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Referential signaling, a complex form of communication in which specific signals are associated with external referents, was once thought to be limited to primates. Recent research has documented referential signaling in several other cooperative taxa, predominantly in kin-based societies. Here, we show that greater anis, communally nesting birds that breed in nonkin groups, give one type of alarm call in response to aerial threats (flying raptors) and another to more general threats (nonaerial predators). Observational data show that anis give these calls in response to different classes of threats, and playback experiments in the field confirmed that the alarm calls alone are sufficient to elicit appropriate behavioral responses even in the absence of an actual threat. Genetic data on a subset of groups confirmed that breeding groups are composed of nonkin, suggesting that referential alarm calls are often given in situations when no genetic relatives are present. These results suggest that complex referential communication can occur in social groups composed of nonrelatives, despite the absence of kin-selected fitness benefits.

Resource limitations, either due to environmental conditions or constraints on parental provisioning effort, can drive intense competition among offspring. In communal groups, resource availability may increase if parents receive assistance from other group members; however, if those caregivers also produce young, offspring demand may increase at the same time. It is possible, therefore, that the costs of intrabrood competition in large broods may outweigh the benefits of provisioning from additional caregivers. We tested the relationships between group size, brood size, and provisioning rates in the greater ani (Crotophaga major), a communally nesting cuckoo in which multiple breeding pairs and nonreproductive helpers cooperatively raise a shared brood. Crucially, brood and group size can vary independently in this species, allowing us to test changes in each variable separately. Using video footage of 2255 prey deliveries across 10 nests, we found that an increase in the number of adult caregivers within a group did not sufficiently offset a corresponding increase in the number of dependent young within a brood: prey availability per average nestling decreased with brood size, regardless of group size. In larger broods, last-hatched nestlings received significantly less prey than their broodmates, in part due to greater hatching asynchrony that exacerbated competitive asymmetries and facilitated inequality in food allocation. Our results indicate that last-hatched ani nestlings suffer a “double cost” in large broods: they must compete with more nestmates, and suffer disproportionately from asynchronous hatching. These costs may contribute to increased parent–offspring conflict and may constrain group size in communal breeders.

Conflicts between groups of animals have individual‐level fitness consequences that can influence the evolution of social behaviour. In the cooperatively breeding greater ani (Crotophaga major), groups occasionally destroy the eggs of their neighbours, causing the attacked group to abandon their nest. Prior research suggested that such conflicts occur when two groups build nests in close proximity, and that established groups tend to evict newcomers. However, inter‐group conflict had never been directly observed. Here, we report the first photographic evidence of egg destruction by greater anis. Twelve artificial nests containing clay eggs were placed in the field with the intent of attracting nest predators. Camera footage revealed that although only two nests were discovered by heterospecific predators (white‐faced capuchins, Cebus capucinus), five nests were visited by resident anis, who in three cases damaged the clay eggs by grasping them with their bills and ejecting them from the nest cup. Nests were discovered between 2 and 96 hr after being placed in the field (mean = 34 hr) and were visited up to 18 times by up to 4 individuals simultaneously. The distance between artificial nests and the nearest known ani territory ranged from 0.13 to 0.28 km (mean = 0.2 km). Resident groups did not subsequently breed at the nest sites that they attacked, consistent with the hypothesis that the main benefit of inter‐group conflict is to reduce competition for local resources rather than to usurp nest sites. This accidental experiment reveals that greater anis closely monitor nesting activity near their territories, which may contribute to the strong “home field advantage” that resident groups hold over intruders.

Avian brood parasites lay their eggs in the nests of other species, leaving the hosts to care for the parasitic offspring. The bookkeeping hypothesis predicts that, in order to reduce competition between parasitic nestlings, female parasites should keep a mental inventory of host nests that they have already parasitized and avoid laying multiple eggs in the same host nest. However, selection against repeat parasitism should be weaker when host nests are limited, or when hosts are able to rear more than one parasitic nestling. Here we use microsatellite genotyping of parasitic eggs to test whether female screaming cowbirds, Molothrus rufoaxillaris, avoid repeatedly parasitizing nests of their primary host, the greyish baywing, Agelaioides badius, in Argentina. Parasitism rates were extremely high (96.5% of 57 host clutches were parasitized with an average of 5.7 cowbird eggs each), indicating that host nests are limited. Although eggs laid by the same female showed moderate spatiotemporal clustering, individual females rarely laid more than one egg in the same host clutch (2 of 57 clutches, 26 of which contained multiple genotyped cowbird eggs). Females were much more likely to lay subsequent eggs in different host nests than to return to the same host nest. We found no evidence for kin structure among female cowbirds parasitizing the same host nest, which were no more closely related than chance would predict. These results suggest that female screaming cowbirds frequently lay eggs in host nests that have already been parasitized by unrelated females. However, they typically lay just one egg per host clutch, even though greyish baywings are capable of rearing several nestlings. Since screaming cowbird laying is often poorly synchronized with that of their host, avoidance of repeat parasitism may be adaptive if it allows females to spread the risk of failure among multiple host nests.

