Mating systems of Coenonympha butterflies in relation to longevity

Anita. Behav., 1992, 44, 141-148

Mating systems of Coenonymphabutterflies in relation to longevity PER-OLOF WICKMAN Department of Zoology, Stockholm University, S-106 91 Stockholm, Sweden

(Received 4 April 1991; initial acceptance 31 May 1991; final acceptance 29 January 1992; MS. number: 3748)

Abstract. The different mating systems of the two monandrous butterfly species Coenonympha tullia and

C.pamphilus can be explained by their different longevities. In this study, virgin females of the shorter-lived C. tullia seemed to be in greater urgency to mate. They were less discriminating towards males and courtships more often resulted in copulation than in C. pamphilus. Virgin C. tullia females also approached passing males to solicit courtship. In contrast, a previous study showed that virgin C. pamphilus females remain quiescent when males pass and are rarely detected before reaching aggregations with territorial perching males. Here they encourage detection with a lengthy conspicuous circling flight. These differences combined result in C. tullia females being mated more rapidly and closer to eclosion sites. The differences in female behaviour appear to be sufficient to explain why C.pamphilus males aggregate in leks to compete for dominance, while C. tullia males engage in scramble-competition searching. According to mating system theory the matesearching behaviour of a species is the result of whether population density, operational sex ratios and the spatial and temporal distributions of receptive females permit males to monopolize females and females to choose among males (Emlen & Oring 1977; Borgia 1979; Thornhill & Alcock 1983; Waage 1984; Odendaal et al. 1985; Bradbury & Davies 1987). In monandrous insects competition will be intense among males to be the first to encounter virgin females. Behaviour that leads to more rapid detection and effective monopolization of females after eclosion will be favoured by selection (Alcock et al. 1978; Ridley 1989). Examples may be found in species where males fight over territories at eclosion areas and over pupae ready to hatch (e.g. Lin 1963; Gilbert 1975; Elgar & Pierce 1988). In many insects, however, males do not localize female eclosion sites and other means to find females have evolved. Basically, males may then either engage in lek polygyny (Emlen & Oring 1977; Thornhill & Alcock 1983; Bradbury 1985) and wait at conventional mating sites (Parker 1978) or engage in scramble-competition searching for already eclosed females (Thornhill & Alcock 1983). A conventional encounter site is commonly a purely symbolic territory, often a perch site by a prominent landmark, which is defended against other males. Typically, encounter sites are dispersed throughout the habitat where eclosion occurs. Waiting and rambling may constitute 0003-3472/92/070141 + 08 $03.00/0

alternative tactics in a population, where rambling males search for females that have not yet reached a conventional encounter site (Baker 1983; Thornhill & Alcock 1983; Wickman 1985b; Courtney & Anderson 1986). This suggest that any factor that increases the detection rate of virgin females and their tendency to accept non-territorial males will select against conventional encounter sites and vice versa. Since both lek polygyny and scramblecompetition polygyny are often associated with similar scattered spatial distributions of receptive females, explanations have focused on the temporal distribution of females. Thornhill & Alcock (1983, page 232) proposed that a crucial difference between the species in each category may be the longevity of females: 'For a long-lived female . . . there may be less urgency in acquiring sperm upon reaching adulthood. If so, females can perhaps afford to be more selective in picking a mate, favouring those that had demonstrated dominance in their interactions with other males because dominant males offer superior genes.' This leads to the little examined prediction that rambling should be more common in short-lived species, specifically because females of these species will show little discrimination between males and therefore will mate more promptly closer to eclosion sites than would be the case in a species with lek polygyny. In this paper I test this hypothesis and examine its consequences by comparing two butterfly

