Kin and social relationships in splendid fairy-wrens: recognition by song in a cooperative bird

Cooperatively breeding splendid fairy-wren,s Malurus splendens, were tested with songs recorded from individuals of known social and kin relationships. Both males and females sang and responded aggressively to songs of wrens from other social groups. Wrens responded similarly to songs of non-kin and songs of close kin in the absence of social familiarity with them. Breeding females responded more intensely to songs of helpers from other groups than to songs of helpers in their own group. The songs of male and female helpers elicited similar responses by breeding females. The response to other females may be associated with competition for breeding status and helpers. Two females sometimes breed in social groups with two older females; no interference was observed. Song may allow individuals to recognize other wrens in their group and to direct their behaviour towards non-dispersing relatives by location and social familiarity rather than by kinship identifiers.     

Cooperative Breeding and Group Structure in the Lake Tanganyika Cichlid Neolamprologus savoryi

As yet, cooperative breeding has been described only for some fish species. However, evidence is accumulating that it is widespread among Lake Tanganyika cichlids. We studied the cooperative breeding system of the substrate breeding cichlid Neolamprologus savoryi. Breeding groups typically consisted of a large breeding male with one to four breeding females and three to 33 helpers (mean group size: 14.3 members). Group size was significantly related to breeding male and female body sizes, and larger males had more breeding females and larger sized male helpers. The size of the largest female in the group was positively related to the number and sizes of secondary breeding females and female helpers. In case of multiple breeding females, these females usually divided the group's territory into sub‐territories, each with its own helpers (subgroups). Interspersed between groups, independent fish were detected defending an individual shelter (4.4% of all fish). In 9% of the groups no breeding female was present. All group members participated in territory defence and maintenance, and showed submissive behaviours to larger group members. As expected, the level of between‐subgroup conflicts was high compared with the level of within‐subgroup conflicts. We compare these results with data available from other cooperatively breeding fishes.     

Maternal investment during pregnancy in wild meerkats

Maternal investment in offspring development is a major determinant of the survival and future reproductive success of both the mother and her young. Mothers might therefore be expected to adjust their investment according to ecological conditions in order to maximise their lifetime fitness. In cooperatively breeding species, where helpers assist breeders with offspring care, the size of the group may also influence maternal investment strategies because the costs of reproduction are shared between breeders and helpers. Here, we use longitudinal records of body mass and life history traits from a wild population of meerkats (Suricata suricatta) to explore the pattern of growth in pregnant females and investigate how the rate of growth varies with characteristics of the litter, environmental conditions, maternal traits and group size. Gestational growth was slight during the first half of pregnancy but was marked and linear from the midpoint of gestation until birth. The rate of gestational growth in the second half of pregnancy increased with litter size, maternal age and body mass, and was higher for litters conceived during the peak of the breeding season when it is hot and wet. Gestational growth rate was lower in larger groups, especially when litter size was small. These results suggest that there are ecological and physiological constraints on gestational growth in meerkats, and that females may also be able to strategically adjust their prenatal investment in offspring according to the likely fitness costs and benefits of a particular breeding attempt. Mothers in larger groups may benefit from reducing their investment because having more helpers might allow them to lower reproductive costs without decreasing breeding success.     

No Evidence for Enforced Alloparental Care in a Cooperatively Breeding Parrot

In cooperatively breeding species, in which non‐breeding helpers assist in rearing the offspring of breeding individuals, conflicts of interest commonly occur between breeders and helpers over their respective contributions to offspring care. During such conflicts, breeders might use aggressive behavior to enforce contributions of helpers to offspring care, especially if helpers are not related to the breeders and their offspring and thus do not stand to gain indirect fitness benefits by helping. Using a combination of behavioral and genetic data, we investigated in the cooperatively breeding El Oro parakeet Pyrrhura orcesi (i) whether breeders are commonly dominant over helpers, (ii) whether they use aggressive behavior toward helpers to enforce offspring provisioning, and (iii) whether the relatedness of helpers to the nestlings affects the frequency of—or the reaction of helpers to—such aggressions. Even though breeders were generally dominant over helpers, we found no evidence for the enforcement of alloparental care. This finding was independent of the relatedness between helpers and nestlings, even though distantly related helpers overall contributed little to offspring care. We suggest that the inability of breeders to properly assess the work rates of their helpers at least partly explains the absence of enforcement. More generally, our results add to a body of evidence suggesting that enforcement might be an exceptional rather than a general mechanism underlying the expression of alloparental care in cooperatively breeding species.     