Cooperative breeding strategies lead to short-term direct fitness losses when individuals forfeit or share reproduction. The direct fitness benefits of cooperative strategies are often delayed and difficult to quantify, requiring data on lifetime reproduction. Here, we use a longitudinal dataset to examine the lifetime reproductive success of cooperative polygamy in acorn woodpeckers ( Melanerpes formicivorus ), which nest as lone pairs or share reproduction with same-sex cobreeders. We found that males and females produced fewer young per successful nesting attempt when sharing reproduction. However, males nesting in duos and trios had longer reproductive lifespans, more lifetime nesting attempts and higher lifetime reproductive success than those breeding alone. For females, cobreeding in duos increased reproductive lifespan so the lifetime reproductive success of females nesting in duos was comparable to those nesting alone and higher than those nesting in trios. These results suggest that for male duos and trios, reproductive success alone may provide sufficient fitness benefits to explain the presence of cooperative polygamy, and the benefits of cobreeding as a duo in females are higher than previously assumed. Lifetime individual fitness data are crucial to reveal the full costs and benefits of cooperative polygamy.

Cooperatively nesting birds are vulnerable to social parasites that lay their eggs in host nests but provide no parental care1–4. Most previous research has focused on the co-evolutionary arms race between host defences and the parasites that attempt to circumvent them5–9, but it remains unclear why females sometimes cooperate and sometimes parasitize, and how parasitic tactics arise in cooperative systems10–12. Here we show that cooperative and parasitic reproductive strategies result in approximately equal fitness pay-offs in the greater ani (Crotophaga major), a long-lived tropical cuckoo, using an 11-year dataset and comprehensive genetic data that enable comparisons of the life-histories of individual females. We found that most females in the population nested cooperatively at the beginning of the breeding season; however, of those birds that had their first nests destroyed, a minority subsequently acted as reproductive parasites. The tendency to parasitize was highly repeatable, which indicates individual specialization. Across years, the fitness pay-offs of the two strategies were approximately equal: females who never parasitized (a ‘pure cooperative’ strategy) laid larger clutches and fledged more young from their own nests than did birds that both nested and parasitized (a ‘mixed’ strategy). Our results suggest that the success of parasites is constrained by reproductive trade-offs as well as by host defences, and illustrate how cooperative and parasitic tactics can coexist stably in the same population. Mixed-effects logistic regression modelling of a dataset of individual reproductive behaviours shows fitness pay-offs of cooperative versus mixed cooperative and parasitic reproductive strategies are approximately equal in female greater anis (Crotophaga major).

Variation in group size is ubiquitous in social animals, but explaining the range of group sizes seen in nature remains challenging.

Research on cooperatively breeding birds usually focuses on social dynamics within the breeding group, but conflict between groups can also affect individual fitness and the evolution of sociality. Here we investigate the causes and consequences of competition between groups of communally breeding greater anis, Crotophaga major , over a 10-year field study. Social groups were spatially clustered into loose aggregations that showed a moderate degree of reproductive synchrony. However, competition between neighbouring groups for nesting sites was intense, occasionally leading to wholesale destruction of a group's nesting attempt and abandonment of the site. We documented 18 cases in which a group's entire clutch of eggs was ejected from the nest during the laying or incubation period, often accompanied by behavioural observations of conflict with a neighbouring group. Clutch destruction typically occurred when two groups attempted to nest in close proximity on high-quality sites: nearest-neighbour distance and nest site type were the strongest predictors of clutch destruction. Surprisingly, group size did not predict whether or not a group's clutch would be destroyed, and small groups sometimes ousted larger groups. By contrast, ‘home field advantage’ did have a significant effect: groups that had previously nested on the site were more likely to destroy the clutches of newly established groups, and this effect increased with the number of years that the group had nested there. Together, these results support previous evidence that competition between groups for high-quality nesting sites is an important driver of communal breeding, and they highlight the importance of location and past history in determining the outcome of intergroup contests in social species.

Hosts of avian brood parasites often use visual cues to reject foreign eggs, and several lineages of brood parasites have evolved mimetic eggshell coloration and patterning to circumvent host recognition. What is the mechanism of parasitic egg color mimicry at the chemical level? Mimetic egg coloration by Common Cuckoos Cuculus canorus is achieved by depositing similar concentrations of colorful pigments into their shells as their hosts. The mechanism of parasitic egg color mimicry at the chemical level in other lineages of brood parasites remains unexplored. Here we report on the chemical basis of egg color mimicry in an evolutionarily independent, and poorly studied, host-parasite system: the Neotropical Striped Cuckoo Tapera naevia and one of its hosts, the Rufous-and-white Wren Thryophilus rufalbus. In most of South America, Striped Cuckoos lay white eggs that are identical to those of local host species. In Central America, however, Striped Cuckoos lay blue eggs that match those of the Rufous-and-white Wren, suggesting that blue egg color in these cuckoo populations is an adaptation to mimic host egg appearance. Here we confirm that Striped Cuckoo eggs are spectrally similar to those of their hosts and consistently contain the same major eggshell pigment, biliverdin. However, wren eggshells lacked protoporphyrin, which was present in the parasitic cuckoo eggshells. Furthermore, biliverdin concentrations were significantly lower in cuckoo eggshells than in host eggshells. Similarity of host-parasite eggshell appearance, therefore, need not always be paralleled by a quantitative chemical match to generate effective visual mimicry in birds.

