Zoological Journal of the Linnean Society. 58: 273.296 . With 1 plate and 4 figures
June 1976
Variation in some moths from the industrial
north-west of England
J . A . BISHOP
Department o f Genetics. University of Liverpool. Liverpool
AND
L . M. COOK AND J . MUGGLETON
Department of Zoology. University o f Manchester. Manchester
Accepted f o r publication August 1975
A survey of five species of moth each showing different degrees of melanism was made in
Greater Manchester and compared with samples from adjacent rural areas . The genetics of the
various systems is discussed .
CONTENTS
Introduction
. . . . . .
Materials and methods
. . .
Results
. . . . . . .
Phigalia pilosaria
. . .
Apamea monoglypha
.
Genetics
. . .
Phenotypic variation
The 1972-74 survey
Discussion
. .
Apameacrenata
. . .
The 1972-74 survey
Discussion
. .
Orthosia incerta
. . .
Discussion
. .
Orthosiagothica
. . .
The present survey
Genetics
. . .
Discussion
. .
Conclusion
. . . . . .
Summary
. . . . . . .
Acknowledgements
. . . .
References
. . . . . .
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J . A. BISHOP, L. M. COOK AND J. MUGGLETON
INTRODUCTION
The striking polymorphism of industrial melanism in the Peppered Moth
Biston betularia (L.) and its relationship to the visible effects of air pollution is
widely recognized as a testimony to the efficacy of natural selection
(Kettlewell, 1955, 1956, 1958). The frequency of melanic morphs of this
species in its populations throughout Britain has been represented in a map, the
latest version of which appears on p.7 3 of Sheppard (1975). This clearly shows
that the carbonarfu morph is most common in industrial regions and in areas to
the east of them.
The large-scale approach to the geographical distributions of the melanic
forms of B. betuluria provided a challenge to students of evolution that was
taken up by Clarke & Sheppard (1963, 1966). These workers initiated a
localized study in Merseyside and adjacent areas of North Wales. Concentration
on a particular area meant that the ecological parameters associated with
selection and polymorphism could be studied in closely related populations
with different morph frequencies. Subsequent ecological studies by Bishop
(1972), Bishop & Cook (1975), Bishop, Cook, Muggleton & Seaward (1975)
and Lees & Creed (1975) have extended our understanding of the nature and
interaction of the forces of natural selection and migration. As well as
confirming that differential predation of morphs by birds is a most important
selective agent, such studies also indicate that other selective pressures, as yet
poorly understood, are active.
In this paper we examine the distribution of the frequency of melanic forms
within a relatively local area in several species which are ecologically and
taxonomically distinct from Biston betuluria, and are liable to respond in
different ways to selection imposed by a polluted environment. Most samples
were taken within the boundaries of Greater Manchester and Merseyside;
counties which include much of the industrial area of north-west England.
They contain a high proportion of species exhibiting melanism, and animals in
them are distinctly darker in general appearance than those from rural areas in
the south of the country. This difference arises from several types of response
to the industrial environment. In the Manchester and Liverpool region samples
of some species, which in rural areas are pale, consist almost entirely of dark
individuals, while others, which have not shown the melanic adaptation, are
absent from the cities. For example, the Marbled Minor and its sibling species
(Oligiu strigilis (Clerk) and 0. lutrunculu (Schiffermuller)) and the Rosy Minor
(Mesoligia literosu (Haworth)) are widespread and almost always melanic, while
the Middle Barred Minor (0.fusciunculu (Haworth)) is pale brown and occurs
only in the rural outskirts (compare Mikkola, 1975). In some other urban
species there is a persistent low level of melanic polymorphism (e.g. in the
Miller, Aputele leporinu L.), while a few other species succeed in flourishing but
do not show any darkening. In Manchester this is true of the Ingrailed Clay,
Diursiu rnendicu Fab., although it is known to possess dark forms elsewhere.
Some other examples of different kinds of response to the polluted
environment are mentioned by Askew, Cook & Bishop (1971). The available
evidence on the incidence of melanism in British moths has been exhaustively
reviewed by Kettlewell (1973). Comparatively few species have been examined
in any detail, however. Over the last five years we have surveyed the
VARIATION IN INDUSTRIAL MOTHS
275
distribution of Biston betularia (L.) and Gonodontis biden tata (Clerck), the
two species which show the most striking association of melanic polymorphism
with industrialization (Bishop & Cook, 1975; Bishop, Cook & Muggleton, in
prep.). At the same time we have collected data on five other species which
exhibit melanism or related variability and are sufficiently common in the area
for series of samples to be taken. The results are presented here. Although they
are incomplete, we think that they provide a useful comparison with the more
detailed surveys, and illustrate some of the varied responses of lepidoptera to
the industrial urban environment. The species described are the Pale Brindled
Beauty Phigalia pilosaria (= pedaria) Fab.; the Dark Arches, Apamea monoglypha (Hufnagel); the Clouded Bordered Brindle, Apamea crenata (Hufnagel);
the Clouded Drab, Orthosia incerta (Hufnagel); and the Hebrew Character,
Orthosia gothica (L.).
MATERIALS AND METHODS
The moths were collected between 1972 and 1975. Most samples were
obtained using mercury-vapour light traps, but the P. pilosaria and some
0.gothica were taken in assembly traps containing pheromone-producing
females. The samples from assembling traps consist entirely of males (the
females of P. pilosaria are in any case wingless). Samples from mercury-vapour
traps show considerable differences in sex-ratio between species. In A . monoglypha males are sometimes only a little more common than females while in
0.gothica there is a great preponderence of males in the samples. These
differences reflect differences in behaviour. In no case does the morph
frequency differ significantly between sexes, so that in the ensuing tables
results are given for the totals from each site irrespective of sex. Most of the
sites were sampled on many nights throughout the flying season. The list of
locations is given in Table 1, together with data on atmospheric pollution for
some of the sites. Figure 1 is a map of the sampling sites in north-west England.
RESULTS
Phigalia pilosaria
The larvae of Phigalia pilosaria feed on the foliage of several species of tree,
particularly on oak. Adult males fly on mild nights between late December and
early April; females are wingless and consequently move very little. Males are
known to fly at least 500 m, possibly much further (D. R. Lees, pers. comm.).
Lees (1974) has shown that a series of three alleles controls the expression of
the common melanic forms of the species; monacharia (the extreme unpatterned morph) is dominant t o “intermediate” (the patterned melanic) and
the black-and-white mottled typical form is recessive to both. The distribution
of the three phenotypes throughout Britain makes it clear that monacharia and
“intermediate” are industrial melanics. The frequency of these morphs differs
consistently from the comparable carbonaria and insularia melanics of Biston
betularia (Lees, 1971).
