Hannah M. Rowland

Masquerade: Camouflage without crypsis

Caterpillars masquerading as twigs are misidentified by chick predators as inanimate objects, rather than remaining undetected. Masquerade describes the resemblance of an organism to an inedible object and is hypothesized to facilitate misidentification of that organism by its predators or its prey. To date, there has been no empirical demonstration of the benefits of masquerade. Here, we show that two species of caterpillar obtain protection from an avian predator by being misidentified as twigs. By manipulating predators’ previous experience of the putative model but keeping their exposure to the masquerader the same, we determined that predators misidentify masquerading prey as their models, rather than simply failing to detect them.

Co-mimics have a mutualistic relationship despite unequal defences

In the first clear mathematical treatment of natural selection, Müller proposed that a shared warning signal (mimicry) would benefit defended prey species by sharing out the per capita mortality incurred during predator education. Although mimicry is a mainstay of adaptationist thinking, there has been repeated debate on whether there is a mutualistic or a parasitic relationship between unequally defended co-mimic species. Here we show that the relationship between unequally defended species is mutualistic. We examined this in a ‘novel world’ of artificial prey with wild predators (great tit, Parus major). We kept the abundance of a highly defended prey (‘model’) constant and increased the density of a moderately defended prey (‘defended mimic’) of either perfect or imperfect mimetic resemblance to the model. Both model and defended mimic showed a net benefit from a density-dependent decrease in their per capita mortality. Even when the effect of dilution through density was controlled for, defended mimics did not induce additional attacks on the model, but we found selection for accurate signal mimicry. In comparison, the addition of fully edible (batesian) mimics did increase additional attacks on the model, but as a result of dilution this resulted in no overall increase in per capita mortality. By ignoring the effects of density, current theories may have overestimated the parasitic costs imposed by less defended mimics on highly defended models.

Can't tell the caterpillars from the trees: countershading enhances survival in a woodland

Perception of the bodys outline and three-dimensional shape arises from visual cues such as shading, contour, perspective and texture. When a uniformly coloured prey animal is illuminated from above by sunlight, a shadow may be cast on the body, generating a brightness contrast between the dorsal and ventral surfaces. For animals such as caterpillars, which live among flat leaves, a difference in reflectance over the body surface may degrade the degree of background matching and provide cues to shape from shading. This may make otherwise cryptic prey more conspicuous to visually hunting predators. Cryptically coloured prey are expected to match their substrate in colour, pattern and texture (though disruptive patterning is an exception), but they may also abolish self-shadowing and therefore either reduce shape cues or maintain their degree of background matching through countershading: a gradation of pigment on the body of an animal so that the surface closest to illumination is darker. In this study, we report the results from a series of field experiments where artificial prey resembling lepidopteran larvae were presented on the upper surfaces of beech tree branches so that they could be viewed by free-living birds. We demonstrate that countershading is superior to uniform coloration in terms of reducing attack by free-living predators. This result persisted even when we fixed prey to the underside of branches, simulating the resting position of many tree-living caterpillars. Our experiments provide the first demonstration, in an ecologically valid visual context, that shadowing on bodies (such as lepidopteran larvae) provides cues that visually hunting predators use to detect potential prey species, and that countershading counterbalances shadowing to enhance cryptic protection.

From Abbott Thayer to the present day: what have we learned about the function of countershading?

Of the many visual characteristics of animals, countershading (darker pigmentation on those surfaces exposed to the most lighting) is one of the most common, and paradoxically one of the least well understood. Countershading has been hypothesized to reduce the detectability of prey to visually hunting predators, and while the function of a countershaded colour pattern was proposed over 100 years ago, the field has progressed slowly; convincing evidence for the protective effects of countershading has only recently emerged. Several mechanisms have been invoked for the concealing function of countershading and are discussed in this review, but the actual mechanisms by which countershading functions to reduce attacks by predators lack firm empirical testing. While there is some subjective evidence that countershaded animals match the background on which they rest, no quantitative measure of background matching has been published for countershaded animals; I now present the first such results. Most studies also fail to consider plausible alternative explanations for the colour pattern, such as protection from UV or abrasion, and thermoregulation. This paper examines the evidence to support each of these possible explanations for countershading and discusses the need for future empirical work.

