Body Size and Evolution of Motion Dazzle Coloration in Lizards

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Body Size and Evolution of Motion Dazzle Coloration in Lizards Behavioral The official journal of the ISBE Ecology International Society for Behavioral Ecology Behavioral Ecology (2017), 00(00), 1–8. doi:10.1093/beheco/arx128 Original Article Body size and evolution of motion dazzle coloration in lizards Gopal Murali and Ullasa Kodandaramaiah IISER-TVM Centre for Research and Education in Ecology and Evolution (ICREEE), School of Biology, Indian Institute of Science Education and Research Thiruvananthapuram, Maruthamala PO, Vithura, Thiruvananthapuram 695 551, India Received 4 April 2017; revised 2 July 2017; editorial decision 22 August 2017; accepted 13 September 2017. “Motion dazzle” patterns are a form of defensive coloration suggested to prevent successful capture during motion by causing preda- tors to misjudge the direction or speed of prey movement. Several studies have found results supporting this idea but little is known about the factors that favor the evolution of these antipredator colorations. A recent experimental study has suggested that the lon- gitudinal striped patterns on the body of lizards can redirect attacks to the tail via the motion dazzle effect. Using a virtual predation experiment with humans and a phylogenetic comparative analysis, we show that evolution of longitudinal striped coloration is associ- ated with prey size. Experiments showed that longitudinal stripes located at the anterior reduced lethal attacks (i.e., attacks directed to the anterior and centre) but this benefit was greater for shorter prey. Our comparative analysis revealed a negative association between stripe occurrence and body length but no association between stripes and body width. Overall, our results suggest that the dazzle effect produced by stripes is more advantageous in shorter lizards than in longer ones and that the error induced by stripes might be distributed along the axis parallel to the prey trajectory. We discuss reasons why dazzle coloration could be associated with evolution of smaller body size in animals. Key words: antipredator adaption, lizards, motion dazzle, prey size, redirection, stripes. INTRODUCTION “motion dazzle” patterns, can inhibit capture by disrupting Animals exhibit a tremendous diversity of color patterns, and predators’ perception of trajectory or speed of a moving prey research over a century has identified numerous ways in which (Thayer 1909). This form of protective color patterns are thus animals use these patterns to reduce predation (Thayer 1909; Cott expected to be found in actively moving animals where the ben- 1940; Ruxton et al. 2004). The most common strategies include efit of the lowered probability of successful capture outweighs camouflage through background matching (Stevens and Merilaita the cost of enhanced detectability (Stevens et al. 2011). Several 2009), masquerade (Skelhorn et al. 2010), disruptive coloration recent studies utilizing humans attacking virtual patterned prey (Cuthill et al. 2005), and countershading (Rowland et al. 2008), all on a computer screen have found support for the idea that of which decrease the probability of detection or recognition, and motion dazzle coloration can reduce predation when the prey is are most effective when the animal remains stationary (Stevens et al. moving (Stevens et al. 2008; von Helversen et al. 2013; Hogan 2011; Hall et al. 2013). However, animals need to move for many et al. 2016). Experimental studies have examined aspects such reasons including foraging and searching for mates, and the proba- as varying speed (Hogan et al. 2017), internal contrast (Scott- bility of detection by predators is higher when the prey is in motion Samuel et al. 2011; Hogan et al. 2016), and orientation of the (Martel and Dill 1995; Hailman 1977; Cooper et al. 2008; Ioannou patterns (Hughes et al. 2015) on the effectiveness of dazzle mark- and Krause 2009). Yet, we are only now beginning to understand ings. Yet, we lack an understanding of why certain species rely how certain color patterns can protect prey during motion (Stevens on motion dazzle coloration, while others rely on camouflage as et al. 2008; Stevens et al. 2011; Pike 2015; Umeton et al. 2017). primary defensive strategy. We also know little about the mor- Thayer (1909) hypothesized that certain high contrast repeti- phological or life-history traits of prey animals that could influ- tive color patterns (stripes, bands, and zigzags) now termed ence the evolution of dazzle markings and their effectiveness. One such trait which can affect the evolution of dazzle patterns could be prey body size. Since large animals are inherently more conspicuous, signals which require conspicuousness are expected to Address correspondence to G. Murali. E-mail: [email protected]. be favored in larger animals (Hagman and Forsman 2003; Hossie © The Author 2017. