The article opens a thematic issue of the
Journal of Ichthyology
, dedicated to Dmitry Viktorovich Radakov, a researcher who made an outstanding contribution to the knowledge of schooling behavior of ...fish. The article deals with many terms and concepts that are widely used in scientific publications on the schooling behavior of fish, but still do not have a generally accepted definition—crowd, aggregation, shoal, school, flock. Attention is drawn to the difficulties caused by the fact that the use of these terms is most often based not on objective criteria, but on the preferences, views or beliefs of individual researchers. General ideas about the prevalence of schooling behavior in fish of different taxonomy, lifestyle, condition and age; about the importance of the visual structuring of the environment for the manifestation of schooling, about the difficulty of dividing fish into facultative and obligate schooling, about the importance of knowledge about schooling behavior for solving applied problems have been considered.
The inner ear position and structure, related parts of the brain and neurocranium, as well as the morphology of the lapillus, sagitta, and asteriscus, are described in climbing perch, an obligate ...air-breathing fish capable of terrestrial movements. The olfactory bulbs and telencephalon are well developed. The dorsal protrusion with two symmetrical lobes is observed on the dorsal posterior surface of the telencephalon. The almost triangular rear part of the brain capsule and a narrow posterior region of the neurocranium represent the border of the suprabranchial chamber. The pars superior of the inner ear is located along the internal triangular part of the brain capsule, and both crus communis and ductus semicircularis posterior are located close to each other in the narrow extreme rear region of the brain capsule. The sacculus is enclosed in the large oval bony capsule (saccular swelling), and the sagitta is large with the average otolith length–total body length (
TL
) ratio equal to 0.06. Linear growth of the lapillus and sagitta is characterized by negative allometry in relation to body length. Despite the slow growth rate of the lapillus, its shape substantially changes during the growth of the fish 36–205 mm
TL
that, most likely, reflects increasing locomotion complexity. Possible adaptations of climbing perch inner ear to terrestrial movements are discussed.
Due to the coordinated reaction of fish to external stimuli and the rapid spread of the excitation wave through a school at a speed much higher than the burst speed of fish (the Trafalgar effect), ...and the so-called movement flow caused by this, the integrity of a school is preserved and the unity of its behavior is achieved—fast protective maneuvering (
f
-maneuver and others), a coordinated change in direction of movement, a change in the shape of a school. These emergent (supraorganismal) properties are inherent in the behavior of an entire school and arise on the basis of innate coordinated reactions of individuals that make up the school. The presence of individually acquired experience and developed imitating abilities in fish leads to the formation of a united pool of conditioned reflexes in a school. Fish schools are equipotential, short-term and rapidly changing leading intra-school groupings (collective leaders) appear in them, and there are no permanent leaders that determine the behavior of an entire school for a long time. This distinguishes fish schools from associations of other vertebrates.
Data on the size and shape of fish schools, number, size, and species composition of individuals included in them have been considered. The largest schools, numbering up to hundreds of thousands of ...individuals or more, are formed by mass marine pelagic fish. The shape of fish schools of the same species is extremely diverse and changes rapidly, depending on the age and size of the fish, their mobility, condition, and other features. The classification of schools has been given—migrating (polarized), feeding, spherical (globular) and others. Schools can become denser or sparse, change the depth of swimming, break up and joint with neighboring ones. The variability of the linear sizes of fish schools and the number of individuals included in them reflects the high plasticity of schooling behavior and its susceptibility to the influence of various factors. Schools are characterized by high homogeneity of the species and size composition of fish and the absence of individual differences in fish. In some cases, schools may consist predominantly of female or male fish. Uniformity is the most important characteristic of fish schools and indicates assortativeness when fish unite into schools. The greatest homogeneity is characteristic of migrating schools of pelagic fish. Multi-species schools are most often formed by juvenile fish.
Protection from predators is the main function of a fish school. Being in a school, fish detect danger faster and from a greater distance, and the distance between a school and a predator allows ...responding to its actions in a timely manner (collective protection). The presence of scout-fish in a school makes it possible to control the position and intentions of a predator (inspection behavior). The density of a school in case of danger, the quick and short bursts of individual fish and the defensive maneuvering of the entire school (
f
-maneuver, or fountain effect) disorientate a predator and reduce the success of its hunt. The larger the school, the faster and more accurately the fish perform defensive reactions, and the higher the protective function of the school. Vulnerability to predators depends on the behavior of schooling fish—individuals that leave a school even for a short time, show increased nervousness and motor activity, and fish that are phenotypically different from the homogeneous majority of the school become prey. Accessibility of schooling fish for predators depends on the illumination. Only lurking predators or predators capable of uniting and using collective attack tactics can overcome schooling defenses during direct attacks on pelagic fish in the daytime. Grouping of fish in a school reduces the risk of infection with some parasites.
