Sperm Competition and Copulation Intervals of the White Spoonbill (Platalea leucorodia,Aves, Threskiornithidae)

Some aspects of sperm competition were studied in the white spoonbill (Platalea leucorodia) breeding in Doñana National Park (SW Spain). Shorter pair copulation intervals occurred during the prelaying period, when females were subjected to a relatively high frequency of extra-pair copulations. Pair copulation intervals with an intermediate extra-pair copulation by the male mate were longer than those without extra-pair copulation. This result indicates that males need a time of recovery between copulations before they can perform another. Extra-pair copulations by the females did not affect the length of intervals between pair copulations. There were no differences between the lengths of the intervals between an extra-pair copulation by the female and the following pair copulation for cases in which the male mate detected an intruder male attempting copulation with his mate and those in which the intruder remained undetected. However, the correlations obtained between copulatory intervals for detected and undetected cases suggest a copulatory response by their mates, although affected by the required recovery time between copulations by the males. Finally, since extra-pair copulations mainly occurred while male mates were collecting nest material, they engaged in this activity shortly after pair copulations, probably to avoid a last-male advantage under the sperm competition pressure.     

Explicit experimental evidence for the role of mate guarding in minimizing loss of paternity in the Seychelles warbler

Extra-pair copulations (EPCs) (copulations outside the pair bond) resulting in extra-pair fertilizations (EPFs) are widespread in birds. To increase reproductive success, males should not only seek EPCs, but also prevent their females from having EPFs. Male Seychelles warblers (Acrocephalus sechellensis) follow their partner closely during the period when these females are most receptive (fertile period). The Seychelles warbler is the first species to offer explicit experimental evidence that mate guarding functions as paternity guarding: in territories where free-living males were induced to stop mate guarding during the pair female''s fertile period, the rates of intrusions by other males and successful EPCs (male mounting female) were significantly higher than those observed in the control group and in the absence of mate guarding the frequency of successful EPCs increased significantly with local male density. Male warblers do not assure their paternity through frequent copulations to devalue any sperm from other males: males do not copulate with their partners immediately following a successful EPC obtained by their partners, the frequency of successful within-pair copulations does not increase with the frequency of successful EPCs and females initiate all successful copulations and are capable of resisting copulation attempts.     

Why Do Female Birds Reject Copulations from their Mates?

Female birds frequently reject copulations from their mates, suggesting a conflict between the sexes. This study analyses behavioural data of socially monogamous razorbills, Alca torda, to examine whether females rejected their mates because of conflicts over fertilization or the pair bond. Among pairs, females rejected 9–70 % of their mates’ copulation attempts and prevented their mates from completing 42–100 % of successful copulations. Copulations terminated by females were half the duration of those terminated by males, and females terminated fewer first copulations than subsequent ones on the same day. These findings indicate that females were motivated to copulate less frequently and for shorter durations than their mates. The sperm competition hypothesis predicts that females reject their mates to increase the probability of being fertilized by extra-pair males. This hypothesis was not supported because females rejected extra-pair males similarly to their mates. The female-mate-guarding hypothesis predicts that females guard their pair bond by copulating frequently with their mates, thereby depriving the males of time and energy to copulate with and form bonds with other females. This prediction was consistent with a significant negative correlation between the percentage of copulation attempts that females accepted from their mates, and the number of extra-pair copulations that their mates attempted. However, this correlation was not caused by a trade-off of males copulating with their mates instead of attempting extra-pair copulation because males attempted most extra-pair copulations on days when their mates were absent. A new hypothesis is proposed, namely, that females reject their mates to test the male's commitment to provide essential parental contributions after egg-laying. The ‘testing-of-the-bond’ hypothesis is consistent with the findings but requires testing.     

Do Female Red-winged Blackbirds Engage in a Mixed Mating Strategy?

