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

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

Size-assorted fish shoals and the majority's choice

Similarity among group members may serve as a defence against visually hunting predators that preferentially attack individuals who are phenotypically different from the group majority. The presence of such odd individuals in an otherwise homogeneous group may, however, increase the vulnerability of the other group members as well. Individuals might thus be expected to form uniform groups in order to decrease predation risk, not only in trying to avoid being odd in a group, but also when attempting to avoid being accompanied by odd individuals. This hypothesis was tested with small and large three-spined sticklebacks, Gasterosteus aculeatus. Focal fish were offered the choice between a shoal consisting of conspecifics that were all similar in body length to the focal fish (matching shoal) and a shoal in which one or a few individuals differed in body length from the focal fish (non-matching shoal). In the control experiment, all individuals in the non-matching shoal differed in size from the focal fish. The control confirmed that individuals preferably joined the matching shoal when the alternative option was to be odd in another one. However, when the alternative for size-assortative shoaling was to belong to the majority in a mixed shoal, the shoal choice of individuals appeared on average to be random. Visual contact with a live pike, Esox lucius, did not affect the shoal choice pattern. Furthermore, despite the frequency-dependent nature of the oddity effect, varying the number of odd individuals in the non-matching shoal did not have a significant effect on individual's shoaling decisions. These results suggest that size-assortativeness in fish shoals is not a result of individuals avoiding being among the majority in a mixed group. Received: 2 September 1998 / Received in revised form: 12 May 1999 / Accepted: 29 May 1999     

Disentangling the effects of group size and density on shoaling decisions of three-spined sticklebacks (<Emphasis Type="Italic">Gasterosteus aculeatus</Emphasis>)

Many animals live in groups most of their life. One function of this behaviour is an increased predator protection whereas larger groups provide better protection than smaller ones. A causal explanation is that due to a higher number of shoal members the individual risk of being predated will decrease (“dilution effect”). Additionally, shoaling leads to increased predator confusion. This “confusion effect” can be strengthened by an increased group density, which often correlates with group size. Many studies found that individuals prefer the larger of two groups. However, whether this preference is due to a larger group size or because of an increased density of the larger group remained unclear. To disentangle these factors we gave three-spined sticklebacks (Gasterosteus aculeatus) the choice between shoals of (1) different group size and density, (2) different group size, but equal density and (3) equal group sizes, but different densities. As expected, test fish preferred the larger and denser shoal over the smaller, less dense one. This preference was lost when shoal size differed but density was kept constant. When shoal size was equal but density differed, test fish preferred the less dense shoal. However, this was only the case when test fish chose between two relatively dense shoals. On the other hand, when overall density was low, test fish did not discriminate between shoals of different densities. This result may be explained in terms of predator avoidance. The results show that shoaling preferences might not always be influenced by a higher number of group members but also by the density and cohesiveness of the respective groups. An erratum to this article can be found at     

A risk-balancing trade off between foraging rewards and predation hazard in a shoaling fish

Summary In controlled experiments, shoaling European minnows fed in equal numbers on two equally-rewarded food patches, and likewise on unequal patches the numbers feeding reflected food levels. For equal food, minnows did not feed at the patch where they had encountered a simulated diving avian predator, whereas they chose to feed at this risky patch when it was more valuable. By avoiding hazard for equal food, but accepting predator risk for higher food rewards, the minnows performed a risk-balancing trade-off.     

Shoaling decisions in three-spined sticklebacks (<Emphasis Type="Italic">Gasterosteus aculeatus</Emphasis>)—familiarity,kinship and inbreeding

Shoaling with familiar kin is a well-known phenomenon. It has been described both for adult and for fry of three-spined sticklebacks (Gasterosteus aculeatus). However, evidence of preference for kin independent of familiarity is scarce. Furthermore, inbreeding effects have not been studied for shoaling preferences and there is a lack of studies about changes in individuals’ ability to recognise kin during different phases of life history. We gave inbred and outbred, nonreproductive sticklebacks of different age the choice to shoal with a group of familiar siblings vs unfamiliar non-siblings and with unfamiliar siblings vs unfamiliar non-siblings. Subadult sticklebacks preferred to shoal with familiar kin over unfamiliar non-kin, but inbred and outbred individuals had similar preferences. When given the choice between unfamiliar siblings and unfamiliar non-sibs, adult outbred fish preferred the shoal of kin, while inbred fish behaved indifferently. Body characteristics of the group such as body mass, standard length and condition of its members did not significantly explain the shoaling preferences for kin. Thus, sticklebacks were capable of recognising familiar and unfamiliar kin. The latter capability was lost by inbreeding.     

