Mate guarding in the swallowHirundo rustica

Summary The importance of mate guarding by males in the monogamous swallowHirundo rustica was studied by temporarily detaining the males. Mate guarding reduced the frequency of extra-pair copulations and of sexual chases involving female mates. Males participated in sexual chases more frequently if they had a non-fertile female. Neighbouring males of ‘widowed’ females increased their own mate guarding presumably in response to the experimentally increased rate of sexual chases. Neighbouring males with a fertile female increased their mate guarding more than did males with a non-fertile female. Addition of eggs to swallow nests in the post-fledging period of the first brood induced mate guarding by male nest owners. These males also copulated more frequently with their mates than did control males. Neighbouring male swallows responded to the increased mate guarding by showing sexual interest in the guarded females. removal of eggs from swallow nests during the laying period, leaving only one egg in the nest, resulted in reduced nest attendance by females. Male mates responded by increasing their mate guarding intensity as compared to controls, and neighbouring males showed an increased sexual interest in these females.     

Non-aggressive mate guarding by the blue-footed booby: a balance of female and male control

Thirteen pairs of blue-footed boobies (Sula nebouxii) were observed on their colony. Pairs courted frequently and, on average, copulated 24 times during the 30 days before laying, with 38% of those copulations occurring in the last 5 days (presumed fertile period). Males and females increased attendance at the nest site as laying approached. Seven females performed an average seven extra-pair copulations, with 1–2 paired male neighbors, but these were less concentrated in the presumed fertile period than within-pair copulations, and the last two copulations of all 7 females were with their social mates. Rates of female extra-pair copulations were six times lower when their social mate was present, and during the presumed fertile period, no female performed an extra-pair copulation in the presence of her mate. Males did not respond to infidelity of social mates with aggression, prompt copulation, retaliatory copulation, or increase in copulation. Seven of 13 males performed an average of five extra-pair copulations, with 1–3 paired female neighbors, before their own mates began egg-laying. The males' extra-pair copulations represented only 4% of their total copulations during their own mates' presumed fertile periods. Females, the larger sex, apparently control sexual access and copulate with extra males to achieve extra-pair fertilization. Males pursue a mixed strategy: they copulate with extra females, mostly outside their own mate's presumed fertile period, and they copulate increasingly with their social mate as laying approaches, probably assuring some paternity by mate guarding, involving attendance and courtship. Behavior of males and females is also consistent with other hypotheses for extensive joint nest site attendance: pairbonding, copulation access, and territory acquisition. Received: 14 November 1997 / Accepted after revision: 16 May 1998     

Female control of extra-pair fertilization in tree swallows

Summary In a Canadian population of tree swallows, Tachycineta bicolor, DNA fingerprinting has previously shown that half of all broods contain many offspring resulting from extra-pair copulations (EPCs), whereas the other half contain only legitimate offspring. This bimodal pattern of extra-pair paternity might be due to variation in the effectiveness of male paternity guards, variation in female ability to resist EPCs, and/or variation in female pursuit of EPCs. Here we report experimental evidence for female control of copulations and fertilizations and the occurrence of two alternative copulation strategies among females in this population. Ten paired male tree swallows were removed on the day their mates laid the first egg. Replacement males took over the nestbox within 0.5–23 h and attempted to copulate with the widowed female. Assuming that eggs were fertilized approximately 24 h prior to laying, the first two eggs were fertilized before the male was removed, while the third and subsequent eggs could potentially be fertilized by the replacement male. Fingerprinting revealed that the first two eggs were sired by the resident males in five nests and by extra-pair males in the remaining five nests. The widows that had been faithful to their initially chosen mate rejected copulation attempts by the replacement male until most of the eggs had been laid. Consequently, nearly all eggs laid by these females were sired by the original male. The widows that had been unfaithful prior to male removal copulated sooner with the replacement male than females that were faithful to their mate. However, these replacement males also had a very low fertilization success; most eggs were sired by males that were not associated with the nest. This is consistent with the situation in non-experimental nests where unfaithful females copulate with their mate at the same rate as faithful females, yet unfaithful females have a majority of offspring sired by extra-pair males. We conclude that fertilization patterns to a large extent are determined by the female through active selection and rejection of copulation partners, though our results also allow some speculation that females have control over sperm competition. Female copulation tactics are probably determined some currently unknown fitness benefits of having the offspring sired by particular males.Correspondence to: Raleigh J. Robertson     

Mate guarding and copulation behaviour in monogamous and polygynous blue tits: do males follow a best-of-a-bad-job strategy?

