Journal of Heredity 2005:96(5):522–528 ª The American Genetic Association. 2005. All rights reserved.

doi:10.1093/jhered/esi082 For Permissions, please email: journals.permissions@oupjournals.org.

Advance Access publication June 30, 2005

Melanic Moth Frequencies in Yorkshire,

an Old English Industrial Hot Spot
L. M. COOK, S. L. SUTTON, AND T. J. CRAWFORD
From the Manchester Museum, University of Manchester, Manchester M13 9PL U.K. (Cook); Institute of Tropical
Biology and Conservation, University Malaysia Sabah, Sabah, Malaysia (Sutton); Department of Biology, University of
York, York U.K. (Crawford).

Address correspondence to L. M. Cook at the address above, or e-mail: lcook@manchester.ac.uk.

Abstract
A survey has been carried out in Leeds, England, in the west Yorkshire industrial heartland, and in neighboring York,
surrounded by agriculture, of melanic frequency in the moth species Biston betularia, Odontoptera bidentata, and Apamea crenata.
All show a decline in melanics in the postindustrial environment, the first over almost the full range from nearly 100% to
less that 10%, the others to smaller extents. Changes in several species over as great a magnitude and as wide an area must
result from selection. The results are compared with others along a transect through northern England. The onset of
response is progressively later from west to east. The rate of decline is lower at the extremes of the transect to west and east
than it is in the center. We still do not have a clear picture of the causes of the changes. One major factor is likely to be
selective predation, which is shown to be critically dependent on predation rate. As a consequence, differences in settling
behavior between the species could account for different responses even if the species are attacked by the same predators.

It is well known that melanic forms in numerous moth
species increased in frequency in parts of Britain following
industrialization in the 18th and 19th centuries (Kettlewell
1965; Kettlewell 1973; Majerus 1998). Northern England,
with its intensive coal-fired manufacturing industry, was
a center both of environmental change and of the earliest
records of response by moth populations (Cook 2003;
Kettlewell 1973; Lees 1981). Blackening of trees, buildings,
and vegetation was extreme, and the atmosphere was heavily
polluted with a variety of toxic gases. The response of moth
populations in west Yorkshire was noteworthy enough for
special comment when the British Association for the
Advancement of Science met in York in 1906 (Porritt 1907).
The earliest indication of an effect was the appearance of
extreme black forms in the peppered moth Biston betularia (L.).
They attracted attention during the 1870s and had become
the prevalent form by the start of the 20th century. In
another species, the scalloped hazel Odontoptera bidentata
(Clerck), melanics began to be seen in the 1890s and within
a decade had become very common. Porritt lists 30 species in
which such distinct black forms were regularly obtained. Of
these, seven had been recorded before industrialization,
whereas others were novel. He added another 21 species in
which dark individuals occurred so frequently as to suggest
they were part of the same phenomenon, among them the
clouded bordered brindle, known then as Xylophasia rurea and
now as Apamea crenata (Hufnagel).
From the middle of the 20th century, there has been
a general environmental improvement and a corresponding
reduction in melanic frequencies (Clarke et al. 1985, 1994;
Cook 2003). Similar changes have been seen in the United
States (Grant and Wiseman 2002). West Yorkshire, with
Leeds and it sister city, Bradford, at its center, was one of the
major British industrial regions and one of the last to
experience a decline in morph frequencies (Cook et al. 2002).
York is situated in an extensive rural region 40 km to the
northeast. Comparatively little information is available from
Yorkshire, compared with industrial Lancashire and rural
north Wales, which lie to the west separated from Yorkshire
by the Pennine chain of mountains. To enlarge the area
examined a study was set up 37 years ago by S. L. Sutton in
Leeds to monitor the change in frequencies in the best
known example, B. betularia, and for comparison, O. bidentata
and A. crenata. The first two species are members of the
subfamily Ennomiinae of the Geometridae. A. crenata
belongs to the subfamily Amphipyrinae of the Noctuidae.
All have annual nonoverlapping generations and fly from
early May to June (O. bidentata) or May to July for the other
two species.
A set of results for the same species were collected by
T. J. Crawford from 1990 to 2004 near York. The new data
extend records eastward, so that we now have a transect over
200 km in extent passing through a full range of available
habitats and climate types in north Wales and northern

