Female Fertile Period Research Articles

The Functions of Song in the Serin

The function of song in the serin Serinus serinus was investigated by measuring variation in singing time and song flights by the male, and nest building by the female during the prelaying and laying period, and by correlating nest building, extra‐pair copulation attempts and chasing of the female with male singing time and song flights between pairs. Both singing time and nest building varied in relation to the female fertile period, peaking at day −4. Moreover, nest‐building activity correlated with singing time, but not song flights, between pairs. This suggests that song may have a function in stimulating the female to nest build or begin rapid yolk deposition. Pair copulations were not correlated with singing time or song flights either over days relative to laying or between pairs and pairs were not more likely to copulate in a given minute of observation when the male had sung in the previous minute than when he had not. However, extra‐pair copulation attempts and chasing of the female showed a tendency to be negatively correlated with song flight but not singing time, between pairs. This suggests that song flight may have a function in discouraging sexual competition from other males.

Individual and Temporal Variation in Cloacal Protuberance Size of Male Bearded Tits (Panurus biarmicus)

The intensity of sperm competition is one of the factors known to determine interspecific variation in the size of male reproductive organs. However, individual variation in the size of reproductive organs and its relation to male quality have not been considered appropriately. We investigated the annual pattern of variation in the size of the cloacal pro- tuberance (CP) in male Bearded Tits (Panurus biarmicus) and correlated CP volume during the fertile period of females with reproductive and morphological features of males. Con- trary to other passerines, the cloacal protuberance does not constitute a sperm reservoir but functions as a copulatory organ in Bearded Tits. CP volume differed significantly between unmated and mated males and provided a good indicator of their reproductive status. With- in individual mated Bearded Tits, CP size changed in conjunction with their mate's fertile cycle, peaking around the day of clutch initiation. During the fertile period, mated Bearded Tits possess the largest CP (relative to body size) known for a passerine (average volume index = 59.14 mm 3 per g; n = 16). The adaptive value of this feature could be that it improves ejaculate transfer owing to better and longer cloacal contact. Relative to unmated males, mated males have more total sperm stored in their seminal glomera and larger testes, sug- gesting the occurrence of large disadvantages for unmated males to gain reproductive suc- cess. An isolation experiment showed that female presence positively influences the devel- opment of CP size in virgin male Bearded Tits. Received 14 April 1997, accepted 12 March 1998.

Extra-Pair Fertilizations in the Sedge Warbler

Parentage of 201 young (from 44 broods) in a population of Sedge Warblers Acrocephalus schoenobaenus in South Central Sweden, 1990-1992, was determined by using multilocus DNA fingerprinting. The frequency of extra-pair young (EPY) was 7.5% and they occurred in 23% of the broods. For 11 out of 15 extra-pair young we could identify the true father; in all of the cases he was a close neighbour. Among ten broods with extra-pair young, nine contained only one extra-pair sire and the remaining brood two extra-pair sires. The frequency of EPF varied among years (1.8-11.8%). The seasonal timing of broods with and without extra-pair young did not differ, and the occurrence of extra-pair fertilizations (EPF) was not related to the length of the pair male's mate-guarding period. EPF were not related to breeding synchrony (estimated as the mean number of fertile females per day during a female's fertile period). Pairs whose nests contained extra-pair young had more territories within 100 m of their nest than pairs without extra-pair young. Females that engaged in EPF had fewer attractive (i.e. singing) males to choose among the day before and at the day they formed their pair bend. Moreover, in all but one case the extra-pair male was not singing (i.e. not available as pair mate) the day the EPF-female settled. Males that fertilized extra-pair young tended to arrive earlier and to have higher pairing success than both males that were cuckolded and other males. Hence, female Sedge Warblers engaged in extra-pair fertilizations with attractive male neighbours. These results are consistent with the hypotheses that females participating in EPF are seeking genetic benefits to their offspring, but we cannot exclude the alternative explanation that attractive males are more efficient in forcing females to accept EPF.

Experimentally reduced paternity affects paternal effort and reproductive success in pied flycatchers

The question of whether, and how, male birds should change their parental effort in response to reduced paternity is a controversial issue among behavioural ecologists. We report a study on pied flycatchers,Ficedula hypoleuca, in which paternity was manipulated through experimentally induced mate switching during the female's fertile period. The paternity of care-giving males ranged from 0 to 100% of the brood. The number of parental males per nest varied between zero and two, and the amount of male assistance in nestling provisioning had a marked effect on female reproductive success. For 17 monogamous males, provisioning effort and the body mass of nestlings on day 12 were reduced at low levels of paternity. However, the shape of the effort function was not unambiguously determined. Male provisioning effort showed a curvilinear decline, whereas nestling body mass showed a linear decline. Two important assumptions of the theory of optimal parental effort seem to be fulfilled in this case: that males had reliable cues to their paternity, and that paternity is likely to be increased in future (normal) breeding attempts. The fact that males reduced their effort at the expense of the welfare of the offspring suggests that there are significant costs of parental care in this species. Whether a similar response to cuckoldry occurs in unmanipulated breeding situations remains to be studied.

