Ecological correlates of social organization in a communally breeding bird,the acorn woodpecker,Melanerpes formicivorus

Summary Acorn woodpeckers (Melanerpes formicivorus) were studied during the summers of 1976 and 1977 in the Chiricahua Mountains of Arizona to determine the ecological correlates of variations in unit size, storage behavior, and home range. Unit size varied from two to five adults, acorn storage capacity varied from 0 to 5,000 individual holes per unit, and home range size varied from 5.2 to 51.2 ha.There was a consistent but nonsignificant trend for units inhabiting pine-oak woodland to be larger and to maintain more food storage holes than units in oak-juniper or oak woodland. Pine-oak woodland had the highest oak species number, density, and basal area of any community in the study area, and showed the least annual variation in percent of oaks producing acorns during the study. However, pineoak woodland also had the lowest acorn productivity per hectare.More than four times as many oak trees produced acorns in 1977 than in 1976. Following the poor 1976 crop, unit home range size increased so that the mean number of oaks contained per home range size increased more than three and a half times in 1977. The number of woodpecker units containing nonbreeding adults decreased from 90% in 1976 to 20% in 1977. These data suggest that the size and reliability of acorn crops control the composition of acorn woodpecker social units.A comparison of acorn woodpecker population parameters in the Chiricahua Mountains and at the Hastings Reservation, California, was made, using data of MacRoberts and MacRoberts (1976). The California population was significantly more dense and maintained more storage trees and more individual storage holes per unit, but there was no evidence that more California units contained nonbreeding adults than did Chiricahua units.A model is presented that emphasizes the importance of acorn crop reliability as the major determinant of acorn woodpecker social organization (Fig. 2). Annual crop fluctuations affect the winter survival and dispersion of woodpecker units, and the density of the population in the following spring. Bad acorn years will result in decreased saturation of woodpecker nesting habitat by established groups. The model predicts a corresponding decrease in the frequency of units with helpers, as young adults take advantage of opportunities to breed on their own. Longer-term crop reliability determines the benefitcost ratio for establishing and maintaining food storage facilities. The observed geographic variation in storage behavior between California and Arizona populations is suggested to reflect differences in the long-term return on investment in expensive storage facilities.     

Positive correlation between helpers at nest and nestling immune response in a cooperative breeding bird

In cooperatively breeding species, helpers may contribute to the success of the brood by increasing the number of independent offspring, but also, they may affect offspring condition and, hence, their survival and recruitment into the breeding population. This second type of benefits is rarely included in theoretical models or assessed in field studies. Immune response is a good proxy of individual quality and fitness, and there is good evidence that the performance of the immune system of chicks during the nestling phase is related to their chances of survival and future reproduction. However, no study has so far explored whether helpers at the nest might contribute to enhance immune functioning of nestlings in species with a cooperative breeding system. Here we investigate this issue in the azure-winged magpie (Cyanopica cyanus) and found for the first time a positive correlation between the number of helpers at nest and the cell-mediated immune response of nestlings. This effect was not explained by a general improvement of body condition of chicks because it was independent of individual variation in body mass or tarsus length. Our results suggest that helping can have subtle effects on the quality of offspring that may influence their survival and future reproduction.     

The dynamics of brood desertion among communally breeding females in the treehopper, Publilia concava

In species that exhibit extended parental care, females sometimes lay eggs communally in order to redistribute the costs of offspring care. Communal egg-laying often involves redundancy in female effort, such that the number of females contributing to reproduction is more than is needed to provide adequate parental care. As a result, a subset of females will often abandon the communal brood, with the time of departure ranging from immediate abandonment after egg-laying (brood parasitism) to delayed abandonment with prolonged care (cooperative breeding). In this paper I approach the parental care dynamics of female-female broods as a desertion game similar to that of mate desertion in species with bi-parental care. I describe a field study of the insect Publilia concava (Hemiptera: Membracidae), a species that exhibits communal oviposition and a full range of egg guarding. This species exhibits full redundancy in female care, with no difference in survival between singly and doubly guarded broods. I find that double guarding is extremely rare in the population, with most communal broods having only one female guard. While this guard was usually the female that initiated the brood, these same females were more likely to abandon when secondary females arrived and when secondary females exhibited longer guarding durations. Paradoxically, the secondary females usually abandoned the broods they visited, resulting in up to 50% of broods with double abandonment. These unguarded broods suffered a 50% reduction in hatching success, reflecting an important risk for primary females that abandon egg masses to secondary females. Overall, P. concava exhibits desertion dynamics similar to mate desertion in vertebrates and it is likely that the theoretical work in this area will be useful for future work that addresses the allocation of parental care among communal breeders.     

