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Does Disruptive Camouflage Conceal Edges and Features?

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Does Disruptive Camouflage Conceal Edges and Features? Current Zoology 61 (4): 708–717, 2015 Does disruptive camouflage conceal edges and features? * Richard J. WEBSTER Department of Biology, Carleton University, Ottawa, K1S 5B6, Canada Abstract Camouflage is ubiquitous in the natural world and benefits both predators and prey. Amongst the range of conceal- ment strategies, disruptive coloration is thought to visually fragment an animal’s’ outline, thereby reducing its rate of discovery. Here, I propose two non-mutually exclusive hypotheses for how disruptive camouflage functions, and describe the visual me- chanisms that might underlie them. (1) The local edge disruption hypothesis states that camouflage is achieved by breaking up edge information. (2) The global feature disruption hypothesis states camouflage is achieved by breaking up the characteristic features of an animal (e.g., overall shape or facial features). Research clearly shows that putatively disruptive edge markings do increase concealment; however, few tests have been undertaken to determine whether this survival advantage is attributable to the distortion of features, so the global feature disruption hypothesis is under studied. In this review the evidence for global feature disruption is evaluated. Further, I address if object recognition processing provides a feasible mechanism for animals’ features to influence concealment. This review concludes that additional studies are needed to test if disruptive camouflage operates through the global feature disruption and proposes future research directions [Current Zoology 61 (4): 708–717, 2015]. Keywords Antipredator, Background matching, Contour, Crypsis, Camouflage, Disruptive coloration, Edge detection, Object recognition Animal camouflage is the phenomenon by which ani- ground perceived by predators at the time and prey’s mals are concealed in plain sight. Offensive camouflage age, and in the microhabitat where the prey is most allows predators to approach their prey without being vulnerable to visually hunting predators” (Endler, 1984). seen (increasing the likelihood of a successful attack), According the success of background matching is en- whereas defensive camouflage allows prey to avoid be- tirely dependent on the visual appearance of the envi- ing seen by their predators (increasing their survival) ronment in which the animal is located (Darwin, 1859; (Cott, 1940; Ruxton et al., 2004; Stevens and Merilaita, Wallace, 1889; Poulton, 1890). Alternatively, disruptive 2011). In addition, there are camouflage strategies that coloration consists of markings that breakup and distort provide concealment for auditory, chemical, tactile, and edge information; i.e. “… a set of markings that creates visual sensory modalities (Ruxton, 2009). Not surpris- the appearance of false edges and boundaries and ingly, there is typically a selective advantage to being hinders the detection or recognition of an object’s, or well camouflaged. A classical evolutionary example is part of an object’s, true outline and shape” (Stevens and the melanistic moths change in colour frequency, with Merilaita, 2009). Although background matching and the dark morphs becoming more common as they had disruptive coloration are thought to be distinct camouf- better camouflage on trees that had become darkened by lage strategies ((Merilaita, 1998; Cuthill et al., 2005) pollution (Kettlewell, 1956; Kettlewell and Conn, 1977). and references therein), an animal can improve its ca- This review focuses on visual camouflage, in particular mouflage by employing a combination of the two. In- the phenomenon of disruptive coloration, its relation- deed, disruptive coloration requires some degree of ship to background matching, and how the visual pro- background matching to be effective (Cott, 1940; Fraser, cessing of disruptive camouflage makes it a unique ca- et al., 2007; Troscianko et al., 2013; Kang et al., 2014). mouflage strategy. Since both offensive and defensive camouflage have Both camouflage strategies, background matching and evolved as protective mechanisms to avoid visual per- disruptive coloration, are thought to be ubiquitous in ception by receivers, it is essential to consider camouf- nature. Background matching occurs when an animal’s lage from the receiver’s perspective (e.g. a sensory eco- colour pattern (a composite of its luminance, coloration, logy approach) (Bennett and Cuthill, 1994; Endler and and texture) resembles “a random sample of the back- Basolo, 1998; Stevens and Merilaita, 2011). Received Mar. 25, 2015; accepted Aug. 21, 2015. Corresponding author. E-mail: [email protected] © 2015 Current Zoology Webster RJ: Disrupting edges and features 709 An important question in camouflage