The problems and prospects of studying schooling behavior of fish have been considered. Areas that remain little developed or have controversial and contradictory results have been noted: the ...hydrodynamics and energetics of fish swimming in a school, the mechanisms of fish interaction and the dissemination of information within a school, the principles of forming a coordinated school response to external stimuli and the rapid decay of the reaction, interaction between different schools during their collision or when being part of large aggregations of many schools, patterns of rapid change in the forms of a school. It has been shown that there are no clear ideas about the formation of mechanisms in the ontogeny of fish that underlie coordinated schooling behavior. The sensory base of schooling behavior requires further study. The origin and evolution of schooling behavior and the formation of emergent properties of a school based on individual actions of fish remain at the level of assumptions and hypotheses. The interspecies differences in the schooling behavior of fish, the interaction of schooling fish with fishing gear and adaptation to them are poorly studied. Attention has been drawn to the need for verification in nature of information obtained in laboratory conditions and on aquarium fish that have undergone selection. The necessity of using new technologies, devices, methods of mathematical modeling and other approaches for the intensification of experimental research has been emphasized. Knowledge of the schooling behavior of fish is important for elucidating the general patterns of social behavior of large associations of animals. The development of research is hampered by the lack of generally accepted terminology and quantitative criteria for schooling behavior, which would make it possible to adequately assess, compare, and analyze it. An exhaustive definition of a fish school has been given.
In most fish species, the transition to a schooling lifestyle occurs soon after the start of exogenous feeding. The age at which juveniles begin to show schooling behavior differs in different ...species and is not related to the level of schooling in adults, i.e., their belonging to obligate or facultative schooling fish. In marine fish passing through the metamorphosis phase, schooling develops, as a rule, after the completion of this process. Among freshwater fish, juveniles living in rivers begin to show schooling behavior earlier than juveniles in stagnant waters. By the time a school is formed, the level of development of sensory systems and locomotion in juveniles is sufficient for intra-school contacts and schooling swimming. As juveniles grow, the coordination of schooling reactions and the ability to maintain the unity of a school during maneuvering increase. Compared to adult fish, schools of juveniles are less uniform in size and species composition.
Despite being innate, schooling behavior is subject to the influence of external factors that change the condition of fish or the conditions of their environment and reception. Of the abiotic ...factors, the strongest influence is exerted by the illumination and the water turbidity, the abundance of visual landmarks, and the flow velocity. The effect of temperature and the gas composition of water (oxygen content) is much less pronounced; only the first information is available about the effect of water salinity. Among biotic factors, schooling behavior is significantly influenced by various social conditions (fish stocking density, social deprivation), feeding and defensive motivations of fish (fish gut fullness, presence of predators), and parasite infestation. The ability of fish to exhibit schooling behavior is reduced in the presence of virtually all pollutants studied.
Data on the role of brain regions (forebrain, midbrain and other structures) in the control of schooling behavior of fish has been systematized. Data have been presented on the influence of the ...presence in the food of certain substances (docosahexaenoic acid) accumulating in the brain on the rate of formation of schooling behavior in fish ontogeny. The neurohormonal system may be involved in the regulation of schooling behavior. The individual behavior of fish in a school depends on the lateralization of brain functions. Attention has been drawn to the extremely poor knowledge of the processes of central and hormonal regulation of schooling behavior of fish. Vision is the leading, and most often the only sensory system that enables fish to demonstare schooling behavior. Monomodality distinguishes schooling behavior from other complex forms of fish behavior. Visual deprivation or deterioration of the conditions for visual reception makes schooling reactions of fish difficult or completely impossible. Existing assumptions about the possible participation in schooling behavior of other sensory systems of fish—lateral line, hearing, olfaction, electroreception—have been critically analyzed. Strict evidence of the real involvement of these sensory systems in the mediation of schooling contacts in fish is still lacking.
The basic mechanisms of schooling behavior of fish, which is a genetically fixed species character, have been considered. The intention of schooling fish to unite with individuals of their own ...species or with fish that are similar in shape, color and motor activity pattern (schooling reaction) is an innate reflex that manifests itself in natural and artificial environments in individuals with different individual experiences. The intention to unite is expressed the stronger, the more schooling behavior is characteristic of fish. The larger the school, the more attractive it is for fish. To choose a school for association, it is enough that it be 2–3 times larger than the rest. This difference decreases with an increase in the number of fish in schools, with the threat of a predator attack and other stresses. In juveniles, the intention to unite with larger schools is more pronounced than in adult fish. Given a choice, fish prefer individuals of their own species and fish similar in size and color. Imitation is an unconditioned reflex, which is another important mechanism of school behavior. Imitative reactions are most pronounced in schooling fish, but their manifestation is possible if the imitated and imitating fish are conspecific and close in size. An innate optomotor reaction (following reflex) ensures that fish maintain a single school during movements and rapid maneuvering. Schooling coordination is achieved by focusing on the actions of one of the closest partners, and the parallel arrangement of fish is achieved by accurately following the leading partner. Recognition of individuals of their own species, mutual orientation and coordination of actions of fish is facilitated by schooling coloration—spots, stripes and patterns on the body, head and fins, differing in position, size, shape, color, brightness and other details. Important visual landmarks are the contrasting eyes of school partners. Schooling coloration is not present in all schooling fish. In many species, schooling coloration changes as the fish grow and develop.
