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.     

The genetic and environmental basis of adaptive differences in shoaling behaviour among populations of Trinidadian guppies,Poecilia reticulata

The degree of plasticity an individual expresses when moving into a new environment is likely to influence the probability of colonization and potential for subsequent evolution. Yet few empirical examples exist where the ancestral and derived conditions suggest a role for plasticity in adaptive genetic divergence of populations. Here we explore the genetic and plastic components of shoaling behaviour in two pairs of populations of Poecilia reticulata (Trinidadian guppies). We contrast shoaling behaviour of guppies derived from high‐ and low‐predation populations from two separate drainages by measuring the shoaling response of second generation laboratory‐reared individuals in the presence and absence of predator induced alarm pheromones. We find persistent differences in mean shoaling cohesion that suggest a genetic basis; when measured under the same conditions high‐predation guppies form more cohesive shoals than low‐predation guppies. Both high and low‐predation guppies also exhibit plasticity in the response to alarm pheromones, by forming tighter, more cohesive shoals. These patterns suggest a conserved capacity for adaptive behavioural plasticity when moving between variable predation communities that are consistent with models of genetic accommodation.     

Influence of black spot disease on shoaling behaviour in female western mosquitofish, <Emphasis Type="Italic">Gambusia affinis</Emphasis> (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.     

Ontogeny of the diel activity patterns in relation to downstream dispersal in riverine cyprinid fishes

It has been shown that the tendency of fish to shoal decreases as night falls. Much is known about shoaling in the daytime, however, little is known about the social behaviour of fish at night. Although the nocturnal disintegration of shoal structure is the conventional expectation for most diurnal marine fish, it has not yet been investigated for diurnal freshwater fish. This possibility has been investigated using guppies ( Poecilia reticulata ), collected from the wild, as an experimental model.
Three preference tanks were used, one of which permitted only visual cues, another only olfactory cues and the other both visual and olfactory cues. Shoaling tendency was observed at four different light intensities (8 wt/m, 0·05 wt/m, 0·025 wt/m, 0·003 wt/m). These light intensities were chosen to mimic daylight, dawn/dusk, clear night and cloudy night conditions, respectively. Trials were carried out on randomly selected male guppies. Results indicated that with both modalities present fish significantly preferred the stimulus shoal at all light intensities. However with only one modality to indicate the presence of the shoal, fish showed no significant shoaling tendency at any of the diminished light intensities. A test of shoal cohesion at the four different light intensities was carried out on freely interacting fish. This test condition was chosen to mimic the situation of guppies in the wild. The results to date suggest that guppies continue to shoal during dusk (at low light intensities) but not during the night. These findings make an important contribution to our understanding of the social behaviour of fish at night and deserve further investigation.     

Effect of light intensity on the shoaling behaviour of the guppy (Poecilia reticulata)

It has been shown that the tendency of fish to shoal decreases as night falls. Much is known about shoaling in the daytime, however, little is known about the social behaviour of fish at night. Although the nocturnal disintegration of shoal structure is the conventional expectation for most diurnal marine fish, it has not yet been investigated for diurnal freshwater fish. This possibility has been investigated using guppies (Poecilia reticulata), collected from the wild, as an experimental model. Three preference tanks were used, one of which permitted only visual cues, another only olfactory cues and the other both visual and olfactory cues. Shoaling tendency was observed at four different light intensities (8 wt/m, 0·05 wt/m, 0·025 wt/m, 0·003 wt/m). These light intensities were chosen to mimic daylight, dawn/dusk, clear night and cloudy night conditions, respectively. Trials were carried out on randomly selected male guppies. Results indicated that with both modalities present fish significantly preferred the stimulus shoal at all light intensities. However with only one modality to indicate the presence of the shoal, fish showed no significant shoaling tendency at any of the diminished light intensities. A test of shoal cohesion at the four different light intensities was carried out on freely interacting fish. This test condition was chosen to mimic the situation of guppies in the wild. The results to date suggest that guppies continue to shoal during dusk (at low light intensities) but not during the night. These findings make an important contribution to our understanding of the social behaviour of fish at night and deserve further investigation.     