This study investigates the importance of mate guarding for males and females in the facultatively polygynous blue tit Parus caeruleus. We present observational data in combination with a paternity analysis using DNA fingerprinting to show that (1) male blue tits guard their mate, since they stay closer to their mate, initiate fewer flights and follow their mate more often during the female's presumed fertile period; (2) polygynous males do not suffer more from lost paternity despite lower mate guarding; (3) in monogamous pairs there is either no relation or a positive relation (depending upon the variable measured) between measures of mate guarding intensity and the proportion of extra-pair young in the nest; and (4) monogamous males that are more often followed by their fertile female suffered less from lost paternity. We conclude that, despite mate guarding, paternity seems to be largely under female control and unattractive males guarding their mate are making the best of a bad situation. Experimental evidence is provided showing that when males were temporarily removed from their territory, their mate suffered from increased harassment from neighbouring males that intruded in the territory and tried to copulate with the female. Almost all of these copulation attempts were unsuccessful because females refused to copulate. We conclude that mate guarding may be beneficial for females because harassment by neigbouring males is prevented.     

Female reactions to male absence after pairing in the pied flycatcher

Mating with an already mated pied flycatcher (Ficedula hypoleuca) male is costly for a female. Two hypotheses explain why some females still mate with already mated males. The deception hypothesis suggests that some females mate with already mated males since it is difficult to assess perfectly the mating status of a male with separate territories (polyterritoriality). The search cost hypothesis states that females are aware of male mating status but the costs of searching for an unmated male exceed costs associated with the status of secondary female. One potential cue that could disclose a male's mating status is the existence of brief visits to the primary territory by polyterritorial males. To mimic such visits I removed the male from the territory for 60 min soon after female settlement. Only few females abandoned their mates as a consequence of male removal even though they had available unmated males close by. This result is most consistent with the deception hypothesis. Females did not use occasional male absence as a cue to avoid presumably polyterritorial males and in this respect they were not perfect in assessing males.     

Multiple mating in a lekking bird: why do peahens mate with more than one male and with the same male more than once?

Summary Approximately 50% of marked peahens (Pavo cristatus) mate more than once with lek males. Some females mate with more than one male, others copulate repeatedly with the same male. The frequency of courtship also shows marked variation. Some females repeatedly engage males in courtship interactions after they have succesfully copulated with them. The likelihood of mating with more than one male increases if a female first mates with a non-preferred (unsuccessful male). There is a non-significant tendency for females to copulate with a more successful male when remating. Peahens may mate with a non-preferred male first if they do not encounter a successful male during their initial period of choice, perhaps because the most successful male on a lek was courting another female and/or was defended by another female. There are more aggressive interactions between females in front of preferred males. Preferred males receive more repetitive courtship behaviour and repeated matings. Dominant females are more likely to engage in repetitive courtship and matings. The number of times a female initiates courtship on any one day increases with the number of other females actively courting males at a lek site on that day. We suggest that there is competition amongst females for access to preferred males and that dominant females try to monopolise these males by repeatedly engaging them in courtship interactions. We discuss the implications of these observations for the idea that female may gain directly from mate choice in a species where males contribute nothing but gametes to their offspring. Correspondence to: M. Petrie at the present address     