522

Figure 1. Sketch map of northern England and Wales showing the approximate locations of the centers mentioned in the text.
C: Caldy, Wirral peninsula, Li: Liverpool, M: Manchester, Le: Leeds, Y: York. The 100 km squares of the National Grid are shown.
England. The main locations referred to are shown in Figure 1.
The efforts of recorders at the beginning of the 20th century
were of immense importance in bringing the phenomenon of
industrial melanism to the attention of the scientific
community. The records were nevertheless often fragmen-
tary and anecdotal. We hope to ensure that more detailed
material is available for analysis from the end of the period of
high melanic frequency.
Materials and Methods
The Leeds survey was carried out from 1967 to 2003 at sites
10 km NE of the city center in an area of suburban building
and farm land. For the first 3 years the site was at Scholes
(National Grid Reference 4377 4366) and subsequently 4 km
distant at Bond Ing meadow, Shadwell (GR 4344 4394),
a mature garden and pasture with extensive planting of trees
and hedges. Sampling was by mercury vapor light trap and
took place throughout the flying season where possible, but
sometimes for shorter periods. This method of trapping
collects almost entirely males in the species concerned, but
the variation is the same in the two sexes. The York site is at
Haxby (GR 4610 4587), about 5 km north of the city center
on the edge of the built-up area. The same type of light trap
was used, and continuous sampling was carried out during
the relevant part of every year.
B. betularia was scored as the dominant melanic carbonaria
Jordan or the dotted white typical. At Leeds the intermediate
insularia forms have been extremely rare. Only about 10
specimens were seen throughout the sampling period, so this
type was ignored. At York, insularia was more common and
has been recorded (see Cook and Muggleton, 2003, for
a summary of information on the melanic types). O. bidentata
was scored as the dominant melanic nigra Prout or as typical.
Typicals from this region are darker than those from
southern England but always clearly distinguishable from
Cook et al.  Melanic Moths in Yorkshire
nigra. The genetics of melanic mutants in both species was
first established by Bowater (1914). A. crenata was scored as
dark or pale. The two types are very distinct. The pale form is
straw-colored with mahogany brown markings at the edges
of the wings, whereas the dark form has the entire forewing
mahogany-colored except for a paler line round the orbicular
and reniform stigmata. Kettlewell (1973) used the name
alopecurus for this form. The correct name is probably combusta
Howarth, which is used by South (1948), Skinner (1984),
Sutton and Beaumont (1989), and other more recent authors,
whereas alepecurus Esper refers to a darker form with black
costal streaks and edge to the reniform stigma (Bretherton
et al. 1983). The dark insects at the sampling sites all have
the same phenotype. The three species are illustrated by
Kettlewell (1973), Bishop and Cook (1980), and Majerus
(1998). All collecting and identification at Leeds was made by
or under the supervision of S. L. Sutton and at York by
T. J. Crawford.
All analysis is based on comparison of melanic and
nonmelanic forms, without reference to genotype (the
melanic forms in the two geometrids are dominant, and we
have no information on A. crenata). The selective disadvan-
tage v of the melanic form relative to the nonmelanic has
been estimated from the equation L0 : M0(1
v)n ¼ Ln : Mn
where the L and M are the initial frequencies and the final
frequencies after n generations of nonmelanics and melanics.
It follows from this relation that when the logarithms of the
ratios show a linear change with generation the slope
provides an estimate of v. The calculation has been found to
give an adequate degree of accuracy and to be robust under
conditions of high or low frequency (Cook et al. 1999a).
Results
The numbers collected at Leeds in the three species are
shown in Table 1. There was a gap in collecting in 1988–89,
523
Journal of Heredity 2005:96(5)