Countershading enhances cryptic protection: an experiment with wild birds and artificial prey

Of the many traits seen in cryptic prey animals, countershading (darker pigmentation on those surfaces exposed to the most lighting) is one of the commonest, and paradoxically one of the least understood. Countershading has been hypothesized to enhance crypsis by shadow-obliteration, in which lighter coloration on the undersides compensates for increased shadow in these regions, thus reducing detection by visually hunting predators. We tested the hypothesis that countershading enhances crypsis in two experiments with artificial prey presented to free-living birds. In the first experiment, artificial prey were presented on lawns to a range of bird species. In the second experiment, the prey were presented on green boards to individual blackbirds, Turdus merula. In both experiments countershaded prey had significantly lower levels of predation than controls. Our results show that countershading can enhance cryptic protection and has important implications for the evolutionary ecology of prey defences.

Density-dependent predation influences the evolution and behavior of masquerading prey

Predation is a fundamental process in the interaction between species, and exerts strong selection pressure. Hence, anti-predatory traits have been intensively studied. Although it has long been speculated that individuals of some species gain protection from predators by sometimes almost-uncanny resemblances to uninteresting objects in the local environment (such as twigs or stones), demonstration of antipredatory benefits to such “masquerade” have only very recently been demonstrated, and the fundamental workings of this defensive strategy remain unclear. Here we use laboratory experiments with avian predators and twig-mimicking caterpillars as masqueraders to investigate (i) the evolutionary dynamics of masquerade; and (ii) the behavioral adaptations associated with masquerade. We show that the benefit of masquerade declines as the local density of masqueraders relative to their models (twigs, in our system) increases. This occurs through two separate mechanisms: increasing model density both decreased predators’ motivation to search for masqueraders, and made masqueraders more difficult to detect. We further demonstrated that masquerading organisms have evolved complex microhabitat selection strategies that allow them to best exploit the density-dependent properties of masquerade. Our results strongly suggest the existence of opportunity costs associated with masquerade. Careful evaluation of such costs will be vital to the development of a fuller understanding of both the distribution of masquerade across taxa and ecosystems, and the evolution of the life history strategies of masquerading prey.

Face, body and speech cues independently predict judgments of attractiveness

Abstract Research on human attraction frequently makes use of single-modality stimuli such as neutral-expression facial photographs as proxy indicators of an individuals attractiveness. However, we know little about how judgments of these single-modality stimuli correspond to judgments of stimuli that incorporate multi-modal cues of face, body and speech. In the present study, ratings of attractiveness judged from videos of participants introducing themselves were independently predicted by judgments of the participants facial attractiveness (a neutral-expression facial photograph masked to conceal the hairstyle), body attractiveness (a photograph of the upper body), and speech attractiveness (the soundtrack to the video). We also found that ratings of the face, body and speech were positively related to each other. Our results support the assumption that the single-modality stimuli used in much attractiveness research are valid proxy indicators of overall attractiveness in ecologically valid contexts, ...