Deceptive behavior in pied flycatchers

Summary One explanation for polygyny in pied flycatchers (Ficedula hypoleuca) is the deception hypothesis, which proposes that females mate with already-mated males only because they are unaware that such males already have a mate on another territory. Recently this hypothesis has been criticized on the grounds that already-mated and unmated males differ sufficiently in their behavior that human observers can discriminate between the two classes fairly easily. Here we test whether male pied flycatchers change their behavior when visited by a female so as to make this discrimination more difficult. In our experiments we presented a caged female near the nestbox of an advertising male, in order to mimic the situation in which a female investigates the male and his nest site. During control periods, when only an empty cage was presented, we found that already-mated males were present on their secondary territories significantly less and sang significantly less than unmated males on their primary territories, confirming the earlier results. When we presented the stimulus female, all behaviors we measured changed significantly relative to control periods for both mated and unmated males: both classes of males increased the time spent on the territory, decreased singing rates, and increased various courtship behaviors. During the experimental periods there were no significant differences between mated and unmated males on any of the behavioral measures. Discriminant analysis was more successful in classifying males as to mating status using data from the control periods (without female) than using data from the experimental periods (with female). We conclude that when a female is present male pied flycatchers change their behavior in ways that make it more difficult to discriminate mated from unmated males.Offprint requests to: W.A. Searcy     

Multiple mate choice criteria and the importance of age for male mating success in the microhylid frog, Cophixalus ornatus

We examined multiple mate choice criteria in Cophixalus ornatus, a terrestrial breeding, microhylid frog. Mate choice consisted of three stages: mate attraction (male calling), courtship (male behavior between the call site and the nest), and nest site selection by the female. For male C. ornatus, the possession of a call with low dominant frequency relative to calling neighbors increased the probability that they would attract females. Dominant frequency was negatively correlated with age independent of male mass and snout vent length. When escorting the female from the call site to their nest, males traveled along more convoluted paths than when returning to the nest alone. The convolution of the path was, therefore, considered an aspect of courtship. Females released eggs into nests with structural characteristics typical of nests constructed by older males. Thus, females increased their chances of locating an acceptable nest by preferentially approaching males with lower dominant frequencies. This study is the first to demonstrate that age, independent of mass or snout-vent length, can influence call characteristics in anurans, and it is also the first to demonstrate the importance of male age to female mate choice in an amphibian.     

Alternative mating strategies in the water strider Gerris elongatus (Heteroptera,Gerridae)

Summary Males of the water strider Gerris elongatus established territories which included copulation and oviposition sites (small pieces of fallen bamboo). Males were aggressive and competition for territory and females was observed frequently. Male midlegs were more developed than female midlegs and were used as weapons. Reproductive behaviour changed as the breeding season advanced. Early in the season immature females were attracted by male surface wave courtship signals, then copulated white floating on the water surface without ovipositing (type 1). In midseason, males established territories, produced calling signals and attracted females which copulated and oviposited there with male postcopulatory guarding (type 2). In late season, many females oviposited without postcopulatory guarding on pondweed mats near fallen bamboo. Non-territorial males waiter for the arrival of these females and copulated without courtship, but mating success was low (type 3). These alternative mating strategies appeared to depend on differences in male size. Larger males were superior to smaller males in many ways (establishing territory, fighting, mating etc.). The largest males defended territories and had higher mating success than small non-territorial males. Medium sized males used all three strategies according to the number of empty territories and seasonal femald distribution.     

Effect of female molt stage and sex ratio on courtship behavior of the blue crab Callinectes sapidus

In many species, males and females actively participate in courtship, and the outcome of pre-mating interactions influences the mating success of both sexes. Female blue crabs, Callinectes sapidus, mate soon after their final molt to maturity; thus female molt stage dictates the timing of mating. In a field experiment, we manipulated female molt stage and sex ratio to test their effects on the courtship behavior of both sexes, if female behavior influences the behavior and pairing success of males, and if male courtship influences male pairing-success. Early-molt-stage females avoided males during courtship, whereas late-molt-stage females sought out males. As a result, males had to pursue and capture early-molt-stage females whereas males displayed to late-molt-stage females and more easily physically controlled them. Males sometimes abandoned late-molt-stage females, but this occurred more often when females were abundant. The rate at which females avoided males was positively correlated with that of males abandoning females, and males that were unsuccessful at pairing met with higher rates of female resistance than successful males, suggesting that female behavior influences male pairing-success. Unlike unsuccessful males, successful males more often made the transition between display and maintaining physical control of the female. At high male sex ratios, males initiated courtship more readily; thus both sexual competition and female behavior influence male courtship in this species. Received: 7 July 1996 / Accepted: 10 January 1998     

