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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% toless that 10%, the others to smaller extents. Changes in several species over as great a magnitude and as wide an area mustresult from selection. The results are compared with others along a transect through northern England. The onset ofresponse 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 beselective predation, which is shown to be critically dependent on predation rate. As a consequence, differences in settlingbehavior 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 mothspecies increased in frequency in parts of Britain followingindustrialization in the 18th and 19th centuries (Kettlewell1965; Kettlewell 1973; Majerus 1998). Northern England,

with its intensive coal-fired manufacturing industry, wasa center both of environmental change and of the earliestrecords of response by moth populations (Cook 2003;Kettlewell 1973; Lees 1981). Blackening of trees, buildings,and vegetation was extreme, and the atmosphere was heavilypolluted with a variety of toxic gases. The response of mothpopulations in west Yorkshire was noteworthy enough forspecial 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 ofextreme black forms in the peppered moth Biston betularia(L.).

They attracted attention during the 1870s and had becomethe prevalent form by the start of the 20th century. Inanother species, the scalloped hazel Odontoptera bidentata(Clerck), melanics began to be seen in the 1890s and withina decade had become very common. Porritt lists 30 species in

which such distinct black forms were regularly obtained. Ofthese, seven had been recorded before industrialization,

whereas others were novel. He added another 21 species inwhich dark individuals occurred so frequently as to suggestthey were part of the same phenomenon, among them theclouded bordered brindle, known then as Xylophasia rureaandnow as Apamea crenata (Hufnagel).

From the middle of the 20th century, there has beena general environmental improvement and a correspondingreduction in melanic frequencies (Clarke et al. 1985, 1994;Cook 2003). Similar changes have been seen in the UnitedStates (Grant and Wiseman 2002). West Yorkshire, withLeeds and it sister city, Bradford, at its center, was one of the

major British industrial regions and one of the last toexperience a decline in morph frequencies (Cook et al. 2002).

York is situated in an extensive rural region 40 km to thenortheast. Comparatively little information is available from

Yorkshire, compared with industrial Lancashire and ruralnorth Wales, which lie to the west separated from Yorkshireby the Pennine chain of mountains. To enlarge the areaexamined a study was set up 37 years ago by S. L. Sutton inLeeds 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 thesubfamily Ennomiinae of the Geometridae. A. crenatabelongs to the subfamily Amphipyrinae of the Noctuidae.

All have annual nonoverlapping generations and fly fromearly May to June (O. bidentata) or May to July for the othertwo species.

A set of results for the same species were collected byT. J. Crawford from 1990 to 2004 near York. The new dataextend records eastward, so that we now have a transect over200 km in extent passing through a full range of availablehabitats and climate types in north Wales and northern

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Journal of Heredity2005:96(5):522528doi:10.1093/jhered/esi082Advance Access publication June 30, 2005

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England. The main locations referred to are shown in Figure 1.

The efforts of recorders at the beginning of the 20th centurywere of immense importance in bringing the phenomenon ofindustrial melanism to the attention of the scientificcommunity. The records were nevertheless often fragmen-tary and anecdotal. We hope to ensure that more detailedmaterial is available for analysis from the end of the period ofhigh melanic frequency.

Materials and Methods

The Leeds survey was carried out from 1967 to 2003 at sites10 km NE of the city center in an area of suburban buildingand farm land. For the first 3 years the site was at Scholes(National Grid Reference 4377 4366) and subsequently 4 kmdistant at Bond Ing meadow, Shadwell (GR 4344 4394),a mature garden and pasture with extensive planting of treesand hedges. Sampling was by mercury vapor light trap andtook place throughout the flying season where possible, but

sometimes for shorter periods. This method of trappingcollects almost entirely males in the species concerned, butthe variation is the same in the two sexes. The York site is atHaxby (GR 4610 4587), about 5 km north of the city centeron the edge of the built-up area. The same type of light trap

was used, and continuous sampling was carried out duringthe relevant part of every year.

