Species-specific schooling behaviour of fish in the freshwater pelagic habitat: an observational study

Social living of animals is a broadly occurring phenomenon, although poorly studied in freshwater systems, fish schooling behaviour is an excellent example. The composition of fish schools, species-specific schooling tendencies and preferences of adult fish were studied in the pelagic habitat of the Římov Reservoir, Czech Republic. Video recordings captured over a total of 34 days (16 h per day) in the clear water period of three seasons were analysed. From four species identified as school-forming species – bream, bleak, roach and perch, 40% of the individuals observed formed schools of 3–36 individuals. Although conspecific schools prevailed, 20% of individuals formed heterospecific schools, except bleak that schooled strictly with conspecifics. Schools were composed of individuals of similar body size and life strategy. Heterospecific schools were significantly larger than conspecific schools and showed uneven proportion among species, that is, one species being more abundant when the school dimension increased. Probability of encounter in bleak was lowest and proved highest inclination for schooling. Gregarianism levels depended on species morphology and body size, with larger and morphologically advanced fish tending less to sociability. This indicates that the antipredator function of schooling behaviour is intensified with increasing vulnerability of the species.     

Schooling preferences for familiar fish in the guppy, Poecilia reticulata

Although schooling behaviour is an important antipredator response of guppies ( Poecilia reticulata ) in Trinidad it is not known whether fish elect to school with particular individuals. Familiarity is a simple mechanism that could lead to non-random associations within schools. In this paper we test the idea that prior experience of particular individuals influences the choice of partners during schooling. We show (in a laboratory study) that female guppies prefer to associate with familiar individuals. However, we are unable to detect any schooling preference for unfamiliar females from the same population.     

School fidelity in fishes: The yellow perch pattern

School fidelity concerns the cohesiveness of social aggregations over time, as measured by the regularity or repeatability with which known individuals re-occur as members of a school. School fidelity was measured by divers who observed yellow perch (Perca flavescens) marked with individually recognizable tags in Cazenovia Lake, New York. Yellow perch were facultative schoolers, with individual differences in schooling tendency (measured as percentage of time in schools) accounting for different numbers of observations of schooled versus solitary fish. The greatest co-occurrence was found between fish with strong schooling tendencies, but within this group co-occurrence was random. Home ranges overlapped greatly between individuals, yet co-occurrence was more a function of schooling tendency than of overlapping home ranges. Individuals with overlapping home ranges but with weak schooling tendencies seldom co-occurred. Home range size increased directly with schooling tendency: the distances that individuals moved apparently depended on the movements of the schools they joined, with strongly schooling fish remaining in schools longer. Individuals joined and left schools frequently; this also reflects a lack of fidelity between fish. Fish schools that form primarily for predator avoidance may show higher levels of fidelity than do schools that form for foraging or hydrodynamic efficiency.     

Aerobic capacity influences the spatial position of individuals within fish schools

The schooling behaviour of fish is of great biological importance, playing a crucial role in the foraging and predator avoidance of numerous species. The extent to which physiological performance traits affect the spatial positioning of individual fish within schools is completely unknown. Schools of juvenile mullet Liza aurata were filmed at three swim speeds in a swim tunnel, with one focal fish from each school then also measured for standard metabolic rate (SMR), maximal metabolic rate (MMR), aerobic scope (AS) and maximum aerobic swim speed. At faster speeds, fish with lower MMR and AS swam near the rear of schools. These trailing fish required fewer tail beats to swim at the same speed as individuals at the front of schools, indicating that posterior positions provide hydrodynamic benefits that reduce swimming costs. Conversely, fish with high aerobic capacity can withstand increased drag at the leading edge of schools, where they could maximize food intake while possibly retaining sufficient AS for other physiological functions. SMR was never related to position, suggesting that high maintenance costs do not necessarily motivate individuals to occupy frontal positions. In the wild, shifting of individuals to optimal spatial positions during changing conditions could influence structure or movement of entire schools.     