Social information,conformity and the opportunity costs paid by foraging fish

Animals pay opportunity costs when pursuing one of several mutually exclusive courses of action. We quantified the opportunity costs of conforming to the behaviour of others in foraging sticklebacks (Pungitius pungitius), using an arena in which they were given the option of shoaling in one area or searching for food in another. Fish foraging in the absence of stimulus conspecifics found the prey patch sooner and spent longer exploiting it than those in trials where a stimulus shoal was present. Furthermore, in trials where the stimulus shoal exhibited feeding cues, subjects approached them sooner and spent more time shoaling with them, exploring less of the arena than in trials where the stimulus shoal exhibited no such cues. This suggests sensitivity not only to the mere presence of conspecifics, but also to the social information that they produce. We also saw that groups of focal fish, compared to single individuals, were less influenced by the stimulus shoal and explored more of the arena, a behaviour that may be attributed to facilitation, competition or both. Such opportunity costs are likely to be offset by benefits such as reduced predation risk, and we discuss this in terms of the trade-offs associated with living in groups.     

Sensory ecology in a changing world: salinity alters conspecific recognition in an amphidromous fish, Pseudomugil signifer

Group fission and fusion processes are driven by state dependence, risk and the availability of information from others. Yet the availability of information changes under different environmental conditions, thus aiding or inhibiting group formation and maintenance. Chemical cues provide information on the location of individuals and can act as a mechanism for individuals to group together, although they can be greatly affected by environmental conditions. Using a flow channel, we studied how one shoaling fish species, the Pacific blue-eye (Pseudomugil signifer), responds to conspecific chemical cues (CCCs) in different environmental conditions (salinities). This species lives in estuarine environments, ranging in salinity from fresh to fully marine. P. signifer responded to CCCs in freshwater but not in saltwater. Furthermore, P. signifer did not respond to saltwater with CCCs added from freshwater. It took significantly longer for fish in saltwater, than in freshwater, to locate and join a shoal when only CCCs from the shoal were present. Finally, fish formed more cohesive shoals in freshwater than in brackish or saltwater. These results suggest that these fish do not rely on chemical cues in saltwater to locate conspecific shoals. Furthermore, the reduced amounts of these cues in saltwater may inhibit the maintenance of tight shoal structures. We suggest that fish utilise different sensory modalities in fresh or saltwater in order to locate one another, or the social structure of these groups is fundamentally different between these two water types. The importance of this study in relation to understanding how animals utilise and change different sensory modalities in varying environmental conditions is discussed.     

Mixed-species shoaling in fish: the sensory mechanisms and costs of shoal choice

The mechanisms and functions of mixed-species shoaling were investigated in two sympatric species of cyprinids, the chub and the European minnow, from the river Wharfe where they comprised approximately 70% of all year 0+ fish over a 20-year survey. Chub preferred conspecific shoals over heterospecific ones with olfactory cues being more important than visual ones for shoal choice. This preference was consistent with measurements of length:flank area ratios and length:weight ratios which suggest that both species are similar in appearance. When presented with mixed-species shoals, chub increased the percentage time spent with stimulus shoals with increasing proportions of conspecifics. Feeding experiments suggest that the preference for conspecific shoals is driven by interspecific competition (with minnows out-competing similar-sized chub) and the oddity effect. The importance of this work in the context of species assortment in free-ranging shoals is discussed.     

The paradox of risk assessment: comparing responses of fathead minnows to capture-released and diet-released alarm cues from two different predators

Summary. Many aquatic prey are known to use chemical alarm cues to assess their risk of predation. In fishes, such alarm cues can be released either through damage of the epidermis during a predatory attack (capture-released) or through release from the predator feces (diet-released). In our study, we compared the importance of capture- versus diet-released alarm cues in risk assessment by fathead minnows (Pimephales promelas) that were na?ve to fish predators. We utilized two different fish predators: a specialized piscivore, the northern pike (Esox lucius) and a generalist predator, the brook trout (Salvelinus fontinalis). Handling time of pike consuming minnows was much shorter than for trout consuming minnows, likely resulting in less epidermal damage to the minnows during attacks by pike. In accordance with this, minnows showed a less intense antipredator response to capture-released cues from pike than capture-released cues from trout. This represents a paradox in risk assessment for the minnows as they respond to the specialized piscivore, the more dangerous predator, with a less intense antipredator response. In contrast, the minnows showed a stronger antipredator response to the specialized piscivore than to the generalist when given diet cues. This work highlights the need for researchers to carefully consider the nature of the information available to prey in risk assessment.     

