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TErritorial defence and mating success in males of the small heath butterfly, coenonympha pamphilus L. (Lepidoptera: Satyridae)
Anita. Behav., 1985, 33, 1162-1168
Territorial defence and mating success in males of the small heath butterfly, CoenonymphapamphilusL. (Lepidoptera: Satyridae) PER-OLOF WICKMAN
Department of Zoology, University of Stockholm, S-106 91 Stockholm, Sweden
Abstract. It has long been recognized that territorial defence in male butterflies must be some sort of mating strategy and that the territories are used as mating stations. However, so far, no systematic study has established the adaptive significance of territorial behaviour. This study is an attempt to fill this gap. By comparing the distribution of territories with the distribution of locations where wild and released virgin females mated this study shows that, in the small heath butterfly (Coenonymphapamphilus), males in territories have higher mating success than males outside territories. This supports the hypotheses that the function of territorial behaviour is to secure more matings and that the territories are mating stations. Wing length measurements suggest the same. Large males residing in territories tended to mate more often than small males, which were usually found outside territories. Since resident males were larger than nonresident males, this size difference was used to see how territorial occupancy influenced longevity. Mark recapture of measured males revealed no significant correlation between wing length and the further life expectancy of males, strongly suggesting that the mating success of males in territories is also higher when measured over their whole lifetime.
By this time an impressive number of papers treating male territorial behaviour in butterflies and other insects have been published (see Baker 1983; Thornhill & Alcock 1983). In most cases these territories have been supposed to be mating stations, i.e. places which receptive females visit to become mated. Since males fight for territory ownership (Wickman 1985), it is difficult to see how this behaviour could have evolved if it did not result in a lower male density on territories and if it did not give the remaining males more matings. Release experiments with virgin butterfly females have shown that females can find male territories from considerable distances and also that they do mate there (Shields 1967; Lederhouse 1982; Wickman & Wiklund 1983). Attempts have also been made to show that residents mate with more females, i.e. have higher mating success, than non-residents. Most of these studies have concerned insect species where males control resources limiting to females and where females mate frequently (e.g. Ueda 1979; Severinghaus et al. 1981; Alcock 1982). In species where males defend mating stations lacking in obvious resources, as in most butterfly species, data are scarce. This is probably because matings are rarely observed in these species, females generally mating only once or just a few times (Shields 1967; Ehrlich & Ehrlich 1978). Davies (1978) tried instead to estimate the
differential number of female encounters made by resident and non-resident males of the butterfly Pararge aegeria. Resident males did encounter more females than non-residents and this suggests that residents may also come upon more virgin females. This is also suggested by a study on the butterfly Papilio polyxenes by Lederhouse (1982) where most matings seemed to occur in territories. However, since Davies (1978) only measured the number of female encounters and not the number of matings, and since data in these two studies did not permit any statistical treatment, evidence that males occupying territories have greater mating success than males outside territories is still lacking. Consequently, the adaptive significance of male perching stations as well as the adaptive significance of defending these sites still needs further examination. Males of the small heath butterfly, Coenonympha pamphilus, can adopt two different mate-locating strategies. Either they can remain stationary, defending a territory, or they can be vagrant, flying over large areas (Wickman 1985). The aim of this study was to see if males in territories really have higher mating success than males outside territories. To do this I recorded where released and wild virgin females mated in relation to territories and compared this result with the male distribution in relation to territories. The wing length of males was
1162
Wickman. Mating success in C. pamphilus also measured to see how size influenced territorial occupancy and mating success. To see if different costs were associated with the two different strategies, I also tried to measure eventual differences in longevity.
Sweden, on sunny days between 31 May and 26 June 1982, 24 July and 31 August 1982 and 28 May and 21 August 1983. The small heath butterfly adults were active from late May until early September and were abundant during both years of the study, especially in heaths dominated by Festuca ovina with sparse bushes and trees. Virgin females were reared from eggs laid in captivity by females collected in Timmernabben. All instars were cultured under outdoor conditions to make sure that the adults eclosed synchronously
METHODS This study was carried out in Timmernabben (56~ 16~ on the coast of south-eastern
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,~2- Gravel roads N ~.~__Sea
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Figure 1. The total number of stationary males observed in each 10 x 10 m square during 22 censuses. To calculate the mean number of stationary males per census, the figure in each square should be divided by 22. Stars indicate where virgin females were released, each star corresponding to one female. One female was released outside this area.
