Mating behavior of Labidocera aestiva (Copepoda: Calanoida)

The calanoid copepod Labidocera aestiva Wheeler exhibits a ritualized mating behavior. Sensory hairs and spines and integumental pores on the male and female are believed to play a regulatory role in the mating encounter. Scanning electron microscopy (SEM) revealed approximately 20 unusual pore structures (pit-pores) on the right ventrolateral surface of the female's abdominal segment, the area where the spermatophore coupling device is attached. Prior to spermatophore transfer, the male vigorously strokes this area with the modified endopod of his left fifth leg to prepare the pit-pore region for attachment of a new spermatophore. Transmission electron microscopy (TEM) indicated that the cells underlying each pit-pore may have a secretory function. We hypothesize that the pit-pores secrete a substance which dissolves the cement binding the coupling device to the abdomen and aids the female to remove a discharged spermatophore from her urosome.Contribution No. 116, Harbor Branch Foundation, Inc.     

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.     

The effect of postcopulatory male behaviour on ejaculate distribution within the female sperm storage organs of the fly,Dryomyza anilis (Diptera : Dryomyzidae)

Summary After sperm transfer, male Dryomyza anilis increase their fertilization success by tapping the female external genitalia with their claspers. In order to clarify the mechanism, we examined the effect of tapping movements on the distribution and fate of the male ejaculate within the female's sperm storage organs. The structure of the female internal genitalia is described and the volume of sperm found within the female is estimated. Experiments show that males place their sperm near the exit of the female's bursa copulatrix: most of the last male's sperm are expelled before oviposition and only 10–30% remain in the female. The results suggest that the mechanism by which male D. anilis gain last male sperm precedence is complex, and two possibilities are suggested. Offprint requests to: M. Otronen     

Paternity assurance by “helpful” males: adaptations to sperm competition in burying beetles

Summary Male burying beetles invest parentally by participating in the burial of a carcass and in provisioning and guarding the larvae that come to the carcass. Since most of the females arriving at a carcass have stored fertile sperm within their spermathecae, sperm transferred by such helpful males must compete with other males' ejaculates for the fertilization of the female's eggs. We showed that these males are able to achieve a high level of paternity (mean=92%). The mechanism they employ is a repeat-mating tactic, i.e., the female is mated very frequently shortly before and during oviposition. Repeated matings are essential for a high reliability of paternity, since single copulations result in the fertilization of only a very small proportion of the female's eggs.     

Why do male Callosobruchus maculatus beetles inseminate so many sperm?

Male Callosobruchus maculatus F. (Coleoptera: Bruchidae) inseminate more sperm than females can effectively store in their spermathecae. This study examines the adaptive significance of excess sperm transfer by measuring components of male and female reproductive success in response to manipulating the number of sperm inseminated. The number of sperm transferred during copulation was reduced from 56,000 ±4,462 to 8,700±1,194 by sequentially mating males to virgin females. Reducing the number of sperm inseminated by the first male to mate had no effect on the extent of sperm precedence, but reducing the number of sperm inseminated by the second male resulted in a significant reduction in the extent of sperm precedence. When large numbers of sperm are inseminated the remating refractory period of females is increased. These results indicate that males transferring large numbers of sperm during copulation have a two-fold advantage at fertilization; they are more effective at preempting previously stored sperm and they are likely to father more offspring by delaying the time of female remating. The transfer of excess sperm does not appear to serve as nonpromiscuous male mating effort; the number of eggs laid, their fertility and the subsequent survival of zygotes were unaffected by manipulating the number of sperm inseminated. The underlying mechanisms of sperm precedence were also examined. Simple models of sperm displacement failed to accurately predict the patterns of sperm precedence observed in this species. However, the results do not provide conclusive evidence against the models but rather serve to highlight our limited understanding of the movement of sperm within the female's reproductive tract.     

Female-enhanced male competition determines the first mate and principal sire in the spider Linyphia litigiosa (Linyphiidae)

