The Enduring Effects of Fear on the Brain and Behaviour in Wildlife

Abstract

Predators affect prey both through direct consumption and through non-consumptive fear effects. Predator induced fear has been shown to alter prey behaviour, where increased vigilance and reduced foraging can scale up to population and community level consequences. In this thesis, I used laboratory model studies for post-traumatic stress disorder (PTSD) as a template to study the neural mechanisms underlying the enduring behavioural response to fear in wildlife. I used audio playbacks in three manipulations in increasingly natural conditions. In all manipulations, playbacks simulated either the presence of predators or non-predator controls. Playbacks were then silenced for one week at which time I tested for enduring effects of predator induced fear in three key brain regions associated with fear processing. In Chapter 2, I quantified the enduring effects of fear on neurogenesis in laboratory housed black-capped chickadees (Poecile atricapillus). I found sex-dependent effects on hippocampal cell proliferation and suppression of immature neurons in the medial ventral arcopallium (avian homologue to the amygdala) for both sexes, consistent with an enduring memory of fear. In Chapter 3, I manipulated fear again in black-capped chickadees but this time they were living outside in semi-natural conditions. I quantified the effects of fear on foraging behaviour, activation, neurogenesis, and neuron structure. Only neuron structure demonstrated enduring effects of fear which included longer dendrites in both the hippocampus and caudolateral nidopallium (avian analogue to the prefrontal cortex) and increased dendritic branching in the caudolateral nidopallium. In Chapter 4, I manipulated fear in free-living meadow voles (Microtus pennsylvanicus). I report enduring, sex dependent, effects of fear on neural activation, neurogenesis, and apoptosis, and enduring effects of fear on neuron structure in both sexes. Enduring effects on neurobiology were accompanied by a behavioural shift in nocturnal activity whereby voles who heard predators one week earlier were caught later in the night. Overall, my thesis demonstrates that wildlife show enduring, PTSD-like effects on neurobiology in response to predator-induced fear and that these effects are often sex dependent. Demonstrating PTSD-like effects on the brains of wild animals suggests that predator-induced fear may have adaptive value for surviving future predator encounters.

Summary for Lay Audience

Predators affect prey by eating them, but the fear of becoming dinner can also have lasting effects. While critical for wildlife survival, fear can be costly as they may have to miss a meal to avoid becoming a meal. I used research on post-traumatic stress disorder (PTSD) as a template to measure the long-lasting effects of fear on the brain and behaviour in wildlife, as PTSD can last a lifetime after even a single life-threatening event. In this thesis, I used sounds of local predator and non-predator species to measure the long-lasting effects of fear in brain regions known to respond to fear. My first chapter measured the effects of fear on newly formed brain cells in black-capped chickadees living in the lab. Males had fewer newborn brain cells, while both sexes had fewer young neurons, when scared. My second chapter looked at how black-capped chickadees respond to fear when living in large outdoor aviaries. Here I measured the long-lasting effects on newly formed brain cells, brain activation, and brain cell structure, and found that one week later the tree-like branches of brain cells (dendrites) got longer and grew more branches when birds were scared. Finally, I measured the effects of fear in a wild rodent species (meadow voles) in their natural habitat. I showed that fear led to changes in newly born brain cells, brain activation, and brain cell death, with males and females showing opposite effects in the brain. I also found that brain cells got longer and had more branches (dendrites) in both male and female voles. Overall, I show how fear can induce long lasting changes in the brain that differ between males and females, suggesting fear memories may be a sign of a healthy mind and have advantages for survival.

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Keywords

predator-prey interaction, fear, post-traumatic stress disorder, fear memory, neurogenesis, FosB, apoptosis, dendritic morphology

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