Parentage analyses of broods of nestling red-winged blackbirds (Agelaius phoeniceus) revealed that extra-pair fertilizations (EPFs) accounted for 24% of the offspring. 8% of attempted copulations and 13% of male courtship displays during observations of focal females were by extra-pair males. In addition, mates and non-mates often chased and occasionally made physical contact with females; 34% of those chases in which contact was made were extra-pair chases. Females behaved variably during both within-pair and extra-pair events; females crouched less and resisted more frequently during extra-pair courtship than during within-pair courtship. All extra-pair events, whether natural or induced by male removal, were either resisted or accepted by the female. In 318 focal female-hours of observation during the fertilizable period, no female was ever seen in another male's territory soliciting a copulation. In addition, removal of females' mates resulted in frequent extra-pair courtship and copulation; all of these occurred on the removed male's territory. Some females left their mates' territories on occasion — these forays were nearly always off the study area, no female was ever seen copulating with an extra-pair male while on these forays, and neither the frequency nor the duration of female forays correlated with the frequency of extra-pair fertilizations within broods. There were no associations between extra-pair fertilizations and female age, settlement order, nest order, or clutch size. The number of fledglings produced from a nest was significantly positively associated with the number of sires of the brood. Fewer offspring apparently starved in broods that were multiply sired, yet males did not provide courtship feedings during either within-pair or extra-pair copulations, nor was any paternal care provided to young sired through extra-pair matings. The frequency of infertile eggs was low (< 1%); in those instances of infertile eggs the territory owner sired some young in the same nest or another nest on his territory. Fewer broods were a mixture of within-pair and extra-pair paternity than expected by chance. Clear evidence implicating a mixed strategy on the part of females could not be gathered. Because females behaved variably and because not all costs and benefits to females of extra-pair copulations could be measured, it remains possible that female behavior patterns are either (1) part of a mixed strategy, or (2) part of a strategy minimizing the costs of copulation.     

Bateman gradients in field and laboratory studies: a cautionary tale

Since tools of molecular genetics became readily available,our understanding of bird mating systems has undergone a revolution.The majority of passerine species investigated are sociallymonogamous, but have been shown to be genetically polygamous.Data sets from natural populations of juncos suggest that multiplemating by females results in a sexual selection gradient assteep for females as for males (a result that does not supportBateman's predictions). However, in males, fitness is enhanceddirectly through fertilization success with multiple matings;in females fitness benefits may be enhanced immediately throughdirect access to food, protection against predators, or otherresources received from males, or they may be delayed throughimprovement in offspring quality (e.g., through good genes,or greater genetic compatibility between the female and theextra-pair male). But a steep sexual selection gradient forfemales can be difficult to interpret. If all females copulatewith multiple partners that are equally likely to fertilizeeggs, then females that produce larger clutch sizes, for anyreason, will appear to have copulated with more males. Thatis, multiple sires have a higher probability of detection inlarger clutches than in smaller ones, giving the impressionthat females that mate with multiple males increase their reproductivesuccess. Yet, in most studies in which there is a correlationbetween number of offspring produced by females and number ofextra-pair males, causation has not been clearly establishedand other factors may explain the results. Additional complicationsin understanding male and female reproductive strategies are:(1) Molecular studies cannot detect extra-pair copulations thatdid not result in fertilizations; yet if a female acquires foodor other resources from extra-pair males, such extra-pair matingsmay have significant effects on female fitness. Thus, molecularstudies provide only a conservative estimate of the number ofextra-pair copulations or "mates" that a female has. (2) Clutchsize affects the probability that any given male will be successfulin fertilizing a female's eggs. Specifically, at any given point,a male's chances of fertilizing at least one egg in the female'sclutch will be greater as clutch size increases. We predictthat in avian species with small clutch sizes, males may beselected to be choosy and avoid extra-pair copulations, whilefemales should be selected to be less discriminating. Moreover,if extra-pair males provide resources that increase female fitness,the females should seek extra-pair copulations, whether or notthe males are likely to fertilize any of her eggs. Laboratory studies with insects have yielded clearer evidenceof the causal relationship between multiple mating and increasedfemale fitness. We review studies on a tenebrionid beetle inwhich female fecundity increases directly with number of mates.In these experiments, the nutritive value of the spermatophoresdoes not fully explain the increase in female reproductive success.     

