Shoal Mates Research Articles

Risk-taking and locomotion in foraging threespine sticklebacks (Gasterosteus aculeatus): the effect of nutritional stress is dependent on social context

The relationship between individual physiological traits and social behaviour is an important research area because it can examine how mechanisms of behaviour link to functional outcomes. It is hypothesised that correlative and causative links between physiology and individual behaviour may be altered by social interactions. Here, we assess how nutritional stress (20-h starved, 90-h starved) and routine metabolic rate (RMR) determine the movement and foraging behaviour of threespine sticklebacks (Gasterosteus aculeatus), both individually and in a social context. Results showed that there was no statistically significant relationship between RMR and behaviour. The nutritional stress treatment had significant opposite effects on voluntary swim speed, dependent on whether fish were assayed asocially (alone) or socially (in shoals of three). Greater nutritional stress caused voluntary swimming speeds to reduce in an asocial context but increase in a social context, although both relationships were not significant. Additional results exploring social behaviour parameters such as the frequency and duration of shoaling interactions suggests that alterations in fish swim speed between the two nutritional stress treatments may be due to competition effects. This study links state-dependent individual behaviour to social foraging performance and reinforces the theory that social context is an important modulator of the relationships between physiology and behaviour. Recent research has highlighted that the social environment may shape how physiology and behaviour are linked. This area of research, however, requires data from empirical studies that measure and experimentally manipulate physiological traits of individually identifiable animals and tests them under asocial and social conditions. Using threespine sticklebacks foraging for bloodworms, we show that routine metabolic rate did not have a statistically significant effect on fish locomotion or risk-taking. Greater nutritional deprivation caused fish to decrease their swimming speed when they were alone (likely in an effort to reduce energy expenditure); however, when assayed in groups, competitive forces between shoal mates caused them to swim at faster voluntary speeds. Nutritional stress therefore had a significant socially dependent effect on fish locomotion.

Lack of social preference between unfamiliar and familiar juvenile Port Jackson sharks Heterodontus portusjacksoni.

This study investigated whether captive-reared juvenile Port Jackson sharks Heterodontus portusjacksoni choose to aggregate and if familiarity is one of the mechanisms driving social preference. In a controlled binary-choice experiment, juvenile sharks were given the option to associate or not with unfamiliar conspecifics, or to associate or not with familiar conspecifics. In neither group did juvenile H. portusjacksoni actively choose to associate with conspecifics, but familiarity decreased the proportion of time spent near a conspecific only during the initial phase of the experiment. Treatment (1 or 3 shoal mates), sex and size had no effect on aggregation behaviour. These findings suggest that familiarity is not a driver of social preferences in juvenile H. portusjacksoni, contrary to results in another shark species. Additionally, adult H. portusjacksoni form large aggregations during the breeding season and actively associate with familiar sex and size-matched individuals, thus our results suggest the species undergoes an ontogenetic shift in social behaviour.

Biological Motion as an Innate Perceptual Mechanism Driving Social Affiliation

Collective behavior, such as shoaling in teleost fish, is driven by the perceptual recognition of conspecific animals. Because social interactions are mutual, it has been difficult to disentangle the exact sensory cues that trigger affiliation in the first place from those that are emitted by receptive and responsive shoal mates. Here, we overcome this challenge in a virtual reality assay in zebrafish. We discovered that simple visual features of conspecific biological motion provide a potent shoaling cue. Individual juvenile fish shoal for hours with circular black dots projected onto a screen, provided these virtual objects mimic the characteristic kinetics of zebrafish swim bouts. Other naturalistic cues previously implicated in shoaling, such as fish-like shape, pigmentation pattern, or non-visual sensory modalities are not required. During growth, the animals' stimulus preferences shift gradually, matching self-like kinetics, and this tuning exists even in fish raised in isolation.Virtual group interactions and our multi-agent model implementation of this perceptual mechanism demonstrate that kinetic cues can drive assortative shoaling, a phenomenon commonly observed in field studies. Coordinated behavior can emerge from autonomous interactions, such as collective odor avoidance in Drosophila, or from reciprocal interactions, such as the codified turn-taking in wren duet singing. We found that individual zebrafish shoal autonomously without evidence for a reciprocal choreography. Our results reveal individual-level, innate perceptual rules of engagement in mutual affiliation and provide experimental access to the neural mechanisms of social recognition. VIDEO ABSTRACT.

