Shoal Choice Research Articles

Illu-Shoal Choice: An Exploration of Different Means for Enrichment of Captive Zebrafish.

Fish of any variety are nowadays being kept captive for several purposes, from recreational to alimentary to research. It is possible that we humans often underestimate or misunderstand the basic, natural needs of the species we use for our purposes. Sociality is likely to play an extensive and fundamental role in the quality of life of animals such as zebrafish. This study aimed to develop a dummy conspecific that included depth and motion illusions in order to assess whether these stimuli could represent a valid alternative to a conspecific in triggering shoaling behaviour in a well-known model in genetics and neuroscience, the zebrafish (Dario rerio). We thus replaced the natural livery of a zebrafish shape with three visual illusions: the Ouchi-Spillmann illusion, which generates an effect of local tilting motion; and another two which should create pictorial cues of tridimensionality. Via a binary shoal choice test, we assessed the time spent close to each of the three artificial dummies compared to neutral control stimuli such as grey ellipses. We found no preference for the illusory patterns, suggesting that the illusion was not perceived or, alternatively, that the perception of the illusion was not enough to elicit recognition of the dummy as conspecific and subsequent social behaviours.

What drives mixed-species shoaling among wild zebrafish? Role of predators, food access, abundance of conspecifics and familiarity.

Mixed-species groups occur across a wide range of faunal communities and provide several benefits to members. While zebrafish have often been observed to form mixed-species shoals with coexisting species, the factors determining their occurrence are not yet fully understood. Shoals comprising zebrafish (Danio rerio), flying barbs (Esomus danricus), and whitespots (Aplocheilus panchax) were collected from a stagnant canal at Haringhata (West Bengal, India), and using laboratory-based experiments, we deciphered likely drivers of mixed-species shoaling among zebrafish. Experiments assessing foraging efficiency revealed that the amount of food consumed by zebrafish individuals in mixed shoals was comparable to the amount consumed by these individuals in conspecific shoals. Within mixed-species shoals, zebrafish individuals, despite being smaller than the other species, consumed a comparable amount of food as the other species. Shoal choice experiments revealed that under predator risk, zebrafish associate more with mixed shoals and showed comparable associations to shoals differing in the abundance of conspecifics. Furthermore, zebrafish preferred associating with familiar conspecifics over unfamiliar mixed and unfamiliar conspecific shoals. Therefore, equitable food consumption in mixed shoals, greater association with mixed shoals in the presence of predators, and familiarity were important in driving zebrafish towards mixed-species shoaling.

Context is Key: Social Environment Mediates the Impacts of a Psychoactive Pollutant on Shoaling Behavior in Fish.

Behavior-modifying drugs, such as antidepressants, are increasingly being detected in waterways and aquatic wildlife around the globe. Typically, behavioral effects of these contaminants are assessed using animals tested in social isolation. However, for group-living species, effects seen in isolation may not reflect those occurring in realistic social settings. Furthermore, interactions between chemical pollution and other stressors, such as predation risk, are seldom considered. This is true even though animals in the wild are rarely, if ever, confronted by chemical pollution as a single stressor. Here, in a 2 year multigenerational experiment, we tested for effects of the antidepressant fluoxetine (measured concentrations [±SD]: 42.27 ± 36.14 and 359.06 ± 262.65 ng/L) on shoaling behavior in guppies (Poecilia reticulata) across different social contexts and under varying levels of perceived predation risk. Shoaling propensity and shoal choice (choice of groups with different densities) were assessed in a Y-maze under the presence of a predatory or nonpredatory heterospecific, with guppies tested individually and in male-female pairs. When tested individually, no effect of fluoxetine was seen on shoaling behavior. However, in paired trials, high-fluoxetine-exposed fish exhibited a significantly greater shoaling propensity. Hence, effects of fluoxetine were mediated by social context, highlighting the importance of this fundamental but rarely considered factor when evaluating impacts of environmental pollution.