1164
Animal Behaviour, 33, 4
with the wild population. As many females as possible were released on each clear day, starting at 0800 hours. Females were released between 11 and 29 August 1982 and 11 and 28 June 1983 in spots where females had earlier been observed to deposit eggs (Fig. 1). Since the larvae of C. pamphilus do not move about much, these spots should have been likely places for eclosing females. All females except one were released outside territories (Fig. 1). Virgin females were marked with permanent ink on their wings for individual recognition and followed until lost or mated. The time, the place (whether in a territory or not) and the duration of all copulations were noted. The data were also recorded for wild females if they were found in copula. O f course there was a risk in including wild females, since observations could easily have been biased towards territories. However, mated pairs were never searched for specifically, but were discovered during other activities such as censuses or observations of males and females. At least as much time was spent outside as inside territories. To estimate the proportion of males inside and outside territories, a part of the habitat was partitioned into 216 10 x 10 m squares. This area was thoroughly searched three times a day, i.e. in the morning, at noon and in the afternoon, on 1, 7, 18 June, 6 July, 9, 16 and 21 August 1983, plus once in the morning on 26 June 1983, a total of 22 times. Each time, the number of stationary, vagrant, nectar-feeding and inactive males in each square was counted. Stationary and vagrant males were separated by their movement patterns. Stationary males were restricted to a small territory, usually a few metres across, while vagrant males flew over much larger areas. Stationary males also spent proportionally more time perching (Wickman 1985). Usually a few minutes or less was enough to establish whether a male was stationary or not. All squares with at least one observation of a stationary male were considered to be territories. The number of males in territories was thus calculated as the total number of males observed in squares where at least one stationary male had been observed, and the number of males outside territories were consequently the total number of males in squares in which a stationary male had never been observed. Wing length (see Lederhouse 1978) was measured with a ruler to the nearest mm through the mesh of the net. All measured males were individually marked with permanent ink on their wings.
Males staying in a territory for two or more consecutive days were classified as residents, the rest as non-residents. The life spans of males in territories and of males outside territories were impossible to measure directly as males could change strategy. Instead the correlation between large size and residentship was used (see below). Since residents were bigger than non-residents, I have assumed that any significant difference in costs between being stationary, defending a territory, and being vagrant must become apparent if the life spans of different-sized males are compared. Between 23 and 30 July 1983, 44 males were measured, marked and released in an area of 160x200 m, in order to estimate the longevity of males with different wing lengths. This area, and an additional surrounding area up to a radius of 300 m, was censused for re-sightings until 20 August when no marked male was left. The migration of males out of this area was considered to be negligible since males rarely seem to become displaced more than 300 m during their life (Wickman 1985). All means are given with standard errors.
RESULTS The distribution of all observed males during the 22 censuses in 1983 can be seen in Fig. 2. The most frequented squares are territories, i.e. squares in which a stationary male had been observed (Fig. 1). Some territories were frequented much more than others. A c o m m o n feature of all territories seems to be their location near prominent vegetation such as trees, bushes and hedges. They were never located in the middle of an open field. Males in territories mated significantly more often than males outside territories (Z2 = 7-26, df 1, P < 0.01; Table I). Out of 30 matings, 86.7~o took place in territories, although only 60"3~ of all males were observed in territories. These figures suggest that, on average, males in territories mated with more than four times as many females as males outside territories. The duration of copulations is shown in Table II. They seem to fall into two categories, i.e. short copulations lasting 1 ~ 3 0 min and long copulations of longer than 100 min. The longest mating recorded lasted more than 291 min. All the long copulations took place in territories. Matings were observed at all times of day except for the first hour
Wickman: M a t i n g success in C. pamphilus @@
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Table II. Durations of copulations 10m
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SECOND GENERATION
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1983
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1982
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Figure 2. The mean number of males (all categories) observed in each 10 x 10 m square during 22 censuses of the same area as in Fig. 1. Table I. Number of males sighted inside and outside territories during 22 censuses and number of males mating inside and outside territories
Location
Number of males
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15
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17
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13
14
15
16
17
13
14
15
16
17
Number of matings*
Inside territories 313 (60.3%) 15+ 11 =26 (86.7%) Outside territories 206 (39.7%) 2+2 =4 (13"3%) Total 519 17+ 13 =30
W I N G LENGTH (mm)
*Number of males mated with released virgin females + number of males found in copulation with wild females. D
14
of the morning 9 Long copulations showed no particular distribution relative to time o f day. Wing length measurements, b o t h in 1982 and 1983, revealed that resident males had significantly longer wings than non-residents ( M a n n - W h i t n e y U-test, one-tailed: 1982, z = - 2 - 7 3 , P<0.005; 1983, z = 4.10, P < 0.0005; Fig. 3). The two different
15
16
17
18
W I N G LENGTH (mm)
Figure 3. The wing lengths of (a) non-resident males (b) resident males and (c) mated males of the first generation of 1983 and of (d) non-resident males and (e) resident males of the second generation of 1982. (a) J~= 15-1 + 0.1, N=47; (b) J~=16.4!0"2, N=13; (c))?=15.7• N = I 1 ; ( d ) ) ? = 1 4 . 2 _+0-1, N=42; (e) J?=15.1_0.3, N=9.