Migratory charr schools exhibit population and kin associations beyond juvenile stages

Few studies have critically investigated the genetic composition of wild fish schools. Yet, such investigations may have profound implications for the understanding of social organization and population differentiation in both fundamental and applied research. Using 20 microsatellite loci, we investigated the composition of 53 schools (total n = 211) of adult and subadult migratory brook charr (Salvelinus fontinalis) sampled from the known feeding areas of two populations inhabiting Mistassini Lake (Québec, Canada). We specifically tested whether (i) school members originated from the same population, (ii) individuals from the same population within schools were kin (half- or full-siblings), and (iii) kin schooling relationships differed between sexes. Randomization tests revealed a tendency for most schools to be population specific, although some schools were population mixtures. Significantly more kin were found within schools than expected at random for both populations (approximately 21-34% of the total number of school members). This result, combined with the observed size range of individuals, indicated that stable associations between kin may occur beyond juvenile stages for up to 4 years. Nevertheless, a high proportion of school members were non-kin (approximately 66-79%). No differences were detected between sexes in the propensity to school with kin. We discuss the hypothesis that the stable kin groups, rather than arising from kin selection, may instead be a by-product of familiarity based on individual selection for the maintenance of local adaptations related to migration (natal and feeding area philopatry). Our results are noteworthy because they suggest that there is some degree of permanence in the composition of wild fish schools. Additionally, they support the hypothesis that schools can be hierarchically structured (from population members down to family groups) and are thus nonrandom genetic entities.     

The social organization of adult blue tangs, <Emphasis Type="Italic">Acanthurus coeruleus</Emphasis>, on a fringing reef,Barbados, West Indies

Blue tangs in Barbados exhibit three distinct social modes: territorial, schooling and wandering. We compared the mobility, foraging, aggression performed and received and the use of cleaning stations of adult blue tangs among modes and among habitats within a single fringing reef in Barbados. Evidence from observed switches during focal observations and multiple observations of tagged individuals indicate that fish are either territorial or non-territorial. Non-territorial fish formed schools and wandered. However, wandering can be used during solitary movements by fish in either type. Fish in the territorial mode, not previously described in adults of this species, restricted activity to a small area overlapping the territories of other tangs. They actively chased conspecifics and were chased mostly by damselfishes. They swam more slowly and fed at higher rates than other modes. Fish in the schooling mode ranged widely in compact, polarized groups of conspecifics, congeners and other species. They were not aggressive and were attacked mostly by damselfishes. They swam rapidly and fed at intermediate rates. Fish in the wanderer mode showed neither aggression nor association with other individuals. They swam rapidly, well above the substrate, fed little, were chased by conspecifics, ocean surgeonfish, A. bahianus, and damselfish and visited cleaning stations more often then other modes. All three modes were observed in all four main zones of the reef, and their behaviour changed quantitatively with habitat type. We suggest that territoriality reduces competition for algal food, schooling allows fish to overcome the food defence by damselfish, tangs and ocean surgeonfish, and wandering permits solitary movement over the reef to cleaning stations, feeding sites and other resources.     

Emergence of Oblong School Shape: Models and Empirical Data of Fish

The main benefit of the oblong shape of schools of fish is supposed to be the protection against predation. Models of self‐organised travelling groups have shown that this shape may arise as a side effect of the avoidance of collisions with group members. These models were developed for schools of fish in open water, whereas the oblong shape of schools of real fish has mostly been observed in schools in tanks. Therefore, it is not known how school shape in a tank originates neither in models nor in real fish. To find out what causes this shape, we use the combination of a theoretical and an empirical study. We test the predictions produced by our earlier models regarding the effect of school size on the school shape both in a model of self‐organised schooling in a tank and empirically. Empirically, we study the 3D positions of all individuals in the schools of 10–60 real mullets (Chelon labrosus). We calculate for each individual its distance to its nearest neighbour and its velocity and we measure per school its length and width. The relation between school shape and size in the model and in the real mullets supports our prediction and thus supports the hypothesis that school shape may be emergent from the avoidance of collisions during coordinated travelling.     