The results are shown in Table 2. Most of the sites at which P. pilosaria was
collected are near sampling sites for B,betularia lying on a cline running
south-west from Liverpool. All along the cline the “intermediate” and the
I
THW'CH
T 1o
54
c7
%5
I
Figure 1. Map showing positions of sample sites in North-West England and adjacent areas of North Wales. Localities are numbered as in Table 1 . Shaded areas
are urbanised and grid lines are 10 km apart.
8
057
,
VARIATION IN INDUSTRIAL MOTHS
277
100.
carbonaria
901’
0
I1
0
80.
-ala
In
.-c
rnonacharia t intermediate
cartwnaria
t
insularia
B
70.
60
.-C
rnonacharia
0
m
?Loggerheads
#
50
40
0
U
0
al
E
30-
o
/
2010-
Mold
Clegyr
Mow
a&
0
0
O Y
I’O
I
30
2’0
Distance
from
4’0
5b
Knowsley (km)
I
60
I
70
Figure 2. Frequency of the monacharia and “intermediate” melanics of Phigalia pilosaria
compared with t h e frequency of the carbonaria and insularia melanics of Biston betularia along
the cline from Knowsley (Site 58, Fig. I ) to Clegyr Mawr (see Bishop, 1 9 7 2 ) in North Wales.
For localities where there are n o open squares (representing carbonaria + insularia frequency)
there were few o r n o insularia in samples. The steep curve is the computed cline using
coefficients based o n selection experiments with heterozygous advantage of 10% (Bishop,
1972: fig. 9 (a)). The less steep curve is similar bu t assumes a much greater degree of migration
(fig. l l a ) . Data are from Table 2 and from Clarke and Sheppard ( 1 9 6 6 ) , Bishop ( 1 9 7 2 ) and
unpublished.
insularia forms are less common than monacharia and carbonaria respectively.
However, the monacharia form of P.pilosaria is at a consistently lower
frequency than carbonaria in B. betularia (Fig. 2). Like that species, P.pilosaria
rests on exposed surfaces such as tree trunks during the day. I t differs in having
the adult stage much earlier in the season when the trees are bare of leaves and
the summer migrant birds are absent while the birds which are present have a
less diverse range of prey available. For these reasons the selection exerted by
visual predation is likely to be different, although not in easily predictable
ways.
Apainea monoglypha
This species is found throughout the study area and is often attracted in
large numbers to the mercury vapour light traps. The colour of the forewings
ranges from the light mottled brown of the typical to the almost uniform
jet-black of the melanic form aethiops. Between these two extremes there is a
wide and probably continuous variation in colour. There are also some very
dark specimens where a brown, rather than a black, pigment has suffused over
the entire wing area giving it a uniform brown appearance. The hindwings are
considerably lighter in colour and subject to less variation; those of the extreme
melanic forms are lightly suffused with black.
J. A. BISHOP, L. M. COOK AND J. MUGGLETON
278
Table 1. List of sampling sites and grid references. Smoke and SO2 levels are
shown where data is available (Warren Spring Laboratory, 1972)
Site
number
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
Name
Disley
Marple
Higher Poynton
Ashton-under-Lyne
Bollington
Royton
Poynton
Prestbury
Stockport
Bramhall (a)
Bramhall (b)
Bramhall (c)
Bramhall ( d )
Heaton Moor
Chcadle Hulme (a)
Levenshulrne
Cheadle Hulrne (h)
Longsight
Rusholrne
Cheadle (a)
Wilmslow (a)
Withington
Didsbury (a)
Cheadle (b)
Moss Side
Didsbury (b)
Gatley
Didsbury (c)
Didsbury (d)
Wilrnslow (b)
Wilmslow (c)
Chorlton (a)
Chorlton (b)
Wythenshawe
Salford
Prestwich
Jodrell Bank
Sale (a)
Sandbach
Stretford
Radcliffe
Hale
Eccles
Sale (b)
Knutsford (a)
Knutsford (b)
Worsley
Boothstown
Crewe
Darwen
Deansgreen
Risley
Leigh
Hartford
Winwick
Walton Lea
Grid
Reference
3 31965846
947888
942839
945988
930776
34/91 7077
3 31907834
904778
903885
897849
896860
895870
894868
882918
882847
872934
870846
863952
858951
855889
853882
852829
851913
851872
849957
849920
849879
843913
84391 1
84-80828802
821939
821935
821889
34/815021
811046
3 31797706
789908
789629
787943
341780070
331777858
776991
764907
762778
758770
341758008
729012
331700511
34170-193 3 1693855
654927
652991
642725
61 7929
602856
Winter smoke
(pg/m3 )
Winter SO,
(ugh )
153
125
72
198
55
155
85
188
75
126
85
141
249
188
117
122
158
164
160
100
201
74
200
105
100
200
77
167
94
149
95
67
160
134
VARIATION IN INDUSTRIAL MOTHS
279
Table 1-cont.
Site
number
57
58
59
60
61
62
63
64
65
66
67
68
69
70
71
72
73
74
75
76
77
78
79
80
81
82
83
84
Name
Grid
Reference
Winter smoke
(pg/m3 )
Mouldsworth
Knowsley
Mossley Hill
Sunnyside
Poulton Hall
lnce Blundell
Willaston
Burton Wood
Bebington
Neston
Northophall
Alltami
Meols
Caldy
Loggerheads
Mold
Maeshafn
Nan t cl wyd
Tregarth
Macduff, Banffshire
Rowarth, Derbys.
Woodchester Park, Glos.
Alvington, Glos.
Coxtie Green, Essex
Staines, Surrey
Nettlecombe, Somerset
Welcombe Mouth,
Devon
Budleigh Sal terton,
Devon
509710
43-95387871
366883
336816
3413242331322782
315744
31-82301769
274670
267657
234898
225858
216633
2 14649
203610
108521
23160-6838170-64431012892
32/811012
321597002
511553960
511038705
3 1105-3 7-
Winter SO,
(figlm )
22
80
2 1/21 781 2
30106-82-
Table 2. Samples of Phigalia pilosaria from the survey area. Data for five sites
taken from Lees (1971)
~
Ref. no.