Tracking the startle response of guppies Poecilia reticulata in three dimensions

A three‐dimensional analysis of startle behaviours of guppies Poecilia reticulata, in dyads or alone, from two populations that show distinct differences in shoaling behaviour was performed. During the first few seconds after a startling stimulus, changes in behaviour, which could be critical if an individual is to survive a predatory attack, and the interactions between pairs of P. reticulata were examined. The enhanced social interactions immediately after the stimulus, as a proxy for shoaling behaviour, and their dissipation were quantified. Social (individuals tested in dyads) v. asocial (tested alone) responses to the startling stimulus were also compared. The three‐dimensional reconstruction, from a two‐camera, high‐frame‐rate tracking system allowed for the tracking of the individuals' speed and speed recovery and, for P. reticulata in dyads, interindividual distance and orientation. For the dyads from the high‐predation population, the closer the individuals were to each other, the more likely they were to be parallel, but no correlation was found for the low‐predation P. reticulata. The startle response of P. reticulata comprised the following sequence: freezing, darting and skittering and recovery to pre‐stimulus swimming behaviour. Upon repeated encounters with the stimulus, a reduced shoaling and startle response was observed, although the rate of reduction was faster in P. reticulata from the high‐predation population than those from the low‐predation population. The results are discussed in light of what is known about the anti‐predator behaviour of this species.     

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.     

LOCAL ADAPTATION AND THE EVOLUTION OF PHENOTYPIC PLASTICITY IN TRINIDADIAN GUPPIES (POECILIA RETICULATA)

Divergent selection pressures across environments can result in phenotypic differentiation that is due to local adaptation, phenotypic plasticity, or both. Trinidadian guppies exhibit local adaptation to the presence or absence of predators, but the degree to which predator‐induced plasticity contributes to population differentiation is less clear. We conducted common garden experiments on guppies obtained from two drainages containing populations adapted to high‐ and low‐predation environments. We reared full‐siblings from all populations in treatments simulating the presumed ancestral (predator cues present) and derived (predator cues absent) conditions and measured water column use, head morphology, and size at maturity. When reared in presence of predator cues, all populations had phenotypes that were typical of a high‐predation ecotype. However, when reared in the absence of predator cues, guppies from high‐ and low‐predation regimes differed in head morphology and size at maturity; the qualitative nature of these differences corresponded to those that characterize adaptive phenotypes in high‐ versus low‐predation environments. Thus, divergence in plasticity is due to phenotypic differences between high‐ and low‐predation populations when reared in the absence of predator cues. These results suggest that plasticity might initially play an important role during colonization of novel environments, and then evolve as a by‐product of adaptation to the derived environment.     

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.      

Picking personalities apart: estimating the influence of predation,sex and body size on boldness in the guppy Poecilia reticulata

Predation is a strong selective force in most natural systems, potentially fueling evolutionary changes in prey morphology, life history and behaviour. Recent work has suggested that contrasting predation pressures may lead to population differentiation in personality traits. However, there are indications that these personality traits also differ between sexes and not necessarily in a consistent way between populations. We used an integrative approach to quantify boldness (latency to emerge from a shelter) in wild‐caught guppies in relation to predation pressure, population origin, sex and size. In addition we quantified the repeatability of these personality traits. We show that predation regime had significant effects on emergence time. In general, fish from high predation localities emerged sooner from the shelter compared to those from low predation localities. We found strong sex differences; males were significantly bolder than females. The relationship between emergence time and body size was non‐significant in all populations. We discuss what responses to expect from predator‐naïve versus predator‐experienced individuals and how this can be linked to the shyness–boldness continuum.     

