Guides and cheats: producer-scrounger dynamics in the human-honeyguide mutualism.

Foraging animals commonly choose whether to find new food (as 'producers') or scavenge from others (as 'scroungers'), and this decision has ecological and evolutionary consequences. Understanding these tactic decisions is particularly vital for naturally occurring producer-scrounger systems of economic importance, because they determine the system's productivity and resilience. Here, we investigate how individuals' traits predict tactic decisions, and the consistency and pay-offs of these decisions, in the remarkable mutualism between humans (Homo sapiens) and greater honeyguides (Indicator indicator). Honeyguides can either guide people to bees' nests and eat the resulting beeswax (producing), or scavenge beeswax (scrounging). Our results suggest that honeyguides flexibly switched tactics, and that guiding yielded greater access to the beeswax. Birds with longer tarsi scrounged more, perhaps because they are more competitive. The lightest females rarely guided, possibly to avoid aggression, or because genetic matrilines may affect female body mass and behaviour in this species. Overall, aspects of this producer-scrounger system probably increase the productivity and resilience of the associated human-honeyguide mutualism, because the pay-offs incentivize producing, and tactic-switching increases the pool of potential producers. Broadly, our findings suggest that even where tactic-switching is prevalent and producing yields greater pay-offs, certain phenotypes may be predisposed to one tactic.

When wax wanes: competitors for beeswax stabilize rather than jeopardize the honeyguide-human mutualism.

Many mutualisms are exploited by third-party species, which benefit without providing anything in return. Exploitation can either destabilize or promote mutualisms, via mechanisms that are highly dependent on the ecological context. Here we study a remarkable bird-human mutualism, in which wax-eating greater honeyguides (Indicator indicator) guide humans (Homo sapiens) to wild bees' nests, in an exchange of knowledge about the location of nests for access to the wax combs inside. We test whether the depletion of wax by mammalian and avian exploiter species either threatens or stabilizes the mutualism. Using camera traps, we monitored feeding visits to wax comb made available following honey harvests. We found that greater honeyguides face competition for wax from conspecifics and nine exploiter species, five of which were not previously known to consume wax. Our results support the hypothesis that heterospecific exploiters stabilize the mutualism, because wax depletion by these competitors probably limits feeding opportunities for conspecific exploiters, favouring the early-arriving individual that guided humans to the bees' nest. These findings highlight the importance of the ecological context of species interactions and provide further evidence for how mutualisms can persist because of, and not in spite of, exploitation by third-party species.

Safeguarding human-wildlife cooperation.

Human-wildlife cooperation occurs when humans and free-living wild animals actively coordinate their behavior to achieve a mutually beneficial outcome. These interactions provide important benefits to both the human and wildlife communities involved, have wider impacts on the local ecosystem, and represent a unique intersection of human and animal cultures. The remaining active forms are human-honeyguide and human-dolphin cooperation, but these are at risk of joining several inactive forms (including human-wolf and human-orca cooperation). Human-wildlife cooperation faces a unique set of conservation challenges, as it requires multiple components-a motivated human and wildlife partner, a suitable environment, and compatible interspecies knowledge-which face threats from ecological and cultural changes. To safeguard human-wildlife cooperation, we recommend: (i) establishing ethically sound conservation strategies together with the participating human communities; (ii) conserving opportunities for human and wildlife participation; (iii) protecting suitable environments; (iv) facilitating cultural transmission of traditional knowledge; (v) accessibly archiving Indigenous and scientific knowledge; and (vi) conducting long-term empirical studies to better understand these interactions and identify threats. Tailored safeguarding plans are therefore necessary to protect these diverse and irreplaceable interactions. Broadly, our review highlights that efforts to conserve biological and cultural diversity should carefully consider interactions between human and animal cultures. Please see AfricanHoneyguides.com/abstract-translations for Kiswahili and Portuguese translations of the abstract.

Social dominance and rainfall predict telomere dynamics in a cooperative arid-zone bird.

In many vertebrate societies dominant individuals breed at substantially higher rates than subordinates, but whether this hastens ageing remains poorly understood. While frequent reproduction may trade off against somatic maintenance, the extraordinary fecundity and longevity of some social insect queens highlight that breeders need not always suffer more rapid somatic deterioration than their nonbreeding subordinates. Here, we used extensive longitudinal assessments of telomere dynamics to investigate the impact of dominance status on within-individual age-related changes in somatic integrity in a wild social bird, the white-browed sparrow-weaver (Plocepasser mahali). Dominant birds, who monopolise reproduction, had neither shorter telomeres nor faster telomere attrition rates over the long-term (1-5 years) than their subordinates. However, over shorter (half-year) time intervals dominants with shorter telomeres showed lower rates of telomere attrition (and evidence suggestive of telomere lengthening), while the same was not true among subordinates. Dominants may therefore invest more heavily in telomere length regulation (and/or somatic maintenance more broadly); a strategy that could mitigate the long-term costs of reproductive effort, leaving their long-term telomere dynamics comparable to those of subordinates. Consistent with the expectation that reproduction entails short-term costs to somatic integrity, telomere attrition rates were most severe for all birds during the breeding seasons of wetter years (rainfall is the key driver of reproductive activity in this arid-zone species). Our findings suggest that, even in vertebrate societies in which dominants monopolise reproduction, dominants may experience long-term somatic integrity trajectories indistinguishable from those of their nonreproductive subordinates.