Animal Behaviour, 33, 4
1166
generations also had significantly different wing lengths (Mann-Whitney U-test, two-tailed, z=5.24, P<0.001), the first generation of 1983 being larger (N=60, J?-= 15.4-4-_0.1 ram) than the second of 1982 (N= 51, )?=14.4 _+0.1 mm). The wing lengths of mated males from the first generation of 1983 were measured and this showed that mated males on average were larger than nonresidents (Mann-Whitney U-test, one-tailed, z = -2-36, P<0.01; Fig. 3). There was no significant difference in wing length between mated and resident males (Mann-Whitney U-test, two-tailed, U = 100, P<0.2). There was no significant correlation between wing length and the number of days between marking and the last re-sighting ( r s = - 0 ' 0 1 1 , N-=44, P > 0 ' 5 0 ; Fig. 4). Nor was there any significant correlation between how often a male was re-sighted and size (r~=-0.133, N=124, P < 0'2). The average expectancy of further life (see Davies 1978) of a male was 7.0 + 0.9 days. During 109 days of observation only three individuals (two males and one female) were observed being caught by predators, one by a swallow (Hirundo rustica) and two by crab spiders (Thomisidae).
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Figure 4. Male longevity (measured as number of days betweenmarking and last re-sighting + 1) as a function of wing length.
DISCUSSION My results confirm that male territories in the small heath butterfly are mating stations. Since males in territories mated more frequently than would be expected by chance, it must be inferred that virgin females behave in a way that increases the probability that they will mate with males in territories. Furthermore, the fact that territories were not found to contain more males supports the notion that interactions between males lower male density in territories and that territories really are competed for. Wickman (1985) has shown that intense and long lasting interactions (never seen between vagrant males outside territories) are common between males at sites where males are stationary (i.e. territories). After an interaction, one of the participants usually leaves the territory. The male that leaves the territory should, according to my results, have a much lower probability of finding a female. The fact that more males were not found in territories thus supports the idea that males are forced to leave the territories during these interactions. That longer interactions between males are true contests is supported by other studies on territorial behaviour in butterflies (Baker 1972; Davies 1978; Wickman & Wiklund 1983). Although sample size is small, the distribution of copulation durations in relation to territories also implies that males in territories have a higher mating success than males outside. It has been shown for several butterfly species that males mating twice within a short time span (1 2 days) remain in copula much longer during the second mating (Scott 1974; Rutowski 1979; Sims 1979; Lederhouse 1981). In territories, 31.6% of all matings were prolonged, in contrast to areas outside territories, where all copulations were of short duration (Table II). Higher mating success achieved by males in territories obviously does not mean that all males in territories were equally successful. The mating success of an individual male must be highly dependent on how long he is able to stay in a territory. Large males (i.e. with long wings) were able to remain longer and tended to mate more frequently than small males. The reason why large size is advantageous can only be speculated about. Large males are probably heavier as well as bigger than small males (Lederhouse 1978). It is known that, in many insect species, big individuals have an advantage in fights, and that they tend to accumu-
Wickman: Mating success in C. p a m p h i l u s late in territories, even in insects with no special weapons (e.g. Alcock et al. 1977; H a m i l t o n 1979; W h i t h a m 1979; Severinghaus et al. 1981; Partridge & F a r q u h a r 1983; O t r o n e n 1984). However, this does n o t always seem to be the case, since no difference in size between residents and non-residents could be found in the butterfly Papilio polyxenes (Lederhouse 1982). In the small h e a t h butterfly there was no correlation between male size a n d the n u m b e r o f days between m a r k i n g a n d last re-sighting. This result, and the observation t h a t size did n o t significantly influence h o w often a male was re-sighted, suggests t h a t being territorial could have h a d only a m i n o r impact on longevity. O n average then, males able to stay in territories p r o b a b l y h a d higher m a t i n g success t h a n expelled males even if measured over their whole lifetime. Rawlins & Lederhouse (1978) m a d e observations indicating t h a t p r e d a t i o n during roosting m i g h t be the m o s t i m p o r t a n t cause o f mortality in adults o f Papilio polyxenes. This is p r o b a b l y also true for the small h e a t h butterfly since so few instances of diurnal p r e d a t i o n were seen. There is no reason to suppose that the roosts of residents should be safer t h a n the roosts o f nonresidents. A l t h o u g h these results clearly show t h a t occupying a territory was, o n average, the most successful option, this was p r o b a b l y not true u n d e r all conditions. W i c k m a n (1985) has s h o w n t h a t the mate-locating b e h a v i o u r o f males is d e p e n d e n t on a m b i e n t temperatures. Whereas males c o m p e t e d for territories at n o r m a l Swedish s u m m e r air temperatures (below 25~ this was not the case when temperatures rose. As t e m p e r a t u r e increased males defended territories to a lesser degree and, at very high temperatures ( a r o u n d 30~ m o s t males showed v a g r a n t behaviour. Thus it is likely that vagrancy is the most successful strategy at higher temperatures. In this study t e m p e r a t u r e has not been considered. T h e higher m a t i n g success enjoyed by males in territories thus must be regarded as a n average for the whole season.
ACKNOWLEDGMENTS I t h a n k Christer W i k l u n d for n u m e r o u s discussions t h r o u g h o u t this study. I also t h a n k L e i f A n d e r s s o n and R o b i n Baker for c o m m e n t s on the manuscript.