Reproductive dominance and differential ovicide in the communally breeding burying beetle Nicrophorus tomentosus

Communal breeding can be characterized by the division of reproduction among cooperating individuals and, if the distribution of reproduction is inequitable, by the mechanisms for achieving skewed reproductive success. The burying beetle (Nicrophorus tomentosus) is a facultative communal breeder. Unrelated adults, especially females, provide extensive parental care to broods of mixed parentage. The frequency and degree of reproductive skew between two females were examined experimentally. On medium-size carcasses, the proportion of eggs attributed to each female was not significantly different from random in 42% of the broods, skewed in 42% and not shared in 16%. Although reproduction was usually skewed in favor of the larger female, the relative sizes of the two females did not predict the degree of skew. On large carcasses, the proportion of eggs attributed to each female was not different from random in 87% of the broods and weakly skewed in 13%. Several mechanisms for biasing reproductive success were investigated. Females increase the proportion of their offspring in the brood by committing differential ovicide. Secondly, burying and preparing a carcass cooperatively stimulates ovarian development of the larger female and slows it for the smaller female, reducing or delaying oviposition by the subordinate. Thirdly, larger females are more likely to be dominant and are more fecund than smaller females. Received: 20 July 1996 / Accepted after revision: 30 November 1996     

The relationship between ecology and the incidence of cooperative breeding in Australian birds

Summary Australia has many cooperatively breeding species of birds. These tend to occur in eucalypt and semi-arid woodlands rather than in rainforests or deserts. They tend to be insectivores that pursue rather than sit and wait for their prey, and tend to forage on the ground rather than above it. We propose that environments where resources do not show marked seasonal fluctuations are those in which cooperative breeding is most likely to evolve. Under these conditions birds might experience difficulty acquiring the extra food necessary to breed, especially if inexperienced. When adult survival was high, young and inexperienced birds could delay breeding. Unpredictable environments may also favor cooperative breeding, but our data do not strongly support this. Groupliving would be favored further if young birds are particularly vulnerable to predators when alone. They should therefore remain in the family group and delay their dispersal unitl a suitable breeding vacancy becomes available. These hypotheses are not mutually exclusive, but are complementary. Both may be required to ensure that at least some year-old birds do not breed and also do not disperse. We believe that they give rise to predictions, which can be tested in future field studies.     

Costs of an immune challenge and terminal investment in a long-lived bird

An induced immune challenge can have two counteracting effects on an individual's reproductive investment. (1) The resource demand could increase to "fuel" the immunologic reaction, which in turn can lead to an adaptive decrease in investment in resource-costly activities, such as reproduction. One the other hand, (2) the individual could assume that the immune activity it experiences is indicative of a serious infection. The latter can lead to an adaptive increase in reproductive investment in response to the reduced prospects of survival and future reproduction, so called "terminal investment." To measure such life-history-related consequences of increased immune activity, one group of incubating female Common Eiders (Somateria mollissima) was injected with a nonpathogenic antigen (sheep red blood cells, SRBC) while controls were injected with sterile saline. The eider is a long-lived sea-duck. Females, who incubate the eggs and care for young without assistance from the male, engage in facultative anorexia during incubation leading to a large reduction in body mass. Eiders can abandon their young to other females at the cost of reduced young survival. The immune challenge resulted in a larger mass loss, a prolonged incubation period, and reduced return rate, demonstrating both short- and long-term costs of immune challenge. Additionally, in response to what might have been interpreted as reduced survival chances in immune-challenged females, these females more often tended their own brood after hatching, despite having suffered higher costs during incubation.     

Biased parental investment and reproductive success in Gabbra pastoralists

Demographic data from 848 Gabbra households are used to examine the relationships between herd size and reproductive success in relation to sex, in a traditional, pastoralist population. The number of camels in the household herd has a significant positive effect on the reproductive success of both men and women, although the effect of wealth is greater for men, as predicted from evolutionary theory. The greater the number of elder brothers a man has, the lower his reproductive success, as a result of a smaller initial herd and a later age at marriage. This is not true for women –number of elder sisters does not have a measurable effect on a woman’s fertility, although it does have a small, negative effect on the size of her dowry. These results are interpreted as competition between same-sex siblings for parental investment, in the form of their father’s herd, which is more intense between sons than daughters as parental investments are greatest in males. Received: 30 June 1995/Accepted after revision: 23 October 1995     