Locality
Date
30
39
58
61
62
63
64
Wilmslow
Sandbach
Knowsley
Poulton Hall
Ince Blundell
Willaston
Burton Wood
Burton Wood
Bebington
Northophall
Alltami
Loggerheads
Mold
Maeshafn
Nan tcl wyd
Tregarth
1968-9
1969
1970
1970
1969
1974
1970
1974
1957
1973
1974
1975
1974
1970
1975
1963-6
65
67
68
71
72
73
74
75
~~
monucharia Intcrmcdiatc Typical
3
3
0
0
9
11
2
11
11
6
14
13
7
5
7
0
0
5
8
1
7
2
1
3
30
18
178
34
31
25
26
7
33
7
9
13
2
5
3
7
2
2
2
4
22
1
Total
42 Lees
4 1 Lees
31
25
46 Lees
15
25
30
29 Lees
8
(1971)
(1971)
(1971)
(1971)
10
5
40
20
188
35 Lees (1971)
J. A. BISHOP, L. M. COOK AND J. MUGGLETON
280
Melanic specimens of A . monogfypha were described by Newman (1869). He
wrote that he had specimens from Scotland that were “almost black”, but he
was not certain whether melanism was constant in Scotland nor whether it was
found elsewhere. Some years later Kirby (1903) recorded that there was
considerable variation in the colour of A . monoglypha and that specimens from
Scotland and Ireland were “unusually dark”. Kettlewell (1957) recorded this
species as a non-industrial melanic but recently he has suggested that melanism
in it takes two forms, one of which is ancient and non-industrial in origin while
the other is more recent in appearance and industrial in origin (Kettlewell
1973). In an earlier survey of the frequency of melanism in moths in
Manchester, Askew, Cook & Bishop (1971) found a low incidence of melanism
in A . monogfypha at all the localities they sampled; they did not find any
evidence of a correlation with atmospheric pollution. Kettlewell (197 3) gives
melanic frequencies for 25 localities in Great Britain and generally these show
an increase in melanic frequency with distance north. There are, however,
exceptions to this trend in both Scotland and southern England.
Genetics
The genetics of the melanic form of this species is unknown. In order to
investigate this problem eggs were obtained in 1972 from three wild females
that had been caught in MV light traps. Two of the females were extreme
melanics, the other was a typical. Each laid about 200 eggs and the larvae were
kept in closed plastic boxes and fed on the leaves of the grasses Dactylis
glomerata L. and Poa annua L. Mortality of half-grown larvae was very high
(death probably resulted from infection by an intestinal virus). Only 1 3 larvae
reached full size, pupated and produced adults (Table 3).
Table 3 . Apamea monogfypha. Phenotypes in progeny of all surviving crosses
Progeny
Parent
Melanic
Melanic
Typical
Melanic
Melanic
Typical
d
9
4
-
1
2
8
3
-
d
1
4
2
9
-
1
1
The adults emerged over a long period, making it impossible to obtain any
matings with these specimens. Many of those caught in mercury-vapour light
traps were virgin, and in 1973 a further series of crosses was made using wild
females and wild males. All the resulting larvae died when about half grown,
again probably as a result of viral infection. Some larvae obtained from the eggs
of a wild-mated melanic female from Manchester were reared in an outside
enclosure in Somerset by Mr A. Liebert. Fourteen moths emerged successfully,
consisting of 11 melanics and 3 typicals (Table 3). In each case melanics and
typicals could be separated without difficulty and no intermediates were
found. These results are in keeping with the hypothesis that there is segregation
VARIATION I N INDUSTRIAL MOTHS
281
at a single locus, melanic being dominant to typical. A melanic and the typical
from mating 2 are illustrated in Plate 1.
Phen o typic variation
In wild-caught samples, as distinct from the bred material, there is overlap
between the melanic and the non-melanic classes. Askew et al. (1971) had
comparatively little difficulty in separating the melanic forms from the
remainder. However, from an examination of the larger samples obtained later
it became apparent that separation of the melanic forms was sometimes by no
means easy. Using two methods we attempted to quantify the amount of
melanic pigment in the forewings by measuring the light-reflectance. The first
method used an SEI reflectance photometer (Salford Electrical Industries,
G.E.C., Heywood, Lancashire). This instrument was developed for professional
photographic purposes, and has been used by Creed et al. (Creed, Lees &
Duckett, 1973; Lees, Creed & Duckett, 1973) and by Bishop et al. (1975) for
recording light-reflectance from tree trunks. I t has the advantage that the angle
subtended for measurement is as little as j", so that measurements may be
made from individual spots on the wings. The second method employed an
EEL reflectance photometer which read through a binocular microscope and
recorded light-reflectance from a field with diameter as great as the breadth of
the forewing. This technique has been used by Boardman et al. (1974). The
first method allows variation between parts of the wing to be examined, while
the second measures the general degree of darkness seen by the observer. After
much experimentation both methods were discontinued because of their
sensitivity to the direction and angle of illumination and to the degree of wear
of the wings. We therefore decided that one observer should score all the moths
by reference to a single standard specimen. Although this method is rather
subjective it allows these sources of error to be reduced. The SEI photometer
was used, however, to investigate phenotypic variation within samples. The
readings used were made by Mr A. Wright.
Specimens in a sample of 96 individuals from Walton Lea were scored at
three positions on the left forewing (see Plate 1).If the animal is not a uniform
black the apical area A is usually relatively pale, while the central area B is
usually dark. Pigmentation in area C appears to vary to some extent
independently of the other two. The partial correlation coefficients for the
three possible pairs are
r.4B.c = 0.479,
rAC.B = 0.47 3 ,
rBC.4 = 0.236.
The correlation between B and C when the effect of A is removed is distinctly
lower than the correlations of the other two pairs. Individuals therefore vary in
pattern as well as in overall darkness. In order to represent the general degree of
darkness the two most highly correlated variables A and B were scored on
several samples, and the first principal components for each point in the
correlated distribution were calculated measured from the overall mean. These
values provide an arbitrary score of darkness based on two records for each
wing. Frequency histograms are given for three samples, from Walton Lea,
Jodrell Bank and Winwick, to show the degree of variation (Fig. 3). The
J. A. BISHOP, L. M. COOK AND J. MUGGLETON
282
12
10.
'
WALTON LEA
%I+. Sb
8.
6.
4.
nil
1.
n
10
'
1ODRELL
8.
BANK
,/I*37
6.
4.
WINWICK
12 '
I,,.
55
10.
8.
6.
4.
n
1.
1
Dark
Reflectance
Score
Pole
Figure 3. Apamea monoglypha. Frequency histograms showing variation in darkness in three
samples. The score is obtained from measurement of light reflectance at positions A and B
shown in Plate 1 . See text for details of method.
distributions are clearly bimodal, but there is considerable overlap between the
modes. These results indicate that other genetic or environmental factors
besides the segregating gene identified by breeding, contribute to the
determination of the phenotype.
The I 9 72-74 survey
Between 1972 and 1974 we collected samples of A.monoglypha from MV
light traps at 36 sites in and around Greater Manchester and also obtained
samples from 11 sites in other parts of Great Britain. These were scored by eye
with reference to a standard specimen chosen to represent the pale end of the
melanic range, and specimens are recorded as darker (melanics) or lighter
(non-melanics) than the standard. Where possible we also re-scored the
specimens collected by Askew et al. (1971) from nine sites in the Manchester
area between 1967 and 1969. The results are shown in Tables 4 and 5 .
