Agonistic behavior in a schooling fish: form,function and ontogeny

Synopsis Although juvenile chum salmon,Oncorhynchus keta, are generally regarded as a schooling fish, when presented with a defensible point-source of food, some individuals abandon schooling, aggressively subordinate competitors, and monopolize food. When food is removed, fish gradually abandon solitary agonistic behaviors and return to schooling behavior. Agonism increases in frequency and intensity as juveniles age. The ability to alternate facultatively between schooling and solitary agonistic behavior may enable juvenile chum to respond to local patterns of food distribution and predation risk. The ontogenetic increase in agonism may result in school dispersal as fish move from the estuary into coastal waters, and may well reflect a shift in the costs versus the benefits of schooling as fish mature and become less vulnerable to predation.     

Squeezing out the last egg—annual fish increase reproductive efforts in response to a predation threat

Both constitutive and inducible antipredator strategies are ubiquitous in nature and serve to maximize fitness under a predation threat. Inducible strategies may be favored over constitutive defenses depending on their relative cost and benefit and temporal variability in predator presence. In African temporary ponds, annual killifish of the genus Nothobranchius are variably exposed to predators, depending on whether larger fish invade their habitat from nearby rivers during floods. Nonetheless, potential plastic responses to predation risk are poorly known. Here, we studied whether Nothobranchius furzeri individuals adjust their life history in response to a predation threat. For this, we monitored key life history traits in response to cues that signal the presence of predatory pumpkinseed sunfish (Lepomis gibbosus). While growth rate, adult body size, age at maturation, and initial fecundity were not affected, peak and total fecundity were higher in the predation risk treatment. This contrasts with known life history strategies of killifish from permanent waters, which tend to reduce reproduction in the presence of predators. Although our results show that N. furzeri individuals are able to detect predators and respond to their presence by modulating their reproductive output, these responses only become evident after a few clutches have been deposited. Overall our findings suggest that, in the presence of a predation risk, it can be beneficial to increase the production of life stages that can persist until the predation risk has faded.     

Bioeconomics of schooling fishes: selfish fish, quasi-free riders, and other fishy tales

Applying the economic theory of clubs to the biological literature on schooling fish, this paper develops a 'selfish fish' club-theoretic paradigm of why fish join a fish school, and arrive at the following conclusions. A selfish fish: (a) joins the fish school because it derives hydrodynamic benefits (a club good); the selfish fish is a 'quasi-free rider'; (b) has no incentive to completely free ride on the benefits of the club good, because it will be, literally, left behind by the school; the fish school is a self-enforcing exclusive club; (c) has no incentive to shirk leadership role in the school because of the role reversibility of leaders and followers; (d) derives benefits from defense, another club good, via the many anti-predator defensive devices provided by club members; (e) has no incentive to discriminate against odd-looking outsiders, since odd-looking fish in a fish school are attacked by predators more frequently than look alikes. But outsiders display xenophobia toward insiders because outsiders do not wish to become prime targets for predators; the result is the formation of homotypic fish schools. Finally, (f) since escape is the main anti-predator defense manoeuvre, the 'any-one leader' rule for making collective choice of escape is the optimal decision-making rule for members of a fish school; this explains the leaderless, completely decentralized form of organization of fish schools. This paper thus contribute to new and deeper insights into various aspects of the bioeconomics of schooling fish.     

Hypoxia and the antipredator behaviours of fishes

Hypoxia is a phenomenon occurring in marine coastal areas with increasing frequency. While hypoxia has been documented to affect fish activity and metabolism, recent evidence shows that hypoxia can also have a detrimental effect on various antipredator behaviours. Here, we review such evidence with a focus on the effect of hypoxia on fish escape responses, its modulation by aquatic surface respiration (ASR) and schooling behaviour. The main effect of hypoxia on escape behaviour was found in responsiveness and directionality. Locomotor performance in escapes was expected to be relatively independent of hypoxia, since escape responses are fuelled anaerobically. However, hypoxia decreased locomotor performance in some species (Mugilidae) although only in the absence of ASR in severe hypoxia. ASR allows fish to show higher escape performance than fish staying in the water column where hypoxia occurs. This situation provides a trade-off whereby fish may perform ASR in order to avoid the detrimental effects of hypoxia, although they would be subjected to higher exposure to aerial predation. As a result of this trade-off, fishes appear to minimize surfacing behaviour in the presence of aerial predators and to surface near shelters, where possible. For many fish species, schooling can be an effective antipredator behaviour. Severe hypoxia may lead to the disruption of the school unit. At moderate levels, hypoxia can increase school volume and can change the shuffling behaviour of individuals. By altering school structure and dynamics, hypoxia may affect the well functioning of schooling in terms of synchronization and execution of antipredator manoeuvres. School structure and volume appear to be the results of numerous trade-offs, where school shape may be dictated by the presence of predators, the need for energy saving via hydrodynamic advantages and oxygen level. The effects of hypoxia on aquatic organisms can be taxon specific. While hypoxia may not necessarily increase the vulnerability of fish subject to predation by other fish (since feeding in fish also decreases in hypoxia), predators from other taxa such as birds, jellyfish or aquatic mammals may take advantage of the detrimental effects of hypoxia on fish escape ability. Therefore, the effect of hypoxia on fish antipredator behaviours may have major consequences for the composition of aquatic communities.     