We studied the diet of Crested Guans (Penelope purpurascens; Galliformes: Cracidae) in lowland tropical forest on Barro Colorado Island, Panama. From June-August 2015 we collected observations of foraging adults using five-minute focal follows of randomly chosen individuals. A total of 141 food items were recorded over 565 minutes of observations. Although Crested Guans are believed to be primarily frugivorous, we found that they consumed a high proportion of leaves (61.7% of items) and insects (24.8%), with fruits comprising a minority of items (13.5%). Guans preferred to eat young leaves, which are more tender and contain higher levels of nitrogen than mature leaves; however, young leaves also contain higher levels of tannins and other secondary defensive compounds, raising new questions about the mechanisms by which arboreal birds digest leaves. Recent studies have found similarly high levels of leaf consumption in other species of guans and chachalacas, suggesting that folivory may be more wi...

Migratory birds generally divide the annual cycle between discrete breeding and nonbreeding ranges. Itinerant breeders, however, reproduce twice at different geographic locations, migrating between them. This unusual flexibility in movement ecology and breeding biology suggests that some species can rapidly modulate the conflicting physiological and behavioral traits required for migration and reproduction. The Phainopepla (Phainopepla nitens), a songbird of the southwestern USA, has long been suspected to breed first in desert habitats in spring, then migrate to woodland habitats to breed again in summer. However, direct evaluation of movement and gene flow among individuals breeding in different locations has previously been logistically intractable. We deployed GPS tags on free-flying Phainopeplas in southern California, all of which migrated to hypothesized woodland breeding habitats after desert breeding (an average distance of 232 km). GPS data also revealed previously unknown fall and spring stopover sites. Population genomic analyses revealed no genetic differentiation among desert and woodland breeding populations, indicating significant movement and gene flow across the region. Finally, we used random forest analyses to quantify substantial environmental differences among temporal stages. Our results provide direct evidence that individual Phainopeplas do indeed move between 2 drastically different breeding habitats in the same year, representing a rare and extreme example of life-history flexibility.

Intermittent breeding, in which an adult skips a breeding opportunity, can represent a non-adaptive constraint or an adaptive response to the tradeoff between current and future reproduction. In group-living animals, the social group may also affect the frequency of reproduction, but this possibility has received little attention. Here we use an 11-year data set to investigate intermittent breeding in the greater ani (Crotophaga major), a tropical bird that nests in stable breeding groups containing several unrelated co-breeding females. Population-wide, an average of 62% of females laid eggs in a given year (range 35–84%), and the average female failed to lay eggs once every 3.2 years. We found little support for the hypothesis that intermittent breeding reflects a tradeoff between current and future reproduction: breeding in year t did not affect a female’s likelihood of breeding in year t + 1, and clutch size in year t did not affect clutch size in year t + 1. Increases in clutch size were associated with decreases in egg mass for eggs laid at the end of that clutch, but this did not affect subsequent nesting attempts. However, reproductive skipping was associated with changes in group membership. Females whose groups changed in composition after year t were significantly less likely to breed in year t + 1 than females whose groups remained stable. These results indicate that breeding group stability influences the frequency of reproduction, suggesting that transitions between groups may be costly to females and their mates.

Classic evolutionary theory predicts that monogamy should be intimately linked with parental care. It has long been assumed, therefore, that avian brood parasites—which lay their eggs in the nests of ‘host’ species and provide little, if any, parental care—should be overwhelmingly promiscuous. However, recent studies have revealed that the social mating systems of brood parasites are surprisingly diverse, encompassing lek polygyny, monogamy, polygamy and promiscuity. What ecological or phylogenetic factors explain this variation, and why are some brood parasites apparently monogamous? Here we review the social and genetic mating systems of all 75 brood parasitic species for which data are available and evaluate several hypotheses that may help explain these patterns. We find that social monogamy is widespread, often co-occurring with territoriality and cooperative behaviour by the mated pair. Comparative studies, though preliminary, suggest that in some species, monogamy is associated with low host density and polygamy with higher host density. Interestingly, molecular data show that genetic and social mating systems can be entirely decoupled: genetic monogamy can occur in parasitic species that lack behavioural pair-bonds, possibly as a by-product of territoriality; conversely, social monogamy has been reported in parasites that are genetically polygamous. This synthesis suggests that social and genetic monogamy may result from very different selective pressures, and that male–female cooperative behaviours, population density and territoriality may all interact to favour the evolution of monogamous mating in brood parasites. Given that detailed descriptive data of social, and especially genetic, mating systems are still lacking for the majority of brood parasitic species, definitive tests of these hypotheses await future work. This article is part of the theme issue ‘The coevolutionary biology of brood parasitism: from mechanism to pattern’.

