The wartbiter spermatophore and its effect on female reproductive output (Orthoptera: Tettigoniidae,Decticus verrucivorus)

Summary Male wartbiters Decticus verrucivorus transfer elaborate spermatophores to females during copulation. The spermatophore is attached externally to the female's genitalia and consists of two parts: a large, gelatinous, sperm-free portion, the spermatophylax, eaten by the female after mating; and a sperm-containing ampulla, eaten after the spermatophylax has been consumed. Since females take longer to eat larger spermatophylaxes, the duration of ampulla attachment is positively correlated with spermatophylax size. Two series of experiments were carried out, one in which the size of the spermatophylax consumed by females and the duration of ampulla attachment were manipulated in concert and another in which they were manipulated independently. Some females were also maintained on a protein-free diet and either supplied with or deprived of spermatophylax material. The amount of protein in the diet, but not the amount of spermatophylax material consumed, influenced female longevity, lifetime fecundity, and egg weight. When females were deprived of the spermatophylax, an experimental increase in the duration of ampulla attachment induced longer periods of unreceptivity in females after mating, a more rapid onset of oviposition, and an increased oviposition rate. Consequently, the number of eggs laid by females during their nonreceptive refractory periods increased significantly with increasing duration of ampulla attachment up to 180 min; however, there was no significant increase in the number of eggs laid beyond 180 min of ampulla attachment. This closely corresponds to an ampulla attachment duration of 188 min expected when a male transfers a natural spermatophylax of mean size to the female. These results suggest that the amount of ejaculate transferred to the female, and not the amount of spermatophylax material per se, is the factor controlling female receptivity and oviposition behavior. Since we did not detect any effect of spermatophylax consumption on female fecundity or egg weight, we conclude that the spermatophylax of D. verrucivorus functions primarily as a sperm protection device rather than as a form of male parental investment.     

Some costs of reproduction for male bushcrickets,Requena verticalis (Orthoptera : Tettigoniidae) allocating resources to mate attraction and nuptial feeding

Summary The cost of reproductive effort is known to result in a trade-off between current and future reproduction. Similarly, trade-offs in energy allocation may occur between components of reproductive effort, mating and parental effort, within a single reproductive episode. We investigated the energy allocated to mating effort (calling to attract females) and parental effort (donation of spermatophore nutrients at mating) by male bushcrickets, Requena verticalis, under two dietary regimes. Males provided with a low quality diet reduced the daily energy allocated to calling activity while maintaining their investment in spermatophores. Males provided with a high quality diet did not allocate more resources per day to their spermatophores but stored excess energy for future reproduction. Thus, on a per day basis, males appear to hold constant their investment in the spermatophore at the cost of reduced mating effort when resources are limited. Males on both diets, however, increased the size of their spermatophore donations when the interval between female encounters was increased. One explanation for this pattern could be a frequency-dependent optimization of spermatophore size. Correspondence to: L.W. Simmons     

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     

Female encounter rate and the calling behavior and mating propensity of male Requena verticalis (Orthoptera: Tettigoniidae)

Mating effort, the energy exerted in finding and persuading a member of the opposite sex to mate, may be influenced by how frequently potential mates are encountered. Specifically, males that frequently encounter females may reduce calling effort and be less eager to mate than males that infrequently encounter females. An experiment was set up to test this hypothesis, using the tettigoniid Requena verticalis. We examined the song structure, calling activity and mating propensity of individual males exposed to one of five different encounter rates with virgin females. Song structure and calling effort were significantly altered by an encounter with a female. After an encounter, males significantly increased chirp rate and decreased variability in interchirp interval. Encounters also stimulated a male to call and to continue to call for up to two hours. The elapsed time since mating affected mating propensity but not calling activity. Mating propensity asymptotically increased to reach a maximum by day 17 since last mating. However, neither the frequency of encounters, nor the number of previous encounters experienced by a male, influenced calling activity or the propensity of a male to mate. The significance of changes in song structure and calling activity following an encounter, and of increasing male mating propensity over time, are discussed. Correspondence to: G.R. Allen     

Role-reversal in katydids: Habitat influences reproductive behaviour (Orthoptera: Tettigoniidae,Metaballus sp.)

