Variation in copulation duration in Mnais pruinosa pruinosa Selys (Odonata: Calopterygidae)

Summary Males of the damselfly Mnais pruinosa pruinosa were observed to use three different tactics to secure mates. The mean duration of copulation differed between the three observed tatics and resulted in varying degrees of sperm removal and insemination. It is shown that the last male to mate had almost 100% sperm precedence immediately after copulation regardless of the duration of copulation and therefore the quantity of sperm removed. In situations where less than 100% of rivals' sperm was removed the sperm from different males mixed within the female sperm storage organs over a period of about 6 days: sperm mixing produced variation in last male sperm precedence. The significance of sperm mixing in M. p. pruinosa is discussed in the context of the observed matesecuring tactics and the frequent female habit (37% of observations) of ovipositing without remating during an oviposition bout.     

Variation in copulation duration and the resultant degree of sperm removal inOrthetrum cancellatum (L.) (Libellulidae: Odonata)

Summary Orthetrum cancellatum showed two distinct copulation durations at a study site in the south of France. These different durations are correlated with different degrees of sperm displacement from the female sperm stores; long copulations (894±142 s) resulting in almost 100% sperm removal, and short copulations (21.0±13.5 s) resulting in 10–15% removal. The difference in copulation duration is also related to the site of copulation and to the relative age of the copulating males. At oviposition sites males who gained copulations were relatively young and copulated for long periods. The difference in the duration of copulation and the degree of sperm removal is discussed with reference to the female habit of ovipositing before remating during oviposition episodes, and the possibility of differences in the rate at which males encounter receptive females at the two sites.     

Choice and utilization of oviposition sites by female Calopteryx maculata (Odonata: Calopterygidae)

Summary Females of the damselfly Calopteryx maculata (de Beauvois) initially choose the larger of a pair of adjacent oviposition sites, about 70% of the time (Table 1), or whichever of two equal sized sites had other ovipositing females on it (about 88% of the time-Table 2). These criteria for initial choice between a pair of sites also interact. Incoming females generally (57 to 74% of the time-Table 3) joined others on the small site rather than ovipositing alone at the adjacent, bigger site. When pairs of large and small sites were replicated across eight locations, there were nonsignificant trends towards greater utilization (eggs laid) of the larger of a pair of oviposition sites within locations (Table 4). The lack of agreement between initial choice and utilization shows that other factors besides size are important in the choice and use of oviposition sites. These include disturbance by males, the presence of other females and choice criteria that can only be assessed during oviposition. When all sites at the eight locations were equal in size, there was considerable day to day and location to location variation in eggs laid (Fig. 1). Viewed over periods of several days, some sites are obviously less attractive than others in terms of cumulative numbers of eggs laid at them. When the amount of vegetation was varied among locations, those with the bigger oviposition sites were used more often, somtimes significantly so, but there were also significant reversals (small sites used more often) (Table 5, Fig. 1). Thus, there is no simple effect of size on the utilization of oviposition sites by Calopteryx maculata females, despite a clear tendency for females to make initial choices based on this criterion. The considerable among and within location variation in number of eggs laid may reflect additional choice criteria or the interaction of size, the presence of other females, disturbance, and location.     

Copulation duration and sperm competition in white-faced dragonflies (Leucorrhinia intacta; Odonata: Libellulidae)

Summary In many odonates, females mate with more than one male while laying a single clutch of eggs. We studied paternity of eggs laid by remated females of Leucorrhinia intacta, a small libellulid dragonfly, at a pond near Syracuse, NY, USA. The probability of a female remating is a function of male density on the pond. The length of copulations differs considerably among males active on the study pond at the same time. Much of this variation was correlated with differences in mating tactics of the males; copulations by males that stayed on their territories during copulation were shorter than those by other males (Fig. 2). Eggs collected from females mated to irradiated, sterile males and to free-living, fertile males indicated that the average paternity expectation was higher for long than for short copulations, and that the variance in paternity expectation was lower for long than for short copulations. Some possible causes of the high variation in paternity at low copulation durations and possible reasons for differences in copulation duration between male mating tactics are discussed.     