Reproduction among members of social animal groups is often highly synchronized, but neither the selective advantages nor the proximate causes of synchrony are fully understood. Here I investigate the evolution of hatching synchrony in the Greater Ani (Crotophaga major), a communally nesting bird in which several unrelated females contribute eggs to a large, shared clutch. Hatching synchrony is variable, ranging from complete synchrony to moderate asynchrony, and is determined by the onset of incubation of the communal clutch. Data from a 10-year field study indicate that individual reproductive success is highest in synchronous groups, and that nestlings that hatch in the middle of the hatching sequence are most likely to survive. Nestling mortality is high in asynchronous clutches because early-hatching nestlings are more likely to be killed by adult group members, whereas late-hatching nestlings are more likely to starve due competition with their older nest-mates. Therefore, the timing of hatching appears to be under stabilizing selection from infanticide and resource competition acting in concert. These results provide empirical support for models predicting that synchrony may evolve as an adaptive counter-strategy to infanticide, and they highlight the importance of competition in shaping the timing of reproduction in social groups.

The study of cooperative breeding in birds has a long history in the New World tropics, beginning with Alexander Skutch’s seminal observations of helpers at the nest. Recent studies of Neotropical birds have revealed a diversity of cooperative systems, ranging from small family groups to complex societies composed of relatives and immigrants. This chapter focuses on the communally breeding cuckoos—the anis and their allies—which breed in social groups with several unrelated co-breeders. Data from a long-term field project on greater anis in Panama sheds light on the selective pressures shaping reproductive strategies, including effects on reproductive fitness, mating and parental care patterns, and alternative reproductive tactics such as conspecific brood parasitism.

Social animals often form long-lasting relationships with fellow group members, usually with close kin. In primates, strong social bonds have been associated with increased longevity, offspring survival and reproductive success. However, little is known about the fitness effects of social bonds between non-kin, especially outside of mammals. In this study, we use long-term field research on a cooperatively breeding bird, the greater ani ( Crotophaga major ), to ask whether adult females benefit by remaining in long-term associations with unrelated, co-breeding females. We find that females that have previously nested together synchronize their reproduction more rapidly than those nesting with unfamiliar partners, which leads to lower competition and higher fledging success. Importantly, although previous experience with a co-breeding female influenced reproductive synchrony, the degree of reproductive synchrony did not influence whether co-breeding females remained together in subsequent years, ruling out the alternate hypothesis that highly synchronized females are simply more likely to remain together. These results indicate that switching groups is costly to females, and that social familiarity improves reproductive coordination. Stable social relationships therefore have significant fitness consequences for cooperatively nesting female birds, suggesting that direct benefits alone may favour the evolution of associations between non-relatives and contribute to long-term group stability.

In many cooperative animal societies, individuals can recognize their relatives and preferentially direct helping behaviors towards them. However, the ability to learn kin recognition cues may be constrained in societies with low relatedness, since group membership alone is not a reliable proxy for kinship. Here, we examine kin discrimination in the greater ani (Crotophaga major), a communally nesting bird in which several unrelated males and females reproduce in a single, shared nest and provide parental care to the mixed clutch of young. Each adult, therefore, is closely related to some nestlings in the clutch and unrelated to others. Food is limited and starvation is a significant cause of nestling mortality, suggesting that adults should increase their fitness by preferentially feeding their own offspring in the mixed clutch. To test this hypothesis, we cross-fostered broods of nestlings between pairs of nests, such that none of the nestlings in the manipulated nests were related to any of the adults feeding them. We found no evidence that adult greater anis discriminate between their own and unrelated nestlings: adults at cross-fostered groups fed nestlings at the same rates as adults at control (sham-manipulated) nests, and rates of nestling starvation were equal at cross-fostered and control nests. These results suggest that adult greater anis do not recognize their own nestlings, and they are consistent with the hypothesis that genetically encoded markers for kin recognition are rare in birds.

Birds’ eggshells are primarily composed of calcite, an abundant polymorph of calcium carbonate (CaCO3). However, the eggshells of some species are coated with spherules of vaterite, a rare and thermodynamically unstable polymorph of CaCO3, the function of which remains unknown. Here we experimentally test the mechanical and physiological effects of the vaterite coating on eggshells of the Greater Ani Crotophaga major, a tropical cuckoo. Vaterite removal did not affect vapour conductance rates across the eggshell, indicating that the vaterite coating does not influence gas exchange during embryonic development. By contrast, nanoindentation revealed that the hardness and elasticity of vaterite is similar to that of calcite, and white light interferometry showed that the vaterite layer increased the total thickness of the shell cuticle by up to 10%. Furthermore, calculations of contact mechanics found that when two eggs come into contact, the depth of the surface deformation caused by the contact is far less than the thickness of the vaterite coating. These results suggest the layer of vaterite spherules may act as a ‘shock absorber’ for the underlying calcite shell, protecting it from mechanical damage caused by collision with other eggs in the nest and reducing the risk of eggshell fracture during incubation.

Social animals vary in how reproduction is divided among group members, ranging from monopolization by a dominant pair (high skew) to equal sharing by cobreeders (low skew). Despite many theoretical models, the ecological and life-history factors that generate this variation are still debated. Here I analyze data from 83 species of cooperatively breeding birds, finding that kinship within the breeding group is a powerful predictor of reproductive sharing across species. Societies composed of nuclear families have significantly higher skew than those that contain unrelated members, a pattern that holds for both multimale and multifemale groups. Within-species studies confirm this, showing that unrelated subordinates of both sexes are more likely to breed than related subordinates are. Crucially, subordinates in cooperative groups are more likely to breed if they are unrelated to the opposite-sex dominant, whereas relatedness to the same-sex dominant has no effect. This suggests that incest avoidance, rather than suppression by dominant breeders, may be an important proximate mechanism limiting reproduction by subordinates. Overall, these results support the ultimate evolutionary logic behind concessions models of skew-namely, that related subordinates gain indirect fitness benefits from helping at the nests of kin, so a lower direct reproductive share is required for selection to favor helping over dispersal-but not the proximate mechanism of dominant control assumed by these models.

