Brood sex ratio is dependent on female mating status in polygynous great reed warblers

Females capable of adjusting the sex ratio of their offspring should be more fit than females lacking such an ability. In polygynous birds where breeding success in males is more strongly influenced by body size and/or attractiveness than in females, females might produce more sons when predicting good conditions or when mating with attractive males. Polygynous great reed warbler, Acrocephalusarundinaceus, males direct most of their feeding effort to the primary (first-hatching) nest and in these nests increase their feeding effort in relation to the brood sex ratio (proportion of sons). Therefore, with the expectation of well-nourished sons, we would predict that females which start breeding first within harems might produce more sons than those which start breeding later, and in anticipation of sons with good genes, that females mated to polygynous males might produce more sons than females mated to monogamous males. I took blood samples from hatchlings and determined the sex using DNA markers. The sex ratio of primary (monogamous and polygynous primary) broods is more male-biased (mean 0.58 males, n = 50) than that of secondary (polygynous secondary and tertiary) broods (mean 0.46, n = 25). Moreover, in the secondary broods with the largest clutch (five eggs), in which offspring are most likely to suffer food shortage, the sex ratio was distinctively female biased (mean 0.33, n = 10). In the primary broods, sex ratio was correlated to harem size. The results suggest that great reed warbler females modify the brood sex ratio to produce both well-nourished sons and sons with good genes, but the former effect is probably stronger than the latter factor. Received: 11 March 1998 / Accepted after revision: 23 May 1998     

Breeding success of a brood parasite is associated with social mating status of its host

Reproductive success of brood parasites varies considerably both among and within host species, mainly due to differences in host egg-rejection rates and survival of parasitic chicks. Here, we investigated the breeding success of the cuckoo (Cuculus canorus) in one of its major hosts, the great reed warbler (Acrocephalus arundinaceus), with respect to host social mating status. In this passerine, polygynous males provide less parental care to their young per nest than monogamous males. Consequently, their less-assisted females may fledge lower numbers of nestlings than monogamous females. This may be especially true for secondary females, which often receive limited or no paternal help with young at all. Based on these findings, we expected higher cuckoo reproductive success in nests of socially monogamous than polygynous great reed warbler males. More specifically, we predicted lower fledging success of cuckoo young in nests of secondary than primary or monogamous females. In line with the prediction, we found higher cuckoo fledging success in nests of monogamous than polygynous males, monogamous nests being more than twice as successful as secondary nests. We detected, however, only a tendency to lower cuckoo success in primary compared to monogamous nests and no differences between primary and secondary nests. Moreover, neither parasitism nor host egg-rejection rates differed among the nests of different status. Our results show, for the first time, that the social mating status of a host may influence the overall reproductive success of a brood parasite and thus should be considered in further studies.     

Paternal expenditure is related to brood sex ratio in polygynous great reed warblers

In many polygynous animals, parents invest more heavily in individual sons than in daughters. However, it is unclear if these differences in investment are a consequence of sex differences in the demand of offspring related to sexual size dimorphism or a consequence of parental manipulation. Here, we report on parental food delivery frequency in relation to brood size and brood sex ratio in a wild population of polygynous great reed warblers Acrocephalus arundinaceus. We used the polymorphic microsatellite loci on the Z chromosome to sex chicks. We found that paternal feeding frequency (times/h per nest) increased not with brood size, but with the proportion of males in the brood, although the demand per nest was more closely related to brood size than to brood sex ratio. Additionally, the increase in rate of paternal feeding frequency in relation to the brood sex ratio was much higher than the increase in rate of nestling food demands. Maternal feeding frequency was independent of both brood size and brood sex ratio. These results strongly suggest that fathers preferentially invest in their sons. We propose that parents can afford sex-biased parental care in animals in which food provisioning is enough for all offspring to survive. Received: 22 January 1996/Accepted after revision: 30 June 1996     

Nestling provisioning in polygynous great reed warblers (Acrocephalus arundinaceus): do males bring larger prey to compensate for fewer nest visits?