Re-scoring the earlier samples has given melanic frequencies between 1 3 and
30% for six of the sites sampled by Askew et al. (1971). The new frequencies
compare favourably with the previous ones, which come from samples scored
by eye but without reference to a standard. Frequencies between 8 and 30%
were recorded from the samples collected in 1972-74. The increased range of
melanic frequencies probably reflects the extension of the trapping area over
that used by Askew et al. (1971). At two localities, Hale and Jodrell Bank,
VARIATION IN INDUSTRIAL MOTHS
283
Table 4.Samples of A . monogypha mostly from within a 30 km radius of
the centre of Manchester, 1972-74
Ref. no.
1
2
3
5
6
7
9
10
11
12
13
15
16
17
20
21
22
24
30
32
35
37
40
41
42
43
44
47
48
52
53
55
56
76
50
58
70
66
78
79
80
81
82
83
Locality
Disley
Marple
Higher Poynton
Bollington
Royton
Poynton
Stockport
Bramhall ( a)
Bramhall ( b )
Bramhall (c)
Bramhall (d)
Cheadle Hulme (a)
Levenshul me
Cheadle Hulme ( b )
Cheadle (a)
Wilmslow (a)
Withington
Cheadle ( b )
Wilmslow ( b )
Chorlton (a)
Salford
Jodrell Bank
Stretford
Radcliffe
Hale
Eccles
Sale ( b )
Worsley
Boothstown
Risley
Leigh
Winwick
Walton Lea
Macduff, Banffshire
Darwen, Lancashire
Mossley Hill, Merseyside
Caldy, Wirral
Caldy, Wirral
Neston, Wirral
Woodchester Park, Glos.
Alvington, Glos.
Coxtie Green, Essex
Staines, Surrey
Nettlecombe, Somerset
Welcombe Mouth, Devon
Oxford (Dr D. L. T. Conn)
Melanic
Non-melanic
Total
% melanic
6
28
24
25
106
21
140
399
466
177
238
132
123
36
65
146
20
34
24 1
162
34
58
195
9
29
40
180
144
64
14
47
164
273
151
143
32 3
34
33
33
120
23
171
474
512
203
262
159
142
45
76
169
25
46
272
192
46
82
223
10
38
46
214
167
77
18
61
193
322
171
163
393
14
452
16
63
140
27
24
44
106
53
197
17.7
27.3
24.2
11.7
8.7
18.1
15.8
9 .O
12.8
9.2
17.0
13.4
20.0
14.5
13.6
20.0
26.1
11.4
15.6
26.1
29.3
12.6
10.0
23.7
13.0
15.9
13.8
16.9
22.2
23.0
15.0
15.2
11.7
12.3
17.8
35.7
7.5
12.5
7.9
0.7
0
4.2
0
9
8
14
2
31
75
46
26
24
27
19
9
11
23
5
12
31
30
12
24
28
1
9
6
34
23
13
4
14
29
49
20
20
70
5
34
2
5
1
0
1
0
0
0
2
9
418
14
58
139
27
23
44
106
53
195
0
0
1.0
collections were made during both periods of sampling. At both these sites the
later data show a fall in melanic frequency of 4.6%; this decrease is not,
however, significant.
Discussion
Askew et al. (1971) found a significant difference in melanic frequency
between successive years at one site, and at a number of the localities listed by
J. A. BISHOP, 1. M. COOK AND J . MUGGLETON
284
Table 5 . Samples of A . rnonoglypha collected by Askew et al. (1971)
and re-scored
Ref. n o .
18
25
26
36
37
42
60
Locality
Longsight
Moss Side
Didsbury (b)
Prestwich
Jodrell Bank
Hale
Sunnyside, Merseyside
Melanic
Non-melanic
Total
% melanic
15
3
11
10
49
5
30
54
19
26
60
243
24
126
69
22
37
70
292
29
156
21.7
13.6
29.7
14.3
16.8
17.2
19.2
Kettlewell (1973) there is similar heterogeneity. In the present survey only two
sites, Poynton and Stockport, were sampled in successive years and at neither
was there any evidence of heterogeneity. However in 1972 sampling was carried
out at two sites in Bramhall (12 and 1 3 ) which are only 1 km apart. The traps
were operated for the same period of time and a frequency of 9.2% melanics
(n = 262) was recorded at site 12 and a frequency of 17.0%melanics at site 1 3
(n = 159). A xz test shows that there is significant heterogeneity between these
sites (xz = 5.684, P = < 0.05). The variations in melanic frequency contrast
with the results we have obtained for B. betularia, G. bidentuta and A . crenuta
where the melanic frequency remains stable even when small samples are
considered. The reason is open to speculation but fluctuation from generation
to generation is more likely if the expression of the melanic gene is modified by
environmental factors than if its control is predominantly genetic.
The samples of A . rnonoglypha from the inner Manchester sites show
considerable variation in melanic frequency (x:~= 84.7, P = < 0.001). In
general higher melanic frequencies are found towards the centre of the city,
and there is a decrease in frequency towards the south and west. In the
south-east, however, melanic frequencies remain high. Fifteen of the ManChester sampling sites can be paired with stations where air pollution is
measured (Warren Spring Laboratory, 1972) but a comparison of melanic
frequency and air pollution levels at these sites fails to show any direct
relationship (Table 6).
We did not find any melanics in the samples we obtained from the south and
south-west of England but they were present in samples obtained at sites to the
north outside Manchester. Although the nature of our technique of scoring
makes a direct comparison with the frequencies recorded by Kettlewell (1973)
impossible, our data would seem to confirm Kettlewell’s conclusion about the
status of melanism in this species. The two sets of data show a distribution of
melanism that suggests a relationship with both climatic and industrial factors.
Kettlewell (1973) lists 259 species of British Macrolepidoptera having melanic
forms, and of these about 30 appear to show both geographic (or climatic) and
industrial melanism similar to A . monoglyphu. Melanism in moths inhabiting
high latitudes is not uncommon and was discussed as long ago as 1883
(Walsingham, 1885). I t is possible that at these latitudes melanic morphs have a
physiological advantage which also manifests itself in industrial areas. Outside
the Lepidoptera, the ladybird beetles Adaliu bipunctutu L. may be taken as a
VARIATION IN INDUSTRIAL MOTHS
285
Table 6. Melanic frequencies of A . rnonoglypha and mean winter sulphur
dioxide and smoke concentrations a t fifteen sites in and around
Greater Manchester
Ref. no.