Measuring the immune system of the three‐spined stickleback – investigating natural variation by quantifying immune expression in the laboratory and the wild

Current understanding of the immune system comes primarily from laboratory‐based studies. There has been substantial interest in examining how it functions in the wild, but studies have been limited by a lack of appropriate assays and study species. The three‐spined stickleback (Gasterosteus aculeatus L.) provides an ideal system in which to advance the study of wild immunology, but requires the development of suitable immune assays. We demonstrate that meaningful variation in the immune response of stickleback can be measured using real‐time PCR to quantify the expression of eight genes, representing the innate response and Th1‐, Th2‐ and Treg‐type adaptive responses. Assays are validated by comparing the immune expression profiles of wild and laboratory‐raised stickleback, and by examining variation across populations on North Uist, Scotland. We also compare the immune response potential of laboratory‐raised individuals from two Icelandic populations by stimulating cells in culture. Immune profiles of wild fish differed from laboratory‐raised fish from the same parental population, with immune expression patterns in the wild converging relative to those in the laboratory. Innate measures differed between wild populations, whilst the adaptive response was associated with variation in age, relative size of fish, reproductive status and S. solidus infection levels. Laboratory‐raised individuals from different populations showed markedly different innate immune response potential. The ability to combine studies in the laboratory and in the wild underlines the potential of this toolkit to advance our understanding of the ecological and evolutionary relevance of immune system variation in a natural setting.     

Morphological differences between wild and farmed Mediterranean fish

Gilthead seabream (Sparus aurata L.) and European seabass (Dicentrarchus labrax L.) are important commercial marine fish species both for aquaculture and fisheries in the Mediterranean. It is known that farmed individuals escape from farm facilities, but the extent of escape events is not easy to report and estimate because of the difficulty to distinguish between wild and farmed individuals. In this study, significant differences provided through morphometry evidence that the cranial and body regions of seabream and seabass are different regarding their farm or wild origin at different scales. Morphological variations have been shown to be a valuable tool for describing changes in shape features. Therefore, the biomass contribution of escapees to local habitats could be determined by identifying escaped individuals from fisheries landings as a first step to assess the potential negative effects of fish farm escapees on the environment, and their influence on wild stocks and local fisheries.     

Antipredator Benefits of Schooling Behaviour in a Cyprinodontid Fish,the Banded Killifish (Fundulus diaphanus)

Fish schools are believed to provide antipredator benefits to their members. Two potential antipredator benefits, the dilution and confusion effects, of schooling were investigated in the laboratory using banded killifish (Fundulus diaphanus). Individual risk of being attacked and killed by a fish predator (white perch, Morone americana) declined with increasing killifish school size in a manner closely predicted by the dilution hypothesis. Perch were apparently not confused by schooling killifish since fish in groups of one did not suffer a disproportionately greater predation rate than fish in all larger school sizes. However, killifish straggling from the school were preferentially attacked and more successfully captured compared with school members. Schooling in the banded killifish therefore confers a considerable antipredator benefit to individual group members, at least through a dilution effect, and straying from a school has an associated increased risk of mortality to predation, which selects for schooling behaviour.     

Further evidence for size-assortative schooling in sticklebacks

Using brook ( Culaea inconstans ) and 10-spined ( Pungitius pungitius ) sticklebacks we examined body-size related schooling behaviour. Small and large sticklebacks were allowed to choose between two test schools, of small and of large individuals, with and without a piscivorous fish ( Oncorhynchus mykiss ) visible. Sticklebacks of both species preferred the company of fish of matching body size: small fish associating with a school of small fish, large fish with a school of large fish. While no interspecific differences were found in responses to school selection, body size and predator presence did affect selection of school-type. In both species, small fish tended to show a stronger preference for matching schools. The preference was enhanced in small fish with presence of a predator, but not in large fish. These observations are further evidence for assortative schooling in sticklebacks.     