Kin selection theory predicts that extrapair mating should be rare in cooperatively breeding birds. However, most cooperative breeders are not genetically monogamous and the relationship between promiscuity and cooperative breeding remains unclear. This relationship is further complicated by a lack of data. The majority of cooperatively breeding birds live in the tropics, and their genetic mating systems are little known. Here we studied the genetic mating system of the Grayish Baywing (Agelaioides badius), a socially monogamous Neotropical blackbird in which most nesting pairs are assisted by helpers, previously assumed to be offspring of the breeding pair. Grayish Baywings are the primary host of the parasitic Screaming Cowbird (Molothrus rufoaxillaris), and previous studies have found a positive association between brood parasitism and helper recruitment in the last part of the nestling period. We used microsatellite markers to analyze the kinship of 192 individuals in 47 breeding groups, finding that 13% of 153 nestlings (in 38% of 47 nests) resulted from extrapair mating. We also documented 2 instances of conspecific brood parasitism and 1 instance of quasiparasitism (the nestling was sired by the social father, but was unrelated to the social mother). Of 8 helpers that were genotyped, 4 (all males) were offspring of the breeding pair and 4 (2 males, 2 females) were unrelated to both members of the breeding pair. None of the helpers produced offspring within the clutch. These results suggest that, although cooperative breeding is frequent, genetic relatedness between Grayish Baywing helpers and the offspring that they raise is highly variable. Future studies are needed to determine why unrelated helpers assist at Grayish Baywing nests, and to understand the role that brood parasitism may have played in the evolution of cooperative breeding in this species. Fil: Ursino, Cynthia Alejandra. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Ecología, Genética y Evolución; Argentina Fil: de Marsico, Maria Cecilia. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Ecología, Genética y Evolución; Argentina Fil: Reboreda, Juan Carlos. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Ecología, Genética y Evolución; Argentina Fil: Riehl, Christina. University of Princeton; Estados Unidos

Inferential reasoning-associating a visible consequence with an imagined event-has been demonstrated in several bird species in captivity, but few studies have tested wild birds in ecologically relevant contexts. Here, we investigate inferential reasoning by the greater ani, a cooperatively breeding cuckoo in which several females lay eggs in one nest. Prior to laying her first egg, each female removes any eggs that have already been laid by other females in the shared nest. After laying her first egg, however, each female stops removing eggs, presumably in order to avoid accidentally rejecting her own. But are anis using inferential reasoning to track the fate of their eggs in the communal nest, or is egg ejection governed by non-cognitive determinants? We experimentally removed eggs from two-female nests after both females had laid at least one egg and used video recording to verify that both females viewed the empty nest. We waited until one female (A) laid an egg in the nest, and video recorded the behavior of the female that had not yet re-laid (B). We predicted that if capable of inferential reasoning, female B should infer that the new egg could not be her own and she should remove it. Five out of five females tested failed to make this inference, suggesting that egg removal is either determined by the female's reproductive status or by the amount of time elapsed between egg removal and re-laying. This apparent cognitive constraint may have implications for the evolutionary stability of the anis' unusual breeding system.

In communally breeding animal societies, theory predicts that a male's investment in parental care should be correlated with his share of paternity in the mixed brood. Here I test this hypothesis in the greater ani, Crotophaga major, a Neotropical cuckoo that nests in groups composed of two to three unrelated, behaviourally monogamous pairs. Each group constructs a single nest in which all of the females lay eggs, and all group members participate in rearing the joint clutch. Previous work has shown that parental investment among males is unequal: just one male in the group performs all nocturnal incubation, and the same male also plays a greater role in diurnal incubation and nest defence. I used parentage and sibling analysis of 357 greater ani nestlings in 53 clutches to investigate genetic mating patterns and the distribution of reproduction within communal groups. Contrary to predictions, male reproductive skew was negligible and nocturnally incubating males did not sire significantly more nestlings than did non-nocturnal incubators. Approximately 75–80% of nestlings were produced by socially monogamous pairs, 12–18% by extrapair fertilizations within the same breeding group, and 3–5% by extrapair fertilizations outside the breeding group. There was no difference in the frequency of extrapair paternity between nocturnally incubating and non-nocturnally incubating males. Compared to other cooperative avian societies, the division of reproduction in greater ani breeding groups is unusually egalitarian, despite marked inequalities in male parental care.

