Noise constrains heterospecific eavesdropping more than conspecific reception of alarm calls.

Many vertebrates eavesdrop on alarm calls of other species, as well as responding to their own species' calls, but eavesdropping on heterospecific alarm calls might be harder than conspecific reception when environmental conditions make perception or recognition of calls difficult. This could occur because individuals lack hearing specializations for heterospecific calls, have less familiarity with them, or require more details of call structure to identify calls they have learned to recognize. We used a field playback experiment to provide a direct test of whether noise, as an environmental perceptual challenge, reduces response to heterospecific compared to conspecific alarm calls. We broadcast superb fairy-wren (Malurus cyaneus) and white-browed scrubwren (Sericornis frontalis) flee alarm calls to each species with or without simultaneous broadcast of ambient noise. Using two species allows isolation of the challenge of heterospecific eavesdropping independently of any effect of call structure on acoustic masking. As predicted, birds were less likely to flee to heterospecific than conspecific alarm calls during noise. We conclude that eavesdropping was harder in noise, which means that noise could disrupt information on danger in natural eavesdropping webs and so compromise survival. This is particularly significant in a world with increasing anthropogenic noise.

Altruism in a volatile world.

The evolution of altruism-costly self-sacrifice in the service of others-has puzzled biologists since The Origin of Species. For half a century, attempts to understand altruism have developed around the concept that altruists may help relatives to have extra offspring in order to spread shared genes. This theory-known as inclusive fitness-is founded on a simple inequality termed Hamilton's rule. However, explanations of altruism have typically not considered the stochasticity of natural environments, which will not necessarily favour genotypes that produce the greatest average reproductive success. Moreover, empirical data across many taxa reveal associations between altruism and environmental stochasticity, a pattern not predicted by standard interpretations of Hamilton's rule. Here we derive Hamilton's rule with explicit stochasticity, leading to new predictions about the evolution of altruism. We show that altruists can increase the long-term success of their genotype by reducing the temporal variability in the number of offspring produced by their relatives. Consequently, costly altruism can evolve even if it has a net negative effect on the average reproductive success of related recipients. The selective pressure on volatility-suppressing altruism is proportional to the coefficient of variation in population fitness, and is therefore diminished by its own success. Our results formalize the hitherto elusive link between bet-hedging and altruism, and reveal missing fitness effects in the evolution of animal societies.

A positive effect of cumulative intergroup threat on reproductive success.

Outgroup conflict is a powerful selective force across all social taxa. While it is well documented that individual outgroup contests can have a range of direct and indirect fitness consequences, the cumulative pressure of outgroup threats could also potentially impact reproductive success. Here, we use long-term life-history data from a wild population of dwarf mongooses (Helogale parvula) to investigate how intergroup interaction (IGI) rate might influence breeding and offspring survival. IGI rate did not predict the number of litters produced in a season or the inter-litter interval. Unexpectedly, IGI rate was positively associated with the number of pups alive three months after emergence from the breeding burrow. This was not due to a difference in how many pups emerged but because those in groups experiencing more IGIs had a higher survival likelihood post-emergence. Detailed natural observations revealed that both IGI occurrence and the threat of intergroup conflict led to more sentinel behaviour by adults, probably reducing the predation risk to young. Our results contrast the previously documented negative effects of outgroup interactions on reproductive success and highlight the need to assess cumulative threat, rather than just the impact of physical contests, when considering outgroup conflict as a social driver of fitness.

Behavioural, demographic and fitness consequences of social instability in cooperatively breeding dwarf mongoose groups.

Social instability frequently arises in group-living species, but the potential costs have rarely been investigated in free-living cooperative breeders, especially across different timeframes. Using natural observations, body mass measurements and life-history data from dwarf mongooses (Helogale parvula), we determined the short- and long-term consequences of a change in one of the dominant breeding pairs. We found that a new breeder led to alterations in both collective and individual behaviours (i.e. increases in communal scent-marking, engagement in intergroup interactions, sentinel activity and within-group grooming), as well as reduced body mass gain, further demographic changes and decreased reproductive success (i.e. fewer pups surviving to adulthood). The effects were particularly apparent when it was the female breeder who changed; new female breeders were younger than more experienced counterparts. Our findings support the idea that stability and cooperation are strongly linked and provide potential reasons for previously documented health and fitness benefits of social stability.