Effects of testosterone on use of space by male dark-eyed juncos when their mates are fertile

Testosterone is an important determinant of spatial activity in male birds. Using radiotelemetry, male dark-eyed juncos,Junco hyemaliswere followed during the period when their mates were fertile to investigate the relationship between testosterone and behaviours (territoriality, consorting with female) through which males might guard paternity. Males with experimentally elevated testosterone levels (T-males) and control males (C-males) did not differ significantly in their use of space during this period. T-males and C-males occupied similar home ranges, used similar-sized core areas (areas enclosing 95% of all activity), spent similar amounts of time close to their mates, and experienced similar intrusion rates onto their territories. Experimentally elevating testosterone above control levels did not detectably affect the spatial activity of male juncos during the female fertile period, although earlier studies have shown that its effects are pronounced during other stages of the nesting cycle.

Non-territorial ‘floaters’ in great horned owls: space use during a cyclic peak of snowshoe hares

The ecology and behaviour of non-territorial owls are little known. During a population peak of snowshoe hares,Lepus americanus, the main prey of great horned owls,Bubo virginianus, in the boreal forest, fledglings were equipped with radiotransmitters, and 30 successful dispersers were monitored in 1988–1991. Of those, nine became resident floaters in the study area. Transient floaters were not recorded, although floaters shifted the centre of their home ranges more than territorial owls. Floater home ranges were about five times larger than defended territories, but the space use did not differ significantly. Floaters intruded regularly into territories and their locations overlapped broadly with those of territory owners and other floaters, but were concentrated on the periphery of defended territories. This is consistent with other evidence that territorial behaviour limits the breeding density of great horned owls even at extreme peaks of prey availability. None of the monitored floaters bred as secondary females, and the intrusion rates and movement patterns of floaters did not change during the fertile period of females, as predicted if male floaters were seeking extra-pair copulations.

Problems with Removal Experiments Designed to Test the Relationship between Paternity and Parental Effort in a Socially Polyandrous Bird

Aspects of sperm-competition research in birds have progressed from purely descriptive studies that establish multiple paternity (e.g. Gowaty and Karlin 1984, Gavin and Bollinger 1985, Westneat 1987) to a more experimental approach that examines the relationship between paternity and male parental effort (e.g. M0ller 1988, Koenig 1990, Davies et al. 1992, Whittingham et al. 1993). These experiments take the form of removing resident males during the female's fertile period as a means of disrupting one of the cues that males presumably use to assess their paternity (Schwagmeyer and Mock 1993), and then retuming them back to their territory and observing their behavior. Parental care by a removed male is predicted to decrease continuously with decreasing paternity in species with more than one male breeder and caregiver at the nest (Whittingham et al. 1992). In addition, removed males with low or no paternity have been known to destroy eggs upon being released back onto their territory, forcing females to renest and thus allowing the males a further reproductive opportunity (Koenig 1990, Robertson 1990). We attempted to test the general prediction that paternal effort should decrease with decreasing paternity using the polyandrous Pukeko (Porphyrio porphyrio). Pukeko exhibit a variable mating system, with about half of our study population composed of groups with two to three unrelated, co-breeding males. Alpha males do not guard the female during her fertile period and will tolerate copulations by other males within the group. This results in shared paternity and low reproductive skew among males (as shown by DNA fingerprinting analysis), and equal contribution in parental effort (Jamieson et al. 1994, Jamieson 1997). According to the predictions, Pukeko males removed early in the egg-laying period should show a reduced effort in parental care in response to decreased paternity, whereas control males removed after the laying period should exhibit normal levels of parental care. As we will show, the results of testing the relationship between paternity and parental effort were inconclusive because residents showed unusually high levels of aggression toward removed males that were released back onto their territories for both experimental and control groups. However, we present the results of the experiment to provide a cautionary note

