llinlni;ii ui Jiitirntil «j Ihr l inntnn Swiip ( 1990 i , ;$.• 335 341.
The reliability of estimates of migration in the
peppered moth Biston betularia and some
implications for selection-migration models
P A U L M. B R A K K F I E L DSection oj' Kvolutionary Min/iigr, Department <>/ Population liiolngv, Stkelpenkadt l-1u, 2313 %1 Inden. The .Netherlands
AND
TONY G. L I K H K R T
The Heatlijield, Crowcomhe Heallifield, Lydeard Si Lawrence, 'launlun
Migration of adult males is one of t h e i i n p o i i . i n i \ a r i a b l c s i m o K c d in t h e mathematical model'- nl induMTJal melanism in fin/mi hrliilntin \ .dues lor this variable .nr based on (I,Ha from a capture-rccapturc performed l>\ Bishop (1972) using bolh lot.il .uul bred mollis v \ h u h \vrrc al Ic.ist one night old at release. We earned out an experiment to compare the r a t e ol r e c a p t u r e (lose lo the point of release l'or m o l l i s allowed lo IK a w a y i m m e d i a t e l y a l l e r t h e i r emerneiu e a r o u n d d u s k and those which were at least one n i g h t old t\\ release I ' n h e l d mollis \ \ c t r less h k c l \ lo be recaptured
suggeslins t h a i in.lies h a \ c an i n i t i a l dispersal phase on t h e i r l i i s t mghl w i n « h r e s u l t s m a h i g h c i r a t e ol e m i g r a t i o n t h a n on subséquent nighls. S u c h a phase would h a \ e been largely missed in Bishop's e x p e r i m e n t . I he implication) ol t h i s type of b e h a M o u r p a t t e r n for the models o f s p a t i a l \ a i i a l i o n li.isrcl ou a sele< l i o n - m i g r a l i o n b a l a i u e are discussed
K E Y W O R D S : Union lululana peppered m o t h i n d u s t r i a l m< I. i n i s m m i g i a l i o n d i s p i i s a l beh,mom mathematical models c \ o l u t i o n
( X ) \ I I M S
Introduction '''i.ri
Background: ]. A. Bishop's experiment 33(i A new experiment
M e t h o d s
R e s u l t s 338 Disc ussion
I m p l i c a t i o n s for sclce lioii-nngr.ilion models 339
Rclcienecs 3 1 1
l\ I R O D I C I I O N
Our i m p o r t . n i t v . u i . i b l r used in mathematical models ol' ( l i e e v o l u t i o n of i n d u s t r i e l l m e l a n i s m in the peppered moth liialon hclulan/i (see review by M a m ,
335
336 P. M BRAKEFIELD AM) I . (;. I . I K H K R I
1990) is the migration rate o f ' a d u l t males. W h i t t l e el nl. (1976) and Bishop, Cook & Muggleton (1978) have argued that migration may be the most i m p o r t a n t lac t o r maintaining polymorphism in regions of' high i n d u s t r i a l air p o l l u t i o n . A l t h o u g h the results of" the mathematieal models developed by M a n i (1980, 1982, 1990) and Cook & Mani (1980) are quite robust with respeet to variation in the average distance-moved by moths, it remains necessary to consider how a c c u r a t e the available estimates of' migration are. The only empirical d a t a describing the movement of' adult males are from an influential capture-recapture e x p e r i m e n t performed by Bishop (1972) as part of his e x p é r i m e n t a l analysis of the dine o f ' d e c l i n i n g frequency o f ' t h e black m e l a n i c form carhonaria from urban Liverpool to rural North Wales. The marked males released by Bishop were not f r e s h l y emerged and in view of the d e c l i n e In f l i g h t activity of female moths w i t h age (Licbert & B r a k e - f i e l d , 1987) we carried out an experiment to examine whether a similar phenomenon occurs in males.
