Local predation risk shapes spatial and foraging neophobia patterns in Trinidadian guppies

Abstract

The “dangerous niche” hypothesis posits that neophobia functions to reduce the cost of habitat use among animals exposed to unknown risks. For example, more dangerous foraging or higher competition may lead to increased spatial neophobia. Likewise, elevated ambient predation threats have been shown to induce phenotypically plastic neophobic predator avoidance. In both cases, neophobia is argued to reduce the cost of living associated with ecological uncertainty. Here, we test the hypothesis that ambient predation shapes both neophobic predator avoidance and spatial and foraging neophobia in Trinidadian guppies. Guppies were exposed to a novel foraging arena paired with a known cue (conspecific alarm cue), a novel cue (lemon odor), or a stream water control in three streams differing in ambient predation risk. We demonstrate that guppies from a high-predation-risk stream exhibited risk-averse foraging patterns regardless of the chemical stimulus presented (high spatial neophobia) and that those from a low-predation-risk stream were only risk-averse when the foraging arenas were paired with conspecific alarm cue (lower spatial neophobia). Those tested in the intermediate-predation-risk stream were consistently intermediate to the high-risk vs. low-risk populations. Our study suggests that ambient predation risk shapes both neophobic predator avoidance and space-use patterns and that neophobia may function as a “generalized” response to ecological uncertainty.

The Influence of Rearing on Behavior, Brain Monoamines, and Gene Expression in Three-Spined Sticklebacks

“…Sticklebacks are a mobile species and exploration is required to find both food and mates; aggression is likely important for both social interactions and for males to establish breeding burrows and attract females; and neophobia is important for avoiding predators [e.g., Ostlund-Nilsson et al, 2007]. Based on previous work, we predict that exposure to predation stress increases aggressiveness [Lima and Dill, 1990;Bell and Sih, 2007] and neophobia [e.g., Elvidge et al, 2016], and decreases exploration [e.g., Abbey- Lee et al, 2016;Moses and Sih, 1998;Hedrick and Kortet, 2006]; exposure to habitat complexity increases exploration behavior and decreases neophobia [e.g., Christensen and Nielsen, 2004]; and exposure to variable social environment increases aggression and decreases neophobia [e.g., Bannier et al, 2017;Naguib et al, 2011]. Additionally, we predict that monoamine levels, their metabolites, and the expression of genes related to monoaminergic transmission will vary in the brain depending on early environmental treatment, but, as the relationship between the environment and monoaminergic systems is not well understood, we have no directional predictions [Winberg and Nilsson, 1992;Carere and Maestripieri, 2013].…”

Social dynamics, network structure, and information diffusion in fish shoals.

“…However, my pilot study demonstrated that responses to conspecific alarm cues in our population were characteristic of anti-predator behaviors exhibited by wild-caught guppies (Brown et al, 2009). In addition, my findings are broadly consistent with prior work carried out on wild guppy populations (Brown et al, 2013;Elvidge et al, 2016;Heathcote et al, 2017). By conducting this study under controlled conditions, I provide experimental evidence that perceived ambient predation risk can influence fine-scale patterns of association, as well as the acquisition and spread of novel information.…”

“…While the benefits of neophobia in dangerous environments can be substantial, the failure of high-risk groups to exploit a novel foraging opportunity demonstrates a potential cost. Similar findings have been reported in wild guppies in which heightened spatial neophobia in populations exposed to high levels of predation risk resulted in decreased foraging success (Elvidge et al, 2016). Consistent with this interpretation, the diffusion analyses for the foraging task supported a baseline solving rate that increased over time, which is suggestive of neophobic responses that eventually waned in those groups that successfully solved the task (Hoppitt, Kandler, et al, 2010).…”

“…For example, guppies repeatedly exposed to conspecific alarm cues exhibited strong anti-predator responses upon detection of novel odors, while control groups that had been repeatedly exposed to water exhibited no such responses (Brown et al, 2015). Comparative work on wild prey populations living under different levels of predation risk has also shown that behavioral responses elicited in captivity are consistent with those observed in the wild (Brown et al, 2013;Elvidge et al, 2016).…”

“…Heightened neophobic responses towards novel habitats and stimuli in high-risk environments assist naïve individuals in recognizing and responding appropriately to potential threats-i.e., the dangerous niche hypothesis (Greenberg, 2003;Brown et al, 2013)-but at the potential cost of being slower to exploit beneficial opportunities (Elvidge et al, 2016). Even when individuals are not confronting novel stimuli or situations, personal sampling of the environment can be risky in high predation environments, as it may increase the likelihood of encountering a predator or necessitate reductions in vigilance (Lima & Dill, 1990;Webster & Laland, 2008).…”