Effect of parentage and relatedness on the individual contribution to cooperative chick care in carrion crows Corvus corone corone

Carrion crows Corvus corone corone in northern Spain form complex cooperative groups that contain non-dispersing offspring and immigrants. Reproduction is often shared among group members, with polyandry prevalent over joint egg laying. However, due to incest avoidance or sexual immaturity, reproduction is potentially available only to a fraction of group members (potential breeders), while others do not breed (non-breeders). We combined molecular data with video-recorded observations at nests in order to investigate whether potential breeders and non-breeders adjust their individual effort in nestling feeding respectively to their level of parentage and the relatedness with the chicks. Overall, parents of at least one chick in the brood showed the highest feeding rates. Among potential breeders, genetic mothers and fathers fed chicks at significantly higher rates than individuals with no parentage, but they did not adjust their effort according to the proportion of offspring generated. Current direct fitness benefits are therefore important in determining a high provisioning effort, but crows may lack a mechanism to finely assess their share of parentage. Among non-breeders, males contributed more than females to chick feeding, but we found no significant correlation between feeding rate and relatedness to the nestling. We discuss how the latter result can be reconciled with the fact that kin selection has been shown to be important in shaping the crow cooperative society.Communicated by C. Brown     

Deception by helpers in cooperatively breeding white-winged choughs and its experimental manipulation

White-winged choughs (Corcorax melanorhamphos) are obligate cooperative breeders, living in groups which may contain up to 20 birds. Although breeding is dominated by a single pair, all birds contribute to rearing young, including the provisioning of nestlings. However, some birds which have carried food to the nest, even to the point of placing the food in the gaping mouth of a nestling, consume the food themselves rather than provision the nestlings. Birds which fail to feed nestlings are typically young, and are only likely to fail to deliver food when they cannot be observed by other group members. Birds which have just failed to deliver food are more likely to engage in alternative helping behaviours such as allopreening the nestlings than are helpers which have just delivered food in the conventional manner. Failure to deliver food is almost eliminated when foraging constraints are experimentally reduced by supplemental feeding of the group. Collectively these observations suggest that young white-winged choughs act deceptively by simulating helping behaviours without sacrificing food supplies. Received: 24 January 1997 / Accepted after revision: 6 June 1997     

Cooperative breeding and immunity: a comparative study of PHA response in African birds

Cooperatively breeding birds might be expected to suffer from higher costs of parasitism than pair-breeding species because of two aspects of their ecology which should facilitate horizontal transmission and possibly select for higher parasite virulence: first, they interact regularly with more individuals than pair-breeding species, and second, these individuals are commonly close relatives that could share similar resistance alleles. This hypothesis predicts that cooperative breeders should invest relatively more in immune defence than closely related species which breed in pairs. I tested this prediction comparatively in African birds by examining the response of the immune system to the mitogenic lectin, phytoahemagglutinin (PHA response) in relation to cooperative breeding. Among 66 species, of which 18 breed cooperatively, PHA response was significantly higher in cooperatively breeding species. This association appeared not to be confounded by body size, clutch size, nest position, coloniality or similarity owing to common phylogenetic descent. These results suggest that cooperatively breeding birds may have been selected to invest more than pair-breeders in defences against parasites. If so, then additional costs of philopatry and helping behaviour might be imposed on breeders, helpers and offspring.     

Social system and reproduction of helpers in a cooperatively breeding cichlid fish (Julidochromis ornatus) in Lake Tanganyika: field observations and parentage analyses

