The influence of hunger,shoal size and predator presence on foraging in bluntnose minnows

This study examines the compromise between predator avoidance and foraging in bluntnose minnows, Pimephales notatus, in shoals of different sizes and at three levels of hunger: 5, 24 or 72 h of deprivation. Trials were carried out in the laboratory with a predator present or absent. Foraging was affected significantly by shoal size, predator presence and hunger. Foraging latency decreased as shoal size and hunger level increased, but latency increased in the presence of a predator. Foraging rate was less when there was a predator present. In the absence of a predator, foraging rate increased as hunger level increased. At the 5 h hunger level, foraging rate increased as shoal size increased, in the absence but not the presence of a predator. At this low level of hunger, innows in all shoal sizes fed at a low rate when the risk of predation was greater. At higher levels of hunger, fish in all shoal sizes fed at a high rate when no predator was present, so that foraging rate did not change across shoal size. When the predator was present at the higher hunger levels, only fish in larger, safer shoals fed at a rate greater than at the lowest hunger level.     

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.     

The effects of predator presence and shoal size on foraging in bluntnose minnows,Pimephales notatus

Synopsis Shoals of 3, 5, 7, 10, 15, and 20 bluntnose minnows,Pimephales notatus, were allowed to forage in the absence and presence of a fish predator, which was separated from the shoal by a clear plexiglass partition. A typical dilution effect was observed in that individual fish in larger shoals were approached less frequently by the predator. In the absence of a predator, foraging latency decreased significantly and the rate of foraging increased with increasing shoal size. Foraging latency for each shoal size tended to increase in the presence of a predator and foraging rate decreased, significantly for shoals of 7, 15, and 20 fish. Members of larger shoals were safer and enjoyed a greater level of food consumption, perhaps due to decreased individual vigilance for predators and social facilitation. However, foraging effort decreased when a predator was present, as more time was allocated to predator avoidance.     

Is there always an influence of shoal size on predator hunting success?

Theoretical and empirical studies predict that there should be a decrease in hunting success of predators with increasing prey group size. Most of these studies investigated situations in which predator and prey were in full view of each other before, during and after an attack. In this study, single rock bass Ambloplites rupestris were given an opportunity to launch surprise attacks at shoals of creek chub Semotilus atromaculatus that ranged in size from two to 13 fish. There was no significant influence of either shoal size or attack distance on predator success rate and no significant relationship between attack distance and shoal size. Furthermore, it was found that the leading fish of a shoal was attacked significantly more often than fish in other shoal positions, indicating that predation risk was not shared equally among shoal members. Also, leading fish in larger shoals (eight to 13 fish) were not more likely to survive a predator attack than ones in small shoals (two to seven fish).The consequences of these results are discussed in the general context of antipredator benefits of grouping.     

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.     

The effects of increasing shoal size on handling time in goldfish, Carassius auratus L.

It is a general assumption that handling time is a constant, given an unvarying size relationship between predator and prey, and an unchanging hunger level. These results indicate that handling times for a pellet of food shown by individual members of a shoal of goldfish decrease by some 20% as the number of fish in the shoal increases from two to 15. Two mechanisms for this reduction are suggested, both of which could act simultaneously. First, there is greater competition for available food resources in a larger shoal and, second, the reduced need for vigilance in a larger shoal will enable individuals to devote more effort to the handling of their food.     

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 genetic structure and microdistribution of shoals of Phoxinus phoxinus, the European minnow

Efficient foraging and a reduction in predation risk have been proposed as reasons for shoal formation. Some behaviours in cyprinid shoals are at first sight altruistic (e.g. predator inspection behaviour, reactions to alarm substance), such that kin selection may have been involved in their evolution. If shoaling behaviour does evolve through kin selection, then genetic differentiation is expected to be greater between shoals than within shoals. Such a hypothesis was tested here by examining shoal integrity and the relatedness of individuals within and between shoals in the European minnow, Phoxinus phoxinus , using nuclear and mitochondrial DNA markers. The breeding structure of 13 minnow shoals collected from Dorset and North Wales, U.K., was examined using allozymes. Genetic affinity within and between shoals was tested using mitochondrial DNA and multi-locus DNA fingerprinting. Shoals consisted of a random assortment of allozyme genotypes, shoal members did not share the same maternal mtDNA lineages and DNA fingerprint profiles were as varied within shoals as between them. The data indicate that it is unlikely that kin selection occurs in P. phoxinus and there is no apparent relationship between shoaling behaviour and genotype distribution in this species.     

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.     

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.      

Context-dependent group size choice in fish

The costs and benefits of group membership vary with the size of groups, and individuals are expected to modify their choice of groups in response to ecological factors such as food availability and predation risk. We experimentally examined context-dependent group size choice in a shoaling fish, the banded killifish, Fundulus diaphanus, by using nondirectional odour cues to simulate a food source or a successful attack by a predator (food or alarm treatments) in the laboratory. Group sizes were significantly smaller in the food treatment and larger in the alarm treatment than in control trials. When presented with food and alarm cues together, fish formed groups that were larger than control groups but smaller than those seen with alarm cues alone. These results are consistent with theoretical predictions based on the known benefits and costs of grouping and with previous laboratory work examining the individual shoal choice behaviour of single fish. To examine possible mechanisms of group formation, we developed an individual-based model of shoaling behaviour in which simulated fish were allowed to modify the area over which they interacted with neighbouring individuals. Group size distributions produced by the model were a good approximation of our experimental data. We suggest that local behavioural interaction rules of this type are a potential mechanism by which fish may individually adjust grouping behaviour without requiring extensive information on the position and movement of all possible shoalmates.     