9 1992 The Association for the Study of Animal Behaviour 141

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142

species of the genus Coenonympha (Satyrinae), C. tullia and C. pamphilus. The average life expectancy has been reported to be twice as long in C. pamphilus (7-0 days; Wickman 1985b) as in C. tullia (3-3 days; Turner 1963). Both species are essentially monandrous and have similarly sized ejaculates (Wickman 1986, unpublished data; Sv/ird & Wiklund 1989). They have similar and cryptic appearances both as pupae and adults and are locally abundant in open grasslands, where enclosing females are diffusely distributed (Wickman 1986, unpublished data, this study). According to the prediction above, (1) receptive females of C. tullia should behave differently from those of C. pamphilus, which should result in more prompt mating in C. tullia, and (2) this behavioural difference should select for scramble-competition rambling in C. tullia males; consequently (3) the male mating system of C. tullia should be more of the scramble-competition searching type than is the case in C. pamphilus. The mating system of C. pamphilus, which fulfills the criteria for a lek polygyny, has been described in an earlier series of papers (Wickman 1985a, b, 1986). Males of this species compete for territories situated beside bushes or trees or ramble over wide areas in search of females (Wickman 1985a). Virgin females search out male territories and solicit courtship there by a conspicuous circling flight eliciting approach by the perched resident males (Wickman 1986). In some butterfly species males elicit approach by females (e.g. Rutowski 1980; Wiklund 1982; Krebs 1988) but this has never been observed in C. pamphilus. Females remain quiescent when males pass (Wickman 1986). Here I present additional results on the mateacquisition behaviour of C. tullia and C. pamphilus. These results, together with the already published observations on C. pamphilus, are used to test the theoretical predictions by comparing the two species. METHODS

C. tullia

I studied C. tullia from 17 July to 13 August 1987, 3 July to 22 July 1988 and 29 June to 12 July 1990 on 131and, south Sweden (56~ 16~ where it inhabits wet meadows with groups of trees and occasional bushes. Time-budget studies were made during sunny weather between 0900 and 1730 hours (Swedish

Daylight Saving Time). Since weather affects flight activity, I regularly measured ambient temperature in the shade 1 m above the ground and wind direction and wind speed at the same height in an open part of the habitat. There was no sign of individuals being disturbed by being followed. I did not mark followed males because this would probably have affected their dispersal rates. Hence, because the originally followed male could not be identified after interactions with other males, each observation period, about 10m in long, could include several individuals. This, however, should not affect average estimates of flight activity. Dispersal rate was calculated from direct flight distance for the longest period of observation of one individual uninterrupted by interactions during each 10-min session. It is necessary to compare virgin and mated females to determine what behaviour of females can be attributed to mate acquisition. Mateacquisition behaviour should be expected among virgins, while mated females should avoid detection. In 1988, I conducted time-budget studies of 26 laboratory reared females (originating from eggs laid by 10 females from 131and) which I released when they were 2-11 days old in the field and followed them until they mated ( N = 24) or were lost (N=2). After mating, as many surviving and healthy females ( N = 14) as possible were released a second time (within 1-3 days), and followed at least until passed by a male within 0-3 m. Two of these females mated again and were then released a third time the next day. If not otherwise stated, all comparisons between virgin and mated females do not include the two sessions when these two females repeated mating. Before and between releases females were kept in a refrigerator (about + 5~ and fed 20% sucrose solution daily. To facilitate comparisons, I made all releases in an open field 15 m from a wood margin (one was used on 3 and 5 July and another one on 8 July onwards). Here females had been observed to lay eggs, and, considering the sluggish nature of the larvae and that there is shallow water between tufts most times of the year, these locations should represent potential eclosion sites. Females were transported in transparent containers in a cooler. I released them individually by permitting them to heat up in their container and start activity voluntarily. For each female direct flight distance (used for calculating dispersal rate) at the time of mating or loss was noted. The orientation of their heads

Wickman: Coenonympha butterfly mating systems when perching (pointing upwards, horizontally or downward) and their position in the herb layer (with or without any vegetation above them) were noted. To enhance detection of passing males, virgin females were expected to perch more often head up and without any vegetation above. The reaction of females to passing males within 1 m of a female was noted. The closest distance to the female was estimated to the nearest 0.1 m by eye. When calculating periods between detections of females, repeated detections in sequence by one individual male have been counted as one. The weather during the releases of the two groups of females was not sufficiently different to account for any of the differences found. I studied the behaviour of wild females by following six egg-laying females found in the field in 1987 and 1988. These were included to control for artefacts in the behaviour of reared females. However, flight activity and oviposition rate of these wild females and released mated females were similar and not significantly different, suggesting no abnormalities in the behaviour of released females. On four dates in 1990 I censused the natural distribution of wild males, females and eggs by transecting an approximately rectangular area of 100 10 x 10 m squares with no elevational differences. Squares of this size were used because this approximately equals the size of aggregations of C. pamphilus males (Wickman 1985a, b). One side of this area was bounded by trees. Squares within 5 m of these trees ( N = 33) are referred to as wood margin and the rest (5-65 m away) as open field. Grasses and sedges, which are used as host plants (Ackery 1988), dominated all squares, and only four squares contained fewer than 50 Potentilla erecta inflorescences, the most used nectar source. Hence, this area was essentially homogeneous except for the distribution of trees. To determine the distribution of eggs, 10 females were followed until lost or for a maximum of 2 h and another 10 until they laid their first egg. C. pamphilus The already published results on C. pamphilus (Wickman 1985a, b, 1986) were necessary to supplement data on dispersal rate and time to mating of females. These data were available from the same data base used in Wickman (1986). Hence, all results on C. pamphilus females presented in this study are derived from the same study on the same set of females.