B. betulariawas scored as the dominant melanic carbonariaJordan or the dotted white typical. At Leeds the intermediate

insularia forms have been extremely rare. Only about 10specimens were seen throughout the sampling period, so this

type was ignored. At York, insularia was more common andhas been recorded (see Cook and Muggleton, 2003, fora summary of information on the melanic types). O. bidentata

was scored as the dominant melanic nigraProut or as typical. Typicals from this region are darker than those fromsouthern England but always clearly distinguishable from

nigra. The genetics of melanic mutants in both species was

first established by Bowater (1914). A. crenata was scored asdark or pale. The two types are very distinct. The pale form isstraw-colored with mahogany brown markings at the edgesof the wings, whereas the dark form has the entire forewingmahogany-colored except for a paler line round the orbicularand reniform stigmata. Kettlewell (1973) used the name

alopecurusfor this form. The correct name is probablycombustaHowarth, 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 blackcostal streaks and edge to the reniform stigma (Bretherton

et al. 1983). The dark insects at the sampling sites all havethe same phenotype. The three species are illustrated byKettlewell (1973), Bishop and Cook (1980), and Majerus(1998). All collecting and identification at Leeds was made byor 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 (themelanic forms in the two geometrids are dominant, and wehave no information on A. crenata). The selective disadvan-tage v of the melanic form relative to the nonmelanic hasbeen estimated from the equation L0 : M0(1 v)n Ln : Mn

where the L and M are the initial frequencies and the final

frequencies after ngenerations of nonmelanics and melanics.It follows from this relation that when the logarithms of theratios show a linear change with generation the slopeprovides an estimate ofv. The calculation has been found togive an adequate degree of accuracy and to be robust underconditions of high or low frequency (Cook et al. 1999a).

Results

The numbers collected at Leeds in the three species areshown in Table 1. There was a gap in collecting in 198889,

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.

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after which sampling was often of limited duration. Capturesare generally lower in later years. This may reflect secularchanges in population densities. In a wide-ranging survey ofover 300 British moth species over the past 35 years, Conradet al. (2004) found that more than twice as many speciesdeclined than increased in numbers. There was also regional

variation in the trends, which are probably the result of bothhabitat and climate changes. The York samples are given in

Table 2. A. crenata is relatively much rarer at York than atLeeds; we know of no reason for this difference. The figuresfor B. betularia19902000 are also given by Cook and Grant(2000).

Except for A. crenata at York, all three species showa drop in melanic frequency at both places, which is mostmarked in B. betularia. Mean frequency estimates areillustrated in Figures 24, with their binomial standarderrors. For some years with low numbers data have beencombined; the horizontal bars indicate the dates involved.

Discussion

B. betularia

In Figure 2 a curve has been fitted by eye to the Leeds data toindicate the observed trend in frequency of carbonaria. From

a situation where there were almost 100% melanics in the late1960s, the frequency has declined to less than 10%. Theterritory extending WSW from Leeds across Lancashire andCheshire and into north Wales has received considerableattention in studies of morph frequency (Bishop, 1972;

Figure 2. Change in frequency of the carbonariamelanic form

of the peppered moth Biston betularia in Leeds and York.

Vertical lines are standard errors, horizontal lines show where

data have been grouped. The curve labeled Leeds is a selection

curve showing the trend in the Leeds data. M and C are similar

curves fitted for comparison to data from Manchester (Cook

et al. 2002) and Caldy, west of Liverpool (Grant et al. 1996).

Inset: records for York 19902000 are superimposed on the

Leeds curve.

Table 2. Numbers of moths in three species caught in York

Date B. betularia O. bidentata A. crenata

1990 11 2 6 2 5 1991 21 1 12 1 4 3 261992 20 0 7 2 4 3 101993 16 1 6 3 7 3 111994 9 0 6 1 6 3 8

1995 6 0 2 4 20 5 121996 19 3 15 6 12 2 51997 8 2 9 5 15 1 51998 7 2 8 3 19 0 61999 10 0 17 7 20 3 42000 5 3 16 3 11 1 42001 7 2 12 4 14 4 82002 14 0 30 3 23 2 62003 7 1 19 3 11 6 102004 2 1 12 2 9 1 3

Note: The columns for B. betulariaare carbonaria, insularia, and typical. For the

other two, melanics in first column, nonmelanics in second.