B A C K e . R O t M): J A. BISHOP'S F . X l ' I . R I M K N T
The mathematical models have assumed that female peppered moths do not move. We have previously made observations on females in cages and when released onto trees following holding in captivity for varying numbers of nights (Liebert & Brakefield, 1987). These showed t h a t females do disperse on the first night following their eclosion. Most females probably only fly for a short time and, therefore, may not move very far. What is probably more significant is that flight activity is greatly reduced on subsequent nights to the extent that the majority of females are likely to mate and oviposit on the same tree they settle on following their initial dispersal phase.
The multiple-capture-recapture experiment performed by Bishop (1972) used releases both of malc-s collected in the field and of male's bred and emerged in captivity. The wild males must have been at least one night old when they were (•(•leased before dark between 18.00 and 21.00 hours B.S.T. Bishop states that the reared males were "stored in pill boxes which were kept cold" and that the experiment allowed him to compare the a b i l i t y to assemble of the wild males with those "known to have emerged in the 24 h previous to their release". Since almost all peppered m o t h s eclose in the evening a f t e r 18.00 hours these comments indie ate t h a t the cohort of bred moths used by Bishop were one n i g h t old at the t i m e o f ' t h e i r release. If males disperse more on t h e ' i r first night, or if they are then more likely te> emigrate from the area they emerge in, the c a p l m c -recapture experiment may have seriously underestimated the rate of migration in the wild.
M l ( , R \ I I0\ l\ />VS 10 \ III- I I I HUA :«7
per cent of moths moved more t h a n 2 km. A b o u l (\\o-thirds ol rce a p i u r c s had moved verv short distances. Clearly any variation in this proportion would g r e a t l y i n f l u e n c e e s t i m a t e s o f ' m i g r a t i o n r a t e . F u r t h e r m o r e , a s u b s t a n t i a l ' t a i l ' of m o t h s m i g r a t i n g long distances (say more th.in 5 k m , see Bishop, 1972) could strongly affect s p a t i a l p a t t e r n s of gene frequency, especially if most of these moths move before pairing. 1 he p r e l i m i n a r y e x p e r i m e n t reported here u as designed to determine whether the age of moths influences the proportion e x h i b i t i n g the s e d e n t a r y mode of behaviour.
Bishop (1972) also developed a m a t h e m a t i c a l model of the dine f r o m Liverpool to North Wales which was based on a series of 27 u n i t s each representing 2 k m of the i line. In addition to incorporating e s t i m a t e s of selective p r é d a t i o n ,
heterozygous adv a n t , i g e and i n i t i a l gene frequency, he assumed t h a t one in five
male m o t h s moved between adjacent u n i t s per generation. The initial model provided a poor fit to the observed dine both in t e r m s of shape and position. The fit was improved somcuh.it when the a p p a r e n t l e p t o k u r t i c p a t t e r n of m o v e m e n t was t a k e n i n t o a c c o u n t , a l t h o u g h the modelled dine remained displaced from the observed ( l i n e . Later and more sophisticated models, both of t h i s dine and other patterns ol s p a t i a l v a r i a t i o n in England and Wales, are based on an
interpretation of Bishop's data as i n d i c a t i n g t h a t males move an a v e r a g e of
2.5 km per night (see M a n i , 1990). Migration is modelled as a Gaussian f u n c t i o n so t h a t l e p t o k u r t o s i s is not t a k e n i n t o a c c o u n t .
