Behavioural trait assortment in a social network: patterns and implications

The social fine structure of a population plays a central role in ecological and evolutionary processes. Whilst many studies have investigated how morphological traits such as size affect social structure of populations, comparatively little is known about the influence of behaviours such as boldness and shyness. Using information on social interactions in a wild population of Trinidadian guppies (Poecilia reticulata), we construct a social network. For each individual in the network, we quantify its behavioural phenotype using two measures of boldness, predator inspection tendency, a repeatable and reliably measured behaviour well studied in the context of co-operation, and shoaling tendency. We observe striking heterogeneity in contact patterns, with strong ties being positively assorted and weak ties negatively assorted by our measured behavioural traits. Moreover, shy fish had more network connections than bold fish and these were on average stronger. In other words, social fine structure is strongly influenced by behavioural trait. We assert that such structure will have implications for the outcome of selection on behavioural traits and we speculate that the observed positive assortment may act as an amplifier of selection contributing to the maintenance of co-operation during predator inspection.     

Effects of relaxed predation pressure on visual predator recognition in the guppy

Many prey species have a genetic predisposition to recognise and respond to predators and can fine-tune their anti-predator behaviour following appropriate experience. Although the Trinidadian guppy ( Poecilia reticulata) has become a model species for the investigation of adaptive behaviour, the extent to which experience mediates predator recognition remains unclear. In this study, we examined the effects of relaxed predation pressure on patterns of anti-predator behaviour in populations differing in evolutionary history. The anti-predator behaviour of wild- and laboratory-born guppies from high- and low-predation localities in Trinidad were compared using three models resembling Crenicichla alta, a dangerous guppy predator, Aequidens pulcher, a less dangerous piscivore, and a snake. Snakes are not known to prey on guppies in Trinidad. Specifically, the following predictions were tested: (1) wild caught fish from the high-predation localities (where guppies co-occur with C. alta and A. pulcher) would respond to the three models according to their perceived level of threat, whereas guppies from the low-predation site would show a reduced response to all of the predator models; (2) high-predation laboratory-reared fish would display a reduced but qualitatively similar response to their wild counterparts; and (3) there would be no behavioural differences between wild- and laboratory-reared low-predation fish. In accordance with these predictions, the results revealed that wild fish originating from high-predation sites responded more strongly to the models than fish from low-predation sites. When reared in the laboratory, guppies from the high-predation population showed a reduced response compared to their wild-caught counterparts, but there was no difference in the behaviour of wild- and laboratory-reared low-predation fish. Model type affected predator inspection behaviour but not schooling tendency, and both wild- and laboratory-reared guppies were more wary of the fish models than the snake. These results suggest that early experience differentially mediates the anti-predator responses of fish from high-risk localities.     

Predation risk reduces male-male sexual competition in the Trinidadian guppy (Poecilia reticulata)

Because agonistic behaviour can increase an individual's risk of predation, natural selection should favour individuals that modify their behaviour in the face of predation hazard in ways that maximise fitness. We investigated experimentally the effects of an increase in the apparent risk of predation on male-male competition within mixed-sex shoals of the Trinidadian guppy (Poecilia reticulata). We show that males engaged in significantly fewer aggressive interactions with conspecific males in the presence of a fish predator. However, they continued to court and attempt copulations with females at the same rate irrespective of the level of predation risk. In comparison, under predation hazard, female guppies were less responsive sexually and avoided fewer male copulation attempts. Such predator-mediated changes in male-male agonistic interactions and female sexual responsiveness towards males have important implications for the mode and intensity of sexual selection within populations.     

Effect of gyrodactylid ectoparasites on host behaviour and social network structure in guppies <Emphasis Type="Italic">Poecilia reticulata</Emphasis>

Understanding how individuals modify their social interactions in response to infectious disease is of central importance for our comprehension of how disease dynamics operate in real-world populations. Whilst a significant amount of theoretical work has modelled disease transmission using network models, we have comparatively little understanding of how infectious disease impacts on the social behaviour of individuals and how these effects scale up to the level of the population. We experimentally manipulated the parasite load of female guppies (Poecilia reticulata) and introduced fish either infected with the ectoparasites Gyrodactylus spp. (experimental) or uninfected (control) into replicated semi-natural populations of eight size-matched female guppies. We quantified the behaviour and social associations of both the introduced fish and the population fish. We found that infected experimental fish spent less time associating with the population fish than the uninfected control fish. Using information on which fish initiated shoal fission (splitting) events, our results demonstrate that the population fish actively avoided infected experimental fish. We also found that the presence of an infected individual resulted in a continued decline in social network clustering up to at least 24 h after the introduction of the infected fish, whereas in the control treatment, the clustering coefficient showed an increase at this time point. These results demonstrate that the presence of a disease has implications for both the social associations of infected individuals and for the social network structure of the population, which we predict will have consequences for infectious disease transmission.     