It is suggested that some fish of the genus Julidochromis, substrate-brooding Tanganyikan cichlids with biparental care, breed cooperatively with helpers. We studied the social system of J. ornatus in the wild and analysed genetic parentage using microsatellites. Within the studied population three patterns of social system were identified: monogamous pairs (61%, 44 of 72 groups), pairs with helpers (29%, 21), and polygamous harems with helpers (controlled by either a large female or large male owner; 10%, 7). In cooperatively breeding groups, the number of helpers at each nest ranged from 1 to 6 (median 1), and male helpers were more numerous than female helpers. In both sexes, the body size was different among individuals of different social status (harem owner > breeder > helper). Helpers and harem owners of both sexes exhibited brood defence although its frequency was low. The molecular analysis revealed that (1) the helpers were mostly unrelated to dominant breeders, (2) many helpers of both sexes contributed genetically to the next generations, (3) male helpers had high siring success (41% of young in total), and (4) large young unrelated to group members were detected at 30% of observed nests, which may be due to breeder (or helper) replacements and immigration of young. We discuss the implications of these results for understanding the complex social system of this species, especially the low reproductive skew in comparison with other cooperatively breeding cichlids.     

Family insurance: kin selection and cooperative breeding in a solitary primate (Microcebus murinus)

Lactation imposes substantial physiological costs on mothers and should therefore not be directed towards foreign offspring. Such allonursing, however, is common in mammal species that share roosts. Hypotheses to explain allonursing among such plural breeders include misdirected parental care, milk evacuation, brood parasitism, reciprocity, and kin selection. The necessary behavioral data, in combination with data on kinship and kin recognition, have rarely been available to distinguish among these explanations, however. In this study, we provide evidence for cooperative nursing and adoption by plural-breeding females in a nocturnal primate, the gray mouse lemur (Microcebus murinus), in which females forage solitarily during the night, but form day-time sleeping groups with one to two other females. We observed 34 resident females in an 8 ha study area in Kirindy Forest, Madagascar, over three consecutive annual breeding seasons and determined genetic relationships among all members of this population. Five sleeping groups of adult females were filmed inside their roosts during one breeding season after females gave birth. The composition of groups changed substantially across years, but they always consisted of close maternal relatives. All females within a group gave birth to one to three infants. They regularly transferred only their own offspring among roosting sites, demonstrating an ability to discriminate between their own and other’s offspring, but they regularly groomed and nursed related offspring other than their own and adopted related dependent young after their mother’s death. Kin selection may therefore be the main selective force behind cooperative breeding among these closely related females with a high mortality risk, providing each of them with family insurance.     

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.     

Reproductive success in a low skew, communal breeding mammal: the banded mongoose, Mungos mungo

In most cooperatively breeding species, reproduction is monopolised by a subset of group members. However, in some species most or all individuals breed. The factors that affect reproductive success in such species are vital to understanding why multiple females breed. A key issue is whether or not the presence of other breeders is costly to an individual’s reproductive success. This study examines the factors that affect the post-parturition component of reproductive success in groups of communal-breeding banded mongoose (Mungos mungo), where up to ten females breed together. Per-litter reproductive success was low (only 18% of pups survived from birth to independence). Whilst singular breeding was wholly unsuccessful, there were costs associated with breeding in the presence of increasing numbers of other females and in large groups. Synchronisation of parturition increased litter success, probably because it minimises the opportunity for infanticide or decreases competitive asymmetry between pups born to different females. There was no evidence of inbreeding depression, and reproductive success was generally higher in litters where females only had access to related males within their group. I conclude that communal breeding in female banded mongooses represents a compromise between the benefits of group-living and communal pup care on the one hand, and competition between females to maximise their personal reproductive success on the other. Such conflicts are likely to occur in most communal breeding species. Whilst communal breeding systems are generally considered egalitarian, negative effects of co-breeders on individual reproductive success is still an issue.     