Most studies of social polygyny in birds have examined male provisioning on the basis of the number of feeding visits. This may be misleading if males compensate for infrequent visits by bringing larger prey at each visit. We investigated nestling provisioning in the socially polygynous great reed warbler, Acrocephalus arundinaceus, in south Central Sweden in 1996–1997. We collected data on rate of feeding visits, prey size and the amount of biomass delivered by males and females. Males had lower rates of feeding visits and provided smaller prey to nestlings in secondary than in monogamous and primary nests. Secondary females had higher rates of feeding visits and brought larger prey than monogamous and primary females. These results confirm that secondary females face a potential cost of polygyny through a lower rate of male feeding, and that this cost was reinforced by the significantly lower male provisioning rate (biomass h^–1) at secondary nests. Secondary females compensated for the lack of male assistance by increasing their rate of feeding and bringing larger prey. As a result, offspring in nests of secondary females received as much food as did those in nests of primary females. Prey load size increased with the parent’s proportion of feeding visits, suggesting that parents use different feeding strategies depending on their amount of responsibility for nestling provisioning. We suggest that parents which take the main responsibility for nestling feeding have to forage further away from the nest, and based on optimal-foraging theory, they should then on average bring larger prey to their nest. Received: 4 April 1999 / Received in revised form: 12 October 1999 / Accepted: 23 October 1999     

Host species affects the growth rate of cuckoo (Cuculus canorus) chicks

The cuckoo (Cuculus canorus) is an obligate interspecific brood parasite. When about to lay an egg, the female must decide which nest to parasitise. A high-quality host species should be preferred, to enhance the possibility of producing a viable offspring. In this study, we investigated the effects of two closely related host species, the great reed warbler (Acrocephalus arundinaceus) and the reed warbler (A. scirpaceus) on the growth rate of cuckoo nestlings. We found that cuckoo nestlings raised by the larger host species, the great reed warbler, grew significantly faster and became statistically significantly larger at fledging than nestlings raised by the smaller host, the reed warbler. Our results indicate a qualitative difference between the two host species. The great reed warbler, considered to be the best host, was parasitised at a higher rate than the reed warbler. Received: 2 February 1999 / Received in revised form: 3 September 1999 / Accepted: 18 September 1999     

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).     

Eggshell strength of an obligate brood parasite: a test of the puncture resistance hypothesis

Eggs of several brood parasites have thicker and stronger shells than expected for their size. The present study evaluated the puncture resistance hypothesis for the occurrence of thick-shelled eggs in common cuckoos Cuculus canorus by investigating costs of cuckoo egg ejection in four Acrocephalus warblers—the great reed warbler A. arundinaceus, reed warbler A. scirpaceus, marsh warbler A. palustris and sedge warbler A. schoenobaenus. The three latter species all suffered ejection costs, while ejection was not costly in the larger great reed warbler. The occurrence of ejection costs was negatively related to host bill size. In the marsh warbler, we compared ejection costs in naturally parasitized nests and two experimental treatments, in which broods were parasitized artificially with great reed warbler and conspecific eggs. Hosts damaged their own eggs significantly more often when ejecting the thick-shelled cuckoo eggs than when ejecting the similarly sized but thinner-shelled great reed warbler eggs, providing some support for the puncture resistance hypothesis. Ejection of conspecific eggs did not involve any costs. Furthermore, contrary to predictions derived from the laying damage hypothesis, there was no evidence that egg damage was associated with cuckoo egg laying. Hosts damaging their own eggs during ejection were more likely to subsequently desert their clutches than those that did not. The frequency of clutches smeared with the contents of the ejected egg were positively related to the hypothesized difficulty of foreign egg puncturing. Potential advantages of thicker shells in common cuckoo eggs are discussed.     

Trade-off between mate guarding and mate attraction in the polygynous great reed warbler

Summary In a Swedish population of the polygynous great reed warbler Acrocephalus arundinaceus, about 40% of the males formed pairs with more than one female. Males sang two completely separated types of song: (1) long song when they tried to attract mates and (2) short shong when they guarded a fertile female. As soon as a male had attracted a female he immediately switched from long to short song and apparently guarded her for at least 3 days. Most males left their female and started singing long several days before her fertile period ended. This behavior probably increased the risk of cuckoldry. By assuming that males of polygynous species maximize their fitness over the whole breeding season (i.e., maximize fitness rate), we predicted longer mate guarding periods when the probability of attracting a second female was low and the risk of cuckoldry was high. These predictions were supported by observations. The probability of attracting a second female decreased during the breeding season and, in accordance, the number of days that males sang long song during the primary female's fertile period was negatively correlated with the time of the season. This trend held also for individual males when comparing mating periods of their primary and secondary female. The increasing rate of male intrusions with season may also have contributed to the increasing mate guarding periods. Offprint requests to: D. Hasselquist     