Summary Two to five days before sexual maturation, female sierra dome spiders (Linyphia litigiosa: Linyphiidae) undergo a transformation in their behavior toward males that visit their webs. During this latter part of their penultimate instar, females change from consistently positioning themselves far away from males to actively maintaining close proximity, reactions I call avoidant and associative behavior, respectively. Consistent associative behavior ceases after the female's first mating and thus is limited to soon-to-mature penultimate females. When a mate-seeking male fords an associative female, he attempts to guard her until she matures; this is often a multi-day affair. In contrast, males guard immature avoidant and mature mated females for only a single day. This dichotomy in male guarding times can be understood by the fact that associative behavior signals that the female will soon develop peak reproductive value. Upon completion of their final molt, 98% of females immediately mate with the current guarding male. Secondary suitors are not as likely to achieve mating. Moreover, first mates father 1.8 times more offspring, on average, than secondary mates. Whenever they meet on any female's web, males fight until one of the contestants withdraws. Fights typically are intensive, occasionally deadly, and often result in usurpation of the web by the newly arriving male. Larger males win more fights, but other qualities (e.g., vigor and persistence) appear to be important when contestants differ by less than 10–20% in body weight. Prolonged (i.e., multi-day) guarding of associative females enhances the intrasexual selection process by ensuring that every male that arrives at the web finds it already guarded. Therefore every male that finds the web becomes a participant in a series of male-male conflicts and web usurpations which span the period between the resident female's commencement of associative behavior and her sexual maturation. Since unforced male departures from the webs of associative females are rare, victors are retained on the web until they themselves lose a fight. This facilitates a steady increase in the fighting ability of sequential guards throughout the associative period, up until female maturation and mating. On my study site, first mates represented the final winners in a combative sorting process based on a minimum average of 2 fights; they were heavier and larger than secondary mates and randomly sampled males. The combination of (1) associative behavior by nearly mature females, (2) high mating propensity of newly mature females, and (3) first male sperm priority, constitutes a system whereby females enhance male-male competition and boost the expected fighting prowess of the principal sire of their progeny. Since males appear to make no material contribution toward progeny, the female's behavior probably functions to improve the genetic constitution of the offspring. In addition, the timing of associative behavior may limit prolonged guarding by food-stealing males to a period (1) encompassing the female's pre-molt fast and (2) before the heavy yolking of eggs, thereby ameliorating the nutritional costs of intrasexual selection.     

The ultimate function of nuptial feeding in the bushcricket Poecilimon veluchianus (Orthoptera : Tettigoniidae : Phaneropterinae)

Summary During mating the males of the bushcricket Poecilimon veluchianus transfer a large spermatophore of about a quarter of their body weight to the female. Such nuptial feeding is often thought to function as paternal investment by increasing the fitness of the male's offspring. According to an alternative, though not mutually exclusive, hypothesis, the size of the spermatophore is maintained because of its function as a sperm protection device. In this case the cost to the male should be classified as mating effort. To discriminate between these two hypotheses we measured the duration of sperm transfer into the female spermatheca and the time taken for spermatophore consumption. A comparison of durations revealed that spermatophore consumption interferes with the process of sperm transfer (Fig. 4). There was no significant effect of spermatophore consumption on number of eggs laid, weight of eggs or absolute weight of hatched larvae. The relative dry weight of hatched larvae, however, was increased as a result of spermatophore consumption (Table 1). Thus spermatophylax size is adjusted in accordance with a sperm protection function and the spermatophylax therefore represents mating effort. The increase in relative dry weight indicates that there may also be a paternal investment effect of the spermatophylax, if the offspring that benefit from spermatophylax materials are fathered by the donating male. Correspondence to: K. Reinhold     

Mating behavior of the marine copepodOithona davisae

Oithona davisae Ferrari and Orsi were collected from the innermost region of Tokyo Bay, Japan, in 1980 and 1981. The mating behavior of this marine cyclopoid copepod consists of several steps, starting with the paddling of the male in random search of a mate. This behavior is followed by a spiraling movement in pursuance of a mate. Next is the copulatory grasp during which the male grasps the fourth swimming legs of the female partner by means of his first antennae. Whilst in this position, the male's urosome vibrates to allow the spermatophores to extrude from his genital openings. The mating behavior then culminates in the spermatophore transfer. Males do not grasp the uro-some or caudal setae of the mating partner before proper copulatory grasp. The specialized setae of the female's fourth legs may help the male to grasp her legs firmly. Spiraling occurs when the male approaches or traverses the trail of a female that is ready to copulate and that presumably emits a sex-attractant pheromone. The turning radius reduces gradually from more than 1 mm to ca. 0.25 mm as the male approaches the mate female. Females may register spiraling as a mate (male)-approaching signal. Spiraling may lead the male to locate a pheromone source more accurately, and to promote diffusion of the pheromone to prevent other males from pursuing the source. This swimming strategy can increase the copulatory chance of mature virgin females.     

