A bird's eye view of the peppered moth M. E. N. MAJERUS, C. F. A. BRUNTON & J. STALKER Department of Genetics, University of Cambridge, Downing Street, Cambridge CB2 3EH, UK Keywords: Abstract Biston betularia; Industrial melanism in Biston betularia is one of the best known examples of crypsis; the role of natural selection in evolution and has received considerable lichen; scrutiny for many years. The rise in frequency of the dark form of the moth melanism; (carbonaria) and a decrease in the pale form (typica) was the result of predation; differential predation by birds, the melanic form being more cyptic than typica ultraviolet. in industrial areas where the tree bark was darkened by air pollution. One important aspect of early work evaluating the relative crypsis of the forms of B. betularia on tree trunks with different lichen ¯ora was the reliance on human observers. Humans, however, do not have the same visual capabilities as birds. Birds have well-developed ultraviolet (UV) vision, an important component of their colour processing system that affects many aspects of behaviour, including prey detection. We examined the UV characteristics of the two forms of B. betularia and a number of foliose and crustose lichens. In human visible light the speckled form typica appeared cyptic when seen against a background of foliose lichen, whereas the dark form carbonaria was conspic- uous. Under UV light the situation was reversed. The foliose lichens absorbed UV and appeared dark as did carbonaria. Typica, however, re¯ected UV and was conspicuous. Against crustose lichens, typica was less visible than carbonaria in both visible and UV light. These ®ndings are considered in relation to the distribution and recolonization of trees by lichens and the resting behaviour of B. betularia. luted woodlands in the 1950s (Kettlewell, 1955, 1956). Introduction The typical, nonmelanic form is well camou¯aged when Industrial melanism in the peppered moth, Biston betu- at rest on trunks covered by foliose lichens, while laria Linn., has been, and is, one of the most widely carbonaria is the more cryptic on bark denuded of lichens quoted examples of evolution in action. During the latter by sulphur dioxide and darkened by particulate air half of the nineteenth century, the white and black pollution (Kettlewell, 1955). Because of the importance speckled form, typica, was all but replaced by the melanic of this case as an example of the role of natural selection form, carbonaria, in many industrial regions, but not in in evolution, the detail of the system has received rural areas little affected by industrial pollution (Tutt, considerable scrutiny over the last four decades (see 1896; Kettlewell, 1973). The rise in the frequency of Majerus, 1998, and references therein). For example, it is carbonaria was a consequence of differential predation of now generally recognized that B. betularia rarely rest by the forms by birds, as demonstrated by Kettlewell's day on tree trunks, preferring to rest higher in the canopy classical predation experiments in polluted and unpol- under horizontal branches and twigs (Kettlewell, 1958; Mikkola, 1979; Howlett & Majerus, 1987; Liebert & Brake®eld, 1987). Correspondence: Dr M. E. N. Majerus, Department of Genetics, University of Cambridge, Downing Street, Cambridge CB2 3EH, UK. One point of controversy that still exists in this case is Tel.: +44 1223 333999; fax: +44 1223 333992; the in¯uence of epiphytic lichens on the relative crypsis e-mail: [email protected] of the forms of B. betularia. A crucial element in J. EVOL. BIOL. 13 (2000) 155±159 ã 2000 BLACKWELL SCIENCE LTD 155 156 M. E. N. MAJERUS ET AL. Kettlewell's initial work on levels of bird predation on Methods and results this species involved evaluation of the relative crypsis of typica and carbonaria on tree trunks with different lichen Lichens were collected from native, deciduous trees in ¯oras. Assessment was made by placing moths of either the New Forest, Hampshire, and Chobham Common, form on oak trunks and assessing the distance from the Surrey, UK, and brought to the laboratory where dead trunks that human observers found them indistinguish- moths of both forms, typica and carbonaria, were placed able from their background. Similar techniques have upon them. These were then viewed with a video been used by other workers subsequently (e.g. Steward, camera, ®rst in human visible light (>400 nm) and then 1977a). The correlation between the frequency of typica in UV light only (300±400 nm). A video camera sensitive and foliose or vegetative lichens has been stressed on to UV light was used to record the images. many occasions (Bishop, 1972; Kettlewell, 1973; Bishop All of the foliose lichens examined (Table 1) absorbed et al., 1978a,b; Liebert & Brake®eld, 1987). However, UV and thus appeared black in the pictures. The recent monitoring of the decline in carbonaria frequency, carbonaria