Variability of the behavioral laterality in Teleostei (Pisces)

Factors causing variability of behavioral laterality in Teleostei are reviewed. The laterality has been revealed in many fish species belonging to various families. The best ever demonstrated example of the laterality is the different use of the right and left eyes when a fish responds to different visual objects. Magnitude and sign of the laterality differ in fishes of different species, gender, and age. Also, an observed laterality depends on how familiar a stimulus is to fishes and what it means to them, as well as their motivational level and various behavioral traits. Therefore, comparisons of the laterality among different fish species should be based on experimental methods that also take into account those behavioral differences among them that are not directly linked to the laterality.     

Righty fish are hooked on the right side of their mouths - observations from an angling experiment with largemouth bass, Micropterus salmoides

The development of muscles and bones in fish is laterally asymmetric (laterality). A "lefty" individual has a "C"-shaped body, with its left-side muscles more developed and the left side of its head facing forward. The body of a "righty" is the mirror-image. This laterality causes asymmetric interactions between individuals of different fish species, in that a righty or lefty fish consumes more lefty or righty fish, respectively. To investigate the coupling mechanisms between body asymmetry and predatory behavior, we conducted angling experiments with largemouth bass (Micropterus salmoides). We used the position of the fishhook set in the mouth to indicate the movement direction of the fish when it took the bait. Righty fish had more hooks set on the right side, whereas lefty fish had more on the left side, indicating that righty fish moved more to the left, and lefty fish moved more to the right, in successful catches. The relationship between the hooked position and movement direction was confirmed by video-image analysis of the angling.     

Laterality Influences Schooling Position in Rainbowfish,Melanotaenia spp

Cerebral lateralization is a widespread trait among animals, is often manifested as side biases in behaviour (laterality) and has been suggested to provide fitness benefits. Here we examined the influence of laterality on the organisation of fish schools using rainbowfish (Melanotaenia spp) as model species. The pattern and strength of laterality for each individual was determined by examining eye preferences whilst examining their reflection in a mirror. Schools of four fish of known laterality were then created and the preferred position for each fish within the school was repeatedly observed in a flume. Fish which showed right eye preferences in the mirror test preferentially adopted a position on the left side of the school. Conversely, fish that showed left eye preferences in the mirror test or where non-lateralised preferentially adopted a position slightly to the right side of the school. However, this general pattern varied depending on the species and sex of the school. Our results strongly implicate individual laterality in the geometry of school formation.     

fsi zebrafish show concordant reversal of laterality of viscera, neuroanatomy, and a subset of behavioral responses

Asymmetries in CNS neuroanatomy are assumed to underlie the widespread cognitive and behavioral asymmetries in vertebrates. Studies in humans have shown that the laterality of some cognitive asymmetries is independent of the laterality of the viscera; discrete mechanisms may therefore regulate visceral and neural lateralization. However, through analysis of visceral, neuroanatomical, and behavioral asymmetries in the frequent-situs-inversus (fsi) line of zebrafish, we show that the principal left-right body asymmetries are coupled to certain brain asymmetries and lateralized behaviors. fsi fish with asymmetry defects show concordant reversal of heart, gut, and neuroanatomical asymmetries in the diencephalon. Moreover, the neuroanatomical reversals in reversed fsi fish correlate with reversal of some behavioral responses in both fry and adult fsi fish. Surprisingly, two behavioral asymmetries do not reverse, suggesting that at least two separable mechanisms must influence functional lateralization in the CNS. Partial reversal of CNS asymmetries may generate new behavioral phenotypes; supporting this idea, reversed fsi fry differ markedly from their normally lateralized siblings in their behavioral response to a novel visual feature. Revealing a link between visceral and brain asymmetry and lateralized behavior, our studies help to explain the complexity of the relationship between the lateralities of visceral and neural asymmetries.     

