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From ecology to neurobiology: spatial cognition in rainforest frogs

Periodic Reporting for period 2 - FrogsInSpace (From ecology to neurobiology: spatial cognition in rainforest frogs)

Reporting period: 2021-07-20 to 2022-07-19

This project aims to better understand the evolution of spatial capabilities in animals and how sex and species differences in behaviour and cognitive abilities arise. Many animals, including humans, rely on their navigation skills to find food, shelter, or mates. In mammals, males tend to roam over larger areas, while females take care of the young and are more sedentary. Males also tend to have better spatial memory, and for decades, scientists have explained this as a necessity for males to navigate larger areas in search of mates. However, some researchers have recently suggested that sex differences in spatial abilities might be a side-effect of sex differences in testosterone levels independent of more extensive male movement range. These two hypotheses are difficult to test in mammals because they require studying species where females roam over larger areas than males, which is uncommon in mammals. Amphibians show a tremendous variation in reproductive strategies and parental roles, including species where males alone take care of offspring while females roam seeking mates. The exceptional variation in life history between closely related amphibian species allows us to test contrasting hypotheses about how navigation skills evolve and differ between sexes and species.

We studied the spatial behaviour, cognition, and neurorendocrine mechanisms in poison frogs, a group of small rainforest frogs with complex parental behaviours and well-developed navigational abilities. The behavioural diversity of poison frogs enabled us to test if differences in male and female navigation skills are related to sex differences in movement patterns and reproductive strategies or if other factors, such as hormone levels, have a stronger influence. Our work has contributed to understanding how sex and species differences in behaviour arise. It also revealed the complexity of amphibian behavior and cognition while laying the foundations for future research on comparative vertebrate spatial cognition.
We used miniature tags and extensive behaviour observations under natural conditions to describe the movement patterns of over three hundred poison frogs belonging to three different species, which differ in their behaviour and male-female roles in parental care. Poison frog parental care primarily consists of parents transporting their tadpoles from land to small water accumulations where tadpoles can develop. In some species, females revisit the tadpoles and feed them by laying unfertilized eggs. We could show that the movement patterns and sex differences in movement scale are primarily shaped by poison frog parental behaviour. In species where males perform the parental duties, males move more because they transport and disperse tadpoles. In species where females take care of the tadpoles, females have larger home ranges and more complex movements than males.

We then compared the navigational abilities of males and females by translocating frogs away from their home territories and tracking their movements as they tried to navigate back home. Contrary to the widely accepted hypothesis that sex differences in reproductive strategies predict sex differences in spatial abilities, we found that poison frog parental roles did not predict sex differences in navigation skills. Males were better at navigating only in one out of two species with male parental care, and we found no sex differences in the species with female parental care. In addition, males were more explorative in all three species regardless of differences in reproductive strategies and parental roles. We could then show that poison frog males have higher testosterone, just like mammals, and we found that higher testosterone levels were associated with more exploration and higher navigational accuracy. Overall, our results do not support the widely accepted paradigm that sex differences in navigational abilities are adaptations to sex differences in movement range and reproductive strategies. Furthermore, our findings suggest that, like in mammals, sex hormones influence amphibian spatial behaviour.

We also studied the neural mechanisms of amphibian spatial behaviour. We found that medial pallium, the brain area responsible for spatial cognition in mammals, was also activated in poison frogs while exploring a novel environment in the lab. However, different forebrain regions were activated when navigating home under natural conditions. These first findings indicate that despite being very distantly related to mammals, frogs share some neural machinery supporting spatial behaviour. But the mechanisms allowing complex navigation over long distances in the wild might be amphibian-specific and have evolved independently. Finally, we also performed experimental and analytical work revealing that, just like mammals, poison frogs rely on flexible spatial memory for navigation. Such cognitive abilities have been previously considered unique to mammals and birds, a view which our findings challenge.

The outcomes of our research have been presented at four international scientific conferences and communicated to broader audiences in public lectures, webinars, and educational videos. In addition, all data and results are being published in peer-reviewed scientific journals and made freely available according to Open Science standards.
Our results challenge some long-held scientific assumptions and shed new light on the evolution of sex differences in spatial abilities and parental behaviour. We reveal that the extent and causes of sex and species differences in spatial behaviour are not well predicted by generalized assumptions based on life-history traits and require detailed descriptive and experimental research, exemplified by our project.

Our project highlights the critical role that parental care plays in animal movement. Parental care is a widespread challenge that shapes the lives of diverse animal groups, from insects to humans. Understanding how caring for the young shapes the behaviour and movements of the parents is essential for understanding how animals adapt to and interact with their environment. We also reveal that despite their tiny brains, tropical frogs rely on flexibly spatial memory for navigation and might share some of the neural machinery underlying this ability with mammals. These findings shed new light on the evolution of animal cognitive abilities by showing that complex behaviours and cognitive mechanisms previously described in mammals might be shared with distantly related amphibians. Understanding how animal cognitive flexibility and mental abilities were shaped by their environment is also crucial for predicting how animals cope with environmental change.

Finally, our work reveals the often neglected diversity behavioural diversity in poorly studied animal groups, such as amphibians. We believe that field research on poorly studied animal groups is key for advancing our fundamental scientific knowledge, mitigating the environmental impacts, and understanding the full scale of diversity loss.
Integrative approach to studying animal behaviour exemplified by the project