Predator inspection behaviour in three-spined sticklebacks (<Emphasis Type="Italic">Gasterosteus aculeatus</Emphasis>): body size,local predation pressure and cooperation

The apparently maladaptive tendency of fish to approach and inspect potential predators has been explained in terms of useful information gathering or as a signal to the predator that it has been seen. We examined this behaviour in 16 populations of wild-caught stickleback (Gasterosteus aculeatus) from ponds with and without predatory perch (Perca fluviatilis). Three large and three small individuals per population were each exposed to three model predators differing in realism. A final cooperative treatment entailed pairing subjects with a second individual from the same population, but of the alternative size class, during predator presentation. As might be expected, predator inspection behaviour was much greater in the predator-sympatric populations, and only these fish increased their level of inspection as the models became incrementally more realistic. This suggests that reductions occur in the level of costly inspection behaviour in populations without predators. Subject body size had no effect on inspection effort, which suggests a limited role for experience (we assumed larger fish to be older than smaller fish), at least over the relative age differences utilized. However, small predator-sympatric fish were the only subjects to increase inspection significantly when in a cooperative context, perhaps reflecting the inherent value of a relatively larger partner in this context. These results confirm that levels of predator inspection are both population- and situation-dependent, suggesting a trade-off in the potential costs and benefits of this behaviour.Communicated by C. St. Mary     

Do sticklebacks cooperate repeatedly in reciprocal pairs?

Summary In a shoal of four sticklebacks (Gasterosteus aculeatus) individual fish had partners with whom they repeatedly performed pairwise predator inspection visits. In six different trials, we found two reciprocal pairs per trial significantly more often than would be expected by chance. These results provide further evidence for a TIT FOR TAT like cooperation strategy in sticklebacks. Offprint requests to: M. Milinski     

Feeding under predation hazard: response of the guppy and Hart's rivulus from sites with contrasting predation hazard

Summary Populations of guppies, Poecilia reticulata and Hart's rivulus, Rivulus harti, in Trinidad experience different levels of predation hazard from piscivorous fish. Those from the larger rivers (downstream sites) experience chronically high predation hazard, while those from headwater streams (upstream sites) have few predators. Guppies and Hart's rivulus, collected from downstream and upstream sites, were assayed for their feeding rate in the presence and absence of predators. We defined tenacity as the ratio of the feeding rates in the presence and absence of a predator stimulus. Thus, tenacity expresses the degree to which the forager maintains its feeding rate when a predator stimulus is present. Previous work by Seghers (1973) showed that non-feeding guppies from downstream sites responded more strongly to predators than did guppies from upstream sites. Based on this, we initially hypothesized that fish from downstream sites would show lower tenacities than fish from upstream sites. However, we found the opposite in every case. When confronted with a predator stimulus, guppies and Hart's rivulus from downstream sites fed at consistently greater rates and displayed greater tenacities than did those from upstream sites. These differences were found in experiments using both live and model predators. The results suggest that upstream fish readily trade off feeding for hiding and avoiding predation hazard, a likely response when predators appear infrequently, while downstream fish appear to be selected for boldness and tenacity while foraging under chronically high hazard.     

The bottlenose dolphin community of Doubtful Sound features a large proportion of long-lasting associations

More than 12 studies of different bottlenose dolphin populations, spanning from tropical to cold temperate waters, have shown that the species typically lives in societies in which relationships among individuals are predominantly fluid. In all cases dolphins lived in small groups characterised by fluid and dynamic interactions and some degree of dispersal from the natal group by both sexes. We describe a small, closed population of bottlenose dolphins living at the southern extreme of the species' range. Individuals live in large, mixed-sex groups in which no permanent emigration/immigration has been observed over the past 7 years. All members within the community are relatively closely associated (average half-weight index>0.4). Both male–male and female–female networks of preferred associates are present, as are long-lasting associations across sexes. The community structure is temporally stable, compared to other bottlenose dolphin populations, and constant companionship seems to be prevalent in the temporal association pattern. Such high degrees of stability are unprecedented in studies of bottlenose dolphins and may be related to the ecological constraints of Doubtful Sound. Fjords are low-productivity systems in which survival may easily require a greater level of co-operation, and hence group stability. These conditions are also present in other cetacean populations forming stable groups. We therefore hypothesise that ecological constraints are important factors shaping social interactions within cetacean societies.Communicated by D. Watts     