Fish predation on epiphytic microcrustacea in Tivoli South Bay,a Hudson River tidal freshwater wetland

The littoral microcrustacean fauna of Tivoli South Bay was studied from July to September, 1989. The effects of fish predation on microcrustacean densities were tested in a short-term predator exclusion experiment. Fish were excluded from water chestnut (Trapa natans) plots in four screened exclosures. An equal number of open cages allowed foraging. Fish predation did not have a significant effect on densities of ostracods or other microcrustaceans. Ostracod densities increased in cages throughout the experimental period, whereas cladoceran and copepod densities decreased in both treatments. Gut contents analysis of banded killifish (Fundulus diaphanus) revealed that ostracods and other microcrustaceans were commonly ingested by larval, juvenile, and adult killifish utilizing T. natans as habitat. These results suggest that ostracods and other microcrustacean epifauna associated with T. natans may represent an important trophic link in the tidal freshwater wetlands of the Hudson River Estuary. Deceased     

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.     

Sex‐Specific Response of Pardosa milvina (Araneae: Lycosidae) to Experience with a Chemotactile Predation Cue

Predators frequently leave behind chemical information (i.e., semiochemicals such as pheromones or kairomones) that can be detected by their prey and used to avoid areas where predators are likely present. Prey that have interacted indirectly with predators via chemical information thus may gain insight into their risk of being consumed that naïve individuals lack. Pardosa milvina (Araneae: Lycosidae) is a chemosensitive wolf spider that shows adaptive responses to chemotactile cues deposited by the larger wolf spider Tigrosa helluo. We raised offspring from P. milvina to examine the effect of experience with a predation cue on activity, foraging, and antipredator behavior. Spiders differed in activity and foraging behavior across ontogeny and between sexes, but there was no effect of experience with a predation cue. However, a sex‐specific effect of experience was found in antipredator behavior. Male spiders, but not females, used experience with a predator cue to increase their survival in the presence of a live predator. Specifically, naïve males were attacked sooner than experienced males, indicating that prior exposure to predator cues can modify Pardosa antipredator behavior. Intersexual differences in how spiders respond to experience with a predation cue likely reflect the risk of predation faced by males and females in nature.     

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.     

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.     

Effects of opportunistic predation on anti-predator behavioural responses in a guild of ground foragers

We studied factors that affect prey selection by a generalist predator that opportunistically attacks prey species, and the associated inter- and intra-specific responses of prey to this type of predation. Our model system was a guild of ground-foraging birds that are preyed upon by magpies (Pica pica) during the breeding season. We found that magpies attacked up to 12 species during three consecutive breeding seasons. The overall capture success was estimated to be 4.9%. Magpies tended to attack from the air, targeting solitary prey, either on the ground or flying. Inter-specific prey responses to the risk of magpie predation included a reduction in the mean number of species occupying a foraging patch when magpies were present and a decrease in the distance between heterospecific neighbours. Intra-specific responses to magpie predation varied between species that were subject to different attack rates. Preferentially attacked prey enhanced their risk responses (increase in scanning time and scanning rate in the presence of magpies) relative to those species attacked in proportion to their abundance (increase only in scanning rate with magpies). Species attacked infrequently, relative to their abundance, showed no antipredator response. The probability of being attacked, rather than mortality rate, appears to be the factor to which prey species respond.     

Back to school: can antipredator behaviour in guppies be enhanced through social learning?

