Experimentally elevated plasma levels of testosterone do not increase male reproductive success in blue tits

In temperate passerines, increased testosterone (T) levels during breeding mediate male aggressive and mating behaviour. If individual variability in T levels is reflected in behavioural differences during mating, males with higher T might gain higher reproductive success. This can be tested experimentally by elevating T levels. However, high exogenous T levels are known to have negative effects on male sperm production. This may reduce male fitness, particularly if sperm competition is intense. We experimentally elevated T levels in breeding blue tit males to investigate how T levels above the natural mean influence male reproductive success. Contrary to most—if not all—previous experimental manipulations of T levels in birds, we restricted the treatment with exogenous T to the time when females were fertile and T levels were naturally high in males. In blue tits, extra-pair paternity is an important component of male reproductive success, and its frequency is likely influenced by androgen-mediated behaviours such as mate attraction and aggression towards other males. Here we show that T-males were equally likely to become cuckolded and did not gain more extra-pair paternity than control males. Cuckolded T-males, however, lost more paternity than control males. We discuss the possibility that this is caused by negative effects of T treatment on sperm production.Communicated by M. Webster     

Effects of paternal care on reproductive success in the polygynous spotless starling Sturnus unicolor

For males of socially polygynous avian species like the spotless starling, there may exist a trade-off between investing in paternal care and controlling several nests. To determine how the intensity of paternal care affects reproductive success per brood sired or expressed as the total number of young raised in all nests controlled by the same male, it is necessary to manipulate paternal care. Testosterone (T) has been shown to depress the tendency for males to care for their young, and induces them to acquire more mates. The effects of paternal care on reproductive success were studied by treating certain male starlings with exogenous T and others with the antiandrogen cyproterone acetate (CA), and comparing the parental behavior of T- and CA-males throughout the breeding season with that of controls. CA-males fed their chicks more during the first week after hatching than T-males, with controls feeding at intermediate rates, both on a per nest basis and as total effort for all nests controlled by the same male. Paternal feeding rates during the first week of chick life had a significant positive effect on the number of fledged young. The hormone treatment significantly affected the number of chicks raised per nest, CA-males having a higher breeding success per nest than T-males, and controls showing intermediate levels of success. There was no significant effect of treatment on total reproductive success attained by males throughout the season. In the polygonous spotless starling, the intensity of paternal care of young affects reproductive success per nest positively but not on a seasonal basis. Received: 6 February 1999 / Received in revised form: 30 June 1999 / Accepted: 11 July 1999     

Social and ecological factors affecting paternity allocation in American robins with overlapping broods

Factors that affect extra-pair mating in birds are likely to vary across the breeding season. Changing densities of active nests may alter the opportunities for extra-pair mating, and parental duties may alter a male’s opportunity to guard his mate from extra-pair mating. The latter affects species with multiple broods, where males care for fledglings from first nests while females initiate second nests. We studied a population of multi-brooded American robins (Turdus migratorius) to assess how seasonal changes in nesting density and changes in mate-guarding opportunity influenced paternity patterns over successive breeding attempts. Extra-pair paternity (EPP) occurred in 71.9% of broods and accounted for 48.1% of young. High nesting densities in the study population may explain the high overall rate of EPP, but seasonal variation in breeding density did not explain patterns of EPP among nests. Contrary to the predictions of the mate-guarding hypothesis, EPP did not increase in the second nests that followed successful first nests, and the percentage of extra-pair young in second nests did not decline as the overlap between successive nests increased. The fact that EPP was actually lower when the interval between clutches was shorter suggests that the sooner the males can assume sole care of first broods and allow their mates to renest (indicative of superior paternal quality), the more paternity they realize in the next nest. These results suggest that mate-guarding opportunity does not influence paternity in this population of American robins and that female robins may allocate paternity based on their assessment of male parental performance at first nests.     