Operational sex ratio versus gender density as determinants of copulation duration in the walnut fly,Rhagoletis juglandis (Diptera: Tephritidae)

In laboratory and field studies of the walnut fly, Rhagoletis juglandis Cresson (Diptera: Tephritidae), we assessed the effect of operational sex ratio on copulation duration and partitioned the sex ratio effect into component effects due to male density and female density. In our first laboratory experiment, results were clearly consistent with theoretical expectation: increases in male density were associated with significant increases in copulation duration while increases in female density were associated with significant decreases in copulation duration. These component effects yielded a striking composite effect of operational sex ratio (OSR) on copulation duration in which male-biased ratios were associated with low frequencies of short copulations and female-biased ratios were associated with high frequencies of short copulations. Consistent with a priori expectations concerning costs of territorial behavior, the effect of male density on copulation duration was stronger than that of female density. There was no significant interaction between the effects of gender density on copulation duration: each gender density contributed additively to the composite OSR effect on copulation duration. In contrast to the effect of OSR, overall density had little effect. Field data corroborated these findings fully and showed additionally that OSR in the vicinity of fruit tended in nature to be male-biased. In a second laboratory experiment, we measured copulation duration for individuals exposed alternately to male-biased and female-biased ratios. Individual flies consistently copulated for longer in male-biased environments than in female-biased ones. We propose that this plasticity permits individuals to track changes in local sex ratio over space and time and respond appropriately. Received: 15 November 1995/Accepted after revision: 27 April 1996     

The effects of operational sex ratio and food deprivation on copulation duration in the water strider (Gerris remigis Say)

Summary A North American water strider, Gerris remigis (Hemiptera) copulates for prolonged periods of time, apparently beyond the time necessary for insemination (Rubenstein 1984; Wilcox 1984; Clark 1987), I tested predictions from two different hypotheses of the adaptive significance of this behavior. Manipulations of the operational sex ratio in artificial streams revealed that water striders copulate significantly longer when the sex ratio is male-biased. This result is consistent with the hypothesis that prolonged copulation functions as a type of contact mate guarding, which reduces sperm competition by preventing the female from remating prior to oviposition. The finding is also consistent with the hypothesis that copulation is prolonged to enhance female foraging efficiency. In a second experiment, sex ratio and total population density were held constant, and the period of food deprivation of females was manipulated. Contrary to the predictions of the female foraging hypothesis, starved females did not copulate longer than fed females. Of the two hypotheses considered, only the copulatory guarding hypothesis explains both results. This does not mean, however, that there is no selective benefit from the enhanced foraging efficiency resulting from prolonged copulation. Nor does it exclude the possibility that this benefit has been necessary for the evolution of prolonged copulation in water striders.     

Cloacal erection promotes vent apposition during forced copulation in the New Zealand stitchbird (hihi): implications for copulation efficiency in other species

Cloacal protuberances (CP) in male birds result from spermatic engorgement of storage tubules around the cloaca during the breeding season. We examined seasonal changes in the volume and orientation of the CP in the New Zealand stitchbird Notiomystis cincta. The male stitchbird has one of the largest recorded CPs for any species (max = 1,570 mm³), with CP volume increasing by almost 400% between the non-breeding and breeding seasons. While sperm competition has been positively correlated with the magnitude of CP storage in other species, no evidence previously existed for the CP improving copulation efficiency. By measuring the relative orientation of the CP throughout the year, we show that not only does the CP increase in size as males become sexually active, it also changes its orientation by approximately 60°. This results in it shifting from facing posteriorly to becoming almost perpendicular to the abdomen. This cloacal erection improves the apposition of the male and female cloacal openings during face-to-face forced copulation in this species. This provides the first reported evidence supporting the copulation efficiency hypothesis of the avian CP. While the magnitude of seasonal changes in female cloacal volume was similar to males, female cloacal orientation remained virtually unchanged across seasons. This difference between the sexes is likely to reflect differing selection pressures for optimizing sperm transfer. In females, a posterior-facing cloaca is ideal for both waste evacuation and sperm reception, whereas, for the male, a posterior-facing cloaca is well suited for waste evacuation, but possibly hinders sperm delivery. Changes in male cloacal orientation from the non-breeding to the breeding season are a likely reflection of conflict in this dual function. Evidence of changes in CP orientation in another passerine species suggests this phenomenon is widespread and also important for understanding related fields such as sperm competition, forced copulation and constraints on the evolution of the avian intromittent organ.     