The Cooperative Breeding System of the Red-cockaded Woodpecker

The breeding system of the red-cockaded woodpecker is described based on data collected over six years from a population of 500 marked individuals in the Sandhills of North Carolina. Male-female pairs were the most common social unit (59%), but 30% of social units contained one or more adult helpers, and 11% consisted of solitary males. Helpers were almost exclusively male: 27% of males remained in their natal group as helpers for at least one year, whereas only four (1%) females did. Most breeding females remained as breeders in the same group from one year to the next (56%), but a surprising number (12%) moved to another group. Many movements were related to incest avoidance or mate death, but 39% involved deserting a mate, usually following successful reproduction. We suggest that females sometimes are forced from groups by immigrants or other group members. The median distance of movements by adult females was only 1.3 km. In contrast to females, no breeding males switched groups. Survival of both breeding (76%) and helper (80%) males was higher than that of breeding females (69%). Males exhibited two distinct life-history strategies. Some remained as helpers on their natal territory for one or more years, and became breeders by inheriting breeding status in the natal group (17% per year) or by replacing a deceased breeder in a nearby group (13% per year, median distance moved 1.0 km). Other males dispersed from their natal group permanently during their first year. Some of these males were floaters at age one year, others were solitary, and a few became helpers in a non-natal group, but many were breeders. In contrast to males that first functioned as helpers, those that dispersed after fledging moved long distances (median dispersal distance 4.5 km), longer even than dispersing female fledglings moved (median distance 3.2 km). The habitat saturation model of the evolution of cooperative breeding is based on selection between the two life-history strategies exhibited by male red-cockaded woodpeckers. The model therefore may be tested directly with this species. Another indication that this model is appropriate for this species is the existence of a resource (cavity trees) that might provide an ecological basis for habitat saturation.     

Group structure,within-group conflict and reproductive tactics in cooperatively breeding Galápagos mockingbirds,Nesomimus parvulus

Reproductive conflict within groups can be an important feature of cooperative breeding systems, especially when more than one individual of a sex breeds within a social group. Relationships between group structure, dominance, within-group conflict and reproductive tactics of cooperatively breeding Galápagos mockingbirds were examined on Isla Genovesa. Territorial groups of 2–24 adults included up to three breeding females, with 42% of the groups containing more than one (plural groups); females in most plural groups nested separately. Territory size increased with group size, but the area available per pair in plural groups was smaller than in singular groups (groups with only one breeding pair). Most pairings were monogamous, and males usually outnumbered females; high-ranking males obtained mates more frequently than subordinate males. In 3 relatively dry years, but not in a wet El Niño year, subordinate pairs in plural groups fledged fewer young than dominant pairs or pairs breeding in singular groups. Interference by dominant breeders, often leading to abandonment of nests by subordinate pairs, appears to account for these differences: through nest disruption in drier years, dominant individuals may reduce the cost of sharing their territories and increase the chances of recruiting helpers. Dominant males in plural groups may also father young through extra-pair copulations with subordinate females. Despite costs imposed by within-group conflict, subordinate breeders have higher long-term reproductive success than birds that defer breeding. Plural group structure is maintained because unpredictable climatic variation favours opportunistic breeding by subordinates.     

Plural Breeding in the Splendid Fairy-wren,Malurus splendens (Aves: Maluridae), a Cooperative Breeder