Assessment of the quality of copulation partners in the monogamous bearded tit

Females try to control paternity in various ways. They may resist copulation attempts by males but they may also feign resistance in order to incite competition between males. In the lifetime monogamous bearded tit,Panurus biarmicuschase-flights, both within pairs and with other males, occur during the female's fertile period. In general, these chase-flights are followed by copulations. Females in this study were able to resist copulations, but they also often approached males and solicited copulations by wing flapping; if males tried to mount the females, they resisted and flew away. During the fertile period females solicited extra-pair males to chase them significantly more often than they solicited chases with their own mate. In isolated pairs chase-flight activity was reduced and most copulations occurred without preceding chase-flights. In addition, females in isolated pairs solicited their partners to chase them significantly less often than females with extra males available. This suggests that females use chases to incite male–male competition and thus to obtain ‘good genes’. In contrast to other studies, females paired to high-ranking males incited more chase-flights than females paired to low-ranking males, perhaps because only high-quality females could afford to perform this energetically expensive activity.

Mate-Guarding, Territorial Intrusions and Paternity Defence in the Polygynous Corn Bunting Miliaria calandra

Mate-guarding behaviour and territorial intrusions were examined in a population of polygynous Corn Buntings Miliaria calandra. All males showed only a weak tendency to mate-guard by close following of the female. Monogamous and polygynous males did not differ in their extent of mate-guarding, and there was no difference in the extent to which polygynous males guarded primary and secondary females. Territorial intrusions and attempted extra-pair copulations were infrequent and not timed to coincide with the fertile period of females. All intrusions were by territory-holding males, the majority of which were immediate neighbours. Unmated males did not intrude more than paired males and were not observed to attempt any extra-pair copulations. Polygynous males did not suffer significantly more intrusions than monogamous males. We suggest that either the high detectability of intrusions in an open habitat or female control over access to fertilizations made close mate-guarding unnecessary. Males may benefit more from maintaining their own territory in the hope of one or more females settling to breed, rather than seeking extra-pair copulations.

Territoriality and song as flexible paternity guards in dunnocks and alpine accentors

I compare paternity defense strategies in the variable mating systems of alpine accentors Prunella collaris and dunnocks P. modularis. I show that in dunnocks breeding territoriality functions exclusively for mate defense. Male investment in territoriality increases with the number of females they are defending, and when females are removed males sharply decrease their song output and eventually abandon their territories. Further, I show that paternity defense strategies vary in relation to group composition. In single-male groups there is greater investment in territorial defense and less investment in mate guarding during the female fertile period than in multimale groups. I discuss the influence of the contrasting habitats of dunnocks and alpine accentors on their paternity defense strategies.

Ranging behaviour of red foxes during the mating and breeding seasons

Ranging behaviour (home range size, core area size, activity levels) of four red foxes (Vulpes vulpes; three males and one female) was studied by radio-tracking in a rural area of Central Italy during the mating and breeding seasons (January to May). Home range size was equal or smaller than in other areas, ranging from 47 to 320 ha (kernel analysis) or from 57 to 394 ha (minimum convex polygon), with the exception of a yearling male, who ranged over a very large area (2307 ha). Core areas ranged from 11 to 29 ha. Foxes were most active between 19:00 and 00:00 hr, then activity decreased slowly until sunrise. Foxes used about 25% of their range each night, with individually different strategies: the two resident males greatly increased their range in the second half of female fertile period, whereas the nomadic male restricted his large range during the peak of matings. Barking bouts (indices of agonistic and contact behaviour) were most common after median ovulation date. The female decreased her range a...

Male vigilance in white-tailed ptarmigan,Lagopus leucurus: mate guarding or predator detection?

Male white-tailed ptarmigan accompany their mates 88-92% of sightings before the onset of incubation, and while accompanying their mates, spend 22-30% of their time displaying vigilant behaviour. Two hypotheses to explain the function of male vigilance before onset of incubation were examined in white-tailed ptarmigan. The protection of paternity hypothesis proposes that male vigilance minimizes the threat of cuckoldry, thereby ensuring paternity in a reproductive attempt. Thus, male vigilance should be greatest during periods when females are fertile, and it should increase when the sex ratio is male-biased. The predator detection hypothesis predicts that increasing male vigilance decreases predation risk to their mates and thus may allow females to increase foraging efficiency. The percentage of time males spent in vigilant behaviour during the pre-incubation period did not change significantly with period of female fertility or with the sex ratio of breeding birds. However, males spent significantly more time vigilant in the year when there were more sightings of predators. The proportion of time females spent foraging was positively correlated with the proportion of time their mates were vigilant. Vigilant behaviour before onset of incubation is likely to increase a male's confidence in paternity of that nesting attempt in white-tailed ptarmigan. However, patterns of variation in male vigilance across seasons and between years suggests that this behaviour also functions to allow females to reduce their vigilance for predators, thereby enabling them to forage more effectively before incubation.

