Post-copulatory mate guarding by males of the demselfly Hetaerina vulnerata Selys (Odonata: Calopterygidae)

Anim. Behav., 1982, 30, 99-107

POST-COPULATORY MATE GUARDING BY MALES OF THE DAMSELFLY HETAERINA VULNERATA SELYS (ODONATA: CALOPTERYGIDAE) BY JOHN ALCOCK Department of Zoology, Arizona State University, Tempe, A Z 85287 Abstract. Males of the calopterygid damselfly Hetaerina vulnerata remain with their mates after copulating with them. The species exhibits two unusual features of post-copulatory mate guarding. First, a male will often leave his territory to accompany a female in tandem on a search for oviposition sites elsewhere. Second, a male will perch near his ovipositing female even though she completely submerges when egg-laying and cannot be captured and mated by another male while she is underwater. These activities carry two potential costs: (1) a male may miss other receptive females while guarding one mate and (2) he may lose his territory to an interloper while he is absent. These costs were low, however, because territorial males secured only one mating per 3.6 days on average. Moreover, 23 times out of 26, territorial males reclaimed their plots quickly after being away for 30-60 rain. The gain from postcopulatory guarding came from being present to recapture a female should she fly up from the water after rejecting an oviposition site. There was a 40 ~o chance that a female would leave one site to search for another during an oviposition bout. If the male were not present, his mate would be captured and mated by another individual (no female ever selected an oviposition site without being carried to it by a male). Her new partner would fertilize the remaining eggs in the female's clutch (if sperm precedence occurs in this species). The total number of eggs fertilized by a male will be affected by how well he prevents any one mate from copulating again before she lays her entire clutch and the total number of receptive females he captures. The variation in the degree of mate guarding by male odonates seems to be the evolutionary outcome of differences in fitness gains derived from these two competing activities in different ecological settings. Among the odonates there is a great diversity in the extent to which males guard their mates after copulating with them (Sakagami et al. 1974; Waage 1979b; Corbet 1980). Males may remain in tandem with their mates while they oviposit (contact guarding) or they may perch or hover by them, repelling competitor males from the area near egg-laying mates (non-contact guarding). A third major alternative is to release the female after mating with her and subsequently to ignore her while she oviposits. Guarding, when it occurs, is thought to represent an attempt by the male to prevent his mate from accepting another male; if the female copulates again she may use her last partner's sperm, resulting in a reduction in egg fertilizations by her original mate (Parker 1970). Waage (1979a,b) has shown that this hypothesis is correct for at least one damselfly, Calopteryx maeulata. In this species ovipositing females may mate more than once during the time they are laying eggs. The males use their penis to remove all or almost all of any sperm stored in the female before they transfer their own gametes and as a result, there is a strong 'last-male advantage'. When territorial males of this species guard their mates, they

prevent the loss of the female to a rival for some time, and therefore do fertilize more of their partner's eggs than they would if they failed to exhibit post-copulatory mate-guarding. Many questions about the diversity of guarding tactics, however, are not yet resolved, and additional data on the ecological correlates of guarding in damselflies may lead to a better understanding of why males vary in their postcopulatory behaviour. To this end, I describe the behaviour of the calopterygid damselfly, Hetaerina vulnerata Selys, a previously unstudied member of a genus whose other North American representatives have been the subject of several papers (Johnson 1961, 1962; Bick & Sulzbach 1966). Males of Hetaerina spp. appear toexhibit two unusual traits. First, unlike most other territorial odonates, they sometimes abandon the areas they have been defending in order to accompany a mate to an oviposition site outside their territory. Second, they will guard the ovipositing female whether she is inside or outside the territory, despite the fact that egglaying females submerge completely underwater where they cannot possibly be captured and mated by another male (Johnson 1961). This 99

ANIMAL

100

BEHAVIOUR,

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paper attempts to explain why males of H. vulnerata have evolved these special aspects of mate guarding.

Between 4 and 11 samples (15-min each) were collected for each hour between 0800 and 1700 hours for use in estimating activity budgets.