Handed foraging behavior in scale-eating cichlid fish: its potential role in shaping morphological asymmetry

Scale-eating cichlid fish, Perissodus microlepis, from Lake Tanganyika display handed (lateralized) foraging behavior, where an asymmetric 'left' mouth morph preferentially feeds on the scales of the right side of its victim fish and a 'right' morph bites the scales of the left side. This species has therefore become a textbook example of the astonishing degree of ecological specialization and negative frequency-dependent selection. We investigated the strength of handedness of foraging behavior as well as its interaction with morphological mouth laterality in P. microlepis. In wild-caught adult fish we found that mouth laterality is, as expected, a strong predictor of their preferred attack orientation. Also laboratory-reared juvenile fish exhibited a strong laterality in behavioral preference to feed on scales, even at an early age, although the initial level of mouth asymmetry appeared to be small. This suggests that pronounced mouth asymmetry is not a prerequisite for handed foraging behavior in juvenile scale-eating cichlid fish and might suggest that behavioral preference to attack a particular side of the prey plays a role in facilitating morphological asymmetry of this species.     

Persistence and fluctuation of lateral dimorphism in fishes

Two morphological types ("righty" and "lefty") have been discovered in several fish species and are referred to as a typical example of antisymmetry. It has been suggested, first, that this dimorphism (called laterality) is inheritable; second, that the frequencies of laterality in each species fluctuate around 0.5; and third, that predators mainly exploit prey of the opposite laterality; that is, lefty and righty predators prey on righties and lefties, respectively. The latter is defined as "cross predation"; the antonym "parallel predation" means predation within the same laterality. We hypothesized that cross predation drives alternation of the survival and reproductive advantages between two morphological types, leading to frequency-dependent selection that maintains the dimorphism. To investigate this, we constructed mathematical models of population dynamics of one prey/one predator systems and three-trophic-level systems with omnivory. Mathematical analysis and computer simulations explained the behavior of the laterality frequency in nature well, insofar as cross predation dominated over parallel predation. Furthermore, the simulations showed that when only one of the morphological types exists in a species, the other type can invade. This suggests that dimorphism is maintained in all interacting species.     

Oxygen consumption by sticklebacks (Gasterosteus aculeatus L.) exposed to zinc

The rate of oxygen consumption by sticklebacks has been studied by long-term continuous-flow respirometry. Exposure to 1 p.p.m. zinc in calcium-free water causes wide variations in individual responses, but oxygen uptake tends to rise and then become extremely erratic, before declining as death approaches. Behavioural abnormalities such as increased ventilation rate, loss of balance, and long periods of inactivity alternating with spasmodic swimming also occur. Exposure to 6.5 p.p.m. zinc in high-calcium water generally causes a rise in oxygen consumption, followed by fluctuations in the rate of uptake, but no behavioural abnormalities occur and deaths are rare even after exposure for 400 h. If restored to zinc-free water after 40 h exposure to zinc, recovery is generally complete, although fluctuating rates of oxygen uptake persist. These results are discussed in relation to previous work on the effects of heavy metals on fish respiration.     

Physiological effects of dominance hierarchies: laboratory artefacts or natural phenomena?

Studies of fish behaviour have demonstrated the existence of social interactions that result in dominance hierarchies. In environments in which resources, such as food, shelter and mates, are limited, social competition results in some fish becoming dominant and occupying the most profitable positions. This behaviour has been observed in natural environments and also in many laboratory‐based experiments. When two fish have been confined in a small tank, one of them usually has exhibited behaviour that suggests it is dominant over the other submissive animal. Physiological consequences of social interaction can be seen in both dominants and subordinates but are more extreme in the subordinate. However, this scenario is without doubt an artificial situation. Fewer experiments have been conducted using laboratory experiments that are more socially and physically complex than those experienced by dyads in tanks. In simple fluvial tanks, through which water is recirculated, the physiological responses of fish to social competition have generally been qualitatively similar to those recorded among dyads. However, when environmental disturbances, complex resource distributions, increase in water flushing, presence of predators and competing species of fish have been included in experimen‐tal designs, there have been fewer, diminished or no physiological dierences between dominant and subordinate fish. There have been very few studies of physiology in relation to dominance in natural habitats, and those that have been conducted suggest that under some circumstances hierarchies may cause less intense physiological responses than have been suggested based on results of laboratory studies in simple environments. Possible reasons for these variations are discussed. The need is identified for a well structured experimental approach to the investi‐gation of the causes and consequences of hierarchies if the ecology of wild fish is to be modelled eectively based on physiological processes. It is also suggested that the further development and application of techniques for monitoring physiologies of fish in the wild is important.     