Influence of lighting environment on social preferences in sticklebacks from twodifferent photic habitats. II. Shoaling and mate preferences of lab-bred fishes.

Different environmental conditions may lead to diverse morphological, behavioral, and physiological adaptations of different populations of the same species. Lighting conditions, for example, vary vastly especially between aquatic habitats, and have been shown to elicit adaptations. The availability of short-wave ultraviolet (UV) light is especially fluctuating, as UV wavelengths are attenuated strongly depending on water properties. The island of North Uist, Scotland, comprises 2 differential habitat types, tea-stained and clear-water lakes, varying considerably in UV transmission. In previous studies, wild-caught 3-spined stickleback Gasterosteus aculeatus populations (3 populations of each habitat type) were tested with respect to their shoaling and mate preferences for fish viewed under UV-present and UV-absent conditions. The results revealed a habitat-dependent preference of UV cues during shoal choice (tea-stained populations: preference for UV-absent condition in tea-stained water; clear-water populations: no preference in clear-water) but an overall preference for UV-present conditions during mate choice. To assess genetic influences on these behavioral patterns, similar experiments were conducted with lab-bred F1-generations of the same stickleback populations that were raised in a common environment (i.e. standardized clear-water conditions). Offspring of sticklebacks from tea-stained lakes tended to prefer shoals viewed under UV-absent conditions (only in tea-stained water), while sticklebacks from clear-water lakes showed a significant preference for the shoal viewed under UV-present conditions in clear-water but not in tea-stained water. Mate-preference experiments demonstrated that females from the tea-stained lakes significantly preferred and females from the clear-water lakes preferred by trend the male viewed under UV-present conditions in the clear-water treatment. The results for both shoaling- and mate-preference tests were largely similar for wild-caught and lab-bred sticklebacks, thus hinting at a genetic basis for the preference patterns.

Odd one in: Oddity within mixed‐species shoals does not affect shoal preference by vagrant tropical damselfish in the presence or absence of a predator

AbstractGrouping behaviour displayed by animals is usually attributed to predation and foraging‐related benefits. The mechanisms of predator protection and foraging efficiency are diverse and often produce conflicting drivers of grouping behaviour. One key conflict is that between group size and phenotypic oddity. Theoretically, individuals should choose the largest available group due to multiple mechanisms associated with “safety in numbers”. However, individuals should also choose the most phenotypically similar group members due to the “predator confusion effect”. This conflict is particularly important within the context of mixed‐species groups because, while their formation may facilitate large group size, phenotypic differences between species may be costly due to oddity. To investigate the interacting effects of shoal size, composition and predator presence on grouping decisions, choice experiments were conducted using displaced tropical damselfish, Abudefduf vaigiensis, settling in temperate south‐eastern Australia (termed vagrants) as a model species. Contrary to predictions, A. vaigiensis displayed no preference for single‐ over mixed‐species shoals, with or without a predator present. These results suggest that shoal composition may not be an important driver of shoal choice in this system. Further, A. vaigiensis showed no preference for larger mixed‐species shoals over smaller single‐species shoals. These outcomes are discussed within the context of climate change‐driven redistribution of A. vaigiensis in temperate south‐eastern Australia.

Juvenile bonefish (Albula vulpes) show a preference to shoal with mojarra (Eucinostomus spp.) in the presence of conspecifics and another gregarious co-occurring species