Predator choice in the field; grouping guppies, Poecilia reticulata, receive more attacks

Capture success of many predator species has been shown to decrease with increasing prey group size and it is therefore suggested that predators should choose to attack stragglers and/or small groups. Predator choice in the laboratory has shown mixed results with some species preferentially attacking large groups and others preferring to attack stragglers over groups. Such predator choices have not been tested in the field. In our study we presented a binary choice between a shoal of guppies and a single guppy to predators in pools in the Arima river, Trinidad. We observed attacks in 11 different pools from a total of 53 predators (20 acara cichlids, Aequidens pulcher, 32 pike cichlids, Crenicichla frenata, and one wolf-fish, Hoplias malabaricus) and found that all predators showed a strong preference for the shoal of guppies in terms of both first choice and total number of attacks. We discuss the implications of these preferences with regards to predator–prey interactions.     

Hunger-dependent predator inspection and foraging behaviours in the threespine stickleback (Gasterosteus aculeatus) under predation risk

Individual fish commonly leave the relative safety of the shoal to approach potential predators at a distance. Not all members of a shoal are equally likely to initiate such predator inspection visits. Here, we show for the first time that the current hunger state of individual fish strongly influences their predator inspection behaviour, as well as their foraging rate, in the face of predation hazard. When all members of threespine stickleback (Gasterosteus aculeatus) test shoals were in a similar hunger state, they were equally likely to inspect a trout predator model alone and did not differ in the frequency of their inspection visits or foraging rate. However, when individual sticklebacks in a shoal differed in their hunger state, the food-deprived (i.e. hungrier) member of the shoal fed at a higher rate, was significantly more likely to initiate solitary predator inspection visits, and inspected the predator model significantly more often than its less hungry (i.e. well-fed) shoal mates. Individual fish which inspected the predator model more frequently also tended to have higher feeding rates. The results indicate that the hungrier fish in a shoal are more willing to take greater risks to inspect a potential threat at a distance, compared with their well-fed shoal mates, and suggest that they may gain a foraging benefit in doing so. If marked asymmetries in hunger state exist among members of fish shoals, then mutual cooperation during predator inspection visits may be difficult to achieve because well-fed individuals are not as likely to initiate or participate in inspection visits as are hungry individuals.Correspondence to: J.-G.J. Godin     

Exposure to variable spatial information in the early rearing environment generates asymmetries in social interactions in cod (Gadus morhua)

Many re-introduction programs used for conservation of populations and species threatened with extinction advocate the use of enriched rearing environments to train animals how to behave appropriately in the wild. Curiously, most of the current fish re-stocking programs have paid little attention to lessons previously learned in bird and mammal re-introductions. Many rehabilitation programs that use releases of hatchery fish observe higher mortality in released fish compared to wild, with most mortality arising shortly after release. One explanation for this mortality is based purely on selection processes; many hatchery fish normally selected out of the population thrive in the predator free, food-rich hatcheries. Alternatively, mortalities may be high because hatchery nursery environments fail to shape fish behaviour appropriately. Here, we empirically address the effect of enrichment in the early rearing environment in coastal cod (Gadus morhua). We find asymmetries in aggressive behaviour when fish reared in plain or enriched environments are allowed to interact. Furthermore, cod reared in standard, impoverished, hatchery environments spend less time in shelter, are more active, and show weaker anti-predator responses than fish reared with access to heterogeneous spatial cues. These results suggest that the constant, plain environments of fish farms may generate behavioural deficits that could reasonably be expected to be associated with lower survival in fish released into the wild.     

Female behaviour mediates male courtship under predation risk in the guppy (Poecilia reticulata)

Previous work has shown that under elevated predation risk, male guppies (Poecilia reticulata) switch from courtship to less conspicuous coercive mating attempts. This behavioural transition is traditionally interpreted as a 'risk-sensitive' response that makes males less conspicuous to predators. However, predation risk leads to behavioural changes (such as schooling and predator inspection) in females that may result in coercive mating attempts being more profitable in high-risk situations. Here, we tested the hypothesis that the switch to coercive mating by male guppies in high-risk situations is mediated by adjustments in female behaviour, rather than directly by the predator. We used replicate models resembling a known guppy predator to simulate predation risk in wild-caught guppies from a high-predation population in Trinidad. Our results revealed that males performed proportionately more coercive mating attempts when presented with a female that had been exposed previously to a model predator compared to when males were paired with non-exposed females. Total mating activity (combined rates of courtship and forced mating attempts) did not differ significantly among the two treatment groups, indicating that overall mating activity is unaffected by predation risk. Importantly, when we subsequently presented both sexes concurrently with a predator model, total mating activity and the proportion of forced mating attempts remained unchanged in the high-risk treatment. Taken together, these results indicate that the transition from courtship to forced mating attempts under elevated predation risk is mediated by changes in female behaviour, which we suggest may favour the use of coercive mating under high predation risk.     

