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Animal Camouflage: Current Issues and New Perspectives Downloaded from rstb.royalsocietypublishing.org on July 15, 2011 Animal camouflage: current issues and new perspectives Martin Stevens and Sami Merilaita Phil. Trans. R. Soc. B 2009 364, 423-427 doi: 10.1098/rstb.2008.0217 References This article cites 39 articles, 5 of which can be accessed free http://rstb.royalsocietypublishing.org/content/364/1516/423.full.html#ref-list-1 Article cited in: http://rstb.royalsocietypublishing.org/content/364/1516/423.full.html#related-urls Subject collections Articles on similar topics can be found in the following collections neuroscience (536 articles) behaviour (2148 articles) cognition (591 articles) ecology (2519 articles) evolution (2810 articles) Receive free email alerts when new articles cite this article - sign up in the box at the top Email alerting service right-hand corner of the article or click here To subscribe to Phil. Trans. R. Soc. B go to: http://rstb.royalsocietypublishing.org/subscriptions This journal is © 2009 The Royal Society Downloaded from rstb.royalsocietypublishing.org on July 15, 2011 Phil. Trans. R. Soc. B (2009) 364, 423–427 doi:10.1098/rstb.2008.0217 Published online 6 November 2008 Introduction Animal camouflage: current issues and new perspectives Martin Stevens1,* and Sami Merilaita2,† 1Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK 2Department of Zoology, Stockholm University, 10691 Stockholm, Sweden 1. THE IMPORTANCE AND HISTORY OF leaf mimicry in butterflies helped convince Wallace CAMOUFLAGE RESEARCH (1889), for example, of the power of natural selection. The study of camouflage has a long history in biology, Other strategies may even stretch to the use of and the numerous ways of concealment and disguise bioluminescence to hide shadows generated in aquatic found in the animal kingdom provided Darwin and environments (Johnsen et al. 2004), and include Wallace with important examples for illustrating and ‘decorating’ the body with items from the general defending their ideas of natural selection and adap- environment, such as do some crabs (Hultgren & tation. Thus, various forms of camouflage have become Stachowicz 2008). This diversity of camouflage classical examples of evolution. In a broader sense, strategies is a testament to the importance of avoiding camouflage has been adopted by humans, most notably predation, as this is surely one of the most important by the military and hunters, but it has also influenced selection pressures an organism can face. Concealment other parts of society, for example, arts, popular culture represents one of the principal ways to do so. and design. Camouflage research has for a significant length of Animals use camouflage to make detection or time linked biology, art and the military, stemming recognition more difficult, with most examples associ- from the work and influence of Abbott Thayer and ated with visual camouflage involving body coloration. Hugh Cott. Indeed, Thayer’s (1896, 1909)andCott’s However, in addition to coloration, camouflage may (1940) works are still hugely influential and contain a make use of morphological structures or material found range of untested ideas. However, in spite of its long in the environment, and may even act against senses history and widespread occurrence, research on other than vision (Ruxton 2009). In nature, some of the natural camouflage has not progressed as rapidly as most striking examples of adaptation can be found with many other areas of adaptive coloration, especially in respect to avoiding being detected or recognized, with the last 60–70 years. There are several reasons for this, the strategies employed diverse, and sometimes extra- including that human perceptions have often been ordinary. Such strategies can include using markings to used to subjectively assess a range of protective match the colour and pattern of the background, as in markings, rather than working from the perspective various moths (e.g. Kettlewell 1955), and to break up of the correct receiver. In general, the mechanisms of the appearance of the body, as in some marine isopods camouflage have often been erroneously regarded as (Merilaita 1998). Camouflage is a technique especially intuitively obvious. Furthermore, many researchers useful if the animal can change colour to match the may have found more showy types of animal background on which it is found, such as can some coloration, for example, aposematism, mimicry and cephalopods (Hanlon & Messenger 1988) and chame- sexual ornamentation, more exciting than the often leons (Stuart-Fox et al. 2008). Further remarkable (but not always) duller colours and patterns used for examples include insects bearing an uncanny resem- camouflage. Thus, until recently, the study of natural blance to bird droppings (Hebert 1974)orfish camouflage has progressed slowly; little had changed resembling fallen leaves on a stream bed (Sazima et al. in our understanding of how camouflage works since 2006), to even making the body effectively transparent, the landmark book of Hugh Cott in 1940. Therefore, as occurs in a range of, in particular, aquatic species many of the striking examples of camouflage, such as (Johnsen 2001; Carvalho et al. 2006). Examples such as those discussed above, have not been formally tested, and the benefit that these different types of conceal- ment bring to animals has rarely been quantified in * Author for correspondence ([email protected]). survival terms and how they specifically work. † ˚ Present address: Environmental and Marine Biology, Abo Akademi However, gradually an appreciation of rigorous and University, 20520 Turku, Finland. objective experimental and analytical methods has One contribution of 15 to a Theme Issue ‘Animal camouflage: increased over descriptive, often subjective, methods current issues and new perspectives’. in the study of camouflage. Norris & Lowe’s (1964) 423 This journal is q 2008 The Royal Society Downloaded from rstb.royalsocietypublishing.org on July 15, 2011 424 M. Stevens & S. Merilaita Introduction Table 1. Terms and definitions relevant to visual camouflage. somewhat confusing use of terms. Above, we suggest a list of terms and definitions (table 1). In defining camouflage, meaning all strategies involved in concealment, different forms of camouflage, we use the term including prevention of detection and recognition ‘function’ to describe broadly what the adaptation crypsis (initially preventing detection): may do (e.g. breaking up form, distracting attention), (a) background matching, where the appearance generally and the term ‘mechanism’ to refer to specific matches the colour, lightness and pattern of one (specialist) or several (compromise) background types perceptual processes (e.g. exploiting edge detection (b) self-shadow concealment, where directional light, which mechanisms, lateral inhibition). Ideally, camouflage would lead to the creation of shadows, is cancelled out by strategies should be defined by how they use or exploit countershading specific mechanistic processes. However, one current (c) obliterative shading, where countershading leads to the problem in defining different forms of camouflage is obliteration of three-dimensional form that we do not know enough about the perceptual (d ) disruptive coloration, being a set of markings that creates mechanisms involved. This is clearly a huge area of the appearance of false edges and boundaries, and hinders work for the future. the detection or recognition of an object’s, or part of an With respect to visual camouflage, some authors object’s, true outline and shape have argued that defining camouflage types based (e) flicker-fusion camouflage, where markings such as stripes primarily on appearance is useful. We do not doubt blur during motion to match the colour/lightness of the general background, preventing detection of the animal that categorisation of appearances has merits in some when in motion circumstances, such as for comparative studies (e.g. ( f ) distractive markings, which direct the ‘attention’ or gaze Stoner et al. 2003). However, others advocate far more of the receiver from traits that would give away the animal extensive uses of descriptive terms. For example, (such as the outline) Hanlon (2007) argues that animal camouflage patterns masquerade, where recognition is prevented by resembling an can effectively be defined by three basic pattern classes, uninteresting object, such as a leaf or a stick ‘uniform’, ‘mottle’ and ‘disruptive’, and that while motion dazzle, where markings make estimates of speed and initially based on appearances in cephalopods, which trajectory difficult by the receiver can adjust their patterning, the grouping seems to apply motion camouflage, movement in a fashion that decreases the to other animals as well. We feel this approach is probability of movement detection counterproductive and will lead to confusion, particu- larly because such an approach does not aid the first objective quantification of coloration was import- understanding of how different forms of camouflage ant, and in particular, the work by Endler (1978, function or the different visual mechanisms involved 1984) pioneered and promoted the rigorous study of and how these, in turn, impose selection on animal animal coloration and had a broader influence outside coloration. Instead, definitions should be based on of the field of camouflage. what camouflage does (even if the specific visual In the last few years, there has been an explosion of processes are uncertain). This is crucial because similar camouflage studies. The renewed
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