Groups of the cooperatively breeding splendid fairy-wren Malurus splendens may include more than one female. Previously this species has been described as singular breeding (only one female breeds). This paper describes the occurrence of plural breeding (PB) groups in 10% of group years, in which two females had separate nests. In all cases, the secondary female (Y) was related to the primary breeding female (X) and was generally a 2-year old female which had helped in the group during the previous breeding season. Plural breeding was correlated with an increase in population density and in the number of female helpers; PB groups were larger than singular-breeding groups. In most cases, the X female was occupied with her own nest or offspring when the Y female began to nest, and there was no aggression between them. Which birds helped the Y female to feed at her nest depended on the time between the hatching of the two nests. If the interval was small, some group members helped at each nest; with longer intervals, the group members began to feed at the earlier nest, and the other female was left to raise her brood alone. Female helpers were very active in feeding at single nestings, and the cost to an X female of a Y female breeding was mainly a loss of this assistance. The success of individual X nests was not affected. Effects on productivity were slight, but fewer X females in PB groups raised second broods than did experienced singular breeding females. Y females were less productive than X females, but no less productive than singular breeding novice females without helpers. It is not known whether Y females copulated with primary or secondary males within their group, or with males from outside the group. Certainly, they did not form an observable pairing with any male in the group. Plural breeding occurred in a minority of group years in response to extrinsic conditions and the current demographic situation, and shows the extreme plasticity of the mating system in M. splendens.     

Facultative dispersal by juvenile males in the cooperative stripe-backed wren

We present genetic and demographic data documenting juveniledispersal in the cooperatively breeding stripe-backed wren (Campylorhynchusnuchalis) of Venezuela. Parentage and DNA fragment-sharing analysesrevealed 12 cases in which juveniles were unrelated to othergroup members. Of these 12 foreign juveniles, (1) all were males,(2) eight of 12 had been found with breeding pairs lacking helpersrather than with groups containing helpers, and (3) four outof seven of those observed as adults courted or sired offspringwith the dominant females in their new groups despite the strongincest avoidance of this species. Furthermore, juvenile maleshad a significant tendency to disappear from natal groups intheir first year, and singleton juveniles observed with pairsafter the breeding season were mostly males. These data supportthe hypothesis that foreign juveniles were dispersers from intactgroups and not products of conspecific brood parasitism or adoptionfollowing group dissolution. We suggest that unassisted pairsmight accept juvenile males into their groups as helpers toincrease their future reproductive success and that dispersersthemselves might leave large natal groups in which their helpingis superfluous to join small groups of nonrelatives in whichthey might soon reproduce.     

Behaviour and breeding biology of the cooperatively breeding Grey-backed Fiscal Shrike Lanius excubitorius in Kenya

Grey-backed Fiscal Shrikes Lanius excubitorius were studied over a 2j year period near Lake Naivasha, Kenya. Grey-backs are cooperative breeders, with group sizes ranging from two to II. Only one pair breeds per group, with all other group members aiding in the rearing of young. The study population ranged from 64 to 79 individuals that occurred in from 13 to 16 groups. Non-breeding helpers made up to 66% of the population, with male helpers being more numerous overall than females. The annual survival rate was 65%, with no differences detected between the survival of males and females, or of breeders and helpers. Only male helpers were observed to acquire breeding status within the natal territory. Some female helpers acquired breeding positions in territories adjacent to their natal territories. Group territorial displays occurred throughout the year but were most pronounced prior to breeding during rainy periods. Reproductive success was very low, with only 14.5% of the recorded breeding attempts leading to fledged young. Large groups (four or more birds) had greater reproductive success than small groups, but many factors other than, or in addition to, group size may have influenced this pattern. The breeding male contributed the most food to the incubating female and to the nestlings. Male helpers and the breeding female contributed more to nestlings than did female helpers. Observations on the post-fledging period indicate that socialization and establishment of dominance may be of importance in group-living species living in a restricted ecological and social setting.     

Social organization and communal breeding in the chestnut-bellied starling (Spreo pulcher)

Chestnut-bellied starlings (Spreo pulcher) live in social groups of 10–30 individuals and during their breeding seasons maintain group ranges which show little overlap with neighbouring groups. A social group may contain two to six breeding pairs, non-breeding adults of both sexes, and immatures. Each breeding female has her own nest and she alone incubates. The parents and up to 12 other starlings feed the nestlings. Individual helpers may successively or simultaneously attend the nests of different breeders. The percentage of nests attended within a group differs for helpers of different sex, age and breeding status: immatures of 1–2 years and non-breeding adult males help most and adult females least. Nests with more helpers have higher fledging success than those with fewer helpers. These results are discussed with reference to the tentative benefits of helping behaviour and kinship relationships within the social group.     

