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.     

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.     

Population dynamics of obligate cooperators

Obligate cooperative breeding species demonstrate a high rate of group extinction, which may be due to the existence of a critical number of helpers below which the group cannot subsist. Through a simple model, we study the population dynamics of obligate cooperative breeding species, taking into account the existence of a lower threshold below which the instantaneous growth rate becomes negative. The model successively incorporates (i) a distinction between species that need helpers for reproduction, survival or both, (ii) the existence of a migration rate accounting for dispersal, and (iii) stochastic mortality to simulate the effects of random catastrophic events. Our results suggest that the need for a minimum number of helpers increases the risk of extinction for obligate cooperative breeding species. The constraint imposed by this threshold is higher when helpers are needed for reproduction only or for both reproduction and survival. By driving them below this lower threshold, stochastic mortality of lower amplitude and/or lower frequency than for non-cooperative breeders may be sufficient to cause the extinction of obligate cooperative breeding groups. Migration may have a buffering effect only for groups where immigration is higher than emigration; otherwise (when immigrants from nearby groups are not available) it lowers the difference between actual group size and critical threshold, thereby constituting a higher constraint.     

Social organization,demography and genetic mating system of a Tibetan cooperative breeder

Knowledge of cooperative breeding in birds from longitudinal studies is available only for a small proportion of species. This paper reports data from a 12‐year study on the Tibetan Ground Tit Pseudopodoces humilis. On average, 27.2% (range: 13.0–36.1%) of monogamous pairs in each year contained one (85.4%) or more (14.6%) male helpers, 83.7% of which were yearlings staying on natal territories. Most helpers (89.6%) helped once and then bred independently. Adults had male‐biased sex ratios, low annual survival rates (averaging 0.50) and shorter longevities (averaging 1.8 years) compared with low‐altitude avian cooperative breeders, suggesting that mate shortage promotes helping behaviour in this species. Incest occurred rarely (2.1% of pairs), probably because kin recognition occurs through year‐around living in family groups. There was a low level (3.1% of broods) of extra‐pair parentage, which could facilitate the maintenance of cooperative breeding.     

Experimental evidence for kin-biased helping in a cooperatively breeding vertebrate

The widespread belief that kin selection is necessary for the evolution of cooperative breeding in vertebrates has recently been questioned. These doubts have primarily arisen because of the paucity of unequivocal evidence for kin preferences in cooperative behaviour. Using the cooperative breeding system of long-tailed tits (Aegithalos caudatus) in which kin and non-kin breed within each social unit and helpers are failed breeders, we investigated whether helpers preferentially direct their care towards kin following breeding failure. First, using observational data, we show that not all failed breeders actually become helpers, but that those that do help usually do so at the nest of a close relative. Second, we confirm the importance of kinship for helping in this species by conducting a choice experiment. We show that potential helpers do not become helpers in the absence of close kin and, when given a choice between helping equidistant broods belonging to kin and non-kin within the same social unit, virtually all helped at the nest of kin. This study provides strong evidence that kinship plays an essential role in the maintenance of cooperative breeding in this species.     

Food Sharing in Lion Tamarins (<Emphasis Type="Italic">Leontopithecus chrysomelas</Emphasis>): Does Foraging Difficulty Affect Investment in Young by Breeders and Helpers?

Food sharing with immatures is an important and relatively well studied aspect of infant care in many cooperative species. A key point that has not yet been fully addressed, however, is how increasing the difficulty of obtaining food influences the willingness of breeders and helpers to provision immature offspring. We used captive golden headed lion tamarins (Leontopithecus chrysomelas) to examine how breeders and helpers differ in provisioning juvenile individuals according to the level of difficulty of obtaining food. The level of difficulty in obtaining food was varied by placing the food inside tubes that allowed access only by adults. When food acquisition became more difficult, food sharing with juveniles and breeding females increased significantly. Begging calls by breeding females and juveniles increased during the experimental condition, which probably led to increases in food sharing. Breeders and helpers did not differ in their contribution to provisioning when food was easily available, nor did they differ in their contribution when food was difficult to obtain. Breeding males in callitrichids have a prominent role in transferring food to offspring, but contrary to our expectations, they did not increase food transfer in the experimental condition. An unexpected result was the increased investment of the breeding female into her current offspring when the level of difficulty of obtaining food was higher. We suggest that breeding lion tamarin females are not as constrained by reproductive costs as breeding females of other callitrichids. Degree of reproductive skew is hypothesized as a factor affecting the contribution of breeders and helpers to offspring care in cooperative breeding mammals, though we suggest that more studies are needed to validate such a generalization.     