moth also absorbed UV, as did the black areas following antipollution legislation in the 1950s and of the typica form. However, the white scales of typica subsequently, has failed to reveal a consistent correlation re¯ected UV strongly and were clearly visible under UV between the concomitant increase in typica and regrowth illumination. Some parts of the crustose lichens including of lichens, either in Britain (Clarke et al., 1985) or in the Leucanora conizaeoides also re¯ected UV while other parts USA (Grant et al., 1995, 1996). These ®ndings have been absorbed it, giving a speckled effect, similar to that of criticised on the grounds that the assessment of changes typica. The inclusion of L. conizaeoides is important as Cook in the lichen ¯ora in relevant locations was not et al. (1990) have noted that this is the most tolerant systematic, and that the assessment was made of lichen lichen to atmospheric pollution and is one of the ®rst recolonization on tree trunks rather than in the canopy species to recolonize. where B. betularia rests by day (Majerus, 1998). Further- While the carbonaria form of the peppered moth was more, other workers have recorded increases in lichens obviously more visible than the typica form in the human following antipollution legislation (e.g. Brake®eld, 1990; `visible' spectrum (>400 nm) when the two were set Cook et al., 1990). against bark covered in foliose lichens (Fig. 1a), the Here, we wish to add to the debate by considering reverse was the case in the UV spectrum (Fig. 1b). another aspect of the possible connection between the Conversely, when set against crustose lichens, typica was relative crypsis of the forms of B. betularia and lichens. less visible than carbonaria, both in human `visible' and Many studies of the role and ef®cacy of defensive colour UV light. patterns in species preyed on by birds have made the This ®nding may be considered in relation to the erroneous assumption that avian vision is similar to, or distribution of lichens on trees and the little that is the same as, that possessed by humans (i.e. colour vision known about the resting behaviour of B. betularia. sensitive to light of wavelengths between 400 and 700 nm). Ultraviolet light (wavelengths less than Discussion 400 nm) is qualitatively no different to human `visible' light, merely being made up of a ¯ow of photons of In parts of rural Britain which have been exposed to shorter wavelengths and, thus, correspondingly higher relatively low levels of atmospheric pollution, foliose energy. Many organic molecules, including DNA, are lichens occur mainly on the less shaded and wetter sides damaged if they absorb the high energy of UV wave- of trunks, upper surfaces of main branches, and more lengths. Thus, human eyes are protected from UV by the generally within the canopy, growing more on upper presence of shielding pigments in the lens and the surfaces of lateral branches and twigs (Liebert & Brake- cornea. Although humans are almost UV-blind, many ®eld, 1987). Crustose lichens occur on these surfaces as insects, ®sh, reptiles, amphibians and birds do not have shielding pigments, and, as a result, are sensitive to UV Table 1 Species of lichen used in the study. All the foliose species wavelengths. Indeed, in many taxonomic groups, absorbed UV light and appeared black in the pictures. Some parts of including Lepidoptera and birds, UV vision appears to the crustose species re¯ected UV while other parts absorbed it giving be well developed, and forms an important component of a speckled effect. their colour processing system relating to many aspects of Crustose species Foliose species behaviour, such as mate recognition and prey detection (Silberglied & Taylor, 1978; Chen et al., 1984; Burkhardt Lecanora chlarotera Hypogymnia sp. & Maier, 1989; Bennett & Cuthill, 1994; Brunton & Lecanora conizaeoides Evernia sp. Majerus, 1995; Brunton et al., 1996). This led us to Lecanora expallens Parmelia acetabulum examine the UV characteristics of B. betularia and a small Lecidea quernea Parmelia saxatilis range of foliose and crustose lichens. Lecidella elaeochroma Parmelia sulcata Ochrolechia yasudae Physcia leptalea Physcia aipolia J. EVOL. BIOL. 13 (2000) 155±159 ã 2000 BLACKWELL SCIENCE LTD A bird's eye view of the pepper moth 157 Fig. 1 The two forms of Biston betularia on foliose lichen (Hypogymnia sp.) as they would look in normal `visible' light (a), and under UV illumination (b). Images were captured from video ®lm. well, and dominate on trunks and the lower surfaces of foliose lichens, which are more susceptible to pollutants main branches. In regions exposed to high pollution than are some crustose species, tend to be rare and levels, lichens are rare on trees, usually only Lecanora restricted to small patches on the upper surfaces of some conizaeoides being found, and even this species being branches or branchlets (Liebert & Brake®eld, 1987).