Reproductive biology of captive male cottontop tamarin monkeys as a function of social environment

The cottontop tamarin, Saguinus oedipus oedipus, is a cooperatively breeding monkey in which mature male and female offspring serve as helpers to assist in rearing younger siblings. Generally, only one female per social group reproduces; breeding restriction is mediated in postpubertal female offspring through low and acyclic levels of reproductive hormones. We investigated (1) reproductive activity of postpubertal male offspring, and (2) whether aggression towards male offspring and a cortisol-mediated stress response might restrict breeding of male offspring in the natal group. We examined sexual behaviour, olfactory communication and urinary hormone levels (testosterone, dihydrotestosterone, luteinizing hormone, cortisol) of the subject males while we manipulated their social environment from housing in natal groups to pairing with a novel female, and after the production of their own offspring. Mounting and erection rates of the male subjects were as high in the natal group as when paired with a novel female. However, most mounts in the natal group were directed towards other males, and complete copulation sequences did not occur with natal-group females. Social environment had no significant effect on olfactory investigation of breeding females. Although hormone levels increased significantly after the subjects were removed from the natal group, the elevation was transient; the hormone levels of subjects in their natal groups did not differ from the levels shown by the same males when successfully producing their own offspring. Male offspring received more contact aggression in the natal group than when paired with the novel female. However, most of the aggression was received from siblings rather than the breeding pair, and levels of cortisol did not correspond with levels of aggression. Thus, at both a behavioural and endocrine level, mature male offspring in captive natal groups were potentially fertile, but sexual activity with natal-group females appeared to be behaviourally restricted and directed instead towards group males. In wild cottontop tamarin groups, this reproductive potential may allow male helpers flexibility to respond to breeding opportunities. Copyright 2001 The Association for the Study of Animal Behaviour.     

Behavioural tactics of breeders in cooperative meerkats

In eusocial invertebrates, queens commonly show morphological and behavioural modifications to their role as the principal breeders in their colonies. With the exception of naked mole-rats, Heterocephalus glaber, morphological modification of breeders has yet to be shown in cooperative vertebrates, but the behaviour of dominant individuals may be modified so as to maximize reproductive success. We studied the cooperative behaviour of dominant and subordinate adults in meerkats, Suricata suricatta, and found that the decision rules governing the contributions of dominant breeders differed from those of subordinate helpers. Dominant breeders contributed less than adult helpers to babysitting and pup feeding, but raised their individual contributions to pup care to a greater extent when helper:pup ratios were low. In contrast to subordinates, dominant breeders did not increase their contributions when they foraged successfully. Finally, while subordinates of both sexes assisted in rearing the young when dominants bred, dominant females contributed little when subordinates attempted to breed, and male helpers (but not females) reduced their contributions to the care of pups. Our results suggest that the division of labour between breeders and helpers in meerkats is intermediate between that of facultatively cooperative species, where parents are principally responsible for rearing young, and that of specialized eusocial species, which show a well-defined division of labour between breeders and workers.     

Load Lightening in Southern Lapwings: Group‐Living Mothers Lay Smaller Eggs than Pair‐Living Mothers

Females of some cooperative‐breeding species can decrease their egg investment without costs for their offspring because helpers‐at‐the‐nest compensate for this reduction either by feeding more or by better protecting offspring from predation. We used the southern lapwing (Vanellus chilensis) to evaluate the effects of the presence of helpers on maternal investment. Southern lapwings are cooperative (some breeding pairs are aided by helpers), chick development is precocial, thus adults do not feed the chicks, and adults offer protection from predators through mobbing behaviors. We tested whether southern lapwing females reduced their reproductive investment (i.e. load‐lightening [LL] hypothesis) or increased their investment (i.e. differential allocation hypothesis) when breeding in groups when compared with females that bred in pairs. We found that increased group size was associated with lower egg volume. A significant negative association between the combined egg nutritional investment (yolk, protein, and lipid mass) and group size was observed. Chicks that hatched from eggs laid in nests of groups were also smaller than chicks hatched in nests of pairs. However, there was no relationship between the body mass index of chicks, or clutch size and group size, which suggests that such eggs are, simply, proportionally smaller. Our results support the LL hypothesis even in a situation where adults do not feed the chicks, allowing females to reduce investment in eggs without incurring a cost to their offspring.     