The influence of changes to river hydrology on freshwater fish in regulated rivers of the Murray–Darling basin

Freshwater fish are often used as an indicator of the response of the ecosystem to the restoration of river flows or the provision of environmental flows. The ability to model the biological response of fish depends on the capacity to establish clear relationships between changes in river hydrology and the fish assemblages in a river. The fish assemblage structure and the abundances of individual fish species were examined in relation to a hydrological index that described hydrological change in six regulated rivers in the Murray–Darling Basin. The hydrological index explained only a small amount of variation in fish assemblage structure. In addition, the abundances of individual fish species were only weakly correlated with the index of flow deviation. It is suggested that these results make the modelling of responses of fish assemblages to environmental water allocations unfeasible at a large scale and that future studies should concentrate on potentially more simple responses, such as the relationships of fish spawning and recruitment to specific aspects of river hydrology.     

Laterality of the initial stage of escape response in roach (<Emphasis Type="Italic">Rutilus rutilus</Emphasis>) upon impact of alternating electric current

The initial stage of the escape response (C-bend of the body) upon sudden impact of electric current on free-swimming fish was studied in young roach (Rutilus rutilus). More than half of the fish showed distinct behavioral laterality, i.e., a stabile tendency to bend either to the left or to the right, and retained it until the next test conducted 10 days later. The majority of fish bent to the left, but the difference between the proportions of individuals that showed opposite lateralities lacked statistical significance. This response and the type of laterality are stable and simple to record, which makes the C-bend a convenient experimental model for studying behavioral asymmetry in fishes.     

Population dynamics of migratory trout, Salmo trutta, in a Lake District stream, 1966–83, and their implications for fisheries management

A short review summarises the chief conclusions of an 18-year investigation of the population dynamics of migratory trout, Salmo trutta L., in a Lake District stream. The chief factors affecting growth, survival and production have been identified and their effects summarized in a series of mathematical models. The implications of this work are discussed in relation to long-term investigations, data analysis and modelling, and the scientific management of trout populations. It is shown that mathematical models, based on long-term investigations, can be used to assess the effects on a fish population of changes due to natural causes (e.g., droughts and spates) or human activities. One of the main objectives of future work should be the development and improvement of models that can be used as tools for the conservation and management of fish stocks.     

Behavioral laterality and morphological asymmetry in the cuttlefish, Sepia lycidas

Behavioral laterality is widely found among vertebrates, but has been little studied in aquatic invertebrates. We examined behavioral laterality in attacks on prey shrimp by the cuttlefish, Sepia lycidas, and correlated this to their morphological asymmetry. Behavioral tests in the laboratory revealed significant individual bias for turning either clockwise or counterclockwise toward prey, suggesting behavioral dimorphism in foraging behavior. Morphological bias was examined by measuring the curvature of the cuttlebone; in some the cuttlebone was convex to the right (righty), while in others, the cuttlebone was convex to the left (lefty). The frequency distributions of an index of cuttlebone asymmetry were bimodal, indicating that populations were composed of two types of individuals: "righty" and "lefty." Moreover, an individual's laterality in foraging behavior corresponded with the asymmetry of its cuttlebone, with righty individuals tending to turn counterclockwise and lefty ones in the opposite direction. These results indicate that cuttlefish exhibit behavioral dimorphism and morphological antisymmetry in natural populations. The presence of two types of lateral morph in cuttlefish provides new information on the relationship between antisymmetric morphologies and the evolution of individual laterality in behavioral responses in cephalopods. The implications of these findings for the interpretation of ecological meaning and maintenance mechanisms of laterality in cuttlefish are also discussed.     

EOD modulations of brown ghost electric fish: JARs, chirps, rises, and dips.

Weakly electric "wave" fish make highly regular electric organ discharges (EODs) for precise electrolocation. Yet, they modulate the ongoing rhythmicity of their EOD during social interactions. These modulations may last from a few milliseconds to tens of minutes. In this paper we describe the different types of EOD modulations, what they may signal to recipient fish, and how they are generated on a neural level. Our main conclusions, based on a species called the brown ghost (Apteronotus leptorhynchus) are that fish: (1) show sexual dimorphism in the signals that they generate; (2) make different signals depending on Whether they are interacting with a fish of the opposite sex or, within their own sex, to a fish of that which is dominant or subordinate to it; (3) are able to assess relative dominance from electrical cues; (4) have a type of plasticity in the pacemaker nucleus, the control center for the EOD, that occurs after stimulation of NMDA receptors that causes a long-lasting (tens of minutes to hours) change in EOD frequency; (5) that this NMDA receptor-dependent change may occur in reflexive responses, like the jamming avoidance response (JAR), as well as after certain long-lasting social signals. We propose that NMDA-receptor dependent increases in EOD frequency during the JAR adaptively shift the EOD frequency to a new value to avoid jamming by another fish and that such increases in EOD frequency during social encounters may be advantageous since social dominance seems to be positively correlated with EOD frequency in both sexes.     

