Eva Ringler

The female perspective of mating in A. femoralis, a territorial frog with paternal care--a spatial and genetic analysis.

The adaptive significance of sequential polyandry is a challenging question in evolutionary and behavioral biology. Costs and benefits of different mating patterns are shaped by the spatial distribution of individuals and by genetic parameters such as the pairwise relatedness between potential mating partners. Thus, females should become less choosy as costs of mating and searching for mates increase. We used parentage assignments to investigate spatial and genetic patterns of mating across a natural population of the Neotropical frog Allobates femoralis, a species characterized by male territoriality and care and female iteroparity. There was no correlation between genetic and spatial distances between adult individuals across the population. In 72% of cases, females mated with males available within a radius of 20 m. Mean pairwise relatedness coefficients of successful reproducers did not differ from random mating but had a lower variance than expected by chance, suggesting maximal reproductive output at intermediate genetic divergence. We also found evidence for selection in favor of more heterozygous individuals between the embryo and adult stage. The level of sequential polyandry significantly increased with the number of spatially available males. Females that had more candidate males also produced more adult progeny. We hypothesize that the benefits associated with female multiple mating outweigh the costs of in- and outbreeding depression, and consequently precluded the evolution of ‘choosy’ mate selection in this species.

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.

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

Lay Summary Caring mothers step in for deadbeat dads. Flexible compensation has evolved as a countermeasure against reduced or lost parental care and is commonly found in biparental species. In the poison frog Allobates femoralis with obligatory male-only care, we show that females flexibly perform tadpole transport when males disappear. This demonstrates that compensatory flexibility also evolved in species with unisexual care, suggesting that parental care systems are more flexible than previously thought.

The Homing Frog: High Homing Performance in a Territorial Dendrobatid Frog Allobates femoralis (Dendrobatidae).

Dendrobatidae (dart-poison frogs) exhibit some of the most complex spatial behaviors among amphibians, such as territoriality and tadpole transport from terrestrial clutches to widely distributed deposition sites. In species that exhibit long-term territoriality, high homing performance after tadpole transport can be assumed, but experimental evidence is lacking, and the underlying orientation mechanisms are unknown. We conducted a field translocation experiment to test whether male Allobates femoralis, a dendrobatid frog with paternal extra-territorial tadpole transport, are capable of homing after experimental removal, as well as to quantify homing success and speed. Translocated individuals showed a very high homing success for distances up to 200 m and successfully returned from up to 400 m. We discuss the potential orientation mechanisms involved and selective forces that could have shaped this strong homing ability.

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.

Intrusion Experiments to Measure Territory Size: Development of the Method, Tests through Simulations, and Application in the Frog Allobates femoralis

Territoriality is a widespread behaviour in animals and its analysis is crucial in several areas of behavioural, ecological and evolutionary research. Commonly, territory size is assessed through territory mapping and the application of simple area estimators such as minimum convex polygons. In the present study we demonstrate that territory size can be determined adequately with an active approach through intrusion experiments, a technique that is commonly used in behavioural research in other contexts. Tests with simulated data indicate that a minimum of twelve trials needs to be performed to establish reliable orders of relative territory size. To estimate absolute territory size, detailed hull techniques are most appropriate when analyzing point patterns of intrusion experiments, while the local convex hull estimator enables the construction of internal utilization distributions based on such point patterns. Additionally we suggest a ‘stretch the centre’ approach to emphasize the actual process of intrusion experiments in the construction of internal utilization distributions. To demonstrate the utility of the method, we apply all findings from the simulations to data from fieldwork with the model species Allobates femoralis, a territorial aromobatid frog from the lowland rainforest of French Guiana.

Where have all the tadpoles gone? Individual genetic tracking of amphibian larvae until adulthood.

Reliably marking larvae and reidentifying them after metamorphosis is a challenge that has hampered studies on recruitment, dispersal, migration and survivorship of amphibians for a long time, as conventional tags are not reliably retained through metamorphosis. Molecular methods allow unique genetic fingerprints to be established for individuals. Although microsatellite markers have successfully been applied in mark–recapture studies on several animal species, they have never been previously used in amphibians to follow individuals across different life cycle stages. Here, we evaluate microsatellites for genetic across‐stages mark–recapture studies in amphibians and test the suitability of available software packages for genotype matching. We sampled tadpoles of the dendrobatid frog Allobates femoralis, which we introduced on a river island in the Nature Reserve ‘Les Nouragues’ in French Guiana. In two subsequent recapture sessions, we searched for surviving juveniles and adults, respectively. All individuals were genotyped at 14 highly variable microsatellite loci, which yielded unique genetic fingerprints for all individuals. We found large differences in the identification success of the programs tested. The pairwise‐relatedness‐based approach, conducted with the programs kingroup or ML‐Relate, performed best with our data set. Matching ventral patterns of juveniles and adult individuals acted as a control for the reliability of the genetic identification. Our results demonstrate that microsatellite markers are a highly powerful tool for studying amphibian populations on an individual basis. The ability to individually track amphibian tadpoles throughout metamorphosis until adulthood will be of substantial value for future studies on amphibian population ecology and evolution.

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

Lay Summary Peccary wallows and footprints are important breeding pools for rainforest frogs. We performed a resource supplementation experiment with artificial pools, simulating peccary actions, in a population of the poison frog Allobates femoralis. The population almost doubled resulting from increased local reproduction, but not from immigration. These findings demonstrate the importance of “ecosystem engineers,” such as peccaries, for other species, the frogs. Our results also indicate that human engineering may help to protect amphibian populations.

High-resolution forest mapping for behavioural studies in the Nature Reserve ‘Les Nouragues’, French Guiana

For animals with spatially complex behaviours at relatively small scales, the resolution of a global positioning system (GPS) receiver location is often below the resolution needed to correctly map animals’ spatial behaviour. Natural conditions such as canopy cover, canyons or clouds can further degrade GPS receiver reception. Here we present a detailed, high-resolution map of a 4.6 ha Neotropical river island and a 8.3 ha mainland plot with the location of every tree >5 cm DBH and all structures on the forest floor, which are relevant to our study species, the territorial frog Allobates femoralis (Dendrobatidae). The map was derived using distance- and compass-based survey techniques, rooted on dGPS reference points, and incorporates altitudinal information based on a LiDAR survey of the area.

Male body size and parental relatedness but not nuptial colouration influence paternity success during scramble competition in Rana arvalis

Female mate choice promotes the development of male secondary sexual traits such as nuptial colouration, whereas scramble competition favours male traits which enhance their ability for access to females. In the explosively breeding moor frog (Rana arvalis), males express a conspicuous blue colouration during a short reproductive period characterised by scramble competition. In the present study we used controlled mating experiments and genetic markers to disentangle the effects of colouration, body size and pairwise genetic relatedness in determining paternity success. Males observed in amplexus with a female prior to spawning were larger than their competitors but did not differ from them in colouration. Polyandry occurred in 67% of the 18 analysed egg clutches, and amplecting males did not always achieve the highest siring success, most likely due to stray sperm. Successful mating pairs were characterised by higher genetic divergence between them than expected by chance. We confirm previous evidence that male nuptial colouration is not a trait selected by females, and provide evidence that male reproductive success is influenced by male size as well as genetic attributes.