Shoal sex composition and predation risk influence sub-adult threespine stickleback shoaling decisions

Group living reduces individual predation risk most effectively when group members are behaviorally and phenotypically similar. Group preferences are influenced by the individual, the members of the shoal, and the environmental conditions. While shoaling behavior has been studied extensively in the threespine stickleback (Gasterosteus aculeatus), it is unclear whether the sex of shoal mates influences the shoal preference of non-reproductive males and females and how this changes under increasing predation risk. Although non-reproductively active sticklebacks are sexually monochromatic in appearance, sex-related differences may result in sexual segregation when shoaling. Here we show that male and female sub-adult threespine sticklebacks had contrasting preferences for shoal mate sex, and that this preference was dependent on the level of predation risk during standardized experimental choice tests. In detail, test fish shoal with the opposite sex within low predation risk trials and with same-sex shoals within high predation risk trials. This difference might be linked to activity patterns; test males were more active than females. Our results demonstrate that differences between the sexes in a species with a sexually monochromatic non-reproductive stage can result in sex-related shoaling preferences. Most studies examining sexual segregation focus on sexually dimorphic species, but these results highlight the potentially widespread occurrence of sexual segregation beyond the sexually dimorphic reproductive stage.

Tributyltin affects shoaling and anxiety behavior in female rare minnow (Gobiocypris rarus)

Effects of tributyltin (TBT) on reproduction are well established in many fish species. However, few studies report the effects of TBT on non-reproductive behaviors, which is a novel aspect of endocrine disruption in fish. Thus, the present study used rare minnow (Gobiocypris rarus) to investigate the effects of TBT, at environmental concentrations of 1, 10 and 100ng/L, on shoaling and anxiety behaviors. The results showed that fish exposed to TBT had less group cohesion during the course of the 10-min observation period as compared with the control fish. Further, TBT altered the shoaling in the Novel tank test, where shoaling is determined as the tendency to leave a shoal of littermates trapped behind a Plexiglas barrier at one end of the test tank. Fish exposed to TBT had shorter latency before leaving shoal mates and spent more time away from shoal than control fish. In addition, we also used Novel tanks to study the anxiety behavior as the tendency to stay at the bottom when introduced into an unfamiliar environment. The fish exposed to TBT showed increased anxiety, manifested as increased latency to enter the upper half and decreased time in upper half when compared with the control fish. TBT exposure increased the levels of dopamine and its metabolite 3,4-dihydroxyphenylacetic acid, and decreased the levels of 5-hydroxytryptamine and its metabolite 5-hydroxy indole acetic acid in the brain. Thus, the hypofunction of the dopaminergic system or of the serotoninergic system or the combination of the two may underlie the observed behavioral change, which might affect the fitness of fish in their natural environment.

Combined effects of flow condition and parasitism on shoaling behaviour of female guppies Poecilia reticulata.

Group living in fish can provide benefits of protection from predators and some parasites, more efficient foraging for food, increased mating opportunities and enhanced energetic benefit when swimming. For riverine species, shoaling behaviour can be influenced by various environmental stressors, yet little is known how flow rate might influence the shoaling of diseased fish shoals. In view of the increasingly unpredictable flow rates in streams and rivers, this study aimed to assess the combined effect of flow condition and parasitism on the shoaling behaviour of a model fish species. Shoal size, shoal cohesion and time spent shoaling of female guppies Poecilia reticulata were compared when infected with the directly transmitted ectoparasite Gyrodactylus turnbulli under flow and static conditions. Flow condition was an important factor in influencing shoaling behaviour of guppies with the fish forming larger shoals in the absence of flow. When a shoal member was infected with G. turnbulli, shoal cohesion was reduced, but the magnitude of this effect was dependent on flow condition. In both flow and static conditions, bigger fish formed larger shoals than smaller counterparts. Future changes to stream hydrology with more frequent flooding and drought events will affect the shoaling tendency of fish. During high-flow events, diseased fish may not be able to keep up with shoal mates and therefore have a higher risk of predation. Additionally, these findings may be important for aquaria and farmed species where an increase in flow rate may reduce aggregation in fish.

Individual-level consistency of different laterality measures in the goldbelly topminnow.

In humans, hemispheric language dominance is, to some degree, associated with handedness. Significant associations have been reported between several other lateralized functions. Much less is known about the organization of cerebral asymmetries in nonhuman species and, in particular, whether the presence of reversed asymmetry of one function is associated with a reversal of other lateralized functions or, instead, if cognitive functions lateralize independently. In this study, we compare four measures of sensory and motor laterality in the same individuals in a sample of goldbelly topminnows. A significant association was found between two measures of eye preference and two measures of motor laterality, but sensory and motor asymmetries were uncorrelated. We found interesting that individuals preferring to examine a predator with the right eye tended to use the left eye to look at a shoal mate and the reverse was true for fish that monitored predators with the left eye. This complementarity of functions could be adaptively advantageous for a small social fish, because it allows an individual to monitor the movements of its shoal mates with one eye as the other eye remains free to scan the surroundings for the presence of predators.