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please e-mail: [email protected] Downloaded from https://academic.oup.com/beheco/article-abstract/doi/10.1093/beheco/arx128/4554414/Body-size-and-evolution-of-motion-dazzle by Central Library, IISER Thiruvananthapuram user on 17 October 2017 Page 2 of 8 Behavioral Ecology et al. 2015) and conversely, evolution of cryptic coloration might in comparative studies on mammals (e.g., Brown and Maurer 1989; be favored in smaller animals (Karpestam et al. 2014). On the Fritz et al. 2009), tetrapods have been excluded in studies on fishes other hand, a larger prey is also more easily caught during motion (Olden et al. 2007) and marine species have been omitted from compared to smaller ones (Van Damme and Van Dooren 1999; studies on birds (Orme et al. 2006). Although snakes are likely Clemente and Wilson 2015). Therefore, dazzle patterns may not nested within lizards (Zheng and Wiens 2016, but see Zhou et al. be effective for larger prey. Thus, the benefit of conspicuous pro- 2006 who show that snakes are sister to lizards), comparative stud- tective patterns such as dazzle markings which operate in motion ies on lizards (e.g., Meiri 2010; Halperin et al. 2016; Gainsbury and may depend on the body size of the animal, although this has not Meiri 2017) have not included snakes because of their distinctness been tested. from lizards. We have similarly excluded snakes in our analysis, as Recently, Murali and Kodandaramaiah (2016) expanded the they are not relevant to our hypotheses, which are explicitly based motion dazzle hypothesis by proposing the redirection hypothesis, on the redirection of attacks by anterior stripes towards plainly where dazzle coloration on the anterior part of a moving prey colored tails. Following a previous study (Halperin et al. 2016), animal can redirect attempted strikes to less vulnerable poste- we also eliminated the below families from the analysis based on rior parts (Murali and Kodandaramaiah 2016). Since high con- specific reasons. Most species in the family Gekkonidae are noctur- trast longitudinal striped color patterns are commonly found nal, which are not directly relevant to the hypotheses under con- on the body (i.e., trunk) of lizards, they proposed that stripes sideration. We also excluded chameleons (Chamaeleonidae), which on lizards might function by redirecting attacks to the expend- are known to change color rapidly based on the signaling context able tail. A recent comparative analysis also supports the idea (Ligon and McGraw 2013). that stripes in lizards may work in motion against predation Color pattern judgment is dependent on many factors, includ- (Halperin et al. 2016). ing the receiver’s visual system and environmental factors (Endler Interestingly, longitudinal stripes in many lizard species are pres- 1991, 1992). Despite this, pattern classification by human observers ent only in juveniles (e.g., Acanthodactylus beershebensis and Plestiodon is commonly employed in comparative studies involving body pat- laticeps; Taylor 1935; Hawlena et al. 2006) and this ontogenic loss terns of animals (Kodandaramaiah 2009; Allen et al. 2013; Kelley of stripes appears to be restricted to species with longer body length et al. 2013; Arbuckle and Speed 2015). Although it would be ideal (Taylor 1935). Moreover, in many lizard species that are polymor- to develop a computer vision based tool to categorize color patterns phic with respect to presence or absence of stripes, striped individu- (e.g., see Stoddard et al. 2014), this requires photographic images als tend to be smaller (Podarcis hispanicus, Ortega et al. 2015; Scelarcis taken in controlled conditions, which is not feasible for the current perspicillata, Carretero et al. 2006). In the skink Plestiodon latiscutatus, study given the large scale. We acknowledge that pattern classifi- individuals of populations with reduced predation pressure become cation by humans can have subjective bias but we employed mul- larger as well as lose stripes (Brandley et al. 2014). The above stud- tiple strategies to ensure that our pattern categorization was robust. ies thus suggest that the functioning of longitudinal stripes in liz- First, pattern classification was performed by 3 volunteers all of ards might be dependent on body size. whom were naïve to the hypotheses and were recruited opportu- We use 2 approaches to address the role of body size in the func- nistically. Volunteers were first year undergraduate students from tioning of longitudinal stripes in attack redirection via the motion the same institute. Each volunteer was given written instructions for dazzle effect.
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