Isolation and the development of shoaling in two populations of the guppy

Socially reared guppies Poecilia reticulata derived from two wild populations (Upper and Lower Aripo River, Trinidad) showed a significant relationship between body size and shoaling tendency, measured as the proportion of time spent in proximity to a bottle containing conspecifics. Larger females shoaled significantly more than smaller females. Fish from the high-shoaling population (Lower Aripo) showed significantly less shoaling behaviour when reared in isolation. In contrast, low-shoaling fish (Upper Aripo) demonstrated no significant change in their shoaling behaviour in response to social isolation.     

Parallel and nonparallel behavioural evolution in response to parasitism and predation in Trinidadian guppies

Natural enemies such as predators and parasites are known to shape intraspecific variability of behaviour and personality in natural populations, yet several key questions remain: (i) What is the relative importance of predation vs. parasitism in shaping intraspecific variation of behaviour across generations? (ii) What are the contributions of genetic and plastic effects to this behavioural divergence? (iii) And to what extent are responses to predation and parasitism repeatable across independent evolutionary lineages? We addressed these questions using Trinidadian guppies (Poecilia reticulata) (i) varying in their exposure to dangerous fish predators and Gyrodactylus ectoparasites for (ii) both wild‐caught F0 and laboratory‐reared F2 individuals and coming from (iii) multiple independent evolutionary lineages (i.e. independent drainages). Several key findings emerged. First, a population's history of predation and parasitism influenced behavioural profiles, but to different extent depending on the behaviour considered (activity, shoaling or boldness). Second, we had evidence for some genetic effects of predation regime on behaviour, with differences in activity of F2 laboratory‐reared individuals, but not for parasitism, which had only plastic effects on the boldness of wild‐caught F0 individuals. Third, the two lineages showed a mixture of parallel and nonparallel responses to predation/parasitism, with parallel responses being stronger for predation than for parasitism and for activity and boldness than for shoaling. These findings suggest that different sets of behaviours provide different pay‐offs in alternative predation/parasitism environments and that parasitism has more transient effects in shaping intraspecific variation of behaviour than does predation.     

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.     

Timing and plasticity of shoaling behaviour in the zebrafish, Danio rerio

The zebrafish has become a major model system for biomedical research and is an emerging model for the study of behaviour. While adult zebrafish express a visually mediated shoaling preference, the onset of shoaling behaviour and of this preference is unknown. To assess the onset of these behaviours, we first manipulated the early social environment of larval zebrafish subjects, giving them three model shoaling partners of the same pigment phenotype. We then assayed the subjects' preferences using binary preference tests in which we presented subjects with two shoals, one shoal of fish exhibiting the same pigment pattern phenotype as their models and another shoal with a radically different pigment pattern. To determine whether or not the visually mediated preference could be altered once it was established, we further manipulated the social environment of a number of subjects, rearing them with one model shoal and testing them, then changing their social consorts and retesting them. Our results demonstrate that larval zebrafish shoal early in their development, but do not exhibit a shoaling preference until they are juveniles. Moreover, we find that the shoaling preference is stable, as changing the social environment of fish after they had acquired a preference did not change their preference. These data will facilitate investigations into the mechanisms underlying social behaviour in this vertebrate model system.     

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.     

