Cooperative Mammal Research Articles

Reproductive competition and the evolution of extreme birth synchrony in a cooperative mammal

Reproductive events in animal societies often show a high degree of temporal clustering, but the evolutionary causes of this synchronization are poorly understood. Here, we suggest that selection to avoid the negative effects of competition with other females has given rise to a remarkable degree of birth synchrony in the communal-breeding banded mongoose (Mungos mungo). Within banded mongoose groups, births are highly synchronous, with 64 per cent of females giving birth on exactly the same night. Our results indicate that this extreme synchrony arises because offspring suffer an increased risk of infanticide if their mother gives birth before other females, but suffer in competition with older littermates if their mother gives birth after them. These findings highlight the important influence that reproductive competition can have for the evolution of reproductive synchrony.

The presence of an avian co-forager reduces vigilance in a cooperative mammal

Many animals must trade-off anti-predator vigilance with other behaviours. Some species facilitate predator detection by joining mixed-species foraging parties and 'eavesdropping' on the predator warnings given by other taxa. Such use of heterospecific warnings presumably reduces the likelihood of predation, but it is unclear whether it also provides wider benefits, by allowing individuals to reduce their own vigilance. We examine whether the presence of an avian co-forager, the fork-tailed drongo (Dicrurus adsimilis), affects rates of vigilance (including sentinel behaviour) in wild dwarf mongooses (Helogale parvula). We simulate the presence of drongos-using playbacks of their non-alarm vocalizations-to show that dwarf mongooses significantly reduce their rate of vigilance when foraging with this species. This is, to our knowledge, the first study to demonstrate experimentally that a mammal reduces vigilance in the presence of an avian co-forager.

False feeding: the trade-off between chick hunger and caregivers needs in cooperative crows

False feeding, where individuals refrain from delivering a food item to a begging dependent young, has been described in several cooperative bird and mammal species, but its function is still unclear. False feeding has been suggested to represent either a deceptive tactic of helpers aimed at showing off provisioning behavior to the rest of the group without paying the costs or a normal provisioning behavior of caregivers mediated by the trade-off between the hunger of the young and caregivers’ own conditions. Here, we employed an experimental approach to test whether false feeding in cooperatively breeding carrion crows responds plastically to variations of chicks’ and caregivers’ needs. In 4 different treatments, we manipulated the hunger of the brood and the conditions of group members by 1) experimentally feeding the chicks, 2) food-supplementing group members during the breeding season or 3) throughout the whole year, and 4) clipping 2 primary feathers from each wing of some individuals to increase the costs of flight. Breeders increased false feeding when the brood was food supplemented (treatment 1) and after their wings were clipped (treatment 4), whereas helpers did not change their false-feeding behavior in response to these treatments. Conversely, helpers decreased false feeding when food was supplemented year-round (treatment 3), whereas fed breeders did not show any significant difference compared with controls. These results indicate that a trade-off between chicks’ needs (current reproduction) and caregivers’ conditions (future reproduction) modulates the occurrence of false feeding, determining different responses in different group members. Key words: carrion crow, cooperative breeding, cost of reproduction, false feeding, helpers at the nest, provisioning adjustment. [Behav Ecol]

Sex differences in responsiveness to begging in a cooperative mammal

In species where young are provisioned by both parents, males commonly contribute less to parental care than females, and are less responsive to variation in begging rates. Similar differences in the care of young occur among adults in cooperative breeders, but fewer studies have investigated whether these are associated with differences in responsiveness. Here, we present results from a playback experiment investigating responsiveness to begging in the meerkat (Suricata suricatta), a cooperatively breeding mammal. Although increased begging rate raised the feeding rate of adults of both sexes, there was no consistent tendency for females to be more responsive than males. However, when we examined changes in the proportion of food items found that were fed to pups (generosity), we found that females were more responsive than males to increased begging rate. These results can be explained in terms of sex differences in dispersal: in meerkats, females are philopatric and receive considerable benefits from investing in young, both directly, by increasing group size, and indirectly, by recruiting helpers if they inherit the breeding position. In addition, they emphasize that generosity provides a more sensitive measure of responsiveness to begging than feeding rate, as it accounts for variation in foraging success.