Reproductive Success of Captive-Bred Steelhead Trout in the Wild: Evaluation of Three Hatchery Programs in the Hood River

Abstract:  Population supplementation programs that release captive-bred offspring into the wild to boost the size of endangered populations are now in place for many species. The use of hatcheries for supplementing salmonid populations has become particularly popular. Nevertheless, whether such programs actually increase the size of wild populations remains unclear, and predictions that supplementation fish drag down the fitness of wild fish remain untested. To address these issues, we performed DNA-based parentage analyses on almost complete samples of anadromous steelhead ( Oncorhynchus mykiss ) in the Hood River in Oregon (U.S.A.). Steelhead from a supplementation hatchery (reared in a supplementation hatchery and then allowed to spawn naturally in the wild) had reproductive success indistinguishable from that of wild fish. In contrast, fish from a traditional hatchery (nonlocal origin, multiple generations in hatcheries) breeding in the same river showed significantly lower fitness than wild fish. In addition, crosses between wild fish and supplementation fish were as reproductively successful as those between wild parents. Thus, there was no sign that supplementation fish drag down the fitness of wild fish by breeding with them for a single generation. On the other hand, crosses between hatchery fish of either type (traditional or supplementation) were less fit than expected, suggesting a possible interaction effect. These are the first data to show that a supplementation program with native brood stock can provide a single-generation boost to the size of a natural steelhead population without obvious short-term fitness costs. The long-term effects of population supplementation remain untested.     

Predator recognition and anti-predator responses in the rainbowfish Melanotaenia eachamensis

Predator evasion behaviour patterns of three populations of rainbowfish (Melanotaenia eachamensis) were compared. The populations differed in the level of complexity of their natural habitats and the type and extent of predation. The predator recognition abilities of fish were assessed by exposing them to models differing in their degree of predator realism. The availability of vegetated cover and the location of the models with respect to cover were manipulated. Fish from Lake Tinaroo, a relatively open habitat containing numerous predators, showed strong changes in elective group size (EGS) in response to the different models but did not rely on cover as a place of refuge. In contrast, Dirran Creek fish originate from a small, fast-flowing, structurally complex stream lacking predatory fish species, and they showed little ability to distinguish between the different models and responded to threat by spending longer in vegetated areas. Members of the Lake Eacham captive stock increased their EGS in response to models representing low threat and with more threatening models increased the amount of time spent in vegetated regions of the arena. The contrasting reactions to predatory threat displayed by these populations highlights the need to use a number of different response indices when comparing the anti-predator responses of different fish populations. These data suggest that the level of habitat complexity as well as prior predator experience influence anti-predator responses of different fish popu-lations. Received: 2 October 1996 / Accepted after revision: 27 March 1997     

The influence of experience on risk taking: results from a common-garden experiment on populations of Eurasian perch

Predation is often thought of as an unforgiving and strong selective force, quickly selecting against maladaptive behaviour in the prey. It is argued that experience is likely to have low influence on the phenotypic response to predation, as failing to react correctly to a predator may mean death to the prey and no second chance to learn and correct the behaviour. Individuals from different populations of Eurasian perch are known to differ in risk-taking behaviour. Variation in predation pressure has been suggested as a key factor causing these differences, but little is known about the underlying mechanism by which predation generates risk-taking phenotypes in perch. We compared the degree of boldness between two natural populations of Eurasian perch, living under different predation regimes, and the same populations hatched and reared under identical conditions, free from predation. By this common-garden approach, we sought to investigate patterns in the influence of inheritance and experience on boldness phenotype. The wild fish differed in risk taking, with fish from the low predation-risk population acting bolder than fish from the high-risk environment. In the reared fish, both populations behaved equally bold. Only the fish originating from the high predation population showed different behaviour when comparing wild and reared ecotypes. Our results suggest that experience has an important impact on the response to predators and that geographic variation in risk taking between populations of Eurasian perch to a high degree is shaped by adjustments to the current environment. Habituation had an effect of risk-taking behaviour over the experimental period, but consistent differences between individuals were also found. Furthermore, we also show, by the estimation of variance components, that the behaviour we observe is affected by a range of random effects, such as aquaria and group membership, that in concert shapes the behaviour of an individual perch.     