The development of individual differences in cooperative behaviour: maternal glucocorticoid hormones alter helping behaviour of offspring in wild meerkats.

The phenotype of parents can have long-lasting effects on the development of offspring as well as on their behaviour, physiology and morphology as adults. In some cases, these changes may increase offspring fitness but, in others, they can elevate parental fitness at a cost to the fitness of their offspring. We show that in Kalahari meerkats ( Suricata suricatta), the circulating glucocorticoid (GC) hormones of pregnant females affect the growth and cooperative behaviour of their offspring. We performed a 3-year experiment in wild meerkats to test the hypothesis that GC-mediated maternal effects reduce the potential for offspring to reproduce directly and therefore cause them to exhibit more cooperative behaviour. Daughters (but not sons) born to mothers treated with cortisol during pregnancy grew more slowly early in life and exhibited significantly more of two types of cooperative behaviour (pup rearing and feeding) once they were adults compared to offspring from control mothers. They also had lower measures of GCs as they aged, which could explain the observed increases in cooperative behaviour. Because early life growth is a crucial determinant of fitness in female meerkats, our results indicate that GC-mediated maternal effects may reduce the fitness of offspring, but may elevate parental fitness as a consequence of increasing the cooperative behaviour of their daughters. This article is part of the theme issue 'Developing differences: early-life effects and evolutionary medicine'.

Rank-Related Contrasts in Longevity Arise from Extra-Group Excursions Not Delayed Senescence in a Cooperative Mammal.

In many cooperatively breeding animal societies, breeders outlive non-breeding subordinates, despite investing heavily in reproduction [1-3]. In eusocial insects, the extended lifespans of breeders arise from specialized slowed aging profiles [1], prompting suggestions that reproduction and dominance similarly defer aging in cooperatively breeding vertebrates, too [4-6]. Although lacking the permanent castes of eusocial insects, breeders of vertebrate societies could delay aging via phenotypic plasticity (similar rank-related changes occur in growth, neuroendocrinology, and behavior [7-10]), and such plastic deferment of aging may reveal novel targets for preventing aging-related diseases [11]. Here, we investigate whether breeding dominants exhibit extended longevity and delayed age-related physiological declines in wild cooperatively breeding meerkats. We show that dominants outlive subordinates but exhibit faster telomere attrition (a marker of cellular senescence and hallmark of aging [12]) and that in dominants (but not subordinates), rapid telomere attrition is associated with mortality. Our findings further suggest that, rather than resulting from specialized aging profiles, differences in longevity between dominants and subordinates are driven by subordinate dispersal forays, which become exponentially more frequent with age and increase subordinate mortality. These results highlight the need to critically examine the causes of rank-related longevity contrasts in other cooperatively breeding vertebrates, including social mole-rats, where they are currently attributed to specialized aging profiles in dominants [4].

Effects of early-life competition and maternal nutrition on telomere lengths in wild meerkats.

Early-life adversity can affect health, survival and fitness later in life, and recent evidence suggests that telomere attrition may link early conditions with their delayed consequences. Here, we investigate the link between early-life competition and telomere length in wild meerkats. Our results show that, when multiple females breed concurrently, increases in the number of pups in the group are associated with shorter telomeres in pups. Given that pups from different litters compete for access to milk, we tested whether this effect is due to nutritional constraints on maternal milk production, by experimentally supplementing females' diets during gestation and lactation. While control pups facing high competition had shorter telomeres, the negative effects of pup number on telomere lengths were absent when maternal nutrition was experimentally improved. Shortened pup telomeres were associated with reduced survival to adulthood, suggesting that early-life competition for nutrition has detrimental fitness consequences that are reflected in telomere lengths. Dominant females commonly kill pups born to subordinates, thereby reducing competition and increasing growth rates of their own pups. Our work suggests that an additional benefit of infanticide may be that it also reduces telomere shortening caused by competition for resources, with associated benefits for offspring ageing profiles and longevity.

The oxidative costs of reproduction are group-size dependent in a wild cooperative breeder.

Life-history theory assumes that reproduction entails a cost, and research on cooperatively breeding societies suggests that the cooperative sharing of workloads can reduce this cost. However, the physiological mechanisms that underpin both the costs of reproduction and the benefits of cooperation remain poorly understood. It has been hypothesized that reproductive costs may arise in part from oxidative stress, as reproductive investment may elevate exposure to reactive oxygen species, compromising survival and future reproduction and accelerating senescence. However, experimental evidence of oxidative costs of reproduction in the wild remains scarce. Here, we use a clutch-removal experiment to investigate the oxidative costs of reproduction in a wild cooperatively breeding bird, the white-browed sparrow weaver, Plocepasser mahali. Our results reveal costs of reproduction that are dependent on group size: relative to individuals in groups whose eggs were experimentally removed, individuals in groups that raised offspring experienced an associated cost (elevated oxidative damage and reduced body mass), but only if they were in small groups containing fewer or no helpers. Furthermore, during nestling provisioning, individuals that provisioned at higher rates showed greater within-individual declines in body mass and antioxidant protection. Our results provide rare experimental evidence that reproduction can negatively impact both oxidative status and body mass in the wild, and suggest that these costs can be mitigated in cooperative societies by the presence of additional helpers. These findings have implications for our understanding of the energetic and oxidative costs of reproduction, and the benefits of cooperation in animal societies.