The greater ani ( Crotophaga major ), a Neotropical cuckoo, exhibits an unusual breeding system in which several socially monogamous pairs lay eggs in a single nest and contribute care to the communal clutch. Cooperative nesting is costly—females compete for reproduction by ejecting each other's eggs—but the potential direct or indirect fitness benefits that might accrue to group members have not been identified. In this study, I used molecular genotyping to quantify patterns of genetic relatedness and individual reproductive success within social groups in a single colour-banded population. Microsatellite analysis of 122 individuals in 49 groups revealed that group members are not genetic relatives. Group size was strongly correlated with individual reproductive success: solitary pairs were extremely rare and never successful, and nests attended by two pairs were significantly more likely to be depredated than were nests attended by three pairs. Egg loss, a consequence of reproductive competition, was greater in large groups and disproportionately affected females that initiated laying. However, early-laying females compensated for egg losses by laying larger clutches, and female group members switched positions in the laying order across nesting attempts. The greater ani, therefore, appears to be one of the few species in which cooperative breeding among unrelated individuals is favoured by direct, shared benefits that outweigh the substantial costs of reproductive competition.

The eggshells of communally breeding greater anis Crotophaga major consist of a blue‐green pigmented calcite matrix overlaid by a chalky white layer of vaterite, both of which are polymorphs of calcium carbonate. The white vaterite layer is intact in freshly laid eggs and may function in protecting the eggs from mechanical damage, but it also abrades during incubation to reveal the blue calcite shell underneath. Previous research has shown that this color change serves a visual signaling function: nesting greater anis can discriminate between eggs that are freshly laid and those that have already been incubated, which allows them to reject asynchronous eggs laid by extra‐group parasites. Here we use avian visual modeling and pigment extraction to assess the perceptual and chemical bases of such egg recognition. We found that there was no overlap between the avian perceptual space occupied by ani eggshells with and without vaterite, and that vaterite lacked both of the pigments found in the eggshell's calcite matrix, bililverdin and protoporphyrin. The visual contrast between the unpigmented vaterite and the blue‐pigmented calcite appears to pre‐date the evolution of the signaling function, since the related guira cuckoo Guira guira, also a communal breeder, lays similarly structured and pigmented eggs but does not use the visual contrast as a signal to detect parasitism.

The Greater Ani (Crotophaga major) is a neotropical cuckoo in which several females lay eggs in a single nest. Group members synchronize egg laying and compete for reproduction by ejecting early-laid eggs from the communal nest. Eggs are large (∼17% of female body mass) and vary greatly in size. I assessed the effects of egg size, hatching asynchrony, and position in the laying order on the survival and growth of nestlings to test the hypothesis that females invest more resources in eggs that are likely to give rise to surviving offspring. The egg's position in the female's laying sequence was a significant predictor of egg mass, with first-laid eggs and last-laid eggs consistently smaller than those in the middle of the clutch. Females that initiated laying in the communal nest almost always lost their first-laid eggs, and these females also exhibited the most extreme variation in egg mass. Nestlings from last-laid eggs were more likely to hatch asynchronously and starve before fledging, and the mass of last-laid eggs decreased as the degree of hatching asynchrony increased. Ejection and starvation probabilities were not affected by egg mass; therefore, low survivorship of first-laid and last-laid eggs was due solely to their position in the laying order, not to their smaller size. These data suggest that individual females allocate more resources to eggs that are likely to survive to fledging and that reproductive competition among communally breeding females explains much of the variation in egg size in this species. Copyright 2010, Oxford University Press.

The Greater Ani (Crotophaga major) is the least well-known of the communally breeding crotophagine cuckoos, although it is locally abundant in Panama and northern South America. We present substantial new life history information from 87 breeding groups of Greater Anis at Gatun Lake, Panama, and the first description of their conspicuous, highly stereotyped communal displays. Breeding groups were composed of two to five socially monogamous pairs; no pairs nested singly. Seven groups also included an unpaired individual, which in three cases was confirmed to be a 1-year-old male from the previous year's nest. Groups of two and three pairs were most common (accounting for 75 and 20% of groups, respectively); groups containing more than three pairs were rare and their nests were abandoned before incubation began. Eggs were large (∼17% of adult body mass) and varied greatly in size (19–37 g). Egg and nestling development were exceptionally rapid: eggs were incubated for 11–12 days and nestlings were ...

