The mechanisms and functions of reversible colour change in arthropods are highly diverse despite, or perhaps due to, the presence of an exoskeleton. Physiological colour changes, which have been recorded in 90 arthropod species, are rapid and are the result of changes in the positioning of microstructures or pigments, or in the refractive index of layers in the integument. By contrast, morphological colour changes, documented in 31 species, involve the anabolism or catabolism of components (e.g. pigments) directly related to the observable colour. In this review we highlight the diversity of mechanisms by which reversible colour change occurs and the evolutionary context and diversity of arthropod taxa in which it has been observed. Further, we discuss the functions of reversible colour change so far proposed, review the limited behavioural and ecological data, and argue that the field requires phylogenetically controlled approaches to understanding the evolution of reversible colour change. Finally, we encourage biologists to explore new model systems for colour change and to engage scientists from other disciplines; continued cross-disciplinary collaboration is the most promising approach to this nexus of biology, physics, and chemistry.
1. Australian crab spiders exploit the plant–pollinator mutualism by reflecting UV light that attracts pollinators to the flowers where they sit. However, spider UV reflection seems to vary broadly within and between individuals and species, and we are still lacking any comparative studies of prey and/or predator behaviour towards spider colour variation. 2. Here we looked at the natural variation in the coloration of two species of Australian crab spiders, Thomisus spectabilis and Diaea evanida, collected from the field. Furthermore, we examined how two species of native bees responded to variation in colour contrast generated by spiders sitting in flowers compared with vacant flowers. We used data from a bee choice experiment with D. evanida spiders and Trigona carbonaria bees and also published data on T. spectabilis spiders and Austroplebeia australis bees. 3. In the field both spider species were always achromatically (from a distance) undetectable but chromatically (at closer range) detectable for bees. Experimentally, we showed species-specific differences in bee behaviour towards particular spider colour variation: T. carbonaria bees did not show any preference for any colour contrasts generated by D. evanida spiders but A. australis bees were more likely to reject flowers with more contrasting T. spectabilis spiders. 4. Our study suggests that some of the spider colour variation that we encounter in the field may be partly explained by the spider's ability to adjust the reflectance properties of its colour relative to the behaviour of the species of prey available. (Résumé d'auteur
The presence of conspicuous colouration in predators is puzzling because natural selection is expected to favour cryptic or disruptive colouration, making predators less detectable by prey. However, the prey attraction hypothesis proposes that conspicuous colour patterns in spiders increase their foraging success by luring prey. Using manipulative experiments we tested the prey attraction hypothesis for the three most common colour morphs of the orb-weaver Gasteracantha cancriformis (yellow, white, and black and white), as well as individuals painted black and individuals painted yellow. Contrary to our predictions, the black painted spiders had the highest number of damaged areas in webs (an indirect measure of foraging success). Black painted spiders were also observed more often consuming prey and with prey remains in the web, although the trend was not significant. Furthermore, there was no difference in the number of prey intercepted by webs of each spider colour and, in the laboratory, Drosophila melanogaster did not choose any of the spider colours preferentially. Our results suggest that colouration in G. cancriformis is costly or neutral in terms of foraging success. Alternatively, we propose that colouration in Gasteracantha could be an aposematic signal.
The development of color vision models has allowed the appraisal of color vision independent of the human experience. These models are now widely used in ecology and evolution studies. However, in common scenarios of color measurement, color vision models may generate spurious results. Here I present a guide to color vision modeling (Chittka (1992, Journal of Comparative Physiology A, 170, 545) color hexagon, Endler & Mielke (2005, Journal Of The Linnean Society, 86, 405) model, and the linear and log‐linear receptor noise limited models (Vorobyev & Osorio 1998, Proceedings of the Royal Society B, 265, 351; Vorobyev et al. 1998, Journal of Comparative Physiology A, 183, 621)) using a series of simulations, present a unified framework that extends and generalize current models, and provide an R package to facilitate the use of color vision models. When the specific requirements of each model are met, between‐model results are qualitatively and quantitatively similar. However, under many common scenarios of color measurements, models may generate spurious values. For instance, models that log‐transform data and use relative photoreceptor outputs are prone to generate spurious outputs when the stimulus photon catch is smaller than the background photon catch; and models may generate unrealistic predictions when the background is chromatic (e.g. leaf reflectance) and the stimulus is an achromatic low reflectance spectrum. Nonetheless, despite differences, all three models are founded on a similar set of assumptions. Based on that, I provide a new formulation that accommodates and extends models to any number of photoreceptor types, offers flexibility to build user‐defined models, and allows users to easily adjust chromaticity diagram sizes to account for changes when using different number of photoreceptors.