Methods

Results In the early morning both males and females perched on bare branch tips and pine-needle clusters in trees well above the stream (2-10 m high) and made repeated forays out from their perches to pursue very small insect prey. On every day, the first male flew to his territory between 0800 and 0900 hours and perched, generally on an exposed rock in the middle of the stream or on a rock at the edge of the stream. Between 1000 and 1200 hours receptive females often left their streamside perches to fly out over the water where they were captured and mated by waiting males. The density of territorial males was greatest at this time (Fig. 1). Although some males left their perches in the early afternoon, m a n y individuals remained on territory until 1600 to 1700 hours. Activity declined precipitously, however, if it became heavily overcast at any time during the day. In the late afternoon on sunny days, males and females once again could be seen in relatively large numbers perched in trees by the stream hawking for insect prey. There was a strong tendency for individuals to remain in the same general area for a period of days. The mean interval between marking and

The damselflies were observed from 1 to 21 August 1980 at Cave Creek a few hundred metres above Herb Martyr D a m at an elevation of about 1800 m in the Chirichahua Mountains of southeastern Arizona. The stream, which passes through an open woodland of oaks, pines, and junipers, is a permanent one, although the flow fluctuates considerably depending upon recent rainfall amounts in the watershed. During the period of the study and prior to it, little rain had fallen and as a result the stream was much reduced. It was rarely more than a metre wide or more than 30 cm deep. A 75 m transect, with as many as 16 territorial males present, was established along the stream on 1 August. Thereafter as many males and females as possible that were perched on or near the stream transect were either captured in a net or by hand (as the animals were remarkably difficult to disturb). Each insect received a distinctive colour combination on its wings, abdomen, or thorax using fast-drying enamel paints or liquid eraser. On each of the 17 days suitable for damselfly activity, I remained at the stream for all of the morning (beginning at 0800 or 0900 hours) and much of the afternoon if it had not become overcast and cool. A total of 82 h of observation were logged. During each day's observation period I made at least one trip per hour up and down the transect recording the location of all the males seen perched b y the water and their sexual activity, if any. In addition, tandem pairs often travelled considerable distances along the stream and I walked after them (using binoculars at times to follow their movements). As I pursued one tandem pair I recorded reproductive activity by any other damselflies along the transect. Because the study site was often covered wholly or in part several times in the intervals between the hourly censuses, and because mated pairs remained together for many minutes, I am confident that I detected most, if not all, of the reproductive events that occurred along the transect during the 82 h of observation. During times when I was not monitoring a mating, I selected one or two territorial males in my field of vision and recorded every flight that the males made from their streamside perches and the stimulus, if any, that provoked the flight.

'LS' a.

I

16-

I 1.4 1.2 ~-

12"

1.0

i

:O.8

8"

.O.6 0.4 ~

g

0800

1000

1200

1400

1600

Fig. 1. The relation between male density and the frequency of copulations over the daily breeding period. Perched males were most numerous along the stream when receptive females were most likely to arrive. The line graph shows the rise and fall of the number of males censused at the start of each hour (each point is the average of from 4 to 15 censuses). The bar graph shows the average total number of matings recorded in each hour of the day along the transect during the study period (each bar is based on from 4 to 15 h of observation, mean = 7.2 h).

ALCOCK: MALE DAMSELFLY POST-COPULATORY MATE GUARDING last sighting for the 53 males marked on the study site between 1 and l 1 August was 8.9 days (st) = 6.2) and 10.7 days (SD = 5.5) for the 43 individuals that were seen at least once after marking. Of the 26 females marked prior to 11 August, 21 were seen again over an average interval of 7.7 days (SD = 4.9; maximum = 18 days). Although some males and females were spotted upstream within 200 m o f the study site, most were seen solely within the transect area, often on a daily basis. This was especially true of territorial males. For the 10 resident males marked on 1 and 2 August, the average interval between capture and last sighting was 15.6 days (and several males were still living at the termination of the study). Johnson (1962) found that adults of 11. americana did not wander widely. He estimated the mean longevity o f adults to be 14.3 days. Male Territorial Behaviour Males defended territories that covered a 2- to 3-m segment of the stream and contained suitable oviposition substrate. Only rapidly flowing portions of the stream with riffles were occupied by territorial males. Individuals made occasional 'spontaneous' flights within their territories and, in addition, promptly pursued any conspecific mate that entered their holdings. Often the other male passed directly out of a male's territory, in which case the defender returned to his perch within a matter of seconds. Sometimes the intruder attempted to remain within the territory; a 'circle flight' then ensued. In this interaction the two males chased each other in a tight circle for a variable period of time before one male broke away in a weaving flight that took h i l T I o u t o f t h e contested area. Commonly, in repelling an invader, the territorial resident flew into the territory of a neighbour. This generally led to a brief circle flight between the two males with the intruder quickly returning to his own perch site. The frequency o f aggressive interactions was highest during the middle of the day, the time when male density was greatest and when receptive females were most abundant (Fig. 2). The average duration of 32 circle flights whose length was recorded during the 15-rain time budget sample periods was 20.6 s (sD -----30.3); 16 of the 32 interactions lasted less than I0 s. Thus males were able to defend their territories relatively economically, as most disputes were resolved quickly in favour of the resident.