! 167
REFERENCES Alcock, J. 1982. Post-copulatory mate guarding by males of the damselfly Hetaerina vulnerata Selys (Odonata: Calopterygidae). Anita. Behav., 30, 99 107. Alcock, J., Jones, C. E. & Buchmann, S. L. 1977. Male mating strategies in the bee Centrispallida Fox (Anthophoridae: Hymenoptera). Am. Nat., 111, 145 155. Baker, R. R. 1972. Territorial behaviour of the nymphalid butterflies, Aglais urticae (L.) and Inaehis io (L.). J. Anita. Ecol., 41, 453M69. Baker, R. R. 1983. Insect territoriality. A. Rev. Entomol., 28, 65-89. Davies, N. B. 1978. Territorial defence in the speckled wood butterfly (Parage aegeria): the resident always wins. Anim. Behav., 26, 138 147. Ehrlich, A. H. & Ehrlich, P. R. 1978. Reproductive strategies in the butterflies: I. Mating frequency, plugging, and egg number. J. Kansas Entomol. Soc., 51, 666-697. Hamilton, W. D. 1979. Wingless and fighting males in fig wasps and other insects. In: Sexual Selection and Reproductive Competition in Insects (Ed. by M. S. Blum & N. A. Blum), pp. 167-220. New York: Academic Press. Lederhouse, R. C. 1978. Territorial behavior and reproductive ecology of the black swallowtail butterfly, Papilio polyxenes asterius Stoll. Ph.D. thesis, Cornell University. Lederhouse, R. C. 1981. The effect of female mating frequency on egg fertility in the black swallowtail Papilio polyxenes asterius (Papilionidae). J. Lepid. Soc., 35, 266-277. Lederhouse, R. C. 1982. Territorial defense and lek behavior of the black swallowtail butterfly, Papilio polyxenes. Behav. Ecol. Socibiol., 10, 109-118. Otronen, M. 1984. The effect of differences in body size on the male territorial system of the fly Dryomyza anilis. Anim. Behav., 32, 882-890. Partridge, L. & Farquhar, M. 1983. Lifetime mating success of male fruitflies (Drosophila melanogaster) is related to their size. Anita. Behav., 31, 871-877. Rawlins, J. E. & Lederhouse, R. C. 1978. The influence of environmental factors on roosting in the black swallowtail, Papiliopolyxenes asterius Stoll. (Papilionidae). J. Lepid. Soc., 32, 145-159. Rutowski, R. L. 1979. The butterfly as an honest salesman. Anim. Behav., 27, 145 159. Scott, J. A. 1974. Adult behavior and population biology of Poladryas minuta, and the relationship of Texas and Colorado populations. Pan-Paeif. Entomol., 50, 9 22. Severinghaus, L. L., Kurtak, B. H. & Eickwort, G. C. 198 I. The reproductive behavior of Anthidium manicatum (Hymenoptera: Megachilidae) and the significance of size for territorial males. Behav. Ecol. Soeiobiol., 9, 51-58. Shields, O. 1967. Hilltopping: an ecological study of summit congregation behavior of butterflies on a southern California hill. J. Res. Lepid., 6, 69 178. Sims, S. 1979. Aspects of mating frequency and reproductive maturity in Papilio zeliacon. Am. Midl. Nat., 102, 3650. Thornhill, R. & Alcock, J. 1983. The Evolution o[lnsect
1168
Animal Behaviour, 33, 4
Mating Systems. Cambridge, Mass.: Harvard University Press. Ueda, T. 1979. Plasticity and the reproductive behaviour in a dragonfly, Sympetrum parvulum Barteneff, with reference to the social relationship of males and the density of territories. Res. Popul. Ecol., 21, 135-152. Whitham, T. G. 1979. Territorial behaviour of Pemphigus gall aphids. Nature, Lond., 279, 324-325. Wickman, P.-O. 1985. The influence of temperature on the territorial and mate locating behaviour of the small
heath butterfly, Coenonympha pamphilus (L.) (Lepidoptera: Satyridae). Behav. Ecol. Sociobiol., 16, 233 238. Wickman, P.-O. & Wiklund,C. 1983. Territorial defence and its seasonal decline in the speckled wood butterfly (Pararge aegeria). Anim. Behav., 31, 1206-1216.