Polygyny and male parental care in Savannah sparrows: effects on female fitness

Summary To determine the effects of male mating status on female fitness, we compared the reproductive success, survival, and future fecundity of female Savannah sparrows (Passerculus sandwichensis) mated to monogamous vs. polygynous males in a 5-year study on Kent Island, New Brunswick, Canada. The proportion of males with more than one mate varied from 15 to 43% between years and sites. Polygynous and monogamous males fledged young of equal size in every year of the study. Females who shared paternal care with other females laid as many eggs per clutch and clutches per season as monogamously mated females. In most years polygynously mated females showed no delay in laying a second clutch, and they suffered no reduction in fecundity the following year. Recruitment of a female's offspring into the breeding population was generally independent of her mating status. Fitness costs of being mated to a polygynous male were only apparent in one year of the study, during which females mated to polygynous males had higher over-winter mortality than those mated to monogamous males. That same year, young raised by polygynous males were only one-third as likely to survive to reproductive maturity (as inferred by returns) as those raised by monogamous males. A male's mating status had no effect on his own survivorship. A male's mating status did not necessarily reflect his contributions to raising nestlings, which may partially explain why monogamously and polygynously mated females had equal fitness. At 35 nests the proportion of food deliveries brought by individual males varied from 0 to 75%; on average, males brought fewer than 30% of all food deliveries. Yet parental care by polygynous males was no less than that of monogamous males, at least at the nests of their primary females. Secondary females tended to receive less male assistance during the nestling stage, but their reproductive success was indistinguishable from that of primary females. Females feeding young without male assistance made as many food deliveries/h as did pairs in which males brought at least 30% of all food deliveries. Unassisted females did not suffer diminished fledging success or produce smaller fledglings. The benefits of polygyny for male Savannah sparrows are clear: polygynous males recruit more surviving offspring into the breeding population than monogamous males. The fitness of females, on the other hand, appears to be unaffected by whether their mate was monogamous or polygynous except in occasional years. Polygyny may be maintained in this population by the constraints of a female-biased sex ratio, the inability of females to predict a male's paternal care based on his morphology or behavior, the poor correlation between a male's mating status and his assistance at the nest, and inconsistent natural selection against mating with a polygynous male. Correspondence to: N.T. Wheelwright     

Paternal care in the European starling,Sturnus vulgaris: nestling provisioning

The extent to which male birds in polygynous species with biparental care assist in nestling feeding often varies considerably between nests of different mating status. Both how much polygynous males assist and how they divide their effort between nests may have a profound effect on the evolution of mating systems. In this study we investigated how males in the facultatively polygynous European starling Sturnus vulgaris invested in their different nests. The amount of male assistance affected the quality of the offspring. Polygynous males invested as much as monogamous males, but divided their effort asymmetrically between nests, predominantly feeding nestlings of first-mated (primary) females. Although females partly compensated for loss of male assistance, total feeding frequency was lower at primary females’ nests than at monogamous females nests. Secondary females received even less assistance with nestling rearing, and the extent to which males assisted decreased with the length of the interval between the hatching of the primary and secondary clutches. These results are contrasted with those from a Belgian populations of starlings with a much more protracted breeding season and thus greater opportunities for males to attract additional mates during the nestling rearing period. The results show that both the “defence of male parental investment model” and the “asynchronous settlement model” have explanatory power, but that their validity depends on the potential length of the breeding season. Received: 21 July 1995/Accepted after revision: 13 July 1996     

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.     

Mate choice in the yellow-shouldered widowbird: correlates of male attractiveness

Recent investigations of male ornaments in sexual selection have used experimental manipulation of tail length in three widowbird species, but only for one of these have correlates of male reproductive success been reported. I examined correlates of male attractiveness to nesting females over two breeding seasons for the polygynous yellow-shouldered widowbird, Euplectes macrourus, in order to discover which cues females may be using to select mates. The black, long-tailed ( 10 cm) males defend large territories and build nest frames, or cock's nests, which females then line and use for nesting. I examined various aspects of male morphology, five behavioral displays, territory characteristics, and the number of cock's nests that males built. Few correlates of mating success were found. The best predictor was the number of cock's nests that a male builds, though one courtship display also correlated with male mating success in 1 year, as did average grass height. Tail length did not correlate with male mating success. A partial correlation analysis confirmed that cock's nests and, in 1 year, grass height, were the primary contributers to male success. Females may choose where to nest primarily on the availability of suitable nesting sites. Long tails may be used by females seeking extra-pair copulations or in male-male competition for territories.     