Kin Blackmail as a Coercive Route to Altruism.

AbstractThe evolution of altruism (helping a recipient at personal cost) often involves conflicts of interest. Recipients frequently prefer greater altruism than actors are prepared to provide. Coercion by recipients normally involves limiting an actor's options. Here, we consider the possibility of a coercive recipient limiting its own options. Forty years ago, Amotz Zahavi suggested that nesting birds may be "blackmailed" into increased parental care if offspring threaten to harm themselves (and therefore jeopardize the direct fitness of their parents). In a simple kin selection model, we expand blackmail to indirect fitness and highlight that blackmail can occur between any kin to drive reproductive division of labor. In principle, a recipient may place its own fitness at risk (brinkmanship), imposing sanctions on a relative's indirect fitness if the relative fails to cooperate. To use its own survival or reproduction as leverage in a sequential game, a recipient must increase the extent to which its existing fitness depends on the actor's behavior and therefore credibly commit to a cost if the actor does not comply. As it requires opportunities for commitment, kin blackmail can arise only under stringent conditions, but existing kin blackmailers may pass unnoticed because of their strategic success.

Extended and cumulative effects of experimentally induced intergroup conflict in a cooperatively breeding mammal.

Conflict between rival groups is rife in nature. While recent work has begun exploring the behavioural consequences of this intergroup conflict, studies have primarily considered just the 1-2 h immediately after single interactions with rivals or their cues. Using a habituated population of wild dwarf mongooses (Helogale parvula), we conducted week-long manipulations to investigate longer-term impacts of intergroup conflict. Compared to a single presentation of control herbivore faeces, one rival-group faecal presentation (simulating a territorial intrusion) resulted in more within-group grooming the following day, beyond the likely period of conflict-induced stress. Repeated presentations of outsider cues led to further changes in baseline behaviour by the end of the week: compared to control weeks, mongooses spent less time foraging and foraged closer to their groupmates, even when there had been no recent simulated intrusion. Moreover, there was more baseline territorial scent-marking and a higher likelihood of group fissioning in intrusion weeks. Consequently, individuals gained less body mass at the end of weeks with repeated simulated intrusions. Our experimental findings provide evidence for longer-term, extended and cumulative, effects of an elevated intergroup threat, which may lead to fitness consequences and underpin this powerful selective pressure.

Experimental evidence for delayed contingent cooperation among wild dwarf mongooses.

Many animals participate in biological markets, with strong evidence existing for immediate cooperative trades. In particular, grooming is often exchanged for itself or other commodities, such as coalitionary support or access to food and mates. More contentious is the possibility that nonhuman animals can rely on memories of recent events, providing contingent cooperation even when there is a temporal delay between two cooperative acts. Here we provide experimental evidence of delayed cross-commodity grooming exchange in wild dwarf mongooses (Helogale parvula). First, we use natural observations and social-network analyses to demonstrate a positive link between grooming and sentinel behavior (acting as a raised guard). Group members who contributed more to sentinel behavior received more grooming and had a better social-network position. We then used a field-based playback experiment to test a causal link between contributions to sentinel behavior and grooming received later in the day. During 3-h trial sessions, the perceived sentinel contributions of a focal individual were either up-regulated (playback of its surveillance calls, which are given naturally during sentinel bouts) or unmanipulated (playback of its foraging close calls as a control). On returning to the sleeping refuge at the end of the day, focal individuals received more grooming following surveillance-call playback than control-call playback and more grooming than a matched individual whose sentinel contributions were not up-regulated. We believe our study therefore provides experimental evidence of delayed contingent cooperation in a wild nonprimate species.

Habitat degradation negatively affects auditory settlement behavior of coral reef fishes.