Structural changes in the pars intermedia of the cichlid teleost Sarotherodon mossambicus as a result of background adaptation and illumination

Summary The pars intermedia of Sarotherodon mossambicus contains two structurally different endocrine cell types. The predominant cell type is assumed to synthesize MSH and related peptides. The second cell type is PAS positive; its function and products are unknown. In this second cell type changes occur in relation to background colour and illumination. Thus, PAS positive cells of fish adapted to a white background are less numerous and metabolically less active than those of fish adapted to a black background, and are most active in fish kept in total darkness. In blinded fish, whether in light or in darkness, the activity of the PAS positive cells is similar to that of the black background-adapted animals. The significance of these responses in relation to the control of background adaptation is discussed.     

The use of chemical cues in the upstream migration of coho salmon, Oncorhynchus kisutch Walbaum

The migratory behaviour of coho salmon was studied in the field. Coho salmon, Oncorhynchus kisutch , exposed to synthetic odours in a hatchery and released into Lake Michigan as juveniles, were recaptured as migrating adults 18 months later. The movements of 43 individuals were followed in experiments examining the role of imprinted chemical cues in the homing migration. Movements in relation to controlled distributions of the imprinting odours revealed that chemical cues are used by the salmon in their upstream migration. Acting with the rheotactic response, fish were guided upstream by imprinting odours simulating their home stream. Coho salmon, in the absence of their imprinting odour, respond negatively to the current. Differential responses to current appear to serve in segregating fish imprinted to odours of different home streams.     

Cognitive ability and sentience: which aquatic animals should be protected?

It is of scientific and practical interest to consider the levels of cognitive ability in animals, which animals are sentient, which animals have feelings such as pain and which animals should be protected. A sentient being is one that has some ability to evaluate the actions of others in relation to itself and third parties, to remember some of its own actions and their consequences, to assess risk, to have some feelings and to have some degree of awareness. These abilities can be taken into account when evaluating welfare. There is evidence from some species of fish, cephalopods and decapod crustaceans of substantial perceptual ability, pain and adrenal systems, emotional responses, long- and short-term memory, complex cognition, individual differences, deception, tool use, and social learning. The case for protecting these animals would appear to be substantial. A range of causes of poor welfare in farmed aquatic animals is summarised.     

Analysis of quantitative trait loci for behavioral laterality in mice

Laterality is believed to have genetic components, as has been deduced from family studies in humans and responses to artificial selection in mice, but these genetic components are unknown and the underlying physiological mechanisms are still a subject of dispute. We measured direction of laterality (preferential use of left or right paws) and degree of laterality (absolute difference between the use of left and right paws) in C57BL/6ByJ (B) and NZB/BlNJ (N) mice and in their F(1) and F(2) intercrosses. Measurements were taken of both forepaws and hind paws. Quantitative trait loci (QTL) did not emerge for direction but did for degree of laterality. One QTL for forepaw (LOD score = 5.6) and the second QTL for hind paw (LOD score = 7.2) were both located on chromosome 4 and their peaks were within the same confidence interval. A QTL for plasma luteinizing hormone concentration was also found in the confidence interval of these two QTL. These results suggest that the physiological mechanisms underlying degree of laterality react to gonadal steroids.     

