Territorial intrusions and copulation patterns in red kites, Milvus milvus, in relation to breeding density

Two main paternity assurance strategies are generally found in birds: mate guarding and frequent copulations. The latter is expected particularly in species such as raptors that cannot guard their mates efficiently because of ecological constraints, such as frequent courtship feeding. I investigated the prelaying behaviour of red kites, in which the males courtship feed. I compared pair behaviour in situations of varying breeding density and simulated male territorial intrusions by presenting decoys. Males' certainty of paternity was likely to decrease with increasing breeding density, because of the proximity of other males and more frequent male territorial intrusions during the presumed fertile period. The percentage of time spent by males within their breeding territory during the prelaying period was positively related to the number of close breeding neighbours, suggesting territory surveillance and mate guarding. The kites copulated frequently and over a long period. Copulation frequency prior to and during laying increased with breeding density, and in isolated pairs in response to simulated male territorial intrusions. The results support the idea of paternity assurance through frequent copulations during the presumed fertile period of the female, and suggest that early copulation activity is related to functions other than fertilization, such as pair bonding or mate assessment. Copyright 2000 The Association for the Study of Animal Behaviour.     

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.     

Factors influencing mate guarding and territory defence in the stitchbird (hihi)

Socially monogamous male birds are predicted to maximise their reproductive success by pursuing extra-pair copulations (EPCs) while engaging in anti-cuckoldry behaviour such as mate guarding. In the stitchbird, Notiomystis cincta, high levels of forced EPCs and a high proportion of nestlings resulting from extra- pair fertilisations lead to the prediction that males of this species should exhibit intense paternity guarding behaviours. While studying an isolated stitchbird population on Tiritiri Matangi Island New Zealand (3636'S, 17453'E), I collected daily behavioural data throughout the breeding season from 15 males in 2000/01 and 27 males in 2001/02. In this study, male stitchbirds demonstrated clear paternity guarding by exhibiting: (1) an increased likelihood of being close to their mate during her fertile period, (2) an increased initiation of mate contact during her fertile period, (3) switching from site-specific territorial defence during the pre-fertile period to defending an area centring on the their female partners location during her fertile period, and (4) an increased following of the female to communal feeding sites outside the territory during her fertile period. For polygynous males, mate guarding and territorial defence were conditional on which of their females was fertile. Additional evidence supporting the hypothesis that mate guarding in this species is a form of paternity assurance, rather than protection from harassment, is that males protected their partner from harassment by other stitchbird males but did not intervene when females were harassed by male bellbirds, Anthornis melanura. While mate-guarding intensity in many species is conditional on the stage of female fertility, male stitchbirds also modified their behaviour depending on the location of the female and the rate of intrusions by extra-pair males. Resident males adopted a best-of-a-bad-job tactic when they were unable to locate their female by defending an area around her last known location. Furthermore, when the rate of intrusions by extra-pair males increased they traded-off the area they could defend within their territory against their ability to guard the female. Territory takeovers were uncommon, but when they did occur older males displaced younger males and healthy birds displaced sick ones. Contrary to the prevailing view that mate guarding is a male response to female infidelity, male stitchbirds appear to use mate guarding primarily to prevent paternity losses from forced EPCs. Future assessments of mate guarding function should consider the possibility that mate guarding involves a combination of conflict and co-operation between the sexes.     

Males of a single-brooded tropical bird species do not show increases in testosterone during social challenges

The challenge hypothesis poses that in socially monogamous vertebrates, males increase circulating testosterone in response to aggressive challenges to promote intense and persistent aggression. However, in bird species that raise only a single brood during short breeding seasons as well as those with essential male parental care, males lack the well-documented testosterone response to social challenges. We tested male behavioral and hormonal responses to social challenges in a neotropical bird species, the buff-breasted wren (Thryothorus leucotis), which is single-brooded with extensive male parental care, but in contrast to most species studied to date, has a long breeding season. We presented live female, male, and paired decoys with song playback for 30 min during pre-breeding and breeding periods. Males responded aggressively to all intruders, but male decoys elicited somewhat weaker responses overall. Responses to female decoys were most intense during pre-breeding, whereas pair decoys elicited stronger responses at breeding. Plasma testosterone concentrations did not differ between challenged and unchallenged males, or among males exposed to different decoys or during different seasons. Plasma corticosterone in pre-breeding males was higher in challenged than unchallenged males and varied positively with the duration of social challenge. Circulating dehydroepiandrosterone concentrations were similar in challenged and unchallenged males, but correlated positively with the proportion of time males spent in close proximity to the decoy. Both testosterone and corticosterone results support recent findings, suggesting that brood number and essential male care, but not breeding-season length, may be important determinants of male hormonal responsiveness during aggressive interactions.     