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.     

Cooperative Breeding in the Lake Tanganyika Cichlid Julidochromis ornatus

Cooperative breeding has been described for several cichlids from the genus Julidochromis (Perciformes: Cichlidae) under laboratory conditions, but field evidence is scarce. Here we describe the breeding system of the cichlid Julidochromis ornatus (Boulenger) in Lake Tanganyika (Zambia). Groups defended a breeding shelter under a large flat stone. Smaller group members stayed and fed under or close to the stone, actively guarded by the larger group members. Six out of 28 groups were newly established by breeders, joined by subordinates from a large pool of independent fish (comprising 50–70% of the total population), and four groups were seen to dissolve during a total of 77 observation days. Breeding groups consisted of a large breeding male and female with zero to five smaller subordinates (average 2). Larger breeders and subordinates were found in larger groups. All group members participated in territory defence and -maintenance, but the breeders were only present at the shelter 48% of the time, in contrast to the subordinates which guarded the breeding shelter 94% of the time. Smaller group members showed submissive behaviours to larger group members. We conclude subordinates in J. ornatus are helpers, but we did not find evidence that helpers increased the group’s current reproductive success. Personal observations combined with a literature review revealed at least 19 species of Lake Tanganyika cichlids show evidence of cooperative breeding, entirely confined to the substrate breeding tribe of the Lamprologini (24% of 80 species in total): 2 Chalinochromis spp., 5 Julidochromis spp., 12 Neolamprologus spp. More effort should be put into detecting cooperative breeding in American and Asian substrate breeding cichlid species.     

First field evidence for alloparental egg care in cooperatively breeding fish

Helping behaviour in cooperative breeders has been intensively studied in many animal taxa, including arthropods, birds and mammals. In these highly social systems, helpers typically engage in brood care and the protection of dependent young. Such helping systems also exist in cooperatively breeding cichlid species of Lake Tanganyika. However, breeding in these species happens in clefts, narrow holes or shelters underneath stones. Therefore, direct brood care by breeders and helpers has thus far only been observed under artificial laboratory conditions. Under natural conditions, brood care behaviour has been estimated indirectly by determining the time spent in the breeding chamber, or by the number of visits to the breeding chamber. The reliability of such substitutes needs to be validated, for instance, by demonstrating alloparental egg care of helpers through direct observations in nature. Here, we describe direct egg care by a male helper of the cooperatively breeding cichlid Neolamprologus savoryi in the field. The helper inspected and cleaned the eggs and defended them against predators. By reconstructing the genetic relatedness using microsatellite markers, we show that the helper was the son of the breeding male, but unrelated to the breeding female. The genetic mother of the helper was defending a different territory next to the one where the helper showed alloparental egg care. This indicates that the helper had dispersed inside the male territory to assist another female to care for his half‐siblings. These results demonstrate alloparental egg care without reproductive share in a fish species under natural conditions, underlining that helping behaviour in cooperatively breeding fish has a strong non‐self‐serving component.     

Avian Helpers at the Nest: Are they Psychologically Castrated?

In cooperatively breeding pied kingfishers (Ceryle rudis) blood plasma levels of LH and testosterone (T) were compared among three types of males: breeders, primary (= related) helpers and secondary (= unrelated) helpers. These categories did not differ in LH, but primary helpers had significantly lower T titers than breeders and secondary helpers. The low levels were paralleled by small gonad sizes and no sperm production, suggesting that primary helpers were not able to fertilize eggs. The differences in T levels could neither be attributed to stochastic variation nor to differences in age, stress, molt, or reproductive activities. The most likely explanation arises from the observation that primary helpers are behaviorally dominated by breeders, whereas secondary helpers are not. The adaptive significance of low T titers and reduced fertility as a result from being dominated is discussed on the basis of empirical data and theoretical models. We argue that primary helpers in the pied kingfisher, and subordinate helpers in many other cooperative breeders, apparently are not “unwillingly” suppressed in their sexual development; they rather “choose” delayed reproduction when the costs from sexual competition with breeders exceed the benefits from cooperative breeding. In contrast, helpers that benefit more from competition than from cooperation, as secondary helpers do, cannot be expected to show reduced fertility.     