Sit-and-wait predators have evolved several traits that increase the probability of encountering prey, including lures that attract prey. Although most crab spiders (Thomisidae) are known by their ability to change colour in order to match the background, a few use a different strategy. They are UV-reflective, creating a colour contrast against UV-absorbing flowers that is attractive for pollinators. The nature of the relationship between colour contrast and foraging success is unknown, as is how spiders trade off the potential costs and benefits of strong colour contrast. Therefore, this study investigated the relationship between spider colouration, foraging success and background colouration in a crab spider species known to lure pollinators via UV reflectance (Thomisus spectabilis). Field data revealed that spider body condition - a proxy of past foraging success - is positively related to overall colour contrast. We experimentally tested the effect of satiation and background colour on spider colour change. Throughout the experiment, spiders changed their colour contrast regardless of their food intake, suggesting that colour contrast and the UV component contributing to overall contrast are not caused by spider condition. Although spiders responded to different backgrounds by subtly changing their body colour, this did not result in colour matching. We believe that the observed variation in colour contrast and hence conspicuousness in the field, coupled with the spiders' reaction to our manipulation, could be the result of plasticity in response to prey. (Résumé d'auteur
Color polymorphisms have been traditionally attributed to apostatic selection. The perception of color depends on the visual system of the observer. Theoretical models predict that differently perceived degrees of conspicuousness by two predator and prey species may cause the evolution of polymorphisms in the presence of anti-apostatic and apostatic selection. The spider Gasteracantha cancriformis (Araneidae) possesses several conspicuous color morphs. In orb-web spiders, the prey attraction hypothesis states that conspicuous colors are prey lures that increase spider foraging success via flower mimicry. Therefore, polymorphism could be maintained if each morph attracted a different prey species (multiple prey hypothesis) and each spider mimicked a different flower color (flower mimicry hypothesis). Conspicuous colors could be a warning signal to predators because of the spider’s hard abdomen and spines. Multiple predators could perceive morphs differently and exert different degrees of selective pressures (multiple predator hypothesis). We explored these 3 hypotheses using reflectance data and color vision modeling to estimate the chromatic and achromatic contrast of G. cancriformis morphs as perceived by several potential prey and predator taxa. Our results revealed that individual taxa perceive the conspicuousness of morphs differently. Therefore, the multiple prey hypothesis and, in part, the multiple predator hypothesis may explain the evolution of color polymorphism in G. cancriformis, even in the presence of anti-apostatic selection. The flower mimicry hypothesis received support by color metrics, but not by color vision models. Other parameters not evaluated by color vision models could also affect the perception of morphs and influence morph survival and polymorphism stability.
Several orb-web spiders build conspicuous decorations in their webs. The prey attraction hypothesis proposes that decorations increase spider foraging success by attracting prey, and that attraction is linked to UV reflectance. Alternatively, the web advertisement hypothesis proposes that decorations are a signal that advertises the presence of the web to large animals. We tested both hypotheses for the web silk tufts of Gasteracantha cancriformis. Even though tufts are UV reflective, we did not find support for the prey attraction hypothesis. In the field, when webs with tufts painted black and control webs were compared, there were no differences in the number of prey captured, number of damaged areas in webs and type of prey captured. In the laboratory, Drosophila melanogaster did not demonstrate preference for tufted silk lines versus non-tufted silk lines. Our data also did not give support for the web advertisement hypothesis. The proportion of web destruction was similar between web with tufts painted black and control webs during four days of experimentation. Therefore, two of the most favoured hypotheses that attempt to explain decorations do not apply for web silk tufts in our study system. Instead we propose that silk tufts might be an aposematic signal.
Summary1. The astounding diversity of animal coloration is indicative of a wide variety of selection pressures. Despite great interest in adaptive function, detailed understanding of the constituent elements of colour traits is lacking for many systems. Such information is important in allowing more accurate appraisals of colour variation and its potential production costs. 2. In this study, we 'dissect' the dorsal colour of crab spiders (Thomisidae) to examine the mechanistic basis of a polyphenic colour trait. These spiders possess the ability to alter reflectance in the ultraviolet (UV), violet and blue wavelengths, changing their colour within days. We investigate and compare the proximate mechanistic basis of colour production in multiple phenotypes of three species using histology and spectrophotometry. 3. Our analyses indicate that the spider cuticle is not equivalently transparent to light across the spectrum (300-700 nm) -as previously argued -and contributes to colour variation. UV light is reflected from guanine crystals, present in storage cells ventral to the hypodermis. The crystals are exposed through a partially UV-transmitting hypodermis and cuticle. Variation from white to yellow is likely mediated through pigments/crystals present in different oxidative stages in the hypodermal cells. 4. Simple mechanistic changes are therefore necessary to produce the observed variation, and likely underlie the evolutionary and ontogenetic lability of this trait. Our findings imply that either a UV-reflective abdomen was the ancestral state for crab spiders, or, if pre-dated by UV-absorbent hypodermal pigments, the evolution of UV reflection has only involved the exposure of underlying guanine crystals through an otherwise clear hypodermis.
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