Immune response in a wild bird is predicted by oxidative status, but does not cause oxidative stress.

The immune system provides vital protection against pathogens, but extensive evidence suggests that mounting immune responses can entail survival and fecundity costs. The physiological mechanisms that underpin these costs remain poorly understood, despite their potentially important role in shaping life-histories. Recent studies involving laboratory models highlight the possibility that oxidative stress could mediate these costs, as immune-activation can increase the production of reactive oxygen species leading to oxidative stress. However, this hypothesis has rarely been tested in free-ranging wild populations, where natural oxidative statuses and compensatory strategies may moderate immune responses and their impacts on oxidative status. Furthermore, the possibility that individuals scale their immune responses according to their oxidative status, conceivably to mitigate such costs, remains virtually unexplored. Here, we experimentally investigate the effects of a phytohaemagglutinin (PHA) immune-challenge on oxidative status in wild male and female white-browed sparrow weavers, Plocepasser mahali. We also establish whether baseline oxidative status prior to challenge predicts the scale of the immune responses. Contrary to previous work on captive animals, our findings suggest that PHA-induced immune-activation does not elicit oxidative stress. Compared with controls (n = 25 birds), PHA-injected birds (n = 27 birds) showed no evidence of a differential change in markers of oxidative damage or enzymatic and non-enzymatic antioxidant protection 24 hours after challenge. We did, however, find that the activity of a key antioxidant enzyme (superoxide dismutase, SOD) prior to immune-activation predicted the scale of the resulting swelling: birds with stronger initial SOD activity subsequently produced smaller swellings. Our findings (i) suggest that wild birds can mount immune responses without suffering from systemic oxidative stress, and (ii) lend support to biomedical evidence that baseline oxidative status can impact the scale of immune responses; a possibility not yet recognised in ecological studies of immunity.

Oxidative stress and life histories: unresolved issues and current needs.

Life-history theory concerns the trade-offs that mold the patterns of investment by animals between reproduction, growth, and survival. It is widely recognized that physiology plays a role in the mediation of life-history trade-offs, but the details remain obscure. As life-history theory concerns aspects of investment in the soma that influence survival, understanding the physiological basis of life histories is related, but not identical, to understanding the process of aging. One idea from the field of aging that has gained considerable traction in the area of life histories is that life-history trade-offs may be mediated by free radical production and oxidative stress. We outline here developments in this field and summarize a number of important unresolved issues that may guide future research efforts. The issues are as follows. First, different tissues and macromolecular targets of oxidative stress respond differently during reproduction. The functional significance of these changes, however, remains uncertain. Consequently there is a need for studies that link oxidative stress measurements to functional outcomes, such as survival. Second, measurements of oxidative stress are often highly invasive or terminal. Terminal studies of oxidative stress in wild animals, where detailed life-history information is available, cannot generally be performed without compromising the aims of the studies that generated the life-history data. There is a need therefore for novel non-invasive measurements of multi-tissue oxidative stress. Third, laboratory studies provide unrivaled opportunities for experimental manipulation but may fail to expose the physiology underpinning life-history effects, because of the benign laboratory environment. Fourth, the idea that oxidative stress might underlie life-history trade-offs does not make specific enough predictions that are amenable to testing. Moreover, there is a paucity of good alternative theoretical models on which contrasting predictions might be based. Fifth, there is an enormous diversity of life-history variation to test the idea that oxidative stress may be a key mediator. So far we have only scratched the surface. Broadening the scope may reveal new strategies linked to the processes of oxidative damage and repair. Finally, understanding the trade-offs in life histories and understanding the process of aging are related but not identical questions. Scientists inhabiting these two spheres of activity seldom collide, yet they have much to learn from each other.

Species interactions and the structure of complex communication networks.

A universal challenge faced by animal species is the need to communicate effectively against a backdrop of heterospecific signals. It is often assumed that this need results in signal divergence to minimize interference among community members, yet previous support for this idea is mixed, and few studies have tested the opposing hypothesis that interactions among competing species promote widespread convergence in signaling regimes. Using a null model approach to analyze acoustic signaling in 307 species of Amazonian birds, we show that closely related lineages signal together in time and space and that acoustic signals given in temporal or spatial proximity are more similar in design than expected by chance. These results challenge the view that multispecies choruses are structured by temporal, spatial, or acoustic partitioning and instead suggest that social communication between competing species can fundamentally organize signaling assemblages, leading to the opposite pattern of clustering in signals and signaling behavior.