Kinship affects investment by helpers in a cooperatively breeding bird

Helping behaviour in cooperative breeding systems has been attributed to kin selection, but the relative roles of direct and indirect fitness benefits in the evolution of such systems remain a matter of debate. In theory, helpers could maximize the indirect fitness benefits of cooperation by investing more in broods with whom they are more closely related, but there is little evidence for such fine-scale adjustment in helper effort among cooperative vertebrates. In this study, we used the unusual cooperative breeding system of the long-tailed tit Aegithalos caudatus to test the hypothesis that the provisioning effort of helpers was positively correlated with their kinship to broods. We first use pedigrees and microsatellite genotypes to characterize the relatedness between helpers and breeders from a 14 year field study. We used both pedigree and genetic approaches because long-tailed tits have access to pedigree information acquired through social relationships, but any fitness consequences will be determined by genetic relatedness. We then show using both pedigrees and genetic relatedness estimates that alloparental investment by helpers increases as their relatedness to the recipients of their care increases. We conclude that kin selection has played a critical role in moulding the investment decisions of helpers in this cooperatively breeding species.     

Cooperative breeding, mate guarding, and nest sharing in two parrot species of New Caledonia

We provide evidence for cooperative breeding in two endemic parrot species of New Caledonia, the New Caledonian Parakeet (Cyanoramphus saisseti) and the Horned Parakeet (Eunymphicus cornutus). We intensively monitored 11 breeding attempts in two nests of New Caledonian Parakeets over 5 years, and noticed that two males of different size fed the female and the chicks in each nest. During one breeding attempt, the larger male guarded the female and the smaller male tried to copulate with her inside the nest. Genetic analyses showed that males shared paternity. During 17 breeding attempts in 11 Horned Parakeet nests, we observed two pairs sharing a nest on one occasion but we never saw feeding helpers.     

An Experimental Study of Chick Provisioning in the Cooperatively Breeding Acorn Woodpecker

Acorn woodpeckers (Melanerpes formicivorus) are cooperative breeders in which groups consist of a variable number of cobreeding males, joint‐nesting females, and non‐breeding helpers of both sexes that are offspring from prior nests. We temporarily manipulated brood size of nests to determine the feeding response of birds in relation to their status (breeder or non‐breeding helper) and sex. All categories of birds responded similarly to brood size increases, adjusting their feeding rate upwards so as to maintain approximately the same per‐nestling feeding rate. Breeders, however, exhibited more flexibility with respect to brood size reductions, decreasing their feeding rate while helpers did not. This suggests that the ‘feeding rules’ of helpers are less flexible than those of breeders, a result not previously detected in other cooperative breeders that have been studied to date. Particularly surprising was the finding that helpers maintain their feeding rates when brood demand is decreased rather than when it was increased, suggesting that the flexibility they exhibit is not a result of birds using the opportunity afforded by reduced brood demand to engage in other less cooperative activities.     

Egg investment in response to helper presence in cooperatively breeding Tibetan ground tits

Life‐history theory predicts a trade‐off between current and future reproduction to maximize lifetime fitness. In cooperatively breeding species, where offspring care is shared between breeders and helpers, helper presence may influence the female breeders’ egg investment, and consequently, survival and future reproductive success. For example, female breeders may reduce egg investment in response to helper presence if this reduction is compensated by helpers during provisioning. Alternatively, female breeders may increase egg investment in response to helper presence if helpers allow the breeders to raise more or higher quality offspring successfully. In the facultatively cooperative‐breeding Tibetan ground tit Pseudopodoces humilis, previous studies found that helpers improve total nestling provisioning rates and fledgling recruitment, but have no apparent effects on the number and body mass of fledglings produced, while breeders with helpers show reduced provisioning rates and higher survival. Here, we investigated whether some of these effects may be explained by female breeders reducing their investment in eggs in response to helper presence. In addition, we investigated whether egg investment is associated with the female breeder's future fitness. Our results showed that helper presence had no effect on the female breeders’ egg investment, and that egg investment was not associated with breeder survival and reproductive success. Our findings suggest that the responses of breeders to helping should be investigated throughout the breeding cycle, because the conclusions regarding the breeders’ adjustment of reproductive investment in response to being helped may depend on which stage of the breeding cycle is considered.     