Paternal investment in Poecilimon veluchianus bushcrickets: beneficial effects of nuptial feeding on offspring viability

In most bushcrickets, males transfer a large spermatophore during copulation that is afterwards consumed by the female. In some species this nuptial gift enhances offspring fitness and is therefore believed to function as paternal investment. To determine whether this is the case, I examined whether a male's own offspring benefit from spermatophore consumption in the bushcricket Poecilimon veluchianus. Females that consumed a spermatophore produced offspring with increased residuals of dry weight compared to females that were prevented from feeding on the spermatophore. This beneficial effect of spermatophore consumption occurred within the first 4 days after copulation. An increased dry weight indicates higher energy reserves because offspring dry weight correlates significantly with the lifespan of starved larvae and because spermatophore consumption increased the lifespan of starved offspring. During egg-laying, females apply a liquid substance to the soil that hardens and probably serves as protection for the egg clutch. The amount of this substance correlated with the number of eggs laid but did not differ between spermatophore treatments. In P. veluchianus, females mate frequently and there is last-male sperm precedence. The spermatophore thus only constitutes paternal investment when offspring produced before female remating benefit from spermatophore consumption. The dry weight of offspring increased during the first 4 days after spermatophore consumption and thus within the natural remating interval. This shows that the spermatophore has a paternal investment function in addition to its already known sperm protection function. Received: 15 May 1998 / Accepted after revision: 11 October 1998     

Female nutritional state affects the rate of male incubation feeding in the pied flycatcher Ficedula hypoleuca

Summary Male pied flycatches Ficedula hypoleuca regularly feed their mates during incubation. By experimentally supplying some females with extra food we studied how the female's nutritional state affected her incubation schedule and the rate at which her mate fed her. Females that received extra food spent more time on the nest and shorter periods away from it, compared with control females. This suggests that nest attentiveness is governed by the amount of energy available to the female. When females reccived extra food, males decreased their rate of incubation feeding. They also did so in response to increasing ambient temperatures, whereas incubation schedules were unaffected. We, therefore, conclude that our results support the female nutrition hypothesis, i.e., that the food provided by the male constitutes a significant nutritional contribution to the incubating female.     

Sequential female choice and the previous male effect in sticklebacks

Summary Female choice, identified as a major force in sexual selection theory, has recently been demonstrated in a number of species. These tests concentrated on simultaneous choice situations although females have to compare males sequentially in most territorial species, which is the more demanding task. Here it is shown that female three-spined sticklebacks, Gasterosteus aculeatus L., rate sequentially presented males according to their brightness. With increasing costs of sampling the females become less choosy. Furthermore, a male's attractiveness has a significant effect on the female's rating of the next male; a given male is rated higher when preceded by a duller male than by a brighter one and vice versa. Female sticklebacks use a stochastic decision rule in sequential mate choice that is attuned to the attractiveness of the present and previously encountered male. This demonstration of a previous male effect not only indicates an efficient mechanism for finding the best of a number of males but also extends the applicability of sexual selection theory.Offprint requests to: T.C.M. Bakker     

Sperm precedence, mating interval, and a novel mechanism of paternity bias in a beetle (Tenebrio molitor L.)

When females mate with more than one male, the ensuing sperm competition leads to the evolution of male mechanisms that skew paternity. Males of the yellow mealworm beetle (Tenebrio molitor) transfer a spermatophore to females during copulation, but sperm release and storage occur later. We investigated how the interval between two matings with different males affects sperm precedence by varying the interval between the copulations so that the second mating was either: (1) before sperm release from the first spermatophore (<5 min); (2) after sperm release but before spermatophore ejection (15–20 min); (3) after spermatophore ejection but before sperm storage (4 h), or (4) after complete sperm storage (24 h). We collected offspring over a period of 2 weeks and determined paternity by protein electrophoresis. There was second-male sperm precedence in all treatments, but when the interval was <5 min, the second male usually (86% of cases) had complete sperm precedence (i.e., P ₂=1). Investigations into the mechanism of second-male sperm precedence during <5-min mating intervals indicate that sperm release from the first spermatophore is inhibited, a phenomenon which has not been previously documented. Received: 31 January 2000 / Revised: 9 June 2000 / Accepted: 26 August 2000     

Female choice on male quantitative traits in lizards — why is it so rare?

Female choice on the basis of male traits has been described in an array of taxa but has rarely been demonstrated in reptiles. In the sand lizard (Lacerta agilis), and possibly in other non-territorial reptiles, a male's contribution to a female's fitness is restricted to his genes. In order to choose males of high genetic quality, females have to trade the fitness gain against the costs of active choice. In a Swedish population of sand lizards, long-lived males sired offspring with higher embryonic survival compared to offspring sired by short-lived males. In spite of this female sand lizards did not mate selectively with older and/or larger males. There appeared to be mo reliable cues to male longevity; age-specific male body size was highly variable. Furthermore, estimates of male nuptial coloration did not covary with ectoparasite load and, hence, females cannot use male coloration as a cue to heritable resistance to pathogenic parasite effects. When cues to male genetic quality are poor, or inaccurate, and males make no parental investment, we predict that female choice will be rare. Sand lizard females mating with many partners lay clutches with higher hatching success. Thus, females may obtain good genes for their young by multiple mating, thereby avoiding costs associated with mate choice.     

