Chapter 7 - Insect Colours and Visual Appearance in the Eyes of Their Predators

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Abstract

The striking diversity in insect colouration, colour pattern and visual appearance (shape, size, texture or movement) has evolved in response to the needs of communication, both with conspecifics and visually guided predators. The question ‘how are insects viewed by their predators?’ hides a complex set of evolutionary processes, which we review here. In addition to a high taxonomic diversity, insectivorous species substantially differ in their visual performance, the mechanisms and flexibility of their predation behaviour, and how they use visual cues for prey detection, recognition, attack and capture. The large variety of predators' visual systems necessitates a thorough measurement of insect colouration (namely spectrometry and photography) ideally coupled to vision modelling to reconstruct colours as likely perceived by predators. In response to visual selection by predators, insects have evolved different strategies to decrease predation risk, such as camouflage—through disruptive colouration, background matching, countershading, masquerade or motion camouflage—or warning colouration in relation to toxicity. The interplay between insects and predators influences the dynamics of insect populations, an aspect of particular interest in the case of populations showing a colour polymorphism. In a critical review of all these aspects, we identify the visual cues most important for predation, the perceptual processes probably operating in predators, the methodological aspects to improve and the future directions for research.

Introduction

Insects exhibit a stunning diversity of colours: consider the splendid spotted butterflies or ladybirds, iridescent odonats or beetles, yellow-and-black striped wasps or flies, brown or green walking sticks or mantids. The previous chapters of this volume have reviewed in great detail the mechanisms of production and development of colouration in insects. It is now time to study insect colours from a more functional and evolutionary perspective and to provide answers to the question ‘why is there such a diversity in insect colouration?’. The vast majority of insect colours and colour patterns is thought to have evolved in relation to the needs of communication with conspecifics, prey and predators. On the one hand, different camouflage strategies are selected to decrease detection probability by non-intentional receivers such as predators or prey. On the other hand, intentional receivers such as conspecifics or predators—in the case of warning colouration—select for more conspicuous colours because they are easier to detect and interpret.

Predators are essential in the evolution of insect colouration. Nearly all animal taxonomic groups comprise insectivorous species and these predators almost all rely, at least partially, on vision for hunting. Spatial vision—the ability to exploit the spatial visual information provided by the environment—appeared more than 500 million years ago (Land and Nilsson, 2002). The advantages that vision provided for orientation, navigation, foraging or reproduction explained its rapid and large evolutionary success, as attested by traces of visual structures in a highly diverse array of fossil records (Land and Nilsson, 2002). Insects, which appeared approximately 100 million years afterwards, had to face visually guided predators from their early evolution. All animals endowed with vision are able to exploit brightness (lightness or luminance) information of their environment. However, some animal species have developed colour vision, that is the ability to distinguish objects differing only by the spectral distribution of the radiant energy (see Kelber et al., 2003 for discussion; Skorupski and Chittka, 2009), to exploit wavelength (chromatic) information independent of brightness. Insect predators add to their taxonomic diversity a diversity in visual performance which results in a manifold pressure on all components of insect colouration, both achromatic (brightness) and chromatic components. In this chapter, we will include all these aspects of colours shown by insects, and we will consider white, grey and black as being colours, to encompass the highest possible number of relevant studies.

It is important to consider all visual features that influence predators' perception of their insect prey. Not only insect colour and colour pattern (i.e. the spatial organization of colour patches on the insect body) are important for perception, but insect size, shape and texture, as many spatial frames in which colouration is expressed, are also important contributors to visual perception (Troscianko et al., 2009). Moreover, insect visual appearance is subject to important temporal and spatial changes due to background and ambient light variability and more importantly to the movements of animals in their environment. Although the central target of this chapter will be colouration and colour pattern, we will also consider the other aforementioned aspects to provide a more complete picture of how predators view insects.

Numerous studies have tackled some issues concerning the appearance of insects to predators, either from a correlative, experimental or from a theoretical modelling approach. Most of them have focused on a few signallers or receivers (e.g. Eisner et al., 1978, Schlee, 1986, Exnerová et al., 2008, Jackson & Pollard, 2007, Ioannou & Krause, 2009). They have explored a variety of colour signals, except iridescent signals, the functional significance of which in relation to predators remains unstudied (Doucet and Meadows, 2009). They rarely considered a comparative approach at a large interspecific scale from the signaller side (but see Robbins, 1981, Williams, 2007, Song & Wenzel, 2008). It is thus interesting to generate a more synthetic view and to consider the strategies evolved by both predators and insects. We will first detail predators' visual performance and their use of vision in prey capture. This will provide the basis for a methodological and conceptual discussion on how to investigate insect colouration viewed by predators. We will then review the strategies evolved by insects to decrease predation risk—namely camouflage and warning colouration—and the impact of the visual interplay between insects and predators on insect population dynamics in the particular case of insect colour polymorphism. We deliberately excluded the evolution of insect Müllerian and Batesian mimicry from this chapter for two reasons. First, the same perceptual principles explain how mimetic and non-mimetic insects are viewed by predators. Second, mimicry itself—origin and maintenance throughout evolution—goes far beyond our initial scope. Similarly, we did not consider in detail cognitive aspects such as learning or memory in predator perception.

