures the exclusive allocation of costly parental care to only related progeny. The selective pressure to evolve offspring discrimination strategies is largely shaped by the likelihood and costs of offspring confusion. We hypothesize that males and females with different reproductive and spatial behaviours face different risks of confusing their own with others' offspring, and this should favour differential offspring discrimination strategies in the two sexes. In the brilliant-thighed poison frog, Allobates femoralis, males and females are highly polygamous, terrestrial clutches are laid in male territories and females abandon the clutch after oviposition. We investigated whether males and females differentiate between their own offspring and unrelated young, whether they use direct or indirect cues and whether the concurrent presence of their own clutch is essential to elicit parental behaviours. Males transported tadpoles regardless of location or parentage, but to a lesser extent in the absence of their own clutch. Females discriminated between clutches based on exact location and transported tadpoles only in the presence of their own clutch. This sex-specific selectivity of males and females during parental care reflects the differences in their respective costs of offspring confusion, resulting from differences in their spatial and reproductive behaviours.

The significance of spatial memory for water finding in a tadpole-transporting frog.

The ability to associate environmental cues with valuable resources strongly increases the chances of finding them again, and thus memory often guides animal movement. For example, many temperate region amphibians show strong breeding site fidelity and will return to the same areas even after the ponds have been destroyed. In contrast, many tropical amphibians depend on exploitation of small, scattered and fluctuating resources such as ephemeral pools for reproduction. It remains unknown whether tropical amphibians rely on spatial memory for effective exploitation of their reproductive resources. Poison frogs (Dendrobatidae) routinely shuttle their tadpoles from terrestrial clutches to dispersed aquatic deposition sites. We investigated the role of spatial memory for relocating previously discovered deposition sites in an experimental population of the brilliant-thighed poison frog, Allobates femoralis, a species with predominantly male tadpole transport. We temporarily removed an array of artificial pools that served as the principal tadpole deposition resource for the population. In parallel, we set up an array of sham sites and sites containing conspecific tadpole odour cues. We then quantified the movement patterns and site preferences of tadpole-transporting males by intensive sampling of the area and tracking individual frogs. We found that tadpole-carrier movements were concentrated around the exact locations of removed pools and most individuals visited several removed pool sites. In addition, we found that tadpole-transporting frogs were attracted to novel sites that contained high concentrations of conspecific olfactory tadpole cues. Our results suggest that A. femoralis males rely heavily on spatial memory for efficient exploitation of multiple, widely dispersed deposition sites once they are discovered. Additionally, olfactory cues may facilitate the initial discovery of the new sites.

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.

Flexible compensation of uniparental care: female poison frogs take over when males disappear.

Parental care systems are shaped by costs and benefits to each sex of investing into current versus future progeny. Flexible compensatory parental care is mainly known in biparental species, particularly where parental desertion or reduction of care by 1 parent is common. The other parent can then compensate this loss by either switching parental roles and/or by increasing its own parental effort. In uniparental species, desertion of the caregiver usually leads to total brood loss. In the poison frog, Allobates femoralis, obligatory tadpole transport (TT) is generally performed by males, whereas females abandon their clutches after oviposition. Nevertheless, in a natural population we previously observed 7.8% of TT performed by females, which we could link to the absence of the respective fathers. In the following experiment, under laboratory conditions, all tested A. femoralis females flexibly took over parental duties, but only when their mates were removed. Our findings provide clear evidence for compensatory flexibility in a species with unisexual parental care. Contrary to the view of amphibian parental care as being stereotypical and fixed, these results demonstrate behavioral flexibility as an adaptive response to environmental and social uncertainty. Behavioral flexibility might actually represent a crucial step in the evolutionary transition from uniparental to biparental care in poison frogs. We suspect that across animal species flexible parental roles are much more common than previously thought and suggest the idea of a 3-dimensional continuum regarding flexibility, parental involvement, and timing, when thinking about the evolution of parental care.

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.

Populations, pools, and peccaries: simulating the impact of ecosystem engineers on rainforest frogs.

"Ecosystem engineering" describes habitat alteration by an organism that affects another organism; such nontrophic interactions between organisms are a current focus in ecological research. Our study quantifies the actual impact an ecosystem engineer can have on another species by using a previously identified model system-peccaries and rainforest frogs. In a 4-year experiment, we simulated the impact of peccaries on a population of Allobates femoralis (Dendrobatidae) by installing an array of artificial pools to mimic a forest patch modified by peccaries. The data were analyzed using a gradual before-after control-impact (gBACI) model. Following the supplementation, population size almost doubled as a result of increased autochthonous recruitment driven by a higher per-capita reproduction of males and a higher proportion of reproducing females. The effect was evenly distributed across the population. The differential response of males and females reflects the reproductive behavior of A. femoralis, as only the males use the aquatic sites for tadpole deposition. Our study shows that management and conservation must consider nontrophic relationships and that human "ecosystem engineering" can play a vital role in efforts against the "global amphibian decline."