143

General

Time of day is given as Swedish Daylight Saving Time (mean solar time+67 min). Statistics are calculated by MINITAB statistical software. Means are given +standard error and all tests are two-tailed. Chi-squared values for d f = l are calculated with Yates' correction. RESULTS

ON INDIVIDUAL

SPECIES

C. tullia

As predicted, scramble-competition searching was the rule among males ofC. tullia. A single male never remained in one area for long, and any area where males were seen was soon emptied of them. They travelled 9_+0.7m/min. Males were randomly distributed over the 100 10-m 2 squares (Poisson distribution: Z42= 1.13, N = 179, P>0.75) and in relation to the wood margin (Z~=2.31, P>0.0. Males seemed to maximize time in flight. Excluding nectar-feeding bouts, their flight duration was 48 + 4 s ( N = 174) and perching duration 39 + 3 s ( N = 174); that is, they spent 55% of their nonfeeding time in flight. The flight activity was highest at midday, but even at air temperatures below 20~ males rarely spent less than 40% of their time in flight. There was no evidence of territorial defence. Male encounters were brief (1-6 ___0-1 s, range 1-8 s, N = 114) with males flying offin different directions afterwards. Compared with males, both virgin and mated females dispersed slowly (Table I). Their lower dispersal rates were explained by their lower flight activities with very short flights (Table I). As expected, virgin females more often perched with their heads pointing upwards than did mated females (l 12 out of 130 observations versus 50 out of 75; ~ = 9 . 7 5 , P<0.01). Virgin females also perched higher in the herb layer, i.e. more often without any vegetation above them (94 out of 180 observations versus 6 out of 60; Z~=31.29, P<0.001). Females and eggs were randomly distributed over the 100 10-m 2 squares (females: Z~=0-361, N = 6 6 , P>0.75; eggs: Z~=3.38, N=50, P>0-1). However, the distribution relative to the wood margin gave a different picture. Females avoided the wood margin in preference to the open field (Z~ = 9.40, P < 0.01). This was also evident from the

Animal Behaviour, 44, 1

144

Table I. Flight activity and detection rates of C. pamphilus and C. tullia females before and after mating

C. pamphilus

Approach males Flight duration (s) Perching duration (s) Flight activity (%) Time to detection (min) Time to mating (min) % Courtships resulting in mating Dispersal rate (m/min) Time to mating dispersal rate (m)

x

C. tullia

Virgin

Mated

Virgin

Mated

No* 7.3 • 0.4* 240 • 32* 2-9* 90* 154 59% (N= 29) 1.2 • 0.4 185

No* 4.4 _ 0.2" 228 4- 40 1.9* 181 * --0.9 + 0.3 --

Yes 4.7 • 0.3 178 _ 20 2.6* 31 35 89% ( N = 27) 0.7 _+0.2 24

No 3.4 • 0.2 300 • 42 1.1 239 --0.2 _+0.06 --

*From Wickman (1986).

[

Observedfemale

45•

/' / 2

6

i Flying and ] followed by male

Perche

whenmale passes

Perchedand is courted

I EscapesI ~

~l

}

0

J Staysperched Copulation II EscopeSor not detected

Figure 1. The possible sequences of behavioural events after a male has passed within 1 m of a female. Bold figures denote the number of events involving a virgin female and italic figures events involving a mated female. distribution of eggs laid by followed females (Z2~= 6.64, P < 0 . 0 1 ) . T h e possible sequences of events after a male passed within 1 m o f a female are s h o w n in Fig. 1. Virgin females almost always t o o k off (91%) a n d a p p r o a c h e d males passing within 1 m (0.4 + 0.04 m, N = 34). The four observations o f virgin females t h a t did n o t a p p r o a c h flying males were produced by two individuals, b o t h o f which later did respond to passing males with which they mated.