Fruit-eating birds are important seed dispersers in tropical forests, but little is known about the extent to which they rely on insects or how their diets vary seasonally. We used field observations of focal adults to quantify the diets of adult and nestling Black-headed Trogons (Trogon melanocephalus) at nine nests in a lowland dry forest in Costa Rica. From May 2004 to August 2004, we documented 540 food deliveries to nests and 1080 food items consumed by adults. Adult and nestling trogons were largely insectivorous, feeding mainly on moth caterpillars (Lepidoptera). Fruit accounted for only 10.5% of items consumed by adults and 2.2% of items delivered to nestlings (6.1% and 0.6% of estimated dry mass, respectively). Adult and nestling diets differed significantly in both composition and prey size, with adults consuming more fruit and fewer large insects (Phasmatodea and Mantodea) than nestlings and eating more types of arthropods and fruit. Although both adults and nestlings relied heavily on moth larvae, adults preferentially consumed small caterpillars and delivered large ones to their nestlings. In addition, the proportion of large caterpillars delivered to nests remained constant throughout the nestling period, whereas the proportion of large caterpillars eaten by adults declined significantly with nestling age. Overall, arthropods delivered to nests averaged 70% heavier than those consumed by adults (estimated dry mass). Our results suggest that Black-headed Trogons time reproduction to coincide with arthropod rather than fruit abundance, a pattern that may be more common among omnivorous forest birds than previously recognized. SINOPSIS Los frugivoros son dispersadores de semillas muy importantes en los bosques tropicales, pero se conoce muy poco sobre su dependecia de insectos y variaciones estacionales en su dieta. Utilizamos observaciones de campo para cuantificar la dieta de adultos y pichones en Trogon melanocephalus, observando nueve nidos en un bosque bajo tropical seco en Costa Rica. De mayo a agosto de 2004, documentamos 540 entregas de comida a los pichones en los nidos y 1080 articulos alimentarios consumidos por los adultos. Durante el tiempo de estudio tanto los adultos como los pichones, ingirieron una dieta insectivora, alimentandose principalmente de orrugas de Lepidoptera. Las frutas proveyeron un 10.5% de los articulos consumidos por los adultos y 2.2% de los articulos que le llevaron a los pichones (6.1% y 0.6% de masa seca estimada, respectivamente). La dieta de adultos y pichones se diferencio significativamente tanto en composicion como en el tamano de la presa, con los adultos consumiendo mas frutas y menos insectos grandes (Plasmatodea y Mantodea) que los pichones los cuales ingirieron mas tipos de artropodos y frutas. Aunque tanto adultos como pichones dependieron principalmente de larvas de alevillas, los adultos ingirieron con preferencia orrugas pequenas y le ofrecieron a los pichones las de mayor tamano. Ademas, la proporcion de orrugas grandes que se llevaron al nido permanecio constante a traves del periodo de crianza, mientras que la proporcion de orrugas grandes consumida por los adultos se redujo significativamente segun fue en incremento la edad de los pichones. En general, la cantidad de artropodos llevados a los nidos promediaron un 70% mas que lo consumido por los adultos (estimado de masa seca). Nuestros resultados sugieren que el periodo de reproduccion del trogon estudiado coincide con la abundancia de artropodos, en vez de frutas, patron que pudiera ser mas comun, que lo previamente reconocido, entre aves omnivoras de bosques.

Many species of trogons (Trogoniformes: Trogonidae) gather in mixed-gender calling assemblages during the breeding season. These assemblages have been compared to leks and are usually assumed to function in mate choice; however, no field data exist to support this hypothesis. I present five non-mutually exclusive hypotheses for the function of mixed-gender calling assemblages and test the predictions using field data from Black-headed Trogons (Trogon melanocephalus) in a lowland dry forest in Costa Rica. Adult trogons gathered in mobile assemblages of 3–12 individuals that called frequently and chased one another from perch to perch while moving through the forest. Groups formed at sunrise throughout all stages of the breeding cycle and were not significantly male-biased. Both breeding and non-breeding individuals participated in assemblages, and copulations were not observed in assemblages. Prey capture rates of individuals foraging in groups did not differ from those foraging alone. Males calle...

Cooperative breeding in birds typically occurs when offspring - usually males - delay dispersal from their natal group, remaining with the family to help rear younger kin. Sex-biased dispersal is thought to have evolved in order to reduce the risk of inbreeding, resulting in low relatedness between mates and the loss of indirect fitness benefits for the dispersing sex. In this review, we discuss several recent studies showing that dispersal patterns are more variable than previously thought, often leading to complex genetic structure within cooperative avian societies. These empirical findings accord with recent theoretical models suggesting that sex- biased dispersal is neither necessary, nor always sufficient, to prevent inbreeding. The ability to recognize relatives, primarily by learning individual or group-specific vocalizations, may play a more important role in incest avoidance than currently appreciated.

I studied the diet and foraging behavior of fledgling Black-crowned Night-Herons (Nycticorax nycticorax) in a mixed-species nesting colony of Black-crowned Night-Herons and Snowy Egrets (Egretta thula) in New Orleans, Louisiana. In 1 of 5 years, cannibalism of nestlings that had fallen or climbed out of nests was common, accounting for 66 of 94 (70.2%) prey items taken by fledglings. Juveniles took younger conspecifics by both predation and scavenging. Isolated incidents of cannibalism among Black-crowned Night-Herons have been reported previously, but not on a colony-wide scale.

Cooperatively breeding animals live in social groups in which some individuals help to raise the offspring of others, often at the expense of their own reproduction. Kin selection—when individuals increase their inclusive fitness by aiding genetic relatives—is a powerful explanation for the evolution of cooperative breeding, particularly because most groups consist of family members. However, recent molecular studies have revealed that many cooperative groups also contain unrelated immigrants, and the processes responsible for the formation and maintenance of non-kin coalitions are receiving increasing attention. Here, I provide the first systematic review of group structure for all 213 species of cooperatively breeding birds for which data are available. Although the majority of species (55%) nest in nuclear family groups, cooperative breeding by unrelated individuals is more common than previously recognized: 30% nest in mixed groups of relatives and non-relatives, and 15% nest primarily with non-relatives. Obligate cooperative breeders are far more likely to breed with non-kin than are facultative cooperators, indicating that when constraints on independent breeding are sufficiently severe, the direct benefits of group membership can substitute for potential kin-selected benefits. I review three patterns of dispersal that give rise to social groups with low genetic relatedness, and I discuss the selective pressures that favour the formation of such groups. Although kin selection has undoubtedly been crucial to the origin of most avian social systems, direct benefits have subsequently come to play a predominant role in some societies, allowing cooperation to persist despite low genetic relatedness.