Longitudinal differences in 15N between mothers and offspring during and after weaning in a small cooperative mammal, the meerkat (Suricata suricatta)

Gestation and subsequent lactation are energetically costly life history events for mammalian females. We used longitudinal delta15N data from hair samples from offspring and their mothers to explore lactation patterns in a small cooperative mammal, the meerkat (Suricata suricatta). Lactation enriched hair from meerkat offspring in 15N compared with that of their mothers, and this enrichment gradually declined after weaning. Although the observed peak enrichment of approximately 1 per thousand was substantially below the predicted levels of trophic enrichment in capital versus income breeders, we suggest that our results reflect an income breeding tactic in this species. Our study supports the notion that delta15N analyses can be a useful tool to investigate lactation schedules in mammals. However, reliable conclusions from 15N data regarding the nutritional tactics of mammalian females during reproduction may be limited by our scant understanding of the effects of various physiological variables on isotope assimilation.

Subordinate male meerkats prospect for extra-group paternity: alternative reproductive tactics in a cooperative mammal

In cooperatively breeding species, subordinates typically suffer strong constraints on within-group reproduction. While numerous studies have highlighted the additional fitness benefits that subordinates might accrue through helping, few have considered the possibility that subordinates may also seek extra-group matings to improve their chances of actually breeding. Here, we show that subordinate males in cooperative meerkat, Suricata suricatta, societies conduct frequent extraterritorial forays, during periods of peak female fertility, which give rise to matings with females in other groups. Genetic analyses reveal that extra-group paternity (EGP) accrued while prospecting contributes substantially to the reproductive success of subordinates: yielding the majority of their offspring (approx. 70%); significantly reducing their age at first reproduction and allowing them to breed without dispersing. We estimate that prospecting subordinates sire 20-25% of all young in the population. While recent studies on cooperative birds indicate that dominant males accrue the majority of EGP, our findings reveal that EGP can also arise from alternative reproductive tactics employed exclusively by subordinates. It is important, therefore, that future attempts to estimate the fitness of subordinate males in animal societies quantify the distribution of extra-group as well as within-group paternity, because a substantial proportion of the reproductive success of subordinates may otherwise go undetected.

Intrasexual competition and sexual selection in cooperative mammals

In most animals, the sex that invests least in its offspring competes more intensely for access to the opposite sex and shows greater development of secondary sexual characters than the sex that invests most. However, in some mammals where females are the primary care-givers, females compete more frequently or intensely with each other than males. A possible explanation is that, in these species, the resources necessary for successful female reproduction are heavily concentrated and intrasexual competition for breeding opportunities is more intense among females than among males. Intrasexual competition between females is likely to be particularly intense in cooperative breeders where a single female monopolizes reproduction in each group. Here, we use data from a twelve-year study of wild meerkats (Suricata suricatta), where females show high levels of reproductive skew, to show that females gain greater benefits from acquiring dominant status than males and traits that increase competitive ability exert a stronger influence on their breeding success. Females that acquire dominant status also develop a suite of morphological, physiological and behavioural characteristics that help them to control other group members. Our results show that sex differences in parental investment are not the only mechanism capable of generating sex differences in reproductive competition and emphasize the extent to which competition for breeding opportunities between females can affect the evolution of sex differences and the operation of sexual selection.

Stress and the suppression of subordinate reproduction in cooperatively breeding meerkats.

In many animal societies, dominant individuals monopolize reproduction, but the tactics they employ to achieve this are poorly understood. One possibility is that aggressive dominants render their subordinates infertile by inducing chronic physiological "stress." However, this hypothesis has been discarded largely for cooperatively breeding species, where reproductive monopolies are often extreme. Here we provide strong support for the stress-related suppression hypothesis in a cooperative mammal, the meerkat (Suricata suricatta). When pregnant, dominant females subject some subordinate females to escalating aggression, culminating in temporary evictions from the group. While evicted, subordinate females suffer chronic elevation of their glucocorticoid adrenal hormone levels, reproductive down-regulation (reduced pituitary sensitivity to gonadotropin-releasing hormone), reduced conception rates, and increased abortion rates. Rather than constantly harassing all subordinate females, dominants only become aggressive when pregnant themselves (when subordinate reproduction would otherwise conflict with their own) and target those females with whom reproductive conflict is most likely (older, pregnant, and more distantly related females). Our findings suggest that dominant female meerkats employ stressful evictions to suppress reproduction among their probable competitors, when attempting to breed themselves. Given the lack of evidence for stress-related suppression in other cooperative breeders to date, it is clear that social stress alone cannot account for the reproductive failure of subordinates across such societies. However, our findings raise the possibility that, in some cooperative breeders at least, dominants may employ stress-related suppression as a backup mechanism to guard against lapses in reproductive restraint by their subordinates.

