Size‐Assortative Shoaling in the Guppy (Poecilia reticulata): The Role of Active Choice

Many fish species exhibit size‐assortative shoaling, which is often thought to be driven by predation risk. Recent fieldwork has revealed that guppies (Poecilia reticulata) are more size assorted in high‐predation populations than in low‐predation ones. However, size assortment does nonetheless occur in some low‐predation populations, suggesting that predation is unlikely the sole driving force behind size‐assortment. Here, we investigated in the laboratory the potential role of active choice in size‐assortative shoaling in wild‐caught female guppies originating from two populations of the same river system in Trinidad. Small or large focal females from each population were offered a binary choice of shoaling with either four small female conspecifics or four large ones. Observed shoaling preferences depended on the body size of the focal fish, suggesting phenotype‐mediated conflict over group composition. Large focal fish preferred to shoal with the size‐matched stimulus shoal of large fish. In contrast, small focal fish did not shoal assortatively but also preferred to shoal with larger females. Our results suggest that size‐assortative shoaling in female guppies is likely to be due to factors other than active choice, such as habitat segregation and sexual harassment.     

Shoaling behaviour of sticklebacks infected with the microsporidian parasite, <Emphasis Type="Italic">Glugea anomala</Emphasis>

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.     

Shoal Choice in the Banded Killifish (Fundulus diaphanus,Teleostei, Cyprinodontidae): Effects of Predation Risk,Fish Size,Species Composition and Size of Shoals

Banded killifish (Fundulus diaphanus) were presented individually with a choice of shoaling with either of two stimulus shoals which differed in shoal size, species composition, and fish body size, before and after a simulated avian predator attack. When threatened, test fish preferred to shoal with the larger of two conspecific shoals, but only if members of both stimulus shoals were of the same size class as the test fish. Otherwise, they preferred to shoal with similarly sized fish irrespective of shoal size; threat of predation increased the magnitude of this preference. Furthermore, test fish preferred a shoal of similarly sized shiners (Notemigonus crysoleucas) over larger killifish, when shoal sizes were identical. This indicates that body size plays a key role in shoal choice, overriding the effects of shoal size and species preference. Notwithstanding the above, shoal choice was affected by predator threat only when differences between shoal size or body size of stimulus fish were large.     

Interpopulation Differences in Shoaling Behaviour in Guppies (Poecilia reticulata): Roles of Social Environment and Population Origin

In Trinidad, guppies (Poecilia reticulata) in high‐predation localities show more cohesive shoaling behaviour than those living with less dangerous predators in low‐predation sites. We evaluated the relative contributions of population origin (i.e. genetic and/or maternal effects) and social environment on the expression of shoaling by assessing the behaviour of juveniles reared in a range of social conditions. Focal individuals, offspring of guppies from populations from high‐ or low‐predation localities, were reared in a multifactorial experiment; we created four different social conditions by manipulating the source and demography of the conspecific residents with whom focal individuals interacted. We found that high‐predation fish displayed a stronger propensity to shoal than low‐predation ones. Our results also suggest a role for interactions between the source of the focal individuals, the demography of the group in which they were reared and the origin of the guppies with whom they were reared. Depending on their origin (high‐ vs. low‐ predation) and rearing density, our focal fish were more likely to shoal if they were reared with high‐predation residents. Learning from high‐predation residents, aggressive interactions with low‐predation residents and/or phenotype matching could have played a role in driving this effect of social environment. This effect of the phenotype of conspecifics on shoaling development would enhance heritable differences in shoaling propensity such that both could contribute to the well‐documented difference in shoaling behaviour of high‐ and low‐predation guppies in natural populations.     

Investigating the Effect of Familiarity on Kin Recognition of Three‐Spined Stickleback (Gasterosteus aculeatus)

The ability to discriminate between related and unrelated individuals has been demonstrated in many species. The mechanisms behind this ability might be manifold and depend on the ecological context in which the species lives. In brood‐caring species, both familiarity and phenotype matching are known to be used in kin recognition. However, results of studies disentangling these two phenomena have proved contradictory. We aimed to broaden our knowledge about the mechanisms of kin recognition using shoaling preferences of three‐spined stickleback (Gasterosteus aculeatus) as a model behavior. In our first experiment, focal fish had the choice to shoal either with kin or unfamiliar non‐kin. In half of the trials, kin groups were composed of familiar individuals, while they were unfamiliar in the other half. Focal fish significantly preferred kin as shoaling partner, a result which was not reinforced by familiarity. In our second experiment, focal fish were given the choice between a shoal of familiar kin and a shoal of unfamiliar kin. Here, focal fish did not show any significant preference. These results indicate that familiarity does not impact stickleback's ability to recognize kin. Furthermore, they show that familiarity does not overrule recognition based on phenotype matching or innate recognition, underlining the importance of these mechanisms. Finally, our results lead to the assumption that individual recognition might play a minor role also in non‐kin‐based preferences for familiars.     