The biology of color

In living color Animals live in a colorful world, but we rarely stop to think about how this color is produced and perceived, or how it evolved. Cuthill et al. review how color is used for social signals between individual animals and how it affects interactions with parasites, predators, and the physical environment. New approaches are elucidating aspects of animal coloration, from the requirements for complex cognition and perception mechanisms to the evolutionary dynamics surrounding its development and diversification. Science, this issue p. eaan0221 BACKGROUND The interdisciplinary field of animal coloration is growing rapidly, spanning questions about the diverse ways that animals use pigments and structures to generate color, the underlying genetics and epigenetics, the perception of color, how color information is integrated with information from other senses, and general principles underlying color’s evolution and function. People working in the field appreciate linkages between these parallel lines of enquiry, but outsiders need the easily navigable roadmap that we provide here. ADVANCES In the past 20 years, the field of animal coloration research has been propelled forward by technological advances that include spectrophotometry, digital imaging, computational neuroscience, innovative laboratory and field studies, and large-scale comparative analyses, which are allowing new questions to be asked. For example, we can now pose questions about the evolution of camouflage based on what a prey’s main predator can see, and we can start to appreciate that gene changes underlying color production have occurred in parallel in unrelated species. Knowledge of the production, perception, and evolutionary function of coloration is poised to make contributions to areas as diverse as medicine, security, clothing, and the military, but we need to take stock before moving forward. OUTLOOK Here, a group of evolutionary biologists, behavioral ecologists, psychologists, optical physicists, visual physiologists, geneticists, and anthropologists review this diverse area of science, daunting to the outsider, and set out what we believe are the key questions for the future. These are how nanoscale structures are used to manipulate light; how dynamic changes in coloration occur on different time scales; the genetics of coloration (including key innovations and the extent of parallel changes in different lineages); alternative perceptions of color by different species (including wavelengths that we cannot see, such as ultraviolet); how color, pattern, and motion interact; and how color works together with other modalities, especially odor. From an adaptive standpoint, color can serve several functions, and the resulting patterns frequently represent a trade-off among different evolutionary drivers, some of which are nonvisual (e.g., photoprotection). These trade-offs can vary between individuals within the same population, and color can be altered strategically on different time scales to serve different purposes. Lastly, interspecific differences in coloration, sometimes even observable in the fossil record, give insights into trait evolution. The biology of color is a field that typifies modern research: curiosity-led, technology-driven, multilevel, interdisciplinary, and integrative. Spectacular changes to color and morphology in a cuttlefish. Color can conceal or reveal. The giant Australian cuttlefish (Sepia apama) alters the relative size of its pigment-bearing chromatophores and warps its muscular skin to switch between camouflage mode (top) and communication mode (bottom) in under a second. Photos:

Prey community structure affects how predators select for Müllerian mimicry

Müllerian mimicry describes the close resemblance between aposematic prey species; it is thought to be beneficial because sharing a warning signal decreases the mortality caused by sampling by inexperienced predators learning to avoid the signal. It has been hypothesized that selection for mimicry is strongest in multi-species prey communities where predators are more prone to misidentify the prey than in simple communities. In this study, wild great tits (Parus major) foraged from either simple (few prey appearances) or complex (several prey appearances) artificial prey communities where a specific model prey was always present. Owing to slower learning, the model did suffer higher mortality in complex communities when the birds were inexperienced. However, in a subsequent generalization test to potential mimics of the model prey (a continuum of signal accuracy), only birds that had foraged from simple communities selected against inaccurate mimics. Therefore, accurate mimicry is more likely to evolve in simple communities even though predator avoidance learning is slower in complex communities. For mimicry to evolve, prey species must have a common predator; the effective community consists of the predators diet. In diverse environments, the limited diets of specialist predators could create ‘simple community pockets’ where accurate mimicry is selected for.

Mimicry between unequally defended prey can be parasitic: evidence for quasi‐Batesian mimicry

The nature of signal mimicry between defended prey (known as Müllerian mimicry) is controversial. Some authors assert that it is always mutualistic and beneficial, whilst others speculate that less well defended prey may be parasitic and degrade the protection of their better defended co-mimics (quasi-Batesian mimicry). Using great tits (Parus major) as predators of artificial prey, we show that mimicry between unequally defended co-mimics is not mutualistic, and can be parasitic and quasi-Batesian. We presented a fixed abundance of a highly defended model and a moderately defended dimorphic (mimic and distinct non-mimetic) species, and varied the relative frequency of the two forms of the moderately defended prey. As the mimic form increased in abundance, per capita predation on the model-mimic pair increased. Furthermore, when mimics were rare they gained protection from predation but imposed no co-evolutionary pressure on models. We found that the feeding decisions of the birds were affected by their individual toxic burdens, consistent with the idea that predators make foraging decisions which trade-off toxicity and nutrition. This result suggests that many prey species that are currently assumed to be in a simple mutualistic mimetic relationship with their co-mimic species may actually be engaged in an antagonistic co-evolutionary process.