Female lizards discriminate between potential reproductive partners using multiple male traits when territory cues are absent

Female choice can powerfully influence the evolution of male phenotypes. In territorial species, it is challenging to determine the targets of female choice because male traits (e.g., behavior and morphology) are often correlated with territory. We sought to elucidate if and how females specifically evaluate male traits in a territorial species. In this study, we presented female fence lizards, Sceloporus undulatus, with two potential mates to examine mate choice in the absence of territory cues. Females associated more with males possessing better body condition, longer heads, and wider throat badges, and that performed more shudder behavior, which females responded to by approaching shuddering males and performing push-ups. A post hoc decision tree analysis suggests that the strongest predictor of female association was an overall quality index that incorporates all of these traits, rather than individual traits. Male snout–vent length, head width, abdominal badge width, and push-up behavior did not affect female association. Further research on why these traits, which are known to correlate with fitness, do not appear to be used by females when selecting mates would improve our understanding of the evolution of male traits. Our study reveals that females of this territorial species possess the ability to use multiple male traits interactively to make fitness-relevant mate choice decisions in the absence of direct territory cues.     

Multiple paternity in meadow voles (Microtus pennsylvanicus): investigating the role of the female

Multiple paternity in single litters conceived in the wild was recently demonstrated in meadow voles (Microtuspennsylvanicus). In this study, we used an experimental approach (males tethered and females allowed to mate freely with one or several males) to investigate the role of female meadow voles in multiple paternity. We found that among 29 (of 39) females that copulated during our experiment, 79.3% chose to mate with more than one male. Female behavior in meadow voles thus clearly promotes multiple paternity and their role is an active one. Some of the hypotheses explaining promiscuity in meadow voles should be reconsidered in light of this result. We do not know the primary determinant of female mate choice, but male body mass played a secondary role in driving female preferences. The partial dependence between male body mass and female choice, coupled with the active role played by females, indicates that intersexual selection has the potential for reinforcing the effects of intrasexual selection (male-male dominance relationships) in this species. Finally, we demonstrate that the time period over which tests are conducted is an important part of the design of experiments aimed at understanding the role of females in multiple paternity. Received: 14 April 1998 / Accepted after revision: 12 September 1998     

Does female aggression prevent polygyny? An experiment with pied flycatchers (Ficedula hypoleuca)

The female aggression hypothesis states that resident females may be able to prevent polygyny by behaving aggressively towards intruding females. A critical test of the hypothesis is to provide prospecting females with a choice between displaying mated males some of which have initial mates with artificially reduced levels of aggressiveness. Here we present a mate choice experiment on pied flycatchers Ficedula hypoleuca. The species is a cavity nester, and resident females were prevented from behaving aggressively by enclosing them within their own nestboxes: narrowing the entrance hole so that they could not escape but could still let their head out and have some contact with their mate. This treament had only a minor influence on male behaviour. We studied whether the experimental males were better able to attract a new female than a control group of mated males. Four predictions from the female aggression hypothesis were supported. (1) Mating success of control males was positively related to the distance between their primary and secondary territory. (2) For experimental males, mating success was unrelated to interterritorial distance. (3) Experimental males had higher mating success than control males when the interterritorial distance was short but (4) not when it was long. Experimental males had much lower mating success than unmated males, as would be expected if prospecting females are able to discover male mating status from cues other than visits by primary females to their mates' secondary nest sites. Received: 5 January 1998 / Accepted after revision: 30 December 1998     

Parental care sex differences in the brown bullhead,Ictalurus nebulosus (Pisces,Ictaluridae)