Table 1. Numbers of moths in three species caught in Leeds(melanics are shown in the first column for each species,nonmelanics in the second)

Date B. betularia O. bidentata A. crenata

1967 47 0 34 10 1968 58 0 44 19 1969 27 0 32 19

1970 75 1 10 20 32 121971 41 0 10 5 40 61972 76 0 22 6 26 61973 40 1 40 20 72 311974 40 0 24 16 25 101975 3 0 28 7 33 101976 19 2 23 21 34 131977 18 0 12 12 4 21978 23 2 75 33 26 151979 43 3 48 35 15 41980 49 2 64 62 74 371981 1982 48 4 53 4 77 331983 57 4 10 9 97 401984 27 1 21 18 69 24

1985 48 5 17 12 56 241986 83 3 23 13 94 581987 12 1 14 13 69 321988 1989 1990 5 2 2 3 51 311991 34 16 3 18 75 371992 27 9 16 20 96 461993 18 11 11 7 19 211994 7 11 4 2 19 201995 1 5 3 4 8 131996 4 1 5 7 3 31997 2 1 0 0 0 01998 1 8 1 3 5 21999 9 13 10 10 8 7

2000 6 18 11 18 33 192001 2002 2003 1 15 8 16 41 28

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Bishop et al. 1978; Clarke and Sheppard 1966; Cook 2003).There are also temporal series of records for Manchester andCaldy. Manchester is separated from Leeds by the Penninesbut is within the region that had over 95% carbonaria duringthe 195070 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 isjust to east of the cline in north Wales, which saw thefrequency drop to 5% over about 25 km. It is the mostcomplete data set, being based on a series of large samplescollected annually until 2002. Manchester is about 65 kmfrom Leeds, and Caldy about 130 km. The data for both sitesare plotted together for comparison in Cook (2003).

Curves M and C in Figure 2 are lines similar to that forLeeds, fitted to the data for Manchester and Caldy,respectively. It can be seen that as one proceeds west theinitial frequency becomes lower, the decline commencesearlier and is less steep. At Leeds the drop to 90% carbonariaoccurred nearly 20 years after that at Caldy. It reached 50%9 years later than at Caldy and 6 years after Manchester. Thedata for York are shown inserted on Figure 2, using the samegrid of frequency and dates and with the Leeds curvesuperimposed as a comparative guide. The commencementof the decline is as delayed at York as at Leeds. Figures fromthe two places for the early 1990s map onto each other.

Thereafter the drop has been slower at York, and thefrequency of carbonaria is probably still appreciably higherthan at Leeds. As noted long ago by Kettlewell (1965, 1973),the effects of industrialization on melanic frequency appearto be displaced to the northeast.

The changes observed result from all the processesoperating on the populations, namely selection, migrationfrom populations with different frequencies, mutation, andrandom drift. Changes of as great a magnitude over as widean area as observed must involve selection, and over themiddle part of the frequency range the contribution of the

other processes is likely to be negligible in comparison. Overthe period 19802003 the disadvantage of the melanicmorph compared with typical (estimated from the slope oflog morph ratio on year for the period when the slope waslinear) 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 washigher (for the comparison of Leeds with Caldy the differ-ence is significant, p , .05).

When initial frequencies are very high, however, thebalance of the different forces changes, and makesestimation difficult. If carbonaria gene frequency in Leeds

was truly 100% before 1970, then no change would havebeen possible without introduction of typicals by mutationor migration of immigrants from regions of lower frequency.Because typical is recessive, these processes would haveintroduced genes in heterozygotes that were not subject toselection, and the response to selection would necessarily be

very slow. It is likely that the response observed was in somepart due to immigration. Population density is probablylower in industrial than in rural areas (Cook 2003), so that tothe west of the Pennines, net migration is likely to beeastward, bringing with it the typicals characteristic of north

Wales. We do not know whether there are areas of lowerfrequency farther east than York from which immigrationmay take place. For two points nearer the east coastBeaumont (2002) notes that at Spurn (; GR 5400 4100)there was recently a rapid change from the majority beingmelanic to the majority being typical, while at Hutton Rudby(GR 4507 5506) there has been a steady decrease in melanicsfrom about 70% in 1990 to about 40% in 2000. Selectionprobably also changes with time. The data for Caldy cannotbe fitted by a constant selection curve (Grant et al. 1996),selection apparently being low at the start, greater during themain period of change, and probably finally falling off. Such

variation in selection may well occur at the other sites.