Sperm transfer,displacement and precedence in Ischnura graellsii (Odonata : Coenagrionidae)

Summary Copulation in Ischnura graellsii may be divided into three stages, according to the movements and position of the male's abdomen. We measured sperm volumes in males and females interrupted at different phases of copulation in laboratory-reared and field specimens. The results showed that males remove sperm from the female during stage I, and do not transfer sperm until stage Il of the copulation. In the field females interrupted during stage I of copulation had less sperm than postcopula females, and the volume of sperm in laboratory females mated once or twice was similar. These results suggest that males can remove most of the sperm during stage I of copulation. Preparations of in-copula specimens showed the horns of the penis (used to remove sperm) inside the bursa copulatoox and the spermatheca. Therefore males can remove sperm from both organs, in contrast to the other Ischnura species so far studied, where males can empty only the bursa. The length of these horns is positively correlated with male body length, and there are significant differences in length between the left and right horns of individual males. This suggests great variability in the male's ability to remove sperm. On the other hand, ejaculate volume is positively related to male and female size, and negatively to male age. Males are likely to be able to detect the presence of sperm in females: if the effect of population density and time of start of copulation are taken into account, copulations are longer with mated than with virgin females. Using genetic markers, sperm precedence was studied by rearing the female offspring of 6 females mated with two males of different genotype. In 5 out of 6 crosses, the second male fertilized all the eggs laid by the female in her first clutch. On average, the following clutches were progressively more fertilized by the first male, but there were striking differences between crosses. These differences are probably due to the variability in the amount of sperm transferred and/or removed. Offprint requests to: A. Cordero     

Occurrence of extra-pair copulation in the tree swallow (Tachycineta bicolor)

Summary A new method to mark sperm transfer events between birds, using microspheres inserted into males' cloacae, was employed to assess the frequency of extra-pair copulation (EPC) in a population of tree swallows (Tachycineta bicolor) in Ontario, Canada, during the summer of 1988. We inserted 25 males with microspheres; spheres from 8 (32%) of these males were found in extra-pair females, from which we infer that males pursue a mixed reproductive strategy of monogamy coupled with seeking EPCs. The cloacae of 10 of 41 (24.4%) females were found to contain microspheres from non-mates. EPCs occur more frequently between neighboring birds than between non-neighbors. Only two within-pair copulations were detected with this method, suggesting that it underestimates the occurrence of all copulations, extra-pair or within-pair. Copulation watches revealed that within-pair copulations occur very frequently. We propose that frequent pair copulations are used by males to ensure their paternity in their mate's offspring. Offprint requests to: R.J. Robertson     

Dominions and site-fixed aggressive behavior in breeding male Leucorrhinia intacta (Odonata: Libellulidae)

Summary We report aggressive spacing behavior in male dragonflies, Leucorrhinia intacta, that is characterized by variations in the probability of chasing conspecific male intruders within a defined area around a male's perch. The chase probability depends on the total intruder pressure and the behavior and distance of the intruder from the perched male (Fig. 2). This nonexclusive, site-fixed area has been called a dominion.We also examined the distribution of intruders among the various behavior-distance categories. Chase rates (per 15 min) were correlated mostly with number of intruders that hovered (rather than flew) close to the territorial male. Finally, we examined the impact of the changing chase probabilities on the variation in aggressive interactions as a function of intruder pressure. We conclude that, to some extent, territorial males stabilized defense costs across a variety of intruder pressures by maintaining dominions.     

Lifetime mating success in a natural population of the damselfly,Enallagma hageni (Walsh) (Odonata: Coenagrionidae)

Summary Variance in lifetime mating success was measured for individuals of a population of Enallagma hageni, a non-territorial damselfly in northern Michigan. E. hageni is an explosive breeder with scramble competition for mates. Highly skewed operational sex ratios resulted in intense male-male competition which took the form of interference with tandem pairs. 41% of the males failed to mate in their lifetime as opposed to only 3.6% mating failure in females. The effect on mating success of size, age, longevity, and time spent at the breeding site were investigated. Intermediate sized males obtained the most matings, and male lifetime mating success was highly correlated with longevity.     

Aggregation during oviposition and predation risk in Sympetrum vulgatum L. (Odonata: Libellulidae)

Summary Tandem pairs of the libellulid dragonfly Sympetrum vulgatum always start oviposition with contact guarding directly over the surface of shallow water, where they are exposed to green frogs (Rana esculenta). Tandems which approached locations with other pairs already present started oviposition nearby regardless of whether or not predators were actually present. With predators present attack rates during arrival were lower on tandem pairs in groups than on pairs that oviposited alone. During oviposition the attack rate on groups was similar to that on solitary pairs, but predation risk to individual tandem pairs was lower due to dilution effects. Predation risk during tandem oviposition was similar for both sexes, but females had a higher risk of falling prey to frogs during post-tandem oviposition than males. If tandems were attacked by frogs, females left the site after tandem oviposition despite the male hovering above her, and the frequency of non-contact guarded post-tandem ovipositions was reduced.     