Summary Males were the principal care-givers in the brown bullhead, Ictalurus nebulosus. Direct observations on individually tagged adults in nature revealed that males attended broods at closer distances than females and were the most frequent lone care-givers. However, females often participated in parental care and in some cases assumed the typical male role in the absence of the male. In the presence of her mate, females generally performed different care-giving functions than males. Females attended broods at a distance and chased other fishes more frequently than males. Males remained directly over the brood guarding. A series of mated pairs in each of three reproductive conditions were captured and examined. Different pairs were compared between reproductive conditions for body weight, body condition, gonadal-somatic index, and a gut-contents index. The inital costs of reproduction, as measured by weight loss, condition change, and gonadal-somatic index change, were more severe in females than males. During breeding and subsequent care-giving, males did little or no feeding whereas females increased their feeding during the same time period. However, males appeared to sustain only minor weight and condition losses due to care-giving. I suggest that males were the principal care-givers because the net benefits of remaining at the nest were greater than the net benefits of leaving. Males had little opportunity to mate with more than one female each season, and offspring had little chance of survival in the absence of a care-giving adult. Considerable variation in female behavior occurred which suggests that the net benefits of care-giving were nearly balanced with the net benefits of leaving the brood. The relative importance of feeding versus care-giving by females may vary with slight differences between females and the behavior of their mates as care-givers.Present address: Department of Zoology, Ohio State University, 1735 Neil Avenue, Columbus, Ohio 43210, USA     

Tests of the mate-guarding hypothesis for social monogamy: does population density, sex ratio, or female synchrony affect behavior of male snapping shrimp (Alpheus angulatus)?

There are at least two mechanisms by which social monogamy in the absence of biparental care may evolve: as a form of territorial cooperation, in which one or both sexes benefits by sharing a territory with a partner, and as a form of extended mate guarding, in which males guard females through entire, and perhaps multiple, reproductive cycles. I examined the effects of population variables (density, sex ratio, female synchrony) on male pairing behavior in the snapping shrimp, Alpheus angulatus, to test the hypothesis that social monogamy in this genus has evolved as a result of selection on males for long-term mate guarding of females. There was no evidence that pairing behavior changes with differences in population density; in a natural population, there was a 1:1 relationship between the number in pairs and local population density. In a laboratory experiment, males altered their pairing behavior in response to manipulated differences in sex ratio. Males in female-biased sex ratios were significantly more likely to abandon recently mated females than males in equivalent sex ratios, though there was no significant difference in the duration of pairing or the number of times males switched females. Observations of shrimp maintained for an extended period in the laboratory revealed no evidence that females molt and become sexually receptive synchronously, which would reduce the likelihood that a searching male would encounter additional receptive females. These data suggest that sex ratio may have contributed to the evolution of social monogamy in snapping shrimp, but provide no evidence that population density or female synchronous receptivity have contributed to the evolution of social monogamy.     

Sexual behavior is related to badge size in the house sparrow Passer domesticus

Summary Badge size, which functions as a signal of dominance status in male house sparrows Passer domesticus, was significantly related to their sexual behavior. Males with large badges participated in communal displays (multi-male chases directed towards single females) more often than males with small badges, irrespective of whether the female involved was the male's mate or not. Experimentally released females were more often chased if they were fertile than if they were nonfertile. Estradiol-implanted females were chased more often than control females without a hormone implant, and males with large badges chased estradiol-implanted females more often than did males with small badges. Both forced extra-pair copulations during communal displays and unforced extra-pair copulations were more often achieved by males with large than small badges. Male house sparrows with large badges also copulated with their mates at a higher rate than did males with small badges. A higher certainty of paternity therefore is hypothetized to accrue to male house sparrows with large badges.     

Adoption or infanticide: options of replacement males in the European starling

The behaviour of a male bird towards a potential mate and her clutch may depend both on his expected paternity and on the likelihood that she will produce a replacement clutch if he commits infanticide. In this study we evaluate the choices made by replacement male European starlings Sturnus vulgaris. By removing males before and during laying, we induced other males, mainly neighbours, to mate with the reproductively active females. When the original male was removed before laying, a new male adopted the subsequent clutch in 14 out of 15 cases. When ten females were widowed during their laying period, replacement males never adopted their clutches. The paternity of replacement males was a function of when they replaced the former male. When replacement occurred more than 3 days before egglaying, the new male fathered nearly all offspring; when it occurred the day before laying, the new male still fathered more than every second young. When the original male was removed during his mate’s laying period, in five out of ten cases a replacement male committed infanticide by throwing out the eggs, but this only occurred in one out of 15 cases when removal took place before laying. The evidence for infanticide actually being committed by the replacement male was circumstantial. Four out of six of the females affected by apparent infanticide produced replacement clutches in which the male presumably had higher paternity than in the original clutch. In all cases, the male adopted the replacement clutch. In five cases when the original male was removed during laying, the neighbours neither adopted the brood nor committed infanticide, although they sometimes were seen courting the widowed female and copulating with her. These cases occurred later during laying than those were males comitted infanticide. The time from infanticide to the laying of the replacement clutch tended to increase as infanticide was committed later in the laying sequence. We conclude that strategies of potential replacement males are influenced by their expected paternity in the current brood and the probability that the female will produce an early replacement clutch. Received: 10 March 1995 / Accepted after revision: 28 October 1995     