Sex-role reversal in willow tit nest defence

Summary The roles of sexes in the nest defence behavior of monogamous willow tit (Parus montanus) were studied near Oulu, northern Finland, in 1988–1990. The relative roles of the sexes changed during the breeding cycle: females defended their nests more vigorously before hatching and males defended more after hatching. This sexual asymmetry was studied by means of the cost/benefit model of optimal parental investment (PI). Because of the monogamous breeding system, sexual differences in future benefits were not a likely explanation for the asymmetry. This was also supported by preliminary results of DNA-fingerprinting analyses. Behavioral observations — sex-role reversal, high correlation between the mates, and equal variations in male and female behavior — indicated the same. In the beginning of the breeding cycle, higher female defence was related to renesting potential. The extra costs of renesting are considerably higher for females than for males, and therefore, females appeared to benefit more than males in keeping the first clutch alive while renesting was still possible. Such a female strategy was possible in this northern population, since the time for renesting was rather short and never lasted beyond the hatching of the first nests. After this point, the male can only invest in the present clutch. By the end of the breeding cycle, increased defence of the nest by males may be a consequence of males being larger and/or in better condition than females. Therefore, in the latter half of the breeding cycle, the sexual differences in nest defence did not indicate any sexual difference in PI. The asynchronous arrival of the parents at the nest also affected individual responses, indicating that defending the nest is a dynamic process.     

Experimental evidence of a testosterone-induced shift from paternal to mating behaviour in a facultatively polygynous songbird

Previous studies have suggested that testosterone (T) profiles of male birds reflect a trade-off between mate attraction behaviours (requiring high T levels) and parental care activities (requiring low T levels). In this study, we experimentally elevated T levels of monogamous males in the facultatively polygynous European starling (Sturnus vulgaris), and compared mate attraction and paternal behaviour of T-treated males with those of controls (C-males). T-males significantly reduced their participation in incubation and fed nestlings significantly less often than C-males. Females paired to T-treated males did not compensate for their mate’s lower paternal effort. The observed reduction in a male’s investment in incubating the eggs was accompanied by an increased investment in typical female-attracting behaviours: T-males spent a significantly higher proportion of their time singing to attract additional females. They also occupied more additional nestboxes than C-males, although the differences just failed to be significant, and carried significantly more green nesting materials into an additional nestbox (a behaviour previously shown to serve a courtship function). T-males also behaved significantly more aggressively than C-males. During the nestling period, the frequency of mate-attracting behaviours by T-treated and control males no longer differed significantly. Despite the reduced paternal effort by T-males and the lack of compensation behaviour by females, hatching and breeding success did not differ significantly between T- and C-pairs. Received: 7 February 2000 / Revised: 10 August 2000 / Accepted: 3 September 2000     

Reproductive defence priorities of male willow ptarmigan (Lagopus lagopus): enhancing mate survival or extending paternity options?

Summary Cock willow ptarmigan (Lagopus lagopus) closely guard their mates from predators and conspecific males, and vigorously defend their nests and young. In view of potential costs and benefits of behavioural guarding descisions, I designed a test to examine if, when and how males altered defence priorities. Cock willow ptarmigan were very attentive to their mates throughout the breeding season, unaccompanied hens comprising less than 3% of the sightings of mated females. From the second week of incubation until shortly after hatch, males attempted to guard both mates and offspring. Males guarded mates preferentially over nests until the third week of incubation; they then changed their priority to defence of offspring (nest and/or chicks). The overall defence response initially was strong, but decreased after the first week of incubation. Strength of response increased again in late incubation, and declined as chicks began to fly. Consistency of defence decisions was highest during prenesting and egg laying and lowest during late incubation. Since males defended their mates for a longer period than required for protection of paternity, hypotheses predicting enhanced mate survival and extended paternity options through renesting were examined. Removal of males did not result in reduced survival or increased weight loss of widows during incubation. In light of heavy nest depredation and displacement pressures by conspecifics, mate guarding throughout incubation enhanced male fitness by ensuring paternity in renesting attempts.     