Sexual Harassment Influences Group Choice in Female Mosquitofish

Male sexual harassment has been demonstrated to result in high costs for females. Male mosquitofish are amongst the most ardent in the animal kingdom and sexual harassment can halve female foraging efficiency. Female mosquitofish have been found to vary their shoaling behaviour when harassed by a male, approaching other males to promote male–male interactions or reducing the distance to another female to dilute male disturbance. The present study tested two predictions about female counterstrategies. As the dilution effect increases with group size, a harassed female was expected to prefer joining a larger group. She should also benefit from joining larger females since males are known to prefer larger mates. When given a choice between a group of two and a group of four females, females harassed by a male spent significantly more time near the larger group. Harassed females also preferred a shoal consisting of larger females over one consisting of smaller females, but no such preferences were observed in the absence of a male. In addition to influencing the individual decision whether to shoal or not, the presence of a harassing male appears to affect group choice. In these fish, sexual harassment might be a powerful factor in shaping both the structure and the composition of shoals.     

Gravidity‐Associated Shoaling Decisions in Three‐Spined Sticklebacks (Gasterosteus aculeatus)

Group living has evolved in many animal species as an antipredator behavior, an evolutionary effect that might be augmented by grouping with similarly looking individuals. Consequently, groups are often composed according to species, size, or coloration. During egg ripening or embryo growth, the outer appearance of females often changes drastically within days, which makes them more prone to predation. Thus, a female's group preference should change according to her reproductive state, an issue that has seldom been investigated. To test this, we gave gravid and non‐gravid three‐spined sticklebacks (Gasterosteus aculeatus) the choice to shoal either with a gravid or a non‐gravid conspecific. The results showed that shoaling preferences of gravid and non‐gravid individuals differed significantly. Non‐gravid females preferred gravid fish as shoaling partners, which might rely on the fact that gravid sticklebacks show reduced escape performance, which in turn might increase a non‐gravid female's chance of survival. However, in contrast to our predictions, gravid fish did not show any significant preference. A reason for this pattern might be competition between gravid females for mating partners, which might overrule benefits of shoaling with similar looking individuals. Hence, gravidity influences social preferences in a shoaling fish, which might pose a largely overlooked form of the cost of reproduction.     

Combined effects of predators and parasites on shoaling behavior of fishes

A review of experimental, field and theoretical papers on several topics related to the study of variability of fish shoaling behavior caused by separate impacts of predators and parasites as well as by combined effects of these factors. First, antipredator functions and changes in fish shoal parameters caused by predation risk are briefly discussed. Then, effects of parasites that have the potential to act as a force that can select for either larger or smaller group size, or even for solitary behavior are reviewed. Predation- and parasitism-induced variations in the shoal size and shape, distance between members of a shoal, position of fish within a shoal, effects of habitat complexity, parasite-assortative shoaling are described. Finally, an interplay between the parasitism and predation risks that could influence protective functions of fish shoaling is discussed. It is emphasized that not only the binary “predator-prey” and “host-parasite” systems, but a three-component system “parasite.-host-predator” which embrace both direct and indirect effects have to be studied.     

Shoaling behaviour in a surface-dwelling and a cave-dwelling population of a barb <Emphasis Type="Italic">Garra barreimiae</Emphasis> (Cyprinidae,Teleostei)

We studied shoaling behaviour in a species of fish (Garra barreimiae) from Oman. We compared two populations (a surface-dwelling and a cave-dwelling population) with different theoretical costs and benefits of shoaling. We measured the tendency to associate with a shoal of conspecifics. The stimulus shoal was confined to (1) clear Plexiglas cylinders in light, (2) wire-mesh cylinders in light, or (3) wire-mesh cylinders in darkness. The surface form exhibited a strong preference for the stimulus shoal during the experiments in light, but also in darkness, when only non-visual cues from the shoal could be perceived. The cave form did not show a preference when solely visual cues were available (Plexiglas cylinder). When non-visual cues from the shoal could be perceived (wire-mesh), the cave form did show a preference to associate with the shoal, but the shoaling tendency was considerably weaker than in the surface form. The shoaling tendency has probably been genetically reduced in the cave form.     