Table 1. Numbers of moths in three species caught in Leeds Table 2. Numbers of moths in three species caught in York
(melanics are shown in the first column for each species,
nonmelanics in the second) Date B. betularia O. bidentata A. crenata
1990 11 2 6 2 5 — —
Date B. betularia O. bidentata A. crenata
1991 21 1 12 1 4 3 26
1967 47 0 34 10 — — 1992 20 0 7 2 4 3 10
1968 58 0 44 19 — — 1993 16 1 6 3 7 3 11
1969 27 0 32 19 — — 1994 9 0 6 1 6 3 8
1970 75 1 10 20 32 12 1995 6 0 2 4 20 5 12
1971 41 0 10 5 40 6 1996 19 3 15 6 12 2 5
1972 76 0 22 6 26 6 1997 8 2 9 5 15 1 5
1973 40 1 40 20 72 31 1998 7 2 8 3 19 0 6
1974 40 0 24 16 25 10 1999 10 0 17 7 20 3 4
1975 3 0 28 7 33 10 2000 5 3 16 3 11 1 4
1976 19 2 23 21 34 13 2001 7 2 12 4 14 4 8
1977 18 0 12 12 4 2 2002 14 0 30 3 23 2 6
1978 23 2 75 33 26 15 2003 7 1 19 3 11 6 10
1979 43 3 48 35 15 4 2004 2 1 12 2 9 1 3
1980 49 2 64 62 74 37
1981 — — — — — — Note: The columns for B. betularia are carbonaria, insularia, and typical. For the
1982 48 4 53 4 77 33 other two, melanics in first column, nonmelanics in second.
1983 57 4 10 9 97 40
1984 27 1 21 18 69 24
1985 48 5 17 12 56 24
1986 83 3 23 13 94 58 Discussion
1987 12 1 14 13 69 32
1988 — — — — — —
B. betularia
1989 — — — — — — In Figure 2 a curve has been fitted by eye to the Leeds data to
1990 5 2 2 3 51 31 indicate the observed trend in frequency of carbonaria. From
1991 34 16 3 18 75 37
1992 27 9 16 20 96 46
a situation where there were almost 100% melanics in the late
1993 18 11 11 7 19 21 1960s, the frequency has declined to less than 10%. The
1994 7 11 4 2 19 20 territory extending WSW from Leeds across Lancashire and
1995 1 5 3 4 8 13 Cheshire and into north Wales has received considerable
1996 4 1 5 7 3 3 attention in studies of morph frequency (Bishop, 1972;
1997 2 1 0 0 0 0
1998 1 8 1 3 5 2
1999 9 13 10 10 8 7
2000 6 18 11 18 33 19
2001 — — — — — —
2002 — — — — — —
2003 1 15 8 16 41 28

after which sampling was often of limited duration. Captures

are generally lower in later years. This may reflect secular
changes in population densities. In a wide-ranging survey of
over 300 British moth species over the past 35 years, Conrad
et al. (2004) found that more than twice as many species
declined than increased in numbers. There was also regional
variation in the trends, which are probably the result of both
habitat and climate changes. The York samples are given in
Table 2. A. crenata is relatively much rarer at York than at
Leeds; we know of no reason for this difference. The figures Figure 2. Change in frequency of the carbonaria melanic form
for B. betularia 1990–2000 are also given by Cook and Grant of the peppered moth Biston betularia in Leeds and York.
(2000). Vertical lines are standard errors, horizontal lines show where
Except for A. crenata at York, all three species show data have been grouped. The curve labeled Leeds is a selection
a drop in melanic frequency at both places, which is most curve showing the trend in the Leeds data. M and C are similar
marked in B. betularia. Mean frequency estimates are curves fitted for comparison to data from Manchester (Cook
illustrated in Figures 2–4, with their binomial standard et al. 2002) and Caldy, west of Liverpool (Grant et al. 1996).
errors. For some years with low numbers data have been Inset: records for York 1990–2000 are superimposed on the
combined; the horizontal bars indicate the dates involved. Leeds curve.