Schooling Fish Under Attack Are Not All Equal: Some Lead,Others Follow

Animal groups such as fish schools, bird flocks and insect swarms appear to move so synchronously that they have long been considered egalitarian, leaderless units. In schooling fish, video observations of their spatial-temporal organization have, however, shown that anti-predator manoeuvres are not perfectly synchronous and that individuals have spatial preferences within the school. Nonetheless, when facing life-or-death situations, it is not known whether schooling fish react to a threat following a random or a hierarchically-based order. Using high-speed video analysis, here we show that schooling fish (Golden grey mullet, Liza aurata) evade a threat in a non-random order, therefore individuals that are first or last to react tend to do so repeatedly over sequential stimulations. Furthermore, startle order is strongly correlated with individual positional preferences. Because school members are known to follow individuals that initiate a manoeuvre, early responders are likely to exert the strongest influence on the escape strategy of the whole school. Our results present new evidence of the intrinsic heterogeneity among school members and provide new rules governing the collective motion of gregarious animals under predator attack.     

Feeding schools among Lake Malawi cichlid fishes

Synopsis Seven species of rock-frequenting cichlids, endemic to Lake Malawi, formed feeding-schools. Petrotilapia genalutea was the nuclear species comprising 92% of the school members (n = 2690 individuals from 50 schools). Fifty-eight per cent of all schools encountered consisted only of P. genalutea. School size ranged from 10 to 300 members (x = 81 ± 74 SD, median = 62). Schooling behaviour was facultative. Ninety-seven per cent of the feeding sites used by the schools occurred within the territories of highly aggressive, territorial species. These sites support considerably greater standing crops of algae, the food of the schooling species, than undefended sites. Individuals of schooling species were unable to gain access to the aggresively defended areas unless they joined schools.     

Schooling preferences for familiar fish vary with group size in a wild guppy population

The ability of fish to recognize and preferentially associate with familiar conspecifics has been well documented in a series of laboratory experiments. In this paper we investigate the schooling preferences of wild female guppies, Poecilia reticulata, in the Upper Tunapuna River in Trinidad and confirm that they do indeed prefer to associate with familiar individuals. The guppies in this river occur in a series of pools that become isolated during the dry season. These fish interact solely with other individuals in their pool for periods of several months at a time and thus have ample opportunity to become accustomed to one another. Our study also reveals that the tendency of female guppies to school with familiar fish declines as the group size in which they naturally live increases. Preferences are strong when there are small numbers of females in a pool, but diminish thereafter. This indicates that the expression of familiarity is constrained by group size. The basis of recognition and the consequences of schooling preferences for familiar individuals are discussed.     

Causes of homing behaviour in a group living reef fish

Homing is a common feature in fish, where for instance many freshwater species return to their place of birth to reproduce. Homing in marine species is, however, less understood. Such homing behaviour may be explained by fitness advantages from staying in a known physical environment as well as a known social environment. Cardinalfish of the family of Apogonidae are small, schooling fish, common in shallow waters in temperate and tropical seas. They form apparently stable group structures both in space and time and it has been shown that they may return to their home site after being experimentally removed up to several kilometres. In order to disentangle whether this homing behaviour in one such cardinalfish species, the Banggai cardinalfish, is driven by preference for the home locality or their original social group, I performed a two part field experiment. Firstly, individuals were allowed to choose between known individuals from their original group and unknown individuals from another group. Secondly, individuals were allowed to choose between their original location inhabited by unknown individuals from another group, and a new location inhabited by individuals from their original group. I discuss the evolution of homing behaviours in fish in light of these experiments.     

Patterns of ectoparasite infection in wild-caught and laboratory-bred cichlid fish,and their hybrids,implicate extrinsic rather than intrinsic causes of species differences in infection

Parasite-mediated selection may initiate or enhance differentiation between host populations that are exposed to different parasite infections. Variation in infection among populations may result from differences in host ecology (thereby exposure to certain parasites) and/or intrinsic immunological traits. Species of cichlid fish, even when recently diverged, often differ in parasite infection, but the contributions of intrinsic and extrinsic causes are unknown. Here, we compare infection patterns between two closely related host species from Lake Victoria (genus Pundamilia), using wild-caught and first-generation laboratory-reared fish, as well as laboratory-reared hybrids. Three of the commonest ectoparasite species observed in the wild were also present in the laboratory populations. However, the infection differences between the host species as observed in the wild were not maintained in laboratory conditions. In addition, hybrids did not differ in infection from either parental species. These findings suggest that the observed species differences in infection in the wild might be mainly driven by ecology-related effects (i.e. differential exposure), rather than by intrinsic species differences in immunological traits. Thus, while there is scope for parasite-mediated selection in Pundamilia in the wild, it has apparently not yet generated divergent evolutionary responses and may not enhance assortative mating among closely related species.