Surgical examination of male genital function of calopterygid damselflies (Odonata)

Male genitalia show rapid and divergent evolution. It is rarely determined whether variation in male genital morphology influences male reproductive success. Male damselflies possess a unique aedeagus with a re-curved head and spiny lateral processes, and most females have two sperm storage organs, a spherical bursa copulatrix and a tubular spermatheca. Previous studies have indicated that the re-curved head may remove bursal sperm, whereas the lateral processes remove spermathecal sperm. However, we need more direct evidence of these functions. We compared sperm number in female sperm storage organs by interrupting copulation to examine sperm removal by the male. In Calopteryx cornelia, males removed almost all bursal sperm but only partially removed spermathecal sperm. In contrast, females of Mnais pruinosa store sperm primarily in the bursa, and males removed only bursal sperm. To examine the functions of male spiny lateral processes, we compared mating behaviour between control and experimental males from which we removed (cut) the lateral processes. In C. cornelia, cutting of the lateral processes resulted in a decreased number of abdominal movements during copulation and no removal of spermathecal sperm. The amount of bursal sperm removed during copulation also decreased in experimental males compared to the unmanipulated males. However, in M. pruinosa, the experimental removal of male lateral processes did not decrease the abdominal movements and little affected the removal of bursal sperm. Inter-specific differences between C. cornelia and M. pruinosa may be caused by variation in the strategies of female sperm storage.     

Copulatory plug displacement and prolonged copulation in the Iberian rock lizard (Lacerta monticola)

Male Iberian rock lizards (Lacerta monticola) produce copulatory plugs that adhere firmly inside the female cloaca and occlude both oviducts. These plugs do not prevent rival male insemination, as they neither reduce female attractiveness or receptivity to rival males nor do they function as chastity belts. Prior to copulation, males bite various regions of the female body, including the cloacal region. A previous plug in the female cloaca is expelled only after rival male intromission. We hypothesized that: (1) such male pre-copulatory behaviours function to loosen plug adherence to the female cloaca, thereby facilitating intromission, and that (2) the hemipenis plays a role in displacing a previous plug prior to the delivery of a new plug. Neither of these hypotheses was supported. Instead, our results indicate that rival males can intromit the hemipenis past a previous plug in the female cloaca and deliver their own plug underneath it. Consequently, previous plugs are pushed away from the oviductal openings and even dislodged from the female cloaca. Copulation duration was determined both by the time used by males to deliver a plug and by the fact that males prolonged copulation beyond plug delivery. There seemed to be sexual conflict over prolonged copulation, which was resolved by the male/female head-length ratio. The adaptive value of Iberian rock lizard copulatory plugs and prolonged copulation in Iberian rock lizards is discussed in the context of sperm competition.Communicated by S. Downes     

Prolonged copulation: A male ‘postcopulatory’ strategy in a promiscuous species,Lygaeus equestris (Heteroptera: Lygaeidae)

Summary Copulation in Lygaeus equestris L. (Heteroptera, Lygaeidae) is known to last 0.5–24 h. Variations in copula duration of field-collected insects were studied in the laboratory, and different hypotheses concerning the significance of prolonged copulations were tested.Through reciprocal matings with normal and sterile (irradiated) males, sperm displacement was estimated at about 90%. A male could thus increase his fitness by preventing subsequent matings of an inseminated female.Copulations with virgin insects, observed over 15 h, were classified in two categories: short (0.5–8.0 h) and long (> 15 h) duration (Fig. 1). No difference in the number of fertilized eggs was found between long and short copulations, and the insemination rate was highest during the first hour of a couplation (Fig. 2). Long-lasting couplations did not give rise to increased sperm displacement (Table 2). These results indicate that there is no difference in the amount of sperm transferred during short and long copulations and that no insemination takes place during the latter part of a prolonged copulation.Longer lasting copulations occurred when the sex ratio was male-biased than when it was female-biased (Fig. 1). The frequency of prolonged copulations was higher when the female was gravid than when she contained no eggs (virgin) (Figs. 3 and 4). Support is thus given to the hypothesis that prolonged copulation is a male postinsemination strategy to prevent subsequent matings of a female.Females subjected to male competition over a longer period, laid fewer eggs and died earlier than females that were mated but subsequently isolated from males (Fig. 5). Egg batches from females living with males were larger than batches from mated, isolated females (Table 3). This is probably due to a combination of many matings with short intermissions and prolonged copulations, both of which postpone oviposition.Comparisons between copulations of males with either gravid or virgin females during these experiments, led to the conclusion that short copulations with virgin females result from a male decision to terminate copulation after insemination is completed, whereas copula duration with gravid females is more likely to depend on a combination of male and female behavior.     