A p p r o a c h flights usually resulted in courtship o n the ground. Occasionally, however, males did n o t detect the female at all (they c o n t i n u e d flying witho u t any reaction, N = 11), or they followed the female b u t did n o t find her landing place ( N = 5). The distance between the male a n d the female at take-off seemed to influence this outcome. Virgin females t h a t were courted o n the g r o u n d were passed by males at a closer distance (0.3 ___0.05 m) t h a n those virgin females t h a t were not detected or

Wickman: Coenonympha butterfly mating systems escaped males (0.6+0.08m; Mann-Whitney Utest, P = 0-037). On four of the five occasions when males did not find the female as she landed, the male remained on the spot flying in circles until he passed the female again. All these four females took off a second time and were courted on the ground, whereupon mating ensued. These results, together with the observation that most courtships on the ground resulted in copulation, suggest that females accept most males that are able to find them. Excluding the two females that mated a second time, both of which flew towards passing males, all other mated females remained perched when males passed within 1 m (Fig. 1). The closest distance at which males passed mated females (0.3_+0.02 m) was shorter than that at which they passed virgin females (Mann-Whitney U-test, P = 0.0054), probably because virgin females took off before males came closer. Despite the close distance at which males passed perching mated females, they were rarely detected. Only on 8 % of the occasions when mated females were passed by males were they detected and followed by passing males, compared to 67% for the virgin females (Fig. 1; ~]=28.15, P<0-001). The behavioural switch at mating resulted in virgin females being detected more rapidly than mated ones (Table I; Mann-Whitney U-test, P=0.013). This was not explained by them using microhabitats where males were more active than in those used by mated females. Virgin females on average were passed by 3.2 males and mated females by 3.3 males per h. On average it took 35 min before a virgin female mated.

C. pamphilus The additional data on dispersal rates and time to mating of C. pamphilus females are compiled in Table I together with other key behavioural data on females of both species.

GENERAL RESULTS DISCUSSION

AND

The mating behaviour of C. tullia and C. pamphilus differs in accordance with predictions derived from their different life spans (Table I). Virgin females of the shorter-lived C. tullia are less selective about which male to mate with, which leads to more rapid mating compared with C. pamphilus. By taking off

145

and approaching flying males they are detected by most males passing close enough to be seen and caught up with. Reliable detection and take-off are aided by perching high in the vegetation with the head directed upwards. In contrast, virgin C. pamphilus females are indifferent to passing males, and, instead, solicit approach from males perching in territories by adopting a lengthy conspicuous circling flight upon arrival. Quiescent females are rarely found by males of either species. Consequently, virgin C. tullia females are detected more rapidly. Virgin C. tullia females are also less discriminating when detected, and on average are courted by fewer males before copulation (;(~=5.08, P<0.025, Table I). Owing to the combined effect of this difference in detection rate and readiness to mate with a courting male, it takes 4.4 times longer before virgin C.pamphilus females mate than for virgin C. tullia females (Mann-Whitney U-test, P = 0.0009). Like virgin C. pamphilus females, virgin C. tullia females tend to fly towards wood margins (unpublished data), with the difference that C. tullia males do not aggregate there. The reason for this behaviour of virgin C. tullia females is not clear, but may occur because these locations will on average be more protected against wind which should result in a more predictable male flight activity, promoting prompt mating. For the same reason, the lower density of ovipositing females at wood margins might be explained by more frequent male harassment there (Odendaal et al. 1989). In agreement with the second and third predictions, the behaviour of virgin females explains why males of C. tullia engage in scramble-competition searching while those of C. pamphilus aggregate to compete for dominance in leks. Although eclosing females of both species show similar scattered distributions (as judged from the distribution of eggs) and, compared with rambling males, travel slowly towards prominent vegetation, those of C. tullia on average travel a shorter distance before mating (time to mating • dispersal rate in Table I). This will reward males searching for females closer to eclosion sites and those that can maintain high flight activity to search large areas to attract perching receptive females. On the other hand, if C. tullia females had shown a lower tendency to mate with the first encountered male, males at wood margins would have higher mating success. By a runaway process similar to that suggested by Parker (1978), an encounter-site convention, like