Parental care of nestlings by male red-winged blackbirds

Summary Nestling feeding by males is less common among birds with polygynous mating systems than in monogamous species, because of the pronounced trade-off between parental behavior and the attraction of additional mates. In this study, however, we found that male red-winged blackbirds (Agelaius phoeniceus) commonly assisted females in feeding nestlings in several Ontario marshes. Male parental care was additional to that provided by females, and it significantly enhanced the fledging success of nests (Table 2). Male redwings did not help to feed all nests on their territories: primary and secondary nests were much more likely to receive male parental care than tertiary and later nests. Contrary to expectation, male parental care was not restricted to the nests of primary females: a greater proportion of secondary than primary nests were assisted (Tables 4a and b). The presence of new females settling on the territory at the same time that a resident female had nestlings, resulted in males deferring parental care until a later brood. This suggests that males trade off the recruitment of females against parental care to an existing brood. Although the number of nestlings fledging from a male's territory was strongly influenced by the number of females in the harem, males could additionally increase their reproductive success by feeding nestlings in one or more nests on their territories (Fig. 2). The reproductive success of females was significantly enhanced by male assistance in feeding nestlings (Table 3). However, those females not receiving male assistance on territories of feeding males did not suffer a significantly reduced reproductive success in comparison to females on territories of non-feeding males (Table 2). Males varied considerably in the quality of brood care given. We therefore suggest that the quality of male parental care may be a factor considered by females in choosing a breeding situation.     

Endocrine influences on parental care during a short breeding season: testosterone and male parental care in Lapland longspurs (Calcarius lapponicus)

In males of socially monogamous birds, plasma testosterone (T) typically declines to low levels during the parental phase. Studies on multiple-brooded species indicate that high T may be incompatible with high-quality paternal care. The length of the breeding season may affect the costs and benefits of high T and its effect on paternal care. We studied the effect of experimentally elevated T on paternal care in a single-brooded species with a short breeding season, the Lapland longspur (Calcarius lapponicus). We monitored T levels and parental behavior in 16 males with subcutaneous T implants, 14 males with empty implants, and 14 unimplanted males. We videotaped nests when nestlings were 2–3 days old and again at 4–5 days. T males with 2- to 3-day-old young visited nests and fed young less often than control males, and the mates of the T males compensated with elevated visits and feedings. However, when nestlings were 4–5 days old, T males visited their nests at normal rates – though feeding movements remained below normal – and T females visited and fed at normal rates. Nestling mass and nest success were similar in both groups. Overall, high T suppresses paternal care in Lapland longspur males. The partial improvement of paternal care when nestlings are older, despite high T, may be related to the short 6-week breeding season of this arctic species, and the consequently reduced benefits of sexual behavior late in the breeding season. Received: 2 February 1998 / Accepted after revision: 2 November 1998     

Seasonal anorexia in the male red-sided garter snake,<Emphasis Type="Italic"> Thamnophis sirtalis parietalis</Emphasis>

Many animals show seasonal shifts in behaviors that coincide with breeding, migration, or hibernation. These behavioral shifts provide ideal opportunities to study the regulation of behavior. The red-sided garter snake (Thamnophis sirtalis parietalis) spends 8 months of the year inactive in underground hibernacula, 1 month breeding, and 3 months feeding to build up enough energy stores to survive the following winter. Although they emerge from 8 months of hibernation with severely depleted energy reserves, they do not feed until weeks later, after the breeding season. We tested the hypothesis that this lack of feeding during the breeding season is due to a shift in behavior rather than the distribution of food and potential mates. Male garter snakes were given a series of choices between pursuing a breeding or feeding opportunity. The proportion of tests in which males selected feeding over breeding gradually increased throughout the study period, reaching almost 100% in the final tests. Males also were given opportunities to feed and court at the beginning and end of the study. Males initially refused food and courted females, but when retested at the end of the study they fed and did not court females. Thus aphagia during the breeding season is due at least in part to an endogenous shift in behavior.Communicated by P. Weatherhead     

Positive association between social and extra-pair mating in a polygynous songbird, the dickcissel (Spiza americana)