524

Figure 3. Change in frequency of the nigra melanic form of
the scalloped hazel moth O. bidentata in Leeds and York. Data
are means of pairs of years, indicated by horizontal lines.
Vertical lines are standard errors.
Bishop et al. 1978; Clarke and Sheppard 1966; Cook 2003).
There are also temporal series of records for Manchester and
Caldy. Manchester is separated from Leeds by the Pennines
but is within the region that had over 95% carbonaria during
the 1950–70 period (Cook et al. 1999b). Caldy is on the
Wirral peninsula west of Liverpool (Clarke et al. 1994; Grant
et al. 1996). In 1959 it had 93% carbonaria, but the location is
just to east of the cline in north Wales, which saw the
frequency drop to 5% over about 25 km. It is the most
complete data set, being based on a series of large samples
collected annually until 2002. Manchester is about 65 km
from Leeds, and Caldy about 130 km. The data for both sites
are plotted together for comparison in Cook (2003).
Curves M and C in Figure 2 are lines similar to that for
Leeds, fitted to the data for Manchester and Caldy,
respectively. It can be seen that as one proceeds west the
initial frequency becomes lower, the decline commences
earlier and is less steep. At Leeds the drop to 90% carbonaria
occurred nearly 20 years after that at Caldy. It reached 50%
9 years later than at Caldy and 6 years after Manchester. The
data for York are shown inserted on Figure 2, using the same
grid of frequency and dates and with the Leeds curve
superimposed as a comparative guide. The commencement
of the decline is as delayed at York as at Leeds. Figures from
the two places for the early 1990s map onto each other.
Thereafter the drop has been slower at York, and the
frequency of carbonaria is probably still appreciably higher
than at Leeds. As noted long ago by Kettlewell (1965, 1973),
the effects of industrialization on melanic frequency appear
to be displaced to the northeast.
The changes observed result from all the processes
operating on the populations, namely selection, migration
from populations with different frequencies, mutation, and
random drift. Changes of as great a magnitude over as wide
an area as observed must involve selection, and over the
middle part of the frequency range the contribution of the
Cook et al.  Melanic Moths in Yorkshire
Figure 4. Change in frequency of the dark form of the
clouded-bordered brindle moth A. crenata in Leeds. Vertical
lines are standard errors, horizontal line shows where data have
been grouped.
other processes is likely to be negligible in comparison. Over
the period 1980–2003 the disadvantage of the melanic
morph compared with typical (estimated from the slope of
log morph ratio on year for the period when the slope was
linear) was 18.9 6 2.6% for York, 27.9 6 2.1% for Leeds,
29.2 6 3.5% for Manchester, and 22.3 6 0.8% for Caldy.
Selection was most intense where initial frequency was
higher (for the comparison of Leeds with Caldy the differ-
ence is significant, p , .05).
When initial frequencies are very high, however, the
balance of the different forces changes, and makes
estimation difficult. If carbonaria gene frequency in Leeds
was truly 100% before 1970, then no change would have
been possible without introduction of typicals by mutation
or migration of immigrants from regions of lower frequency.
Because typical is recessive, these processes would have
introduced genes in heterozygotes that were not subject to
selection, and the response to selection would necessarily be
very slow. It is likely that the response observed was in some
part due to immigration. Population density is probably
lower in industrial than in rural areas (Cook 2003), so that to
the west of the Pennines, net migration is likely to be
eastward, bringing with it the typicals characteristic of north
Wales. We do not know whether there are areas of lower
frequency farther east than York from which immigration
may take place. For two points nearer the east coast
Beaumont (2002) notes that at Spurn (; GR 5400 4100)
there was recently a rapid change from the majority being
melanic to the majority being typical, while at Hutton Rudby
(GR 4507 5506) there has been a steady decrease in melanics
from about 70% in 1990 to about 40% in 2000. Selection
probably also changes with time. The data for Caldy cannot
be fitted by a constant selection curve (Grant et al. 1996),
selection apparently being low at the start, greater during the
main period of change, and probably finally falling off. Such
variation in selection may well occur at the other sites.
525
Journal of Heredity 2005:96(5)