Grouping behavior occurs across a wide variety of taxa, both within and between species. While members are thought to obtain foraging and antipredator advantages, they can also experience costs in the forms of competition or increased conspicuity to predators. The mechanisms behind these costs and benefits can vary depending on group composition, ultimately influencing the choice of which groups to join. Mixed-species fish shoals are common in shallow nearshore habitats, where research has shown that juvenile bonefish (Albula vulpes) occur among similarly-sized mojarras (Eucinostomus spp.) at a rate far exceeding that predicted given the fishes overlapping habitat use, suggesting that bonefish may actively select to join mojarras. To evaluate this hypothesis experimentally, we assessed the shoaling preferences of bonefish when presented with shoals of conspecifics, mojarras, or another gregarious co-occurring fish (pilchard; Harengula jaguana) in a laboratory setting. Focal juvenile bonefish (n = 25) were given the choice between: (i) conspecifics or mojarra, and (ii) conspecifics or pilchard, tested in shoal sizes of one, two, four, and eight. Bonefish were also given the choice between a mixed shoal (two conspecifics, two mojarra) as an alternative to single species shoals of either: (iii) four conspecifics, or (iv) four mojarra. Juvenile bonefish exhibited a strong association with mojarra, spending significantly more time with them than conspecifics in all but one treatment. Moreover, focal fish showed no detectable preference between conspecifics or pilchard, regardless of shoal size. In mixed shoal treatments, focal fish spent significantly more time wherever there was a higher proportion of mojarra. These findings imply that the co-occurrence of bonefish and mojarra in nature is largely a product of bonefish shoal choice behavior, and likewise that any costs that bonefish might incur by joining mojarras (i.e., oddity effects) are likely outweighed by the putative benefits of doing so, which potentially include access to social information and/or reduced intraspecific competition.

Individual differences in numerical skills are influenced by brain lateralization in guppies (Poecilia reticulata)

A large number of studies showed that fish possess numerical abilities similar to those reported in mammals and birds. However, inter-individual differences in numerical performance are repeatedly found with different types of stimuli and methodological approaches. A recent study on guppies, Poecilia reticulata, suggested that strongly lateralized individuals, assayed for eye preference in a mirror test, were better than poorly lateralized ones when tested for numerical abilities in a natural shoal choice. This study, however, had a potential confound; both the mirror and the shoal choice tests exploit the higher sociality and schooling tendencies in guppies. It is therefore possible that sociality rather than lateralization per se may have been responsible for the observed differences. In the present study, guppies were selected for high or low lateralization using a non-social test, the detour test. Subjects preferentially turning rightward (RD) or leftward (LD) when facing a dummy predator visible behind a barrier proved better than those with no preference (NL) when required to choose the larger of two groups in a shoal choice test. Our study supports the notion that inter-individual differences in the numerical abilities of guppies are related to their degree of cerebral lateralization.

Numerical ability and improvement through interindividual cooperation varied between two cyprinid fish species, qingbo and crucian carp.

We used qingbo (Spinibarbus sinensis) and Chinese crucian carp (Carassius auratus) to test whether numerical discrimination could be improved by the coexistence and possible cooperation of conspecies or heterospecies. We conducted a spontaneous shoal choice test of singletons, conspecific dyads and heterospecific dyads under different numerical comparisons (8 vs. 12, 9 vs. 12 and 10 vs. 12). Singletons of qingbo could discriminate only 8 vs. 12, whereas the dyads of qingbo showed better numerical acuity, as they could discriminate 10 vs. 12. Crucian carp may have poor numerical ability, as both singleton and dyads showed no significant preference for larger stimulus shoals, even at the ‘easier’ numerical discrimination, that is, 8 vs. 12. Furthermore, heterospecific dyads of crucian carp and qingbo did not show significant preference for larger shoals at any numerical comparison in the present study. It is suggested that both the numerical ability and the possibility for improvement by interindividual interaction and hence cooperation might vary among fish species, and the interaction between heterospecies in the present study showed negative effect on numerical ability possibly due to the different behavioural and cognitive traits which make the information transfer and consensus difficult to reach.

Rational choice of social group size in mosquitofish.

Choice of social group can affect the likelihood of survivorship and reproduction for social species. By joining larger social groups-shoals-small freshwater fish like the mosquitofish Gambusia affinis can reduce predation risk and forage more efficiently. We tested shoal choice in mosquitofish to determine whether such choices are economically rational, i.e. consistent and optimal. Although many studies of decision-making assume rational choice, irrational decision-making is common and occurs across contexts. We tested rationality of shoaling decisions by testing the constant ratio rule, which states that the relative preference for two options should not change in the presence of a third option. Female mosquitofish upheld this rule when tested for shoal preference based on group size. Our results contrast with other studies showing violations of the constant ratio rule in foraging and mate choice decision-making contexts. These results suggest that decisions that immediately influence survivorship or decision-making along a single dimension may favour rational decision-making.