(Received 2 May 1984; revised 5 September 1984; MS. number." 2535)
Territorial defence and mating success in males of the small heath butterfly, CoenonymphapamphilusL. (Lepidoptera: Satyridae) PER-OLOF WICKMAN
Department of Zoology, University of Stockholm, S-106 91 Stockholm, Sweden
Abstract. It has long been recognized that territorial defence in male butterflies must be some sort of mating strategy and that the territories are used as mating stations. However, so far, no systematic study has established the adaptive significance of territorial behaviour. This study is an attempt to fill this gap. By comparing the distribution of territories with the distribution of locations where wild and released virgin females mated this study shows that, in the small heath butterfly (Coenonymphapamphilus), males in territories have higher mating success than males outside territories. This supports the hypotheses that the function of territorial behaviour is to secure more matings and that the territories are mating stations. Wing length measurements suggest the same. Large males residing in territories tended to mate more often than small males, which were usually found outside territories. Since resident males were larger than nonresident males, this size difference was used to see how territorial occupancy influenced longevity. Mark recapture of measured males revealed no significant correlation between wing length and the further life expectancy of males, strongly suggesting that the mating success of males in territories is also higher when measured over their whole lifetime.
By this time an impressive number of papers treating male territorial behaviour in butterflies and other insects have been published (see Baker 1983; Thornhill & Alcock 1983). In most cases these territories have been supposed to be mating stations, i.e. places which receptive females visit to become mated. Since males fight for territory ownership (Wickman 1985), it is difficult to see how this behaviour could have evolved if it did not result in a lower male density on territories and if it did not give the remaining males more matings. Release experiments with virgin butterfly females have shown that females can find male territories from considerable distances and also that they do mate there (Shields 1967; Lederhouse 1982; Wickman & Wiklund 1983). Attempts have also been made to show that residents mate with more females, i.e. have higher mating success, than non-residents. Most of these studies have concerned insect species where males control resources limiting to females and where females mate frequently (e.g. Ueda 1979; Severinghaus et al. 1981; Alcock 1982). In species where males defend mating stations lacking in obvious resources, as in most butterfly species, data are scarce. This is probably because matings are rarely observed in these species, females generally mating only once or just a few times (Shields 1967; Ehrlich & Ehrlich 1978). Davies (1978) tried instead to estimate the
differential number of female encounters made by resident and non-resident males of the butterfly Pararge aegeria. Resident males did encounter more females than non-residents and this suggests that residents may also come upon more virgin females. This is also suggested by a study on the butterfly Papilio polyxenes by Lederhouse (1982) where most matings seemed to occur in territories. However, since Davies (1978) only measured the number of female encounters and not the number of matings, and since data in these two studies did not permit any statistical treatment, evidence that males occupying territories have greater mating success than males outside territories is still lacking. Consequently, the adaptive significance of male perching stations as well as the adaptive significance of defending these sites still needs further examination. Males of the small heath butterfly, Coenonympha pamphilus, can adopt two different mate-locating strategies. Either they can remain stationary, defending a territory, or they can be vagrant, flying over large areas (Wickman 1985). The aim of this study was to see if males in territories really have higher mating success than males outside territories. To do this I recorded where released and wild virgin females mated in relation to territories and compared this result with the male distribution in relation to territories. The wing length of males was
1162
Wickman. Mating success in C. pamphilus also measured to see how size influenced territorial occupancy and mating success. To see if different costs were associated with the two different strategies, I also tried to measure eventual differences in longevity.
Sweden, on sunny days between 31 May and 26 June 1982, 24 July and 31 August 1982 and 28 May and 21 August 1983. The small heath butterfly adults were active from late May until early September and were abundant during both years of the study, especially in heaths dominated by Festuca ovina with sparse bushes and trees. Virgin females were reared from eggs laid in captivity by females collected in Timmernabben. All instars were cultured under outdoor conditions to make sure that the adults eclosed synchronously
METHODS This study was carried out in Timmernabben (56~ 16~ on the coast of south-eastern
I~
Bushesand trees Buildings
~ ~
,~2- Gravel roads N ~.~__Sea
:''~ .... " ", " ~ - ~ :
~/~
10m
1163
~:::..i~i~~
1
/'
'",
N
@',,
~
] '/i 1
'/
.....~i....
."3.
...... -.~il
1 .....
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,
4~. 2 1
33
"" ~'9-:~
,
~r
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~7
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,'"
1
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'~l
;
',5',
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,';~ .,,//
li ~ i
/7
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Figure 1. The total number of stationary males observed in each 10 x 10 m square during 22 censuses. To calculate the mean number of stationary males per census, the figure in each square should be divided by 22. Stars indicate where virgin females were released, each star corresponding to one female. One female was released outside this area.