O. bidentata numbers of A. crenata collected in York are small. There is no

detectable change over the 14 years of recording. The mean
This species is similar in size to B. betularia, although with
frequency of melanic is 23.9%, much lower than in Leeds or
differently shaped wings, and flies at roughly the same time
Manchester and comparable with rural sites in other parts of
of year, when it will encounter similar predators. Patterns of
Britain.
morph frequency distribution and results from mark-release-
recapture experiments suggest that it is much less mobile
than B. betularia (Bishop et al. 1978; Bishop and Cook 1980). Causes of Change
The melanic form nigra is absent from the south of England,
Following the advent of effective clean air legislation and
but high frequencies have been recorded in the industrial
monitoring in the late 1950s, the old industrial environment
north. Variation in nigra frequency is more closely associated
has been cleaned or demolished and rebuilt. The amount of
with urbanization than is carbonaria in B. betularia, frequencies
vegetation has greatly increased compared with the early 20th
rising in major centers and falling between them (Bishop et al.
century. Atmospheric pollution has declined dramatically.
1978). In the 1970s the frequency of nigra was over 70% in
Data for Bradford show that by 1971 the concentration of
central Manchester, falling to 20% in suburbs a few km to the
sulfur dioxide was half that in 1962 and that it had halved
south. In Liverpool, however, it did not rise above 50% in
again by 1980. The 1962 concentration of smoke was halved
conditions superficially very like those of urban Manchester,
by 1966 and halved again by 1973. The data presented here
and there was an undulating rise and fall in frequency as one
show that three species of moths have all responded to
moved eastward between the two centers. Sample sizes are
changing ecological conditions with a fall in frequency of
relatively low, and to show the patterns more clearly, means
melanic forms. In the case of B. betularia in Leeds, the change
for pairs of years are illustrated in Figure 3 (calculations are
is parallel with but more extreme than other declines
based on individual years). In Leeds the frequency of nigra
observed in locations to the west. In the other two species
may have been initially even higher than in Manchester at
the decline is less marked but nevertheless appreciable.
about 75%, although there is no indication that it ever rose to
Together they demonstrate the power of selection brought
the level of carbonaria in B. betularia. Since then, there has been
about by a changing environment. Majerus (1998) has argued
a steady but shallow decline to 30–40%. We have no
strongly that the explanation for industrial melanism in
explanation for the unusually low frequencies in 1970 and
B. betularia, and probably generally in moths with melanic
1991. In York, frequencies are much lower but also appear to
forms, can be found in selective predation by birds. There
have declined. The apparent selection against nigra is 3.8 6
has been considerable discussion of whether the experiments
1.1% per year at Leeds, whether or not the low figures are
on selective predation carried out to date show its nature and
excluded (p , .01 in either case). At York the estimate is
strength (Grant and Howlett 1988; Howlett and Majerus
3.7 6 2.4, which is not significant. Very similar changes have
1987; Mikkola 1979). Whether or not the experiments
been observed in the Manchester area (Cook et al. 2004).
actually demonstrate that predation is sufficient to account
Four km south of central Manchester the frequency has
for the observed patterns, the difference in response between
declined from 69% in the 1970s to 51% now, with selection
different species may indicate that additional forces operate
against nigra of 3.5 6 0.5%. Two more westerly locations
as well. Industrial melanism is also seen in two-spot ladybirds
that scored 58% in the 1970s now have 39%. Because the
(coccinellid beetles) that are distasteful to many predators
species moves less than B. betularia immigration will corre-
(Benham et al. 1974; Creed 1971; Majerus 1998). The situa-
spondingly lave a lesser effect on morph frequency.
tion in A. crenata, and in other species such as Apocheima
pilosaria (Cook et al. 2002; Lees 1971, 1981) that are poly-
morphic in rural areas, raises the question whether equilibria
A. crenata
are sometimes the result of selective forces independent of
The clouded-bordered brindle is polymorphic for the dark industrial conditions.
and pale forms through most of Britain and Europe. The One point to be made with respect to selective predation,
dark form is not restricted to industrial regions, although it however, is that the three species discussed here have
has been at higher frequencies there. Kettlewell (1973) gave different daytime resting places that probably make them
80–93% for Bradford, compared with 28% in Hampshire, visible to potential predators to different extents. B. betularia
60% in other parts of southern England and 41–50% in rests exposed on surfaces. It may be found on tree trunks,
northern Scotland. On a smaller scale, Bishop at al. (1976) but observations have shown that a preferred location is on
recorded over 92% for 13 sites near the center of Manchester narrow branches in the upper parts of trees (Howlett and
and found that the frequency fell steadily to 60% over Majerus 1987; Liebert and Brakefield 1987; Mikkola 1979).
a 30-km transect into farm land to the south. The present Where trees were not available and disturbing lights were
records for Leeds (Figure 4) show that the correspondence present, as would have been the case in industrial cities in the
with changing conditions also occurs in time; the frequency past, it would have been likely to have rested on walls.
of combusta has fallen from about 75% in the 1970s to below O. bidentata sometimes settles on surfaces but may also crawl
50% now. Selection against the dark form is 3.6 6 0.7% into cracks or under leaves where it is less exposed.
(p , .01). In both starting frequency and slope the change In experiments by Bishop et al. (1975) B. betularia and
therefore closely follows that of nigra in O. bidentata. The O. bidentata were allowed to emerge from pupae into