Summary Mating behaviour of the katydid Metaballus sp. varies. At sites QS and DB (in 1982) females competed for access to calling males and males chose mates by mating with heavier, more fecund females. At another site (BR) there was no evidence of role-reversal in reproductive behaviour, and males were observed to compete for mates. This species has a large spermatophore, a product of male reproductive glands, that is eaten by the female after mating. Males at the DB site had small reproductive glands. This suggests that some aspect of the QS and DB environments decreases spermatophore production; spermatophores become a limiting resource for females resulting in the reversal in reproductive roles observed at these sites. A field experiment that involved moving individuals from site BR to QS in 1983 determined that mating system was influerced by site (Table 1). At BR, males produced a continuous calling song, a third of the males observed attracted mates, and called for about 30 min before the female arrived; courtship duration was short. Males that were moved from BR to QS encountered a higher density of receptive females as all males attracted females after an average of just 3 min of calling. They changed their behaviour by producing short periodic bursts of song (zipping), and by courting females for long periods of time. The long courtship period may function as as a mate-assessment period for males. The reproductive behaviour of BR males moved to QS differed from that of native QS males only in the length of time spent in copula.     

Some constraints on reproduction for male bushcrickets,Requena verticalis (Orthoptera : Tettigoniidae) diet,size and parasite load

Summary Reproduction for male bushcrickets is energetically expensive. Male Requena verticalis invest 70% of their daily energy reserves in calling to attract a female and providing her with a nutritious spermatophore. Males are thereby likely to be constrained in their mating frequency. I investigated constraints on reproduction imposed by body size and the levels of a protozoan gut parasite when males were fed diets that differed in their nutritional value. Males suffered a cost of reproduction in terms of an increasing interval between matings that was independent of diet and parasitic infection. After three successive matings, males decreased the magnitude of investment in courtship feeding when fed a diet poor in protein. Furthermore, these males suffered a reduction in the number of times they were capable of mating relative to males fed a diet rich in protein. Male size constrained mating frequency on both rich and poor diets; small males were able to mate less frequently than large males. There was an interaction between the effects of diet and parasitic infection on male mating frequency. Heavily infected males mated less frequently than uninfected individuals when fed the poor diet. However, males fed the rich diet were able to overcome the constraints imposed by parasitic infection. Reproductive constraints are discussed in relation to the costs of reproduction and their effects on courtship roles.     

The sex in short supply for matings varies over small spatial scales in a katydid (Kawanaphilanartee, Orthoptera: Tettigoniidae)

In katydids such as Kawanaphilanartee, a female bias in the operational sex ratio (OSR) results in female competition for mates and male choice of mates. Previous work showed that the excess of sexually active females occurs when food availability is low, in part because less food increases the propensity of females to mate as they forage for the large edible spermatophores produced by males. In this study with K.nartee, a pollen-feeding species, we estimate natural variation in numbers of sexually active males and females by assessing male calling activity and the propensity of females to respond to experimental calling males. We found an excess of sexually active males at a site with many flowers and an excess of sexually active females at a site with few flowers about 900 m away. Between-site differences in gut masses of calling males were consistent with the hypothesis that pollen availability controls OSR. Finally, at a third site where flowers were at first scarce, we found that the initial excess in sexually active females changed to an excess of sexually active males after a clump of grass-trees flowered. The mean gut mass of all sampled males from this site increased after flowering. The large variation in OSR that we document for K. nartee highlights the importance of identifying the appropriate spatial and temporal scales over which OSRs are measured in studies of factors controlling sexual selection. Received: 13 May 1997 / Accepted after revision: 27 October 1997     

Close-range acoustic signaling and mate choice in Hawaiian crickets (Gryllidae: Laupala)

Evolution of the mate recognition system (MRS) can play a central role in animal speciation. One dramatic consequence of changes in the MRS is the failure of individuals from divergent lineages to successfully court and mate, thereby reducing gene flow between these groups. Here, we test the role of an acoustic mating signal on mate choice in a Hawaiian cricket genus (Gryllidae: Laupala). Speciation in Laupala is proceeding at an extremely rapid rate, apparently driven by divergence in aspects of the mate recognition system, most conspicuously the pulse rate of male calling song. Previous studies demonstrate that females prefer the pulse rate of a conspecific male’s song when perceived at long range, in laboratory phonotaxis trials. In this study, we examined mate choice in two species that differ dramatically in pulse rate: Laupala paranigra and Laupala kohalensis. We tested the female’s preference in both species for pulse rates at close range, by providing females an opportunity to mate with hybrid males producing a range of intermediate pulse rates. Results of our study demonstrate that while strong behavioral barriers exist between these two species, variation in the pulse rate of male calling song did not predict female mate choice at close range. These results suggest a more complex architecture to mate recognition in Laupala than previously hypothesized.     