1164
Animal Behaviour, 33, 4
with the wild population. As many females as possible were released on each clear day, starting at 0800 hours. Females were released between 11 and 29 August 1982 and 11 and 28 June 1983 in spots where females had earlier been observed to deposit eggs (Fig. 1). Since the larvae of C. pamphilus do not move about much, these spots should have been likely places for eclosing females. All females except one were released outside territories (Fig. 1). Virgin females were marked with permanent ink on their wings for individual recognition and followed until lost or mated. The time, the place (whether in a territory or not) and the duration of all copulations were noted. The data were also recorded for wild females if they were found in copula. O f course there was a risk in including wild females, since observations could easily have been biased towards territories. However, mated pairs were never searched for specifically, but were discovered during other activities such as censuses or observations of males and females. At least as much time was spent outside as inside territories. To estimate the proportion of males inside and outside territories, a part of the habitat was partitioned into 216 10 x 10 m squares. This area was thoroughly searched three times a day, i.e. in the morning, at noon and in the afternoon, on 1, 7, 18 June, 6 July, 9, 16 and 21 August 1983, plus once in the morning on 26 June 1983, a total of 22 times. Each time, the number of stationary, vagrant, nectar-feeding and inactive males in each square was counted. Stationary and vagrant males were separated by their movement patterns. Stationary males were restricted to a small territory, usually a few metres across, while vagrant males flew over much larger areas. Stationary males also spent proportionally more time perching (Wickman 1985). Usually a few minutes or less was enough to establish whether a male was stationary or not. All squares with at least one observation of a stationary male were considered to be territories. The number of males in territories was thus calculated as the total number of males observed in squares where at least one stationary male had been observed, and the number of males outside territories were consequently the total number of males in squares in which a stationary male had never been observed. Wing length (see Lederhouse 1978) was measured with a ruler to the nearest mm through the mesh of the net. All measured males were individually marked with permanent ink on their wings.
Males staying in a territory for two or more consecutive days were classified as residents, the rest as non-residents. The life spans of males in territories and of males outside territories were impossible to measure directly as males could change strategy. Instead the correlation between large size and residentship was used (see below). Since residents were bigger than non-residents, I have assumed that any significant difference in costs between being stationary, defending a territory, and being vagrant must become apparent if the life spans of different-sized males are compared. Between 23 and 30 July 1983, 44 males were measured, marked and released in an area of 160x200 m, in order to estimate the longevity of males with different wing lengths. This area, and an additional surrounding area up to a radius of 300 m, was censused for re-sightings until 20 August when no marked male was left. The migration of males out of this area was considered to be negligible since males rarely seem to become displaced more than 300 m during their life (Wickman 1985). All means are given with standard errors.
RESULTS The distribution of all observed males during the 22 censuses in 1983 can be seen in Fig. 2. The most frequented squares are territories, i.e. squares in which a stationary male had been observed (Fig. 1). Some territories were frequented much more than others. A c o m m o n feature of all territories seems to be their location near prominent vegetation such as trees, bushes and hedges. They were never located in the middle of an open field. Males in territories mated significantly more often than males outside territories (Z2 = 7-26, df 1, P < 0.01; Table I). Out of 30 matings, 86.7~o took place in territories, although only 60"3~ of all males were observed in territories. These figures suggest that, on average, males in territories mated with more than four times as many females as males outside territories. The duration of copulations is shown in Table II. They seem to fall into two categories, i.e. short copulations lasting 1 ~ 3 0 min and long copulations of longer than 100 min. The longest mating recorded lasted more than 291 min. All the long copulations took place in territories. Matings were observed at all times of day except for the first hour
Wickman: M a t i n g success in C. pamphilus @@
>0
~
>
Table II. Durations of copulations 10m
~/~
Duration Number in Total (min) territories number
N
_>V4 ->
1165
~/2
_>1
F-
0-4 5 9 10-14 15-19 20-24 25-29 30-99 /> 100
0 0 4 7 0 2 0 6
0 0 6 8 0 3 0 6
Total
19
23
FIRST GENERATION
SECOND GENERATION
d
1983
'a
1982
V:i! ' d:i
"~
b;!
z I?ii:i!i
N-
10-
9
Figure 2. The mean number of males (all categories) observed in each 10 x 10 m square during 22 censuses of the same area as in Fig. 1. Table I. Number of males sighted inside and outside territories during 22 censuses and number of males mating inside and outside territories
Location
Number of males
,:4.:b:>
.=.. ,.
k (H,
"~k~|
5;-
.
. ,.,,.,,
k{i~!:!
~-{Lr
14
15
16
17
18
14
15
16
17
18
13
14
15
16
17
13
14
15
16
17
Number of matings*
Inside territories 313 (60.3%) 15+ 11 =26 (86.7%) Outside territories 206 (39.7%) 2+2 =4 (13"3%) Total 519 17+ 13 =30
W I N G LENGTH (mm)
*Number of males mated with released virgin females + number of males found in copulation with wild females. D
14
of the morning 9 Long copulations showed no particular distribution relative to time o f day. Wing length measurements, b o t h in 1982 and 1983, revealed that resident males had significantly longer wings than non-residents ( M a n n - W h i t n e y U-test, one-tailed: 1982, z = - 2 - 7 3 , P<0.005; 1983, z = 4.10, P < 0.0005; Fig. 3). The two different
15
16
17
18
W I N G LENGTH (mm)
Figure 3. The wing lengths of (a) non-resident males (b) resident males and (c) mated males of the first generation of 1983 and of (d) non-resident males and (e) resident males of the second generation of 1982. (a) J~= 15-1 + 0.1, N=47; (b) J~=16.4!0"2, N=13; (c))?=15.7• N = I 1 ; ( d ) ) ? = 1 4 . 2 _+0-1, N=42; (e) J?=15.1_0.3, N=9.