Evidence of equal maternal investment in the sexes in the polygynous and sexually dimorphic grey seal (Halichoerus grypus)

In polygynous and sexually dimorphic mammals, parents may be expected to bias their investment towards sons because variation in reproductive success is usually higher among males than among females. Moreover, male reproductive success often depends on adult body size, which, in turn, may depend on the level of parental investment. We therefore predicted that in the grey seal (Halichoerus grypus), a polygynous and sexually dimorphic phocid seal, females should invest more in individual sons than in individual daughters. We found that male pups were born heavier than female pups, but that the growth rates and suckling behaviour were similar for the two sexes. The growth rates and the birth weights were not correlated for the pups of either sex. Mothers did not behave differentially towards offspring of the two sexes, except that mothers of male pups spent more time in visual contact with their pups. Male and female pups had similar activity levels and begged at similar rates. We argue that reports of equal expenditure on the two sexes can be accepted as evidence of equal investment, provided that three assumptions are fulfilled. First, parental care must be costly to the parent. Second, energy expenditure must be the most important component of parental investment. Third, there must be no negative correlation between maternal body condition and the ratio of sons to daughters produced. We argue that these assumptions are met in our study, and that our results provide evidence of equal maternal investment in the sexes in grey seals.     

Cuckoo growth performance in parasitized and unused hosts: not only host size matters

The quality and quantity of food delivered to young are among the major determinants of fitness. A parental provisioning capacity is known to increase with body size. Therefore, brood parasitism provides an opportunity to test the effects of varying provisioning abilities of different-sized hosts on parasitic chick growth and fledging success. Knowledge of growth patterns of common cuckoo, Cuculus canorus, chicks in nests of common hosts is very poor. Moreover, no study to date has focused on any currently unused hosts (i.e., suitable cuckoo host species in which parasitism is currently rare or absent). Here, I compare the growth performance of cuckoo chicks in nests of a common host (the reed warbler, Acrocephalus scirpaceus) and two unparasitized hosts (the song thrush, Turdus philomelos, and the blackbird, Turdus merula). Parasitic chicks were sole occupants of the observed nests, thus eliminating the confounding effect of competition with host chicks. Experiments revealed striking differences in parasitic chick growth in the two closely related Turdus hosts. Cuckoo chicks cross-fostered to song thrush nests grew much quicker and attained much higher mass at fledging than those in nests of their common reed warbler host. Alternatively, parasitic chicks in blackbird nests grew poorly and did not survive until fledging. I discuss these observations with respect to host selection by parasitic cuckoos.     

Interactions among females in polygynous yellow-headed blackbirds

Summary Two alternative hypotheses which attempt to predict how females within harems in polygynous species should behave toward one another were examined in a population of yellow-headed blackbirds (Xanthocephalus xanthocephalus). The hypothesis that females within a harem are co-operative was not supported. Females in large harems did not enjoy higher reproductive success than those in smaller harems and females within a territory did not initiate their nests close in time or space. The alternative hypothesis that females within a harem are competitive was also not supported. Nest density did not have a negative effect on female reproductive success, females within a territory did not initiate their nests far apart in time or space, and resident females were not very aggressive toward intruding female mounts during the settling period. The data support the idea that females settled independently of one another and had no effect on one another's reproductive success.     

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.     

Tests for a biased sex ratio when the data are clustered

In behavioral ecology the overall sex ratio in a population of birds is often tested to see if it differs from a 50/50 ratio. In recent publications the binomial test or the ² test are carried out although the sexes of chicks within the same nest may not be independent. The lack of independence occurs since female birds can adjust the sex ratio in an adaptive way as demonstrated in recent studies. In order to take dependence into consideration the Wilcoxon signed rank test based on the within-brood differences between the proportions of sons and daughters was performed in a study investigating great tit hatchling sex ratios. We compare this test with a test based on an optimally weighted estimator recently proposed for medical studies with clustered binary data. According to our simulation results, this novel test is more powerful than the Wilcoxon signed rank test and should be used for the analysis of avian sex ratios. The methods are illustrated with real data from the great reed warbler.     