Shoaling Decisions in Angelfish: The Roles of Social Status and Familiarity

Abstract Past research has shown that angelfish, Pterophyllum scalare , are capable of discriminating between shoals composed of familiar dominant and subordinate companions, whereas they show no preference for shoals of unfamiliar conspecifics. In this study, the relative importance of familiarity and social status (shoal factors) on the shoaling decision of juvenile angelfish, which also differed in social status (individual factor), was investigated as very little is known about such tradeoffs in fishes. Dominant and subordinate individuals were given the choice to shoal with a group of conspecifics composed of familiar dominants vs. unfamiliar dominants and composed of familiar subordinates vs. unfamiliar subordinates. The findings demonstrate that fish with different social status differed in their shoaling preference. Subordinate test fish showed a preferential association with familiar subordinates over unfamiliar subordinates, but preferred the unfamiliar shoal over the familiar one when both shoals were constituted by dominant individuals. The shoaling behaviour shown by dominant test fish, on the other hand, indicated no significant preference for any of the shoals regardless of their composition. A replicate preference test carried out 2 h 30 min after the first one indicated that the association pattern was relatively consistent. Results suggest that angelfish are able to differentiate between the stimulus shoals and demonstrate that the pervasive influence of familiarity on the shoaling decision may be restrained or overridden by the composition of the familiar shoals and the social status of the test fish.     

Recent social environment affects colour-assortative shoaling in juvenile angelfish (Pterophyllum scalare)

Theory predicts that fish should show colour-assortative shoaling in order to avoid the oddity effect whereby individuals that differ in some feature from the group majority appear to incur increased risk of predation. It has also been shown that early experience plays an important role in affecting social preferences in some fish species. In this study, the importance of colour phenotype in promoting assortative shoaling and the role played by the recent social environment on its expression were investigated in juvenile angelfish, Pterophyllum scalare. Individuals of the uniformly black and golden colour morphs were housed in a group with conspecifics of like and unlike body colour to themselves, as well as in mixed-colour groups for 4 weeks. Subsequently, they were subjected to a binary choice to shoal with a group of conspecifics composed of unfamiliar fish of either a like or unlike colour phenotype to themselves. The response of the individuals to the colour attributes of the shoals was related to their recent social environment. Fish in like- and mixed-colour previous treatments showed a preferential association with like colour conspecifics. In contrast, the shoaling behaviour exhibited by fish previously maintained with a group of unlike-coloured conspecifics (cross-housed treatment) indicated no significant preference for any of the shoals. The results suggest that angelfish use body colouration as an intraspecific shoaling cue and that learning, in the form of recent familiarisation with a specific colour phenotype of conspecifics, can affect colour-assortative shoaling preferences in this species. This learning component of the choice need not be restricted to early developmental stages.     

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.     

LIFE-HISTORY EVOLUTION IN GUPPIES (POECILIA RETICULATA) 6. DIFFERENTIAL MORTALITY AS A MECHANISM FOR NATURAL SELECTION

We have previously reported a correlation between the life-history patterns of guppies and the types of predators with which they coexist. Guppies from localities with an abundance of large predators (high predation localities) mature at an earlier age and devote more resources to reproduction than those found in localities with only a single, small species of predator (low predation localities). We also found that when guppies were introduced from a high to low predation locality, the guppy life history evolved to resemble what was normally found in this low predation locality. The presumed mechanism of natural selection is differences among localities in age/size-specific mortality (the age/size-specific mortality hypothesis); in high predation localities we assumed that guppies experienced high adult mortality rates while in the low predation localities we assumed that guppies experienced high juvenile mortality rates. These assumptions were based on stomach content analyses of wild-caught predators and on laboratory experiments. Here, we evaluate these assumptions by directly estimating the mortality rates of guppies in natural populations. We found that guppies from high predation localities experience significantly higher mortality rates than their counterparts from low predation localities, but that these higher mortality rates are uniformly distributed across all size classes, rather than being concentrated in the larger size classes. This result appears to contradict the predictions of the age/size-specific predation hypothesis. However, we argue, using additional data on growth rates and the probabilities of survival to maturity in each type of locality, that the age-specific mortality hypothesis remains plausible. This is because the probability of survival to first reproduction is very similar in each type of locality, but the guppies from high predation localities have a much lower probability of survival per unit time after maturity. We also argue for the plausibility of two other mechanisms of natural selection. These results thus reveal mortality patterns that provide a potential cause of natural selection, but expand, rather than narrow, the number of possible mechanisms responsible for life-history evolution in guppies.     

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.