Predation avoidance and foraging efficiency contribute to mixed-species shoaling by tropical and temperate fishes

The formation of mixed-species social groups, whereby heterospecifics form and maintain either transient or stable groups with each other, can confer substantial fitness benefits to individuals. Such benefits may arise via multiple mechanisms associated with both predation avoidance and foraging efficiency. In fishes, mixed-species shoaling reportedly occurs where displaced tropical species (known as “vagrants”) interact with resident temperate species, although little is known about the nature and frequency of such interactions. To investigate this phenomenon, we used displaced tropical Indo-pacific Sergeant Abudefduf vaigiensis settling in temperate south-eastern Australia as a model system. Underwater visual surveys revealed shoal composition and size differed significantly between open-water and reef habitats, with shoals in open habitats being larger and more speciose. Shoals containing A. vaigiensis were mainly mixed-species, and larger and more speciose in open habitats than nearer to reef. Since both foraging efficiency (via access to plankton) and predation threat likely increase with increasing distance from reef habitat, we suggest that mixed-species shoaling mitigates predation risk whilst allowing increased foraging opportunities for A. vaigiensis in open areas. These findings provide support for the importance of mixed-species shoaling to the persistence of tropical reef fishes in temperate regions.     

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.     

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.     

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.     

Size-segregative behaviour in minnow shoals

Shoals composed of equal numbers of two size-classes of European minnows were observed undisturbed, feeding and after threat from a pike in a large arena tank.
The time/frequency budget and analysed sequences of behaviour of the two size-classes were very similar. Irrespective of size, for standard behaviour measures, fish in the shoal behaved similarly under the same external influences, including predator threat.
In contrast, however, the distribution of the two size-classes provided evidence of size segregation within the shoal. This was brought about by individual minnows making shoaling responses preferentially to their own size-class. After exposure to the predator, shoaling responses changed and differed between small and large minnows.
The outcomes of contests at foraging patches were governed primarily by fish size and information asymmetry rather than by occupation of a feeding site.
The experiment shows that asymmetrical pay-offs in foraging and in response to predator threat are the probable reasons for size-segregation behaviours. This conclusion supports the views of earlier workers that mechanical sorting by swimming speed is not an important factor in size segregation in shoals.     

The social organization of free-ranging fish shoals

The phenotypic composition of social groups can affect the foraging efficiency and predation risk of their individual members. In shoaling fishes, active choice of shoal companions on the basis of phenotypic characters such as body length has been reported. In this study, we investigated the phenotypic composition of free-ranging, multi-species fish shoals in a temperate freshwater lake. We collected 21 entire shoals, each consisting of up to four species and comprising 3622 fish in total. Shoals were strongly assorted by species, body length, parasite prevalence and parasite load. Using a mark-recapture procedure involving 785 banded killifish ( Fundulus diaphanus ), we found no evidence for shoal fidelity or site fidelity, as individuals from different shoals mixed extensively after just 24 h and ranged all over the study site irrespective of initial capture locations. Killifish showed strong changes in shoal-size choice over 24 h, and no evidence was found that shoals might break up into sub-units of individuals that are more phenotypically assorted than their original shoals. The mechanisms by which assortative groups may arise and the consequences of low group fidelity for the evolution of cooperative behaviour are discussed.     

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.     

Modelling density-dependent fish shoal distributions in the laboratory and field

Density-dependent variables have long been established as an important area of ecological research, but the effects of the local density of conspecifics on grouping behaviour are less well-studied. We compared the influence of the density of conspecifics on the shoal size distribution of killifish, Fundulus diaphanus , in the laboratory and the field. In both environments we observed an increase in shoal size and shoal number with the density of individuals present. The increase in shoal size was markedly steeper in the field than in the laboratory, but direct comparison of the two was complicated by the fact that the absolute numbers of fish present at the field site were considerably higher than those used in the laboratory trials. We developed an individual-based model that was first used as a null model of shoal formation (defined by proximity to others) in fish with no shoaling tendency over the same range of densities used in the laboratory. Group size increased much more rapidly with increasing density in the laboratory than predicted by the null model. When we incorporated shoaling behaviour into our model, the laboratory results could be reproduced with high accuracy. However, when extrapolated to match conditions in the field, the model predicted smaller, more numerous shoals than were actually observed. We suggest this is due to heterogeneity of the field environment because fish were found to be highly aggregated in certain areas of our field site. The predictive power of laboratory studies for the field is discussed with regards to using individual-based modelling as a tool for deriving such predictions.     

Body length variation within multi-species fish shoals: the effects of shoal size and number of species

Theory predicts that selection should favour phenotypic homogeneity in fish shoals, and field studies have indeed confirmed that variation in body length within fish shoals is significantly lower than expected from a random distribution of fish among shoals. We investigated the extent to which variation in fish body length within shoals is determined by the shoal mean of body length, the number of species in a shoal, and the overall shoal size. We collected 34 fish shoals, ranging in size from 6 to 776 individuals, from the littoral zone of a Canadian lake. Shoals consisted of up to four different species, with multi-species shoals being larger and more frequent than single-species ones. The strongest determinant of body length variation within shoals was the shoal mean of body length, followed by the number of fish species in a shoal; i.e. multi-species shoals were less size-assorted than single-species ones. A more detailed analysis showed that the higher body length variation observed in multi-species shoals was due to increased body length variation both within and between component species. Shoal size had no significant effect on body length variation within shoals. Potential explanations of the positive relationship between body length variation and the number of species in a shoal are suggested. The implications of the above results for the evolution of multi-species shoals are discussed. Received: 6 May 1997 / Accepted: 14 October 1997