Experimental support for the use of egg uniformity in parasite egg discrimination by cuckoo hosts

Common cuckoo (Cuculus canorus) parasitism drastically reduces the reproductive success of their hosts and selects for host discrimination of cuckoo eggs. In a second stage of anti-parasite adaptation, once cuckoos can lay eggs that mimic those of their hosts, a high uniformity of host egg appearance within a clutch may favour cuckoo egg discrimination. Comparative evidence provides indirect support for this hypothesis although experimental support is currently lacking. Here, we studied the effect of experimentally decreased uniformity of host egg appearance on cuckoo egg discrimination by great reed warbler (Acrocephalus arundinaceus) hosts in a population in which long-term cuckoo parasitism has led to high levels of cuckoo–host egg mimesis. We manipulated host clutch uniformity by adding extra spots to fresh host eggs just after they were laid. Rejection of non-mimetic experimental eggs added to these nests was compared with those in control nests in which uniformity was not altered. Previously, by over-painting real spots in a control group of nests, we showed a negligible effect of our paints on hosts’ perception of their eggs. We show that for the great reed warbler, non-mimetic experimental eggs were relatively more tolerated in experimental nests, i.e. with lower uniformity (40%) than in control nests (5%). This is the first experimental study, to our knowledge, which demonstrates a reduced discrimination of foreign eggs as a consequence of an increase of egg phenotypes variation perception in a cuckoo host.     

Female-biased sex allocation of offspring by an <Emphasis Type="Italic">Apodemus</Emphasis> mouse in an unstable environment

We investigated the effects of population fluctuation on the offspring’s sex allocation by a weakly polygynous mouse, Apodemus argenteus, for 3 years. In acorn-poor seasons, heavier mothers invested more in sons, and lighter mothers invested more in daughters. In acorn-rich seasons, heavier mothers invested more in daughters, and lighter mothers invested more in sons. Maternal body condition and litter size affected the sex allocation. Furthermore, there was a maternal investment trade-off between a son’s birth mass and the number of daughters. Based upon the effect of population fluctuation on the lifetime reproductive success of each sex, we proposed the new “safe bet hypothesis”. This hypothesis predicts that frequent and unpredictable change in female distribution, which is often caused by abrupt fall in food condition, favors female-biased maternal investment to offspring by polygynous mammals and is applicable to many small mammals inhabiting in unstable environments.     

Adaptive significance of sex ratio adjustment in semifree-ranging Barbary macaques (Macaca sylvanus) at Salem

Summary New data on the secondary sex ratio in semi-free-ranging Barbary macaques at Salem confirm the observation that the offspring of high-ranking females in this colony are biased towards sons while the offspring of low-ranking females are biased towards daughters. Analysis of interbirth intervals yielded no consistent differences in the relative costs of rearing male and female offspring for either high- or low-ranking females. Survivorship to adulthood of male and female offspring born to mothers of all rank classes was remarkably high, and there was no indication that juvenile females of low-ranking mothers face any greater risk. Daughters of high- and low-ranking mothers showed no substantial differences in reproductive success, while mating and probably reproductive success of sons seemed to be dependent on maternal rank, at least at the beginning of their reproductive career. The results suggest that variation in sex ratio does increase parental fitness. Offprint requests to: A. Paul     

Cooperatively breeding carrion crows adjust offspring sex ratio according to group composition

In cooperatively breeding species, parents should bias offspring sex ratio towards the philopatric sex to obtain new helpers (helper repayment hypothesis). However, philopatric offspring might increase within-group competition for resources (local resource competition hypothesis), diluting the benefits of helper acquisition. Furthermore, benefits of offspring sex bias on parents’ fitness may depend on different costs of production and/or different breeding opportunities of sons and daughters. Because of these counteracting factors, strategies of offspring sex allocation in cooperative species are often difficult to investigate. In carrion crows Corvus corone corone in northern Spain, sons are more philopatric and more helpful at the nest than daughters, which disperse earlier and have higher chances to find a breeding vacancy. Consistent with the helper repayment hypothesis, we found that crows fledged more sons in groups short of subordinate males than in groups with sufficient helper contingent, where daughters were preferred. Crow females also proved able to bias primary sex ratio, allocating offspring sex along the hatching sequence in a way that provided the highest fledging probability to sons in the first breeding attempt and to daughters in the following ones. The higher cost of producing male offspring may explain this pattern, with breeding females shifting to the cheapest sex (female) as a response to the costs generated by previous reproductive attempts. Our results suggest complex adjustments of offspring sex ratio that allowed crows to maximize the value of daughters and sons.     