Animal Behaviour, 33, 4
1166
generations also had significantly different wing lengths (Mann-Whitney U-test, two-tailed, z=5.24, P<0.001), the first generation of 1983 being larger (N=60, J?-= 15.4-4-_0.1 ram) than the second of 1982 (N= 51, )?=14.4 _+0.1 mm). The wing lengths of mated males from the first generation of 1983 were measured and this showed that mated males on average were larger than nonresidents (Mann-Whitney U-test, one-tailed, z = -2-36, P<0.01; Fig. 3). There was no significant difference in wing length between mated and resident males (Mann-Whitney U-test, two-tailed, U = 100, P<0.2). There was no significant correlation between wing length and the number of days between marking and the last re-sighting ( r s = - 0 ' 0 1 1 , N-=44, P > 0 ' 5 0 ; Fig. 4). Nor was there any significant correlation between how often a male was re-sighted and size (r~=-0.133, N=124, P < 0'2). The average expectancy of further life (see Davies 1978) of a male was 7.0 + 0.9 days. During 109 days of observation only three individuals (two males and one female) were observed being caught by predators, one by a swallow (Hirundo rustica) and two by crab spiders (Thomisidae).
O z I-"tO
Q
,~ 20 I-..-
Z 15" <
O z
II
< lo2 z~ z I=I,M e~
:'i
5.
Ill
I
13
I
I
t5
I
I
~l~
17
WINGLENGTH (ram)
Figure 4. Male longevity (measured as number of days betweenmarking and last re-sighting + 1) as a function of wing length.
DISCUSSION My results confirm that male territories in the small heath butterfly are mating stations. Since males in territories mated more frequently than would be expected by chance, it must be inferred that virgin females behave in a way that increases the probability that they will mate with males in territories. Furthermore, the fact that territories were not found to contain more males supports the notion that interactions between males lower male density in territories and that territories really are competed for. Wickman (1985) has shown that intense and long lasting interactions (never seen between vagrant males outside territories) are common between males at sites where males are stationary (i.e. territories). After an interaction, one of the participants usually leaves the territory. The male that leaves the territory should, according to my results, have a much lower probability of finding a female. The fact that more males were not found in territories thus supports the idea that males are forced to leave the territories during these interactions. That longer interactions between males are true contests is supported by other studies on territorial behaviour in butterflies (Baker 1972; Davies 1978; Wickman & Wiklund 1983). Although sample size is small, the distribution of copulation durations in relation to territories also implies that males in territories have a higher mating success than males outside. It has been shown for several butterfly species that males mating twice within a short time span (1 2 days) remain in copula much longer during the second mating (Scott 1974; Rutowski 1979; Sims 1979; Lederhouse 1981). In territories, 31.6% of all matings were prolonged, in contrast to areas outside territories, where all copulations were of short duration (Table II). Higher mating success achieved by males in territories obviously does not mean that all males in territories were equally successful. The mating success of an individual male must be highly dependent on how long he is able to stay in a territory. Large males (i.e. with long wings) were able to remain longer and tended to mate more frequently than small males. The reason why large size is advantageous can only be speculated about. Large males are probably heavier as well as bigger than small males (Lederhouse 1978). It is known that, in many insect species, big individuals have an advantage in fights, and that they tend to accumu-
Wickman: Mating success in C. p a m p h i l u s late in territories, even in insects with no special weapons (e.g. Alcock et al. 1977; H a m i l t o n 1979; W h i t h a m 1979; Severinghaus et al. 1981; Partridge & F a r q u h a r 1983; O t r o n e n 1984). However, this does n o t always seem to be the case, since no difference in size between residents and non-residents could be found in the butterfly Papilio polyxenes (Lederhouse 1982). In the small h e a t h butterfly there was no correlation between male size a n d the n u m b e r o f days between m a r k i n g a n d last re-sighting. This result, and the observation t h a t size did n o t significantly influence h o w often a male was re-sighted, suggests t h a t being territorial could have h a d only a m i n o r impact on longevity. O n average then, males able to stay in territories p r o b a b l y h a d higher m a t i n g success t h a n expelled males even if measured over their whole lifetime. Rawlins & Lederhouse (1978) m a d e observations indicating t h a t p r e d a t i o n during roosting m i g h t be the m o s t i m p o r t a n t cause o f mortality in adults o f Papilio polyxenes. This is p r o b a b l y also true for the small h e a t h butterfly since so few instances of diurnal p r e d a t i o n were seen. There is no reason to suppose that the roosts of residents should be safer t h a n the roosts o f nonresidents. A l t h o u g h these results clearly show t h a t occupying a territory was, o n average, the most successful option, this was p r o b a b l y not true u n d e r all conditions. W i c k m a n (1985) has s h o w n t h a t the mate-locating b e h a v i o u r o f males is d e p e n d e n t on a m b i e n t temperatures. Whereas males c o m p e t e d for territories at n o r m a l Swedish s u m m e r air temperatures (below 25~ this was not the case when temperatures rose. As t e m p e r a t u r e increased males defended territories to a lesser degree and, at very high temperatures ( a r o u n d 30~ m o s t males showed v a g r a n t behaviour. Thus it is likely that vagrancy is the most successful strategy at higher temperatures. In this study t e m p e r a t u r e has not been considered. T h e higher m a t i n g success enjoyed by males in territories thus must be regarded as a n average for the whole season.