Parasitic infection of the eye lens affects shoaling preferences in three-spined stickleback

The ability to compete with conspecifics and to adequately respond to visual stimuli of group mates are important prerequisites for profiting from group benefits such as confusion of predators and greater efficiency in acquiring food. By impairing their host’s physical abilities or making the host conspicuous, even non-contagious parasites that do not pose a direct risk of infection can interfere with group dynamics. Diplostomum pseudospathaceum, a widespread parasite of freshwater fishes, infects the eye lens and can impair the vision of its fish host. To test whether this eyefluke affects competitiveness and/or shoaling behaviour in three-spined stickleback (Gasterosteus aculeatus), experimentally infected fish were kept in mixed groups comprising infected and uninfected sticklebacks under limited food availability in semi-natural outdoor tanks. Change in body mass over time was measured and sticklebacks were given the choice to shoal with uninfected conspecifics or a mixed group in binary shoal choice experiments. Surprisingly, uninfected sticklebacks spent significantly more time with mixed shoals than with uninfected shoals while this preference was not found in infected sticklebacks. Infection did not significantly affect body condition or immune parameters indicative of stress level (relative spleen mass, granulocyte-to-lymphocyte ratio). The results suggest that sticklebacks can distinguish mixed from uninfected groups, but that they are also able to tolerate potential detrimental effects of infection. Whether uninfected fish can benefit from shoaling with infected but non-contagious conspecifics remains to be tested. Although the present data do not indicate a significant effect of infection on competitiveness, this should be examined further.

Laterality enhances numerical skills in the guppy, Poecilia reticulata.

It has been hypothesized that cerebral lateralization can significantly enhance cognition and that this was one of the primary selective forces shaping its wide-spread evolution amongst vertebrate taxa. Here, we tested this hypothesis by examining the link between cerebral lateralization and numerical discrimination. Guppies, Poecilia reticulata, were sorted into left, right and non-lateralized groups using a standard mirror test and their numerical discrimination abilities tested in both natural shoal choice and abstract contexts. Our results show that strongly lateralized guppies have enhanced numerical abilities compared to non-lateralized guppies irrespective of context. These data provide further credence to the notion that cerebral lateralization can enhance cognitive efficiency.

Shoal choice and ultraviolet reflections in stickleback populations from different photic habitats

Grouping is a widespread phenomenon in the animal kingdom and the decision to join a group is a function of individual and environmental conditions, meaning that any advantages and disadvantages have to be pondered constantly. Shoaling decisions in fishes are communicated via a variety of factors, such as colour signals, amongst other ultraviolet (UV) signals. The sensitivity for ultraviolet signals is assumed to be costly and a function of the predominant ecological conditions. The island of North Uist, Scotland, comprises bodies of water that possess great variation in their spectral distribution, especially in the UV spectral range. We examined different populations of three-spined stickleback (Gasterosteus aculeatus L.), which is known to use UV for visual tasks, consisting of three populations from tea-stained lakes and four from clear-water lakes, concerning their preferences to join a shoal viewed under UV-present and UV-absent conditions. Nonreproductively active sticklebacks from tea-stained lakes significantly preferred the shoal under UV-absent conditions, whereas sticklebacks from clear-water lakes did not show a significant preference. Reflection measurements showed that the UV chroma (intensity) of sticklebacks from tea-stained lakes was higher than that of sticklebacks from clear-water, most likely contrasting maximally against the UV-poor background or compensating for a stronger attenuation of the signal.