Extra-pair paternity in the shag, Phalacrocorax aristotelis as determined by DNA fingerprinting

The frequency of chicks resulting from extra-pair copulation in the shag, Phalacrocorax aristotelis , was measured by DNA fingerprinting. DNA fingerprints were taken from both sexes of 15 pairs and their chicks (28) in a subcolony on the Isle of May, UK. It was found that 18% of the chicks had extra-pair paternity, and one chick (3.5%) was not the offspring of either member of the pair, implying either a polygynous male whose second female was fertilized by another male or adoption. Although no observations of courtship and copulation were made in the same season, observations in a previous year on the same colony of shags showed that 14.1% of the copulations by males were not with the female with whom that male reared young. The similarities and differences are discussed between these results on the level of extra-pair copulations and of extra-pair paternity and those of other studies where both observations of extra-pair copulations and various measures of the degree of extra-pair paternity have been made.     

Sperm competition in birds

Ornithologists have known for a long time that males of monogamous bird species sometimes copulate with females from other pairs, but it is only in the last few years that researchers have shown that these extra-pair copulations can result in offspring and increase male reproductive success. Males time their extra-pair copulations to coincide with the period when females are fertilizable, and they show a range of remarkable behaviours to help them secure these matings, since in most cases females attempt to avoid them. At the same time, males of most species employ one of two strategies (mate guarding or frequent copulation) to avoid being cuckolded themselves.     

Paternal care declines with increased opportunity for extra-pair matings in fairy martins

Following the discovery that extra-pair fertilizations are common in many birds, it has been predicted that male participation in parental care may be influenced by their opportunity for extra-pair copulations. However, such a trade-off between male contribution to parental care and the availability of fertile females has not been confirmed. Here we use a novel remote monitoring technique to show that participation in incubation by male fairy martins, Hirundo ariel, declines with the increasing availability of fertile females in the breeding colonies. Furthermore, male contribution to incubation is most responsive to change in the availability of fertile females in the early morning, when most copulations occur, and also if their clutches are smaller than average. Both of these patterns support the presence of a trade-off between parental and extra-pair copulation effort. We suggest that this trade-off may be widespread among the 90% of bird species where males contribute to parental care.     

Adjustment of copula duration and ejaculate size according to the risk of sperm competition in the golden egg bug (Phyllomorpha laciniata)

Several hypotheses have been proposed to explain the adaptivesignificance of prolonged copulations in insects, which includemate guarding and sperm loading functions. We have exploredthe adaptive significance of the prolonged copulations in thegolden egg bug (copulations up to 50 h) and the effect of anincreased risk of sperm competition on ejaculate investment.Our data support predictions derived from sperm competitiontheory, which posits that males are expected to increase ejaculateexpenditure in response to an increased risk of sperm competition.Results show a combined response by males that has not beenpreviously described: males in the presence of rivals increasecopulation duration and the rate of sperm transfer. No relationshipwas found between male or female size and copulation durationor ejaculate size. Golden egg bug males transfer sperm slowlyand gradually throughout copulation; thus an increase in theamount of sperm transferred and the corresponding increase inthe male's numerical representation in the female's storageorgans could be particularly important in a system in whichso few sperm are transferred and in which so few sperm are storedby females. In addition, copulation duration may not only serveto increase the total amount of sperm transferred, but it mayalso increase the chances that the female will lay an egg soonafter copulation has ended. This could explain why males tendto accept eggs after copulation, since they could be maximizingthe chances that such eggs are fathered by them, and in thisway they would substantially increase the survival rates oftheir offspring because eggs laid on plants suffer high mortalityrates.     

