Foster carers influence brood pathogen resistance in ants

Social organisms face a high risk of epidemics, and respond to this threat by combining efficient individual and collective defences against pathogens. An intriguing and little studied feature of social animals is that individual pathogen resistance may depend not only on genetic or maternal factors, but also on the social environment during development. Here, we used a cross-fostering experiment to investigate whether the pathogen resistance of individual ant workers was shaped by their own colony of origin or by the colony of origin of their carers. The origin of care-giving workers significantly influenced the ability of newly eclosed cross-fostered Formica selysi workers to resist the fungal entomopathogen Beauveria bassiana. In particular, carers that were more resistant to the fungal entomopathogen reared more resistant workers. This effect occurred in the absence of post-infection social interactions, such as trophallaxis and allogrooming. The colony of origin of eggs significantly influenced the survival of the resulting individuals in both control and pathogen treatments. There was no significant effect of the social organization (i.e. whether colonies contain a single or multiple queens) of the colony of origin of either carers or eggs. Our experiment reveals that social interactions during development play a central role in moulding the resistance of emerging workers.     

Individual-level personality influences social foraging and collective behaviour in wild birds

There is increasing evidence that animal groups can maintain coordinated behaviour and make collective decisions based on simple interaction rules. Effective collective action may be further facilitated by individual variation within groups, particularly through leader–follower polymorphisms. Recent studies have suggested that individual-level personality traits influence the degree to which individuals use social information, are attracted to conspecifics, or act as leaders/followers. However, evidence is equivocal and largely limited to laboratory studies. We use an automated data-collection system to conduct an experiment testing the relationship between personality and collective decision-making in the wild. First, we report that foraging flocks of great tits (Parus major) show strikingly synchronous behaviour. A predictive model of collective decision-making replicates patterns well, suggesting simple interaction rules are sufficient to explain the observed social behaviour. Second, within groups, individuals with more reactive personalities behave more collectively, moving to within-flock areas of higher density. By contrast, proactive individuals tend to move to and feed at spatial periphery of flocks. Finally, comparing alternative simulations of flocking with empirical data, we demonstrate that variation in personality promotes within-patch movement while maintaining group cohesion. Our results illustrate the importance of incorporating individual variability in models of social behaviour.     

Modes of cooperation during territorial defense by African lions

Cooperation during territorial defense allows social groups of African lions to defend access to resources necessary for individual reproductive success. Some forms of cooperation will be dependent upon cognition: reciprocity places greater cognitive demands on participants than does kinship or mutualism. Lions have well-developed cognitive abilities that enable individuals to recognize and interact with others in ways that seem to enhance their inclusive fitness. Male lions appear to cooperate unconditionally, consistently responding to roaring intruders regardless of their male companions’ kinship or behavior. Female lions, however, do keep track of the past behavior of their female companions, apparently using the reliability of a companion as one means of assessing the risks posed by approaching intruders. Some “laggard” females may exploit the cooperative tendencies of “leaders” during territorial encounters. Although leader females clearly recognize laggards as such, the costs of tolerating laggards may be less than the benefits leaders gain through territorial defense behavior. Thus, although lions clearly have the cognitive ability to base cooperation on reciprocity, territorial defense cooperation appears instead to be based primarily on mutual benefits to participants for both male and female lions.     

Size and experience matter: diving behaviour of juvenile New Zealand sea lions (Phocarctos hookeri)

The diving ability of juvenile animals is constrained by their physiology, morphology and lack of experience, compared to adults. We studied the influences of age and mass on the diving behaviour of juvenile (2–3-year-old females, n = 12; 3–5-year-old males, n = 7) New Zealand (NZ) sea lions (Phocarctos hookeri) using time–depth recorders (TDRs) from 2008 to 2010 in the NZ subantarctic Auckland Islands. Diving ability (e.g. dive depth, duration and bottom time per dive) improved with age and mass. However, the percentage of each dive spent at the bottom, along with percentage time at sea spent diving, was comparable between younger and lighter juveniles and older and heavier juveniles. These suggest that younger and older juveniles expend similar foraging effort in terms of the amount of time spent underwater. Only, 5-year-old male juveniles dove to adult female depths and durations and had the highest foraging efficiency at depths >250 m. It appears that juvenile NZ sea lions attain adult female diving ability at around 5 years of age (at least in males), but prior to this, their performance is limited. Overall, the restricted diving capabilities of juvenile NZ sea lions may limit their available foraging habitat and ability to acquire food at deeper depths. The lower diving ability of juvenile NZ sea lions compared to adults, along with juvenile-specific constraints, should be taken into consideration for the effective management of this declining, nationally critical species.     