Performance level and efficiency of two differing predator-avoidance strategies depend on nutritional state of the prey fish

Animal prey has developed a variety of behavioural strategies to avoid predation. Many fish species form shoals in the open water or seek refuge in structurally complex habitats. Since anti-predator strategies bear costs and are energy-demanding, we hypothesised that the nutritional state of prey should modify the performance level and efficiency of such strategies. In aquaria either containing or lacking a structured refuge habitat, well-fed or food-deprived juvenile roach (Rutilus rutilus) were exposed to an open-water predator (pikeperch, Sander lucioperca). Controls were run without predators. In the presence of the predator, roach enhanced the performance of the anti-predator strategy and increased the use of the refuge habitat whereby food-deprived roach were encountered more often in the structure than well-fed roach. Nonetheless more starved than well-fed roach were fed upon by the predator. In the treatments offering only open-water areas, roach always formed dense shoals in the presence of the predator. The shoal density, however, was lower in starved roach. Starving fish in shoals experienced the highest predation mortality across all experimental treatments. The experiment confirmed the plasticity of the anti-predator behaviour in roach and demonstrated that food deprivation diminished the efficiency of shoaling more strongly than the efficiency of hiding. The findings may be relevant to spatial distribution of prey and predator–prey interactions under natural conditions because when prey are confronted with phases of reduced resource availability, flexible anti-predator strategies may lead to dynamic habitat use patterns.     

Kin recognition in rainbowfish (Melanotaenia eachamensis): sex, sibs and shoaling

Living with relatives can be beneficial to individuals via the evolution of kin-directed altruism, but this is tempered by the increased risk of inbreeding. Therefore, in social species, the ability to recognise relatives can be highly advantageous. This study focuses on kin discrimination in the Lake Eacham rainbowfish, Melanotaenia eachamensis, an endangered freshwater species from north-east Queensland, Australia. First, I examined kin recognition abilities when a combination of both chemical and visual recognition cues was available. When given a choice of shoaling with same-sex groups, females spent significantly longer with full-sibs rather than half-sibs, full-sibs rather than non-relatives and half-sibs rather than non-relatives. Males spent significantly longer shoaling with full-brothers versus half-brothers, but showed no other shoalmate preferences. Second, in the presence of only chemical cues, females did not discriminate among groups of different levels of relatedness, but males showed a non-significant tendency to associate with full-sibs rather than non-relatives. Male shoaling behaviour seemed to be more influenced by factors other than relatedness, e.g. intra-sexual competition. Finally, I found that the shoaling preferences of females changed when exposed to groups of males. Females preferred to associate with non-relatives rather than half-brothers and non-relatives rather than full-brothers. There was no significant difference in the time spent with half-brothers versus full-brothers. Taken together, my results suggest that females have very good kin recognition abilities. They prefer to shoal with female relatives but avoid male relatives, and so are able to balance the benefits of nepotism and the costs of incest. Received: 2 May 2000 / Revised: 26 July 2000 / Accepted: 30 July 2000     

Shoaling as an anti-ectoparasite mechanism in juvenile sticklebacks (Gasterosteus spp.)

Summary In laboratory experiments, we tested the hypothesis that by living in larger shoals, juvenile threespine (Gasterosteus aculeatus) and blackspotted (G. wheatlandi) sticklebacks lower their risk of being parasitized by the crustacean ectoparasite Argulus canadensis. An increase in shoal size resulted in a lower average number of attacks received by individual fish, but had no negative effect on the attack performance (attack rate and attack success) of the parasites. In addition, more fish formed shoals and shoal sizes were larger in the presence of parasites. We conclude that ectoparasitism may have been a strong selective factor in the evolution of social behaviour in juvenile sticklebacks.     

