Organisms possess a wide variety of strategies for avoiding predation. Crypsis provides a means of avoiding detection; aposematism makes use of warning colouration; mimicry imitates an organism that has better defenses; masquerade "closely resembles inedible and generally inanimate objects". Graeme Ruxton and Michael Speed, who were coauthors of a book on this general theme, have recently coauthored a research paper on masquerade.
"Plants from the genus Lithops look remarkably like stones; stick insects resemble twigs; the Amazon fish Monocirrhus polyacanthus is visually almost indistinguishable from leaves, and birds from the family Nyctibiidae bear an uncanny likeness to tree stumps."

Leaf insects set a high standard for looking like something that's inedible (Credit: (Kirsty Wigglesworth/AP Photo, source here)
My personal favourite examples relate to stick insects and leaf insects. Not only do stick insects resemble the plants on which they live, they sway just as though they are being fanned by a gentle breeze. Furthermore, their eggs look exactly like their own fecal pellets. Newly emerged leaf insects have beautifully formed leafy appendages that allow them to blend in immediately with their surroundings. These characteristics, whilst remarkable, have not been seriously researched:
"one aspect of adaptive coloration has been almost completely ignored: masquerade."
The first research challenge is to determine whether masquerade is a distinctive phenomenon or another form of crypsis. The two relevant hypotheses are:
(a) The predator detects but misidentifies the prey (masquerade)
(b) The predator fails to detect the prey (crypsis)
The researchers set up a set of experiments using domestic chicks as predators and two species of twig-resembling caterpillars. The experimental area contained a hawthorn branch with twigs and leaves. Some experiments were undertaken with a branch that had been bound in purple cotton thread to change its visual appearance.
"Birds with prior experience of twigs took longer to attack both species of twig-resembling caterpillars, and handled them more cautiously, compared with birds that had either no experience of twigs or experience only of twigs whose visual appearance had been manipulated by binding them in colored thread. Our results show that masquerade functions to promote misidentification of the masquerading organism."
Thus far, the authors have demonstrated that hypothesis (a) above is substantiated. Then, in their paper, they proceed with an evolutionary explanation of the phenomenon.
"Our results show that predators' cognitive strategies (recognition and identification), rather than their sensory capabilities, are the selective force driving the evolution of masquerade and raise the possibility that predator cognition may be a more important selective agent than previously realized."
It is a fair conclusion to say that cognitive strategies are significant, as all the birds were able to sense the caterpillars. However, what is the rationale for saying that cognitive strategies have "driven the evolution of masquerade"? Can these experiments tell us anything about the origins of the phenomenon? They tell us that predation is affected by the predator's cognitive strategies, but not that these same strategies have driven the evolution of masquerade as an adaptive response. At best, this is an initial hypothesis awaiting testing. It is a hypothesis based on the assumptions of Darwinism - that masquerade is an adaptation driven by natural selection. To claim this as a conclusion is an indication that theory, rather than data, is dictating the outcome.
The examples of natural selection that we do have fall far short of showing the reasonableness of identifying it as the mechanism for explaining masquerade. We have finch beak length changes, lizard leg length changes, peppered moth colouration, and the like. To demonstrate the reasonableness of explaining masquerade in this way means having multiple factors - including behavioural - all responding to the same selection pressure. Such evidence may be forthcoming but, in the words of the authors (in a different context): "there is certainly no empirical evidence to support this theory". Instead, it is appropriate to propose multiple working hypotheses and proceed to construct ways of testing them. In particular, we can note here the hypothesis that organisms are designed with the potential for radiations linked to adaptive, developmental and epigenetic factors.
Masquerade: Camouflage Without Crypsis
John Skelhorn, Hannah M. Rowland, Michael P. Speed, and Graeme D. Ruxton
Science 327, 1 January 2010: 51.
Abstract: 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.
See also:
Tyler, D., Stasis in the fossil record of leaf insects, ARN Literature Blog (14 January 2007)
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