Section snippets

Visual equipment of insect predators

Insects are preyed upon by a large array of organisms. All vertebrate classes (amphibians, reptiles, birds, mammals and fish) and major invertebrate classes (insects and chelicerates) contain a large number of insectivorous predators. For more information, the reader can consult extensive reviews specific of insects (Briscoe and Chittka, 2001), birds (Hart, 2001b, Ödeen & Håstad, 2003), mammals (Jacobs, 1993), other animal groups (Kelber et al., 2003, Warrant & Nilsson, 2006) or more up-to-date

Measuring colouration

Most studies of insect colouration, especially those conducted before the 1990s, involve a qualitative measurement of insect colouration, mainly through scores or human vision-based colour categorization, like ‘green’, ‘brown’ or ‘black’ (e.g., Kettlewell, 1955a, Sandoval, 1994, Harmon et al., 1998, Civantos et al., 2004, Hochkirch et al., 2008). This categorization did not only apply to insects, targets or fruit items in general but also to light and visual background. At first, such a

Features of insect camouflage

One way to understand how insects are viewed by their predators is through the study of camouflage. Indeed, insect camouflage is often interpreted as the result of natural selection to avoid detection and recognition by predators, frequently involving body colouration. Therefore, identifying the features of camouflage could reveal how predator visual systems might be lured by insect prey. However, since the landmark books of Thayer, 1909, Cott, 1940, research on natural camouflage has not

Warning colourations and patterns viewed by predators

The effectiveness of warning colouration has been largely supported in a wide range of wild and domestic insect predator species (Table 3). Colours avoided by predators are often red and black-and-yellow stripes. One caveat of studies of warning colouration is the frequent absence of appropriate colour measurement and consideration of predators' visual sensitivities. To our knowledge, only Lyytinen et al., 2001, Schultz, 2001, Gamberale-Stille, 2001, Tullberg et al., 2005, Prudic et al., 2007

Predator visual mimicry

In the preceding section, we have seen that butterfly eyespots have long been thought to mimic large predators' eyes to deter predators from attacking prey. However, in that case, it was the predator's predator that was supposed to be mimicked. Another rarely reported case is that of predator mimicry by insect prey. Both colouration and movement are important components to mimic a predator and effectively decrease predation risk. To our knowledge, the first experimental demonstration of

The representative case of the peppered moth

Colour polymorphism is commonly encountered in camouflaged insect species. Particularly, widespread in nocturnal moths (Kettlewell, 1973, Majerus, 1998), it is also common in other groups like grasshoppers (Dearn, 1990), walking sticks (Sandoval, 1994), water boatmen (Popham, 1941), homoptera or mantids (Evans and Schmidt, 1990). How can polymorphism be maintained through evolutionary time despite the erosive actions of natural selection or genetic drift on genetic variation? Several different

Discussion

This review has concentrated on decrypting how predators see insects' colouration and more generally insects' visual appearance and on detailing how predators use the visual information provided by insects to detect and capture them. Through examples taken from various predator–prey systems, we have revealed the evolutionary interplay between insect colouration and predator behaviour. Visual predation generates an important evolutionary pressure that can determine the evolution of specific

Acknowledgements

We thank Alan Bond for producing Fig. 7 especially for this chapter. We are grateful to Martin Stevens, Joanne T. Kell, William Piel and Antónia Monteiro for providing pictures. We thank the editor Jérôme Casas for inviting us to write this review, and Lars Chittka, Alexandra Barbosa and one anonymous reviewer for their comments on the manuscript.

References (348)

  • L.J. Fleishman et al.

    Colour perception and the use of video playback experiments in animal behaviour

    Anim. Behav.

    (1998)
  • G. Gamberale-Stille et al.

    Contrast versus colour in aposematic signals

    Anim. Behav.

    (2003)
  • J. Ahnesjo et al.

    Differential habitat selection by pygmy grasshopper color morphs; interactive effects of temperature and predator avoidance

    Evol. Ecol.

    (2006)
  • H. Autrum et al.

    Spectral sensitivity of single visual cells of Aeschnidae

    Zeitschrift Fur Vergleichende Physiologie

    (1968)
  • W. Backhaus et al.

    Color distance derived from a receptor model of color vision in the honeybee

    Biol. Cybern.

    (1987)
  • R.S. Bain et al.

    The key mimetic features of hoverflies through avian eyes

    Proc. R. Soc. Lond. B

    (2007)
  • G.P. Bell

    The sensory basis of prey location by the California leaf-nosed bat Macrotus californicus (Chiroptera: Phyllostomidae)

    Behav. Ecol. Sociobiol.

    (1985)
  • A.T.D. Bennett et al.