A N K \ V K X I ' K R I M K N I
Method*
The new experiment was performed in the ( entre of the small city of Leiden in The N e t h e r l a n d s . Males used in the e x p e r i m e n t were c i t h e r local males collée ted in assembly I raps or moths bred from an Faiglish stock. Moths were released daily from 23.J une to 1 9 . J u l y 1988. Most of this period corresponded to a time of
comparatively high moth density. It fell at the end of the f l i g h t season; no moths
being c a u g h t before 20 May or a f t e r 19 . J u l y . Three assembly t r a p s were d i s t r i b u t e d over an area of several hectares centred on the B o t a n i c Gardens. In addition, about ten lemale moths which were three n i g h t s old were rc-leascd e.u h n i g h t d u r i n g the carl v p a r t of the e x p e r i m e n t i up to 1 J u l y ) o n t o trees spaced out around a 'ring' of some 150m in diameter extending into a built-up area to one side of t h e B o t a n i c Gardens. This m e t h o d of release was d e v e l o p e d bv Lieber! & Brakdicld ( 1987) to study female behaviour. Most of these fern,des remain on t h e tree of their release and any pairings w i t h free-Hying males can be recorded and the males marked. A d d i t i o n a l assemblv t r a p s or released f e m a l e s placed at v a r i o u s sitc-s a b o u t 1 km or 5 km d i s t a n t f r o m t h e - s t u d y area f a i l e d to c a t c h a n y marked males.
Almost all bred m o t h s emerged between 18.00 and 21.00 hours, d u s k f a l l i n g .it about 22.'W hours. The d i s t r i b u t i o n of male emergence over t h i s t i m e ' u hen divided i n t o t h r e e consecutive periods of about 2 h, approximated the r a t i o 1 : 2 : 1 ( T a b l e 1 ) . Moths were date-marked w i t h colour dots f r o m p e r m a n e n t marker pens. Moths successfully emerging in covered tubs between 18.00 and
c. 22.00 hours could be marked and placed on perches in bushes, trees or \ \ a l K
338 l' M I S R A K h l I I , ] . I ) AM) I C , U K H I . R l
I A I U l 1 N u m l i e r s dl i n , l i e lii\l<»i hi'lii/iinn rele.ised , u u l rei . i p l u r e d i n e,n h period of t h e e x p e r i m e n t performed <u I.cidcn m I ')f(!i : see text for details). Onl) ihc d.u.i for new releases are included I he
proportions of rc< ;iptnres nuide for dillen ni < ohm Is .ire < oinp.ired li\ ihr / lesl
( lohoT 1
1 nue ol Ai;e .il release Number ol riiirr^eiiee .' nights) releases
Number ol recaptura
/ (d.f. = 1)
A. First period of releases, 23 |uuc lo 28 June: t'nheld bred
I ' l l l i e l d f i l e d
1 oi, d unlield
Held/bred
I.o. ,il wild
18 20.110 20 22.00 >22.00 ! > 0 0 0 1 1 39 72 1 1 1 48 32
i l
21
n
( iotiip, inson nl lol, d 'iinheld' at;ainsi lol, d field + loi , il'
0 1')
H.7(i**
0.49
12.39***
fi Sei oud pi 1 lod ol releases, 29 June lo 4 J l l K : Held lilell Lo. al wild ( '. 1 liird period Held/lind I. oi , d/wild ( îomparison loi Companion loi 18 24.00 ' >
ol rele.ises, !> July lo 19 |iil\: 18 24 00 ! > 2 1 2 1 M> 46 45 84 3 7 1 20 [
held mollis m e.n h period fd.f. = 2)
loi al mollis m rai h pel n u l df'. = 2)
0.81
3.69 0.90
**/J<0.01; ***/J<0.001
'unhelcT moths in the e x p e r i m e n t were made up- ol such insects. Males which were not t r e a t e d in t h i s way were held in the tubs for their first night and t h e n released or transferred to cylindrical hanging n e t s lor a f u r t h e r n i g h t before release. These 'held' males were marked w i t h a d i f f e r e n t code to any ' u n h e l d moths released a t the same t i m e . Local m a l e s were date-marked before release on i he e v e n i n g after capture.
Both local males and bred m o t h s were released w i t h i n the 'ring' ol'released l e m a l c s in the first period of the experiment from 23 J u n e to 28 J u n e . Some of the local moths in this early part of the experiment were i n i t i a l l y collected in o t h e r areas o l ' L e i d e n . D u r i n g the second period of the experiment from 29 J u n e to 4 . J u l y , the bred moths were released within the 'ring' while most of the local m o t h s were released ( l o s e to the assembly traps in the Botanic Gardens ( t h e exception being f i v e males a t t r a c t e d to females in the 'ring' on 29 . J u n e ) . In t h e t h i r d period from 5 July to 19 J u l y , all bred moths were like the local m o t h s released w i t h i n the Botanic Gardens.