Generalization of learned predator recognition: an experimental test and framework for future studies

While some prey species possess an innate recognition of their predators, others require learning to recognize their predators. The specific characteristics of the predators that prey learn and whether prey can generalize this learning to similar predatory threats have been virtually ignored. Here, we investigated whether fathead minnows that learned to chemically recognize a specific predator species as a threat has the ability to generalize their recognition to closely related predators. We found that minnows trained to recognize the odour of a lake trout as a threat (the reference predator) generalized their responses to brook trout (same genus as lake trout) and rainbow trout (same family), but did not generalize to a distantly related predatory pike or non-predatory suckers. We also found that the intensity of antipredator responses to the other species was correlated with the phylogenetic distance to the reference predator; minnows responded with a higher intensity response to brook trout than rainbow trout. This is the first study showing that prey have the ability to exhibit generalization of predator odour recognition. We discuss these results and provide a theoretical framework for future studies of generalization of predator recognition.     

Speed–accuracy trade-offs during foraging decisions in the acellular slime mould Physarum polycephalum

Speed–accuracy trade-offs (SATs) are thought to be a fundamental feature of biological information processing, yet most evidence of SATs comes from animals. Here, we examine SATs in the foraging decisions of an acellular, amoeboid organism: the slime mould Physarum polycephalum. Slime moulds were given a simple discrimination task: selecting the highest-quality food item from a set of three options. We investigated the effect of two stressors, light exposure and hunger, on the speed and accuracy of decision-making. We also examined the effect of task difficulty. When given a difficult discrimination task, stressed individuals tend to make faster decisions than non-stressed individuals. This effect was reversed in plasmodia given easy discrimination tasks, where stressed individuals made slower decisions than non-stressed individuals. We found evidence of SATs, such that individuals who made fast decisions were more likely to make costly errors by selecting the worst possible food option. Our results suggest that SATs occur in a wider range of taxa than previously considered.     

Delayed song maturation and territorial aggression in a songbird

Asymmetries in competitive ability can determine the outcome of social interactions in animals and are often expressed through differences in sexual traits. Competitive ability (resource holding potential, RHP), trait expression and ultimately reproductive success may vary with an individual's age or experience. In some species, reproductively mature males delay acquisition of some adult traits and thereby signal their young age. Theory on animal contests predicts that individuals assess the RHP of an opponent relative to their own, such that escalation is more common between evenly matched opponents. Here, we test predictions from this hypothesis that males respond to a territorial intruder based on their RHP relative to the intruder's RHP. We simulated white-crowned sparrows (Zonotrichia leucophrys) intruding into the territory of a recruit or return. Playback of a song repertoire simulating a young male (recruit) elicited a weaker response from established territory holders (return), but a stronger response from recruits. Playback of a single song type simulating an older male elicited the opposite responses. This indicates that males distinguished between simulated young and old intruders based on song, and responded differently depending on their own experience. Our study highlights the possibility that receiver as well as sender traits should be considered when interpreting animal interactions.     

Size-structured risk assessments govern Daphnia migration

One of the more fascinating phenomena in nature is animal mass migrations and in oceans and freshwaters, diel variations in depth distribution of zooplankton are a phenomenon that has intrigued scientists for more than a century. In our study, we show that zooplankton are able to assess the threat level of ultraviolet radiation and adjust their depth distribution to this level at a very fine tuned scale. Moreover, predation risk induces a size-structured depth separation, such that small individuals, which we show are less vulnerable to predation than larger, make a risk assessment and continue feeding in surface waters during day, offering a competitive release from down-migrating larger animals. Hence, we mechanistically show that such simple organisms as invertebrate zooplankton are able to make individual, size-specific decisions regarding how to compromise between threats from both predators and UV radiation, and adjust their diel migratory patterns accordingly.     

Field crickets change mating preferences using remembered social information

Plasticity in female mate choice can fundamentally alter selection on male ornaments, but surprisingly few studies have examined the role of social learning in shaping female mating decisions in invertebrates. We used the field cricket Teleogryllus oceanicus to show that females retain information about the attractiveness of available males based on previous social experience, compare that information with incoming signals and then dramatically reverse their preferences to produce final, predictable, mating decisions. Male ornament evolution in the wild may depend much more on the social environment and behavioural flexibility through learning than was previously thought for non-social invertebrates. The predictive power of these results points to a pressing need for theoretical models of sexual selection that incorporate effects of social experience.     

