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.     

Mate guarding in the Seychelles warbler is energetically costly and adjusted to paternity risk

Males may increase their fitness through extra-pair copulations (copulations outside the pair bond) that result in extra-pair fertilizations, but also risk lost paternity when they leave their own mate unguarded. The fitness costs of cuckoldry for Seychelles warblers (Acrocephalus sechellensis) are considerable because warblers have a single-egg clutch and, given the short breeding season, no time for a successful replacement clutch. Neighbouring males are the primary threat to a male's genetic paternity. Males minimize their loss of paternity by guarding their mates to prevent them from having extra-pair copulations during their fertile period. Here, I provide experimental evidence that mate-guarding behaviour is energetically costly and that the expression of this trade-off is adjusted to paternity risk (local male density). Free-living males that were induced to reduce mate guarding spent significantly more time foraging and gained significantly better body condition than control males. The larger the reduction in mate guarding, the more pronounced was the increase in foraging and body condition (accounting for food availability). An experimental increase in paternity risk resulted in an increase in mate-guarding intensity and a decrease in foraging and body condition, and vice versa. This is examined using both cross-sectional and longitudinal data. This study on the Seychelles warbler offers experimental evidence that mate guarding is energetically costly and adjusted to paternity risk.     

Age-Related Variation in Mate-Guarding Intensity in the Bluethroat (Luscinia s. svecica)

Female extra‐pair copulations (EPCs) have selected for male paternity guarding strategies in many bird species. In the bluethroat, Luscinia s. svecica, males guard their mates closely during the last 2 d before the start of egg laying, but there is great individual variation in the intensity of mate guarding. Here we show that some of this variation is related to male age. Old males guarded their mates with much lower intensity and sang more than young males, although the latter difference was not statistically significant. Controlling for male age, male and female coloration and size were not significantly related to the intensity of mate guarding. We have previously shown that young and old males had a similar paternity loss in their own broods. On the other hand, old males were far more successful than young males in achieving extra‐pair fertilizations. These patterns suggest that young and old males have different trade‐offs between preventing paternity loss in own nest and gaining paternity in others, because male skills in obtaining EPCs improve with experience and/or because of female preferences for old males as copulation partners. There were no significant relationships between paternity and male mate‐guarding behaviour during the fertile period, indicating that mate guarding is not a very effective paternity‐assurance strategy in the bluethroat.     

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.     

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.     

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.     

Variation in Song Rate during the Breeding Cycle of the Chaffinch,Fringilla coelebs

The variation in song rate during the breeding season was studied in two individually marked chaffinch Fringilla coelebs populations. We gathered data to investigate especially the recently presented mate-guarding hypothesis. The active singing has been supposed to function as a form of mate guarding during the female's fertile period by announcing the high status of the male and preventing extra-pair copulations by neighbouring males. There was no clear dawn chorus in the chaffinch, i.e. a peak in the song rate before sunrise. Male chaffinches continued to sing after mating, but the song rate dropped significantly. In contrast to the mate-guarding hypothesis the song rate was lower during the fertile period of the female than during pre-mating and incubation. Thus, the males do not announce the fertility status of their mates or their own quality and status by active singing. The song does not function as a form of mate guarding in the chaffinch. One function of the song of the chaffinch is mate attraction: singing activity was highest before pair formation in early spring and decreased after mating but increased again if the male lost his mate later in the breeding season.     

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.     

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.     

Testosterone, cuckoldry risk and extra-pair opportunities in the Seychelles warbler

In male birds, testosterone (T) plays an important role in aggressive and mate-attraction behaviour. In the cooperatively breeding Seychelles warbler, Acrocephalus sechellensis, extra-group copulations (EGCs) occur frequently, but are not accompanied by sexual courtship displays as in within-pair copulations. Paternity is nearly always gained by primary males. We investigated whether T levels and sperm storage capability (cloacal protuberance (CP)) in adult primary and subordinate males were related to timing of egg laying, levels of cuckoldry and extra-group paternity (EGP) opportunities. During the sexually active period before egg laying, T levels and CP were only elevated or enlarged (respectively) in primary males, and some suggestion was found that subordinate males do not invest in elevated T levels. The peak in T occurred during the fertile period of the female partner and corresponded to the peak period of male sexual displays and mate guarding, but was independent of cuckoldry risk (density of neighbouring primary males). CP was also enhanced during this period; however, CP but not T remained elevated after egg laying by their mates, and CP but not T was positively related to EGP opportunities (density of neighbouring fertile females). We conclude that T is involved in sexual courtship displays and mate guarding, but not in gaining EGCs. These findings contrast with those in other species where EGP involves elaborate sexual displays.     

Coevolution of female fidelity and male help in populations with alternative reproductive tactics

In socially monogamous species, pair-bonded males often continue to provide care to all offspring in their nests despite some degree of paternity loss due to female extra-pair copulation. Previous theoretical models suggested that females can use their within-pair offspring as ‘hostages'' to blackmail their social mates, so that they continue to provide care to the brood at low levels of cuckoldry. These models, however, rely on the assumption of sufficiently accurate male detection of cuckoldry and the reduction of parental effort in case of suspicion. Therefore, they cannot explain the abundant cases where cuckolded males continue to provide extensive care to the brood. Here we use an analytical population genetics model and an individual-based simulation model to explore the coevolution of female fidelity and male help in populations with two genetically determined alternative reproductive tactics (ARTs): sneakers that achieve paternity solely via extra-pair copulations and bourgeois that form a mating pair and spend some efforts in brood care. We show that when the efficiency of mate guarding is intermediate, the bourgeois males can evolve to ‘specialize'' in providing care by spending more than 90% of time in helping their females while guarding them as much as possible, despite frequent cuckoldry by the sneakers. We also show that when sneakers have tactic-specific adaptations and thus are more competitive than the bourgeois in gaining extra-pair fertilizations, the frequency of sneakers and the degrees of female fidelity and male help can fluctuate in evolutionary cycles. Our theoretical predictions highlight the need for further empirical tests in species with ARTs.     