526

enclosures with both exposed surfaces and features that
allowed the moths to hide. There was a very strong tendency
for O. bidentata to find covered or protected sites whereas
B. betularia remained exposed (v2 ¼123.7 and 285.7, d.f. ¼ 1,
respectively, in two trials). Like many other noctuids,
A. crenata spends the day near the ground in long grass or
herbage (Bretherton et al. 1983). Apart from differences in
appearance that will make them differently visible, these
species are likely to experience different levels of predation
even within the same location. It is therefore interesting to
consider the possible effect of intensity of predation, as
distinct from predator discrimination.
Consequences of Selective Predation
Suppose there are N individuals in a predation experiment or
natural predated population, of which L are typical and M are
melanic (L þ M ¼ 1). In the absence of selective removal
a fraction I is eaten (0 , I , 1). Predators detect the two
forms differently. Suppose that for every typical detected 1
a
melanics are detected. Choice by predators is exerted
through prey individuals eaten, while the effect on the prey
population is measured on those left. This can be expressed
as a coefficient v, such that
L : ð1
vÞM ¼ Lð1
I Þ : M ½1
I ð1
aÞ:
Consequently, the fitness (1
v) of melanics compared to
typicals as a result of selective predation is
1
v ¼ ½1
I ð1
aÞ=ð1
I Þ
and
v ¼
aI =ð1
I Þ:
It is evident from these expressions that dv/dM ¼ 0,
dv/da ¼
I/(1
I ) and dv/dI ¼
a/(1
I )2. The
expected estimate of v is not influenced by differences in
initial frequency between different experiments or locations,
but is highly dependent on the predation rate experienced.
High predation magnifies the selection resulting from a given
difference in detectability, while reduction in predation
decreases its effect. Only if I ¼ 1/2 does v ¼
a.
The maximum likelihood variance of 1
v is
2 R Soc B, 281:489–542.
V ¼ ð1
vÞð1
MvÞ =fLMN ½1
I ð1
M aÞg:
The denominator of this expression shows that the variance
tends to infinity as M tends to zero or 1. There will be low
accuracy when there are high or low melanic frequencies,
compensated for if the population size N is large. The
variance also tends to infinity as
pffiI increases. However, until
I gets close to 1, the deviate v/ V also increases, so that as
long as predation is not heavy enough to endanger the
population or to modify predator behavior, the effectiveness
of selection will increase with fraction taken. There may also
be interactions between these variables and predator
response, for example a might be a function of I, but we
have no direct evidence on predator reaction.
If selective predation is the main cause of the patterns
seen, then it operates under quite strong constraints.
Effective population size must be large to reduce drift,
Cook et al.  Melanic Moths in Yorkshire
especially when there are high or low frequencies. Predation
rate must be substantial to ensure that predator choice is
translated into change in the prey population, but this will
put the continued survival of the population at risk.
