Behavioural flexibility in anuran amphibians

Studies on behavioural flexibility in animals have largely focussed on higher vertebrates, i.e. mammals, birds and fish. Amphibians have traditionally been assumed to be highly instinct-bound with highly stereotyped behaviour. Due to the lack of research in this field, little is known about cognitive processes in amphibians, such as strategic planning and behavioural flexibility. The general aim of the proposed project is to investigate mechanisms of behavioural flexibility in anuran amphibians. I plan to perform a set of field and laboratory experiments on two anuran model species. Comparing the results to findings in other taxa will provide important insights into the evolution of behavioural plasticity in parental care and sexual selection, not only in anuran amphibians but also in vertebrates in general. Poison frogs (Dendrobatidae) show a remarkable diversity of parental behaviour and recent research has demonstrated the presence of behavioural plasticity in tadpole deposition strategies for several dendrobatid species. The dendrobatid frog Allobates femoralis is widely used as a model organism for research on behaviour, population genetics, ecology and evolution. Observations in the field and preliminary experiments in the lab indicate that A. femoralis females show behavioural plasticity with respect to tadpole transport. Although tadpole transport is performed almost exclusively by males, females flexibly take over parental duties in the event of male absence. In contrast, A. femoralis males probably exhibit a fixed action pattern with regard to tadpole transport, transporting all clutches within their territorial boundaries, regardless of whether they are their genetic fathers. In the proposed project I shall investigate the mechanisms that trigger female parental behaviour, e.g. acoustic or spatial properties of the male advertisement call. The work will provide the first evidence for spontaneous behavioural flexibility in a uni-parental species with generally fixed sex-specific parental roles. One of the fundamental prerequisites of behavioural plasticity is the ability to perceive, identify and respond to changes in the environment. Studies in mammals including humans have assigned specific regions in the brain to stereotyped and highly flexible behaviours and have shown that differential activation potentials are elicited in the associated areas of the brain. I plan to perform functional magnetic resonance imaging (fMRI) using a manganese-enhanced protocol to localize and quantitatively map differences in metabolic brain activity when processing familiar and novel (acoustic and visual) stimuli in the Northern Leopard Frog Rana (Lithobates) pipiens. This will be the first functional brain imaging study on an amphibian species and will investigate for the first time the representation of a novel stimulus in a non-primate vertebrate. As amphibians are considered to be the most basal vertebrate group, my findings will provide important implications on the neuronal structures required for the evolution of flexible behaviour.

In the project 'Behavioural flexibility in anuran amphibians' we have investigated reasons for and mechanisms of behavioural plasticity in two anuran model species, Allobates femoralis and Rana (Lithobates) pipiens, by using an integrative approach of field experiments, behavioural experiments in the laboratory, molecular analyses and brain imaging technology. One major part of this project has focused on parental decision-making in the neotropical poison frog Allobates femoralis. Via male removal experiments we discovered that in this species with obligatory male parental care females flexibly compensate the loss of their offspring's father. Clutch manipulation experiments further revealed different offspring discrimination strategies are employed by male and female A. femoralis, highlighting respective sex-specific differences in risks and costs of misdirected care. Male removal experiments in the field suggested that males exhibit cannibalistic behaviour when taking over a new territory. Follow-up experiments in the lab confirmed this hypothesis and showed that also females prey on unrelated clutches in the absence of a guarding male. We also recently discovered that parental behaviour (i.e. tadpole transport) can be experimentally induced in both male and female A. femoralis, by transferring unrelated tadpoles to the backs of adults in the field. Via molecular parentage analysis we were able to establish cross-generational pedigrees in an experimental population of A. femoralis on a river island, which allowed us to investigate the logistics of tadpole transport and the associated patterns of space use. Taken together, our research clearly demonstrates that that poison frogs exhibit highly flexible parental behaviours and are capable of strategic planning when it comes to parental decision-making. This fellowship also allowed me to spend one year at the University of California Los Angeles (UCLA), where I performed brain imaging experiments (using fMRI technology) to study directed attention to acoustic stimuli in the frog brain. The general aim of the study was to investigate cognitive mechanisms of behavioural flexibility in anuran amphibians. Specifically, I was interested in how individuals manage to 'filter out' socially relevant information from the general background noise. We found significant differences in signal intensity within different brain regions in frogs that had been exposed to conspecific calls compared to noise or silence conditions, indicating that signals with contrasting social relevance are differentially processed in the amphibian brain. This study clearly demonstrates that MEMRI provides a powerful approach to studying brain activity patterns with high spatial resolution in frogs.