Genetic analysis reveals diverse kin‐directed routes to helping in the rifleman Acanthisitta chloris

The social organization of cooperatively breeding species is extremely variable, with diverse social group composition and patterns of relatedness. Species that exhibit alternative routes to helping within the same population are potentially useful systems to investigate the causes and fitness consequences of diverse evolutionary pathways to cooperative behaviour. In this study, we use microsatellite markers and field observations to describe helping behaviour and patterns of relatedness in the unusual cooperative breeding system of the rifleman Acanthisitta chloris. First, we show that rifleman helpers consist of a remarkably diverse demographic, including males and females, who may be adult or juvenile, failed breeders or nonbreeders, or even successful breeders that simultaneously feed their own brood. Adult helpers mostly helped at first‐brood nests, while first‐brood juveniles assisted their parents at second broods. Second, we show that rifleman pairs are strictly sexually monogamous, and helpers did not gain any current reproductive success through helping. Third, genotyping showed that contrary to previous assumptions, helpers were closely related to the recipients of their care and preferentially directed care towards relatives over contemporaneous nests of nonrelatives. Finally, we show that variation in helper provisioning effort was attributed to age: juvenile helpers provisioned less than adults and were less responsive to the demands of a growing brood. Overall, our results show that the diverse routes to helping in this unusual species are driven by the common theme of kinship between helper and recipients, resulting in a previously underestimated potential for helpers to gain indirect fitness benefits.     

Helper effects in the azure‐winged magpie Cyanopica cyana in relation to highly‐clumped nesting pattern and high frequency of conspecific nest‐raiding

In avian cooperative breeding systems, many benefits obtained by social pairs from the presence of helpers have been uncovered. However, until now, the factors that determine the type of assistance helpers provide and the responses of social pairs have not been well illustrated. We examined the contribution of helpers to cooperative groups and the relevant responses of dominant pairs in the azure‐winged magpie Cyanapica cyana which breeds on the Tibetan Plateau. We used the capture–mark–recapture method to identify helpers. Results showed that helpers were mostly the yearling sons of dominant pairs. They mainly contributed to the cooperative group in three ways, courtship‐feeding the incubation female, provisioning the brood, and defending the nest. For responses of dominant pairs, we unexpectedly found that clutch size was not influenced by the presence of helpers at the nest. However, cooperative groups had higher brood feeding rates than biparental nests and their feeding pattern also differed to that of the latter. Consequently, nestlings in cooperative groups had larger fledging body mass than that in biparental nests. By examining reasons for nest failure, we revealed that conspecific nest‐raiding contributed to more nest failure than any other natural predators. Because of the contribution of helpers in defending against both predators and conspecific nest‐raiders, cooperative groups had higher survival rate than biparental nests. Thus, our findings suggest that in a highly‐clumped nesting pattern, factors concerning the risk of nest predation, rather than that influencing food supply, play an important role in determining helper effects and responses of aided dominant pairs.     

Characterization of microsatellites for parentage studies of white‐throated magpie‐jays (Calocitta formosa) and brown jays (Cyanocorax morio)

White‐throated magpie‐jays (Calocitta formosa) and brown jays (Cyanocorax morio) are cooperative breeders that live in complex groups composed of helpers and multiple male and female breeders. Behavioral observations and multilocus DNA fingerprinting have indicated that the social and genetic mating systems of these two species are diverse. Extra‐group paternity appears to be common in both species, necessitating the use of single locus genetic methods to efficiently search for fathers. We therefore characterized 19 microsatellite loci for these two species (12 for magpie‐jays and seven for brown jays) to aid in parentage studies.     