Behavioural syndromes and shoaling: connections between aggression, boldness and social behaviour in three different Danios

While many behavioural syndrome studies focus on individual-level correlations of behaviors across various contexts, it is also possible to examine these syndromes on a population level, comparing various species or groups. In this study we tested wild type zebrafish (Danio rerio), longfin zebrafish (Danio rerio lof mutants) and the closely related pearl danio (Danio albolineatus) to determine whether aggression and boldness varied and whether population-level differences in these behavioural types were linked to differences in shoaling preferences among the three Danio types. We found significant differences in overall levels of boldness and aggression between the three Danio groups. Pearl danios were the most ‘aggressive’ type, and wildtype zebrafish were relatively ‘passive’. In contrast, wildtype zebrafish showed the most ‘boldness’ while longfin zebrafish were comparatively ‘shy’. We also found subsequent differences in social behaviour, with pearl danios showing significant preferences for conspecific shoals. Our results indicate that fish may not only be making social decisions based on the behaviour, health and appearance of potential shoal mates, but their own temperament may be important in mediating social interactions as well.

17α-Ethinyl estradiol affects anxiety and shoaling behavior in adult male zebra fish ( Danio rerio)

Ethinyl estradiol is a potent endocrine disrupting compound in fish and ubiquitously present in the aquatic environment. In this study, we exposed adult zebra fish ( Danio rerio) males to 0, 5 or 25 ng Ethinyl estradiol/L for 14 days and analyzed the effects on non-reproductive behavior. Effects of treatment of the exposed males was shown by vitellogenin induction, while brain aromatase (CYP 19B) activity was not significantly altered. Both concentrations of Ethinyl estradiol significantly altered the behavior in the Novel tank test, where anxiety is determined as the tendency to stay at the bottom when introduced into an unfamiliar environment. The effects were, however, opposite for the two concentrations. Fish that were exposed to 5 ng/L had longer latency before upswim, fewer transitions to the upper half and shorter total time spent in the upper half compared with control fish, while 25 ng Ethinyl estradiol treatment resulted in shorter latency and more and longer visits to the upper half. The swimming activity of 25, but not 5 ng-exposed fish were slightly but significantly reduced, and these fish tended to spend a lot of time at the surface. We also studied the shoaling behavior as the tendency to leave a shoal of littermates trapped behind a Plexiglas barrier at one end of the test tank. The fish treated with Ethinyl estradiol had significantly longer latency before leaving shoal mates and left the shoal fewer times. Further, the fish exposed to 5 ng/L also spent significantly less time away from shoal than control fish. Fertilization frequency was higher in males exposed to 5 ng/L Ethinyl estradiol when compared with control males, while no spawning was observed after treatment with 25 ng/L. The testes from both treatment groups contained a normal distribution of spermatogenesis stages, and no abnormality in testis morphology could be observed. In conclusion, we have observed effects on two behaviors not related to reproduction in zebra fish males after treatment with Ethinyl estradiol, adding to the ecological consequences of contamination of aquatic environments with estrogenic substances.

Fish in a ring: spatio-temporal pattern formation in one-dimensional animal groups

In this work, we study the collective behaviour of fish shoals in annular domains. Shoal mates are modelled as self-propelled particles moving on a discrete lattice. Collective decision-making is determined by information exchange among neighbours. Neighbourhoods are specified using the perceptual limit and numerosity of fish. Fish self-propulsion and obedience to group decisions are described through random variables. Spatio-temporal schooling patterns are measured using coarse observables adapted from the literature on coupled oscillator networks and features of the time-varying network describing the fish-to-fish information exchange. Experiments on zebrafish schooling in an annular tank are used to validate the model. Effects of group size and obedience parameter on coarse observables and network features are explored to understand the implications of perceptual numerosity and spatial density on fish schooling. The proposed model is also compared with a more traditional metric model, in which the numerosity constraint is released and fish interactions depend only on physical configurations. Comparison shows that the topological regime on which the proposed model is constructed allows for interpreting characteristic behaviours observed in the experimental study that are not captured by the metric model.