Predation rate in the wild is very difficult to measure now,
and it is impossible to know what it was under the conditions
that brought about industrial melanic patterns; it may have
been higher in industrial regions than in rural ones because
fewer inconspicuous resting sites were available. Different
exposure to predation and different average densities may
generate widely different results in species subject to the
same predators. It is therefore to be expected that response
will differ even if selective predation is the common factor
involved. New experimental information would help us
understand the interactions, but practical problems of
translating results into reliable evidence of causation remain.
Acknowledgments
We thank Pam, Norman, and David Taylor, Dan Houldsworth, and Sam
Rose for help with collecting in Leeds and John Muggleton for comments on
the draft. Information on atmospheric pollution in Bradford is from
www.bradford.gov.uk.
References
Beaumont HE, 2002. Butterflies and moths of Yorkshire: a millennium
review. Weymouth: Yorkshire Naturalists Union.
Benham BR, Lonsdale D, and Muggleton J, 1974. Is polymorphism in the
two-spot ladybird an example of non-industrial melanism? Nature 249:
179–180.
Bishop JA, 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.
Bishop JA and Cook LM, 1980. Industrial melanism and the urban
environment. Adv Ecol Research 11:373–404.
Bishop JA, Cook LM, and Muggleton J, 1976. Variation in some
moths from the industrial north-west of England. Zool J Linn Soc
58:273–296.
Bishop JA, Cook LM, and Muggleton J, 1978. The response of two species
of moths to industrialization in north-west England. I. Polymorphism for
melanism. II. Relative fitness of morphs and population size. Philos Trans
Bishop JA, Cook LM, Muggleton J, and Seaward MRD, 1975. Moths,
lichens and air pollution along a transect from Manchester to north Wales.
J Appl Ecol 12:83–98.
Bowater W, 1914. Heredity of melanism in Lepidoptera. J. Genet 3:
299–314.
Bretherton RF, Goater B, and Lorimer RI, 1983. Noctuidae (Part II) and
Agaristidae. In: The moths and butterflies of Great Britain and Ireland,
vol. 10 (Heath J and Emmet AM, eds). Colchester: Harley Books; 189–190.
Clarke CA and Sheppard PM, 1966. A local survey of the distribution of the
industrial melanic forms in the moth Biston betularia and estimates of the
selective values of these in an industrial environment. Proc R Soc Lond B
165:424–439.
Clarke CA, Mani GS, and Wynne G, 1985. Evolution in reverse: clean air
and the peppered moth. Biol J Linn Soc 26:189–199.
Clarke CA, Grant B, Clarke FMM, and Asami T, 1994. A long term
assessment of Biston betularia (L.) in one UK locality (Caldy Common near
527
Journal of Heredity 2005:96(5)
West Kirby, Wirral), 1959–1993, and glimpses elsewhere. Linnean 10:
18–26 (addendum 12:40–41).
Conrad KF, Woiwod IP, Parsons M, Fox R, and Martin S, 2004. Long-term
population trends in widespread British moths. J Insect Conservation
8:119–136.
Cook LM, 2003. The rise and fall of the carbonaria form of the peppered
moth. Quart Rev Biol 78:399–417.
