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BEHAVIORAL RESPONSES TO THE ENVIRONMENT | Anthropogenic Influences on Fish Behavior
Anthropogenic Influences on Fish Behavior KA Sloman, University of the West of Scotland, Paisley, Scotland, UK ª 2011 Elsevier Inc. All rights reserved.
Interactions between Physiology and Behavior Disruption of Sensory Information Neurotoxins and Interference with Brain Function Toxicants that Interfere with Respiration
Glossary Acetylcholine A neurotransmitter particularly associated with motor control. Acetylcholinesterase An enzyme that degrades the neurotransmitter acetylcholine. Alarm substance A chemical or group of chemicals released in some species of fish from the skin of injured individuals. Cholinesterase An enzyme (technically a group of enzymes) that degrades acetylcholine and butyrylcholine. Endocrine disruptor An exogenous substance that causes adverse health effects in an organism or its
Interactions between Physiology and Behavior The physiology and behavior of fish are closely related and as such represent a fragile link vulnerable to anthropogenic disturbances. There are a myriad of ways in which humans have altered the aquatic environment, including chemical pollution, acoustic disturbances, physical disturbances, such as habitat destruction, and the release of invasive or transgenic species. The effects of human disturbance on fish behavior and physiology have been most studied in relation to chemical contaminants, including organic pol lutants (e.g., some pesticides; see also Toxicology: The Toxicology of Organics in Fishes), pharmaceuticals, inor ganic pollutants (e.g., metals; see also Toxicology: The Toxicology of Metals in Fishes), and radionuclides. Many types of anthropogenic disturbance target specific physio logical systems and may exert their effects on fish behavior via physiological pathways. The performance of behaviors by individual fish generally follows specific physiological sequences acting as a link between physiological and eco logical processes. Indeed, the use of fish behavior as a sensitive and ecologically relevant tool for monitoring anthropogenic effects in the aquatic environment is widely accepted. This article considers the main ways in which
Reproductive Impairment Future Studies Further Reading
progeny, subsequent to changes in endocrine function. Monoamine neurotransmitter A group of neurotransmitters that contain one amino group in their chemical structure. Neurotransmitters A group of chemicals that are released from nerve endings that transmit information to neighboring cells. Ototoxin A chemical that causes damage to hair cells of the ear or lateral line. Rheotaxis Orientation in a water current; most fish orientate to face into the water current.
human activities are known to affect the fragile link that exists between behavior and physiology, focusing particu larly on the effects of chemical contaminants.
Disruption of Sensory Information Olfaction The sense of smell is a key factor in allowing a fish to gain information about its surrounding environment and to behaviorally respond in an appropriate way. Olfaction is important in a plethora of behaviors. For example, salmo nids rely on their sense of smell to find their way back to natal streams during migration (see also Fish Migrations: The Biology of Fish Migration). Many fish species, when injured by a predator, release a chemical known as ‘alarm substance’ into the water, sending olfactory warning signals to neighboring individuals that there is a predator present (see also Behavioral Responses to the Environment: A Survival Guide for Fishes: How to Obtain Food While Avoiding Being Food). Reproductive pheromones play a vital role in courtship behaviors of many fish species (see also Social and Reproductive Behaviors: Sexual Behavior in Fish and Hormones in Communication: Hormonal Pheromones). Therefore, any chemicals that
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damage or interfere with the olfactory system in fish could disrupt a vast array of behavioral processes. The olfactory system of fish consists of an olfactory rosette in direct contact with the external environment. Receptors in the rosette send information about olfactory stimuli via the olfactory nerve to the olfactory bulb located in the brain (see also Smell, Taste, and Chemical Sensing: Chemoreception (Smell and Taste): An Introduction and Morphology of the Olfactory (Smell) System in Fishes). Direct contact between the olfactory rosette and the environment of the fish can allow damage of the olfactory rosette by waterborne contaminants and some may actually be transported along the olfactory nerve to the brain. In pike, Esox lucius, mercury is transported along olfactory nerves, and, in salmonids (e.g., salmon and trout), cadmium has been found to accumulate in the
olfactory rosette, olfactory nerve, and the anterior part of the olfactory bulb of the brain of fish held in cadmiumcontaminated water, as illustrated in Figure 1. Figure 1(a) shows a cross section through a rainbow trout, Oncorhynchus mykiss, that has been exposed to waterborne radiolabeled cadmium. The olfactory system can be clearly seen. Figure 1(b) shows exactly the same section of fish but viewed using whole body phosphor screen autoradiogra phy, which highlights the areas where radiolabeled cadmium has accumulated. From this, it is possible to see that cadmium has accumulated in the olfactory rosette, olfactory nerve, and olfactory bulb. Accumulation of tox icants in the olfactory rosette may also lead to a decrease in the number of functional receptors. Contaminant accumulation in the olfactory system and the knock-on effects they have on cellular and
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Figure 1 (a) Cross section through a rainbow trout showing a variety of tissues, including the olfactory bulb (OB), the olfactory nerve (ON), and the olfactory rosette (OR). (b) The same cross section of a rainbow trout viewed using phosphor screen autoradiography showing accumulation of radiolabeled cadmium following a waterborne exposure. Reproduced from Scott GR, Sloman KA, Rouleau C, and Wood CM (2003) Cadmium disrupts behavioural and physiological responses to alarm substance in juvenile rainbow trout (Oncorhynchus mykiss). Journal of Experimental Biology 206: 1779–1790, with permission from The Company of Biologists.