Mouth asymmetry in the textbook example of scale-eating cichlid fish is not a discrete dimorphism after all

Individuals of the scale-eating cichlid fish, Perissodus microlepis, from Lake Tanganyika tend to have remarkably asymmetric heads that are either left-bending or right-bending. The ‘left’ morph opens its mouth markedly towards the left and preferentially feeds on the scales from the right-hand side of its victim fish, and the ‘right’ morph bites scales from the victims’ left-hand side. This striking dimorphism made these fish a textbook example of their astonishing degree of ecological specialization and as one of the few known incidences of negative frequency-dependent selection acting on an asymmetric morphological trait, where left and right forms are equally frequent within a species. We investigated the degree and the shape of the frequency distribution of head asymmetry in P. microlepis to test whether the variation conforms to a discrete dimorphism, as generally assumed. In both adult and juvenile fish, mouth asymmetry appeared to be continuously and unimodally distributed with no clear evidence for a discrete dimorphism. Mixture analyses did not reveal evidence of a discrete or even strong dimorphism. These results raise doubts about previous claims, as reported in textbooks, that head variation in P. microlepis represents a discrete dimorphism of left- and right-bending forms. Based on extensive field sampling that excluded ambiguous (i.e. symmetric or weakly asymmetric) individual adults, we found that left and right morphs occur in equal abundance in five populations. Moreover, mate pairing for 51 wild-caught pairs was random with regard to head laterality, calling into question reports that this laterality is maintained through disassortative mating.     

Ammonia in estuaries and effects on fish

This review aims to explore the biological responses of fish in estuaries to increased levels of environmental ammonia. Results from laboratory and field studies on responses of fish to varying salinity and their responses increased ammonia will be evaluated, although studies which examine responses to ammonia, in relation to varying salinity, pH and temperature together are rare. In a survey of British estuaries the continuous measurement of total ammonia showed values that ranged from background levels increasing up to c. 10 mg N l^?1 although higher values have been noted sporadically. In outer estuaries pH values tended to stabilize towards sea water values (e.g. c. pH 8). Upper reaches of estuaries are influenced by the quality of their fresh waters sources which can show a wide range of pH and water quality values depending on geological, climatic and pollution conditions. In general the ammonia toxicity (96 h LC₅₀) to marine species (e.g. 0·09–3·35 mg l^?1 NH₃) appears to be roughly similar to freshwater species (e.g. 0·068–2·0 mg l^?1 NH₃). Ammonia toxicity is related to differences between species and pH rather than to the comparatively minor influences of salinity and temperature. In the marine environment the toxicity of ionized ammonia should be considered. The water quality standard for freshwater salmonids of 21 μg l^?1 NH₃–N was considered to be protective for most marine fish and estuarine fish although the influence of cyclical changes in pH, salinity and temperature were not considered. During ammonia exposures, whether chronic or episodic, estuarine fish may be most at risk as larvae or juveniles, at elevated temperatures, if salinity is near the seawater value and if the pH value of the water is decreased. They are also likely to be at risk from ammonia intoxication in waters of low salinity, high pH and high ammonia levels. These conditions are likely to promote ammonia transfer from the environment into the fish, both as ionized and unionized ammonia, as well as promoting ammonia retention by the fish. Fish are more likely to be prone to ammonia toxicity if they are not feeding, are stressed and if they are active and swimming. Episodic or cycling exposures should also be considered in relation to the rate at which the animal is able to accumulate and excrete ammonia and the physiological processes involved in the transfer of ammonia. In the complex environment of an estuary, evaluation of ammonia as a pollutant will involve field and laboratory experiments to determine the responses of fish to ammonia as salinity and temperature vary over a period of time. It will also be necessary to evaluate the responses of a variety of species including estuarine residents and migrants.     

Lateralisation of visual function in yellow-eyed mullet (Aldrichetta forsteri) and its role in schooling behaviour

Lateralisation of cognitive function is a common phenomenon found throughout the animal kingdom. In fish, lateralisation is involved in visually mediated behaviours such as schooling, predator avoidance and foraging. This study sought to quantify visual laterality in yellow-eyed mullet (Aldrichetta forsteri), to determine visual asymmetries and the significance of lateralisation, and the factors which influence functional behaviours in schooling fish. Tank-based experiments investigated individual and population level lateralisation, schooling behaviour, and optic lobe asymmetry. Variation in direction and strength of lateralisation in individuals was found in juveniles, but at a population level significant bias was found in adults. Right eye biased fish had a larger right optic lobe than control fish. Strongly lateralised fish showed a tendency to occupy positions of safety within the school more frequently than control fish. In combination with observed differences in schooling behaviour, the possibility of ontogenetic plasticity in behavioural lateralisation and optic lobe morphology is suggested.