6
20
22
24
25
26
35
36
41
42
47
52
53
55
56
Locality
Royton
Cheadle (a)
Withington
Cheadle ( h )
Moss Side
Didshury (b)
Salford
Prestwich
Radcl i ffe
Hale
Worsley
Risley
Leigh
Winwick
Walton Lea
Correlation coefficient against
% melanic. r =
Winter smoke
(pg/m’ )
Winter SO,
153
55
85
75
126
85
117
122
201
74
100
77
167
95
67
125
155
188
141
249
188
158
164
200
105
200
94
149
160
134
0.04
% melanic
(ah’)
8.7
13.6
26.1
11.4
13.6
29.7
29.3
14.3
23.7
14.7
16.9
23.0
15.0
15.2
11.7
0.21
well documented example of a species which is both a geographic and an
industrial melanic. I t appears that in this species the physiological advantages of
the melanic in areas of low sunshine are reflected in the high frequencies of
melanic morphs found in smoky, as well as cloudy, regions (Benham et al.,
1974; Muggleton et al., 1975).
Apamea crenata
This moth is found throughout the study area from early June until late
July. The larvae, which hatch after 7-9 days feed on the leaves and stems of
grasses, the young larvae feeding within the grass stem. They hibernate when
about half-grown and recommence feeding in the spring, producing adults in
the summer. The larvae are nocturnal feeders and in Manchester they can
frequently be found among the roots of Poa annua L. during the day.
The typical morph of this species is straw coloured with the thorax
mahogany brown and with similarly coloured markings at the edges of the
wings. The dark coloured morph alopecurus is readily distinguishable from the
typical and has the entire forewing mahogany coloured except for a more or
less well-defined pale line around the orbicular and reniform stigmata.
Humphreys and Westwood (1897) described dark varieties of A . crenata
(=rurea) and referred the extreme dark forms t o a distinct species, A .
combusta, although they pointed out that this may be only a variety of A
crenata. The dark morphs were also known t o Newman (1869) who described
them as belonging t o two forms, alopecurus and combusta. Kettlewell (1957)
originally described the form alopecurus as a non-industrial melanic but he now
considers that in many urban areas it is responding to industrial conditions,
286
J. A. BISHOP, L. M. COOK A N D J. MUCGLETON
although in other parts of its range it is an ancient geographic melanic
(Kettlewell 1973). The genetics of these forms is unknown. Askew et al. (1971)
collected samples of A . crenata from nine sites in and around Manchester
between 1966 and 1969 and concluded that the frequency of melanism
declined with the decrease in the amount of air pollution on leaving the urban
areas of Manchester.
The 1 9 72-74 survey
Between 1972 and 1974 we collected samples from mercury-vapour moth
traps at 35 sites in and around Greater Manchester. We also obtained samples
from Nettlecombe in Somerset and Woodchester Park in Gloucestershire. The
samples were scored by eye and no difficulty was experienced in separating the
morphs. The results, together with those from the earlier survey (Askew et al.,
1971) are shown in Table 7.
Discussion
The data we have collected appear to confirm Askew et al.’s conclusion
that in the Manchester area A . crenata is behaving as an industrial melanic. A
high frequency of melanism is maintained throughout the conurbation and
there is no evidence of heterogeneity in the samples from the fourteen
21.7, P > 0.05). In this respect the distribution of
innermost sites (x:,
melanism in this species resembles that of Biston betularia (Bishop & Cook,
1975). There is also a high frequency of melanism at the three sites sampled
between Manchester and Liverpool. The rural area between Manchester and
these three sites yielded only small samples of A . crenata and we were unable
to discover whether the high frequency of melanism is maintained across the
area. The frequency of the melanic falls quite rapidly in the rural areas t o the
south of Manchester (Fig. 4). In spite of this, for the twelve sites where the
frequency of alopecurus can be compared with air pollution data there is no
formal correlation between melanic frequency and either smoke or sulphur
dioxide levels (Table 8).
Kettlewell (1973) stated that A crenata is unusual in that the melanic
polymorphism is present throughout its range. The data he gives for the British
Isles suggests that the melanic frequency does not fall much below 30% even in
rural areas in the south of England.
Orthosia incerta
In Manchester this moth has a long flight period and can be found from early
March until early June. The ova are laid in several batches and the larvae feed at
night on the leaves of a wide range of trees. The larvae pupate in the summer
and the moth remains in the pupal stage throughout the autumn and ensuing
winter, emerging the following year. The life-cycle of this species in the British
Isles has recently been described by Alford (1973).
The coloration of the forewings can be very variable; a number of morphs
are illustrated by South (1961). Two colour classes can be recognized, one
based on a grey pigment and the other on a reddish-brown pigment. Within
these classes the morphs range from uniform grey or reddish-brown to a pale
VARIATION IN INDUSTRIAL MOTHS
287
Table 7. Frequency of the morph alopeczirus in samples of Apamea crenata
~
Ref. no. Locality
1
2
3
4
5
6
7
Disley
Marple
Higher Poynton
Ashton-under-Lyne
Bollington
Royton
Poynton
8
Prestbury
alopecurus
11
7
12
9
31
39
18
22
w
18
1
9
14
16
18
21
22
23
26
27
29
30
31
Stockport
Heaton Moor
Levenshulrne
Longsight
Wilrnslow (a)
Withington
Didsbury (a)
Didsbury (b)
Gately
Didsbury (d)
Wilmslow (b)
Wilrnslow (c)
33
35
36
37
Chorlton (b)
Salford
Prestwich
Jodrell Bank
38
40
41
42
Sale (a)
Stretford
Radcliffe
Hale
43
44
45
46
47
48
49
50
51
52
53
54
55
56
78
Eccles
Sale (b)
Knutsford (a)
Knutsford (b)
Worsley
Boothstown
Crewe
Darwen
Deansgreen
Risley
Leigh
Hartford
Winwick
Walton Lea
Woodchester Park, Glos.
82
Nettlecornbe, Somerset
~~~
Typical
~
Total
15
% alopecurus
Date
73.3
1974
1974
1974
1966-69
1973
1973
1973
1974
4
1
2
1
11
6
3
4
14
10
42
45
85.7
7
37
85.1
8
73.8
86.6
3
2
ig
5
60
72
132
42
39
121
3
18
73
17
6
25
44
19
3
7
9
-
16
5
1
13
1
6
4
3
2
2
23
5
1966-69
1974
22
-
79.1
1972
1973
148
47
40
134
4
24
77
20
8
27
67
89.2
89.0
98.0
97.0
75.0
94.8
85.0
93.0
66.0
1
21
a
ZII
78.6
1
155
82
4
8
1
0
8
3
6
2
1
1
163
85
95.0
97.0
T3
9
21
29
23
8
10
19
2
1
0
5
2
7
1
4
31
24
8
rn
Jz;
16
62
15
58
1
1
48
37
34
47
5
5
26
2
39
17
9
7
3
3
17
11
i6
2i3
w
9
34
43
0
1
0
1
55
39
44
55
7
5
28
2
42
20
7
2
10
8
2
0
2
0
59.1
94.0
96.0
80.5
93.7
94.0
87.3
95.0
77.0
85.5
93.0
93.0
85.0
36.3
20.9
1972
1972
1966-69
1974
1973
1973
1966-69
1966-69
1972
1966-69
1972
1973
1974
1972
1966-69
1966-69
1972
1973
1972
1972
1974
1966-69
1972
1972
1972
1972
1974
1973
1972
1973
1973
1973
1972
1972
1974
1972
1972
1971
1974
1972
J. A. BISHOP, L. M. COOK AND J. MUGGLETON
288
'I'able 8. Frequencies of the morph alopecurus of A . crenata and mean winter
sulphur dioxide and smoke concentrations at 12 sites in and around
Greater Manchester
Ref. no.