101

Turnover in territorial possession was infrequent. At the nine territories along the transect that were occupied on every suitable day during the study, the average total number of owners per territory was 3.2 (SD -- 1.1). Thus the mean time per turnover at these presumably desirable territories was 6.5 days; one male held his site for the entire 21-day period. Turnovers in the ownership of territories were probably caused by mortality, voluntary abandonment, and forcible takeover. Although I did not directly observe a territory owner killed while on his perch, male damsellties were taken by a jumping spider and an asilid fly. The lizard, Sceloporus jarrovi, was a common streamside predator that m a y have captured s o m e damselflies although all three observed attacks by the lizard were unsuccessful. At least five turnovers in territory ownership occurred when males abandoned one territory 'voluntarily' (no fighting was seen at the site prior to the departure of the resident) and were Iater seen at another location. Ten forcible takeovers occurred during the study. In every case, prior to the takeover, an intruder male persisted in entering the territory repeatedly, each time engaging the resident in a circle flight, many of which were unusually prolonged. These interactions occurred sporadically over a period of hours or sometimes over the course of two days before the original resident left and the intruder perched in the area and began to repel other individuals. Three of these takeovers were initiated when the territory owner

-1,s

10 O ~ 9 D. o

zr

0800

1000

1200

1400

1600

Time

Fig. 2. The relation between mating frequency (open bars) and the frequency of aggressive interactions at a territory (black bars). The data for aggressiveencounters is based on a sample of from 4 to 11 periods of 15 rain each. Malemale interactions are most frequent in the period from 0900 to 1300 hours when females are most abundant along the stream.

102

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temporarily abandoned his site to accompany a female to an oviposition site outside his territory (see below). Typically the displaced male returned from time to time on the day or two following his defeat but was always chased away promptly. Only 1 of 10 defeated males was able to acquire a new territory and this was in a previously unoccupied (low-quality?) site. But after two days as the owner of this site, he was chased away by another 1/lale and shortly thereafter disappeared.

Satellite Males Not all males defended territories at the stream. At least 23 of the 53 males marked from 1 to 11 August practised a 'satellite' role at some point in their lives. These males attempted to slip onto a perch in another male's territory, often while the resident was occupied in territory defence or mate acqu,.'sition. Once perched, these individuals did not react to approaching males. Because they remained motionless, the satellite males often were not detected by the resident male for some time, but if the territory owner did perceive a satellite, he flew at the intruder persistently until the other male left. Frequently, a satellite would be seen in several different territories in the course of a single morning. Unlike other nonterritorial males (which perched above the stream and fed), satellites attempted to acquire mates through the passive occupation of a perch in another male's territory. Although 11 individuals were observed only as satellites (for from 1 to 13 days), other males practised both roles. Four individuals made the transition from satellite to territory owner and 8 of the territorial males that were displaced from their location were later seen as satellites in territories other than their original pl0t. One ousted territory owner remained in the transect area as a satellite male for 13 days following his defeat. Another defeated male succeeded in finding and briefly holding a new territory after a three-day interval as a satellite. Territorial males secured far more copulations than satellites. Of the 36 copulations seen along the transect during the study, 32 involved marked territory owners, 2 were by unmarked males whose status was not known but which may have been young satellites, and 2 were by known satellite males. The role of satellite therefore appears to be a relatively unproductive option that is adopted by young males not yet ready to compete for territory ownership and by older damselflies after they have lost a territory.