Reproductive allocation in female house wrens is not influenced by experimentally altered male attractiveness

The differential allocation hypothesis proposes that females mated to attractive males should invest more resources in their offspring than those mated to less-attractive males, whereas the compensation hypothesis posits that females mated to less-attractive males should invest more resources in their offspring to compensate for lower-quality young. We tested these hypotheses by manipulating attractiveness of male house wrens (Troglodytes aedon) prior to female arrival by adding extra nest sites to territories of some males while leaving control males with only a single nest site. Females laid their eggs sooner in the nests of attractive males, and attractive males were more likely to retain their territory over successive broods and were marginally more likely to obtain a mate for a second brood later in the season than were control males, thereby confirming the effect of our manipulation on male attractiveness. Experimentally enhanced attractiveness also led to increased hematocrit in males. However, there were no consistent differences in the number, size, or quality of eggs laid by females mated to attractive and control males, nor were there any differences in the size, health state, or immune function of nestlings produced from these eggs. There was also no effect of treatment on the number of nestlings surviving to fledging. Collectively, these results are inconsistent with both the differential allocation hypothesis and the compensation hypothesis. Future studies should consider the possibility that the criteria used by females in selecting a mate may vary temporally and be more flexible than generally thought.     

Male choice and sperm competition as constraints on polyandry in the red-necked phalarope Phalaropus lobatus

Summary The mating system of the red-necked phalarope Phalaropus lobatus is usually classed as polyandrous, but studies show that the majority of females are monogamous. Polyandry appears to be constrained because later arriving males do not usually nest with females that have already laid a clutch that season (C1-females), despite the sexual receptiveness of these females. Rather they nest with females that have not previously laid a clutch that season (C0-females). Five potential explanations of this constraint on polyandry were tested. Two hypotheses, invoking female-female competition, were not supported as female agonistic success appeared to be unrelated to priority of access to males, and there was no apparent difference between C0- and C1-females in their ability to find unpaired males. Two hypotheses suggest that C0-females are preferred by males either because they can initiate a clutch more rapidly or because they lay larger eggs. Neither hypothesis was supported by the available data. The data upheld a third male choice hypothesis that C1-females are discriminated against because they have copulated previously with another male and this may compromise paternity. Secondary males copulated and attempted to copulate more often when paired with C1-females, suggesting that sperm competition was greater and confidence of paternity was lower. Corroborative evidence of active male choice showed that males were more aggressive towards associating C1-females than towards C0-females, although how males discriminated between the two classes of females was not determined.     

The basis for female choice in an avian brood parasite

Summary Behavioral observation and experimental manipulation of a marked population of brood parasitic brown-headed cowbirds (Molothrus ater) were conducted to determine whether or not females exhibit mate choice and to elucidate the ultimate basis for any such choice. Female choice was indicated by the fact that each female copulated with only one male, although most were courted by several. Patterns of female aggression towards males also revealed that females had the opportunity to display choice. Courtship by males was sometimes treated by females as harassment, but there was no conclusive evidence that a male provided his mate with protection from harassment by other males. Nor was there any indication of other proximate benefits or services males might have provided for females. Thus, there is no evidence that males provide females with anything other than their genes. An experimental removal of mated males and the pattern of subsequent remating of widowed females are consistent with female choice for male genetic quality. Offprint requests to: D.A. Yokel at the present address