Territoriality as a paternity guard in the European robin, Erithacus rubecula

To investigate the relative importance of paternity defences in the European robin we used behavioural observations, simulated intrusions and temporary male removal experiments. Given that paired males did not increase their mate attendance, copulation rate or territory size during the female's fertile period, the most frequently quoted paternity assurance strategies in birds were absent. However, males with fertile females sang and patrolled their territories more regularly, suggesting that territorial motivation and vigilance were elevated when the risk of cuckoldry was greatest. In addition, there was a significant effect of breeding period on response to simulated intrusions: residents approached and attacked freeze-dried mounts more readily in the fertile period. During 90-min removals of the pair male in the fertile period, neighbours trespassed more frequently relative to prefertile and fertile period controls and appeared to seek copulations with unattended females. When replaced on their territories, males immediately increased both song rate and patrolling rate in comparison with controls. We propose that male robins sing to signal their presence, and increase their territorial vigilance and aggression in the fertile period to protect paternity. Copyright 2000 The Association for the Study of Animal Behaviour.     

Conflict between sexes in the water strider, Gerris lacustris: a test of two hypotheses for male guarding behavior

We studied the effect of operational sex ratio on female reluctanceand male persistence to mate as well as on the length of copulationand postcopulatory guarding in Gerris lacustris by adding fivesurplus males or females to the basin with a pair in tandem.In the control treatment, a pair alone was tested. Accordingto the copulatory guarding hypothesis (CGH), males should prolongmating and guard females in the presence of surplus males. Accordingto the convenience polyandry hypothesis (CPH), females shouldshow lower levels of resistance to prolonged mating in the presenceof surplus males because the mating male protects the femaleagainst harassment from other males. As expected on the basisof both the CGH and CPH, mating (copulation + guarding) averagedlonger in the male-biased treatment. The behavior of males andfemales during mating suggested that both hypotheses hold true:females showed less resistance to prolonged mating (as predictedfrom CPH), and male behavior suggested stronger efforts to stayon the female when surplus males were present (as predictedfrom CGH). Comparisons of the treatment with surplus femaleswith the results from the mating pair without surplus individualssuggested that the capabilities of water striders in tandemto assess the sex of nearby nonmating striders are limited.     

Breeding density, cuckoldry risk and copulation behaviour during the fertile period in raptors: a comparative analysis

Extrapair copulations (EPCs) and fertilizations (EPFs) occur in many socially monogamous bird species, including raptors. In this group of species, males invest heavily in reproduction through the feeding of female and young, so the cost of cuckoldry is particularly high. The feeding of females by males, characteristic of most species, conflicts with mate guarding, so raptors are expected to use frequent within-pair copulations (WPCs) for paternity assurance. In this study, I reviewed information on copulation behaviour of diurnal raptors, and used regression analyses and phylogenetic comparative analyses to investigate relations between density, EPC frequency and WPC behaviour. EPCs occurred in most raptor species studied (68%, N=19), mostly during the presumed fertile period of females. EPC frequency, measured as the percentage of females engaging in EPC but not the percentage of extrapair copulations, was positively related to breeding density. The rate and relative duration of WPCs were also positively related to breeding density, but only WPC rate was positively related to EPC frequency (percentage of females). Frequently copulating species had relatively larger testes, underlying higher sperm production capacities. The results support the hypotheses that sperm competition intensity increases with breeding density, and that male raptors rely on frequent copulations to ensure paternity. Despite the risk, EPFs rarely occurred in raptors, suggesting efficient paternity guards.     

Part-Time Mate Guarding Affects Paternity in Male Reed Buntings (Emberiza schoeniclus)

Male mate guarding by close following has been reported in many socially monogamous bird species and is generally believed to function as a paternity guard. Many aspects of the dynamics and effectiveness of this behavior are still however poorly understood. Here, we describe the temporal variation in mate guarding behavior in male reed buntings (Emberiza schoeniclus) with a particular focus on how males allocate their mating effort between mate guarding and extrapair mating in a context of intense sperm competition. In our highly synchronous study population most males have to balance the simultaneous and mutually exclusive demands of mate guarding and seeking extrapair copulations (EPCs). We found that males frequently switched between guarding their mates and performing intrusions to neighboring territories. Both activities seemed to have significant fitness payoffs, as male mate guarding effort had a positive effect on paternity, and a large fraction of extrapair fertilizations occurred during the days when the sire guarded its own female. The reed bunting is thus an example of how discontinuous or part‐time mate guarding can still be effective in securing paternity. Female reed buntings were not particularly active in initiating EPCs as they never were observed performing extraterritorial forays. We argue that the absence of female‐initiated EPCs is a prerequisite for males to trade mate guarding against seeking EPCs. Otherwise, if females circumvent male mate guarding by timing their EPCs to periods of male absence, males should guard their mates almost continuously or rely on alternative paternity guards.     