Coral reefs are increasingly degraded by climate-induced bleaching and storm damage. Reef recovery relies on recruitment of young fishes for the replenishment of functionally important taxa. Acoustic cues guide the orientation, habitat selection, and settlement of many fishes, but these processes may be impaired if degradation alters reef soundscapes. Here, we report spatiotemporally matched evidence of soundscapes altered by degradation from recordings taken before and after recent severe damage on Australia's Great Barrier Reef. Postdegradation soundscapes were an average of 15 dB re 1 µPa quieter and had significantly reduced acoustic complexity, richness, and rates of invertebrate snaps compared with their predegradation equivalents. We then used these matched recordings in complementary light-trap and patch-reef experiments to assess responses of wild fish larvae under natural conditions. We show that postdegradation soundscapes were 8% less attractive to presettlement larvae and resulted in 40% less settlement of juvenile fishes than predegradation soundscapes; postdegradation soundscapes were no more attractive than open-ocean sound. However, our experimental design does not allow an estimate of how much attraction and settlement to isolated postdegradation soundscapes might change compared with isolated predegradation soundscapes. Reductions in attraction and settlement were qualitatively similar across and within all trophic guilds and taxonomic groups analyzed. These patterns may lead to declines in fish populations, exacerbating degradation. Acoustic changes might therefore trigger a feedback loop that could impair reef resilience. To understand fully the recovery potential of coral reefs, we must learn to listen.

Credible signalling and social bonds: Ultimately drawing on the same idea.

The hypotheses in both target articles rely implicitly on much the same logic. For a "social-bonding" device to make sense, there must be an underlying reason why an otherwise-arbitrary behaviour sustains alliances - namely, credible signals of one's value to partners. To illustrate our points, we draw on the parallels with supposed bonding behaviours in nonhuman animals.

Dwarf mongoose alarm calls: investigating a complex non-human animal call.

Communication plays a vital role in the social lives of many species and varies greatly in complexity. One possible way to increase communicative complexity is by combining signals into longer sequences, which has been proposed as a mechanism allowing species with a limited repertoire to increase their communicative output. In mammals, most studies on combinatoriality have focused on vocal communication in non-human primates. Here, we investigated a potential combination of alarm calls in the dwarf mongoose (Helogale parvula), a non-primate mammal. Acoustic analyses and playback experiments with a wild population suggest: (i) that dwarf mongooses produce a complex call type (T3) which, at least at the surface level, seems to comprise units that are not functionally different to two meaningful alarm calls (aerial and terrestrial); and (ii) that this T3 call functions as a general alarm, produced in response to a wide range of threats. Using a novel approach, we further explored multiple interpretations of the T3 call based on the information content of the apparent comprising calls and how they are combined. We also considered an alternative, non-combinatorial interpretation that frames T3 as the origin, rather than the product, of the individual alarm calls. This study complements previous knowledge of vocal combinatoriality in non-primate mammals and introduces an approach that could facilitate comparisons between different animal and human communication systems.

Hormone-mediated dispersal and sexual maturation in males of the social paper wasp Polistes lanio.

Sex-biased dispersal is common in social species, but the dispersing sex may delay emigration if associated benefits are not immediately attainable. In the social Hymenoptera (ants, some bees and wasps), newly emerged males typically disperse from the natal nest whilst most females remain as philopatric helpers. However, little information exists on the mechanisms regulating male dispersal. Furthermore, the conservation of such mechanisms across the Hymenoptera and any role of sexual maturation are also relatively unknown. Through field observations and mark-recapture, we observed that males of the social paper wasp Polistes lanio emerge from pupation sexually immature, and delay dispersal from their natal nest for up to 7 days whilst undergoing sexual maturation. Delayed dispersal may benefit males by allowing them to mature in the safety of the nest and thus be more competitive in mating. We also demonstrate that both male dispersal and maturation are associated with juvenile hormone (JH), a key regulator of insect reproductive physiology and behaviour, which also has derived functions regulating social organisation in female Hymenoptera. Males treated with methoprene (a JH analogue) dispersed earlier and possessed significantly larger accessory glands than their age-matched controls. These results highlight the wide role of JH in social hymenopteran behaviour, with parallel ancestral functions in males and females, and raise new questions on the nature of selection for sex-biased dispersal.

Experimental evidence that intruder and group member attributes affect outgroup defence and associated within-group interactions in a social fish.

In many social species, individuals communally defend resources from conspecific outsiders. Participation in defence and in associated within-group interactions, both during and after contests with outgroup rivals, is expected to vary between group members because the threat presented by different outsiders is not the same to each individual. However, experimental tests examining both the contributions to, and the consequences of, outgroup conflict for all group members are lacking. Using groups of the cichlid Neolamprologus pulcher, we simulated territorial intrusions by different-sized female rivals and altered the potential contribution of subordinate females to defence. Dominant females and subordinate females defended significantly more against size- and rank-matched intruders, while males displayed lower and less variable levels of defence. Large and small, but not intermediate-sized, intruders induced increased levels of within-group aggression during intrusions, which was targeted at the subordinate females. Preventing subordinate females from helping in territorial defence led to significant decreases in post-contest within-group and female-specific submissive and affiliative displays. Together, these results show that the defensive contributions of group members vary greatly depending both on their own traits and on intruder identity, and this variation has significant consequences for within-group social dynamics both during and in the aftermath of outgroup contests.