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.

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.

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O. bidentata

This species is similar in size to B. betularia, although withdifferently shaped wings, and flies at roughly the same timeof year, when it will encounter similar predators. Patterns ofmorph frequency distribution and results from mark-release-recapture experiments suggest that it is much less mobilethan B. betularia(Bishop et al. 1978; Bishop and Cook 1980).

The melanic form nigra is absent from the south of England,but high frequencies have been recorded in the industrialnorth. Variation in nigrafrequency is more closely associated

with urbanization than is carbonariain B. betularia, frequenciesrising in major centers and falling between them (Bishop et al.1978). In the 1970s the frequency of nigra was over 70% incentral Manchester, falling to 20% in suburbs a few km to thesouth. In Liverpool, however, it did not rise above 50% inconditions superficially very like those of urban Manchester,and there was an undulating rise and fall in frequency as onemoved eastward between the two centers. Sample sizes arerelatively low, and to show the patterns more clearly, means

for pairs of years are illustrated in Figure 3 (calculations are

based on individual years). In Leeds the frequency of nigramay have been initially even higher than in Manchester atabout 75%, although there is no indication that it ever rose tothe level ofcarbonariain B. betularia. Since then, there has beena steady but shallow decline to 3040%. We have noexplanation for the unusually low frequencies in 1970 and1991. In York, frequencies are much lower but also appear tohave declined. The apparent selection against nigra is 3.8 61.1% per year at Leeds, whether or not the low figures areexcluded (p , .01 in either case). At York the estimate is

3.76 2.4, which is not significant. Very similar changes havebeen observed in the Manchester area (Cook et al. 2004).Four km south of central Manchester the frequency has

declined from 69% in the 1970s to 51% now, with selectionagainst nigra of 3.5 6 0.5%. Two more westerly locationsthat scored 58% in the 1970s now have 39%. Because thespecies moves less than B. betularia immigration will corre-spondingly lave a lesser effect on morph frequency.

A. crenata

The clouded-bordered brindle is polymorphic for the darkand pale forms through most of Britain and Europe. Thedark form is not restricted to industrial regions, although ithas been at higher frequencies there. Kettlewell (1973) gave8093% for Bradford, compared with 28% in Hampshire,60% in other parts of southern England and 4150% innorthern Scotland. On a smaller scale, Bishop at al. (1976)recorded over 92% for 13 sites near the center of Manchesterand found that the frequency fell steadily to 60% overa 30-km transect into farm land to the south. The present

records for Leeds (Figure 4) show that the correspondence with changing conditions also occurs in time; the frequencyofcombusta has fallen from about 75% in the 1970s to below50% now. Selection against the dark form is 3.6 6 0.7%(p , .01). In both starting frequency and slope the changetherefore closely follows that of nigra in O. bidentata. The

numbers ofA. crenatacollected in York are small. There is nodetectable change over the 14 years of recording. The meanfrequency of melanic is 23.9%, much lower than in Leeds orManchester and comparable with rural sites in other parts ofBritain.

Causes of Change

Following the advent of effective clean air legislation andmonitoring in the late 1950s, the old industrial environmenthas been cleaned or demolished and rebuilt. The amount of

vegetation has greatly increased compared with the early 20thcentury. Atmospheric pollution has declined dramatically.Data for Bradford show that by 1971 the concentration ofsulfur dioxide was half that in 1962 and that it had halvedagain by 1980. The 1962 concentration of smoke was halvedby 1966 and halved again by 1973. The data presented hereshow that three species of moths have all responded tochanging ecological conditions with a fall in frequency ofmelanic forms. In the case ofB. betulariain Leeds, the changeis parallel with but more extreme than other declinesobserved in locations to the west. In the other two speciesthe decline is less marked but nevertheless appreciable.