Female mate choice in the non-territorial lizard Ameiva plei (Teiidae)

Mate choice by females has been documented in a variety of taxa. Female mate choice in species lacking male resource control or paternal care might occur if preferred males provide protection from harassment. Female mate choice was investigated in a natural population of the non-territorial lizard Ameiva plei (Teiidae). Consort pairs were allowed to form naturally. Consort males were significantly larger than non-consort males. After removal of consort males, the “abandoned” female's reaction to the first male who approached her was recorded. Females rejected all small males. Female preference for large males was significantly higher than preference for small males. Large males may be better equipped to guard the females from harassment and behavior of large males is less harassing than behavior of small males, thereby affording the female increased foraging time. Received: 21 June 1996 / Accepted after revision: 28 December 1996     

Studies on the maturation-accelerating pheromone of the desert locustSchistocerca gregaria (Orthoptera: Acrididae)

Summary The accelerating effect of mature males of the desert locust,Schistocerca gregaria, on the maturation of immature male and female conspecifics was confirmed. The onset of sexual activity was found to correlate with yellowing of the male insects. Using the colour as an indicator of maturation, the maturation-hastening effect of an hexane extract from mature males was also confirmed. Likewise, volatiles from mature males placed in the upper storey of a two-chamber bioassay system (no visual or tactile contact possible) and charcoal-trapped volatiles from the mature males also induced accelerated maturation in recipient males placed in the lower storey. GC and GC-MS analysis of volatiles collected from 4-week-old mature males showed the presence of anisole, benzaldehyde, veratrole, phenylacetonitrile and 4-vinylveratrole, roughly at the ratio 4.8:7.0:3.3:79.8:5.0. In addition, guaiacol, phenol, benzoylnitrile, benzyl alcohol and 2-benzoyloxyphenylacetonitrile were present in smaller amounts. These compounds were either absent or found only in trace amounts in the female volatiles. Earlier, we had shown that essentially the same blend collected from younger males (10–20 d old, not yet demonstrating signs of maturation) induced strong aggregation of both sexes of adult desert locusts, suggesting a parsimonious role for the pheromone system: as an adult aggregation signal and as a maturation accelerant in young adults.     

Discovery of postcopulatory mate guarding in Copepoda Harpacticoida (Crustacea)

Mating behaviour of four species of Tisbe (Tisbidae) and of Paramphiascella fulvofasciata (Diosaccidae) was filmed with a videocamera during 1992 and 1993 at the University of Oldenburg. This behaviour is complex and can be divided into different phases: grasping of the female; courtship; copula and postcopulatory mate guarding. During courtship both partners lie parallel in opposite directions with their ventral sides facing each other. The male strokes the abdomen of the female with his second to fourth peracopods. As a result the female becomes motionless. The copula is a quick process of only a few seconds during which spermatophore transfer takes place. When this has happened, males do not leave the females but become inactive and are carried around by them for varying lengths of time. This pattern and the fact that only adult partners are involved in these associations prove that this behaviour is very different from the precopulatory mate guarding presumed to be ubiquitous among Harpacticoida. Cases of postcopulatory mate guarding have never been explicitly demonstrated for Harpacticoida. The minimum duration of guarding was found to match the time necessary for spermatophore discharge. Guarding is, therefore, interpreted as a strategy to secure paternity. New definitions are given for courtship, copula and postcopulatory mate guarding in Harpacticoida to help avoiding misinterpretations of associations between adult partners. Such misinterpretations abound in the literature.     

