Colour change of twig-mimicking peppered moth larvae is a continuous reaction norm that increases camouflage against avian predators

Abstract

Camouflage, and in particular background-matching, is one of the most common anti-predator strategies observed in nature. Animals can improve their match to the colour/pattern of their surroundings through background selection, and/or by plastic colour change. Colour change can occur rapidly (a few seconds), or it may be slow, taking hours to days. Many studies have explored the cues and mechanisms behind rapid colour change, but there is a considerable lack of information about slow colour change in the context of predation: the cues that initiate it, and the range of phenotypes that are produced. Here we show that peppered moth (Biston betularia) larvae respond to colour and luminance of the twigs they rest on, and exhibit a continuous reaction norm of phenotypes. When presented with a heterogeneous environment of mixed twig colours, individual larvae specialise crypsis towards one colour rather than developing an intermediate colour. Flexible colour change in this species has likely evolved in association with wind dispersal and polyphagy, which result in caterpillars settling and feeding in a diverse range of visual environments. This is the first example of visually induced slow colour change in Lepidoptera that has been objectively quantified and measured from the visual perspective of natural predators.

Keywords: Biston betularia; Camouflage; Colour change; Masquerade; Polyphenism; Predator-prey interactions; Reaction norm.

Figure 1. Possible camouflage strategies of caterpillars in response to visually heterogeneous environments.

(A) In an environment composed of different coloured patches, caterpillars with a fixed genetic phenotype achieve compromised crypsis on all backgrounds. (B) The same habitat scenario as A but with larvae specialised to match one patch type, either by genetic polymorphism, restricting individuals to one patch colour, or by plastic polyphenism, in principle allowing individual larvae to move between patches and switch colour to match their background. (C) Larvae with genetic polymorphism or plastic polyphenism inhabiting a graded environment with intermediate colour patches, where phenotypes match the extreme, but not the intermediate backgrounds. (D) An environmental gradient with intermediate backgrounds, where larvae produce a continuous colour response to background colour, allowing utilisation of each patch colour.

Figure 2. Dowels used for luminance, colour, and heterogeneous environment experiments.

(A–L) represent IB, IG, Bl, BW1, BW2, BW3, Wh, Br, BG1, BG2, BG3, and Gr, respectively.

Figure 3. The response of B. betularia larvae to a difference in dowel colour.

(A) Representative final instar B. betularia larvae from each isoluminant treatment resting on their corresponding dowel. (B) The average position of final instar B. betularia larvae and their corresponding dowels within the ultraviolet-sensitive (UVS) avian tetrahedral colour space when viewed by a blue tit, Cyanistes caeruleus, under bright daylight conditions. Asterisks represent dowels, rhombuses represent larvae, from brown and green treatments, respectively. The plot illustrates the stimulation of the short (S), medium (M), long (L), and UV (U/V) wavelength-sensitive photoreceptors and is shown from the MW–LW plane. (C) Greenness as perceived by a blue tit under bright daylight conditions of final instar B. betularia larvae reared under isoluminant dowel treatments, where IBL, isoluminant brown larvae and IGL, isoluminant green larvae. The numbers following the letters indicate replicate boxes within each treatment. IBD, isoluminant brown dowel and IGD, isoluminant green dowel. Photo credit: Arjèn Van’t Hof.

Figure 4. The response of B. betularia larvae to a gradient in dowel luminance.

(A) Representative final instar B. betularia larvae from each luminance treatment resting on their corresponding dowel. Dowel treatments shown from left to right: Black (Bl), Dark grey (BW1), Mid grey (BW2), Light grey (BW3), White (Wh). (B) Average luminance of final instar B. betularia larvae reared under the five luminance treatments, as perceived by a blue tit (Cyanistes caeruleus) under bright daylight conditions. Solid line is the fitted cubic polynomial; dotted and dashed lines, provided for comparison, represent the linear (idealised continuous reaction norm) and stepped (two-state polyphenism) responses, respectively. Photo credit: Arjèn Van’t Hof.

Figure 5. The response of B. betularia larvae to a gradient in dowel colour and luminance.

(A) Photograph of final instar B. betularia larvae from each colour treatment resting on their corresponding dowel. Dowel treatments shown from left to right: Brown (Br), More brown (BG1), Brown-green (BG2), More green (BG3), Green (Gr). (B) Average greenness of dowels vs. B. betularia larvae exposed to dowels from each of the five treatment groups, as perceived by a blue tit (Cyanistes caeruleus) under bright daylight conditions. Solid line is the fitted quadratic polynomial; dotted and dashed lines, provided for comparison, represent the linear (idealised continuous reaction norm) and stepped (two-state polyphenism) responses, respectively. Photo credit: Lukasz Lukomski.

Figure 6. The response of B. betularia larvae to different ratios of green and brown dowels.

Percentage of green dowels in each treatment vs. the percentage of greenness of B. betularia larva as calculated by RGB analysis.