ACKNOWLEDGMENTS I t h a n k Christer W i k l u n d for n u m e r o u s discussions t h r o u g h o u t this study. I also t h a n k L e i f A n d e r s s o n and R o b i n Baker for c o m m e n t s on the manuscript.
! 167
REFERENCES Alcock, J. 1982. Post-copulatory mate guarding by males of the damselfly Hetaerina vulnerata Selys (Odonata: Calopterygidae). Anita. Behav., 30, 99 107. Alcock, J., Jones, C. E. & Buchmann, S. L. 1977. Male mating strategies in the bee Centrispallida Fox (Anthophoridae: Hymenoptera). Am. Nat., 111, 145 155. Baker, R. R. 1972. Territorial behaviour of the nymphalid butterflies, Aglais urticae (L.) and Inaehis io (L.). J. Anita. Ecol., 41, 453M69. Baker, R. R. 1983. Insect territoriality. A. Rev. Entomol., 28, 65-89. Davies, N. B. 1978. Territorial defence in the speckled wood butterfly (Parage aegeria): the resident always wins. Anim. Behav., 26, 138 147. Ehrlich, A. H. & Ehrlich, P. R. 1978. Reproductive strategies in the butterflies: I. Mating frequency, plugging, and egg number. J. Kansas Entomol. Soc., 51, 666-697. Hamilton, W. D. 1979. Wingless and fighting males in fig wasps and other insects. In: Sexual Selection and Reproductive Competition in Insects (Ed. by M. S. Blum & N. A. Blum), pp. 167-220. New York: Academic Press. Lederhouse, R. C. 1978. Territorial behavior and reproductive ecology of the black swallowtail butterfly, Papilio polyxenes asterius Stoll. Ph.D. thesis, Cornell University. Lederhouse, R. C. 1981. The effect of female mating frequency on egg fertility in the black swallowtail Papilio polyxenes asterius (Papilionidae). J. Lepid. Soc., 35, 266-277. Lederhouse, R. C. 1982. Territorial defense and lek behavior of the black swallowtail butterfly, Papilio polyxenes. Behav. Ecol. Socibiol., 10, 109-118. Otronen, M. 1984. The effect of differences in body size on the male territorial system of the fly Dryomyza anilis. Anim. Behav., 32, 882-890. Partridge, L. & Farquhar, M. 1983. Lifetime mating success of male fruitflies (Drosophila melanogaster) is related to their size. Anita. Behav., 31, 871-877. Rawlins, J. E. & Lederhouse, R. C. 1978. The influence of environmental factors on roosting in the black swallowtail, Papiliopolyxenes asterius Stoll. (Papilionidae). J. Lepid. Soc., 32, 145-159. Rutowski, R. L. 1979. The butterfly as an honest salesman. Anim. Behav., 27, 145 159. Scott, J. A. 1974. Adult behavior and population biology of Poladryas minuta, and the relationship of Texas and Colorado populations. Pan-Paeif. Entomol., 50, 9 22. Severinghaus, L. L., Kurtak, B. H. & Eickwort, G. C. 198 I. The reproductive behavior of Anthidium manicatum (Hymenoptera: Megachilidae) and the significance of size for territorial males. Behav. Ecol. Soeiobiol., 9, 51-58. Shields, O. 1967. Hilltopping: an ecological study of summit congregation behavior of butterflies on a southern California hill. J. Res. Lepid., 6, 69 178. Sims, S. 1979. Aspects of mating frequency and reproductive maturity in Papilio zeliacon. Am. Midl. Nat., 102, 3650. Thornhill, R. & Alcock, J. 1983. The Evolution o[lnsect
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Mating Systems. Cambridge, Mass.: Harvard University Press. Ueda, T. 1979. Plasticity and the reproductive behaviour in a dragonfly, Sympetrum parvulum Barteneff, with reference to the social relationship of males and the density of territories. Res. Popul. Ecol., 21, 135-152. Whitham, T. G. 1979. Territorial behaviour of Pemphigus gall aphids. Nature, Lond., 279, 324-325. Wickman, P.-O. 1985. The influence of temperature on the territorial and mate locating behaviour of the small
heath butterfly, Coenonympha pamphilus (L.) (Lepidoptera: Satyridae). Behav. Ecol. Sociobiol., 16, 233 238. Wickman, P.-O. & Wiklund,C. 1983. Territorial defence and its seasonal decline in the speckled wood butterfly (Pararge aegeria). Anim. Behav., 31, 1206-1216.
(Received 2 May 1984; revised 5 September 1984; MS. number." 2535)