Cere Colour as a Basis for Extra-pair Preferences of Paired Male Budgerigars (Melopsittacus undulatus: Psittacidae: Aves)

Male budgerigars may be limited in the time they have available to pursue extra-pair copulations because of conflicts with other reproductive behaviour. If males could selectively court only immediately fertilizable extra-pair females they should do so. The cere colour of a female budgerigar may be used as a cue to her reproductive readiness. We experimentally tested the hypothesis that males prefer females with dark ceres, which are indicative of developed ovaries, over females with light-coloured ceres, characteristic of birds with undeveloped ovaries. In a pairwise choice experiment between females that had their cere colour artificially manipulated, pair-bonded males were more likely to choose the female with the dark-coloured cere.     

Explicit experimental evidence for the effectiveness of proximity as mate-guarding behaviour in reducing extra-pair fertilization in the Seychelles warbler

Extra-pair copulations (EPCs; copulations outside the pair bond) are widespread in birds and may result in extra-pair fertilizations (EPFs). To increase reproductive success, males should not only seek to gain EPFs, but also prevent their own females from gaining EPFs. Although males could reduce the number of EPCs by their mates, this does not necessarily mean that they reduce the number of EPFs; indeed several studies have found no association between EPCs and EPFs. Male Seychelles warblers (Acrocephalus sechellensis) follow their partner closely during the period when the pair female is most receptive (fertile period). We show that males that guarded their mates more closely were less likely to have extra-pair young in their nest. This study on the Seychelles warbler is the first to provide explicit experimental evidence that mate guarding is effective in reducing EPFs. First, in territories where free-living males were induced to stop mate guarding during the pair female's fertile period, extra-pair parentage was higher than in the control group. Second, in the experimental group, the probability of having an extra-pair nestling in the nest was positively associated with the number of days during the fertile period for which mate guarding was artificially stopped. Thus, male mate guarding was effective in reducing the risk of cuckoldry.     

Experimental manipulation of timing of breeding suggests laying order instead of breeding synchrony affects extra-pair paternity in house sparrows

The timing of breeding may not only affect breeding patterns such as the overlap of chick rearing period with the peak in food availability but also the opportunity for extra-pair mating. A negative relationship has been predicted between extra-pair paternity and breeding synchrony, assuming that male extra-pair activity is traded against mate guarding and parenting duties. In contrast, if female ability to assess male quality is temporally constrained, sperm competition might be a positive function of breeding synchrony. Here we manipulated the progress of nesting by nest material exchange within nesting aggregations to see whether the timing of breeding affects extra-pair paternity in house sparrows. We found that late broods within nesting clusters contained extra-pair young more often than early broods, but breeding synchrony did not turn out to be a significant predictor of extra-pair paternity. Our study indicates that temporal constraints of male extra-pair activity may account for extra-pair paternity levels, but it is also possible that late-breeding females may accept extra-pair copulations to ensure egg fertilization.     

Extra-pair matings and mate guarding in the common murre Uria aalge

Forced extra-pair copulations (FEPC) are frequent and mate guarding well developed among common murres. Male murres were at the colony almost continuously through the pre-laying period, but females were present only infrequently, and the frequency of FEPCs was significantly correlated with the relative number of males present. Males vigorously defended their partners from other males and females attempted to resist extra-pair matings. Females whose mates were absent were particularly vulnerable to FEPCs. The number of extra-pair copulations performed by males was estimated to vary between 0–32/season. The reproductive successes of males not performing FEPC, and those performing at the mean and maximum rate are estimated. Males most active in FEPC may substantially increase their reproductive success compared with males not performing FEPC. Ecological conditions in the common murre probably favour prolonged sperm storage, which in turn provides opportunities for sperm competition and favours both effective mate guarding and extra-pair copulations.     