Predator inspection behaviour in minnow shoals: differences between populations and individuals

Summary When minnows (Phoxinus phoxinus) detect a stalking pike (Esox lucius) one of their first responses is to perform inspection behaviour during which individuals or small groups approach the predator. This paper compares the inspection behaviour of two contrasting groups of minnows: Dorset minnows which have been heavily predated by pike for many thousands of years and Gwynedd minnows which have spent an equivalent period of time in a pike free environment. Minnows sympatric with pike inspected a realistic model pike more frequently and in larger shoals. Although they commenced inspection earlier they were more timid and kept a greater distance between themselves and the predator. After an inspection they were less likely to recommence foraging than minnows from the Gwynedd population. Individual differences in inspection found within the two populations suggest that selfish behaviour was present.     

The avoidance response of fathead minnows to chemical alarm cues: understanding the effects of donor gender and breeding condition

Summary. All animals are vulnerable to predation at some point in their lives and consequently prey organisms often develop effective risk assessment systems. For many aquatic species predation risk assessment occurs through the use of olfactory cues, including predator odours and alarm cues from damaged or disturbed conspecifics. When aquatic species encounter conspecific alarm cues they may respond, or not, based on specific information including cue concentration, health and size of the conspecific donor and potentially the gender and breeding condition of the donor. Previous laboratory studies have demonstrated that fathead minnows (Pimephales promelas) fail to respond to the skin extracts of breeding male minnows. The purpose of the current study was to verify these early laboratory findings in the field as well as to further investigate the effect of female reproductive state and donor gender on the response of minnows to damage-release alarm cues. Our results indicate that male breeding condition has a significant effect on how minnows will respond to conspecific cues. Minnows showed avoidance of cues of female minnows and male minnows not in breeding condition, in comparison to cues of breeding male minnows and cues of male and female swordtails. Neither the gender of non-breeding minnows nor the reproductive state of female minnows influenced the avoidance of minnows to alarm cues.     

Predator choice in the field; grouping guppies, Poecilia reticulata, receive more attacks

Capture success of many predator species has been shown to decrease with increasing prey group size and it is therefore suggested that predators should choose to attack stragglers and/or small groups. Predator choice in the laboratory has shown mixed results with some species preferentially attacking large groups and others preferring to attack stragglers over groups. Such predator choices have not been tested in the field. In our study we presented a binary choice between a shoal of guppies and a single guppy to predators in pools in the Arima river, Trinidad. We observed attacks in 11 different pools from a total of 53 predators (20 acara cichlids, Aequidens pulcher, 32 pike cichlids, Crenicichla frenata, and one wolf-fish, Hoplias malabaricus) and found that all predators showed a strong preference for the shoal of guppies in terms of both first choice and total number of attacks. We discuss the implications of these preferences with regards to predator–prey interactions.     

Behavioral diversification in a young species flock of pupfish (<Emphasis Type="Italic">Cyprionodon</Emphasis> spp.): shoaling and aggressive behavior

Increasing empirical and theoretical evidence supports the idea that sympatric speciation is operating, for example, in species flocks comprising several closely related fish species within one lake. Divergent natural selection (promoting spatial and food niche partitioning) and sexual selection (assortative mating) have been identified as key selection factors in intralacustric adaptive radiations. However, the evolution of social behaviors accompanying such adaptive radiations is less well understood. Using a phylogenetically young species flock of pupfish (Cyprinodon spp.) as a model, we examined differences among six sympatric species and compared their shoaling, aggressive, and territorial behaviors with that of a sister species (C. artifrons). Despite an estimated age of the species flock of less than 8,000 years, pronounced behavioral differentiation was found. C. simus, the smallest species in the flock, shoaled more than the other species and was less aggressive and less territorial than C. beltrani. F₁-hybrids between C. simus males and C. beltrani females showed an intermediate expression of shoaling and aggressive behavior. Niche partitioning among the members of this species flock appears to be accompanied by rapid divergent evolution of social behaviors. We discuss the potential role of phenotypic plasticity and within-species variation of social behaviors for such rapid behavioral diversifications in sympatric speciation processes.     