Behavioral Responses to the Environment | Anthropogenic Influences on Fish Behavior
physiological processes can ultimately affect the behavior of the fish. Alarm substance is a chemical or group of chemicals that is released when a fish is injured and its skin cells are ruptured. For example, in rainbow trout, individuals will demonstrate freezing behaviors and an overall decrease in activity when alarm substance is added to the water – characteristic behaviors seen in response to a potential predation threat. However, in rainbow trout that have been exposed to waterborne cadmium prior to the addition of alarm substance, no changes in behavior are seen. In contrast, exposure to dietary cadmium does not affect the behavioral response of fish to alarm substance. The effects of waterborne cadmium on the ability of fish to respond to alarm sub stance can be seen at relatively low concentrations that do not cause mortality or major physiological distur bances. However, the inability to detect and respond to alarm substance when a predator is present is a poten tially lethal situation for the fish. Toxicants that interfere with detection of olfactory stimuli can also disrupt other behaviors, including courtship, prey capture, migration, and social interaction.
Mechanoreception The lateral line functions to detect vibrations and water movement and allows fish to orientate themselves in a water current (rheotaxis), gain information about their spatial environment, and also plays a vital role in school ing (see also Hearing and Lateral Line: Lateral Line Structure). The sensory cells within the lateral line are known as hair cells and are also present in the ear. In the lateral line, hair cells are contained in sensory units known as neuromasts. Toxicants that interfere with hair-cell function, therefore, have the potential to disrupt behaviors reliant on hearing and the lateral line. Ototoxins are contaminants known to specifically affect hair-cell function and include the pharmaceuticals such as gentamicin sulfate, streptomycin, and amiloride.
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Trace metals may also interfere with lateral line func tion. For example, banded kokopu (Galaxius fasciatus) exposed to waterborne cadmium show a reduced ability to orientate in a water current. Waterborne copper expo sure in zebrafish larvae reduces the number of functional neuromasts in the lateral line. In control zebrafish larvae, functional neuromasts can be visualized by staining with the fluorescent dye, 2-(4-dimethylaminostyryl)-N-ethyl pyridinium iodide) (DASPEI). Figure 2(a) shows control zebrafish larvae with functional neuromasts running along either side of the body in the lateral line stained with DASPEI. Figure 2(b) shows zebrafish larvae exposed to waterborne copper before staining with DASPEI; a clear reduction in functional neuromasts can be seen. In con sequence, zebrafish larvae exposed to waterborne copper during development have a reduced ability to orientate and maintain their position within a water current. Sound Sound plays a major role in many fish behaviors, includ ing social communication and mating (see also Sensory Systems, Perception, and Learning: How Fishes Use Sound: Quiet to Loud and Simple to Complex Signalling). In species with planktonic dispersal, for example many coral reef fish, sound also plays a vital role in locating a suitable habitat. Studies using artificial reefs with audio recordings of reef sounds have demon strated how important sound is for settlement and habitat choice. In addition to ototoxins that can damage the hair cells of the ear, anthropogenic noise pollution can be problematic for fish although not all noise pollution has been found to have an effect on fish beha vior (see also Hearing and Lateral Line: Effects of Human-Generated Sound on Fish). Marine fish from an inshore reef in Loch Ewe, Scotland, displayed a startle response to deployment of seismic air guns; however, there was little effect on day-to-day behavior of the fish. In the laboratory, initial exposure of Chinook salmon, Oncorhynchus tshawytscha, and rainbow trout to
Figure 2 (a) Control and (b) copper-exposed zebrafish larvae stained with DASPEI illustrating the presence (in (a)) and absence (in (b)) of DASPEI-stained neuromasts. Scale ¼ 0.25 mm. Reproduced from Johnson A, Carew E, and Sloman KA (2007) The effects of copper on the morphological and functional development of zebrafish embryos. Aquatic Toxicology 84: 431–438, with permission from Elsevier.