ResulU
Table 1 gives a comparison ol the r a t e - of r e c a p t u r e of the d i f f e r e n t cohorts of moths. All except six of the recaptures were made on the n i g h t following their release.
MIGRATION IN BISTOMBETULARLA 339
because of mating) suggesting that such a difference between fresh and older moths is likely to occur in fully natural conditions. A higher r e c a p t u r e rale lid moths which are at least one n i g h t old was m a i n t a i n e d in the second part of the experiment. The third part of the experiment emphasizes t h a t when local moths and bred moths which have been held for two nights are released in the v i c i n i t y of assembly traps, about one in five of each cohort are likely to be recaptured. There is no heterogeneity in recapture rate among the three cohorts of local males or of held moths.
DISCUSSION
Release experiments must always be interpreted with caution. The experiments w i t h /?. bclulann i n v o l v e releases of an u n n a t u r a l l y high density of m o t h s and however carefully the mark-release procedure is carried out it is likely to cause some elfect on b e h a v i o u r . Aliens may be more likely to emigrate t h a n locals (see Endler, 1977). Nevertheless in the present experiment the lower rate of recapture among moths released immediately after cclosion t h a n among those released when they were at least one night old requires explanation. Although numbers of recaptures are small, there was a roughly tenfold différence in r e c a p t u r e rate in the first period o f ' t h e experiment (Table 1). The most likely e x p l a n a t i o n is t h a t males are more l i k e l y to e m i g r a t e from the vicinity of their site of cclosion or of d a y t i m e resting during their first night t h a n on subsequent nights. Most males are probably u n l i k e l y to lind a receptive f e m a l e on their first night because of competition w i t h older, local males whose wings and genitalia are fully hardened. Released females which pair u s u a l l y assemble males and m a t e shortly after dark before about 23.00 hours (Lieber! & Brakelield, 1987). Inspection of oui' released ' n n h e l d ' moths on t h e i r perches showed t h a t some m o t h s had not left by t h i s time. Therefore, by the t i m e freshly eclosed males, especially those emerging in the hour or two before dusk, are likely to be capable of pairing, most receptive females w i l l have mated. Our released moths on taking flight around dusk tended to fly rapidly more or less directly upwards and out of sight. These observations suggest that males exhibit an i n i t i a l active dispersal or migratory phase and thai this is unlikely to result in a reduced pairing success relative to males which do not e x h i b i t this behaviour. I t would be interesting to d e t e r m i n e w h e t h e r males are responsive to the female pheromone d u r i n g their i n i t i a l f l i g h t .
Our observations from t h i s s t u d y and the earlier work (Lieberl & Brakefield, 1987) can be summari/ed by the following scenario. Most females probably m a t e on their first night soon after a short dispersal (light following dusk. In contrast, many males migrate on their first night and are u n l i k e l y to m a t e because of competition from local, old males for the comparatively small proportion of calling females. Females will tend to pair w i t h males which have survived at le.ist one day in the vicinity of the p a i r i n g site a l t h o u g h t h i s may be some kilometres away from where they developed and emerged. Further detailed work is necessary to s u b s t a n t i a t e t h i s scenario and to quantify the phenomena.
