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Optimizing Countershading Camouflage Optimizing countershading camouflage Innes C. Cuthilla,1, N. Simon Sangheraa, Olivier Penacchiob, Paul George Lovellc, Graeme D. Ruxtond, and Julie M. Harrisb aSchool of Biological Sciences, University of Bristol, Bristol BS8 1TQ, United Kingdom; bSchool of Psychology and Neuroscience, University of St. Andrews, St. Andrews, Fife KY16 9JP, United Kingdom; cDivision of Psychology, Social and Health Sciences, Abertay University, Dundee DD1 1HG, United Kingdom; and dSchool of Biology, University of St Andrews, St Andrews, Fife KY16 9TH, United Kingdom Edited by Raghavendra Gadagkar, Indian Institute of Science, Bangalore, India, and approved September 30, 2016 (received for review July 14, 2016) Countershading, the widespread tendency of animals to be darker rates on animals with or without the observed coloration, we on the side that receives strongest illumination, has classically cannot tell whether there is a causal effect on detectability. been explained as an adaptation for camouflage: obliterating cues Although some tests with artificial prey show reduced avian to 3D shape and enhancing background matching. However, there predation rates on two-tone, dorsally darker treatments (21–24), have only been two quantitative tests of whether the patterns the relationship between the color contrasts in these experiments observed in different species match the optimal shading to obliter- and the predicted optima are unknown. We have recently filled ate 3D cues, and no tests of whether optimal countershading this important gap by using a general theory of optimal coun- actually improves concealment or survival. We use a mathematical tershading to derive the predicted optimal patterns for different model of the light field to predict the optimal countershading for weather conditions at a specific location, time of year and day concealment that is specific to the light environment and then test (25). Modeling of the light field shows that a sharp transition this prediction with correspondingly patterned model “caterpillars” between dark and light, as used in previous experimental studies, exposed to avian predation in the field. We show that the optimal provides optimal countershading only in direct, overhead sun- countershading is strongly illumination-dependent. A relatively light (25). Only one of the previous experimental studies (24) sharp transition in surface patterning from dark to light is only was carried out under conditions where direct sun was a plau- optimal under direct solar illumination; if there is diffuse illumina- sible illuminant, the others taking place in woodland (22) or tion from cloudy skies or shade, the pattern provides no advantage including trials with overcast or rainy weather (21), or carried out over homogeneous background-matching coloration. Conversely, a in winter (21, 23). This mismatch between the illuminant and the smoother gradation between dark and light is optimal under cloudy correct countershading pattern, and the fact that all previous skies or shade. The demonstration of these illumination-dependent experiments involved trials lasting throughout the day, when the effects of different countershading patterns on predation risk sun is continually moving and so very different patterns of strongly supports the comparative evidence showing that the type countershading are required for camouflage, raises the possi- of countershading varies with light environment. bility that factors other than self-shadow concealment [e.g., dis- ruptive coloration (9, 13, 26, 27)] were responsible for detection camouflage | defensive coloration | animal coloration | differences. A strong test of the self-shadow concealment theory shape-from-shading | shape perception of countershading therefore requires proof that the survival ben- efits are illumination dependent. Here, we have tested the illu- any animals, across diverse taxa and habitats, are darker mination dependence of countershading empirically by measuring Mon their dorsal than ventral side (1–8). One of the oldest avian predation on artificial caterpillar-like prey with these puta- theories of animal camouflage (9–13) suggests that this “coun- tively optimized patterns, under different illumination conditions. tershading” has evolved to cancel the dorsoventral gradient of We produced large numbers of cylindrical paper “caterpillars” illumination across the body, thus obliterating cues to 3D form with different dorsoventral color gradients. Two were designed and enhancing background matching. Indeed, so common are dorsoventral gradients of pigmentation that Abbott Thayer Significance branded his explanation as “The law which underlies protective coloration” (12). Countershading also became one of the most popular early tactics