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Non-visual crypsis: A review of the empirical evidence for camouflage to senses other than vision

Article · Literature ReviewinPhilosophical Transactions of The Royal Society B Biological Sciences 364(1516):549-57 · December 2008with45 Reads
DOI: 10.1098/rstb.2008.0228 · Source: PubMed
Abstract
I review the evidence that organisms have adaptations that confer difficulty of detection by predators and parasites that seek their targets primarily using sensory systems other than vision. In other words, I will answer the question of whether crypsis is a concept that can usefully be applied to non-visual sensory perception. Probably because vision is such an important sensory system in humans, research in this field is sparse. Thus, at present we have very few examples of chemical camouflage, and even these contain some ambiguity in deciding whether they are best seen as examples of background matching or mimicry. There are many examples of organisms that are adaptively silent at times or in locations when or where predation risk is higher or in response to detection of a predator. By contrast, evidence that the form (rather than use) of vocalizations and other sound-based signals has been influenced by issues of reducing detectability to unintended receivers is suggestive rather than conclusive. There is again suggestive but not completely conclusive evidence for crypsis against electro-sensing predators. Lastly, mechanoreception is highly understudied in this regard, but there are scattered reports that strongly suggest that some species can be thought of as being adapted to be cryptic in this modality. Hence, I conclude that crypsis is a concept that can usefully be applied to senses other than vision, and that this is a field very much worthy of more investigation.

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  • ... Being decorated could reduce predation risk in several ways, one of the most obvious being via camouflage. Among antipredator mechanisms, camouflage is unique in that it allows organisms to remain effectively concealed by disrupting the sensory pathways predators use to find prey ( Ruxton 2009). Decorations could reduce the ability of predators to initially perceive an individual, by blending it into the surrounding visual or chemical environment or by breaking up its visual outline, that is, background pattern matching or disruptive crypsis ( Ruxton and Stevens 2015). ...
  • ... We speculate, however, that while this mismatch is most likely real, it may reflect a functional compromise. The syrinx is not constrained to producing signals only within the range of avian best hearing (2–5 kHz), as evidenced by the seet calls of songbirds (greater than or equal to 8 kHz) that are used as short-range alarm calls that are difficult for predatory birds to detect or localize[60]. The echolocation signals of oilbirds are also apparently specialized for short-range transmission, in this case auto-communication. ...
  • ... Animals use many sensing strategies, including time differences in bilateral odour detection (Gardiner & Atema, 2010), time-averaging of odour concentrations (Wilson & Weissburg, 2012), and making simultaneous comparisons of odour concentration (Page et al., 2011;Vergassola, Villermaux & Shraiman, 2007). To avoid such detection, prey may try to limit the amount of olfactory cue that they release or otherwise make it difficult for predators to detect them (Ruxton, 2009).To reduce the risk from predators that hunt using vision, prey can group together to increase the time taken for a hunting predator to locate them. ...
  • ... For instance,Ruxton et al. (2004)brought up the question, when herbivores pass over a stone-mimicking plant, is it a case of crypsis via background matching or of masquerade? Masquerade is usually considered to operate visually, although there are cases of chemical masquerade by caterpillars as defense against predaceous ants (Ruxton 2009) and a parallel situation of plants mimicking feces or carrion odors for defense (Lev-Yadun et al. 2009;Lev-Yadun 2014c, 2016). In recent years, studies in animal behavior have revealed that successful masquerade depends not only on the quality of mimicry, but also on the context. ...
  • ... True " mimicry " means that the entity is misidentified, but detected and treated as a specific object. The term " crypsis " instead is referred to the ability of the entity to match the environment, therefore items are generally unidentified and ignored [133]. Myrmecophiles use various strategies termed as: ...
  • ... The first involves investigating how closely putative examples of mimicry comply with traditional definitions of Batesian (see Glossary) and/or M€ ullerian mimicry (re- views: Roy & Widmer 1999; Maynard-Smith & Harper 2003; Wickler 2013; empirical studies: Londo~ no et al. 2014; Penney et al. 2014; Igic et al. 2015 ). However, these venerable definitions were developed for static visual signals, and do not always extend easily to dynamic signals that change rapidly over time, or to signals that are conveyed through non-visual modalities (Ruxton 2009; Schaefer & Ruxton 2009; Schiestl & Johnson 2013; Dalziell et al. 2015 ). Despite their relatively specific applicability , Batesian and M€ ullerian mimicry still dominate general discussions of mimicry. ...
  • ... We will limit our discussion to camouflage in the visual domain, since most research into the function and evolution of camouflage focuses on this. However, the principles can be broadly applied to camouflage in other sensory modalities [30]. We will begin by discussing the evidence demonstrating that predator cognition is an important selective agent driving the evolution of masquerade and move on to argue that there is reason to believe that it may also play an important role in the evolution of crypsis. ...
  • ... Daboia) that are likely to experience high predation rates because of the diverse macrosmatic, scent-orientated predatory communities in those regions. Ruxton [53] concluded that even though the investigation of crypsis has been applied almost exclusively to visual systems in biology, the concept can be applied to many other modalities (e.g. sound, olfaction, electrical fields, pressure change and vibration). ...
    ... sound, olfaction, electrical fields, pressure change and vibration). The bias for vision comes primarily from the fact that this modality is the predominant human sense [53]. Because olfaction is often a largely unconscious process in humans [54], perceptual dimensions of odours are not well understood and olfaction lacks an intrinsic spatial topology in comparison to other modalities [55]. ...
  • ... The importance of preventing detection by predators is most obvious in visually camouflaged species, which are often matched to their background to render themselves nearly invisible to receivers [1 –3]. Cephalopods have long been of interest to researchers due to their ability to modify their appearance under changing conditions123. Within this group, behavioural mechanisms that either prevent detection by predators (camouflage) or that avoid attack after detection has occurred (visual displays, fleeing and inking) have been frequently studied in the common cuttlefish Sepia officinalis4567891011. ...
    ... Within this group, behavioural mechanisms that either prevent detection by predators (camouflage) or that avoid attack after detection has occurred (visual displays, fleeing and inking) have been frequently studied in the common cuttlefish Sepia officinalis4567891011. Selective pressures for the evolution of visual camouflage have also influenced adaptive cryptic mechanisms in non-visual modalities [3], but these mechanisms remained understudied [4,7,8]. Freezing behaviours, defined as temporary cessations of body movement or ventilation, often co-occur with background matching and visual displays to evade predation by both visual and non-visual predators [8,9,12,13]. ...
  • ... Many organisms have evolved mechanisms to match elements of their environment , to avoid detection or recognition by either predators or prey [1]. Research has focused on forms of visual camouflage, such as crypsis, likely owing to our own reliance on vision [2]. However, organisms often rely on non-visual sensory systems to interact with their environments [3], and recent empirical evidence suggests a variety of taxa have also evolved mechanisms to 'blend in' with various non-visual habitat components (reviewed in [2]). ...
    ... Research has focused on forms of visual camouflage, such as crypsis, likely owing to our own reliance on vision [2]. However, organisms often rely on non-visual sensory systems to interact with their environments [3], and recent empirical evidence suggests a variety of taxa have also evolved mechanisms to 'blend in' with various non-visual habitat components (reviewed in [2]). For instance, many species have highly developed olfactory capabilities, relying on chemical, not visual, cues to locate and identify predators or prey [4,5]. ...
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