The ability to recognize and respond to predators often has a learned component, but few studies have examined the role of social learning in the development of antipredator behaviour. We investigated whether wild-caught juvenile guppies, Poecilia reticulata, from a low-predation river in Trinidad increase their response towards a novel predator through association with conspecifics from a high-predation river. We assigned fish to one of three treatment groups: (1) repeated exposure to a model accompanied by high-predation conspecifics; (2) repeated exposure to a model with low-predation conspecifics; (3) a control group in which focal fish interacted with high-predation fish in the absence of the model. Guppies trained with high-predation, but not low-predation, ‘demonstrators’ significantly improved their antipredator behaviour (spent more time schooling and inspected the model from further away). The guppies assigned to the control group showed no significant improvement in antipredator behaviour after the training period, suggesting that association with experienced conspecifics in the absence of the model is not sufficient to enhance the antipredator behaviour of na?ve fish. We conclude that guppies can improve their antipredator behaviour through association with more experienced conspecifics in the presence of visual cues simulating high predation risk. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.        

Size-assortativeness in multi-species fish shoals

Theory predicts that fish should assort in shoals on the basis of similar phenotypic traits to minimize predation risk and to maximize foraging efficiency. A single phenotypic character, body size, was considered and the hypothesis tested that free-ranging fish shoals are sizeassorted. Furthermore, a second test investigated whether fish within multi-species shoals are more strongly size-assorted with conspecifics than with heterospecifics. Twelve fish shoals, each comprising two different species (golden shiner Notemigonus crysoleucas , and banded killifish Fundulus diaphanus ) were caught in the littoral zone of a north temperate lake using a beach seine. Shoal membership size ranged from 36 to 776 fish, and mean standard body length of members ranged from 18 to 34 mm. Fish were assorted by body size at two different levels, namely, between shoals and at the level of species within shoals. Body sizes of shiners and killifish within shoals were significantly different in seven out of 12 shoals, with killifish being the larger species in five cases and shiners being the larger one in two cases. Because there is considerable overlap in body size between the two species in the population, the observed species-related size-assortativeness within shoals was not just the by-product of a directional size difference (between species) in the population. These findings provide strong quantitative evidence for size-sorting in free-ranging fish shoals and raise questions concerning the formation of multi-species fish shoals.     

Olfactorily-mediated cortisol response to chemical alarm cues in zebrafish Danio rerio

Chemical cues released as a by-product of predation mediate antipredator behaviour, but little is known about the physiological responses to olfactory detection of predation risk. In this study, zebrafish Danio rerio were exposed to either chemical alarm cues from conspecifics, or water (control). Compared with water controls, D. rerio exposed to alarm cues responded behaviourally with antipredator behaviours such as erratic dashing and an increase in time spent near the bottom of the test aquarium. Danio rerio were sacrificed 5 min after exposure to test cues (alarm cues or water). Enzyme-linked immunosorbent assay (ELISA) revealed whole-body levels of cortisol that were significantly higher for fish exposed to alarm cues (mean ± SE, 11.9 ± 3.4 ng g⁻¹) than control fish (1.5 ± 0.7 ng g⁻¹). These data provide a benchmark for future studies of the proximate mechanisms of olfactorily mediated antipredator responses, modelling effects on aquatic life in a changing climate and, as a model organism, Danio rerio can further our understanding of anxiety in humans.     

Aggressive Interactions and Risk of Fish Predation for Larval Damselflies

Larval damselflies frequently engage in aggressive interactions that may increase their risk of fish predation. To test this we analyzed the behavior of larval Ischnura verticalis exposed to both conspecifics and fish predators. Larvae in the presence of conspecifics oriented, struck, and swam more but crawled less compared to solitary larvae; the presence of fish reduced, or tended to reduce, all behaviors. Fish struck more at interacting larvae compared to noninteracting larvae. Increased attack rate by fish likely reflects the increase in the very active swimming behavior by larvae and suggests a conflict between antipredator behaviors. Swimming is an appropriate response to avoid predation by odonate larvae which normally ambush prey but is clearly dangerous when fast-swimming fish that cue in on movement are nearby.     

Antipredator Behaviour and Suppressed Aggression by Convict Cichlids in response to Injury-released Chemical Cues of Conspecifics but not to those of an Allopatric Heterospecific

In aquatic environments, chemical cues serve as an important source of information for the detection of predation risk. Here, we investigate the response of convict cichlids, Cichlasoma nigrofasciatum, to injury-released chemical cues. We exposed pairs of juvenile convict cichlids first to dechlorinated tap water (control), then later to one of two test stimuli: 1. chemical cues from injured convict cichlids; or 2. chemical cues from injured mosquito fish, Gambusia affinis. Gambusia are allopatric and phylogenetically unrelated to convict cichlids. Gambusia skin was used to control for a general response to injured fish. In response to conspecific cues, convict cichlids significantly increased time spent near the bottom of test aquaria and time under a shelter object. In response to Gambusia skin, convict cichlids tended to increase time spent near the tank bottom but did not increase use of the shelter object. There was a trade-off between antipredator and agonistic behaviours. In response to convict cichlid cues, there was a significant reduction in the frequency of approaches and bites. Gambusia skin extract had no significant effect on aggressive behaviour. These data suggest a species-specific antipredator response to conspecific alarm pheromones in a New World cichlid fish and demonstrate a trade-off between predator avoidance and intraspecific aggression. Further, the presence of an alarm response in this model species sets the stage for the use of chemical cues as a research tool to manipulate predation risk in studies of the interaction between predation risk and reproductive behaviour.     