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Reproductive Behaviour Males waited at the stream in order to capture receptive females that were attracted to regions of the stream with fast-flowing water. After grasping an incoming female in mid-air, the pair alighted in tandem on a rock in the stream near the point of capture. After a period of inactivity, the male pulled the female forward so that her head was close to his thorax. Simultaneously he flicked open his wings several times, exposing the bright crimson patch at the base of the fore and hindwings. After the male completed what was presumably sperm translocation, the female coiled her abdomen under her body and placed her genitalia over the male's penis. There then followed a period of rhythmic abdominal movements of the sort described by Waage (1979a) for the calopterygid damselfly Calopteryx maculata. These movements are associated in C. maculata with the removal of any sperm donated by another male that happens to be present in the female's bursa copulatrix and spermatheca. The duration of copulation in H. vulnerata from the moment of genital linkage to separation averaged 229 s (so = 88.5, N = 27). After completion of sperm transfer, the male retained his tandem grip on the female and soon the pair flew out over the water. Of the 32 observed copulations by territory owners, 30 took place within the male's territory; data were recorded on the initial oviposition site for 27 of these 30 cases. Although in every instance the male first flew with the female around his territory, in only 18 of 27 cases did the pair alight on a rock or tree limb in the territory. Soon after landing the female separated from the male to submerge. Once she was completely underwater the female used the tip of her abdomen to probe waterlogged plant material of all sorts, including pine needles, tree limbs and twigs, presumably laying her eggs in the process. In the other 9 of the 27 cases, the male abandoned his territory to accompany the female in a trip along the stream in search of an oviposition site elsewhere. When a male left his territory, he and his female were sometimes attacked by owners of the territories through which they passed. These assaults regularly prevented males from releasing their mates at potential oviposition sites and lengthened the period of travel in tandem. (The attacks, however, never resulted in visible injury to a male or his mate.)But if a pair were not molested at a suitable location and if the female stopped or slowed her wing beat, the male alighted quickly and released the

ALCOCK: MALE DAMSELFLY POST-COPULATORY MATE GUARDING

103

side her mate's territory on one day's egg-laying session (e.g. one female was underwater for 50, 1, 9, 4, and 60 rain at five sites). When a female visited more than one site, she generally spent a relatively long time at her last choice (Table I). Five marked females were seen ovipositing on 2 or 3 days during the study period with a mean interval of 4.9 days (N ---- 8) between oviposition bouts. Three of the 8 records involve females that laid eggs on consecutive days; in two of the cases the total period o f oviposition over both days is known to be approximately 110 and 145 rain. The maximum total time spent underwater on one day was 156 min. These limited data suggest that females usually have a sufficiently large clutch of eggs to require 90-150 min oviposition time. I f one site does not provide enough oviposition substrate, a female will emerge to search for another location. Often the clutch may be laid on a single day, but sometimes a 2-day period is necessary, after which an interval of 4-6 days passes before the female has a new mature clutch of eggs to lay.

female at once, permitting her to slip down into the water to explore the plant matter there. I f a female oviposited within a male's territory, he generally remained close to the spot where she had been released but would also repel intruders in the typical manner. After each chase, the male returned to perch near the release point for some time and was almost always in position to recapture the female should she emerge and fly (see below). In contrast, territorial males that accompanied their mates outside their territories behaved in a most inconspicuous manner while perched at a release point. They ignored passing males and made no effort to defend the area about the perch unless detected and driven up by a resident male in whose territory they had released the female. When this happened a spirited series of chases and circle flights often resulted which eventually ended with the departure of the intruder. But because guarding males remained motionless they were infrequently assaulted by the resident male if they had been able to avoid him in locating an oviposition site. Female Oviposition Behaviour

The Duration of M a t e Territory

Guarding Outside the

The duration of the first underwater oviposition attempt by a female varied from 1 to 106 min (Table I). There was a 40 % chance that the female would oviposit o r inspect a spot for less than 15 rain on her first oviposition attempt, after which she would re-emerge and fly up from the water. I was present on 10 occasions when this happened within the territory of a female's mate. The guarding male recaptured the female but did not copulate again; instead the tandem pair promptly resumed the search for another oviposition site. Twice the male escorted the female to a new location within his territory b u t on 8 occasions the pair left the area and found a new site elsewhere. A female might submerge and re-emerge at as many as five different locations within and out-

As a result of the often episodic oviposition pattern of females on any one day and the reluctance of some individuals to lay any or all of a clutch of eggs within a mate's territory, resident males often had to travel away from their territories in order to guard their females (17 of the 27 matings were followed sooner or later by extra-territorial travel). When a male left his territory, the time he spent away was a function of how long it took him to find a suitable site acceptable to his mate plus the time he devoted to perching by his submerged partner near the release point (Table II). Typically males were gone for 30-60 rain with much of that time spent perched. No male perched by his mate for more than 60 rain outside his territory. In some instances the guarding