The effects of familiarity and social hierarchy on group membership decisions in a social fish

Members of animal groups face a trade-off between the benefits of remaining with a familiar group and the potential benefits of dispersing into a new group. Here, we examined the group membership decisions of Neolamprologus pulcher, a group-living cichlid. We found that subordinate helpers showed a preference for joining familiar groups, but when choosing between two unfamiliar groups, helpers did not preferentially join groups that maximized their social rank. Rather, helpers preferred groups containing larger, more dominant individuals, despite receiving significantly more aggression within these groups, possibly owing to increased protection from predation in such groups. These results suggest a complex decision process in N. pulcher when choosing among groups, dependent not only on familiarity but also on the social and life-history consequences of joining new groups.     

The ontogeny of social play in a feral troop of vervet monkeys (Cercopithecus aethiops sabaeus): The function of early play

We describe the ontogeny of social play over the first 30 weeks of age in a troop of feral vervet monkeys (Cercopithecus aethiops sabaeus) in Barbados. Play time increased rapidly for the first 10 weeks but remained relatively constant thereafter. The form of play changed with infant age; bouts became more frequent but of shorter duration. Play time, bout frequency, and bout duration at a given age differed between infants; younger infants altered their play patterns to complement those of older infants. All infants played more within their own year class than with older juveniles; play time increased with decreasing age difference between the infant and the play partner. Infants terminated a higher proportion of their play bouts the greater the age difference between themselves and their play partners. Preferred play partners are therefore individuals of similar age that will be similar in size and have matched motivation to play and form of play. Neither play time nor proportion of bouts initiated or terminated was correlated with the social rank of the play partner, which suggests that play is not directed toward individuals that may be high-value alliance partners. Maternal intervention in play occurred primarily when infants were<10 weeks old. It was not correlated with the age or social rank of the mother or with the age or social rank of her infant's play partner. Infants played more and terminated a lower proportion of their play bouts in the absence of their mothers than in their presence. Our results are consistent with the hypothesis that the primary function of early play is to enhance physical fitness and to develop coordination and other fighting skills, with minimal risk of injury.     

Induced tolerance expressed as relaxed behavioural threat response in millimetre-sized aquatic organisms

Natural selection shapes behaviour in all organisms, but this is difficult to study in small, millimetre-sized, organisms. With novel labelling and tracking techniques, based on nanotechnology, we here show how behaviour in zooplankton (Daphnia magna) is affected by size, morphology and previous exposure to detrimental ultraviolet radiation (UVR). All individuals responded with immediate downward swimming to UVR exposure, but when released from the threat they rapidly returned to the surface. Large individuals swam faster and generally travelled longer distances than small individuals. Interestingly, individuals previously exposed to UVR (during several generations) showed a more relaxed response to UVR and travelled shorter total distances than those that were naive to UVR, suggesting induced tolerance to the threat. In addition, animals previously exposed to UVR also had smaller eyes than the naive ones, whereas UVR-protective melanin pigmentation of the animals was similar between populations. Finally, we show that smaller individuals have lower capacity to avoid UVR which could explain patterns in natural systems of lower migration amplitudes in small individuals. The ability to change behavioural patterns in response to a threat, in this case UVR, adds to our understanding of how organisms navigate in the ‘landscape of fear’, and this has important implications for individual fitness and for interaction strengths in biotic interactions.     

Responses of the black sea urchin Tetrapygus niger to its sea-star predators Heliaster helianthus and Meyenaster gelatinosus under field conditions