Trade-offs between extraterritorial prospecting and helping in a cooperative mammal

Males commonly face a trade-off between investment in offspring care and time spent seeking additional breeding opportunities. Although this trade-off is central to our understanding of the evolution of male parental care, it has been largely ignored by studies of male alloparental care in cooperative societies, where male helpers could face a similar problem. We investigated whether male helpers in cooperative societies of meerkats Suricata suricatta trade off their cooperative contributions to pup feeding against extraterritorial prospecting for mating and dispersal opportunities. Not only did male helpers spend extended periods away from the group during pup care periods, but those that spent most time prospecting also contributed least to pup feeding when present in the group. Regular prospectors lost the most weight over the pup-feeding period and male testosterone levels increased in association with prospecting. As both reduced body condition and elevated testosterone have been shown to compromise the expression of offspring care, these findings provide likely explanations for the reduced pup-feeding rates of regular prospectors. Despite their lapses in contributions to cooperative activities, we found no evidence for punishment of prospectors by other group members, suggesting that helpers are able to adjust their contributions according to their own optima. These findings reveal that male helpers in cooperative species can face similar trade-offs to male parents in noncooperative species, between investment in offspring care and alternative fitness-maximizing tactics such as prospecting. We discuss the broader implications of this work for our understanding of both individual variation and sex differences in contributions to cooperative behaviour.

Play does not enhance social cohesion in a cooperative mammal

The social cohesion hypothesis of play asserts that the adaptive function of social play is to strengthen affiliative ties between group members, thereby increasing cohesion within the social group. Although this hypothesis is frequently cited, it has never been quantitatively tested. I used data collected from a wild population of cooperative mongoose (the meerkat, Suricata suricatta) to test four predictions arising from the hypothesis: first, that an individual's frequency of play, and mean number of play partners, will be positively correlated with group size (because individuals in large groups must strengthen ties with a greater number of animals); second, an individual's frequency of play will be positively related to frequency of other affiliative interactions such as allogrooming; third, an individual's frequency of play will be positively correlated with level of contribution to cooperative group activities (based on the assumption that individuals that are closely bonded to their group will invest more heavily in the group than those with weak ties); and finally, an individual's frequency of play will be positively correlated with duration of tenancy in the natal group. The behaviour of young meerkats failed to fulfil any of these predictions, and I conclude that social play is unlikely to have the capacity to promote social cohesion in mammals.

Dispersal, Eviction, and Conflict in Meerkats (Suricata suricatta): An Evolutionarily Stable Strategy Model

Decisions regarding immigration and emigration are crucial to understanding group dynamics in social animals, but dispersal is rarely treated in models of optimal behavior. We developed a model of evolutionarily stable dispersal and eviction strategies for a cooperative mammal, the meerkat Suricata suricatta. Using rank and group size as state variables, we determined state-specific probabilities that subordinate females would disperse and contrasted these with probabilities of eviction by the dominant female, based on the long-term fitness consequences of these behaviors but incorporating the potential for error. We examined whether long-term fitness considerations explain group size regulation in meerkats; whether long-term fitness considerations can lead to conflict between dominant and subordinate female group members; and under what circumstances those conflicts were likely to lead to stability, dispersal, or eviction. Our results indicated that long-term fitness considerations can explain group size regulation in meerkats. Group size distributions expected from predicted dispersal and eviction strategies matched empirical distributions most closely when emigrant survival was approximately that determined from the field study. Long-term fitness considerations may lead to conflicts between dominant and subordinate female meerkats, and eviction is the most likely result of these conflicts. Our model is computationally intensive but provides a general framework for incorporating future changes in the size of multimember cooperative breeding groups.

Sex ratio variation in the cooperatively breeding alpine marmot Marmota marmota

In cooperatively breeding vertebrate species, a clear theoretical prediction about the direction of sex ratio adjustment can be made: mothers should bias the sex ratio of their offspring towards the helping sex when helpers are absent. A consistent trend in the direction predicted by theory exists in cooperative birds, but theory is still poorly tested in cooperative mammals. Here, multivariate analyses are applied to a long-term data set to test this prediction in two ways in the alpine marmot: (1) across females in a population and (2) in individual females across multiple years. It was shown that in the alpine marmot offspring sex ratio was biased towards the helping sex (males) when helpers were absent, whereas helped mothers produced unbiased sex ratio. Unhelped mothers did not adjust the litter size but produced more sons and fewer daughters than helped mothers. These results support the theoretical prediction and explain well the male bias observed among juvenile alpine marmots at the population level. The occurrence of possible sex ratio manipulations in cooperatively breeding vertebrates is also discussed. Copyright 2004.