Adaptive significance of permanent female mimicry in a bird of prey

Permanent female mimicry, in which adult males express a female phenotype, is known only from two bird species. A likely benefit of female mimicry is reduced intrasexual competition, allowing female-like males to access breeding resources while avoiding costly fights with typical territorial males. We tested this hypothesis in a population of marsh harriers Circus aeruginosus in which approximately 40 per cent of sexually mature males exhibit a permanent, i.e. lifelong, female plumage phenotype. Using simulated territorial intrusions, we measured aggressive responses of breeding males towards conspecific decoys of females, female-like males and typical males. We show that aggressive responses varied with both the type of decoys and the type of defending male. Typical males were aggressive towards typical male decoys more than they were towards female-like male decoys; female-like male decoys were attacked at a rate similar to that of female decoys. By contrast, female-like males tolerated male decoys (both typical and female-like) and directed their aggression towards female decoys. Thus, agonistic responses were intrasexual in typical males but intersexual in female-like males, indicating that the latter not only look like females but also behave like them when defending breeding resources. When intrasexual aggression is high, permanent female mimicry is arguably adaptive and could be seen as a permanent 'non-aggression pact' with other males.     

Female aggressiveness towards female decoys decreases with mate T level in the pied flycatcher

Social selection is expected to favour the evolution of female aggressive defence of nesting resources in cavity-nesting birds, which may be also mediated by testosterone (T) levels. Male T levels could express male dominance and thereby territorial safety for female partners and thereby reduce their need for aggressive defence. Here, we explored the role of T levels in female-female competition in a songbird, the pied flycatcher Ficedula hypoleuca. In an experiment with female decoys placed close to the nestbox at the end of laying, we explored if female aggressiveness is related to their own T level or to mate T level. T levels of males and females were measured in the middle of the nestling period. Mean female aggressiveness towards decoys in three presentations was estimated through proximity to the decoy and number of attacks by females, two variables which were positively associated. Aggressiveness by female nest owners to female decoys was negatively related to male T level but unrelated to own T level. There was no assortative mating with respect to T level. Female aggressiveness is more strongly related to the hormonal status of mates than to their own.     

Delayed copulation as a means of female choice by the hermit crab Pagurus filholi

Male hermit crabs perform precopulatory mate-guarding behavior during their reproductive season. As females generally cannot reject guarding attempts by males, male guarding prevents females from inspecting and choosing other male mates. However, as guarding males are often replaced by other males through competition for females during the guarding phase, females may be able to select males by delaying their copulation. To examine the possibility of female choice by hermit crabs, we investigated whether female Pagurus filholi that were being guarded in the field were ready to copulate and spawn. We found that about 30% of females guarded in the field were ready to spawn, indicating that guarded females delayed copulation with their current male. Our results suggest that by delaying copulation females may exploit male–male competition to choose dominant males. However, delaying copulation reduced the spawning potential of females. Hence, there is a trade-off between waiting for the opportunity to mate with a dominant male and decreased spawning success if females exploit male–male competition.     

Context matters: female aggression and testosterone in a year-round territorial neotropical songbird (Thryothorus leucotis)

Testosterone promotes aggressive behaviour in male vertebrates during the breeding season, but the importance of testosterone in female aggression remains unclear. Testosterone has both beneficial and detrimental effects on behaviour and physiology, prompting the hypothesis that selection favours an association between aggression and testosterone only in certain contexts in which intense or persistent aggression may be beneficial. We tested this hypothesis in a year-round territorial female buff-breasted wrens (Thryothorus leucotis), by exposing free-living females to experimental intrusions in different social (either single female or male, or paired decoys) and seasonal (pre-breeding or breeding) contexts. Females responded more aggressively to intrusions by females and pairs than to males. However, female intrusions elicited stronger responses during pre-breeding, whereas responses to pair intrusions were more intense during breeding. Territorial females had elevated testosterone levels after female intrusions and intermediate levels after pair intrusions during pre-breeding, but the levels of testosterone remained low after these intrusions during breeding. These results demonstrate seasonal differences in circulating testosterone following territorial aggression in female buff-breasted wrens and are suggestive of differences according to social context as well. Context-dependent elevation of testosterone implies that selection acts directly on female vertebrates to shape patterns of testosterone secretion.     