The evolution of cooperation remains a central paradox in biology. As Charles Darwin remarked in On the Origin of Species [1], “Natural selection will never produce in a being anything injurious to itself, for natural selection acts solely by and for the good of each”. An operation harming the actor at the benefit of somebody else cannot be easily explained by the theory of natural selection. For this reason, Darwin regarded sterility in female insects to be “by far the most serious special difficulty, which my theory has encountered” [1]. When dealing with human evolution in The Descent of Man [2], Darwin further expounded “He who was ready to sacrifice his life … rather than betray his comrades, would often leave no offspring to inherit his noble nature. … Therefore, it seems scarcely possible … that the number of men gifted with such virtues … could be increased through natural selection, that is, by the survival of the fittest”. Much progress has been made on the paradox of cooperation since the publication of Darwin's epochal work. Major advances include the development of kin selection theory [3] and the insight that all major transitions in biological evolution from simple to complex structures are characterized by some degree of cooperation and sacrifice [4]. But despite decades of study, the 125th anniversary issue of the journal Science still identified the question of ‘how did cooperative behaviour evolve?’ as one of the top 25 challenges scientists would be facing over the next quarter-century [5]. To take up this challenge, we organized two symposia on the evolution of cooperation based on direct fitness benefits in Arolla, Switzerland (supported by CUSO) and at the VIIth ECBB in Prague, Czech Republic. The current theme issue originated at these meetings because the stimulating discussions decidedly revealed that this subject has not received the scientific attention it deserves. Several of the contributors to these meetings have agreed to contribute to this special theme issue, in addition to other experts we invited to share their results, concepts and views on this topic with us. The resulting theme issue on ‘The evolution of cooperation based on direct fitness benefits’ combines 17 articles that are closely linked by a common question: what mechanisms promote cooperation between unrelated individuals, and how is such cooperation evolutionarily stable? This question is not new (cf. [6]), but it has received increased attention over the past several years, driven by new empirical data as presented in [7–11], as well as by novel theoretical and conceptual approaches [12–16]. Empirically, there is a growing realization that the direct fitness benefits of cooperation must be quantified as carefully as kin-selected benefits have been in the past [17]. Studies on human hunter–gatherer societies, for instance, as well as on natural groups of non-human primates and cooperatively breeding vertebrates have provided opportunities for direct measurements of reciprocity and negotiation [18,19]. Theoreticians have moved beyond the tit-for-tat models of reciprocity that held sway over this field for many years, and are now building more complex models to understand cooperation in larger, multi-level societies [20–22] and to consider the importance of individual variation in the evolution of such societies [23]. We have structured this theme issue in three main parts focusing on the evolution of cooperation based on direct fitness benefits at the levels of (i) theoretical models, (ii) animal societies and (iii) humans. We are confident that the contributions to this theme issue will advance the research field by synthesizing our current understanding of cooperation between non-kin, and by pointing out problems that are still outstanding.

The general belief that cooperation and altruism in social groups result primarily from kin selection has recently been challenged, not least because results from cooperatively breeding insects and vertebrates have shown that groups may be composed mainly of non-relatives. This allows testing predictions of reciprocity theory without the confounding effect of relatedness. Here, we review complementary and alternative evolutionary mechanisms to kin selection theory and provide empirical examples of cooperative behaviour among unrelated individuals in a wide range of taxa. In particular, we focus on the different forms of reciprocity and on their underlying decision rules, asking about evolutionary stability, the conditions selecting for reciprocity and the factors constraining reciprocal cooperation. We find that neither the cognitive requirements of reciprocal cooperation nor the often sequential nature of interactions are insuperable stumbling blocks for the evolution of reciprocity. We argue that simple decision rules such as ‘help anyone if helped by someone’ should get more attention in future research, because empirical studies show that animals apply such rules, and theoretical models find that they can create stable levels of cooperation under a wide range of conditions. Owing to its simplicity, behaviour based on such a heuristic may in fact be ubiquitous. Finally, we argue that the evolution of exchange and trading of service and commodities among social partners needs greater scientific focus.

Summary How do cooperatively breeding groups resist invasion by parasitic "cheaters," which dump their eggs in the communal nest but provide no parental care [1,2]? Here I show that Greater Anis ( Crotophaga major ), Neotropical cuckoos that nest in social groups containing several breeding females [3], use a simple rule based on the timing of laying to recognize and reject eggs laid by extragroup parasites. I experimentally confirmed that Greater Anis cannot recognize parasitic eggs based on the appearance of host egg phenotypes or on the number of eggs in the clutch. However, they can discriminate between freshly laid eggs and those that have already been incubated, and they accordingly eject asynchronous eggs. This mechanism is reliable in naturally parasitized nests, because group members typically lay their eggs in tight synchrony, whereas the majority of parasitic eggs are laid several days later. Rejection of asynchronous eggs therefore provides a rare empirical example of a complex, group-level behavior that arises through relatively simple "rules of thumb" without requiring advanced cognitive mechanisms such as learning, counting, or individual recognition.