In polygynous species, males appear to gain additional offspring by pairing with multiple females simultaneously. However, this may not be true if some females copulate outside of the social pair bond. Polygynous males could experience lower paternity because of trade-offs among gaining multiple social mates, guarding fertility with these mates, and pursuing extra-pair matings. Alternatively, polygynous males could simultaneously gain extra social mates and have high paternity, either because of female preferences or because of male competitive attributes. We tested four predictions stemming from these hypotheses in a facultatively polygynous songbird, the dickcissel (Spiza americana). Unlike most previous studies, we found that males with higher social mating success (harem size) also tended to have higher within-pair paternity and that the number of extra-pair young a male sired increased significantly with his social mating success. Females that paired with mated males were not more likely to produce extra-pair young. In contrast, extra-pair paternity was significantly lower in the nests of females whose nesting activity overlapped that of another female on the same territory. This pattern of mating was robust to differences in breeding density. Indeed, breeding density had no effect on either extra-pair mating or on the association between polygyny and paternity. Finally, nest survival increased with harem size. This result, combined with the positive association between polygyny and paternity, contributed to significantly higher realized reproductive success by polygynous male dickcissels.     

Recruitment of mates and deceptive behavior by male Tengmalm's owls

Summary Tengmalm's owl Aegolius funereus is a hole-nesting polygynous species in which female nomadism is a reaction to cyclic lows of staple prey. For 2 years during a peak in vole abundance, I examined recruitment of mates and male singing behavior in a local population. Females and about half of the breeding males seemed to arrive successively throughout the breeding period of the first year. In contrast, a majority of the breeding males and likely also females were already on the breeding grounds at the beginning of the breeding season in the second year. Before breeding in the first peak year, males were singing at up to five different nest holes. All early breeding males (67% of total number) continued to sing at secondary nest holes after attracting and installing primary females. Secondary singing locations were never closer than 300 m from primary females' nest holes, although closer locations were used for singing before mating. All bigynous males with nests within the study area were also singing at tertiary nest holes, but none successfully attracted a third female. Polyterritoriality was confirmed by a late male settling between primary and secondary nest holes of a bigynous male. Polyterritorial behavior and reduced breeding success of secondary females are in line with the deception model. Females apparently could not discriminate between paired and unpaired singing males. Females made short visits to different males before mating. During courtship, the number and quality of nest holes defended by males may have been of particular importance to female choice.     

Sexual selection for male parental care in the sand goby, Pomatoschistus minutus

Male parental care is typically thought to come at a cost to mate attraction and future mating success. However, it has also been hypothesized that paternal care may be under sexual, as well as natural, selection, such that good fathers actually attract more mates. Here we show experimentally that in the sand goby, Pomatoschistus minutus, females prefer to mate with males that provide higher levels of parental care. We manipulated male behavior using (1) different nest sizes and (2) an application of low-O₂ water in the nests, and found that females consistently preferred males with elevated levels of care in dichotomous mate choice tests. This complements our earlier study in which we showed that males increase the amount and quality of care they provide in the presence of females. Our results demonstrate that male care may have evolved as a result of sexual selection rather than natural selection alone, and furthermore, that male care may not necessarily be in conflict with mate attraction.     

Maternal investment in eggs is affected by male feet colour and breeding conditions in the blue-footed booby, <Emphasis Type="Italic">Sula nebouxii</Emphasis>

Females are expected to vary investment in offspring according to variables that may influence the offspring fitness in a way that optimises her inclusive fitness for a particular context. Thus, when sexual ornaments signal the quality of the male, females might invest in reproduction as a function of the attractiveness of their mate. We tested whether breeding conditions and male feet colour influence reproductive decisions of blue-footed booby females. In the blue-footed booby, male feet colour is a dynamic condition-dependent sexually selected trait that is related to paternal effort. During two consecutive years, an El Niño year (poor breeding conditions) and a year with good breeding conditions, we experimentally reduced male attractiveness by modifying their feet colour after the first egg was laid and recorded female investment in the second egg. We found that, relative to the first egg in the clutch, females laid heavier second eggs during the poor year than during the good year. Females paired with males with duller feet colour reduced second-egg mass and volume and delayed the laying of the second egg, independently of the year. Absolute yolk androstenedione (A4) concentration (but not testosterone, T) in second eggs was higher during a poor year than during a good year. Only during a year with poor breeding conditions, females paired with experimental males decreased the relative A4 concentration (but not T) in the second egg compared to control females. Thus, blue-footed booby females probably favour brood reduction by decreasing egg quality and increasing size asymmetry between chicks when the breeding and the mate conditions are poor.     