Prolonged copulation, sperm reserves and sperm competition in the Aquatic Warbler Acrocephalus paludicola

The Aquatic Warbler Acrocephalus paludicola has a quasi-promiscuous mating system with high levels of multiple paternity and, thus, intense sperm competition. The duration of copulation in the Aquatic Warbler is unusually long. In hand-reared, captive birds the duration of mounting was 23.7 ± 11.8 min (mean ± s.d.). On average, six cloacal contacts (inseminations) occurred during each copulation. Between inseminations the male remained in contact with the female, either on top of or directly behind her. Protracted copulation may be a form of contact mate guarding, a behaviour not previously recorded in birds. Copulation was most frequent during the evening and early morning. Male Aquatic Warblers also exhibit extreme morphological adaptations of their reproductive system compared with other Acrocephalus species and other birds: their testes, cloacal protuberance and seminal glomera (which contain 198 × 10⁶ spermatozoa) are all relatively large. Frequent insemination during protracted copulation and contact mate guarding may be alternatives to paternity guarding found in other birds.     

Genetic monogamy in the absence of paternity guards: the Capricorn silvereye, Zosterops lateralis chlorocephalus, on Heron Island

We investigated the genetic mating system of a socially monogamous passerine bird, the Capricorn silvereye Zosterops lateralis chlorocephalus, on an island of the Great Barrier Reef. Therewere no cases of extrapair paternity (EPP) among 122 offspringfrom 53 broods detectable by minisatellite or microsatelliteDNA fingerprinting. Behavioral observations of paired birdsshowed that this was not a consequence of efficacious paternityguards and that females did not engage in extrapair copulation(EPC). Frequency of intrapair copulations was also low, withonly 14 cases observed during 199 hours of observations ofthe 11 focal pairs in the fertile periods of females, and thiswas consistent with anatomical features of the cloacal protuberancein males. In this population, young birds form life-time pairbonds soon after gaining independence but females are obviouslynot attempting EPC possibly to redress this early mate choice.This is despite the fact that they breed in high density witha synchronous start and asynchronous spread of laying in aprotracted season and males do not positively exhibit mateguarding behavior when females are fertile. Our results supporthigh fidelity of socially monogamous birds on islands and are consistent with the hypothesis that sexual selection is reducedwhere genetic variation in fitness is limited.     

Experimentally Simulating Paternity Uncertainty: Immediate and Long-Term Responses of Male and Female Reed Warblers Acrocephalus scirpaceus

In many socially monogamous species, both sexes seek copulation outside the pair bond in order to increase their reproductive success. In response, males adopt counter-strategies to combat the risk of losing paternity. However, no study so far has tried to experimentally prove the function of behaviour for paternity assurance. Introducing a potential extra-pair partner during the female fertile period provides a standardised method to examine how pair members respond immediately (e.g. increase mate guarding or copulation frequency) or long term (e.g. later parental investment and paternity uncertainty). In this study on a socially monogamous passerine species, we experimentally confronted pairs of reed warblers with a conspecific male (caged male simulating an intruder) during egg-laying. Our results revealed that occurrence of an intruder during that period triggered aggression against the intruder, depending on the presence of the female. The male territory owner also attacked the female partner to drive her away from the intruder. Thus territory defence in reed warblers also serves to protect paternity. The increase in paternity uncertainty did not affect later paternal investment. Paternal investment was also independent of the actual paternity losses. In females, the experiment elicited both, immediate and long-term responses. E.g. female copulation solicitations during the intruder experiment were only observed for females which later turned out to have extra-pair chicks in their nest. In relation to long term response females faced with an intruder invested later less in offspring feeding, and had less extra-pair chicks in their nests. Extra-pair paternity also seems to be affected by female quality (body size). In conclusion female reed warblers seem to seek extra-pair fertilizations but we could demonstrate that males adopt paternity assurance tactics which seems to efficiently help them to reduce paternity uncertainty.     

The causes of mating abstention in male tsetse flies Glossina morsitans

ABSTRACT. The sexual response of a Glossina morsitans morsitans Westw. male towards a decoy consisting of a dead male dosed with synthetic sex pheromone, was depressed by the presence of the cuticular lipids of the decoy male. However, addition of a C24 paraffin, not normally found on or in the cuticle of male or female G.m.morsitans , to a decoy male from which cuticular lipids were removed had a similar effect. Addition of either the C24 paraffin or an extract of male cuticular lipids to decoy females which possess natural sex pheromone in their cuticles, again depressed the sexual responses of males towards the decoys. The n-hexane solvent used in the application of compounds to decoys, itself depressed responses towards natural pheromone on a dead female at volumes in excess of 100μl, presumably because it mixed the surface waxes which masked the pheromone. Occlusion experiments implied that sex pheromone receptors are present on both the tarsi and tibiae of the male. No evidence was found for the existence of a specific mating deterrent on or in the cuticle of male G.m. morsitans.     