Implications for selection-migration model.\
340 P. M. B R A K K F I K M ) AND I (;. I . I I . B K K I
release was at 8.4%, intermediate between our rates of recapture lor local and unheld moths (21.0 and 1.8%, respectively). There may he a more specific problem in trying to relate our observations to the results of Bishop's e x p e r i m e n t . While our held moths were able to fly when in captivity the bred males which were released by Bishop had been held in cooled pill boxes and, therefore, had not flown prior to release. The same is clearly not the case for his wild males which were presumably in a similar state to the local males we released. Furthermore, Bishop's table 9 indicates that bred males comprised the minority of his releases (about 13%). Therefore, a stronger tendency of'freshly eclosed males to emigrate than moths which are older than one night may mean that the estimates of'migration rate from Bishop's experiment seriously u n d e r e s t i m a t e t h i s parameter. The effect of any such discrepancy on the average distance-moved is likely to be exaggerated by a leptokurtic distribution of distance-moved as demonstrated by Bishop (1972). Perhaps fortunately the extraction from Bishop's data of a value for the average distance-moved by a male moth per night for i n p u t into the later mathematical models (Mani, 1990) appears to have-erred on the generous side. Thus his tables 3 and 4 show that this mean value lor his releases was 1.15km while the models have concentrated on a value of 2.5km. Even so we consider that attention should be paid to obtaining more reliable estimates of migration and also of taking the probability of long-distance movement of many males in their initial dispersal phase into account. Similarly, long-distance movement, perhaps more directional in nature, may also occur by passive dispersal of newly hatched larvae on the wind or thermals (sec Liebert & Brakefield, 1987).
A general point of concern about the models is that they assume that selection takes place before migration for the r u n s corresponding to each day of the f l i g h t period. If the above scenario is largely t r u e and, in particular, if m a l e (and female) migration tends to occur on the f i r s t n i g h t , m o t h s emerging around dusk, then prédation by birds in n a t u r e w i l l lend to occur aller, r a l l i e r than before, migration. The short expectation of a d u l t l i f e would increase the possible bias which may be introduced by applying selection before migration in the models.
We also note w i t h respect to (he models of the dine ol'decreasing frequency of
carhiinaria melanics from Liverpool to North Wales that one ol the seven selective
prédation experiments using c o h o r t s of dead moths glued to tree t r u n k s was carried out at Hawarden about h a l l w a y along the transect and near l i r e point of inflexion in the dine (Bishop, 1972). This l o c a l i t y was dose to the large coal-fired steel works at Shotton and was associated w i t h local increases in air pollution and m e l a n i c frequencies in K. helulana and (ionndonln hitli'iiltila (Bishop, 1972; Bishop & Cook, 1975; Bishop et «/., 1978). The frequency of airbonarin at Hawarden was 87",, (Bishop, 1972) and the species d i v e r s i t y of epiphytes on oak trees was low (Bishop el a/, 1975). The estimated selection coefficient derived from the p r é d a t i o n e x p e r i m e n t performed at Hawarden suggested ( h a t , if anything, lypica n o n - r n e l a n i c s were favoured over carbonaria. It is u n f o r t u n a t e that the e x p e r i m e n t was not replicated to check the r e l i a b i l i t y of t h i s estimate based on 104 moths since this p o i n t has a s u b s t a n t i a l i n f l u e n c e on the form ol the f i l n e s s curve employed in the models. If visual sélection a c t u a l l y favoured
carbonaria at Hawarden in 1972 it is u n l i k e l y t h a t the f i t n e s s c u r v e would
M I G R A T I O N I N H!S/O.\ /!!•:/1 ' / . . l A ' / . l 341
observed clinc and (lie inodd dines based on a balance between visual selection and migration; the l a t t e r being displaced towards Liverpool. It would also be interesting to exclude t h e estimates lor Hawarden and model the dine r u n n i n g along a more direct transect from the Liverpool sites to those in N o r t h Wales (see fig. 1 in Bishop, 1972). The dine along such a transect would have had a point of inflexion substantially closer to the model elines involving only visual selection and migration which have already been (leveloped (see Mani, 1990).
While we reeogni/e t h a t the modelling approach has not been t a k e n in an a t t e m p t to provide any more or less complete e x p l a n a t i o n of industrial m e l a n i s m in R. belt/lurid, our remarks emphasi/e t h e need for more detailed information on the p o p u l a t i o n biology of t h e species and lor more experimental work. This w i l l be required before a n y such explanation can be expected.
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