research is to The local edge disruption hypothesis proposes that determine what type of visual information is exploited concealment is achieved by breaking up of edges, a by disruptive coloration (Troscianko et al., 2009). Does concept that has strong empirical support (Stevens and it operate by concealing the entire animal (i.e. by dis- Cuthill, 2006). Markings that breakup an animal’s edges rupting the animal’s entire outline), or, instead, by con- make the animal less visible because their edges are cealing discrete portions of its edge that form highly discontinuous, which degrades the boundary between recognizable structures (i.e. ‘features’ such as an eye or the animal and its environment. Stevens and Cuthill (2006) ear)? This is a vital question because each scenario and Webster et al. (2013) used artificial moth targets to likely interferes with different levels of perceptual or- show that edge markings make targets harder to detect ganization (Wagemans, 2015). Researchers are currently (as quantified by computer vision algorithms using a uncertain if masking feature information contributes to vision model of edge detection). Kang et al. (2015) pro- camouflage, or if this type of information takes too long vided further insight into the importance of edge visibi- to be processed to have any meaningful influence on lity for animal concealment in the field. They showed camouflage tasks. that moth re-positioning behaviour increases the break- To begin this discussion we require clear definitions up of their edges, inter alia, thereby enhancing their of edges and features. An ‘edge’ is a line or curve that is camouflage. This experiment also demonstrated that a the boundary between where the animal ends and the small increase in the amount of boundary that is broken background begins and is visible due to a sharp discon- up produces a substantial increase in concealment. tinuity in appearance between the two surfaces (Elder The second hypothesis is the global feature disrup- and Velisavljevic, 2009, and references therein). Such tion hypothesis which proposes that disruptive colora- edge detection relies on spatial contrast between animal tion produces concealment by obscuring the outlines of and background and occurs early in perceptual organi- characteristic features of an animal. For global feature zation (Perrinet and Bednar, 2015). In contrast, a feature disruption, markings are distributed to intersect distinc- is defined as object-related information that is used for tive features (e.g. the corners of triangle-like moths to recognition. For example, if searching for a cat, then the impair predators shape perception). Alternatively, for collection of edges that resemble a cat’s face will con- local edge disruption, markings would be distributed tribute to the cat’s visibility in the scene. Such features either randomly (assuming all edge fragments equally influence detection) or to break the long edge fragments likely contribute to the search images used by animals (Panis and Wagemans, 2009). Both hypotheses are com- when visually seek familiar objects (sensu (Lawrence pared in Figure 1. Evidentially, these two hypotheses and Allen, 1983)). While much is still unknown about are not mutually exclusive; rather, they are suggestive how object recognition contributes to visual search and of the spectrum of possible sources of visual informa- the possible role of gestalt principles (Wagemans et al., tion (Panis and Wagemans, 2009) that disruptive camou- 2012a; Wagemans et al., 2012b), what is clear is that flage might exploit. beyond edge detection, grouping of edge elements is Since edge and feature disruption are not mutually required. The visual process responsible for this aggre- exclusive (and it is challenging to identify the source of gating of edge elements into shapes is called ‘contour visual information that is being exploited by the re- integration and completion’ (and is described more com- ceiver), there have been few empirical studies that deal pletely later). These definitions suggest that there might specifically with feature disruption. Compelling evi- be a difference between camouflaging edges and fea- dence for the role of feature disruption is that having tures. Further it could be possible that different types of additional edge markings has been show to, not only disruption exist in different ecological contexts. improve concealment, but to make the target harder to 1 Disruptive Coloration: Edges versus recognise (Webster et al., 2013). If edge markings only Features provide concealment by reducing edge detection, then ability to recognize these targets would not change in The differences between features and edges have led the presence/absence of edge markings (i.e., edge mar- to the proposal of two hypotheses for explaining how kings would only increase detection
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