Making sense of predator scents: investigating the sophistication of predator assessment abilities of fathead minnows

According to the threat-sensitive predator avoidance hypothesis, selection favors prey that accurately assess the degree of threat posed by a predator and adjust their anti-predator response to match the level of risk. Many species of animals rely on chemical cues to estimate predation risk; however, the information content conveyed in these chemical signatures is not well understood. We tested the threat-sensitive predator avoidance hypothesis by determining the specificity of the information conveyed to prey in the chemical signature of their predator. We found that fathead minnows (Pimephales promelas) could determine the degree of threat posed by northern pike (Esox lucius) based on the concentration of chemical cues used. The proportion of minnows that exhibited an anti-predator response when exposed to a predator cue increased as the concentration of the pike cue used increased. More surprisingly, the prey could also distinguish large pike from small pike based on their odor alone. The minnows responded more intensely to cues of small pike than to cues of large pike. In this predator–prey system small pike likely represent a greater threat than large pike.Communicated by A. Mathis     

Localized defecation by pike: a response to labelling by cyprinid alarm pheromone?

Fathead minnows (Pimephales promelas) that have never encountered a predatory pike (Esox lucius), are able to detect conspecific alarm pheromone in a pike's diet if the pike has recently consumed minnows. It remains unclear how this minnow alarm pheromone is secreted by pike and if a pike is able to avoid being labelled as a potential predator by localizing these cues away from its foraging range. The first experiment determined that minnow alarm pheromone is present in pike feces when pike are fed minnows. Individual fathead minnows exhibited a fright response to a stimulus of pike feces if the pike had been fed minnows, but not if the pike had been fed swordtails, which lack alarm pheromone. Individual minnows also exhibited a fright reaction to alarm pheromone in the water (which contained no feces) housing pike which had been fed minnows, suggesting that alarm pheromone is also released in urine, mucous secretions and/or via respiration. The second experiment determined that test pike spent a significantly greater proportion of time in the home area of the test tanks (i.e. where they were fed) but the majority of feces were deposited in the opposite end of the test tank. By localizing their defecation away from the home or foraging area, pike may be able to counter the effects of being labelled as a predator by the alarm pheromone of the prey species.     

Shoal composition, body size and foraging in sticklebacks

Individuals which deviate from the majority in groups are likely to be most vulnerable to predation. This oddity effect, by definition, is frequency dependent, eventually fading at equal frequencies of the phenotypes in a group. It has been hypothesized that the increased predation risk of odd individuals may play an important role in the formation of phenotypically uniform shoals of fish. However, recent work has indicated that individuals may experience, or value, their predation hazard differently depending on their own size in relation to that of other group members: single large fish, but not small ones, appear concerned about their oddity in a shoal. Here I show that the apparent wariness of large fish is also expressed in a frequency-dependent manner, closely conforming to what is predicted if the oddity effect is responsible for their behavior. Using foraging activity of individuals as a means to evaluate their predation risk, I demonstrate with shoals comprising 12 threespine sticklebacks (Gasterosteus aculeatus) that large fish forage least actively when in a shoal consisting of 2 large and 10 small fish. An increase in the number of large fish to 4 among 8 small individuals clearly results in an increase in their foraging activity. However, having reached an equal frequency with small fish in a shoal, large fish do not seem to change their foraging activity much even when their number in a shoal increases further. In contrast, foraging activity of small sticklebacks remains fairly constant throughout the entire range of tested shoal compositions, providing further evidence that small and large fish respond to their oddity differently. Received: 12 February 1998 / Accepted after revision: 7 May 1998     

Aggresive competition and individual food consumption in wild brown capuchin monkeys (Cebus apella)

Summary The impact of aggresive competition on food intake at all the resources used is analysed for every member of a group of brown capuchin monkeys (Cebus apella) in the Manu National Park, Peru, where they live in groups of 8–14 animals. An individual's food intake at a given tree was affected independently both by its domirance rank (Fig. 1) and by how much aggression it received (Table 5). Food intake was not strongly affected by body size when dominance rank was held constant by partial correlation. At food sources where high rates of fighting occurred, an individual's food intake depended more on its domirance status than on the rate of aggression it received (Fig. 2). However, food intake at resources where rates of fighting were low depended mostly on the rate of aggression received. When aggression over food was absent, the food intakes of dominants and subordinates were equal. Dominants had significantly greater total energy intake (20.5% more) than did subordinates, even though more than one third of their diet came from food sources where little or no fighting occurred (Fig. 3). Energy intake was also significantly greater for individuals that received little aggression. The only adult that emigrated from the main study group was the individua with the lowest energy intake. Competition for food within groups was more than ten times as intense as competition between brown capuchin groups.