Balancing the dilution and oddity effects: decisions depend on body size

Background

Grouping behaviour, common across the animal kingdom, is known to reduce an individual''s risk of predation; particularly through dilution of individual risk and predator confusion (predator inability to single out an individual for attack). Theory predicts greater risk of predation to individuals more conspicuous to predators by difference in appearance from the group (the ‘oddity’ effect). Thus, animals should choose group mates close in appearance to themselves (eg. similar size), whilst also choosing a large group.

Methodology and Principal Findings

We used the Trinidadian guppy (Poecilia reticulata), a well known model species of group-living freshwater fish, in a series of binary choice trials investigating the outcome of conflict between preferences for large and phenotypically matched groups along a predation risk gradient. We found body-size dependent differences in the resultant social decisions. Large fish preferred shoaling with size-matched individuals, while small fish demonstrated no preference. There was a trend towards reduced preferences for the matched shoal under increased predation risk. Small fish were more active than large fish, moving between shoals more frequently. Activity levels increased as predation risk decreased. We found no effect of unmatched shoal size on preferences or activity.

Conclusions and Significance

Our results suggest that predation risk and individual body size act together to influence shoaling decisions. Oddity was more important for large than small fish, reducing in importance at higher predation risks. Dilution was potentially of limited importance at these shoal sizes. Activity levels may relate to how much sampling of each shoal was needed by the test fish during decision making. Predation pressure may select for better decision makers to survive to larger size, or that older, larger fish have learned to make shoaling decisions more efficiently, and this, combined with their size relative to shoal-mates, and attractiveness as prey items influences shoaling decisions.     

Response of shoaling fish to the threat of aerial predation

Synopsis Many species of shoaling fish are preyed upon by aerial predators. However, to date there has been no analysis of the evasive response of a group of shoaling fish to an aerial threat or attack. The response of a shoal of fish encompasses a suite of behaviors starting with a startle response. Shoals of golden shiner, Notemigonus crysoleucas, responded to the threat of aerial predation from a kingfisher model with a startle response, an increase in shoal depth, an increase in polarity, swimming in the opposite direction under the model predator, shoal compression along the depth axis, and shoal expansion on the plane perpendicular to the depth axis. It was hypothesized that shoal compression along the depth axis serves to increase predator confusion by placing more fish in the predator's visual field. This compression was termed the ‘plane of confusion’.     

The Effect of Hunger on Shoal Choice in Golden Shiners (Pisces: Cyprinidae,Notemigonus crysoleucas)

When an animal has a choice of joining one group over another, its decision may depend on its relative vulnerabilities to predation and starvation. For example, a well-fed animal may choose a large group of individuals with body size matching its own because this gives good protection against predators, but a hungry animal may prefer smaller groups made up of smaller individuals because this decreases food competition. To test this idea, a choice between various shoals was given to golden shiners, Notemigonus crysoleucas, that were either well fed or deprived of food for 48 h. In a choice of 10 vs. 3 shoalmates, both well-fed and hungry shiners spent more time near the shoal of 10. In a choice of 20 vs. 3 shoalmates, both well-fed and hungry shiners again preferred the larger shoal, but in one replicate this preference was significantly weaker in the hungry fish. This reduced preference did not appear to be an artefact of increased mobility by hungry fish searching for food. In a choice between shoals of small vs. large conspecifics, small well-fed shiners, small hungry shiners, and large well-fed shiners preferred shoalmates with body size matching their own, but large hungry shiners preferred smaller individuals. These results are consistent with the hypothesis that hungry fish sacrifice safety from predation in their shoaling behaviour (by avoiding larger groups to a certain extent and by risking the oddity effect) so as to decrease food competition.     