We ran field experiments to examine the responses of the black sea urchin Tetrapygus niger to predatory sea stars. Trials involving simulated attacks (one or several arms of a sea star being placed on top of half the urchin) showed that the urchin differentiated between the predatory sea stars, Heliaster helianthus and Meyenaster gelatinosus, and a non-predatory sea star, Stichaster striatus, and showed almost no response to a sea star mimic. We further compared the responses of the urchin to different threat levels presented by the two predatory sea stars. The highest threat level was a simulated attack, then mere contact, and subsequently sea stars being placed at different distances from the urchin. All urchins responded to simulated attacks and contact with both sea stars. The proportion responding decreased with distance and more rapidly in trials with H. helianthus (0% at a distance of 30 cm) than with M. gelatinosus (33% at a distance of 50 cm). At each of the threat levels where there was a response to both sea stars, the urchins responded more rapidly to M. gelatinosus than to H. helianthus. In a third experiment where a predatory sea star was added to a circular area (1-m diameter) in which either 4-8 or 11-19 undisturbed urchins were present, the urchins fled the area more rapidly when the added sea star was M. gelatinosus, but the rate of fleeing did not vary with density, as might occur if there was communication among urchins using alarm signals. Our observations suggest that M. gelatinosus presents a stronger predatory threat than H. helianthus. This corresponds to field observations showing that the urchins are more frequently consumed by M. gelatinosus. These are the first field experiments demonstrating distance chemodetection by a marine invertebrate under back-and-forth water flow from wave activity.     

Social genetic and social environment effects on parental and helper care in a cooperatively breeding bird

Phenotypes expressed in a social context are not only a function of the individual, but can also be shaped by the phenotypes of social partners. These social effects may play a major role in the evolution of cooperative breeding if social partners differ in the quality of care they provide and if individual carers adjust their effort in relation to that of other carers. When applying social effects models to wild study systems, it is also important to explore sources of individual plasticity that could masquerade as social effects. We studied offspring provisioning rates of parents and helpers in a wild population of long-tailed tits Aegithalos caudatus using a quantitative genetic framework to identify these social effects and partition them into genetic, permanent environment and current environment components. Controlling for other effects, individuals were consistent in their provisioning effort at a given nest, but adjusted their effort based on who was in their social group, indicating the presence of social effects. However, these social effects differed between years and social contexts, indicating a current environment effect, rather than indicating a genetic or permanent environment effect. While this study reveals the importance of examining environmental and genetic sources of social effects, the framework we present is entirely general, enabling a greater understanding of potentially important social effects within any ecological population.     

Does coping style predict optimization? An experimental test in a wild passerine bird

A number of studies have suggested that avian brood size is individually optimized. Yet, optimal reproductive decisions likely vary owing to among-individual differences in environmental sensitivity. Specifically, ‘proactive’ individuals who do not track environmental changes may be less able to produce optimal brood sizes than ‘reactive’ individuals who have more precise local environmental knowledge. To test this, we quantified exploratory behaviour (a proxy for proactivity) in a great tit (Parus major) population, manipulated brood sizes (reduced, control, enlarged) and evaluated whether individuals of dissimilar coping style differed in their level of optimization. If reactive females behaved optimally, any deviation from their original brood size should lower fitness, whereas this should not be the case for proactive females. Reactive females indeed performed best at their natural brood size, whereas proactive females performed best when raising an enlarged brood. These findings imply that proactive females produced sub-optimal brood sizes. We speculate that proactive females might (i) take decisions based on biased perception of their environment, (ii) face energetic constraints in offspring production and/or (iii) be more willing to invest into current reproduction when given the option. Our findings provide experimental evidence for coping style-related differences in optimal reproductive decisions and life-history strategies.     

Evidence of social niche construction: persistent and repeated social interactions generate stronger personalities in a social spider

While there are now a number of theoretical models predicting how consistent individual differences in behaviour may be generated and maintained, so far, there are few empirical tests. The social niche specialization hypothesis predicts that repeated social interactions among individuals may generate among-individual differences and reinforce within-individual consistency through positive feedback mechanisms. Here, we test this hypothesis using groups of the social spider Stegodyphus mimosarum that differ in their level of familiarity. In support of the social niche specialization hypothesis, individuals in groups of spiders that were more familiar with each other showed greater repeatable among-individual variation in behaviour. Additionally, individuals that were more familiar with each other exhibited lower within-individual variation in behaviour, providing one of the first examples of how the social environment can influence behavioural consistency. Our study demonstrates the potential for the social environment to generate and reinforce consistent individual differences in behaviour and provides a potentially general mechanism to explain this type of behavioural variation in animals with stable social groups.     

