SEARCH

SEARCH BY CITATION

Keywords:

  • Biston betularia;
  • crypsis;
  • lichen;
  • melanism;
  • predation;
  • ultraviolet

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods and results
  5. Discussion
  6. Acknowledgments
  7. References

Industrial melanism in Biston betularia is one of the best known examples of the role of natural selection in evolution and has received considerable scrutiny for many years. The rise in frequency of the dark form of the moth (carbonaria) and a decrease in the pale form (typica) was the result of differential predation by birds, the melanic form being more cyptic than typica 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 flora 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 conspicuous. Under UV light the situation was reversed. The foliose lichens absorbed UV and appeared dark as did carbonaria. Typica, however, reflected UV and was conspicuous. Against crustose lichens, typica was less visible than carbonaria in both visible and UV light. These findings are considered in relation to the distribution and recolonization of trees by lichens and the resting behaviour of B. betularia.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods and results
  5. Discussion
  6. Acknowledgments
  7. References

Industrial melanism in the peppered moth, Biston betularia Linn., has been, and is, one of the most widely quoted examples of evolution in action. During the latter half of the nineteenth century, the white and black speckled form, typica, was all but replaced by the melanic form, carbonaria, in many industrial regions, but not in rural areas little affected by industrial pollution ( Tutt, 1896; Kettlewell, 1973). The rise in the frequency of carbonaria was a consequence of differential predation of the forms by birds, as demonstrated by Kettlewell’s classical predation experiments in polluted and unpolluted woodlands in the 1950s ( Kettlewell, 1955, 1956). The typical, nonmelanic form is well camouflaged when at rest on trunks covered by foliose lichens, while carbonaria is the more cryptic on bark denuded of lichens by sulphur dioxide and darkened by particulate air pollution ( Kettlewell, 1955). Because of the importance of this case as an example of the role of natural selection in evolution, the detail of the system has received considerable scrutiny over the last four decades (see Majerus, 1998, and references therein). For example, it is now generally recognized that B. betularia rarely rest by day on tree trunks, preferring to rest higher in the canopy under horizontal branches and twigs ( Kettlewell, 1958; Mikkola, 1979; Howlett & Majerus, 1987; Liebert & Brakefield, 1987).

One point of controversy that still exists in this case is the influence of epiphytic lichens on the relative crypsis of the forms of B. betularia. A crucial element in Kettlewell’s initial work on levels of bird predation on this species involved evaluation of the relative crypsis of typica and carbonaria on tree trunks with different lichen floras. Assessment was made by placing moths of either form on oak trunks and assessing the distance from the trunks that human observers found them indistinguishable from their background. Similar techniques have been used by other workers subsequently (e.g. Steward, 1977a). The correlation between the frequency of typica and foliose or vegetative lichens has been stressed on many occasions ( Bishop, 1972; Kettlewell, 1973; Bishop et al., 1978a , b; Liebert & Brakefield, 1987 ). However, recent monitoring of the decline in carbonaria frequency, following antipollution legislation in the 1950s and subsequently, has failed to reveal a consistent correlation between the concomitant increase in typica and regrowth of lichens, either in Britain ( Clarke et al., 1985 ) or in the USA ( Grant et al., 1995 , 1996). These findings have been criticised on the grounds that the assessment of changes in the lichen flora in relevant locations was not systematic, and that the assessment was made of lichen recolonization on tree trunks rather than in the canopy where B. betularia rests by day ( Majerus, 1998). Furthermore, other workers have recorded increases in lichens following antipollution legislation (e.g. Brakefield, 1990; Cook et al., 1990 ).

Here, we wish to add to the debate by considering another aspect of the possible connection between the relative crypsis of the forms of B. betularia and lichens. Many studies of the role and efficacy of defensive colour patterns in species preyed on by birds have made the erroneous assumption that avian vision is similar to, or the same as, that possessed by humans (i.e. colour vision sensitive to light of wavelengths between 400 and 700 nm). Ultraviolet light (wavelengths less than 400 nm) is qualitatively no different to human ‘visible’ light, merely being made up of a flow of photons of shorter wavelengths and, thus, correspondingly higher energy. Many organic molecules, including DNA, are damaged if they absorb the high energy of UV wavelengths. Thus, human eyes are protected from UV by the presence of shielding pigments in the lens and the cornea. Although humans are almost UV-blind, many insects, fish, reptiles, amphibians and birds do not have shielding pigments, and, as a result, are sensitive to UV wavelengths. Indeed, in many taxonomic groups, including Lepidoptera and birds, UV vision appears to be well developed, and forms an important component of their colour processing system relating to many aspects of behaviour, such as mate recognition and prey detection ( Silberglied & Taylor, 1978; Chen et al., 1984 ; Burkhardt & Maier, 1989; Bennett & Cuthill, 1994; Brunton & Majerus, 1995; Brunton et al., 1996 ). This led us to examine the UV characteristics of B. betularia and a small range of foliose and crustose lichens.