Plasma levels of androgens and gonadal development of breeders and helpers in the bell miner (Manorina melanophrys)

Plasma concentration of androgens and gonad development were studied in wild cooperatively breeding bell miners (Manorina melanophrys) of different age, sex and social status. Plasma levels of androgens increased with age of birds. For sexually mature (SM) bell miners, androgen levels were higher in breeders than in nonbreeding (NB) helpers (P < 0.005), and they were marginally higher in females than in males (P < 0.10). Thus female breeders showed the highest plasma levels of androgens. This pattern may be explained by an asymmetry between the sexes in the levels of competition needed to reach and defend breeding status; the degree of intra-sexual competition seems to be higher among female bell miners than among males. In general, male breeders had larger gonads than male SMNB helpers; male breeder gonads produced spermatozoa whereas most helpers' gonads did not. However, old (i.e. 34 months) SMNB male helpers had large gonads producing spermatozoa in spite of having low plasma levels of androgens. We suggest that young male bell miners may be under a voluntary mechanism of reproductive suppression perhaps favoured by inbreeding avoidance; although some aggressive interactions observed between very young helpers (about 2 months) and adult members of the breeding unit suggests that a certain degree of imposition also occurs at young ages. Older male helpers may avoid aggression with the male breeder and imposed reproductive suppression, hence the low circulating levels of androgens, but they have the potential to sneak extra-pair copulations. Gonad size decreased during the non-breeding season in both sexes.     

Aggression and submission reflect reproductive conflict between females in cooperatively breeding meerkats Suricata suricatta

In many cooperatively breeding species, dominant females suppress reproduction in subordinates. Although it is commonly assumed that aggression from dominant females plays a role in reproductive suppression, little is known about the distribution of aggressive interactions. Here, we investigate the distribution of aggressive and submissive interactions among female meerkats (Suricata suricatta). In this species, dominant females produce more than 80% of the litters, but older subordinates occasionally breed. Dominant females commonly kill the pups of subordinates and usually evict older female subordinates from the group 1–3 weeks before the birth of the dominant female's litter. The aggression frequency of the dominant female toward subordinates and the submission frequency that each subordinate female showed to the dominant female increased as the age of the subordinate female increased and as the birth of the dominant female's pups approached. Moreover, as birth approached, both of these behaviors intensified more quickly between the dominant female and older subordinates than between the dominant female and younger subordinates. The aggression frequency of the dominant female toward each subordinate female predicted whether that subordinate female was evicted from the group; the submission frequency by each subordinate female predicted the timing of their eviction during the pregnancy period of the dominant female. These results support the idea that conflict between dominant and subordinate females increases with the age of subordinates and, since older subordinate females are most likely to reproduce, suggest that dominant females may less easily control reproductive attempts by older subordinate females.     

Delayed dispersal as a potential route to cooperative breeding in ambrosia beetles

Xyleborini are a species-rich tribe of ambrosia beetles, which are haplodiploid and typically mate among siblings within their natal brood chamber. Several characteristics of this tribe would predict the evolution of higher levels of sociality: high genetic relatedness within galleries due to inbreeding, high costs of dispersal and the potential benefit of cooperation in brood care within the natal gallery (e.g. by fungus gardening, gallery extension, offspring feeding and cleaning). However, information on the social system of these beetles is very limited. We examined the potential for cooperative breeding in Xyleborinus saxeseni by monitoring dispersal in relation to brood size and composition. Results show that adult female offspring delay dispersal despite dispersal opportunities, and apparently some females never disperse. The females’ decision to stay seems to depend on the presence of eggs and dependent siblings. We found no indication that female offspring reproduce in their natal gallery, as colonies with many mature daughters do not contain more eggs than those with few or no daughters. There is a significant positive relationship between the number of females present and the number of dependent siblings (but not eggs), which suggests that cooperative brood care of female offspring raises colony productivity by improving survival rates of immatures. Our results suggest that cooperative breeding is likely to occur in X. saxeseni and possibly other xyleborine species. We argue that a closer look at sociality within this tribe may yield important information on the factors determining the evolution of cooperative breeding and advanced social organization.     