Motion-guided attention promotes adaptive communications during social navigation

Animals are capable of enhanced decision making through cooperation, whereby accurate decisions can occur quickly through decentralized consensus. These interactions often depend upon reliable social cues, which can result in highly coordinated activities in uncertain environments. Yet information within a crowd may be lost in translation, generating confusion and enhancing individual risk. As quantitative data detailing animal social interactions accumulate, the mechanisms enabling individuals to rapidly and accurately process competing social cues remain unresolved. Here, we model how motion-guided attention influences the exchange of visual information during social navigation. We also compare the performance of this mechanism to the hypothesis that robust social coordination requires individuals to numerically limit their attention to a set of n-nearest neighbours. While we find that such numerically limited attention does not generate robust social navigation across ecological contexts, several notable qualities arise from selective attention to motion cues. First, individuals can instantly become a local information hub when startled into action, without requiring changes in neighbour attention level. Second, individuals can circumvent speed–accuracy trade-offs by tuning their motion thresholds. In turn, these properties enable groups to collectively dampen or amplify social information. Lastly, the minority required to sway a group''s short-term directional decisions can change substantially with social context. Our findings suggest that motion-guided attention is a fundamental and efficient mechanism underlying collaborative decision making during social navigation.     

‘Selfish herds’ of guppies follow complex movement rules,but not when information is limited

Under the threat of predation, animals can decrease their level of risk by moving towards other individuals to form compact groups. A significant body of theoretical work has proposed multiple movement rules, varying in complexity, which might underlie this process of aggregation. However, if and how animals use these rules to form compact groups is still not well understood, and how environmental factors affect the use of these rules even less so. Here, we evaluate the success of different movement rules, by comparing their predictions with the movement seen when shoals of guppies (Poecilia reticulata) form under the threat of predation. We repeated the experiment in a turbid environment to assess how the use of the movement rules changed when visual information is reduced. During a simulated predator attack, guppies in clear water used complex rules that took multiple neighbours into account, forming compact groups. In turbid water, the difference between all rule predictions and fish movement paths increased, particularly for complex rules, and the resulting shoals were more fragmented than in clear water. We conclude that guppies are able to use complex rules to form dense aggregations, but that environmental factors can limit their ability to do so.     

Living with the enemy: avoidance of hyenas and lions by cheetahs in the Serengeti

Predator avoidance is likely to play a strong role in structuringspecies communities, even where actual mortality due to predationis low. In such systems, mortality may be low because predatoravoidance is effective, and if the threat of predation is liftedthen entire community structures may be altered. Where competitionis intense, then competitor avoidance may have a similar impacton communities. Avoidance behaviors have been documented fora wide range of species, but this is the first attempt to documentavoidance behavior within a large carnivore community. Audioplayback techniques are used to examine the risk perceivedby cheetahs from their two main competitors that are also theirmain predators, lions and hyenas. The results from these experimentsshow that cheetahs actively moved away from lion and hyenaplayback experiments, compared with dummy playbacks where no sound was played. Cheetahs showed no differences in their responsesto playbacks dependent on their sex or reproductive status,suggesting they were responding principally to a competitionrather than a predation threat. However, cheetahs were muchless likely to hunt after competitor playbacks than after dummyplaybacks, and this resulted in a lower kill rate after competitorplaybacks, demonstrating that the perceived presence of competitors had a noticeable impact on the foraging rate of cheetahs. Furthermore,while cheetahs moved just as far following lion playbacks asafter hyena playbacks, they spent significantly more time lookingat the loudspeaker and were less likely to make a kill afterlion playbacks, suggesting that cheetahs perceive lions tobe a greater threat than hyenas.     

Shy birds play it safe: personality in captivity predicts risk responsiveness during reproduction in the wild

Despite a growing body of evidence linking personality to life-history variation and fitness, the behavioural mechanisms underlying these relationships remain poorly understood. One mechanism thought to play a key role is how individuals respond to risk. Relatively reactive and proactive (or shy and bold) personality types are expected to differ in how they manage the inherent trade-off between productivity and survival, with bold individuals being more risk-prone with lower survival probability, and shy individuals adopting a more risk-averse strategy. In the great tit (Parus major), the shy–bold personality axis has been well characterized in captivity and linked to fitness. Here, we tested whether ‘exploration behaviour’, a captive assay of the shy–bold axis, can predict risk responsiveness during reproduction in wild great tits. Relatively slow-exploring (shy) females took longer than fast-exploring (bold) birds to resume incubation after a novel object, representing an unknown threat, was attached to their nest-box, with some shy individuals not returning within the 40 min trial period. Risk responsiveness was consistent within individuals over days. These findings provide rare, field-based experimental evidence that shy individuals prioritize survival over reproductive investment, supporting the hypothesis that personality reflects life-history variation through links with risk responsiveness.