Group-size-dependent punishment of idle subordinates in a cooperative breeder where helpers pay to stay

In cooperative breeding systems, dominant breeders sometimes tolerate unrelated individuals even if they inflict costs on the dominants. According to the ‘pay-to-stay’ hypothesis, (i) subordinates can outweigh these costs by providing help and (ii) dominants should be able to enforce help by punishing subordinates that provide insufficient help. This requires that dominants can monitor helping and can recognize group members individually. In a field experiment, we tested whether cooperatively breeding cichlid Neolamprologus pulcher subordinates increase their help after a forced ‘idle’ period, how other group members respond to a previously idle helper, and how helper behaviour and group responses depend on group size. Previously, idle helpers increased their submissiveness and received more aggression than control helpers, suggesting that punishment occurred to enforce help. Subordinates in small groups increased their help more than those in large groups, despite receiving less aggression. When subordinates were temporarily removed, dominants in small groups were more likely to evict returning subordinates. Our results suggest that only in small groups do helpers face a latent threat of punishment by breeders as predicted by the pay-to-stay hypothesis. In large groups, cognitive constraints may prevent breeders from tracking the behaviour of a large number of helpers.     

Extra‐group mating increases inbreeding risk in a cooperatively breeding bird

In many cooperatively breeding species, females mate extra‐group, the adaptive value of which remains poorly understood. One hypothesis posits that females employ extra‐group mating to access mates whose genotypes are more dissimilar to their own than their social mates, so as to increase offspring heterozygosity. We test this hypothesis using life history and genetic data from 36 cooperatively breeding white‐browed sparrow weaver (Plocepasser mahali) groups. Contrary to prediction, a dominant female's relatedness to her social mate did not drive extra‐group mating decisions and, moreover, extra‐group mating females were significantly more related to their extra‐group sires than their social mates. Instead, dominant females were substantially more likely to mate extra‐group when paired to a dominant male of low heterozygosity, and their extra‐group mates (typically dominants themselves) were significantly more heterozygous than the males they cuckolded. The combined effects of mating with extra‐group males of closer relatedness, but higher heterozygosity resulted in extra‐group‐sired offspring that were no more heterozygous than their within‐group‐sired half‐siblings. Our findings are consistent with a role for male–male competition in driving extra‐group mating and suggest that the local kin structure typical of cooperative breeders could counter potential benefits to females of mating extra‐group by exposing them to a risk of inbreeding.     

Life histories and the evolution of cooperative breeding in mammals

While the evolution of cooperative breeding systems (where non-breeding helpers participate in rearing young produced by dominant females) has been restricted to lineages with socially monogamous mating systems where coefficients of relatedness between group members are usually high, not all monogamous lineages have produced species with cooperative breeding systems, suggesting that other factors constrain the evolution of cooperative breeding. Previous studies have suggested that life-history parameters, including longevity, may constrain the evolution of cooperative breeding. Here, we show that transitions to cooperative breeding across the mammalian phylogeny have been restricted to lineages where females produce multiple offspring per birth. We find no support for effects of longevity or of other life-history parameters. We suggest that the evolution of cooperative breeding has been restricted to monogamous lineages where helpers have the potential to increase the reproductive output of breeders.     

Testis size depends on social status and the presence of male helpers in the cooperatively breeding cichlid Julidochromis ornatus

Cooperatively breeding animals, in which helpers may participatein reproduction with dominant breeders, are ideal species forexamining intraspecific variation in testis size because theyoften exhibit both monogamous breeding (low risk of sperm competition)and polyandrous breeding (high risk) within a population. However,little is known about testis investment as a result of spermcompetition in these animals. The substrate-brooding cichlidfish Julidochromis ornatus has a cooperatively breeding system,in which some males mate monogamously and other males reproduceas dominant breeders or helpers within cooperatively breedinggroups, in which male helpers frequently sire young. We examinedthe relationship between testis investment and male social statusin relation to the risk of sperm competition. As predicted fromsperm competition models, in groups with male helpers, boththe male breeders and the male helpers invested more in testesmass, compared to breeding males without male helpers. We alsofound a positive relationship between the testes mass of malebreeders and their male helpers, suggesting that males increasetheir investment in reproductive capability under the risk ofsperm competition. Sperm competition models also predict thatlarger testes are associated with increased siring success.Our paternity analysis supported this prediction; we found apositive relationship between testis investment by male helpersand the number of offspring they sired.     