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.      

Transplant experiments demonstrate that larger brains are favoured in high-competition environments in Trinidadian killifish

The extent to which the evolution of a larger brain is adaptive remains controversial. Trinidadian killifish (Anablepsoides hartii) are found in sites that differ in predation intensity; fish that experience decreased predation and increased intraspecific competition exhibit larger brains. We evaluated the connection between brain size and fitness (survival and growth) when killifish are found in their native habitats and when fish are transplanted from sites with predators to high-competition sites that lack predators. Selection for a larger brain was absent within locally adapted populations. Conversely, there was a strong positive relationship between brain size and growth in transplanted but not resident fish in high-competition environments. We also observed significantly larger brain sizes in the transplanted fish that were recaptured at the end of the experiment versus those that were not. Our results provide experimental support that larger brains increase fitness and are favoured in high-competition environments.     

Preferences for familiar fish do not vary with predation risk in the European minnow

In the near-natural conditions of a fluvarium in the River Frome, U.K., European minnows Phoxinus phoxinus displayed schooling preferences for familiar conspecifics. Schools were composed of 75% familiar fish. The minnows in this river co-occur with many piscivores, the most notable being the pike Esox Iucius . The preference for familiar shoalmates was not increased by the threat of predatory attack from a model pike, despite the antipredator benefits afforded to individual members of schools of familiar fish.     

Predator-induced neophobia in juvenile cichlids

Predation is an important but often fluctuating selection factor for prey animals. Accordingly, individuals plastically adopt antipredator strategies in response to current predation risk. Recently, it was proposed that predation risk also plastically induces neophobia (an antipredator response towards novel cues). Previous studies, however, do not allow a differentiation between general neophobia and sensory channel-specific neophobic responses. Therefore, we tested the neophobia hypothesis focusing on adjustment in shoaling behavior in response to a novel cue addressing a different sensory channel than the one from which predation risk was initially perceived. From hatching onwards, juveniles of the cichlid Pelvicachromis taeniatus were exposed to different chemical cues in a split-clutch design: conspecific alarm cues which signal predation risk and heterospecific alarm cues or distilled water as controls. At 2 months of age, their shoaling behavior was examined prior and subsequent to a tactical disturbance cue. We found that fish previously exposed to predation risk formed more compact shoals relative to the control groups in response to the novel disturbance cue. Moreover, the relationship between shoal density and shoal homogeneity was also affected by experienced predation risk. Our findings indicate predator-induced, increased cross-sensory sensitivity towards novel cues making neophobia an effective antipredator mechanism.     

Sensory complementation and antipredator behavioural compensation in acid-impacted juvenile Atlantic salmon

Prey incorporate multiple forms of publicly available information on predation risk into threat-sensitive antipredator behaviours. Changes in information availability have previously been demonstrated to elicit transient alterations in behavioural patterns, while the effects of long-term deprivation of particular forms of information remain largely unexplored. Damage-released chemical alarm cues from the epidermis of fishes are rendered non-functional under weakly acidic conditions (pH < 6.6), depriving fish of an important source of information on predation risk in acidified waterbodies. We addressed the effects of long-term deprivation on the antipredator responses to different combinations of chemical and visual threat cues via in situ observations of wild, free-swimming 0⁺ Atlantic salmon (Salmo salar) fry in four neutral and four weakly acidic nursery streams. In addition, a cross-population transplant experiment and natural interannual variation in acidity enabled the examination of provenance and environment as causes of the observed differences in response. Fish living under weakly acidic conditions demonstrate significantly greater or hypersensitive antipredator responses to visual cues compared to fish under neutral conditions. Under neutral conditions, fish demonstrate complementary (additive or synergistic) effects of paired visual and chemical cues consistent with threat-sensitive responses. Cross-population transplants and interannual comparisons of responses strongly support the conclusion that differences in antipredator responses between neutral and weakly acidic streams result from the loss of chemical information on predation risk, as opposed to population-derived differences in behaviours.