Long-term mate and territory fidelity in neotropical buff-breasted wrens (Thryothorus leucotis)

Among sedentary species, mate and site fidelity may be imposed by year-round territoriality and high annual survivorship, both of which theoretically lead to few opportunities to move between mates and breeding territories. We examined mate and territory fidelity in sedentary neotropical buff-breasted wrens (Thryothorus leucotis) in relation to the opportunities to divorce (vacancies on neighbouring territories), breeding experience and site of origin (within vs outside local breeding population). Overall, buff-breasted wrens showed high rates of mate and territory fidelity between years, with individuals significantly more faithful to their territories than to their partners. Mate and territory fidelity was not forced upon buff-breasted wrens, as most individuals had opportunities to switch mates and territories. However, this was not uniform among all individuals. Individuals that had bred together displayed 100% mate and territory fidelity despite the fact that males and females in almost all experienced pairs had opportunities to switch mates and territories. Local recruits (philopatric offspring that acquired territories in the local breeding population) also displayed mate and territory fidelity, but fidelity occurred because recruits rarely had the opportunity to divorce prior to initiating their first breeding attempt. By contrast, almost half of all territorial individuals that originated outside the local breeding population (immigrants) had opportunity to divorce, with approximately two thirds of them switching mates and territories. Divorces occurred within the first 5 months of pairing, suggesting that immigrants may have sampled mates and territories before forming permanent partnerships.     

A dusk chorus effect in a nocturnal bird: support for mate and rival assessment functions

The dawn chorus is a striking feature of spring mornings and a characteristic behaviour of many bird species, particularly the passerines. Dawn singing has been considered a reliable signal of male quality for mate and rival assessment. Singing is presumed to be relatively costly at dawn both because air temperatures are relatively low and because birds have not fed overnight. Models of optimal daily routine predict the existence of a “dusk chorus” in nocturnal birds, although this prediction has received little empirical attention. Nocturnal birds at dusk may be energy-limited because of a lack of daytime feeding, and singing at dusk may thus ensure signal reliability. Here, we used an observational and experimental approach to study vocal behaviour at dusk and dawn in a nocturnal raptor, the little owl Athene noctua. We assess whether male little owls adjust their vocal behaviour according to feeding stage (i.e. period of the night), ambient air temperature and territorial context (i.e. spontaneous calling behaviour vs elicited calling by intrusion). Across different temperatures, we find that both spontaneous vocal activity and inter-individual variability in call duration increased at dusk, clearly indicating a dusk chorus phenomenon. Results from playback presentations suggest that food, rather than air temperature, is likely to be more constraining at dusk. We discuss how comparing dusk and dawn choruses in nocturnal and diurnal species can provide insights into both mechanistic and functional aspects of signalling behaviour.     

Protandry in western cicada killer wasps, (Sphecius grandis,Hymenoptera: Sphecidae): an empirical study of emergence time and mating opportunity

Summary Sphecius grandis is a univoltine, colonial wasp. Females mate once and are sexually receptive when they emerge in July and early August. Males generally emerge earlier in the summer than females. The opportunity for each male to acquire mates is a function of the number of females emerging during his lifetime and the number of competitiors that are active when the females emerge. I determined a mating opportunity index (MOI) for each male in an aggregation of wasps for three separate summers, and correlated the MOI of individual males with their emergence date. The MOI of a male estimates the potential contribution that timing of emergence makes to his reproductive success. In 1984 males emerging near the mean of the male emergence distribution had the highest MOI. These males emerged between one and two weeks prior to the mean female emergence date. However, in 1981 late emerging males had the highest MOI. In 1983 there was no significant difference in MOI among males. As a result of between-year variation in female emergence schedules and in the duration of male lifetime, the selection pressures influencing male emergence time vary between years.     

Assessments and decisions in Metellina segmentata (Araneae: Metidae): evidence of a pheromone involved in mate guarding

Assessments and decision-making underlying the initiation of mate guarding in a common web-building spider, Metellina segmentata, are examined in a series of field and laboratory studies. Adult males do not build webs but wander in search of females and mating opportunities. Adult males then wait at the edge of the webs of females and guard them prior to courtship and mating. Guarded females were heavier, larger and carried more mature eggs than solitary females. An active process of information gathering is apparent from introductions of males to the webs of females. Males make accurate assessments about female quality, even in the absence of the resident female. Cues involving web architecture are not used. Males may assess pheromonal cues on the web of the female in deciding whether to guard or abandon a female.     