Locality
Smoke pg/m3
Royton
Heaton Moor
Withington
Didsbury ( b )
Salford
Prestwich
Sale (a)
Hale
Worsley
Leigh
Winwick
Walton Lea
6
14
22
26
35
36
38
42
47
53
55
56
Correlation coefficient against
% alopecurus, r =
P=
<0.1
SO, pglm'
153
72
85
85
117
122
160
74
100
167
95
67
125
198
188
188
158
164
100
105
200
149
160
134
0.52
>0.05
0.19
0.1
% alopecurus
86.6
89.0
75.0
85.0
95.0
97.0
94.0
84.0
87.3
93.0
93.0
85.0
cream colour with grey or reddish-brown mottling. The abdomen and thorax
take the basic colour of the forewing. The genetic control of this polymorphism is not known.
Between 1967 and 1974 we collected samples from mercury-vapour traps at
27 sites in the study area and from four sites elsewhere. These have been scored
for the frequency of the grey and red morphs, and for the frequency of
mottled as against uniformly coloured forewings. In the former case the colour
of the thorax was used for scoring. The results are given in Table 9.
4
Crewe A
C l o d c e l l Bank
I
2
i
6
8
f0
Distance from
11
(4
Ib I 8 2'0 2'2
Central
24
26
28
30
32
__
48
Manchester (km)
Figure 4. Frequency of the alopecutus melanic of Apamea crenata from Manchester south to
Crewe. Data from Table 7.
VARIATION IN INDUSTRIAL MOTHS
289
Table 9. Frequency of grey and mottled morphs in samples of 0. incertu
collected between 1967 and 1974
Ref. no. Locality
4
7
8
9
14
16
18
21
25
26
28
31
33
34
35
37
38
42
43
45
46
49
52
54
55
57
60
77
81
82
84
Ashton-under-Lyne
Poynton
Prestbury
Stockport
Heaton Moor
Levenshulme
Longsight
Wilmslow (a)
Moss Side
Didsbury (b)
Didsbury (c)
Wilmslow (c)
Chorlton (b)
Wythenshawe
Salford
Jodrell Bank
Sale (a)
Hale
Eccles
Knutsford (a)
Knutsford (b)
Crewe
Risley
Hartford
Winwick
Mouldsworth
Sunnyside
Rowarth, Derbys.
Staines, Surrey
Nettlecombe, Somerset
Budleigh Salterton, Devon
Year
Grey
1967
1974
1974
1974
1972
1972
1967
1974
1968
1967
1972
1972
1974
1972
1972
1972
1972
1967
1972
1973
1975
25
0
25
0
100
1
0
0
-
-
32
33
17
5
12
5
19
16
9
5
5
65
12
89
5
22
33
10
12
77
29
4
6
29
3
20
5
17
59
57
3
34
3
3
2
0
3
2
1
1
91.3
94.3
100
8.6
5.7
5.9
100
0
0
1
35
35
17
5
12
5
20
16
0
9
0
0
5
5
71
12
118
5
23
33
12
16
84
29
6
7
38
3
23
5
19
65
59
3
71
3
1972
1972
1974
1973
1972
1974
1972
1974
1969
1968
1974
1972
1974
.
Red
0
0
0
1
6
0
29
0
1
0
2
4
7
0
2
1
9
0
3
0
2
6
2
0
37
0
Total Mottled
0
0
0
1
0
0
0
3
1
6
0
0
%grey
-
-
95
100
-
91.5
100
75.4
-
% mottled
0
-
0
6.3
-
4.2
8.3
5.1
-
3
0
3
91.7
100
0
76.3
0
87.0
0
-
13.0
3
89.5
90.8
96.6
15.8
0
-
4
47.9
5.6
6
0
0
0
0
0
3
0
1
0
-
-
-
7.1
-
-
0
1.7
-
Discussion
Table 9 shows that the grey morphs predominate in the study area although
there is some indication of a declining frequency towards the south. In
contrast, greys account for less than 50% of the sample from Nettlecombe,
Somerset. The two highest frequencies of the mottled morph were found at
Mouldsworth and Hartford (16 and 13%) in the west of the study area in
relatively small samples, but the frequency of mottled is always low. On the
strength of the available data there is no evidence of association of mottling
with one colour.
Ford (1972) cites 0. incerta as an example of a moth showing a large degree
of variation in colour and marking throughout the whole of a more or less
continuous range. He suggests that the wide range of variability shown by a
number of common moths may serve to prevent the formation of a searching
image by avian predators. However in Manchester this variation does not appear
to exist to any appreciable extent and the conclusion could be drawn that the
21
290
J . A. BISHOP, L. M. COOK AND J. MUGGLETON
grey form has some selective advantage over the other morphs. I t is tempting to
think that this might be another example of industrial melanism in which the
grey morphs match their grimy surroundings more closely than the other
morphs. A contrasting situation is found in Noctua pronuba, another very
variable and widespread moth, in which the morph frequency throughout Great
Britain is more or less constant and there is no indication of an increase of the
darker morphs in Manchester (C. E. M. Dale, unpublished data).
Orthosia gothica
The life-cycle of this species is similar to that of Orthosia incerta. The
general colour of the forewing ranges from a pale grey to a pale red or pink,
with a considerable amount of variation between these extremes. There is a
distinctive black mark around the orbicular stigma which gives the species its
English name (the Hebrew Character). This mark is subject to some variation, it
is reddish in the form gothicina and may be absent or indistinct in specimens
from Scotland (South 1961). Another form with a slightly differently shaped
mark is known as circumsignata and is associated with sterility (Ford, 1972).
Askew et al. (1971) referred t o the form gothicina in the study area, but this
name should not in fact be applied to these specimens as the black markings are
quite distinct, although the general ground colour is red or pink. For the
purpose of this paper they will be referred to as “red”.
The present survey
Between 1971 and 1974 we obtained samples of 0. gothica from 28 sites in
the study area, and from four sites elsewhere. The samples from two of these
sites, Meols and Rusholme, came from an assembling trap. The remainder were
taken in mercury-vapour light traps. The samples were examined for the
frequency of the grey and red ground coloration. As the detailed patterning of
the forewings made scoring difficult in some specimens the colour of the
thoracic scales which is the same as the ground colour of the forewings, was
used to distinguish the grey from the red morphs. The samples collected by
Askew et al. (1971) were also re-scored, and the results are shown in Table 10.