Meerkat helpers do not specialize in particular activities

Differences in the relative contributions of individual helpers to cooperative activities in vertebrate societies are sometimes interpreted as evidence of functional specialization and have been compared with the incipient subcaste systems found in some social insects. However, it is not yet clear whether some helpers specialize in particular tasks throughout their life span or whether variation in cooperative behaviour represents a temporary, age-related polyethism. We describe the development of cooperative behaviour in female helpers in meerkats, Suricata suricatta, an obligately cooperative mammal where young produced by the dominant female are reared by up to 30 helpers. Using a combination of field experiments and long-term records of the development of individuals, we investigated whether particular helpers specialize in particular activities. In the first year of life, variation in body weight affected overall levels of involvement in cooperative behaviour as well as relative contributions to different activities, generating contrasting activity profiles between light and heavy helpers. However, the effects of body weight disappeared by the second year of life, and individual differences in foraging success became the principal factor affecting contributions to cooperative behaviour. Contributions to different cooperative activities were positively correlated across individuals, with some helpers consistently contributing more than others to all cooperative activities. Our study provides no evidence that meerkat helpers specialize in particular cooperative activities.

Effects of helpers on juvenile development and survival in meerkats.

Although breeding success is known to increase with group size in several cooperative mammals, the mechanisms underlying these relationships are uncertain. We show that in wild groups of cooperative meerkats, Suricata suricatta, reductions in the ratio of helpers to pups depress the daily weight gain and growth of pups and the daily weight gain of helpers. Increases in the daily weight gain of pups are associated with heavier weights at independence and at 1 year of age, as well as with improved foraging success as juveniles and higher survival rates through the first year of life. These results suggest that the effects of helpers on the fitness of pups extend beyond weaning and that helpers may gain direct as well as indirect benefits by feeding pups.

Offspring food allocation by parents and helpers in a cooperative mammal

In cooperatively breeding species, helpers and parents commonly face two decisions when they find a food item: first, whether to feed the item to a young group member or to eat it themselves; and second, which offspring to feed. Little is known about the factors that influence these decisions in cooperative mammals, though optimal foraging theory provides a basis for a range of predictions. In this article we describe pup feeding behavior by helpers and parents in a cooperative mongoose, the meerkat (Suricata suricatta). When meerkat pups begin accompanying the group, they beg food from older group members, who dig up dispersed prey items. As predicted, the probability of a prey item being fed to a pup shows a positive relationship with prey size and a negative relationship with pup distance. Meerkats apparently follow a ‘‘feed the nearest pup rule’’ and are more likely to feed the nearest pup if it is hungry. Hungrier pups beg more and follow older group members more closely. Across all age categories, females feed pups more frequently than males, both in terms of the relative frequency of feeds, and the proportion of prey biomass found by each individual that is fed to pups. Females also feed female pups significantly more than male pups, while males feed pups of both sexes equally. These sex biases in feeding contributions may result from female group members benefiting more than males from higher pup survival, and in particular higher female pup survival, because females are the philopatric sex. Key words: cooperative breeding, group augmentation, kin selection, meerkat, offspring feeding rules, sex-biased parental care. [Behav Ecol 12:590–599 (2001)]

The effect of pup vocalisations on food allocation in a cooperative mammal, the meerkat ( Suricata suricatta )

In the meerkat (Suricata suricatta), a cooperative mongoose, pups follow potential feeders while the group is foraging and emit incessant calls when soliciting food from them. In contrast to a ’stationary’ brood of chicks, in which nestlings are fed at a fixed location, meerkat pups are ’mobile’ and become spread out. The question arises whether meerkat pups that experience different constraints to those facing chicks have evolved similar begging strategies. This paper describes the vocalisations that meerkat pups emit in the context of begging and investigates the influence of these calls on food allocation by older group members and on the behaviour of littermates. Meerkat pups use two types of calls when soliciting food from a potential feeder. The most common is a ’repeat’ call, which pups emit continuously when following an older forager over several hours a day. In addition, when a potential feeder finds a prey item, the pups next to it emit a bout of calls with increased calling rate, amplitude and fundamental frequency, termed ’high-pitched’ calls. Observations, together with playback experiments, showed that more prey was allocated to pups that called longer and more intensely. The pup closest to a feeder was almost always fed. The probability of emitting high-pitched calls did not depend on the time since a pup had received food, and the change from repeat to high-pitched calls occurred suddenly. The main function of the high-pitched call, therefore, does not appear to be to signal a pup’s hunger state. More likely, the two calls, in the context of begging, may be an adaptation to energetic constraints in a mobile feeding system. Pups, which are dispersed during foraging, may emit repeat calls over long periods to prevent potential feeders from eating all the prey themselves. At the moment a potential feeder finds prey, pups may give the more intense high-pitched calls to direct feeders to bring the food item to them and not to a littermate. Therefore, unlike the stationary feeding system where chicks emit one type of begging call when the feeder approaches the nest, meerkats, with a mobile feeding system, have evolved two discrete types of vocalisations in the context of begging.