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.     

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.     

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.     

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.     

Weather conditions affect levels of extra-pair paternity in the reed bunting Emberiza schoeniclus

Extra-pair paternity (EPP) is common in many socially monogamous birds, but large variations in frequency of EPP are found both between and within species. Local ecological factors can affect the costs and benefits of extra-pair mating behaviour, and may therefore influence the chance that individuals engage in extra-pair copulations (EPCs). We investigated the effect of weather conditions during the peak fertile period of the female on the levels of EPP in reed buntings Emberiza schoeniclus . The reed bunting is a socially monogamous passerine, with extremely high levels of EPP (50% of offspring in 80% of broods). We found that higher daily minimum temperatures and more rainfall during the peak fertile period were associated with lower proportions of EPP. As during adverse weather conditions individuals have to invest more in self maintenance, we suggest that during long periods of rain the extra-pair mating behaviour of all individuals will be restricted, leading to lower proportions of EPP. During cold mornings, time-consuming activities such as mate guarding are likely to be more strongly affected than less time-consuming activities such as EPCs, leading to higher proportions of EPP.     

Spatial and Temporal Distribution of Song in the Yellowhammer Emberiza citrinella

The temporal and spatial distribution of song was studied in a population of yellowhammers Emberiza citrinella. Song was most frequent during the breeding season, and within the breeding season during the fertile period of both first, second, and replacement clutches. Song activity peaked at sunrise and sunset. During the fertile period most singing took place in the central parts of the territory. Song post heights peaked during the fertile period, and more song posts lacked foliage at that time. Intrusions by male conspecifics peaked in the fertile period and in territories where males sang relatively little. Song activity and mate guarding were strongly positively correlated. Song volume was loud and song was thus apparently used in long-distance communication. These observations are in accordance with a male deterrence hypothesis, suggesting that males sing to deter neighbouring males from trespassing during the fertile period of their mate. A female attraction hypothesis, suggesting that males sing to attract neighbouring females and thereby obtain extra-pair copulations, and a female reproduction hypothesis, suggesting that males sing to start the female reproductive cycle, were partly supported by observations.     

Genetic monogamy in blue-headed vireos and a comparison with a sympatric vireo with extrapair paternity

Based on the breeding synchrony hypothesis, we predicted, intwo congeners that nest in simiilar habitat but differ in nestingsynchrony, that blue-headed vireos (Vireo solitarius) wouldhave fewer extrapair fertilizations (EPFs) thaii red-eyed vireos(V. olivaceus EPFs were rare in blue-headed vireos (1/37 nestlings),but common in red-eyed vireos (11/19 nestlings). We studiedthe behavior of blue-headed vireos to determine what factorscould promote genetic monogamy. We found no evidence that malesmate guarded to prevent extrapair copulations from occurring.Males did not follow fertile mates closely when mates left thenest (14–25% of female departures) and, during the egg-layingperiod, males were often alone on the nest (22.3 mm/h). Femaleblue-headed vireos, but not red-eyed vireos, obtain direct benefitsfrom social mates such as nest building and incubation (49.1%of the total), and they assess male quality long before becomingfertile. Female blue-headed vireos spent more time incubatingwhen their mates had low incubation effort. Furthermore, maleincubation effort was positively correlated with nest survivalduring incubation. We discuss the evolution of genetic monogamyand sex role convergence in blue-headed vireos in relation toasynchronous breeding.     

Mate switching and copulation behaviour in King Penguins

Extra‐pair paternity (EPP) in monogamous birds may result from either extra‐pair copulations (EPCs) or mate switching. In this study of King Penguins in South Georgia, we observed no EPCs at all, an effect of very efficient mate guarding. Onshore males fast and need not divert attention to foraging or to defending nest or territory, as this species has neither. However, we found that mate switching was common. On average 38% (range: 29%–56%; three years pooled) of the birds established pair bonds with at least one initial partner before switching to the partner they bred with (i.e. the “pair mate”). Of the observed copulations of 44 studied females, 22% were with initial partners and 78% with the pair mate. This and the high proportion of mate switching suggest that roughly 10% of the females could have received sperm from males other than the pair mate. The average copulation frequency was 0.026 h^?1, resulting in an estimated 8.2 copulations per clutch (which consists of one egg). That more copulations than necessary for fertilisation occur suggests that males try to protect paternity by sperm competition, and that this is a result of the potential for EPP due to mate switching in King Penguins. All observed copulations except one took place between days 13 and 5, with the peak 7.5 days prior to egg‐laying. The birds found their pair mates (often not the same as in the previous year) on average about 10 days before egg‐laying, and always established themselves at the outskirts of the colony about 8 days before egg‐laying. Thus, most copulations occurred around the time the birds joined the colony. We suggest that it is adaptive to obtain a breeding spot early, because the colony will grow and pairs joining later will protect the offspring. Additionally, we suggest that early copulation outside the colony is adaptive because of the risk of failing to fertilise the egg when copulating among aggressive neighbours inside the dense colony. Based on these two arguments we suggest a “safe place hypothesis” to explain the early copulation peak in King Penguins.