Natural and anthropogenic sources of habitat variation influence exploration behaviour, stress response, and brain morphology in a coastal fish

Abstract

Evolutionary ecology aims to better understand how ecologically important traits respond to environmental heterogeneity. Environments vary both naturally and as a result of human activities, and investigations that simultaneously consider how natural and human‐induced environmental variation affect diverse trait types grow increasingly important as human activities drive species endangerment. Here, we examined how habitat fragmentation and structural habitat complexity affect disparate trait types in Bahamas mosquitofish Gambusia hubbsi inhabiting tidal creeks. We tested a priori predictions for how these factors might influence exploratory behaviour, stress reactivity and brain anatomy. We examined approximately 350 adult Bahamas mosquitofish from seven tidal‐creek populations across Andros Island, The Bahamas that varied in both human‐caused fragmentation (three fragmented and four unfragmented) and natural habitat complexity (e.g. fivefold variation in rock habitat). Populations that had experienced severe human‐induced fragmentation, and thus restriction of tidal exchange from the ocean, exhibited greater exploration of a novel environment, stronger physiological stress responses to a mildly stressful event and smaller telencephala (relative to body size). These changes matched adaptive predictions based mostly on (a) reduced chronic predation risk and (b) decreased demands for navigating tidally dynamic habitats. Populations from sites with greater structural habitat complexity showed a higher propensity for exploration and a relatively larger optic tectum and cerebellum. These patterns matched adaptive predictions related to increased demands for navigating complex environments. Our findings demonstrate environmental variation, including recent anthropogenic impacts (<50 years), can significantly affect complex, ecologically important traits. Yet trait‐specific patterns may not be easily predicted, as we found strong support for only six of 12 predictions. Our results further highlight the utility of simultaneously quantifying multiple environmental factors—for example had we failed to account for habitat complexity, we would not have detected the effects of fragmentation on exploratory behaviours. These responses, and their ecological consequences, may be complex: rapid and adaptive phenotypic responses to anthropogenic impacts can facilitate persistence in human‐altered environments, but may come at a cost of population vulnerability if ecological restoration was to occur without consideration of the altered traits.

The costs and benefits of larger brains in fishes

“…Given the amount of work pointing towards links between habitat features and brain evolution in fishes, it is somewhat surprising that there was no detectable correlation in our dataset. For example, effects of habitat complexity on brain size and/or organization have been shown for cichlids (Shumway, 2010), gobies (White & Brown, 2015), mosquito fish (Jenkins et al, 2021), salmon (Kihslinger & Nevitt, 2006), sunfish (Axelrod et al, 2018) and sticklebacks (Gonda et al, 2009). That being said, a previous analysis on a smaller dataset did not find evidence for an influence of brain size on invasion success in fishes (Drake, 2007), one of the key arguments for the ‘cognitive buffer hypothesis’ (Sol, 2009).…”

Resource competition explains rare cannibalism in the wild in livebearing fishes

“…This pervasive ecosystem fragmentation has caused strong and consistent ecological changes in tidal creeks-for example, reduced tidal exchange, reduced species diversity, increased density of Gambusia, decreased density (or extirpation) of piscivorous fish (e.g., Layman et al, 2004;Valentine-Rose et al, 2007a, 2007b-and led to a number of phenotypic shifts in Bahamian mosquitofish (e.g., Giery et al, 2015;Heinen-Kay et al, 2014;Jenkins et al, 2021;Riesch et al, 2015), including dietary changes (Araújo et al, 2014;Langerhans et al, 2021). Prior work has characterized many of these tidal creeks regarding the population density of Gambusia and the density of predatory fish using visual surveys, and we aimed to use general linear models to test for associations between these variables and cannibalism in this study (N = 3,173 specimens from 24 fragmented and 22 unfragmented tidal creeks).…”

Predation risk and the evolution of a vertebrate stress response: Parallel evolution of stress reactivity and sexual dimorphism

“…Romero, 2004;Sapolsky et al, 2000) as shown in, e.g., fish prey living in high-predation localities (e.g. Archard et al, 2012;Brown et al, 2005;Fischer et al, 2014;Jenkins et al, 2021). Moreover, as the predation regimes in the blue holes have been relatively constant for thousands of years (Heinen-Kay & Langerhans, 2013;Langerhans et al, 2007;Martin et al, 2015;Riesch et al, 2013), we hypothesized that differences in stress reactivity would reflect evolutionary divergence rather than phenotypic plasticity.…”