Sperm storage reflects within- and extra-pair mating opportunities in a cooperatively breeding bird

In passerine birds, storage and maturation of sperm takes place in the cloacal protuberance (CP), an external swelling of the reproductive organ. The considerable variation in CP size among species is presumed to be a consequence of varying levels of sperm-competition, but whether individual variation in CP size within a species also reflects sperm competition is not well established. Here, we study temporal variation in male CP size in relation to within-pair and extra-pair mating opportunities and cuckoldry risk in purple-crowned fairy-wrens Malurus coronatus. This is a socially monogamous cooperatively breeding passerine that can breed year-round and has low levels of extra-pair paternity (in 6?% of broods). We show that male CP size sharply increased a few weeks before, and rapidly regressed after his partner laid eggs, consistent with a cost of its maintenance and/or sperm production. Surprisingly, despite low levels of extra-pair paternity, CP size of non-breeding and pre-breeding males was positively correlated with the number of breeding females in the population, suggesting that CP size is sensitive to extra-pair mating opportunities. However, CP sizes do not seem to reflect cuckoldry risk: CP size of dominant males was unaffected by the presence of a subordinate that was unrelated to the dominant female, although those subordinates occasionally sire offspring, and had a larger CP than subordinates living with their mother. Our results suggest that, even in a species with low levels of extra-pair paternity, individual investment in sperm storage reflects both within-pair and, albeit to lesser extent, extra-pair mating opportunities.     

Brood parasitism disproportionately increases nest provisioning and helper recruitment in a cooperatively breeding bird

Obligate avian brood parasites lay their eggs in nests of other species (hosts), which raise parasitic young. Parasitic nestlings are likely to influence host’s parental behaviours as they typically beg for food more vigorously than young host for a given hunger level. However, few studies have tested this idea, with conflicting results. These prior studies were largely limited to biparental hosts, but little is known about the effect of brood parasitism on parental behaviours in hosts that breed cooperatively. We followed a multimodel approach to examine the effect of brood parasitism on nest provisioning and helper recruitment in the baywing (Agelaioides badius), a cooperative breeder parasitised by screaming (Molothrus rufoaxillaris) and shiny (Molothrus bonariensis) cowbirds. Multimodel inference results indicated that feeding visits increased with nestling age, cooperative group size and number of cowbird nestlings in the brood. Brood size had little influence on feeding visits, which further suggests that baywings adjusted their provisioning effort in response to cowbird parasitism. In addition, nests parasitised artificially with shiny cowbird eggs or hatchlings recruited more helpers than unmanipulated nests having only host or screaming cowbird young. Our results provide novel evidence that brood parasitism and cooperative breeding interact in determining the levels of nest provisioning.     

Neophobia and social tolerance are related to breeding group size in a semi-colonial bird

In semi-colonial species, some individuals choose to breed in isolation while others aggregate in breeding colonies. The origin and the maintenance of this pattern have been questioned, and inherited phenotype dependency of group breeding benefits has been invoked as one of the possible mechanisms for the evolution of semi-coloniality. Using field observations and behavioural tests in the semi-colonial barn swallow (Hirundo rustica), we tested the hypothesis that breeding group size is related to personality. We measured neophobia (the fear and avoidance of new things) and social tolerance of adults and showed that these two independent traits of personality are strongly related to breeding group size. The biggest colonies hosted birds with higher neophobia, and larger groups also hosted females with higher social tolerance. This parallel between group size and group composition in terms of individual personality offers a better understanding of the observed diversity in breeding group size in this species. Further studies are, however, needed to better understand the origin of the link between individual personality and group breeding strategies.     

Intra-group relatedness affects parental and helper investment rules in offspring care

In any system where multiple individuals jointly contribute to rearing offspring, conflict is expected to arise over the relative contributions of each carer. Existing theoretical work on the conflict over care has: (a) rarely considered the influence of tactical investment during offspring production on later contributions to offspring rearing; (b) concentrated mainly on biparental care, rather than cooperatively caring groups comprising both parents and helpers; and (c) typically ignored relatedness between carers as a potential influence on investment behavior. We use a game-theoretical approach to explore the effects of female production tactics and differing group relatedness structures on the expected rearing investment contributed by breeding females, breeding males, and helpers in cooperative groups. Our results suggest that the breeding female should pay higher costs overall when helpful helpers are present, as she produces additional offspring to take advantage of the available care. We find that helpers related to offspring through the breeding female rather than the breeding male should contribute less to care, and decrease their contribution as group size increases, because the female refrains from producing additional offspring to exploit them. Finally, within-group variation in helper relatedness also affects individual helper investment rules by inflating the differences between the contributions to care of dissimilar helpers. Our findings underline the importance of considering maternal investment decisions during offspring production to understand investment across the entire breeding attempt, and provide empirically testable predictions concerning the interplay between maternal, paternal and helper investment and how these are modified by different relatedness structures.     