High indirect fitness benefits for helpers across the nesting cycle in the tropical paper wasp Polistes canadensis.

Explaining the evolution of helping behaviour in the eusocial insects where nonreproductive ("worker") individuals help raise the offspring of other individuals ("queens") remains one of the most perplexing phenomena in the natural world. Polistes paper wasps are popular study models, as workers retain the ability to reproduce: such totipotency is likely representative of the early stages of social evolution. Polistes is thought to have originated in the tropics, where seasonal constraints on reproductive options are weak and social groups are effectively perennial. Yet, most Polistes research has focused on nontropical species, where seasonality causes family groups to disperse; cofoundresses forming new nests the following spring are often unrelated, leading to the suggestion that direct fitness through nest inheritance is key in the evolution of helping behaviour. Here, we present the first comprehensive genetic study of social structure across the perennial nesting cycle of a tropical Polistes-Polistes canadensis. Using both microsatellites and newly developed single nucleotide polymorphism markers, we show that adult cofoundresses are highly related and that brood production is monopolized by a single female across the nesting cycle. Nonreproductive cofoundresses in tropical Polistes therefore have the potential to gain high indirect fitness benefits as helpers from the outset of group formation, and these benefits persist through the nesting cycle. Direct fitness may have been less important in the origin of Polistes sociality than previously suggested. These findings stress the importance of studying a range of species with diverse life history and ecologies when considering the evolution of reproductive strategies.

Between-group attack and defence in an ecological setting: Insights from nonhuman animals.

Attempts to understand the fundamental forces shaping conflict between attacking and defending groups can be hampered by a narrow focus on humans and reductionist, oversimplified modelling. Further progress depends on recognising the striking parallels in between-group conflict across the animal kingdom, harnessing the power of experimental tests in nonhuman species and modelling the eco-evolutionary feedbacks that drive attack and defence.

Factors influencing within-group conflict over defence against conspecific outsiders seeking breeding positions.

In social species, groups face a variety of threats from conspecific outsiders. Defensive actions are therefore common, but there is considerable variation in which individuals contribute and to what extent. There has been some theoretical exploration of this variation when the defence is of shared resources, but the relative contributions when a single intruder threatens a particular breeding position have received less attention. Defensive actions are costly, both for the individual and dependent young, and contributions are likely to differ depending on individual sex, rank and size, current breeding stage, infanticide risk and relatedness levels. Here, we model analytically the relative fitness benefits of different group members to engaging in defence against individual intruders and determine when within-group conflicts of interest might arise over these defensive contributions. Conflicts of interest between the challenged breeder and other group members depend on relatedness to the brood and the potential relatedness reduction if an intruder acquires breeding status. Conflicts are more likely to occur when there is a low chance of winning the contest, low infanticide rates, inefficient defence from helpers, a long remaining brood-dependency period and high external (non-contest-related) mortality. Our work can help explain variation in defensive actions against out-group threats.

Fish in habitats with higher motorboat disturbance show reduced sensitivity to motorboat noise.

Anthropogenic noise can negatively impact many taxa worldwide. It is possible that in noisy, high-disturbance environments, the range and severity of impacts could diminish over time, but the influence of previous disturbance remains untested in natural conditions. This study demonstrates the effects of motorboat noise on the physiology of an endemic cichlid fish in Lake Malawi. Exposure to motorboats (driven 20-100 m from fish) and loudspeaker playback of motorboat noise both elevated the oxygen-consumption rate at a single lower-disturbance site, characterized by low historic and current motorboat activity. Repeating this assay at further lower-disturbance sites revealed a consistent effect of elevated oxygen consumption in response to motorboat disturbance. However, when similar trials were repeated at four higher-disturbance sites, no effect of motorboat exposure was detected. These results demonstrate that disturbance history can affect local population responses to noise. Action regarding noise pollution should consider the past, as well as the present, when planning for the future.

Expanding the Link between Out-Group Threats and In-Group Behavior: (A Reply to Kavaliers and Choleris).