Monogamy in Leach's Storm-Petrel: DNA-Fingerprinting Evidence

We used multilocus minisatellite DNA fingerprinting to estimate the frequency of extrapair fertilizations in a population of Leach's Storm-Petrel (Oceanodroma leucorhoa) on Kent Island, New Brunswick, Canada. Leach's Storm-Petrel is a member of Procellariiformes, an order of long-lived pelagic birds characterized by long-term pairbonds, single-egg clutches, and extended periods of parental care. We found no evidence of extrapair fertilizations in 48 families (42 full families and 6 partial families consisting of the putative father and the single offspring). Thus, our results indicate that the breeding system (genetic monogamy) matches the mating system (social monogamy) in our study population, a condition that no longer can be assumed in socially monogamous bird species. Genetic monogamy in Leach's Storm-Petrels may be maintained by last-sperm precedence and frequent copulation by mates during the female's fertile period. Such tactics employed by a male may yield a high prob- ability of fertilizing the single egg laid by his mate. Received 15 June 1994, accepted 31 August

Dominance status, mating strategies and copulation success in cooperatively polyandrous white-winged trumpeters, Psophia leucoptera (Aves: Psophiidae)

In groups of white-winged trumpeters, dominant and subordinate males used different strategies to obtain copulations with the dominant, breeding female. The dominant male initiated copulation attempts slowly and often copulated when subordinate males were standing nearby; in contrast, subordinate males tended to copulate rapidly and surreptitiously, taking advantage of moments when the dominant male was relatively far from the female or engaged in an activity that made it difficult for him to watch the female. The dominant male usually interrupted subordinates' copulation attempts aggressively and always interrupted alone. Subordinate males, however, generally interrupted the dominant simply by approaching him, and collaborated in 19% of their interruptions. Although the dominant male obtained significantly more successful copulations than did subordinate males during the breeding female's fertile period, subordinate males still accounted for one-third of the successful copulations during this period. While relatively few birds or other vertebrates have been reported to breed polyandrously, it is suggested that the frequency with which multiple males sire offspring within a group may be underestimated because of the difficulty of observing copulations by subordinate males in many multi-male groups.

Forced extra-pair copulation and mate guarding in the white-cheeked pintail: timing and trade-offs in an asynchronously breeding duck

Abstract. Males employing a mixed reproductive strategy may increase their fitness through extra-pair copulations (EPCs), but also risk lost paternity when they leave their own mate unguarded. How males maximize the effectiveness of forced extra-pair copulation (FEPC) attempts while minimizing the risk of cuckoldry was studied in a non-migratory population of the white-cheeked pintail, Anas bahamensis bahamensis, a tropical species with extended breeding seasons. Despite substantial asynchrony in the laying dates of females, males directed FEPC attempts primarily at females in fertile condition. The rate of pair copulations also peaked during the female's fertile period, but 23.1% of all successful copulations with laying females were FEPCs. Males guarded their paternity by vigorously defending their mates from males attempting FEPC, by escorting females to their nests, by defending a territory, and by forcing copulation on their own mates after they had been subjected to an FEPC attempt by another male. Contrary to expectation, males did not temporally partition mate guarding and FEPC activity but pursued FEPCs primarily during the period when their own mates were fertile. There was no evidence, however, of a trade-off between FEPC activity and the quality of male mate guarding. Females paired to males with the highest FEPC rates were rarely subjected to FEPCs themselves. In addition, although females that abandoned nesting efforts suffered a high frequency of FEPC attempts, their mates were much less active in FEPCs than the mates of females that nested successfully. These results suggest substantial variation in male quality: some males excelled at both guarding their mates and achieving FEPCs, while others neither pursued FEPCs nor mate-guarded effectively.

Forced Extra-Pair Copulation in the White-Cheeked Pintail: Male Tactics and Female Responses

I studied tactics used by males to detect fertile females and achieve forced extra-pair copulations (FEPC) and female responses to FEPCs in a non-migratory, asynchronously breeding population of White-cheeked Pintails (Anas bahamensis) in the Bahamas. Males assessed female reproductive status by (1) monitoring behavior of neighboring pairs, (2) visiting the island nesting site and observing laying females directly, and (3) chasing females. FEPC attempts directed at neighboring females were more likely to occur during the female's fertile period than FEPC attempts directed at non-neighbors and a large proportion (44%) of FEPC attempts involved neighboring pairs. Sexual chases of fertile females were more frequent and of longer duration than chases of non-fertile females suggesting that males gain information on female reproductive status in initial chases. Males employed sophisticated tactics to achieve FEPCs, including waylaying females as they left their nests, approaching females surreptitiously by swimming "submarine" style, and capturing and mounting females underwater. Females vigorously resisted FEPC attempts by repeatedly diving, flying away and hiding and were sometimes chased to exhaustion. The high costs of resistance and observations that females resisted copulations from all extra-pair males, regardless of quality, make "resistance-as-a-ploy" and "genetic-quality" hypotheses unlikely explanations for why females resist EPCs. I argue that females resist EPCs to preserve the pairbond and investments of their mates, which in turn protects their investment.