    Sexual selection and the mismeasure of color

    Am. Nat.

    (1994)
  • G.D. Bernard et al.

    Spectral sensitivities of retinular cells measured in intact, living flies by an optical method

    J. Comp. Phys.

    (1979)
  • J.A. Bishop

    An experimental study of the cline of industrial melanism in Biston betularia (L) (Lepidoptera) between urban Liverpool and rural North Wales

    J. Anim. Ecol.

    (1972)
  • J.A. Bishop et al.

    Response of two species of moths to industrialization in Northwest England. Part 1. Polymorphisms for melanism

    Phil. Trans. R. Soc. Lond. B

    (1978)
  • A.D. Blest

    The function of eyespot patterns in the Lepidoptera

    Behaviour

    (1957)
  • A.D. Blest

    The fine structure of spider photoreceptors in relation to function

  • A.D. Blest et al.

    The spectral sensitivities of identified receptors and the function of retinal tiering in the principal eyes of a jumping spider

    J. Comp. Phys.

    (1981)
  • A.B. Bond et al.

    Apostatic selection by blue jays produces balanced polymorphism in virtual prey

    Nature

    (1998)
  • A.B. Bond et al.

    Visual predators select for crypticity and polymorphism in virtual prey

    Nature

    (2002)
  • A.B. Bond et al.

    Spatial heterogeneity, predator cognition, and the evolution of color polymorphism in virtual prey

    Proc. Natl. Acad. Sci. USA

    (2006)
  • T.I. Bowdish et al.

    Visual cues used by mantids in learning aversion to aposematically colored prey

    Am. Midl. Nat.

    (1993)
  • C.J. Breuker et al.

    Female choice depends on size but not symmetry of dorsal eyespots in the butterfly Bicyclus anynana

    Proc. R. Soc. Lond. B

    (2002)
  • A.D. Briscoe et al.

    The evolution of color vision in insects

    Annu. Rev. Entomol.

    (2001)
  • D. Burkhardt

    UV vision: a bird's eye view of feathers

    J. Comp. Physiol. A

    (1989)
  • N.G. Caine et al.

    Demonstration of a foraging advantage for trichromatic marmosets (Callithrix geoffroyi) dependent on food colour

    Proc. R. Soc. Lond. B

    (2000)
  • J.B. Calderone et al.

    Cone receptor variations and their functional consequences in two species of hamster

    Vis. Neurosci.

    (1999)
  • M.R. Canfield et al.

    The double cloak of invisibility: phenotypic plasticity and larval decoration in a geometrid moth, Synchlora frondaria, across three diet treatments

    Ecol. Entomol.

    (2009)
  • P. Chai et al.

    Predation and the flight, morphology, and temperature of neotropical rain-forest butterflies

    Am. Nat.

    (1990)
  • D.M. Chen et al.

    Ultraviolet receptor of bird retinas

    Science

    (1984)
  • L. Chittka

    The colour hexagon: a chromaticity diagram based on photoreceptor excitations as a generalized representation of colour opponency

    J. Comp. Physiol. A

    (1992)
  • L. Chittka et al.

    Cognitive dimensions of predator responses to imperfect mimicry?

    PLoS Biol.

    (2007)
  • S.C. Church et al.

    Does lepidopteran larval crypsis extend into the ultraviolet?

    Naturwissenschaften

    (1998)
  • E. Civantos et al.

    Indirect effects of prey coloration on predation risk: pygmy grasshoppers versus lizards

    Evol. Ecol. Res.

    (2004)
  • B.C. Clarke

    Balanced polymorphism and the diversity of sympatric species

  • C.A. Clarke et al.

    Genetic control of melanic form insularia of moth Biston betularia (L)

    Nature

    (1964)
  • R.P. Coppinger

    The effect of experience and novelty on avian feeding behavior with reference to the evolution of warning coloration in butterflies. Part I. Reactions of wild-caught adult blue jays to novel insects

    Behaviour

    (1969)
  • R.P. Coppinger

    The effect of experience and novelty on avian feeding behavior with reference to the evolution of warning coloration in butterflies. Part II. Reactions of naive birds to novel insects

    Am. Nat.

    (1970)
  • C. Cordero

    A different look at the false head of butterflies

    Ecol. Entomol.

    (2001)
  • H.B. Cott

    Adaptive Coloration in Animals

    (1940)
  • J.A. Cowing et al.

    Cone visual pigments in two marsupial species: the fat-tailed dunnart (Sminthopsis crassicaudata) and the honey possum (Tarsipes rostratus)

    Proc. R. Soc. Lond. B

    (2008)
  • E.R. Creed et al.

    Pre-adult viability differences of melanic Biston betularia (L) (Lepidoptera)

    Biol. J. Linnean Soc.

    (1980)
  • J.M. Cundy et al.

    Two models for exploring the anti-predator function of eyespots

    J. Biol. Educ.

    (1988)
  • E. Curio

    The Ethology of Predation

    (1976)
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