Do male paternity guards ensure female fidelity in a duetting fairy-wren?

Most socially monogamous bird species engage in extra-pair mating,and consequently males may adopt various behavioral strategiesto guard paternity. However, the relationship between mate guardingand extra-pair paternity is unclear: low levels of extra-pairpaternity can be associated either with no mate guarding orwith intense mate guarding. We investigate paternity guardsin the purple-crowned fairy-wren (Malurus coronatus), a duettingspecies where extra-pair paternity is rare. This species isunusual in a genus known for extremely high levels of extra-pairmating. We examine the behavioral interactions between the sexesunderlying these low rates of extra-pair paternity and showthat male purple-crowned fairy-wrens do not use frequent copulationor courtship feeding to assure paternity or guard females acousticallyby duetting. Males maintain close proximity to females bothwhen they are fertile and when they are not breeding and donot invest in courtship displays to extra-pair females. Consistentwith predictions of theoretical models, low extra-pair paternityin this species may be related to female fidelity rather thanmale paternity assurance strategies, but short-term removalof males would be necessary to test this experimentally.     

The effectiveness of mate guarding by male black-throated blue warblers

In many socially monogamous birds, males maintain close proximityto their mates during the fertile period. This is often consideredan effort on the male's part to prevent other males from copulatingwith his mate, but other functions have been suggested andthe effectiveness of males in preventing extrapair fertilizationshas come into question. Moreover, it is unclear whether mateguarding conflicts with other male activities, particularlythe pursuit of extrapair fertilizations. We examined mate guardingby male black-throated blue warblers (Dendroica caerulescens).Behavioral observations showed that males that guarded theirmates more closely were less likely to have extrapair youngin their nests. Moreover, the experimental detention of a malefor 1 h during the fertility risk period increased the probabilitythat a brood would contain extrapair young. Thus, male mate guarding was effective in reducing the risk of extrapair fertilization.Males with many opportunities for extrapair copulations appearedto guard their mates less and consequently had more extrapairyoung in their broods than males with few such opportunities.This suggests that mate guarding may conflict with the pursuitof extrapair fertilizations.     

Effects of territorial intrusions, courtship feedings and mate fidelity on the copulation behaviour of the osprey

We studied copulation behaviour of the osprey, Pandion haliaetus, a semicolonial, fish-eating raptor, in Corsica (Mediterranean). Pairs copulated over a long period (45 days) and at a high rate, with, on average, 288 within-pair copulations (WPCs) for a clutch. Pairs breeding at higher density faced more frequent territorial intrusions than others and were potentially at an increased cuckoldry risk. However, and contrary to predictions of the ‘paternity assurance’ hypothesis for frequent copulations, we found that WPC rate decreased with increasing frequency of territorial intrusions. Male territory attendance increased with territorial intrusion frequency, to the detriment of the food provisioning of the female. Both attempted and successful WPC rates were positively related to the amount of food delivered by the male. Thus, the more frequent the territorial intrusions, the more time the male spent within his territory, the less he courtship fed and the smaller the fish he delivered, and the less the pair copulated successfully. WPC rate was also higher in newly formed pairs than in established pairs, and decreased with increasing pair bond length. The results suggest that males rely on mate guarding rather than frequent copulations to ensure paternity, and do not support the idea that sperm competition is the main cause of frequent WPCs. Nonfertilization functions of frequent copulations, such as pair bonding, mate assessment and mate retention, were likely early in the prelaying period. The findings that WPC rate decreased with mate fidelity and that females traded copulations for food suggest that mate retention was a possible function of frequent copulations in this species. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

The roles of vision and olfaction in mate location by males of the tsetse fly Glossina morsitans morsitans

The roles of visual and/or olfactory stimuli in eliciting mating responses from male Glossina morsitans morsitans Westwood were examined, using a system for automatically recording the number and duration of mating strikes made towards decoys, under controlled conditions. The results confirm that there is no olfactory component of the female sex recognition pheromone sensed by the male antennae, and the attraction of males to females appears to be visual. The absence of male-male mating strikes was the result of the absence of female sex-pheromone, rather than the presence of a repellent mating deterrent in the male cuticle. Experiments with coloured, artificial, sex-pheromone-dosed, cotton decoys showed that colour had only weak effects on attractiveness and number of encounters with decoys, and that no colour caused significant enhancement of mating responses over those shown to decoy females.