Table I. Duration of Time Spent Underwater by Females at Any One Potential Oviposition Site

Time spent submerged on oviposition attempt (in minutes) 1-15 16-30 31-45 45-60 61+ Total First oviposition attempt of the day Last oviposition attempt of the day,

if female submerges in more than one location

11

3

3

2

8

27

0

1

1

3

5

10

ANIMAL

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male was driven away, but in others the male left his perch site 'voluntarily' to return to his territory. Table II presents data for all those cases in which territorial males were seen outside their territories with a female (for 17 records I had seen the male transfer sperm to his partner but for another 15 I did not see the pair until after they had mated and were in tandem, searching for an oviposition site). F o r 26 of these 32 records, I was able to inspect the temporarily abandoned territory in time to determine if it was occupied during the resident's absence. On 16 occasions it was. When the original resident returned to find his territory held by another male, he was able to eject the interloper in 14 of the 16 cases. The time required to reclaim the territory was only 155 s on the average (N = 14), although the circle flights were more intense and lasted longer than the typical clash between a casual intruder and an established resident (which, as noted before, lasted an average o f 21 s). But twice the original resident was defeated by the newcomer that day after a long series of encounters and in a third case, the intruder was repelled initially but persisted in his attacks and the next day took the territory from its previous owner. Thus by leaving the territory unprotected while travelling with a female, a resident male ran a 12 % chance of being displaced by a male that had occupied his territory during his absence. Discussion W h y D o Females Oviposit Outside Their M a t e ' s Territory ?

The typical mating system of territorial odonates is resource defence potygyny (Emlen Table II. Duration of Time a Territorial Male Remained Away from His Territory while Travelling with a Mate to Other Oviposition Sites

Total minutes of an extra-territorial foray 1-15 N

4

16--30 31-45 46-60 13

5

6

61-75 4

Minutes spent during a foray perched near a submerged, ovipositing female N*

1-15

16-30

2

9

31-45 46-60 4

5

61-75 0

*The number of records of perching time is not the same as the number of records of extra-territorial forays because in some cases I was able to determine how long a male was absent from his territory but was not able to observe the male over the entire period.

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& Oring 1977) in which males defend oviposition sites and thereby gain access to the receptive females that c o m e to the area to lay their eggs. In some respects, the mating behaviour of H. vulnerata appears to fit this classic pattern as males do defend stretches of stream (always in areas with fast-moving water) that are preferentially visited by females about to oviposit. Moreover, territory owners always copulate with females in their territories and then usually release their mates in the area under their control to permit them to submerge and oviposit. However, many females do not spend their entire period of oviposition in their mate's territory but instead move in tandem elsewhere on the stream to oviposit, for a time, in some other male's territory. An egg-laden female cannot assess the quality of the oviposition substrate in a male's territory with complete accuracy while perched on vegetation overlooking the stream. A female might enter the water only to find inadequate oviposition substrate in her mate's territory, thus favouring a move to another location. Travel elsewhere might also benefit the female by enabling her to disperse her eggs more widely, thereby reducing the risk that unpredictable fluctuations in stream flow would result in the destruction of an entire clutch. Because of these factors, the relationship between female preferences for mating sites and their preferences for oviposition areas is ambiguous (Fig. 3). Although females do tend to submerge first within their mate's territory, there was no significant correlation between the number of copulations and the number of lengthy ovipositions (greater than 15 min) that took place at a territory (rs = 0.11, P > 0.05, N = 16). However, this negative result is largely a product of the data from two adjacent territories that contained popular oviposition sites but were in an area with few streamside shrubs and trees. Receptive females may not have found perches near these sites and so were unlikely to fly out over the stream, there to be captured and mated. I f we exclude these two data points, the correlation rises to 0.61 (P < 0.001, N = 14). Thus although for the moment we must reject the hypothesis that territories that attracted receptive females were also superior oviposition sites, the possibility remains that this relationship is generally true but was obscured by unusual conditions affecting a few territories.