Fitness consequences of divorce in the azure-winged magpie depends on the breeding experience of a new mate

Sexual conflict in producing and raising offspring is a critical issue in evolutionary ecology research.Individual experience affects their breeding performance,as measured by such traits of provisioning of offspring and engagement in extra-pair copulations,and may cause an imbalance in sexual conflict.Thus,divorce is hypothesized to occur within aged social pairs,irrespective of current reproductive success.This concept was explored in the azure-winged magpie Cyanopica cyanus by investigating the divorce of a social pair and its relationship to their changes in breeding performance with prior experience.Females engaging in extra-pair copulation may intensify sexual conflicts and may be the main reason for divorce.Once divorced,females repairing with an inexperienced male realized higher reproductive success than that repairing with an experienced male;males repairing with an experienced female realized higher reproductive success than that repairing with an inexperienced female.This finding indicates that the fitness consequence of divorce depends on the breeding experience of new mates.Divorced females can obtain more extra-pair copulations,whereas divorced males cannot,when they repair with inexperienced breeders.Divorced females provisioned a brood at lower rates than inexperienced females whereas divorced males had no such difference.It appears that divorced females can obtain an advantage in sexual conflicts with inexperienced mates in future reproduction.Consequently,females are probably more active than males in divorcing their aged mates so as to select an inexperienced male as a new mate.Azure-winged magpies thus provide novel insights into the implicaticns of sexual conflict in birds.     

Does male extra‐territory foray effort affect fertilization success in hooded warblers Wilsonia citrina?

Hooded warbler Wilsonia citrina males vary greatly in the frequency and duration of their off-territory forays in search of extra-pair copulations. We used radiotracking and microsatellite parentage analysis in high and low density populations to determine if (1) high foray rate or time off-territory reduces within-pair fertilization success, and (2) if a high foray rate onto the territory of a fertile female increases the likelihood of obtaining EPFs with that female. Males who left their territory often, or for longer periods, did not have lower within-pair fertilization success. Some males repeatedly visited a neighboring fertile female, but in only 3 of 19 cases where radiotagged males visited a fertile female did the male actually sire offspring with that female. Male foray rate onto a fertile female's territory was not a good predictor of whether or not he sired extra-pair offspring with that female. We suggest that mate choice and extra-pair behavior by females may explain why male foray behavior does not correspond closely with actual fertilization success.     

Copulation behaviour and paternity in shy albatrosses (Thalassarche cauta)

We investigated the mating system of shy albatrosses Thalassarche cauta by combining behavioural observations during the pre-laying period with genetic paternity analysis. Genetic data on the mating systems of several procellariiform seabirds have recently become available, but data on the reproductive behaviour of these species are rarely obtained. Our main aims were to describe the copulatory behaviour of this species and identify how males achieve within-pair and extra-pair paternity (EPP). Most copulations occurred on the nest, were unforced and were within-pair. Females controlled the success of copulations and were observed soliciting extra-pair matings. Within-pair and extra-pair copulations were behaviourally similar. A low frequency (7–10%, n =29 chicks) of EPP was detected despite male use of frequent copulation as a paternity guard. The pre-laying foraging exodus of female shy albatrosses differed from that in other albatrosses: it was relatively short in length, lasting c . 2 days, and within-pair copulations occurred after the female's return 2 days before laying. This may reflect the close proximity of feeding grounds to the breeding colony.     

Polygynandry,face-to-face copulation and sperm competition in the Hihi Notiomystis cincta (Aves: Meliphagidae)

The Hihi or Stitchbird Notiomystis cincta breeding system is highly variable and includes monogamy, polyandry, polygyny and polygynandry. Males have large testes (4.2% of body mass), very large numbers (1460 × 10⁶) of sperm in their seminal glomera and an unusually enlarged cloacal protuberance. These features are also found in other species with highly variable mating systems where males are under intense sperm competition. Hihi copulate in two different positions: face to face and, more conventionally, with the male on the female's back. Face-to-face copulation is unique among birds and appears to be a form of forced copulation. The presence of enlarged cloacas in both sexes could aid the transfer of sperm. Both male and female Hihi appear to benefit from a mixed reproductive strategy where a female Hihi can solicit copulations from males other than her partner and male Hihi can perform extra-pair copulations both with willing females or by forced copulation.     