In social species, groups and their members face a variety of threats from conspecific outsiders. Such out-group conflict is predicted to influence within-group behavior, with empirical work demonstrating this link in humans, primates, and birds. In our note "Out-Group Threat Promotes Within-Group Affiliation in a Cooperative Fish," appearing in The American Naturalist in February 2016, we provided experimental evidence that simulated territorial intrusions result in subsequent increases in affiliation among groupmates in a cichlid fish (Neolamprologus pulcher). Martin Kavaliers and Elena Choleris, in their comment "Out-Group Threat Responses, In-Group Bias, and Nonapeptide Involvement Are Conserved Across Vertebrates," appearing in this issue, commented on our cichlid-fish article; they consider the conserved nature of the link between out-group threat and in-group behavior and bias in vertebrates, the influence of pathogens in the process, and the potential underpinning hormonal mechanisms. Here, we provide clarification and expansion of some of the core points that are discussed in the comment by Kavaliers and Choleris.

Anthropogenic noise pollution from pile-driving disrupts the structure and dynamics of fish shoals.

Noise produced from a variety of human activities can affect the physiology and behaviour of individual animals, but whether noise disrupts the social behaviour of animals is largely unknown. Animal groups such as flocks of birds or shoals of fish use simple interaction rules to coordinate their movements with near neighbours. In turn, this coordination allows individuals to gain the benefits of group living such as reduced predation risk and social information exchange. Noise could change how individuals interact in groups if noise is perceived as a threat, or if it masked, distracted or stressed individuals, and this could have impacts on the benefits of grouping. Here, we recorded trajectories of individual juvenile seabass (Dicentrarchus labrax) in groups under controlled laboratory conditions. Groups were exposed to playbacks of either ambient background sound recorded in their natural habitat, or playbacks of pile-driving, commonly used in marine construction. The pile-driving playback affected the structure and dynamics of the fish shoals significantly more than the ambient-sound playback. Compared to the ambient-sound playback, groups experiencing the pile-driving playback became less cohesive, less directionally ordered, and were less correlated in speed and directional changes. In effect, the additional-noise treatment disrupted the abilities of individuals to coordinate their movements with one another. Our work highlights the potential for noise pollution from pile-driving to disrupt the collective dynamics of fish shoals, which could have implications for the functional benefits of a group's collective behaviour.

Motorboat noise impacts parental behaviour and offspring survival in a reef fish.

Anthropogenic noise is a pollutant of international concern, with mounting evidence of disturbance and impacts on animal behaviour and physiology. However, empirical studies measuring survival consequences are rare. We use a field experiment to investigate how repeated motorboat-noise playback affects parental behaviour and offspring survival in the spiny chromis (Acanthochromis polyacanthus), a brooding coral reef fish. Repeated observations were made for 12 days at 38 natural nests with broods of young. Exposure to motorboat-noise playback compared to ambient-sound playback increased defensive acts, and reduced both feeding and offspring interactions by brood-guarding males. Anthropogenic noise did not affect the growth of developing offspring, but reduced the likelihood of offspring survival; while offspring survived at all 19 nests exposed to ambient-sound playback, six of the 19 nests exposed to motorboat-noise playback suffered complete brood mortality. Our study, providing field-based experimental evidence of the consequences of anthropogenic noise, suggests potential fitness consequences of this global pollutant.

Shipbuilding Docks as Experimental Systems for Realistic Assessments of Anthropogenic Stressors on Marine Organisms.

Empirical investigations of the impacts of anthropogenic stressors on marine organisms are typically performed under controlled laboratory conditions, onshore mesocosms, or via offshore experiments with realistic (but uncontrolled) environmental variation. These approaches have merits, but onshore setups are generally small sized and fail to recreate natural stressor fields, whereas offshore studies are often compromised by confounding factors. We suggest the use of flooded shipbuilding docks to allow studying realistic exposure to stressors and their impacts on the intra- and interspecific responses of animals. Shipbuilding docks permit the careful study of groups of known animals, including the evaluation of their behavioral interactions, while enabling full control of the stressor and many environmental conditions. We propose that this approach could be used for assessing the impacts of prominent anthropogenic stressors, including chemicals, ocean warming, and sound. Results from shipbuilding-dock studies could allow improved parameterization of predictive models relating to the environmental risks and population consequences of anthropogenic stressors.