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Animal Behaviour, 44, 1

that in C. pamphilus, would result. Approach behaviour might then be lost secondarily to increase the probability of being mated to a dominant male. For C. pamphilus, staying on a territory and waiting for flying females produces higher mating success than searching outside (Wickman 1985b). Males on territories consequently show low flight activity (,~= 13%) and compete for ownership with lengthy interactions (.~= 12 s; Wickman 1985a) compared with C. tullia. These results have implications for theories advanced to explain the evolution of leks. Because the differences in mating systems between these two species are difficult to explain without initial reference to female behaviour, the 'hotshot' theory of Beehler & Foster (1988; see also Arak 1983) seems not to be applicable in this case. They reasoned that the significance of female preferences and female mate choice has been overstated, and the starting point of their model is a dispersed male setting with aggressive males holding display courts. This system is not the evolutionary alternative to a lek here, which instead is scramblecompetition searching. Differences in virgin female behaviour of these two species directly affect the size of their home ranges. With larger and more overlapping home ranges more females can potentially be found at a single location and lekking with territorial behaviour is more likely to result. This agrees better with the competing 'hotspot' and 'female preference' theories (Bradbury 1981; Bradbury & Gibson 1983). Territorial and mating behaviour of animals may be affected by population density (e.g. Baker 1972; Sillrn-Tullberg 1981; Arak 1983; Hoffmann & Cacoyianni 1989). There is no evidence that this accounted for the differences in mating systems observed here. The similar time intervals between detections of mated females of both species (Table I) suggest similar activity levels of males in both studies. Fundamental to the line of argument given here is the difference in lifetimes of the two species. Independent support for this difference, and for C. tullia having less time available, comes from data from South Sweden on how rapidly body reserves are transformed into eggs. This rate should be inversely related to longevity (cf. Boggs 1986), particularly since both species start with similar relative amounts of resources and feed mainly on nectar (unpublished data). Females of C. tullia oviposit 4.2% of their body weight per h compared

to 1-7% for its congener (recalculated from field oviposition rates given in Wickman 1986; this study; and weights of adults and eggs from Wiklund et al. 1987). This agreement between the degree of haste of females before and after mating also supports the idea that a change in longevity and hence time available for reproduction (e.g. because of predation or host-plant changes) has caused the change in mate selection rather than the reverse. Males of C. tullia seem to be obligate ramblers in Britain as well (Dennis & Shreeve 1988), i.e. where its life expectancy was determined. Theoretically, on the assumption that female choice carries a time cost, it is well established that life expectancy will affect how choosy females can afford to be (e.g. Janetos 1980; Hubbel & Johnson 1987; Real 1990). Accordingly, for these species, what is the fitness cost of postponing insemination 2 h to choose a better mate (the difference in time to mating, Table I)? These animals depend on sunshine for activity. Hence, the time available to a female each day that can be traded between mate acquisition and oviposition is defined by the proportion of time that is sunny. Assuming an average daytime cloudiness of 65% in July (data for South Sweden from the Swedish Meteorological and Hydrological Institute's reports for 1984-1990) and at most 8 h available for activity per day, one can calculate that, on average, the active life of C. tullia is 9 h and that of C. pamphilus 20 h. This would suggest that increased quality of males has to compensate for a 10% ( = 2 h / 2 0 h) reduction of fecundity in C. pamphilus to maintain the species' difference in female behaviour. Using the same rationale, in C. tullia this compensation would have to exceed a 20% ( = 2 h/9 h) reduction in fecundity if it were to behave like C. pamphilus. Hence, it is interesting to note that a female of C. tullia spends only 7% of its active life searching for mates, proportionately less than the 13% of C. pamphilus. Taken together, this suggests that mate choice has to compensate for substantial fitness costs in these animals to be maintained by selection, and that 2 h constitute significant fractions of the lifetimes of these, and probably many other, ectotherm animals.

ACKNOWLEDGMENTS I thank Carol Boggs, Enrique Garcia-Barros, Roger Dennis, Srren Nylin, Risa Rosenberg,

Wickman: C o e n o n y m p h a butterfly mating systems R o n Rutowski, Birgitta Sillrn-Tullberg, Christer W i k l u n d a n d two a n o n y m o u s referees for comm e n t i n g o n different versions o f this paper. This w o r k was supported by grants to the a u t h o r f r o m the Swedish N a t u r a l Science Research Council.

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