Methods and results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods and results
  5. Discussion
  6. Acknowledgments
  7. References

Lichens were collected from native, deciduous trees in the New Forest, Hampshire, and Chobham Common, Surrey, UK, and brought to the laboratory where dead moths of both forms, typica and carbonaria, were placed upon them. These were then viewed with a video camera, first in human visible light (>400 nm) and then in UV light only (300–400 nm). A video camera sensitive to UV light was used to record the images.

All of the foliose lichens examined (Table 1) absorbed UV and thus appeared black in the pictures. The carbonaria moth also absorbed UV, as did the black areas of the typica form. However, the white scales of typica reflected UV strongly and were clearly visible under UV illumination. Some parts of the crustose lichens including Leucanora conizaeoides also reflected UV while other parts absorbed it, giving a speckled effect, similar to that of typica. The inclusion of L. conizaeoides is important as Cook et al. (1990 ) have noted that this is the most tolerant lichen to atmospheric pollution and is one of the first species to recolonize.

Table 1.   Species of lichen used in the study. All the foliose species absorbed UV light and appeared black in the pictures. Some parts of the crustose species reflected UV while other parts absorbed it giving a speckled effect. Thumbnail image of

While the carbonaria form of the peppered moth was obviously more visible than the typica form in the human ‘visible’ spectrum (>400 nm) when the two were set against bark covered in foliose lichens ( Fig. 1a), the reverse was the case in the UV spectrum ( Fig. 1b). Conversely, when set against crustose lichens, typica was less visible than carbonaria, both in human ‘visible’ and UV light.

image

Figure 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 film.

Download figure to PowerPoint

This finding may be considered in relation to the distribution of lichens on trees and the little that is known about the resting behaviour of B. betularia.

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods and results
  5. Discussion
  6. Acknowledgments
  7. References

In parts of rural Britain which have been exposed to relatively low levels of atmospheric pollution, foliose lichens occur mainly on the less shaded and wetter sides of trunks, upper surfaces of main branches, and more generally within the canopy, growing more on upper surfaces of lateral branches and twigs ( Liebert & Brakefield, 1987). Crustose lichens occur on these surfaces as well, and dominate on trunks and the lower surfaces of main branches. In regions exposed to high pollution levels, lichens are rare on trees, usually only Lecanora conizaeoides being found, and even this species being absent from the most heavily polluted localities ( Cook et al., 1990 ). In areas subjected to moderate air pollution, foliose lichens, which are more susceptible to pollutants than are some crustose species, tend to be rare and restricted to small patches on the upper surfaces of some branches or branchlets ( Liebert & Brakefield, 1987). The pattern of recent recolonization of trees by lichens, following reductions in pollution levels, is also of interest. Initial recolonization of older trees tends to be on new branch growth in the canopy, with low residual surface pollution and comparatively high light intensity ( Brakefield, 1987). Trunks are the last areas of the trees to be recolonized, largely as a result of the down-wash of pollutants onto the trunk. The first species to return is usually L. conizaeoides, followed by other crustose lichens, with foliose lichens lagging some way behind ( Cook et al., 1990 ).

It is our view that the peppered moth habitually rests by day on the undersurfaces of horizontal branches and twigs, and that its colour pattern provides an effective cryptic match, both in the human-visible and UV spectra, to the crustose lichens that grow on such surfaces. We contend that the failure of some workers to find a correlation between recent increases in typica and increases in lichens is a consequence of monitoring lichens on the wrong parts of trees, i.e. the trunks rather than the branches, and including in the assessment the wrong types of lichens, i.e. foliose species.

While we are confident that differences in the relative crypsis of the forms of the peppered moth, leading to differential bird predation of these forms, has been, and is, crucial to the temporal and spatial changes in frequencies of the forms, it is our view that past attempts to assess the relative fitnesses of the forms, using formal predation experiments, have been flawed for two reasons. First, moths have been placed out on the wrong parts of trees (e.g. Howlett & Majerus, 1987; Majerus, 1989). Second, moths have been placed out in positions appropriate to their phenotype on the basis of human perception, without consideration of the UV element of the moths’ pattern, or that of the substrates. The same criticism may be made of assessments of the relative crypsis of the forms of the peppered moth in different regions when these have been made by humans, with moths placed on tree trunks. The inclusion of these flawed assessments in multiple regression analyses (e.g. Lees et al., 1973 ; Bishop et al., 1975 ; Steward, 1977a, b) will lead to misleading deductions of the importance of crypsis, relative to other variables, in the evolution of melanism, at least in the case of the peppered moth.