Genetics
Ova were obtained from three wild females caught in MV traps in 1972. Two
of these females were “grey” the other was “red”. One female laid about 250
eggs, the others laid rather less. The ova were laid in batches on the netting
covering the sides of the boxes in which the adults were kept. The larvae were
reared throughout on Hawthorn (Crataegus monogyna Jacq.), and mortality
was very low. The adults emerged from the pupae early the following year.
Some crosses were obtained from these progeny and were reared in the same
manner. However on this occasion there was considerable mortality in both the
larval and pupal stages.
The results of these breeding experiments are shown in Table 11. With the
exception of the red x red crosses none of the morph ratios is significantly
different from 1:1 using the x2 test. This indicates that there is segregation at a
single locus. If red was dominant to grey the parents of the two red x red
VARIATION I N INDUSTRIAL MOTHS
29 1
Table 10. The frequency of the “grey” morph of Orthosiu gothicu in samples
collected 1)etween 1967 and 1974
Ref. n o . Locality
Date
Grey
Red
Total
% grey
1
2
4
5
7
Disley
Marple
Ashton-under-Lyne
Bollington
Poynton
1974
1974
1967
1973
1973
1974
7
8
57
12
23
1Y
60
16
5
w
111
49
20
29
44
1974
1972
1972
1973
1974
1967
1968
88
41
15
27
36
45
24
28
31
33
34
35
37
38
41
42
Didsbury ( c )
Wilmslow ( c )
Chorlton ( b )
Wythenshawe
Salford
Jodrell Bank
Sale ( a )
Radcliffe
Hale
1972
1972
1974
1972
1972
1972
1972
1974
1972
1973
1975
13
54
8
61
104
101
17
2
13
3
1972
1972
1972
1974
1973
1972
1974
1972
1974
1969
1972
1968
1974
1974
1972
1974
3
4
3
1
8
23
8
5
2
8
9
6
15
7
13
2
18
16
48
5
1
7
2
4
Prestbury
Heaton Moor
Levenshulme
Rusholme
Wilmslow (a)
Didsbury (b)
Ecclcs
Sale (b)
Knutsford (a)
Knutsford ( b )
Deansgreen
Risky
Hartford
Win wi ck
Mouldsworth
Sunnyside
Meols
Rowarth, Derbys.
Woodchester. Glos.
Staines, Surrey
Nettlecornbe, Somerset
Budleigh Salterton, Devon
-
41
8
14
16
19
21
26
43
44
45
46
51
52
54
55
57
60
69
77
78
81
82
84
7
~
a
10
-
26
25
3
26
12
4
5
12
21
13
71
16
57
6
2
21
2
i-5
10
2
10
6
1
1
5
3
12
22
24
18
5
2
232
12
84
20
67
10
79
120
149
22
3
39
35
5
36
18
5
6
17
24
25
93
40
75
11
4
253
14
-
95.0
75.0
91.3
79.3
83.7
75.0
93.1
81.8
82.1
65.0
80.6
-
77.2
86.7
67.8
77.3
-
66.6
71.4
-
72.2
66.7
-
70.6
87.5
52.0
76.3
40.0
76.0
.~
-
8.3
14.3
crosses would be heterozygous and should produce segregating progeny. The
observed result suggests that red is recessive.
Discussion
The results of our sampling show that a high frequency of the grey morph is
found throughout the built-up part of Greater Manchester although the
frequencies are not so high as those for the grey morph of Orthosia incertu.
There is some indication of an increase in the red forms towards the periphery
of the conurbation and the highest frequencies of red are found at two western
J. A. BISHOP, L. M. COOK AND J . MUGGLETON
292
Table 11. Results of breeding experiments with grey and red morphs of
0. gothica
Parents
Brood
Progeny
grey
d
G1172
unknown
G2/72
unknown
G3/72
unknown
G1173
red
ex G1l72
grey
e x <;2/72
red
ex G2l72
red
ex GI172
G2/73
G417 3
G6173
9
gre Y
Jodrell Bank
greY
Wythenshawe
red
Sale (a)
red
ex G1172
red
ex G2172
grey
ex G2172
red
ex GI172
red
d
9
d
9
65
56
54
57
21
13
10
10
32
43
34
27
0
0
20
17
6
16
10
12
12
4
5
7
0
0
13
11
sites, Mouldsworth and Meols. The sample from Nettlecombe in Somerset is
strikingly different in appearance from the Manchester samples and has only
8.3% of the grey morph. A rather small sample from Budleigh Salterton in
Devon shows a similar predominance of red.
In addition to 0. gothica and 0. incerta there are a number of other species
which show a grey/red dimorphism. Of particular interest are Paradiarsia
gZareosa and Xestia agathina both of which have distinct black markings, similar
to those of 0. gothica, together with grey and red forms. In both these species
the red forms are most common in the west of England and the darker forms
are commoner towards the north (South, 1961). This may indicate that there is
a common selective factor influencing the greyhed dimorphism in all four
species.
CONCLUSION
The polymorphism in Biston betularia is rightly considered to be the classic
example of industrial melanism. The morphs are very distinct from each other,
and the insects are undoubtedly exposed to predation. In extreme polluted and
unpolluted habitats the carbonaria melanic and the typical are respectively very
cryptic on their usual resting background while the other form stands out. In
addition, within the United Kingdom the species is not polymorphic in the
least polluted regions. I t has been suggested that it may have been polymorphic
in the remote past (Kettlewell, 1961), and there may be melanics in unpolluted
regions of the Netherlands and southern Scandinavia (Lempke, in Kettlewell,
1973; Douwes e t al., 1973). Boardman e t al. (1974) speculate on a possible
reason for this. Mikkola (1975) has recently studied the Oligia species in
Finland, however, where they are responding to urban pollution.
There are over 150 other species of moths which exhibit industrial melanism.
VARIATION I N INDUSTRIAL MOTHS
29 3
They are a diverse group which have a variety of behaviour patterns and a
variety of typical colours, patterns and sizes. The common response of all these
species implies that the selection imposed operates to favour dark colour, as
such, rather than working indirectly, as it might, for example through a greater
resistance of dark individuals t o a particular pollutant. Nevertheless, few species
show responses which are as clear-cut as those of Biston betularia.
The best parallels are found in Phigalia pilosaria and Gonodontis bidentata.