Female guppies shorten brood retention in response to predator cues

Predation risk influences the duration of offspring development in many species where embryos develop from externally shed eggs. Surprisingly, such predator-mediated effects on offspring development have rarely been explored in live-bearers. In this paper, we use the guppy (Poecilia reticulata), a live-bearing freshwater fish, to test whether the duration of brood retention (the time from mating to parturition) is influenced by experimental changes in the perceived level of predation. Because the swimming performance of female guppies is impaired during late pregnancy, we predicted that females would withhold broods for shorter periods when they are exposed to cues that signal a heightened risk of predation on adults rather than on juveniles. We therefore simulated increased risk of predation on adults by using a combination of pike-shaped models (resembling natural predators that prey on adult guppies) and ‘alarm substances’ derived from the skin extracts of adult conspecific females. Our results revealed that, under simulated predation risk, female guppies produced broods significantly more quickly than their counterparts assigned to a control group where predator cues were absent. A subsequent evaluation of offspring swimming performance revealed a significant positive association between neonate swimming speeds and the duration of brood retention, suggesting that by accelerating parturition, females may produce offspring with impaired locomotor skills. These findings, in conjunction with similar results from other live-bearing species, suggest that the conditions experienced by gestating females can generate significant variation in the timing of offspring development with potentially important implications for offspring fitness.     

Guppies and the TIT FOR TAT strategy: preference based on past interaction

Summary The evolution of cooperation requires either (a) nonrandom interactions, such that cooperators preferentially interact with other cooperators, or (b) conditional behaviors, such that individuals act cooperatively primarily towards other cooperators. Although these conditions can be met without assuming sophisticated animal cognition, they are more likely to be met if animals can remember individuals with whom they have interacted, associate past interactions with these individuals, and base future behavior on this information. Here we show that guppies (Poecilia reticulata), in the context of predator inspection behavior, can identify and remember (for at least 4 h) the more cooperative among two conspecifics and subsequently choose to be near these individuals in future encounters. Offprint requests to: L.A. Dugatkin     

Provenance and threat-sensitive predator avoidance patterns in wild-caught Trinidadian guppies

The antipredator behaviour of prey organisms is shaped by a series of threat-sensitive trade-offs between the benefits associated with successful predator avoidance and a suite of other fitness-related behaviours such as foraging, mating and territorial defence. Recent research has shown that the overall intensity of antipredator response and the pattern of threat-sensitive trade-offs are influenced by current conditions, including variability in predation risk over a period of days to weeks. In this study, we tested the hypothesis that long-term predation pressure will likewise have shaped the nature of the threat-sensitive antipredator behaviour of wild-caught Trinidadian guppies (Poecilia reticulata). Female guppies were collected from two populations that have evolved under high- and low-predation pressure, respectively, in the Aripo River, Northern Mountain Range, Trinidad. Under laboratory conditions, we exposed shoals of three guppies to varying concentrations of conspecific damage-released chemical alarm cues. Lower Aripo (high-predation) guppies exhibited the strongest antipredator response when exposed to the highest alarm cue concentration and a graded decline in response intensity with decreasing concentrations of alarm cue. Upper Aripo (low-predation) guppies, however, exhibited a nongraded (hypersensitive) response pattern. Our results suggest that long-term predation pressure shapes not only the overall intensity of antipredator responses of Trinidadian guppies but also their threat-sensitive behavioural response patterns.     

The social network structure of a wild meerkat population: 1. Inter-group interactions

Groups of individuals frequently interact with each other, but typically analysis of such interactions is restricted to isolated dyads. Social network analysis (SNA) provides a method of analysing polyadic interactions and is used to analyse interactions between individuals. We use a population of 12 groups (ca. 250 animals) of wild meerkats (Suricata suricatta) to test whether SNA can also be used to describe and elucidate patterns of inter-group interactions. Using data collected over 24 months, we constructed two sets of networks, based on direct encounters between groups and instances of roving males visiting other groups. We analysed replicated networks of each type of interaction to investigate similarities between networks of different social interactions as well as testing their stability over time. The two network types were similar to each other when derived from long-term data, but showed significant differences in structure over shorter timescales where they varied according to seasonal and ecological conditions. Networks for both types of inter-group interaction constructed from data collected over 3 months reliably described long-term (12- and 24-month) patterns of interactions between groups, indicating a stable social structure despite variation in group sizes and sex ratios over time. The centrality of each meerkat group in roving interactions networks was unaffected by the sex ratio of its members, indicating that male meerkats preferentially visit geographically close groups rather than those containing most females. Indeed, the strongest predictors of network structure were spatial factors, suggesting that, in contrast to analyses of intra-group interactions, analyses of inter-group interactions using SNA must take spatial factors into account.