Tactics, effectiveness and avoidance of mate guarding in the blue-footed booby (Sula nebouxii)

We examined the dynamics and avoidance of mate guarding, by males and females, in the blue-footed booby, in which the two social mates are usually simultaneously present on the territory but each of them is unmonitored by the other for one-quarter of its time. Both sexes were promiscuous and liable to switch mates. Cuckolded individuals did not increase their overall presence on the territory, but in response to the extra-pair (EP) courtships of their mates, both sexes doubled their rate of intra-pair (IP) courtship and sometimes showed aggression. The male or female's presence depressed the social mate's EP activity, but intra-pair courtship had no such effect, tending even to propitiate that EP activity. Similarly, when females responded to their social mates' EP courtship with approach or aggression, disruption of EP activity was short-lived. Promiscuous females modified their diurnal pattern of attendance, as if attempting to sidestep monitoring by their mates, but cuckolded males matched the modification. Both sexes tended to perform their EP activities at a distance when their mates were present, possibly to evade monitoring or disruption by their mates. Male and female boobies cannot monitor their mates continuously, they do little to facultatively adjust their presence on territory to the risk of infidelity, and their immediate responses to overt infidelity have only the briefest impact; but the information they acquire while monitoring their mates may be critical to constraining their mates' infidelity and also to calibrating their own reproductive investment.     

Female mate choice in the gray treefrog (Hyla versicolor) in three experimental environments

We studied female mate choice by Hyla versicolor in three venues to examine how acoustic and spatial complexity, background noise, and the calling behavior of males might influence preferences manifest in previous laboratory two-stimulus choice tests. Our laboratory-based two-stimulus choice tests with and without broadcasts of chorus noise demonstrated that females prefer long calls relative to short calls when calling efforts of alternatives are equivalent. Background noise impaired the ability of females to discriminate in favor of longer over shorter calls, but the magnitude of the effect was small. Captures of females at eight speakers broadcasting 6- to 27-pulse calls at the edge of a pond revealed strong discrimination against only the shortest call variant. In natural choruses, females may only rarely encounter males using such unattractive vocalizations. Female phonotaxis at an artificial pond with caged and electronically monitored calling males also indicated that consequences of female preferences for temporal aspects of calling observed in two-stimulus choice tests are much attenuated in choruses and explain only small portions (<10%) of the variation in male mating success. Nevertheless, relatively high call duration and calling effort increased male attractiveness. Acoustic interference emerged as another significant factor influencing male mating success and possibly the differences in female choice observed in laboratory and chorus settings. We suggest that the bias of females against both overlapped and very short calls may help explain why males lengthen their calls but lower their rate of delivery in response to increases in chorus size.     

Extra-pair paternity in the monogamous alpine marmot (Marmota marmota): the roles of social setting and female mate choice

Extra-pair paternity (EPP) can be influenced by both social setting and female mate choice. If evidence suggests that females try to obtain extra-pair copulations (EPCs) in order to gain genetic benefits when mated to a homozygous and/or to a related male, females may not be able to choose freely among extra-pair mates (EPMs) as the social mate may constrain female access to EPMs. In this study, we investigated, first, how EPP depended on social setting and specifically on the number of subordinate males in the family group in a highly social and monogamous mammal, the alpine marmot. Second, we investigated how EPP depended on female mate choice for genetic benefits measured as male mate-heterozygosity and within-pair relatedness. Our results reveal, first, that EPP depended on the social setting, increasing with the number of subordinate males. Second, EPPs were related to relatedness between mates. Third, EPMs were found to be more heterozygous than within-pair males. Thus, social setting may constrain female choice by limiting opportunities for EPC. However, after accounting for social confounding factors, female choice for genetic benefits may be a mechanism driving EPP in monogamous species.     

Trade-off between mate guarding and mate attraction in the polygynous great reed warbler

Summary In a Swedish population of the polygynous great reed warbler Acrocephalus arundinaceus, about 40% of the males formed pairs with more than one female. Males sang two completely separated types of song: (1) long song when they tried to attract mates and (2) short shong when they guarded a fertile female. As soon as a male had attracted a female he immediately switched from long to short song and apparently guarded her for at least 3 days. Most males left their female and started singing long several days before her fertile period ended. This behavior probably increased the risk of cuckoldry. By assuming that males of polygynous species maximize their fitness over the whole breeding season (i.e., maximize fitness rate), we predicted longer mate guarding periods when the probability of attracting a second female was low and the risk of cuckoldry was high. These predictions were supported by observations. The probability of attracting a second female decreased during the breeding season and, in accordance, the number of days that males sang long song during the primary female's fertile period was negatively correlated with the time of the season. This trend held also for individual males when comparing mating periods of their primary and secondary female. The increasing rate of male intrusions with season may also have contributed to the increasing mate guarding periods. Offprint requests to: D. Hasselquist     

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.