Higher rate of nest loss among primary than secondary females: infanticide in the great reed warbler?

An individually marked population of great reed warblers Acrocephalus arundinaceus was studied between 1984 and 1991 in South Central Sweden. The fates of 279 nests were analysed for the 25 days following clutch initiation. The average frequency of nest loss (43%) did not differ significantly between years or between four periods of the breeding season. After a breeding failure, 70% of the females laid a replacement clutch, most of them together with the same male. On polygnous territories, males assisted the female who first hatched young regardless of her initial mating status (Fig. 2). According to the acutal status of the females attending the nests, for each day nests were classified as being of either monogamous (M), primary (P) or secondary (S) status. From egg-laying to fledging the rate of nest loss decreased among nests of primary status whereas it increased among nests of monogamous and secondary status. During the egg-laying period, the rate of nest loss was 3 times higher among nests of primary than among nests of monogamous and secondary status (Fig. 3). Thus, the high loss level among nests of primary status during the laying period was closely associated with the presence of a female with a less advanced nest on the territory. All nests were situated in reed beds above deep water and most of them at a height at which possible inter-specific nest predators would have caused disturbance to the nest itself. The suspicion that secondary females committed sexually selected infanticide was supported by an experiment with dummy eggs that revealed bill peck markings identical to those obtained from great reed warblers (Fig. 4).     

Operational sex ratios and behavioural sex differences in a pipefish population

In the pipefish Syngnathus typhle, only males brood embryos in specially developed brood pouches, supplying oxygen and nutrients. Laboratory studies have shown that this elaborate paternal care has led to sex-role reversal in this species: males limit female reproductive rate, females are the primary competitors for mates and males exercise greater selectivity in accepting mates. In the first field study of this pipefish, we describe mating behaviour in the wild and test the hypothesis that temporal variations in the operational sex ratio (OSR) determine sex differences in mating behaviour. Our study comprised two reproductive seasons of two sequential mating periods each, the latter separated by a lengthy interval of male brooding. During mating periods, females displayed to all males without wandering and males moved about searching for females, without reacting to all females. The OSR was least female-biased (or even male-biased) at the onset of the breeding season, when most pipefish were simultaneously available to mate, but became strikingly female-biased as males' pouches were filled. The OSR remained substantially female-biased during the second mating period, because few males became available to remate at any one time. As hypothesised, female-biased OSRs resulted in more female-female meetings. As well, females were above the eelgrass more often than brooding males, thus exposing themselves to conspecifics and/ or predators. In the second year, males arrived earlier than females on the breeding site and male pregnancies were shorter, because of higher water temperatures, so rematings occurred earlier. Males met more often during that year than the previous one, but male competitive interactions were still not observed. The field results support laboratory studies and demonstrate that behaviours associated with female-female competition are more prominent when the OSR is more female-biased. Correspondence to: A. Vincent     

Responses of male white ibises to their mate's extra-pair copulations

Summary I intensively observed the mating behavior of 134 pairs of white ibises for over 15 000 pair hours to examine the responses of males to extrapair copulations (EPC) involving their mates. Females often cooperated completely in apparently fertile EPCs. Male mate-guarding was vigorous and effective. Males did not respond to apparent sperm competition with forced-pair copulation, physical punishment, or abandonment of their mates. I found no negative correlation between degree of female promiscuity and the amount of parental care her mate gave to the entire brood. Males also did not reduce paternal care given to the young most likely to be the result of an EPC. I hypothesize that males are constrained in the behaviors they can use to avoid misplaced paternity in this species. While male mate-guarding reduces the opportunities for female involvement in EPC, the behaviors used by males to protect paternity apparently have not prevented the evolution of female receptiveness during EPC attempts.