Prey animals must constantly stay alert and rely on publicly available information to avoid being eaten, find suitable foraging and mating opportunities, and to assess local competition for resources. Reliable information allows prey to make behavioural decisions in order to ensure sufficient foraging and mating gains while reducing predation risks. However, complete information is rarely available to prey. Spatial and temporal variability or, unpredictability in the distribution of resources, or the intensity of risk would lead to increasing levels of ‘ecological uncertainty’. Broadly defined as the lack of complete information, uncertainty is expected to increase the cost of making a bad decision among prey individuals. Choosing to forage on a patch with a high density of competitors, for example, would lead to decreased energy intake, while failing to respond to an unknown predator could lead to death. Given that the cumulative effects of climate change, invasive species, and habitat degradation are all expected to increase ecological uncertainty, understanding how prey deal with a lack of information is a question of critical importance to ecologists.
In the absence of adequate information regarding local conditions, prey can reduce their costs by behaving in an increasingly vigilant or risk-averse manner. Often referred to as neophobia, these cautious responses would reduce the short-term risks and allow prey time to learn about the actual value of specific habitats. Thus, extreme fear may be highly rational and can be considered an adaptive response to ecological uncertainty.
Increased spatial neophobia, or a fear of unfamiliar territory, for example, is commonly reported among birds in habitats containing dangerous foraging opportunities or high competition. Likewise, a variety of aquatic prey animals from populations exposed to high density and diversity of predators show strong neophobic predator avoidance towards a novel cue, while the same prey animals from low predation risk populations are indifferent to the same cue. If neophobia is, as argued, to be a generalized response to ecological uncertainty, we might expect an increase in ambient predation risks to lead to both increased neophobic predator avoidance and increased neophobic space use.
We tested this hypothesis by exposing wild Trinidadian guppies to a novel foraging patch containing an unfamiliar food (commercial fish food-flavored gelatin cubes) in three Trinidadian streams differing in the diversity and density of predators. We also paired the novel patch with one of three chemical cues: a known risky chemical cue (recognizable chemical signals released from injured prey of the same species), a stream water control, or a novel chemical cue (dilute lemon oil). We predicted that guppies from a high-predation risk population should show higher levels of spatial neophobia (longer latency to enter the foraging patch and longer latency to forage) regardless of the chemical cue presented. Conversely, guppies from a low-predation risk population should only show increased spatial neophobia when the foraging patch was paired with a known risky chemical cue.
Our results demonstrate that guppies in the high-predation stream show high spatial neophobia (they took longer to enter and forage) regardless of the chemical information associated with the patch. They treated all patches as equally dangerous. Conversely, we found that guppies from the low-predation risk stream only exhibited risk-averse foraging when the novel patch was labeled with the known high risk cue; when paired with the control or novel cue, guppies entered and foraged significantly faster than when labeled with the high risk cue (low spatial neophobia). Our study suggests that when exposed to greater levels of uncertain predation risk, guppies show both neophobic predator avoidance and spatial neophobia, thus supporting the hypothesis that neophobia may function as a generalized response to ecological uncertainty.
Featured image credit: Fish by Josefa Holland. CC0 Public Domain via Unsplash.