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10-Hz-frequency sound causes a flight response away from the source; however, upon repeated exposure, this behavior changes to a less-dramatic avoidance response. This kind of sound avoidance by fish is well documen ted. Indeed, sound is often used as a fish repellent. For example, an acoustic deterrent system producing 20– 600 Hz sound resulted in a 60% avoidance of a power station cooling water inlet by estuarine fishes. The clu peiod species, Atlantic herring, Clupea harengus, and European sprat, Sprattus sprattus, were most affected; a characteristic feature of the Clupeidae family is their advanced hearing capacity (see Hearing and Lateral Line: Physiology of the Ear and Brain: How Fish Hear).
Taste Feeding behavior of fish depends on taste with many fish being able to distinguish between different food sources and display food preferences. Fish may also rely on taste to alter their diet in response to environmental change; for example, there may be potential for them to select a highsodium diet, which is known to counteract the toxicity of some trace metals. In yellow bullheads, Ictalurus natali, detergents cause disintegration of taste buds and reduce the ability of individuals to chemically detect food. In catfish, such as yellow bullheads, taste buds, known as barbels, are located on whisker-like projections from the mouth, which are used for probing the sediment and searching for food. Damage to these sensory receptors may reduce the ability of individuals to detect potential prey.
Vision The major anthropogenic influence affecting the vision of fish is increased turbidity through increased suspended material in the water column. Dredging, soil erosion, and sewage output are just a few examples of activities that can increase turbidity. The variety of bright colors utilized by fish indicates the importance of vision in fish communication for a myriad of reasons, including indivi dual recognition and mate attraction (see also Sensory Systems, Perception, and Learning: Communication Behavior: Visual Signals). A reduction in visibility in the surrounding environment can disrupt fish visual commu nication and, in extreme cases, can lead to constraints in color vision. Some toxicants, including methylmercury, may also interfere directly with the eye. Optic nerve function can be affected by the drug ethambutol, which is used to treat tuberculosis, and signal processing in the eye may be disrupted by the herbicide thiobencarb and the insecti cide dichlorodiphenyltrichloroethane (DDT).
Neurotoxins and Interference with Brain Function Neurotransmitters are chemicals that transmit signals both within the nervous system and from the nervous system to other cells. These chemicals play a vital role in many physiological and behavioral processes and, in order to function as reliable signals, they must be effec tively degraded to give the signal a temporal property. Production and breakdown of the neurotransmitter allow transmission of a signal from one cell to another. A vast array of different neurotransmitters exists and several have been closely associated with behavioral patterns. Acetylcholine (ACh) is a neurotransmitter particularly involved with motor coordination and is broken down after release by the enzyme acetylcholinesterase (AChE). Total brain cholinesterase (ChE) activity is often measured as an indicator of AChE activity. Many studies have considered the impact of toxicants on fish brain ChE activity. The insecticides malathion and diazinon are known to inhibit ChE activity, resulting in a buildup of ACh and subsequent effects on motor function. Studies on rainbow trout found that exposure to both of these insecticides resulted in fish swimming shorter dis tances at slower speeds. Other chemicals known to affect ChE activity include the organophosphate insecticides chloropyrifos and fenitrothion and several carbamate pes ticides and herbicides, including thiobencarb and diuron. A group of monoamine chemicals, which includes serotonin (5-hydroxytryptamine, 5-HT) and dopamine, also function as neurotransmitters. These monoamines are associated with the stress response and social beha viors. Elevated concentrations of serotonin and dopamine have been linked to submissive and aggressive behaviors, respectively. Methylmercury, the organochlorine pesti cide lindane, polychlorinated biphenyls (PCBs), and copper can disrupt levels of these monoamines and, there fore, have the potential to impact behaviors associated with these neurotransmitters. Toxicants may also inter fere with brain function through direct damage to brain tissue, including the formation of vacuoles within cell body layers and decreases in antioxidant enzymes, which function to break down free radicals and protect tissues from DNA damage. Disruption of neurotransmitters and damage to brain tissue have many implications for behavior. The vital role of ChE activity in motor control means that chemicals, such as organophosphate pesticides that inhibit ChE activity, have profound effects on the myriad of behaviors that are dependent on locomotion. In particular, the decrease in swimming speeds associated with impaired ChE activity has implications for predator avoidance and prey capture. The escape response in most fish in response to a predatory threat occurs via the Mauthner