UV Deprivation Influences Social UV Preference in Juvenile Sticklebacks

Social aggregations occur in many different animal taxa and mainly result from non-random assortment. Investigating factors that shape and maintain the composition of social aggregations are among others a main topic for understanding ecological speciation processes. Aggregation decisions are mediated by olfactory and visual cues, which in many animals are extended into the UV part of the electromagnetic spectrum. Here, we were interested in developmental plasticity of social preferences with respect to UV radiation in aquatic organisms. Specifically, we tested whether different lighting environments with respect to UV wavelengths during early life stages influence the shoaling preference in juvenile threespine sticklebacks (Gasterosteus aculeatus). Family (full-sibling) groups were split and reared under UV-lacking (UV-) and UV-present (UV+) lighting conditions. Subsequent shoal choice experiments, in which test fish from both rearing conditions could simultaneously choose between a shoal seen behind a UV-blocking (UV-) and a shoal seen behind a UV-transmitting (UV+) filter, revealed a significant effect of lighting condition during rearing on association preference. Test fish that had been deprived of UV spent significantly more time near the UVshoal compared to the test fish reared under full-spectrum lighting conditions. The results are discussed with respect to plasticity of the visual system and environmental lighting conditions.

Familiarity affects social network structure and discovery of prey patch locations in foraging stickleback shoals.

Numerous factors affect the fine-scale social structure of animal groups, but it is unclear how important such factors are in determining how individuals encounter resources. Familiarity affects shoal choice and structure in many social fishes. Here, we show that familiarity between shoal members of sticklebacks (Gasterosteus aculeatus) affects both fine-scale social organization and the discovery of resources. Social network analysis revealed that sticklebacks remained closer to familiar than to unfamiliar individuals within the same shoal. Network-based diffusion analysis revealed that there was a strong untransmitted social effect on patch discovery, with individuals tending to discover a task sooner if a familiar individual from their group had previously done so than if an unfamiliar fish had done so. However, in contrast to the effect of familiarity, the frequency with which individuals had previously associated with one another had no effect upon the likelihood of prey patch discovery. This may have been due to the influence of fish on one another's movements; the effect of familiarity on discovery of an empty ‘control’ patch was as strong as for discovery of an actual prey patch. Our results demonstrate that factors affecting fine-scale social interactions can also influence how individuals encounter and exploit resources.

Diet-mediated social networks in shoaling fish

Very little is known about interaction patterns within animal groups, such as flocks of birds, swarms of insects, or shoals of fish, or the mechanisms which mediate interactions between group members. Fish, such as three-spined sticklebacks (Gasterosteus aculeatus), are known to use a variety of visual and olfactory cues to inform shoal choice and to maintain shoal cohesion. However, whether these cues may also mediate interactions within a shoal is not known. This study aimed to investigate individual level interactions between shoaling sticklebacks under different diet treatments. Fish fed on either bloodworm- or Daphnia-based diets were used to generate replicated social networks (n = 65), in which the constituent fish differed in diet treatment. The results showed that the structure of stickleback networks is nonrandom and mediated by an association preference for fish from the same diet treatment, most likely through diet-derived chemical cues. The findings of this study provide insights into the causes of intragroup interactions in shoaling fish and highlight the importance of chemical cues in stickleback communication

Impact of benzyl butyl phthalate on shoaling behavior in Fundulus heteroclitus (mummichog) populations

Fundulus heteroclitus preference for association with familiar conspecifics of similar body length was impacted by benzyl butyl phthalate (BBP); this was found to be a statically significant result with a p < 0.0001. When presented with equally sized shoals consisting of either large or small fish, the majority of unexposed (84%) and acetone exposed control (82%) fish selected the shoal of large fish. A small number of control fish chose either the shoal of small fish (6% and 10%) or the neutral zone (10% and 8%) where they were clear morphological outliers. Fish exposed to 0.1 mg/L BBP exposure daily for four weeks selected the shoal of small fish more often than unexposed or acetone controls (7.5- and 4.5-fold respectively). They also remained in the neutral zone and displayed agitation at levels more than twice that of control. Agitation and shoal choice disruption are quantifiable behavioral responses that support the use of F. heteroclitus as a model for detecting sub-lethal BBP exposure.