Reproductive success depends on the quality of helpers in the endangered,cooperative El Oro parakeet (Pyrrhura orcesi)

In cooperative species, helping behaviour and reproductive success can be correlated, but understanding this correlation is often impaired by the difficulty to correctly infer causation. While helpers can incur costs by participating in brood care, it is yet unclear if their help depends on their individual quality. We address these questions in the previously unknown cooperative breeding system of the endangered El Oro parakeet (Pyrrhura orcesi). Specifically, we ask (i) whether breeders benefit directly from helpers by an enhanced reproductive success and if so, (ii) whether the amount of this potential benefit is regulated by the quality of contributing group members. Groups consist of a dominant breeding pair accompanied by helpers, but cooperation is not obligate. Microsatellite heterozygosity was used to assess individual quality; its suitability as indicator of quality was reflected in the positive relationship between offspring heterozygosity and recruitment into the population. The reproductive success of breeding pairs depended on helper (genetic) quality and the number of helpers. This relationship occurred on two different levels: clutch size and fledging success, indicating (i) that females profit from high‐quality helpers and probably adjust clutch size accordingly and (ii) that the helpers increase fledging success. Congruently, we found that offspring body condition is positively affected by helper quality, which is most probably explained by the increased feeding rates when helpers are present. We suggest a causal link between cooperation and reproductive success in this frugivorous, endangered parakeet. Further, helper (genetic) quality can be a relevant factor for determining reproductive fitness in cooperative species, particularly in small and bottlenecked populations.     

Reproductive skew, costs, and benefits of cooperative breeding in female wood mice (Apodemus sylvaticus)

Two current models seek to explain reproduction of subordinatesin social groups: incentives given by dominants for peacefullyremaining in the group (reproductive skew model) or incompletecontrol by dominants. These models make different predictionsconcerning genetic relatedness between individuals for thedistribution of reproduction and the stability of cooperativebreeding associations. To test these models and to furtherexplore the relationships between reproductive skew, geneticrelatedness, and investment of each participant, we performedbehavioral observations of female wood mice (Apodemus sylvaticus)raising pups communally. Our results do not support previousmodels. Differences in lifetime reproductive success were significantlygreater within mother—daughter pairs than within pairsof sisters or unrelated females. Subordinate females of eitherbreeding unit did not differ in their direct reproduction.Calculations of inclusive fitness based on our results leadto the following predictions: (1) Communal nests should occuronly when ecological circumstances prevent solitary breeding.(2) Subordinate females gain the highest inclusive fitnessjoining their mothers; they also show the highest nursing investment.(3) Mothers should accept daughters, who have no opportunityfor solitary breeding. (4) Dominant sisters and unrelated femalesshould reject subordinate females because cooperative breedingreduces their reproductive success. However, breeding unitsof dominant sisters and unrelated females nevertheless occurand can be explained by our finding that such females significantlyreduce nursing time, which may help them save energy for futurebreeding cycles. Our data demonstrate that both genetic relatednessand investment skew are important in the complex evolutionof reproductive skew in cooperative breeding.     

Grandparent helpers: the adaptive significance of older, postdominant helpers in the Seychelles warbler

The possibility that older, often nonreproductive, individuals may engage in kin-directed cooperative behavior has been largely overlooked in the study of cooperative breeding. Here, we describe and investigate the adaptive significance of such "grandparent" helpers in the Seychelles warbler, the first bird species in which this phenomenon has been observed. On Cousin Island, over a period of 24 years, a significant proportion (13.7%) of females, but few males (3.0%), was deposed from dominant positions. Deposed females were replaced by related females. However there was no evidence that older, senescent females were stepping aside to gain greater fitness benefits by increasing the reproductive success of their offspring, rather than breeding themselves; deposed females were not postreproductive, nor was being deposed linked to age or reproductive senescence. Of the deposed females, 68% became subordinates and helped to raise group offspring, accounting for ca. 10% of subordinates in any year. Demoted females were related (r= 0.24) to the group offspring and, consequently, could gain indirect benefits through helping. As direct benefits appeared to be limited, we suggest that indirect benefits have driven the evolution of such "grandparent helpers." This study now provides evidence for a new route to cooperative breeding in birds.