ALCOCK: MALE D A M S E L F L Y POST-COPULATORY MATE G U A R D I N G

Why Do Males Leave Their Territories To Accompany Their Mates ? The most unusual feature of the reproductive behaviour of H. vulnerata was the readiness of territorial males to leave their territories to accompany females in tandem to an additional oviposition site or sites elsewhere. There were two major costs to males of this option. First, during the time the male was away from his territory, he was unable to capture and copulate with any females that might arrive there during his absence. While escorting a female off his territory, no male ever responded sexually to another female. However, the probability that a receptive female would appear in his territory in the 30-75 min of his absence was extremely low. There were a total of 53 matings by territory owners during the study period (32 observed copulations and 21 additional cases in which a resident male was seen already in tandem carrying a female to an oviposition site). The average number of territorial-days per copulation was 3.6 for the owners of the 16 sites along the stream. The maximum number of matings for a male during one day was 2. These results suggest that the hourly probability of securing a female was so low that a guarding male lost few opportunities to copulate with additional females while guarding a recent mate. A second potential cost, the permanent loss of a territory to an interim resident male, may be the most serious disadvantage of leaving a terri:::,.,

o

I< 6"

9

"0

8 tr

4

-

0 A

8

2 - AA

9

5 A

Z

[

I

I

2

4

6

Number Of Ovipositions Recorded At A

Territory

Fig. 3. Territories at which many matings occur are not necessarily those at which females are most likely to oviposit for periods in excess of 15 min (but see text).

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tory site unguarded even for a short time. By permitting a newcomer to establish himself, an absentee owner probably contributed to his downfall in some cases. When a male left his territory, he incurred an approximately 12% risk that he would not be able to reclaim his territory when he returned (or that he would lose it soon thereafter). Once ousted, a male's reproductive potential fell nearly to zero because his chance of acquiring another territory was close to nil and the satellite option was so unprofitable. Males gained by leaving a territory to escort a female to another oviposition site because this enabled them to perch by the submerged female and recapture her should she reject that site. Females frequently spent only a short time at any given oviposition area, particularly at the start of a period of egg-laying. I f they emerged and were recaptured by another male they copulated promptly with the new individual and then resumed ovipositing under his control (N = 3). Sperm precedence is thought to be characteristic of the Odonata (Parker 1970; Waage 1979b). A male that fails to recapture a female which leaves one oviposition area with more eggs to lay probably does not fertilize those remaining eggs. Thus males probably leave their territories in order to fertilize more eggs of one mate.

A Comparative Analysis of Mate-Guarding in Odonates As noted before, there are three major kinds of post-copulatory activities performed by male dragonflies and damselflies: (1) tandem (contact) guarding; (2) non-contact guarding; and (3) no guarding. Tandem guarding probably provides the greatest certainty that a female will lay eggs fertilized by the guarding male. The non-contact guarder runs some risk of a takeover if other males are present but he still potentially can improve his egg-fertilization chances with the female he defends. Males that do not guard a female must invest all their energies into efforts to secure additional mates and so may more than compensate for any loss of egg fertilizations to other males by copulating with additional individuals. Evolutionary logic generates the hypothesis that male damselflies should attempt to maximize the number of eggs they fertilize. This leads to the prediction that the intensity of mate guarding will be (1) positively correlated with the probability that an unguarded female will mate promptly with a sperm-displacing competitor male and (2) negatively correlated with the likeli-

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hood of missing additional mates during the period of guarding. The guarding behaviour of males o f H. vulnerata makes biological sense in this context. Receptive females are scarce; when males secure a mate they escort her in tandem when they are above water and the risk of takeover is relatively high. They perch by their mates during the time they are underwater when the risk of takeover is slight. Although in many species of odonates the absence of mate guarding is related to underwater oviposition (Sakagami et al. 1974; Waage 1979b), in H. vulnerata and H. americana (Bick & Sulzbach 1966) females may oviposit in a series o f locations, emerging from the water in one place to be taken toanother. Each time they emerge they are receptive and will mate with a new male if captured by him. Thus by guarding a mate, a male reduces the risk that she will mate again with the probable loss of the opportunity to fertilize the remainder of her clutch. The same relation between intermittent underwater oviposition and male mate-guarding by perching or hovering above the submerged female occurs in Agrion lindeni (Heymer 1973) and Enallagma civile (Bick & Bick 1963), two coenagrionid damsel flies. In contrast, males of another calopterygid damselfly, Calopteryx maculata, only perch by their mates while these individuals are in their territories and do not accompany females to new sites (Waage 1973, 1979b; Alcock 1979). Extraterritorial mate guarding may be ineffective for males o f C. maculata because their females oviposit above water, where they are easily detected and captured by the owner o f the area. Moreover, the probability of acquiring additional mates by remaining in a territory unattached to any one female is high in C. maculata relative to H. vulnerata. Males in one population studied by Waage (1979b) averaged about 4.7 matings per day versus 0.3 for males o f H . vulnerata in the present study. Finally, males of C. maculata that leave their territories undefended temporarily (something that happens rarely) run a high risk o f losing it to an interloper (Waage, personal communication). Thus the adaptive value of extra-territorial guarding of one mate (and her eggs) at the risk o f failing to secure new partners m the short- and long-run appears low in C. maculata relative to H. vulnerata. Finally, in at least one odonate, there is intraspecific variation in the intensity with which males guard a recent partner. U r d a (1979) found that non-territorial males of Sympetrum parvu-