Personality counts: the effect of boldness on shoal choice in three-spined sticklebacks

The grouping behaviour of fish is a widespread phenomenon of high biological significance but little is known as to how consistent individual behavioural differences may affect group joining preferences. When given the option to join either a shy or a bold shoal of three-spined sticklebacks, Gasterosteus aculeatus, both shy and bold individuals showed a strong preference for associating with bold fish. Personality type interacted with individual hunger levels to affect the extent of association, suggesting important strategy variation by focal fish in a competitive foraging environment. Furthermore, shoals modified their behaviour in relation to the focal individual. Individual behavioural differences were shown to have a complex role in influencing association preferences as well as driving previously unrecognized behavioural modifications in foraging groups.

Shoal choice in juvenile angelfish (Pterophyllum scalare): effects of social status and activity

Previous experiments have shown that angelfish are capable of discriminating between shoals composed of conspecifics of different social status and that familiarity mediates the decision. In the present work, the shoaling behaviour of dominant and subordinate angelfish, Pterophyllum scalare, was again examined and the role that potential behavioural differences between the stimulus shoals may play in the shoaling decisions was investigated. In binary shoal choice tests, the stimulus shoals were composed of dominant and subordinate conspecifics from the same dominance hierarchy as the test fish but, in contrast with most studies of this type, the stimulus shoals were placed in tanks that allowed for the full expression of behavioural patterns. Test fish, regardless of social status, showed an association preference for a shoal of dominant over a shoal of subordinate conspecifics. The tendency was significant in the second observation period, which took place about 2 hr and 30 min after the first one, when the swimming activity of the stimulus shoals of dominants was significantly greater than that of subordinates and the shoaling preference for dominants was significantly related to activity differences between the shoals. The results contrast with those previously found in this species when test fish preferred to aggregate with shoals of familiar subordinate conspecifics placed in small display compartments and indicate that angelfish take shoal activity into account when making a shoaling decision. Thus, depending on the situation, shoal activity may take priority over other attributes of the shoals. The preferential association is considered in the context of the potential benefits to the fish when joining a group of active fish in our experimental situation.

UV matters in shoaling decisions

Shoaling behaviour in fish is influenced by numerous factors, such as familiarity, kinship, group size and shoal composition. Grouping decisions are based on both olfactory and visual cues. The visual system of many vertebrates is extended into the ultraviolet (UV) wave range as in three-spined sticklebacks (Gasterosteus aculeatus, L.). We investigated whether the presence or absence of UV wavelengths has an influence on shoaling behaviour in this species. Reproductively non-active three-spined sticklebacks were given the choice between two shoals, equal in numbers of individuals, which could be seen either through a UV-transmitting [UV(+)] or a UV-blocking [UV(-)] filter. Test fish preferred to join the shoal seen under UV(+) conditions. Due to differences in quantal flux between the UV(+) and UV(-) filters used, control experiments with neutral-density optical filters were performed in order to clarify the role of luminance. Here, test fish spent significantly more time near shoals that were seen in a darker environment, suggesting a potential trade-off between UV radiation and lower brightness during shoal choice. To our knowledge, these results demonstrate for the first time that shoaling decisions are influenced by UV wavelengths.

Shoaling behaviour of sticklebacks infected with the microsporidian parasite, Glugea anomala

We compared the shoaling behaviour of three-spined sticklebacks, Gasterosteus aculeatus, infected with the microsporidian, Glugea anomala, to that of non-infected conspecifics. Infected fish lost significantly more weight than non-infected fish during a period of food deprivation, suggesting a metabolic cost to parasitism. In binary shoal choice tests, non-infected test fish showed an association preference for a shoal of non-infected over a shoal of infected conspecifics; infected test fish displayed no preference. Infected fish, however, showed a higher overall tendency to shoal than non-parasitised fish. Furthermore, infected fish occupied front positions within a mixed school. We consider the behavioural differences between infected and uninfected fish in the context of their potential benefits to the fish hosts and the parasites.