Correlation between boldness and body mass in natural populations of the poeciliid Brachyrhaphis episcopi

The boldness of individual Brachyrhaphis episcopi, collected from regions of high and low predation, was investigated using two independent assays: (1) the time to emerge from cover and (2) the propensity to leave shoal mates and investigate a novel object. A strong correlation between the two assays was revealed such that fish that emerged from shelter sooner were also more likely to approach a novel object. This is indicative of a boldness personality axis acting across both behavioural contexts. Fish from high‐predation areas were bolder than those from low‐predation areas and males were bolder than females. A significant correlation between body mass, standard length (LS) and boldness score was also found. In general, bold fish had a greater body mass at a given LS than shy fish. These results suggest that personality traits are strongly influenced by population‐specific ecological variables and may have fitness consequences in wild populations.

Influence of black spot disease on shoaling behaviour in female western mosquitofish, Gambusia affinis (Poeciliidae, Teleostei)

Parasites can fundamentally alter the cost–benefit ratio of living in a group, e.g. if infected individuals increase the predation risk of shoal mates. Here, the effect of an infection with a trematode, Uvulifer sp. (Diplostomatidae) on the shoaling behaviour of female western mosquitofish, Gambusia affinis, was investigated. The parasite examined causes a direct phenotypical change of the host by forming black spots on its body surface. When given a choice between a stimulus shoal and no shoal, we found shoaling tendencies to be significantly reduced in infected focal fish. In another experiment, we tested for association preferences relative to the infection status of the stimulus fish. Given the choice between an infected and a healthy stimulus fish, both infected and healthy focal fish preferred to associate with non-infected stimulus fish. Our results suggest that (1) the cost–benefit ratio of shoaling might be different for infected and non-infected individuals. Infected fish may be more affected by competition for food within a shoal. (2) Associating with infected conspecifics appears to be costly for female mosquitofish, maybe due to increased predation risk.

Shoal Choice in Swordtails when Preferences Conflict

AbstractIndividuals obtain a range of benefits from aggregating with others. Evidence suggests that group size and the phenotypic characteristics of potential group mates are both important attributes influencing the grouping decisions of prospective group members. Their interaction, however, remains poorly understood. Here we investigate, in a series of dichotomous choice experiments, what happens when a preference with respect to group size is pitted against a preference for assorting on the basis of body size in swordtail fish. When controlled for body size, we found that swordtails preferred to associate with a larger shoal. When controlled for group size, we found that swordtails preferred to associate with similar‐sized fish. However, when offered the choice between a single size‐matched shoaling partner and four dissimilar‐sized shoal mates, we found that females associated randomly. Our results suggest that, depending on context, group size and body size may be equally important in guiding the aggregating decisions of swordtails. Future studies will likely offer valuable insights into shoaling behaviour by considering how, and under what circumstances, different grouping preferences might be prioritized.

Cross-species familiarity in shoaling fishes.

Preferential association with familiar shoal mates confers a number of potentially important benefits to individuals, including improved anti-predator effects and the reduction of aggression in competitive interactions. Until now, however, familiarity has been demonstrated purely between conspecifics. Here, we present evidence that familiarity preferences can override natural preferences for conspecifics. Individual focal fishes (chub, Leuciscus cephalus) were given a choice of two stimulus shoals of the same size composed of conspecifics or of heterospecifics (minnows, Phoxinus phoxinus) in a flow tank. A series of four treatments was carried out to investigate the effects of familiarity, induced by a 15 day association between the focal fish and the stimulus fishes, on the choices made by the focal fish. Focal fishes showed a significant preference for conspecifics over heterospecifics when both stimulus shoals were composed of non-familiar individuals. Focal fishes also showed a significant preference for stimulus shoals composed of familiar fishes over stimulus shoals composed of non-familiar fishes when both shoals were conspecific and when both shoals were heterospecific. Finally, the preference of focal fishes for conspecifics disappeared when the alternative, a shoal of heterospecifics, was composed of familiar individuals. The importance of this work is discussed in the context of species interactions in free-ranging shoals.

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.

Kin recognition and choice of shoal mates by threespine sticklebacks

In this study we addressed five questions concerning kin recognition and shoaling in threespine stickleback Gasterosteus aculeatus fry. Our results were: (1) fry distinguished between similar-aged sibs and non-sibs when tested at 18, 30 and 45 days of age, (2) fry reared with maternal half-sibs distinguished sibs from half-sibs; fry reared with paternal half-sibs did not discriminate between paternal half-sibs and either sibs or non-sibs, (3) the ability to discriminate sibs from non-sibs did not require experience, but the strength of the shoaling preference was modified by events early in life, (4) fry spent more time near kin when a predator was present and (5) fry did not distinguish between non-sib conspecifics and heterospecifics.