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1

lum escort their ovipositing females in tandem

but only when the density of males is high in their environment (presumably at these times the risk of losing a mate to a more dominant male is relatively high). Territorial males never employ contact guarding but instead fly near their recent mates. These males should encounter additional receptive females at higher frequency than the wandering males which are excluded from prime oviposition habitat. By virtue of practising noncontact guarding, the dominant male is free to capture and mate with new arrivals, if they become available. (However, territory owners may also be better able to defend their territories if they are not in tandem.) The findings of U r d a in conjunction with the divergence in behaviour of the calopterygid damselflies are at least consistent with the argument that the intensity of mate guarding is the outcome of conflicting selection pressures, with selection for egg fertilization gain from one mate at odds with selection for maximizing of the rate of encounters with receptive females. Acknowledgments This paper has benefited from the thoughtful and detailed reviews of J. K. Waage and R. Rutowski. Through the cooperation of L. Knutson, the identification of the damselfly was confirmed by O. S. Flint. REFERENCES Alcock, J. 1979. Multiple mating in Calopteryx maculata (Odonata: Calopterygidae) and the advantage of non-contact guarding by males. J. nat. Hist., 13, 439--446. Bick, G. H. & Bick, J. C. 1963. Behavior and population structure of the damselfly, Enallagma civile (Hagen). SWest. Nat., 8, 57-84. Bick, G. H. & Sulzback, D. 1966.Reproductive behaviour of the damselfly, Hetaerina americana (Fabricius) (Odonata: Calopterygidae). Anita. Behav., 14, 156--158. Corbet, P. S. 1980. Biology of Odonata. Ann. Rev. Ent., 25, 189--217. Emlen, S. T. & Oring, L. W. 1977. Ecology, sexual selection and the evolution of mating systems. Science, N.Y., 197, 215-223. Heymer, A. 1973. Ethologische Freilandbeobachtungen an der Kleinlibelle dgrion lindeni Selys, 1840. Rev. Comport. Anita., 7, 183-189. Johnson, C. 1961. Breeding behaviour and oviposition in Hetaerina americana (Fabricius) and H. titia (Drury). Can. Ent., 93, 260-266. Johnson, C. 1962. A description of territorial behavior and a qualitative study of its function in males of Hetaerina americana (Fabricius) (Odonata: Agriidae). Can. Ent., 94, 178-190. Parker, G. A. 1970. Sperm competition and its evolutionary consequences in the insects. Biol. Rev., 45, 525-567.

ALCOCK: MALE DAMSELFLY POST-COPULATORY MATE G U A R D I N G Sakagami, S. F., Ubukata, H., Iga, N. & Toda, M.J. 1974. Observations on the behavior of some Odonata in the Bonin Islands, with considerations on the evolution of reproductive behavior in Libellulidae. J. Fac. ScL Hokkaido Univ. Ser. 6, 19, 722-757. U6da, T. 1979. Plasticity of the reproductive behaviour in a dragonfly, Sympetrum parvulum Barteneff, with reference to the social relationship of males and the density of territories. Res. Pop. Ecol., 21, 135-152. Waage, J. K. 1973. Reproductive behaviour and its relation to territory in Calopteryx maculata (Beauvois)

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(Odonata: Calopterygidae). Behaviour, 47, 240256. Waage, J. K. 1979a. Dual function of the damselfly penis: Sperm removal and transfer. Science, N.Y., 203, 916-918. Waage, J. K. t979b. Adaptive significance of postcopulatory guarding of mates and nonmates by male Calopteryx rnaculata (Odonata). Behav. Ecol. Sociobiol., 6, 147-154.

(Received 21 January 1981; revised 18 May 198l; MS. number: A2598)