The latter species, not considered in detail here, has a melanic form nigra which
is present in London and the north of England, but not in all industrial areas
(Kettlewell, 1973). In the north-west it shows a better correspondence with
urbanization than B. betularia (Bishop & Cook, 1975), which is somewhat
surprising since the available evidence suggests that the insects tend t o hide in
cracks or under logs, leaves etc. rather than resting in exposed positions (Bishop
et al., 1975). P. pilosaria is similar to B. betularia in resting position, and in
England and Wales shows a pattern of variation similar t o that species (Lees,
1971). In our area the change in frequency from Liverpool t o North Wales is
similar though displaced towards Liverpool when compared t o that shown by
B. betularia (Fig. 2) (Bishop, 1972). The main difference between the two
species is that P. pilusaria flies during winter, whereas B. betularia is present
from June t o August, and is therefore subject to predation by a different group
of birds. There is evidence that predation does indeed occur in P. pilosaria and
imposes differential selection (D. R. Lees, pers. comm.).
In P. pilosaria, the melanics are not entirely restricted t o polluted areas.
Bishop (1972) calculated a theoretical curve of change in melanic morph
frequency for B. betularia based on data on selective predation at sites along
the Liverpool, North Wales cline. If visual predation is similar in the two species
it is perhaps reasonable t o compare this curve with the frequencies of the dark
melanics in P. pilosaria. The data fit the curves better than do those for the
carbonaria morph of B. betularia (Fig. 2 ) , but there are too many melanics at
the western end to be accounted for by the estimated visual selection. In other
parts of Wales and in Scotland (Lees, 1971) there are high frequencies of
melanics in rural, unpolluted environments, so that the association with
industrialization appears to be superimposed on an existing polymorphism. The
other species discussed in this paper favour a similar interpretation.
With some exceptions the melanic form of Apamea monoglypha increases in
frequency from south t o north in Britain. There is little evidence from the
Manchester survey that it is an industrial melanic. Two figures of over 70%
melanics from Yorkshire quoted by Kettlewell (1973) are much higher than
any of ours, but there too the frequency fluctuates erratically from site t o site.
Our breedings suggest that we are dealing with a true polymorphism, which is
obscured by environmentally induced variation in expression.
Apamea crenata, which has two very distinct morphs, is polymorphic
throughout its range, but the available data show no geographical clines. The
highest frequencies of melanics (70 t o 95%) come from the industrial north of
England, and they drop t o around 50% both to the north in Scotland and to
the south. There is a small-scale decline to the south of Greater Manchester
(Fig. 4).
Orthosia incerta and 0. gothica are likewise polymorphic outside of polluted
294
J. A. BISHOP, L. M . COOK AND J. MUCCLETON
areas. Both species are darker in north-west England than in the less polluted
south-west; the change is from grey to reddish. Neither species exhibits a
clearcut correspondence with degree of urbanization in the region of study.
For the examples considered the environmental changes brought about by
industrialization appear to have added another selective component to a
pre-existing polymorphism. The new selective pressures probably arise primarily from visual predation, but it is not known whether the polymorphisms
themselves are maintained by visual selection. One possibility is that they are
due to apostatic or reflexive selection (Clarke, 1962; Moment, 1962). The
argument was applied to moths by Ford, 1972); another is density dependent
selection against different backgrounds in a mosaic environment (Bishop &
Cook, 1975). These suggestions, as well as possible modes of non-visual
selection, would repay investigation. One essential requirement is to gain more
information on settling and hiding behaviour of the species concerned.
SUMMARY
(1) Samples of moths taken in industrial north-west England contain a higher
proportion of species exhibiting melanism, as well as being distinctly darker
than those from rural areas in the south of the country. A survey of five species
was made in Greater Manchester and adjacent areas of Lancashire, Cheshire,
Merseyside and North Wales.
(2) The Pale Brindled Beauty Phigalia pilosaria has two melanic forms
rnonacharia and “intermediate” determined by a series of three alleles. Both
melanics are commonest in urban areas, though at a lower frequency than
comparable forms in the Peppered Moth Biston betularia. There is a marked
cline of these melanic morphs in Cheshire and Wales to the south-west of
Liverpool. Its point of inflexion lies approximately 2 0 km closer to sites of air
pollution in Merseyside than the cline in the carbonaria form of B. betularia.
Notwithstanding, melanic P. pilosaria still appear to be commoner in North
Wales than one would expect if frequency is determined solely by differential
predation of morphs by birds.
( 3 ) Limited breeding data from the Dark Arches Aparnea monoglypha
suggests that the jet-black form aethiops is determined by a single dominant
gene. There is complete segregation of this melanic from the pale typical form.
However in wild-caught samples there is overlap between the forms suggesting
that further genetic or environmental factors influence the expression of the
gene. An arbitrary, but standardized division of the classes showed that the
frequency of melanism in the area varied from 8 to 30%. There were no
melanics at all in samples from south-west England though they are present
from samples taken elsewhere in northern England and from rural Scotland.
The distribution of melanism in A . rnonoglypha may be associated with both
climatic and industrial factors.
(4)The genetics of the mahogany-coloured morph alopecurus of the
Clouded Bordered Brindle Aparnea crenata is not known. The morph is at high
frequency (6597%) throughout Greater Manchester. (In this way it resembles
the carbonaria melanic of Biston betularia. ) There is a decline in alopecurus to
VARIATION IN INDUSTRIAL MOTHS
29 5
the south of Manchester. Data collected by Kettlewell indicate that it does not
fall much below 30%even in unpolluted areas.
( 5 ) Samples of both the Clouded Drab Orthosia incerta and of the Hebrew
Character 0. gothica can be separated into two classes: one based on pink
pigment and the other on grey pigment. The grey class of 0. ivacerta is
commoner in north-west England than the same class in 0. gothica. In both
species grey animals were commoner near the centre of Manchester than in
peripheral areas. The pink form predominates in samples of both species taken
in south-west England. Results of a number of crosses of pink and of grey 0.
gothica indicate that a single gene is involved and the pink character is
recessive.
(6) In each species environmental changes due to air pollution appear to have
added a further selective component t o a pre-existing polymorphism.
ACKNOWLEDGEMENTS
We are indebted t o the many people who allowed us to collect moths in their
gardens. The following were good enough to make samples available t o us:
Mr R. Abbott, Mr C. E. M. Dale, Miss E. Livett, Dr J. H. Kennaugh, Mr G.
Kenyon, Mr G. S. Kloet, Mr K. Noble, Professor P. M. Sheppard and Mr P. J.
Wanstall. Mr Kenyon also rendered valuable technical assistance and Mr P. G.
McIntyre prepared the line drawings. We are grateful t o Professor P. M.
Sheppard and Professor J. J. Murray, who kindly criticized a draft of the paper
and t o N.E.R.C. for financial support.
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EXPLANATION O F PLATE
PLATE 1
Apamea monoglypha. Melanic and non-melanic progeny from a melanic female. The positions
marked A, B and C were scored for light reflectance. Photo by L. Lockey.