     

Risk of predation,hydrodynamic efficiency and their influence on school structure

Synopsis Laboratory studies were conducted on 15 schools of blackchin shiners, Notropis heterodon, to determine if they altered their structure in response to changing environmental demands. The hypothesis tested was that fish schools should sacrifice a flat, hydrodynamically efficient structure in favour of an unobstructed visual field in the presence of a predator by staggering in the vertical plane. Ten schools were exposed for two weeks to a simple environment with only a current. For the next two-week period a predator was added. Five control schools were exposed to the simple environment for both two-week periods. Six of the ten treated schools increased their staggering in the vertical dimension as predicted while none of the control schools changed. This result was suggestive that hydrodynamic advantages were sacrificed. Respirometer experiments indicated these fish were capable of achieving some hydrodynamic benefits from schooling but these benefits may be a function of fish size.     

Diurnal patterns in the spatial relationships between saithe, Pollachius virens, schooling in the wild

Six saithe, length 35 to 43 cm, were tagged with acoustic transmitters and individuals tracked for between 9 and 508 h during May 1989. The tagged fish were members of a schooling group and during the study, pairs of tagged fish were tracked simultaneously for periods ranging from 9 to 139 h. These data have been used to investigate the spatial relationships between individuals schooling in the wild. Distances between individuals showed a distinct diel pattern. Tagged fish were generally closer together during the day, than either at night or the periods of dawn and dusk. Those circumstances under which pairs of tagged fish could be shown to school together were investigated by analysing the differences in their swimming directions. Schooling was generally evident during the hours of daylight, although the degree to which fish schooled varied between pairs. The degree to which the fish schooled was also dependent upon distance between the tagged individuals. Schooling could be demonstrated for saithe within 20 m of each other during the day and within 10 m in two out of three pairs at night.     

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     

The effect of progressive hypoxia on school structure and dynamics in Atlantic herring Clupea harengus

The effect of progressive hypoxia on the structure and dynamics of herring (Clupea harengus) schools in laboratory conditions was investigated. The length, width and depth of schools of about 20 individuals were measured from video recordings to test the hypothesis that during hypoxia fish schools change their shape and volume. School shape (calculated as the ratios of length/depth, width/depth and length/width) did not change significantly during hypoxia. School length, width, depth, area and volume were all significantly increased at 20% oxygen saturation. Volume, area and width were more sensitive to hypoxia; volume and width were also increased at 25% and area at 30% oxygen saturation. The degree of position changing (shuffling) of individuals within the school was also analysed. Shuffling in normoxia was observed to occur largely through 'O-turn' manoeuvres, a 360( degrees )turn executed laterally to the school that allowed fishes in the front to move to the back. O-turn frequency during normoxia was 0.69 O-turns fish(-1) min(-1) but significantly decreased with hypoxia to 0.37 O-turns fish(-1) min(-1) at 30% oxygen saturation. Shuffling was also investigated by measuring the persistence time of individual herring in leading positions (i.e. the first half of the school). No significant changes occurred during hypoxia, indicating that the decrease in O-turn frequency does not affect shuffling rate during hypoxia, and that position shuffling in hypoxic conditions is mainly due to overtaking or falling back by individual fishes. School integrity and positional dynamics are the outcome of trade-offs among a number of biotic factors, such as food, predator defence, mating behaviour and various physical factors that may impose certain limits. Among these, our results indicate that oxygen level modulates schooling behaviour. Oxygen alters whole-school parameters at oxygen saturation values that can be encountered by herring in the field, indicating that oxygen availability is an important factor in the trade-offs that determine school volume. An increase in school volume in the wild may increase the oxygen available to each individual. However, shuffling rate is not affected by hypoxia, indicating that the internal dynamics of positioning is the result of the balance of other factors, for example related to the nutritional state of each individual fish as suggested by previous studies.