Insemination success discrepancy between long-term and short-term copulations in the provisioning shield bug, Parastrachia japonensis (Hemiptera: Cydnidae)

The duration of copulation in the gregarious shield bug, Parastrachia japonensis Scott (Hemiptera: Cydnidae), is of two types, the far more prevalent short-term copulation (average, 15 s) and the long-term coupulation (average, 23 min). Both types were thought to be equally effective in inseminating females. Recent evidence has suggested that there is, in fact, a discrepancy in insemination success between the two duration types of copulations. We carried out manipulated field studies to clarify the difference in insemination success between the two duration types and to determine whether there is some physical or physiological variability in females or males that might affect female receptivity to a long-term copulation. The findings indicated that, although a small percentage of short-term copulations resulted in some sperm transfer, long-term copulations were a far more effective way for males to inseminate females. Further, females experiencing long-term copulations were found to be at a slightly more advanced stage of ovarian development than those experiencing only short-term copulations, and may be deciding whether a long-term copulation occurs. Male size does not appear to affect copulation duration. It is concluded that the long-term type of copulation is the actual effective copulation duration in this species and the objective of all females. Possible factors that might contribute to the prevalence of these two copulation durations are discussed. Received: June 21, 1999 / Accepted: September 6, 1999     

A spatial genetic structure and effects of relatedness on mate choice in a wild bird population

Inbreeding depression, as commonly found in natural populations, should favour the evolution of inbreeding avoidance mechanisms. If natal dispersal, the first and probably most effective mechanism, does not lead to a complete separation of males and females from a common origin, a small-scale genetic population structure may result and other mechanisms to avoid inbreeding may exist. We studied the genetic population structure and individual mating patterns in blue tits (Parus caeruleus). The population showed a local genetic structure in two out of four years: genetic relatedness between individuals (estimated from microsatellite markers) decreased with distance. This pattern was mainly caused by immigrants to the study area; these, if paired with fellow immigrants, were more related than expected by chance. Since blue tits did not avoid inbreeding with their social partner, we examined if individuals preferred less related partners at later stages of the mate choice process. We found no evidence that females or males avoided inbreeding through extra-pair copulations or through mate desertion and postbreeding dispersal. Although the small-scale genetic population structure suggests that blue tits could use a simple rule of thumb to select less related mates, females did not generally prefer more distantly breeding extra-pair partners. However, the proportion of young fathered by an extra-pair male in mixed paternity broods depended on the genetic relatedness with the female. This suggests that there is a fertilization bias towards less related copulation partners and that blue tits are able to reduce the costs of inbreeding through a postcopulatory process.     

The effect of breeding density and male quality on paternity-assurance behaviours in the house sparrow, <Emphasis Type="Italic">Passer domesticus</Emphasis>

Several factors can influence the risk of cuckoldry through extra-pair paternity for male birds. The number of neighbouring males is thought to affect the chance of females engaging in extra-pair copulations, and species which breed both socially (colonially) and solitarily provide an ideal opportunity to test the effect of close proximity on extra-pair behaviour and paternity guards. In this study, the extent to which male house sparrows, Passer domesticus, used two alternative strategies, namely frequent copulation and mate-guarding, to ensure paternity was investigated. We also examined how males vary the two paternity guards according to their breeding sociality. Pairs at the dense colony started to copulate at a higher rate at the beginning of the fertile period than those of the medium-sized colony and solitary breeding pairs. Male house sparrows appear to fine-tune their strategies according to the breeding density. Both strategies are alternatively used in the weak fertile period but are simultaneously used in the peak fertile period. Our results suggest that males modify their strategy according to their individual abilities: mate-guarding intensity was positively correlated with the black breast badge size.