Tug-of-war over reproduction in a cooperatively breeding cichlid

In group-living animals, dominants may suppress subordinate reproduction directly and indirectly, thereby skewing reproduction in their favour. In this study, we show experimentally that this ability (‘power’) is influenced by resource distribution and the body size difference between unrelated dominants and subordinates in the cichlid Neolamprologus pulcher. Reproduction was strongly skewed towards the dominant female, due to these females producing more and larger clutches and those clutches surviving egg eating better than those of subordinate females, but was not so when subordinates defended a patch. If breeding shelters were provided in two patches, subordinate females were more likely to exclusively defend a patch against the dominant female and breed, compared to when the same breeding resource was provided in one patch. Relatively large subordinate females were more likely to defend a patch and reproduce. Females also directly interfered with each other’s reproduction by eating the competitors’ eggs, at which dominants were more successful. Although dominant females benefited from subordinate females due to alloparental care and an increase in egg mass, they also showed costs due to reduced growth in the presence of subordinates. The results support the view that the dominant’s power to control subordinate reproduction determines reproductive partitioning, in agreement with the predictions from tug-of-war models of reproductive skew.     

Behavioral and demographic changes following the loss of the breeding female in cooperatively breeding marmosets

Recent models of the evolution and dynamics of family structure in cooperatively breeding vertebrates predict that the opening of breeding vacancies in cooperatively breeding groups will result in (1) dispersal movements to fill the reproductive position, and (2) within-group conflict over access to reproduction. We describe the behavioral and demographic changes that followed the creation of breeding vacancies in three wild groups of cooperatively breeding common marmosets (Callithrix jacchus). Replacement of the breeding female was rapid when no adult females remained in the group, but did not occur for several months when other adult females were present. Aggression of adult animals towards same-sex potential immigrants was associated with a period of reduced affiliation, increased intragroup agonism, no intragroup sexual behavior, and frequent extragroup copulations. This ended with the fissioning of groups along sexual lines. After replacement, multiple males copulated with multiple females and vice versa, with no increases in sexually related aggression. Female-female conflict was resolved through infanticide. The lack of direct conflict between males is consistent with cooperative polyandry. After a breeding vacancy appeared, marmoset groups showed conflict of interests among group members similar to those shown by cooperatively breeding birds, but they used different behavioral mechanisms to resolve those conflicts. Our data provide important evidence from a cooperatively breeding mammal to support Emlen’s model for the evolution of vertebrate families, but they suggest that species-specific inter- and intrasexual competitive strategies should be considered before the model can be applied to other cooperatively breeding vertebrates. Received: 23 November 1999 / Received in revised form: 28 March 2000 / Accepted: 1 April 2000     

The relationship between presumed gamete contribution and parental investment in a communally breeding bird

Summary Measures of relative gamete contribution were related to degree of parental investment for both males and females from six groups of communally breeding pukeko (Porphyrio porphyrio). If there is a fitness cost to participation in parental duties, then for males parental investment should relate to degree of confidence of paternity while for females investment should relate to the number of eggs laid. Data were analysed in two ways: (1) by looking at individuals of the same sex within the same group to see if males that had a greater probability of paternity and females that had greater number of eggs in a nest subsequently invested relatively more in parental duties and (2) by pooling the data from the six groups and determining if there was a positive correlation between measures of presumed gamete contribution and amount of parental investment. The results from both types of analyses are variable and give no clear support for a positive relationship between presumed gamete contribution and parental investment even though a possible fitness cost is suggested. Factors which might influence investment are discussed.     

Helpers and egg investment in the cooperatively breeding acorn woodpecker: testing the concealed helper effects hypothesis

In cooperatively breeding acorn woodpeckers (Melanerpes formicivorus), helper males have a large positive effect on fledging success in good acorn crop years but only a small positive effect in poor acorn crop years, while helper females exhibit the opposite pattern. Based on these findings, we tested the “concealed helper effects” hypothesis, which proposes that laying females reduce investment in eggs (with respect to their size, number, or quality) in a way that confounds helper effects and results in an absence of a relationship between helpers and breeding success. Results generally failed to support the hypothesis. Mean egg size was positively related to temperatures during the 10 days prior to egg-laying and negatively related to the food supply as indexed by the prior fall’s acorn crop, but there were no significant differences vis-à-vis helpers except for interactions with the acorn crop that only partly corresponded to those predicted. With respect to clutch size, females laid larger clutches when assisted by female helpers, opposite the pattern predicted. Although our results suggest that egg size is adjusted to particular ecological circumstances, we conclude that neither egg nor clutch size is adjusted in a way that confounds the apparent effects of helpers, as proposed by the concealed helper effects hypothesis.     