in military camouflage (14, 15). However, Because the sun and sky are above us, natural illumination is somewhat ironically, given that the theory was inspired by ob- directional and the cues from shading reveal shape and depth. servations of nature, a role in biological camouflage remains However, many animals are darker on their backs and, over equivocal. The present paper uses predation rate to test directly 100 years ago, it was proposed that this phenomenon was whether countershading affects detectability and the degree to camouflage: countering the cues to shape that directional il- which the pattern has to be tightly matched to the illumination lumination creates. However, does this camouflage work in conditions to be effective. practice? We predicted the optimal countershading for differ- ent lighting conditions and tested this possibility with corre- Assessments of coat pattern in relation to positional behavior “ ” and body size in primates are consistent with the pattern func- spondingly patterned model caterpillars predated by birds in tioning as camouflage (5, 16). Primate species that spend more the wild. Predation rates varied with coloration and lighting in time oriented vertically, and thus do not experience strong dif- exactly the manner predicted. Such subtlety in the effects of ferential illumination between belly and back, are less intensely countershading vindicates conclusions from prior evidence countershaded. The most powerful quantitative test to date used demonstrating stronger countershading in animals in more ECOLOGY empirically derived predictions from the pattern of illumination brightly lit habitats. on a model deer under different illumination conditions (1). This Author contributions: I.C.C., O.P., P.G.L., G.D.R., and J.M.H. designed research; I.C.C. and study found a broad correspondence between correlates of illu- N.S.S. performed research; O.P. and P.G.L. contributed analytic tools; I.C.C. and N.S.S. mination and the observed countershading on 114 species of analyzed data; and I.C.C., N.S.S., O.P., P.G.L., and J.M.H. wrote the paper. ruminant. Such a comparative approach provides powerful cor- The authors declare no conflict of interest. relative evidence for countershading as an adaptation to lighting This article is a PNAS Direct Submission. conditions but, of itself, does not prove that camouflage is the Data deposition: The data reported in this paper have been deposited in the Dryad Digital function being optimized. One problem is that the predictions Repository (dx.doi.org/10.5061/dryad.rd47f). This facility has been approved by the UK for UV protection are very similar to those for optimized cam- research councils and fulfils our funder’s requirements. ouflage (17–20). Therefore, without measurement of predation 1To whom correspondence should be addressed. Email: [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.1611589113 PNAS | November 15, 2016 | vol. 113 | no. 46 | 13093–13097 Downloaded by guest on September 30, 2021 to counterbalance direct sun or diffuse illumination and so each should be the optimal countershading in its own, and only its Illuminant own, light environment (Fig. 1). Control patterns were uniform or two-tone. We then attached these patterns to vegetation, in a diffuse direct randomized block design, on both sunny and cloudy days, directly in sun or in shade. We predicted that countershading optimized Light 28:75 16:36 for the prey-specific illumination conditions would suffer lower predation rates by wild birds than those with countershading op- SunnyMean timized for different lighting, or with no countershading at all. 46:60 21:30 Results CloudyMean 78:26 27:25 We can model illumination conditions at the level of the indi- vidual prey item or at the level of the block. The former provided TwoToneCS a better fit to the data [Akaike’s information criterion (AIC): 68:41 30:15 1,166.8 vs. 1,179.2, both models with treatment and illumination Dark condition and their interaction as fixed effects, with block as a 82:21 33:19 random effect; Materials and Methods]. The results that follow (and shown in Fig. 2) therefore refer to the former model CloudyCS 98:8 37:11 structure. The treatment by illumination interaction was significant (χ2 = SunnyCS 28.08; df = 6; P < 0.0001). (Note that modeling illumination 80:23 49:5 conditions at the level of the block also gave a significant treatment by illumination interaction: χ2 = 15.65; df = 6; P = 0 255075100 0255075100 0.0158.) Because the interaction was significant, we performed % alive separate analyses for diffuse and direct illumination. For diffuse χ2 = = P < illumination, treatment was significant ( 171.39; df 6; Fig. 2. Proportion surviving (mean ± SEM) in each treatment and illumi- 0.0001), with the countershaded
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