Juvenile convict cichlids shoaling decisions in relation to shoal size and age

Many animals form groups and socialize in response to evolutionary pressures such as predation, food availability, and mate acquisition. Evidence of social choice based on various phenotypic characters (Group Phenotypic Composition [GPC]) has been observed in several animal species. In addition to the physical characteristics of the social group, it is also interesting to consider how decisions of who to socialize with might be expected to change for an individual over time. Younger individuals with limited life experience may discriminate differently between social groups than older conspecifics who have had the opportunity to learn and who may be faced with different ecological or environmental pressures. Here, we used a traditional two‐choice design to explore the shoaling behavior of juvenile convict cichlids and determine whether the number of fish and/or the size/life stage of the individuals within a shoal influenced social choices. We found that juvenile convict cichlids spent more time shoaling with similarly sized juvenile individuals and also preferred to shoal with larger shoals, but not when shoals were comprised of adult fish. The size of the individuals in a shoal was a more influential factor than the size of the shoal itself. Size of individual juveniles was correlated with tendency to visit shoals, but was not correlated with overall time spent shoaling, regardless of shoal composition. As juveniles, convict cichlids can make discriminatory choices that are influenced by specific aspects of shoal composition.     

The effect of hunger, shoal size and the presence of a predator on shoal cohesiveness in bluntnose minnows, Pimephales notatus Rafinesque

Shoals of fish vary in their degree of cohesiveness as certain conditions such as hunger, predation risk and shoal size vary: this study relates this variation to the benefits of shoaling. Shoals of bluntnose minnows, Pimephales notatus Rafinesque, consisting of different numbers of individuals were starved for 5, 24 or 72 h and allowed to forage in the presence or absence of a predator. Cohesiveness was measured as the dispersion offish within the shoal (the radius of the longest axis of the shoal corrected for the number of fish in the shoal), straggle frequency (the number of movements by individuals of at least 5 body lengths away from the shoal) and aggressive interactions between shoal members. Cohesiveness increased as shoal size and the benefits per individual increased. Cohesiveness also increased in the presence of a predator, as did the importance of shoaling as a means of reducing predation risk. Cohesivenes decreased as hunger level increased, possibly as a result of increased competition for food among shoal members.     

Parallel evolution leads to reduced shoaling behavior in two cave dwelling populations of Atlantic mollies (<Emphasis Type="Italic">Poecilia mexicana</Emphasis>, Poeciliidae,Teleostei)

Shoaling behavior protects fishes from avian and piscine predation, but at the same time costs of group living arise due to several mechanisms including increased food competition. Most cave fishes live in an environment in which avian and piscine predators are lacking, and cave environments are often characterized by low food availability, leading to increased food competition. Altogether, this should favor the reduction of shoaling in cave fishes. We compared shoaling behavior (i.e. the tendency to associate with a stimulus shoal) among surface dwelling populations of the Atlantic molly, Poecilia mexicana, and two cave forms of that species. The first cave population of P. mexicana originated from the Cueva del Azufre and was previously recognized as the only cave form of a poeciliid fish. The second cave population examined came from a cave that was discovered only recently (Cueva Luna Azufre). In both cave forms shoaling behavior was reduced compared with surface dwelling mollies.     

A test for conspecific cueing in two sympatric species of pupfish (<Emphasis Type="Italic">Cyprinodon beltrani</Emphasis>, <Emphasis Type="Italic">C. simus</Emphasis>)

In many fishes, individuals prefer to associate with phenotypically similar or conspecific individuals (conspecific cueing). Such phenotypic segregation can be an important evolutionary driver, for example, in intralacustric sympatric speciation processes. I examined conspecific cueing in two species of sympatric pupfish from Laguna Chichancanab in southern Mexico: the little shoaling and highly territorial Cyprinodon beltrani and the highly shoaling but non-territorial C. simus. Females were tested for shoal species preferences in two testing scenarios: (1) a sequential choice test where shoals of four conspecific or four heterospecific (Cyprinodon sp. or Poecilia reticulata) females were presented in succession, and (2) a simultaneous choice test where female shoals of both Cyprindon species were presented concurrently. Overall, higher shoaling in C. simus was corroborated in this study. In the sequential test, no effect of the type of stimulus shoal (con- or heterospecific) on shoaling behavior was detected. In the simultaneous tests, C. beltrani, but not C. simus females showed a preference for the conspecific shoal. It seems possible that C. simus females did not evolve species recognition mechanisms because no other Cyprinodon species in the Laguna Chichancanab shows equally high shoaling, which automatically leads to the formation of single-species (i.e., C. simus-) shoals. C. simus males do not establish long-term territories, but rather spawn within shoals, whereas C. beltrani females approach males in their breeding territories to spawn. I discuss that this behavioral difference still provides a powerful reproductive isolation mechanism even in the absence of conspecific cueing in C. simus.     