Sex and status in a cooperative breeding fish: behavior and androgens

Among taxonomically widespread cooperatively breeding vertebrates, those with non-breeding helpers-at-the-nest provide an excellent opportunity to understand the proximate mechanisms underlying care and allocare. In this study, we examined androgen levels in relation to care behavior in a cooperatively breeding cichlid fish, Neolamprologus pulcher, from Lake Tanganyika. We concentrated on androgens, as these hormones have been linked to the defense behavior, and the defense of young is a common form of parental care in fishes. N. pulcher dominant female breeders performed the most care and also displayed the highest levels of plasma testosterone (T) compared with other individuals within the social group. We also found that dominant male breeders provided a similar amount of care as did the subordinate helpers, but breeding males had the highest levels of 11-ketotestosterone (11KT), an important androgen in fish. Breeders had higher levels of both androgens (T and 11KT) compared to helpers. There was a weak but significant positive correlation between T levels and the frequency of care regardless of sex and status. Our results suggest that androgens may promote defense of young and are in contrast to the commonly reported trade-off between androgen and parental care.     

Seasonal variation in the relationship between cellular immune response and badge size in male house sparrows (Passer domesticus)

The immunocompetence handicap hypothesis postulates that secondary sexual traits are honest signals of male quality because steroid hormones (such as corticosteroids and sex steroids), which are supposed to favor the development of secondary sexual traits, may also have immunosuppressive effects. Certain secondary sexual traits are not only used as mate choice signals but also play a role as badges of status. In the house sparrow (Passer domesticus), males have a bib of black feathers which is used both as a signal of social status in male-male interactions and by females when choosing a mate. We investigated the relationships between bib size and cellular immune response in male house sparrows during and outside the reproductive season. Males with large badges were found to have lower levels of immunocompetence, as assessed using a T-cell-mediated immunity assay, during the reproductive season, as predicted by the immunocompetence handicap hypothesis. Conversely, in November, the correlation between badge size and cellular immune response was positive, possibly reflecting the better access to trophic resources of large-badged dominant males in winter flocks. Received: 24 September 1998 / Received in revised form: 2 February 1999 / Accepted: 14 February 1999     

Relationships between Plant and Animal Species Richness at a Regional Scale in China

Abstract:  Important questions in conservation biology and ecology include whether species diversities of different groups of organisms are correlated and, in particular, whether plant diversity influences animal diversity. I used correlation and partial regression analyses to examine the relationships between species richness of vascular plants and four major groups of terrestrial vertebrates (mammals, amphibians, reptiles, and birds) in 28 provinces in China. Species richness data were obtained from the literature. Environmental variables included normalized difference vegetation index, mean January temperature, mean annual temperature, annual precipitation, May through August precipitation, actual evapotranspiration, potential evapotranspiration, and elevation range. Species richness was strongly and positively correlated among the five groups of organisms. Plant richness was correlated with animal richness more strongly than the richness of different animal groups correlated with each other except for reptile richness, which had a slightly higher correlation with amphibian richness than with plant richness. Plant richness uniquely explained 41 times more variance in the species richness of the four vertebrate groups combined than environmental variables uniquely did, suggesting that plant richness influences terrestrial vertebrate richness at the regional scale examined. Because of strong correlations between the diversity of vascular plants and vertebrates, the diversity of vascular plants may be used as a surrogate for the diversity of terrestrial animals in China. My results have implications for selection of areas to be protected at both regional and local scales.