Adaptive sex allocation by brood reduction in antechinuses

Antechinuses (Dasyuridae: Marsupialia) exhibit dramatic interpopulation variation in the sex ratio at birth, a pattern which has previously been interpreted in terms of both local resource competition and Trivers/Willard effects. However, Antechinus stuartii usually fail to wean all the young that attach to their teats. At least in captivity, this is because they often eat their young. In free-living populations, brood reduction affects sons and daughters differently. Mothers virtually always wean some daughters. The probability that a daughter will be weaned declines with the number of daughters in the pouch. The health or quality of the mother does not affect the number of daughters weaned. By contrast, mothers tend to wean all or none of their sons. A strong correlate of infanticide against sons is senescence. Old mothers rarely invest in sons, and produce low-quality daughters. Mothers suffer a direct cost (mortality during lace lactation) of male-biased litters. Coupled with data on prenatal sex allocation, these results support the conjoint influence of local resource competition and the Trivers-Willard effect. However, they suggest that in populations where females are largely semelparous, the population optimum generated by local resource competition may be unattainable, because of the importance of producing at least one daughter. These observations support recent theoretical claims that the sex ratio at the population level is not easily predicted, but suggest that the diversity of mammalian sex allocation tactics has been underestimated.     

Relatedness and sex ratio in a primitively eusocial halictine bee

Lasioglossum laevissimum was studied in Calgary, Alberta, where it is eusocial with one worker brood. Estimates of relatedness were obtained among various categories of nestmate based upon four polymorphic enzyme loci, two of which exhibited significant levels of linkage disequilibrium. Relatedness estimates among workers and among reproductive brood females were very close to the expected 0.75 value that obtains when nests are headed by one, singly mated queen. However, relatedness between workers and the reproductive brood females they reared was significantly lower than 0.75. A low frequency of orphaning with subsequent monopolisation of oviposition by one worker brood female in orphaned nests may explain these results. Workers were significantly more and queens significantly less closely related to male reproductives than expected if all males were to have resulted from queen-laid eggs. Orphaning and worker-produced males contribute to this result. The sex investment ratio was 1:2.2 in favour of females, in excellent agreement with the predictions based upon relative relatednesses between workers and reproductive brood males and females. Adaptive intercolony variation in investment ratios was detected: the sex ratio was more heavily female-biased in nests in which the relative relatedness asymmetry between workers and reproductive brood was more female-biased. The study species is the most weakly eusocial hymenopteran for which relatedness estimates and sex ratio data are available. With high relatedness among nestmates and a strongly female-biased sex ratio, this study suggests the importance of indirect fitness contributions in the early stages of social evolution. Correspondence to: L. Packer     

Extra-pair paternity in the facultatively polygynous spotless starling,<Emphasis Type="Italic"> Sturnus unicolor</Emphasis>

A potential cost of polygyny that may have restrained its evolution in some avian species is the presence of extra-pair offspring in the nests of males mated with several females. However, this relationship is not frequently found and an experimental approach investigating the association between extra-pair offspring and polygyny, while controlling for male traits related to polygyny, has not been undertaken. In this study, we manipulated the testosterone levels of facultatively polygynous spotless starlings, Sturnus unicolor, to establish experimentally different groups of polygyny and analyse its influence on levels of extra-pair offspring in males for which other traits were randomised. During two consecutive breeding seasons, we examined the effects of harem size on the ability of males to assure genetic paternity, assessed by DNA fingerprinting, and on reproductive success in their own nests. The frequency of extra-pair fertilisations varied between 10% (14/140) in 1996 and 20% (39/194) in 1997. Year-to-year analyses of extra-pair paternity variables with treatment as factor and harem size (number of simultaneous mated females) as covariate, were significant only in relation to harem size. Males with few simultaneously mated females were less cuckolded than more polygynous males in 1997 but not in 1996, indicating that mating costs of polygyny occurred, at least in the year with the higher rate of extra-pair paternity. Because polygynous males have more social mates, they may accrue higher reproductive success irrespective of their risk of being cuckolded. However, our results suggest that to be polygynous is costly in terms of paternity loss when we experimentally induce mating status controlling for individual male traits. However, the low values of our power tests for the statistically non-significant results of hormone on cuckoldry do not allow us to discard this hormone effect altogether.