Acknowledgments

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods and results
  5. Discussion
  6. Acknowledgments
  7. References

We thank Laurence Hurst for helpful comments on the text and MedIT Ltd for technical assistance. C.F.A.B. was supported by a grant from NERC.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods and results
  5. Discussion
  6. Acknowledgments
  7. References
  • 1
    Bennett, A.T.D. & Cuthill, I.C. 1994. Ultraviolet vision in birds: what is its function? Vis. Res. 34: 1471 1478.
  • 2
    Bishop, J.A. 1972. An experimental study of the cline of industrial melanism in Biston betularia (L.) (Lepidoptera) between urban Liverpool and rural North Wales . J. Anim. Ecol. 41: 209 243.
  • 3
    Bishop, J.A., Cook, L.M., Muggleton, J., Seaward, M.R.D. 1975. Moths, lichens and air pollution along a transect from Manchester to north Wales. J. Appl. Ecol. 12: 83 98.
  • 4
    Bishop, J.A., Cook, L.M., Muggleton, J. 1978a. The response of two species of moths to industrialization in northwest England. I. Polymorphism for melanism. Phil. Trans. Royal Soc. Lond. B 281: 489 515.
  • 5
    Bishop, J.A., Cook, L.M., Muggleton, J. 1978b. The response of two species of moths to industrialization in northwest England. II. Relative fitness of morphs and population size. Phil. Trans. Royal Soc. Lond. B. 281: 517 542.
  • 6
    Brakefield, P.M. 1987. Industrial melanism – do we have the answers? TREE 2: 117 122.
  • 7
    Brakefield, P.M. 1990. A decline of melanism in the peppered moth Biston betularia in the Netherlands. Biol. J. Linn. Soc. 39: 327 334.
  • 8
    Brunton, C.F.A. & Majerus, M.E.N. 1995. Ultraviolet colours in butterflies: intra- or inter-specific communication? Proc. Royal Soc. Lond. B. 260: 199 204.
  • 9
    Brunton, C.F.A., Russell, P.J.C., Majerus, M.E.N. 1996. Variation in ultraviolet wing patterns of Brimstone butterflies (Gonepteryx: Pieridae) from Madeira and the Canary Islands . Entomologist 115: 30 39.
  • 10
    Burkhardt, D. & Maier, E. 1989. The spectral sensitivity of a passerine bird is highest in the UV. Naturwissenschaften 76: 82 83.
  • 11
    Chen, D., Collins, J.S., Goldsmith, T.H. 1984. The UV receptor of bird retinas. Science 225: 337 339.
  • 12
    Clarke, C.A., Mani, G.S., Wynne, G. 1985. Evolution in reverse: clean air and the peppered moth. Biol. J. Linn. Soc. 26: 189 199.
  • 13
    Cook, L.M., Rigby, K.D., Seaward, M.R.D. 1990. Melanic moths and changes in epiphytic vegetation in north-west England and north Wales. Biol. J. Linn. Soc. 39: 343 354.
  • 14
    Grant, B., Owen, D.F., Clarke, C.A. 1995. Decline of melanic moths. Nature 373: 565565.
  • 15
    Grant, B.S., Owen, D.F., Clarke, C.A. 1996. Parallel rise and fall of melanic peppered moths in America and Britain. J. Hered. 87: 351 357.
  • 16
    Howlett, R.J. & Majerus, M.E.N. 1987. The understanding of industrial melanism in the peppered moth (Biston betularia) (Lepidoptera: Geometridae) . Biol. J. Linn. Soc. 30: 31 44.
  • 17
    Kettlewell, H.B.D. 1955. Selection experiments on industrial melanism in the Lepidoptera. Heredity 9: 323 342.
  • 18
    Kettlewell, H.B.D. 1956. Further selection experiments on industrial melanism in the Lepidoptera. Heredity 10: 287 301.
  • 19
    Kettlewell, H.B.D. 1958. The importance of the micro-environment to evolutionary trends in the Lepidoptera. Entomologist 91: 214 224.
  • 20
    Kettlewell, H.B.D. 1973. The Evolution of Melanism. Clarendon Press, Oxford.
  • 21
    Lees, D.R., Creed, E.R., Duckett, J.G. 1973. Atmospheric pollution and industrial melanism. Heredity 30: 227 232.
  • 22
    Liebert, T.G. & Brakefield, P.M. 1987. Behavioural studies on the peppered moth Biston betularia and a discussion of the role of pollution and epiphytes in industrial melanism. Biol. J. Linn. Soc. 31: 129 150.
  • 23
    Majerus, M.E.N. 1989. Melanic polymorphism in the peppered moth, Biston betularia, and other lepidoptera . J. Biol. Edu. 23: 267 284.
  • 24
    Majerus, M.E.N. 1998. Melanism: Evolution in Action. Oxford University Press, Oxford.
  • 25
    Mikkola, K. 1979. Resting site selection of Oliga and Biston moths (Lepidoptera: Noctuidae and Geometridae). Acta Ent. Fenn. 45: 81 87.
  • 26
    Silberglied, R.E. & Taylor, O.R. 1978. Ultra-violet reflection and its behavioural role in the courtship of the sulphur butterflies Colias erytheme and C. philodice. Behav. Ecol. Sociobiol. 3: 203 243.
  • 27
    Steward, R.C. 1977a. Industrial and non-industrial melanism in the peppered moth Biston betularia (L.). Ecol. Ent. 2: 231 243.
  • 28
    Steward, R.C. 1977b. Industrial melanism in the moths Diurnea fagella and Allophyes oxyacanthae (Caradrinidae). J. Zool. Lond. 183: 47 62.
  • 29
    Tutt, J.W. 1896. British Moths. George Routledge.