Do Parents and Helpers Discriminate between Related and Unrelated Nestlings in the Cooperative Breeding Silver‐Throated Tit?

When benefits exceed costs, natural selection may favor adults that develop the ability to recognize and preferentially direct care toward their own offspring to maximize their fitness. Investigations into the ability of adults to recognize offspring in offspring's early development period may help to understand when the ability of kin recognition starts to develop. In birds, studies of offspring recognition have mainly been conducted on bi‐parental breeding species, but relatively seldom on cooperative breeding species, despite that kin recognition may be of particular importance for cooperative breeders. The silver‐throated tit Aegithalos glaucogularis is a small passerine in which some nests have helpers during breeding. We tested whether silver‐throated tit parents and helpers were able to distinguish between their own and alien nestlings 2–5 d before fledging when recognition mechanisms were likely to have been developed. Through two forced choice experiments, of which one was conducted right beside the experimental nests (<0.8 m) and the other far away from the experimental nests (~6 m), we found that neither parents nor helpers discriminatively fed their own and alien nestlings, which suggested that at least during the experimental nestling age, and within the 6‐m‐radius area around the nests, they might not have the ability to recognize offspring. The possibility that silver‐throated tits use a larger area (>6 m radius) around their nests as a location‐based cue for offspring recognition, or would develop an offspring recognition ability at an older nestling age and/or even after fledging, warrants future studies.     

Flexible Helping Behaviour in the Azure-Winged Magpie

Helping to rear the offspring of others may be a way for younger birds to gain access to future reproduction especially when turnover of breeding opportunities is low. However, this explanation is not applicable to cases where adults also help, or when roles shift between helpers and breeders. Over a period of 6-yr, we studied a marked population of azure-winged Magpie (Cyanopica cyanus) breeding in a non-territorial, colonial system. Magpies bred in a highly flexible cooperative system, in which individuals helped at different stages of the breeding cycle, including nest building, feeding the incubating female and feeding the young and removing the faecal sacs. On average, 50% of hatched nests were assisted by helpers-at-the-nest, and nest success appeared to be positively related to the presence of helpers. Helpers were predominantly males. Although juveniles were more likely to help, both juvenile and adult birds helped. Individual birds behaved as helpers either as a first-option or after having attempted their own breeding (second-option helpers). An individual helper may assist more than one nest during the same breeding season and in different breeding seasons. Reversals between breeder and helper roles were common in both directions, within a breeding season and between years. Helping behaviour is an option for almost any member of the colony. Therefore, hypotheses related to the enhancement of future breeding opportunities for juveniles can be discarded as general explanation of helping in this species. Although the decision to help appeared to be influenced by proximal environmental conditions hindering successful breeding, the associated benefits of helping as opposed to simply recovering for future reproduction, especially for former breeders, deserve further study.     

Variable helper effects, ecological conditions, and the evolution of cooperative breeding in the acorn woodpecker

The ecological conditions leading to delayed dispersal and helping behavior are generally thought to follow one of two contrasting scenarios: that conditions are stable and predictable, resulting in young being ecologically forced to remain as helpers (extrinsic constraints and the habitat saturation hypothesis), or that conditions are highly variable and unpredictable, leading to the need for helpers to raise young, at least when conditions are poor (intrinsic constraints and the hard life hypothesis). We investigated how variability in ecological conditions influences the degree to which helpers augment breeder fitness in the cooperatively breeding acorn woodpecker (Melanerpes formicivorus), a species in which the acorn crop, territory quality, and prior breeding experience all vary in ways that have important effects on fitness. We found that the relationship between ecological conditions and the probability that birds would remain as helpers was variable but that helpers generally yielded greater fitness benefits when ecological conditions were favorable, rather than unfavorable, for breeding. These results affirm the importance of extrinsic constraints to delayed dispersal and cooperative breeding in this species, despite its dependence on a highly variable and unpredictable acorn crop. Our findings also confirm that helpers can have very different fitness effects, depending on conditions, but that those effects are not necessarily greater when breeding conditions are unfavorable.