Adjustment of female reproductive investment according to male carotenoid-based ornamentation in a gallinaceous bird

Carotenoid-based ornaments (many yellow–orange–red colourations) may signal the genetic or parental quality of the bearer. Thus, their expression could influence the amount of resources/energy that the mate will invest in the production of offspring, thereby optimising its reproductive fitness. The differential allocation hypothesis (DAH) predicts that females mated with more attractive males should lay more and better eggs. This has been explored only in few bird species with carotenoid-based traits. We tested this hypothesis in the red-legged partridge (Alectoris rufa), a gallinacean with very variable laying capacity. Both sexes display carotenoid-based ornamentation that gradually fades throughout the laying period. Here, the redness of beak and eye rings of captive males was intensified after mating by means of paint. The proportion of females that laid eggs did not differ between treatments. Amongst laying females, those mated with colour-enhanced males (experimental females) tended to lay earlier and produced significantly more eggs than controls, but of similar quality (egg mass and composition). We additionally investigated whether male attractiveness influenced egg components depending on the clutch size and laying sequence. The testosterone level in eggs from experimental females was positively related to the laying order, whereas control eggs did not show any trend. Our results provided mixed support for the DAH, but nevertheless revealed that female red-legged partridges may adjust their breeding investment according to male carotenoid-based ornamentation.     

Yolk hormones and sexual conflict over parental investment in the pied flycatcher

Female birds might be able to manipulate the parental effort of their male partner through elevated transfer of hormones to the eggs, since these hormones affect many chick traits that males might use as cues for adjusting the level of their investment. We experimentally studied whether female pied flycatchers Ficedula hypoleuca could manipulate male investment via yolk androgens. There is much more variation in yolk androgen levels between females than within clutches, and in order to change the androgen levels of the eggs, we swapped whole clutches between nests. To estimate the androgen levels of the clutch, we measured the androgen content of a single egg per clutch. Females did not succeed in manipulating male effort using yolk androgens, since there was no relationship between the division of parental care within a pair and either original or foster egg androgen levels. One of these relationships should have occurred if females were manipulating males. The proportion of feeding visits by the male was higher when the male was old (55%) than when he was young (45%) and females laid eggs with higher androgen levels when mated with a young male. Young males did not exhibit any responses to yolk androgen levels either, which indicates that females cannot exploit their effort more than that of old males. We suggest that females may allocate yolk androgens to adjust the growth trajectories of the chicks to poor growing conditions when mated with young males that are poor providers or occupying a poor territory.     

Mean colony relatedness is a poor predictor of colony structure and female philopatry in the communally breeding Bechstein's bat (Myotis bechsteinii)

In order to understand why animals are social and how group members interact with each other it is important to know their relatedness. However, few studies have investigated the genealogy in complete social groups of free-living animals with low reproductive skew. This holds particularly true for bats. Although almost all bat species are social, their sociobiology is not well understood. Because they are volant, nocturnal and have a rather cryptic life-style, bats are difficult to observe in the wild. Furthermore females are generally gregarious making genetic parent-offspring assignment a challenging task. We used genetic markers in combination with knowledge about age and colony membership of individually marked bats to construct pedigrees in completely sampled maternity colonies of Bechstein's bats (Myotis bechsteinii). Despite considerable fluctuations in population size, no immigration occurred over 5 years in four colonies living in close proximity. Additionally, confrontation tests showed that females of one maternity colony were able to detect and attempted to prevent the intrusion of foreign females into a roost they occupy. Although colonies were absolutely closed, and 75% of the colony members lived together with close relatives (rS=0.25), mean colony relatedness was nearly zero (0.02). Average relatedness therefore is a poor estimator for the potential of kin selection in Bechstein's bat colonies and may be misleading when attempting to understand the social structure of animals living in groups where many members breed. Based on our results we discuss the potential adaptive value of living in closed societies with low reproductive skew.