The Conflict between Nest Guarding and Mate Guarding in Penduline Tits (Remiz pendulinus)

AbstractIn penduline tits (Remiz pendulinus), polygynous males build several very elaborate nests successively during one breeding season to attract females. The time and effort invested in nest building is positively related to their mating success. Intraspecific competition for nest material resulting in nest material theft, delays males' nest building progress which in turn decreases their mating success. Therefore, a nest guarding strategy was predicted. In many bird species, males develop some kind of paternity strategy during the female fertile phase. However, as nest building and the female fertile phase frequently coincide, one would expect a trade‐off between these strategies. In this study we determined in particular how nest guarding in males conflicts with their mate guarding behaviour in penduline tits.Our results show that nest building is costly in terms of a male's time budget. Thieves benefit by increasing their rate of acquiring nest material which reduces the effort invested in nest building. Nest guarding is an efficient strategy to avoid thieves, as indicated by the negative relation between the presence of the male near the nest and the frequency of nest material theft. Nest guarding is required for the whole building period but males, however, increased their mate guarding effort during the peak fertile phase to ensure their paternity. The data suggest that, for the trade‐off “mate guarding versus nest guarding”, paternity insurance seems to be more important.

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

AbstractThe 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.

Prospective infanticide and ovulation retardation in free-living house sparrows

Abstract. Replacement male house sparrows, Passer domesticus, invariably committed infanticide when they took over a nest after a female's fertile period had recently ended ( N = 8). Males that took over a nest during egg laying destroyed eggs in 58% of the cases ( N = 12), whereas those arriving before clutch initiation never committed infanticide ( N = 32). Seven out of 12 nests in which the replacement male arrived during laying suffered egg losses (58%). In six of them the female owner stopped laying, while the remaining female left her nest. Two more females whose original males were replaced during the laying period (17%) and two out of seven females whose males were replaced during the 4 days prior to clutch initiation (29%) stopped laying even though they had not suffered egg losses. In contrast, females that initiated laying 5 days or more after the arrival of the replacement male did not stop laying. Nine out of 11 females initiated a new clutch with the replacement male on average 7·3 days after they stopped laying. The results suggest that male prospective infanticide functions to ensure genetic paternity, and that females use strategic ovulation retardation to cope with the risks of infanticide.

Why do male birds stop copulating while their partners are still fertile?

Abstract. In most monogamous birds copulation frequency peaks a few days before the start of egg laying and then either ceases or drops markedly. This decline occurs despite the fact that females remain fertile until the day their penultimate egg is laid. Several hypotheses to explain the decline in copulation frequency following the onset of egg laying were tested, using data from different species. There was no evidence that the decline was a consequence of (1) one or other partner being involved in incubation and hence unavailable to copulate, (2) male partners being unavailable because they were seeking extra-pair copulations, (3) there being fewer eggs to fertilize as egg laying proceeds, (4) offspring from late hatched eggs being of lower value, or (5) copulations being costly in terms of the risks of damage to unlaid eggs. There were insufficient data to test (6) the egg-predation hypothesis: that for species that copulate at or near their nest those vulnerable to egg predation should cease copulation relatively early in their cycle. The hypothesis (7) that copulations were less efficient once egg laying has started was supported, as was (8) the sperm competition hypothesis across different mating systems. Where there is little sperm competition, as in lekking species, copulation ceases very early, but with intense sperm competition, as in simultaneously polyandrous species, copulations continue until the end of the female's fertile period. In polyandrous species continued copulation may benefit both sexes: males because it increases their probability of fathering offspring, and females because by continuing to copulate they obtain material benefits (paternal care) from their male partners. With intermediate sperm competition (monogamy) copulation shows an intermediate pattern, but within monogamous birds factors, as yet unidentified, affect the temporal pattern of copulation. In most birds copulation frequency is controlled by the female: a female requires only a single insemination to fertilize her eggs. Male interests differ: because of last male sperm precedence, males benefit from more frequent copulation and over a longer period to ensure their paternity. Within species this conflict between the sexes is evident from the temporal pattern of female- and male-initiated copulations.