Influence of Parasitism on Shoal Choice in the Banded Killifish (Fundulus diaphanus,Teleostei, Cyprinodontidae)

Banded killifish, Fundulus diaphanus, were presented individually with a choice of ‘shoaling’ with either of two conspecific stimulus shoals, one consisting of fish with externally visible black spots (indicating the presence of a parasitic trematode worm, Crassiphiala bulboglossa), the other consisting of fish without such spots. Both parasitized and unparasitized test fish significantly preferred to shoal with unparasitized stimulus shoals over parasitized ones. The relative preference of unparasitized killifish for unparasitized shoals increased with increasing degree of parasite load in parasitized stimulus fish. However, no significant preference by unparasitized fish for unparasitized shoals was observed if unparasitized shoals were presented versus mixed shoals consisting of parasitized and unparasitized fish. We conclude that killifish preferred unparasitized shoals over parasitized shoals only if all fish in the respective stimulus shoals were phenotypically uniform (either with or without black spots). A final experiment showed that killifish used black spots as an indicator of parasite presence to make their shoal choice. The significance of these results for the formation of parasite-assorted shoals is discussed.     

Effects of nutritional state on the shoaling tendency of banded killifish, Fundulus diaphanus, in the field

Although group living can confer benefits to individuals in terms of reduced predation risk and enhanced foraging success, it may also be associated with costs, such as increased competition for food. The nutritional state of an individual could therefore affect its readiness to join or remain in groups. We investigated the shoaling behaviour of banded killifish by following marked individuals, whose nutritional state had been experimentally manipulated, and recording their shoaling behaviour in a field enclosure containing unmarked conspecifics. Overall, food-deprived fish spent more time alone, and therefore less time shoaling, than well-fed individuals. When shoaling, however, food-deprived fish were not found in smaller shoals than well-fed conspecifics. Furthermore, they did not show a greater latency to shoal initially. Having joined a shoal, however, food-deprived fish left shoals more frequently to be alone than fed fish. Rates of change in the membership size of shoals occupied by either well-fed or food-deprived fish did not differ. We conclude that nutritional state seems to affect an individual's decision to continue shoaling once an association has been made. This study is the first to investigate experimentally state-dependent changes in the size of social groups in fish under field conditions. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Shoaling in juvenile guppies: the effects of body size and shoal size

While factors affecting shoal mate choice have been examined extensively in adult guppies (Poecilia reticulata), few studies have focused on the shoaling behavior of juveniles. In this study, juvenile guppies were tested for their ability to shoal as well as their response to shoal mates of different body size and to shoals with different numbers of individuals. In dichotomous choice tests, 10-day-old guppies (mean body length=8.83 mm), 30-day-old guppies (13.17 mm) and 50-day-old guppies (18.6mm) were given the opportunity to swim near shoals of five fish or an empty chamber. In most cases, the juvenile fish demonstrated shoaling behavior, swimming near a group of fish rather than an empty chamber, regardless of the age of the stimulus shoal. When presented with two shoals, one of similar age and body size and one of dissimilar age and body size, only the 50-day-old guppies showed a significant preference for the age-matched shoal. Similarly, when choosing between a large shoal and a small shoal, only the 50-day-old guppies spent significantly more time near the larger shoal. Thus, while juveniles at each age shoaled, only 50-day-old fish demonstrated the shoal mate discrimination seen in adult fish.     

Cave molly females (<Emphasis Type="Italic">Poecilia mexicana</Emphasis>) avoid parasitised males

Cave mollies (Poecilia mexicana) inhabit a dark Mexican cave, where visual communication is impossible. I observed the preference of cave molly females to associate with a non-infected male or a male infected with a pathogenic bacterium (Mycobacterium sp.) which causes the formation of large blisters around the eyes of infected fish. Females preferred to stay near the non-infected male only when the two stimulus males were separated from the female by transparent Plexiglas in light, but not when the males were separated by a wire-mesh in light (where vision was to some extent hindered, but the females perceived non-visual cues) or in darkness (where only non-visual cues were available). I conclude that the visually mediated preference for non-infected males has been maintained during the colonisation of the lightless habitat, but a preference for this trait on the basis of non-visual cues did not evolve. The cave habitat may be poor in pathogens, resulting in low selection pressure to evolve a non-visual preference for males without bacterial infection.Communicated by R.F. Oliveira