Together they demonstrate the power of selection broughtabout by a changing environment. Majerus (1998) has arguedstrongly that the explanation for industrial melanism in

B. betularia, and probably generally in moths with melanicforms, can be found in selective predation by birds. Therehas been considerable discussion of whether the experimentson selective predation carried out to date show its nature andstrength (Grant and Howlett 1988; Howlett and Majerus1987; Mikkola 1979). Whether or not the experimentsactually demonstrate that predation is sufficient to accountfor the observed patterns, the difference in response betweendifferent species may indicate that additional forces operateas well. Industrial melanism is also seen in two-spot ladybirds(coccinellid beetles) that are distasteful to many predators(Benham et al. 1974; Creed 1971; Majerus 1998). The situa-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

are sometimes the result of selective forces independent ofindustrial conditions.

One point to be made with respect to selective predation,however, is that the three species discussed here havedifferent daytime resting places that probably make them

visible to potential predators to different extents.B. betularia

rests exposed on surfaces. It may be found on tree trunks,but observations have shown that a preferred location is onnarrow branches in the upper parts of trees (Howlett andMajerus 1987; Liebert and Brakefield 1987; Mikkola 1979).

Where trees were not available and disturbing lights were

present, as would have been the case in industrial cities in thepast, it would have been likely to have rested on walls.O. bidentatasometimes settles on surfaces but may also crawlinto cracks or under leaves where it is less exposed.In experiments by Bishop et al. (1975) B. betularia and

O. bidentata were allowed to emerge from pupae into

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enclosures with both exposed surfaces and features thatallowed the moths to hide. There was a very strong tendencyfor O. bidentata to find covered or protected sites whereas

B. betulariaremained exposed (v2 123.7 and 285.7, d.f. 1,respectively, in two trials). Like many other noctuids,

A. crenata spends the day near the ground in long grass orherbage (Bretherton et al. 1983). Apart from differences inappearance that will make them differently visible, thesespecies are likely to experience different levels of predationeven within the same location. It is therefore interesting toconsider the possible effect of intensity of predation, asdistinct from predator discrimination.

Consequences of Selective Predation

Suppose there are Nindividuals in a predation experiment ornatural predated population, of which Lare typical and Mare

melanic (L M 1). In the absence of selective removala fraction I is eaten (0 , I, 1). Predators detect the twoforms differently. Suppose that for every typical detected 1

a

melanics are detected. Choice by predators is exertedthrough prey individuals eaten, while the effect on the preypopulation is measured on those left. This can be expressedas a coefficient v, such that

L : 1 vM L1 I : M1 I1 a:Consequently, the fitness (1 v ) of melanics compared totypicals as a result of selective predation is

1 v 1 I1 a=1 Iand

v aI=1 I:It is evident from these expressions that dv/dM 0,dv/da I/(1 I) and dv/dI a/(1 I)

2

. Theexpected estimate of v is not influenced by differences ininitial frequency between different experiments or locations,but is highly dependent on the predation rate experienced.High predation magnifies the selection resulting from a givendifference in detectability, while reduction in predationdecreases its effect. Only if I 1/2 does v a.

The maximum likelihood variance of 1 v isV 1 v1 Mv2= LMN1 I1 Maf g:

The denominator of this expression shows that the variancetends to infinity as M tends to zero or 1. There will be lowaccuracy when there are high or low melanic frequencies,compensated for if the population size N is large. The

variance also tends to infinity as I increases. However, until

Igets close to 1, the deviate v/ffip

Valso increases, so that aslong as predation is not heavy enough to endanger thepopulation or to modify predator behavior, the effectivenessof selection will increase with fraction taken. There may also

be interactions between these variables and predatorresponse, for example a might be a function of I, but wehave no direct evidence on predator reaction.

If selective predation is the main cause of the patternsseen, then it operates under quite strong constraints.Effective population size must be large to reduce drift,

especially when there are high or low frequencies. Predationrate must be substantial to ensure that predator choice istranslated into change in the prey population, but this willput 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 conditionsthat brought about industrial melanic patterns; it may havebeen higher in industrial regions than in rural ones becausefewer inconspicuous resting sites were available. Differentexposure to predation and different average densities maygenerate widely different results in species subject to thesame predators. It is therefore to be expected that response

will differ even if selective predation is the common factorinvolved. New experimental information would help usunderstand the interactions, but practical problems oftranslating 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 onthe draft. Information on atmospheric pollution in Bradford is from

www.bradford.gov.uk.

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Received November 17, 2004Accepted April 6, 2005

Corresponding Editor: Stephen OBrien

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Journal of Heredity2005:96(5)