Inbreeding avoidance and reproductive skew in a cooperative mammal.

In animal social groups, socially subordinate individuals frequently show low reproductive success or completely fail to breed. This suppression of subordinate reproduction is currently typically attributed to control by dominant individuals. However, subordinates in cooperative groups often lack access to unrelated mates, and an alternative possibility is that their reproduction is limited by inbreeding avoidance. Using the eusocial Damaraland mole-rat Cryptomys damarensis, this paper provides the first experimental evidence, to our knowledge, for this explanation. Subordinate, non-breeding female mole-rats were given access to unrelated mates while remaining in the presence of dominant females, and many became reproductively active soon after unrelated males were introduced. Inbreeding avoidance and the availability of unrelated mates provides a plausible and untested explanation for variation in reproductive skew across animal societies.

Reproductive skew and the threat of eviction: a new perspective

Most recent models of the partitioning of reproduction attempt to explain patterns of skew on the assumption that dominant individuals have complete control over breeding opportunities within the group, but may nevertheless concede a share of direct reproduction to subordinates as an incentive to remain peacefully in the association. Although these models may be applicable to some animal societies, we argue that they fail to provide a comprehensive theory of skew. Instead, we suggest that subordinates may often be able to claim unsanctioned reproduction for themselves, but will be forced to exercise a degree of reproductive restraint lest they incite ejection by the dominant. Reproductive skew, in other words, may reflect the threat of ejection (inducing subordinate restraint) rather than the threat of subordinate departure (inducing reproductive concessions by dominants). We present a simple ESS model of reproductive skew under these circumstances, which demonstrates that a shift in emphasis from reproductive concessions by dominants to reproductive restraint on the part of subordinates, radically alters the predictions of skew models. High group productivity, high relatedness and (when group members are related) strong ecological constraints are all expected to lead to reduced skew (the opposite conclusions to those of previous, concession-based analyses). The reason is that these factors reduce the benefits (or increase the costs) of ejection to the dominant, who therefore does best to tolerate more subordinate reproduction.

Infanticide and expulsion of females in a cooperative mammal.

In cooperative groups of suricates (Suricata suricatta), helpers of both sexes assist breeding adults in defending and feeding pups, and survival rises in larger groups. Despite this, dominant breeding females expel subordinate females from the group in the latter half of their (own) pregnancy apparently because adult females sometimes kill their pups. Some of the females that have been expelled are allowed to rejoin the group soon after the dominant female's pups are born and subsequently assist in rearing the pups. Female helpers initially resist expulsion and repeatedly attempt to return to their natal group, indicating that it is unlikely that dominant females need to grant them reproductive concessions to retain them in the group.

Helping is costly to young birds in cooperatively breeding white-winged choughs

Cooperative breeding among birds is at its most extreme in white-winged choughs ( Corcorax melanorhamphos ). Choughs have never been observed to breed successfully without helpers, and reproductive success increases linearly across all group sizes (maximum = 16). Further, helpers contribute to every aspect of reproduction, including nest building and incubation. Here we show that the contribution of young helpers (one year old and less) to incubation depends on the group in which they live. In small groups (3-5 birds), young helpers contribute as much to incubation as older birds, but in large groups they contribute little. In large groups, help increases sharply with age. Old birds contribute equally, regardless of group size. Although choughs generally do not lose body mass over incubation, young helpers lose mass in proportion to the amount of incubation they perform, independent of any effect of group size. This provides evidence that helpers in cooperatively breeding birds suffer costs from providing help additional to the costs incurred from remaining philopatric. It also demonstrates that the needs of the group influence whether young birds provide help.