Temporal trends in urban and rural blood lead concentrations

A long term programme to assess the impact of reduced lead emissions in the UK has been established in central London and rural Suffolk. Blood lead concentrations of 5 and 6 year old children and their mothers both show an urban-rural difference of about 1.5 g/dl, which is related to the urban-rural differences in air and dust lead concentrations between areas.This paper is also being published in Proceedings of the Conference on Lead in the Home Environment and is one of several selected from SEGH sponsored conferences for simultaneous publication in this journal.     

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     

Reversal and transfer of spermatophores by Octopus vulgaris and O. hummelincki

Copulatory behavior in the octopus consists of a patterned series of movements whose individual functions are not well understood. Observations and experiments on mating in Octopus vulgaris and O. hummelincki from Bimini, Bahamas and Haiti were made over a number of years in the laboratory. The study reveals how the male octopus reverses its spermatophore prior to transferring it to the female. The male’s terminal organ (penis) extrudes the sperm end of the spermatophore as it exits from Needham’s sac up to the cap or filament thread and then, holding onto the cap thread, inserts the ejaculatory end of the spermatophore into the groove of the hectocotylus, thus reversing it. It is hypothesized that the primary function of the cap or filament thread, one part of the spermatophore, is to be a handle by which the reversal and transfer is accomplished. The siphon is merely a conduit through which the terminal organ functions and plays no role whatsoever in either the reversal of the spermatophore or in its insertion into the groove. The stimulus to which the male orients to find the groove of the hectocotylus is the apex of the retracted interbrachial membrane between the third and fourth right arms, which bears a fixed spatial relationship to the origin of the groove. A number of deviations from the successful transfer process, which represent loss of sperm from the reproductive process, are illustrated. Despite these deviations, the delicately balanced integration of the various movements serves to transfer the spermatophore to the female to ensure reproductive success.     

Analysing sperm competition data: simple models for predicting mechanisms

Summary Prospective models are developed for analysing sperm competition data so as to predict the underlying mechanisms determining paternity in multiply mated females. The models require: 1) estimations of proportion of offspring sired by the last male to mate (P ₂), 2) knowledge of the number of sperm transferred by each male, and 3) knowledge of the sperm storage capacity of the female, should this be limited. They will distinguish between raffles (sperm mixing without displacement) and sperm displacement mechanisms. The sensitivity of the techniques can be increased by manipulating the number of sperm transferred by each male. Typically, this can be done by manipulating copula duration or number of ejaculations, given a knowledge of the rate of sperm transfer. Data from two contrasting insect species are fitted to the models to demonstrate the techniques. These models are prospective only, and their limitations are discussed. The principal limitation is that we assume that sperm used for fertilization mix randomly in a fertilization set immediately prior to fertilization; in reality this may be difficult to identify. When sperm mixing is very rapid, the fertilization set will often be equivalent to the sperm stores, but with slow mixing, the fertilization set may be equivalent to a much more restricted zone and may change with time. Offprint requests to: G.A. Parker     

Spirorbinae (Serpulidae: Polychaeta) from South Africa,including three new species

Five Antarctic or south-temperate species of Spirorbiaae are centred in south-west Africa, whilst 6 tropical species extend round the south-east and another 4 are recorded from Mozambique. Of the three new species, Pileolaria (Pileolaria) annectans sp. n. has a rudimentary opercular plate surmounting a sort-walled sac of embryos, which somewhat resembles a thoracic brood pouch. Pileolaria (Pileolaria) dayi sp. n. has a helmet-like brood chamber, but this opens distally, like the brood cups found in the subgenus Duplicaria. Janua Pil-natalensis sp. n. has the dorsal collar folds usually separate, but partially fused in some juveniles.     

Ecological and evolutionary significance of pelagic spermatophores of vermetid gastropods

Sperm are disseminated in vermetid gastropods by spermatophores released freely into the ocean. Spermatophores from 7 species of vermetids, including 3 genera, were obtained from reproductively active males or offshore plankton tows or both. Each vermetid spermatophore consists of a sperm mass containing highly ordered eupyrene and apyrene sperm enveloped concentrically by 3 transparent capsules. Generic and specific differences occur in the size, shape and composition of the sperm mass and capsule. The complexly layered spermatophore is assembled in the male reproductive tract, which includes and elaborate set of pallial reproductive glands for capsule production. Spermatophores are liberated by males into the seawater, and there dispersed by water movements. Some of these drifting spermatophores become entangled in the mucous feeding nets of female vermetids and are then activated by feeding movements. Activation of the complex ejaculatory apparatus appears to result from an interplay of osmotic and mechanical mechanisms. Spermatophores remain viable in the laboratory for 12 to 20 h after release from the male; after 20 h, the sperm mass breaks down and the sperm become immotile. Plankton tows capture some spermatophores with motile sperm and others in which sperm are no longer active. Evolutionary implications of the relationship between production of pelagic spermatophores, sessile mode of life and other aspects of vermetid biology are discussed.