Cook LM and Grant BS, 2000. Frequency of insularia during the decline in
melanics in the peppered moth Biston betularia in Britain. Heredity 85:
580–585.
Cook LM and Muggleton J, 2003. The peppered moth, Biston betularia
(Linnaeus, 1758)(Lepidoptera:Geometridae): a matter of names. Ent
Gazette 54:211–221.
Cook LM, Cowie RH, and Jones JS, 1999a. Change in morph frequency in
the snail Cepaea nemoralis on the Marlborough Downs. Heredity 82:336–342.
Cook LM, Dennis RLH, and Mani GS, 1999b. Melanic morph frequency in
the peppered moth in the Manchester area. Proc R Soc Lond B 266:
343–354.
Cook LM, Dennis RLH, and Dockery M, 2004. Fitness of insularia
morphs of the peppered moth Biston betularia. Biol J Linn Soc 82:359–366.
Cook LM, Riley AM, and Woiwod IP, 2002. Melanic frequencies in
three species of moths in post industrial Britain. Biol J Linn Soc 75:
475–482.
Creed ER, 1971. Melanism in the two-spot ladybird, Adalia bipunctata, in
Great Britain. In: Ecological genetics and evolution (Creed ER, ed).
Oxford: Blackwell; 134–151.
Grant B and Howlett RJ, 1988. Background selection by the peppered
moth (Biston betularia Linn.): individual differences. Biol J Linn Soc 33:
217–232.
Grant BS and Wiseman LL, 2002. Recent history of melanism in American
peppered moths. J Hered 93:86–90.
Grant BS, Owen DF, and Clarke CA, 1996. Parallel rise and fall of melanic
peppered moths in America and Britain. J Hered 87:351–357.
528
Howlett RJ and Majerus MEN, 1987. The understanding of industrial
melanism in the peppered moth (Biston betularia)(Lepidoptera: Geo-
metridae). Biol J Linn Soc 30:31–44.
Kettlewell HBD, 1965. A 12-year survey of the frequencies of Biston betularia L.
and its melanic forms in Great Britain. Ent Record 77:195–218.
Kettlewell B, 1973. The evolution of melanism. Oxford: Clarendon Press;
1–423.
Lees DR, 1971. The distribution of melanism in the pale brindled beauty
moth, Phigalia pedaria, in Great Britain. In: Ecological genetics and evolution
(Creed ER, ed). Oxford: Blackwell; 152–174.
Lees DR, 1981. Industrial melanism: genetic adaptation of animals to air
pollution. In: Genetic consequences of man made change (Bishop JA and
Cook LM, eds). London: Academic Press; 129–176.
Liebert TG and Brakefield PM, 1987. Behavioral studies on the peppered
moth Biston betularia and a discussion of the role of pollution and lichens in
industrial melanism. Biol J Linn Soc 31:29–150.
Majerus MEN, 1998. Melanism: evolution in action. Oxford: Oxford
University Press; 1–338.
Mikkola K, 1979. Resting site selection by Oligia and Biston moths
(Lepidoptera: Noctuidae and Geometridae). Acta Entom Fennici 45:81–87.
Porritt GT, 1907. Melanism in Yorkshire Lepidoptera. Rep Brit Ass Adv Sci
316–325.
Skinner B, 1984. Color identification guide to moths of the British Isles.
Harmondsworth: Viking; 1–267.
South R, 1948. The moths of the British Isles. Series II. London: Warne;
1–399.
Sutton SL and Beaumont HE, 1989. Butterflies and moths of Yorkshire:
distribution and conservation. Doncaster: Yorkshire Naturalists Union;
1–367.
Received November 17, 2004
Accepted April 6, 2005
Corresponding Editor: Stephen O’Brien