Predation selects for smaller eye size in a vertebrate: effects of environmental conditions and sex

Abstract

Increased eye size in animals results in a larger retinal image and thus improves visual acuity. Thus, larger eyes should aid both in finding food as well as detecting predators. On the other hand, eyes are usually very conspicuous and several studies have suggested that eye size is associated with predation risk. However, experimental evidence is scant. In this study, we address how predation affects variation in eye size by performing two experiments using Eurasian perch juveniles as prey and either larger perch or pike as predators. First, we used large outdoor tanks to compare selection due to predators on relative eye size in open and artificial vegetated habitats. Second, we studied the effects of both predation risk and resource levels on phenotypic plasticity in relative eye size in indoor aquaria experiments. In the first experiment, we found that habitat altered selection due to predators, since predators selected for smaller eye size in a non-vegetated habitat, but not in a vegetated habitat. In the plasticity experiment, we found that fish predators induced smaller eye size in males, but not in females, while resource levels had no effect on eye size plasticity. Our experiments provide evidence that predation risk could be one of the driving factors behind variation in eye size within species.

More than meets the eye: Predator‐induced pupil size plasticity in a teleost fish

“…(2016) found that that three‐spined sticklebacks Gasterosteus aculeatus show plasticity in eye size and induce relatively larger eyes when reared in presence of chemical cues from predatory Eurasian perch Perca fluviatilis . Furthermore, juvenile perch have recently also been shown to express plasticity in overall eye size as a response to predation risk (Svanbäck & Johansson, 2019). However, in our study, we found no evidence of predator‐induced plasticity in overall eye size.…”

“…This lack of response in overall eye size among predator‐exposed fish can be due to various reasons. Phenotypic plasticity and capability of trait modulation can vary substantially over ontogeny (Fawcett & Frankenhuis, 2015; Hochberg et al., 2011; Hoverman & Relyea, 2007; Meuthen et al., 2018), and while the sticklebacks and perch in the studies mentioned above were exposed to chemical cues from predators from the onset of the larval/juvenile stage (Ab Ghani et al., 2016; Svanbäck & Johansson, 2019), we performed our experiments on larger and sexually mature fish (the majority of experimental subjects showed fully developed gonads). Moreover, as pigmented eyes with high contrast against the background can increase the risk of detection by predators, small eyes may have been suggested to be favoured under predator‐driven selection (Beston et al., 2017; Svanbäck & Johansson, 2019).…”

“…Phenotypic plasticity and capability of trait modulation can vary substantially over ontogeny (Fawcett & Frankenhuis, 2015; Hochberg et al., 2011; Hoverman & Relyea, 2007; Meuthen et al., 2018), and while the sticklebacks and perch in the studies mentioned above were exposed to chemical cues from predators from the onset of the larval/juvenile stage (Ab Ghani et al., 2016; Svanbäck & Johansson, 2019), we performed our experiments on larger and sexually mature fish (the majority of experimental subjects showed fully developed gonads). Moreover, as pigmented eyes with high contrast against the background can increase the risk of detection by predators, small eyes may have been suggested to be favoured under predator‐driven selection (Beston et al., 2017; Svanbäck & Johansson, 2019). Furthermore, as eyes are energetically costly to develop and maintain (Moran, Softley, & Warrant, 2015), the costs associated with changes to pupil size may be significantly lower than investment into construction and maintenance of larger eyes, especially, as an increased eye size ultimately requires a reconstruction and enlargement of the orbit part of the cranium (Goatley, Bellwood, & Bellwood, 2010; Rohner et al., 2013).…”

“…From the digital images we extracted morphological variables using the image analysis software ImageJ v. 1.49 (https://imagej.nih.gov/ij/). We measured the widest part of the eye and pupil at the horizontal plane (Beston, Wostl, & Walsh, 2017; Svanbäck & Johansson, 2019). In addition, we measured standard length (the distance between the tip of the snout to the end of the last scale anterior to the caudal fin) of all fish to account for potential body size differences and enable calculation of relative eye and pupil size.…”

“…Such changes may be of particular importance in the many teleost fish that lack a pupillary sphincter muscle and, hence, have a pupil that is fixed in size and not responsive to ambient light intensity (Douglas, 2018; Helfman et al., 2009). Yet, while numerous studies have unravelled how predation risk can affect prey eye and pupil size, both at micro‐ and macro‐evolutionary scales (Banks et al., 2015; Beston, Dudycha, Post, & Walsh, 2019; Land & Nilsson, 2012; Møller & Erritzoe, 2010; Nilsson et al., 2012), few have examined whether individuals can implement changes to eye morphology traits in response to environmental variation within their lifetime (but see Ab Ghani, Herczeg, & Merilä, 2016; Svanbäck & Johansson, 2019 for examples of predator‐induced plasticity in overall eye size). The high energetic costs of neural tissue make the eye one of the most energetically expensive organs in the vertebrate body (Laughlin, de Ruyter van Steveninck, & Anderson, 1998; Moran, Softley, & Warrant, 2015; Niven & Laughlin, 2008).…”