Underwater oviposition in a damselfly (Odonata: Coenagrionidae) favors male vigilance,and multiple mating by females

Summary Female Enallagma hageni oviposit underwater where they are inaccessible to males. I demonstrate that males guard submerged females rather than perch sites, and are behaviorally distinct from lone males at the water. In contrast to lone males, which always attempt to copulate with females presented to them, guarding males exhibit a conditional latency to remating which corresponds closely to the time required by females to oviposit a complete clutch of eggs. By ovipositing underwater, females decrease the risk that their eggs become exposed. Risks associated with submerged oviposition favor both mate guarding, and multiple, within-clutch matings by females. Both guarding mates and lone males rescue females that float on the water surface as the result of improper resurfacing. Such behavior reduces the mortality risk to females from 0.06 to 0.02 per oviposition bout. By remating between bouts, females benefit from the additional vigilance of lone males, who rescue floating females 1.4 times as often as original mates. A second consequence of multiple mating is an increase in the selective advantage of vigilance by mates. Because receptive females become scarce by early afternoon, whereas male density remains high, a male has little (3%) chance of encountering a second receptive female that day. However, he incurs a 42% risk of losing fertilizations if he abandons a mate. For male E. hageni mate guarding functions in the context of both natural and sexual selection. It insures that a mate lives to lay a complete egg clutch in addition to protecting a male's sperm investment.     

Direct and indirect estimates of sperm precedence and displacement in the dragonfly Sympetrum danae (Odonata: Libellulidae)

Summary The non-territorial dragonfly Sympetrum danae shows a high degree of post-copulatory mate-guarding, which suggests precedence of the last male's sperm. Irradiated male techniques revealed that the last male that mates with a female fertilizes an average of 95% (100% in 28% of the cases) of the clutch laid immediately after copulation, irrespective of any previous matings. Sperm volume estimates in both sexes and sperm opacity changes in females at 7 stages of copulation and oviposition indicated that males remove 41–87% of previously deposited sperm from the female's storage organs during the first 5 min of the copulation. Ejaculation takes place during the remaining 10–15 min. We maintain that indirect estimates of precedence in libellulids, based on sperm volume changes, always understimate reality because of the supplementing effect of a first-in, last out mechanism. Because males are skilled at achieving sperm precedence, they are forced to be good guards as well, since a risk of take-overs exists. Females are believed to benefit from contact guarding because it results in a lowered risk of male harassment and predation as well as a lower energy expenditure during oviposition.     

Timing of copulation in the molting and reproductive cycles in a grapsid crab,Gaetice depressus (Crustacea: Brachyura)

From the seasonal changes in the amount of semen in the sperm ducts of males and in the fullness of spermatheca of females, the copulation season of Gaetice depressus in central Japan is considered to approximately coincide with the oviposition season, from March to October. The sperm ducts of all the large males examined contained semen, the amount of which did not vary obviously with stages of the molt cycle or with seasons. The genital apertures of females were normally covered with calcified immobile opercula in this species. The opercula decalcified after molting and again shortly before oviposition, and retained mobility for 1 to 3 d. Shortly after molting, soft-shelled females with mobile opercula did not have well-developed ovaries nor did they copulate with males even if they had a chance. In contrast, all of the hard-shelled females with mobile opercula had well-developed ovaries, and laid eggs within 2 d after the decalcification of opercula regardless of the occurrence of copulation. Laboratory experiments showed that the females normally copulated with males before oviposition. Crabs examined in this study were collected from Shirahama, Wakayama Prefecture, Japan between March 1988 and March 1989.     

Sperm competition in the damselfly Enallagma hageni Walsh (Odonata: Coenagrionidae): benefits of multiple mating to males and females

Summary Sperm competition was investigated in the non-territorial damselfly, Enallagma hageni. Using irradiated (sterile) male techniques, the last male to mate was found to fertilize up to 95% of the eggs of the first clutch laid after mating. Dissection of females collected before, during, and after copula showed that a male removes a maximum of 87% of the sperm by volume of a previous mate. These data verify an earlier estimate of lifetime reproductive success in this species which was based on mating success, and suggest that indirect dissection methods offer minimum estimates of sperm precedence. Male E. hageni have ample opportunity to benefit from sperm precedence, since at least 10% of the receptive females encountered had already mated once that day, but still contained complete or partial clutches of eggs. Female E. hageni benefit directly from high sperm precedence because it allows them to exchange matings for guarding service by males during oviposition bouts under water.