Behavioral Responses to the Environment | Anthropogenic Influences on Fish Behavior
system, consisting of two large nerve fibers located on either side of the brainstem with connections to hair cells of the lateral line (see also Brain and Nervous System: Physiology of the Mauthner Cell: Discovery and Properties). Activation of these nerve fibers in response to detecting pressure waves on one side of the body results in a classic reflex response away from the potential predator. This response occurs within milliseconds and is an extremely effective predator-avoidance mechanism. Exposure to the broad-spectrum insecticide, carbaryl or the chemical phenol, affected Mauthner cell function in medaka, Oryzias latipes. Sublethal concentrations of ammonia also affect the fast-start escape response in fish by interfering with the function of the Mauthner cells, and, additionally, by exerting toxic effects on white mus cle. Exposures to sublethal levels of contaminants that impair swimming ability and reduce the effectiveness of the escape response can become lethal situations for the fish if they are unable to escape predation. Likewise, if fish are unable to catch their prey, then sublethal exposure to a toxicant can soon lead to starvation. Neurotoxins are also known to interfere with fish social behavior. Exposure of rainbow trout to the neuro toxic metal, cadmium, decreased their ability to form social hierarchies and socially compete with nonexposed fish. Social hierarchies are known to form among groups of juvenile salmonid fish over resources such as food and shelter (see also Social and Reproductive Behaviors: Dominance Behaviors). The ability to win dominance contests can, therefore, translate into increased food acquisition and better territories. Initial competitions between pairs of juvenile trout often involve chases and bites by each fish, and occasionally mouth fighting until dominance is ascertained. In cadmium-exposed fish, it has been noted that individuals have difficulty making accu rate judgments of the exact location of their competitor, resulting in aggressive chases that fail to make physical contact with their opponent. Consequently, hierarchy formation is either delayed where both competitors have been exposed to this neurotoxin, or cadmium-exposed fish are at a disadvantage when paired with a nonexposed fish.
Toxicants that Interfere with Respiration There are two major ways in which fish gills or respira tory organs come into direct contact with contaminants. Some toxicants dissolve directly in the water column and thus are passed over the gills during ventilation. Other immiscible toxicants, such as oil, form layers on top of the water surface and can be inhaled by fish coming to the water surface to breathe air (Behavioral Responses to the Environment: Behavioral Responses to Hypoxia). Fish coughing has been observed as a general behavioral
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response to many waterborne toxicants. Aluminum is a trace metal that has been particularly associated with respiratory toxicity in fish, causing changes in gill mor phology and impaired respiratory function. Fish exposed to waterborne aluminum reduce metabolically costly fast swimming behavior, suggesting a decrease in respiratory efficiency and, therefore, available energy. Other trace metals that can negatively impact on the energetic capa city of fish include copper and nickel. Many fish species show adaptations to low oxygen levels in the water which involve moving to the water surface either to ventilate their gills in the thin layer of water in immediate contact with the air (aquatic surface respiration) or to actually breathe air (see Behavioral Responses to the Environment: Behavioral Responses to Hypoxia). When a contaminant forms a thin layer on the water surface, such as in the case of oil spills, there can be severe consequences for fish that rely on access to the water surface. Some fish, such as the piraracu, Arapaima gigas, are obligate air breathers and will die when denied access to air, regardless of levels of dissolved oxygen in the water. These fish are particularly susceptible to pol lutants, such as oil, which can enter their air-breathing organs causing respiratory distress and suffocation.
Reproductive Impairment Research into the effects of contaminants on fish repro duction has focused in recent years on compounds that can act as endocrine disruptors. An endocrine disruptor is an exogenous substance that causes adverse health effects in an organism or its progeny subsequent to alterations in endocrine function. Many endocrine disruptors mimic endogenous hormones, while others may interfere with the production of endogenous hormones or block their effects. In particular, a vast array of estrogenic endocrine disruptors have been identified, chemicals that mimic the natural hormone estrogen with potentially more potent effects. Androgenic endocrine disruptors also exist along with known anti-androgens and anti-estrogens that inter fere with the functioning or production of male or female hormones, respectively. Estrogenic chemicals, such as nonylphenol, used as a surfactant in detergents, bisphenol A, an important com ponent of many plastics and the synthetic estrogen found in the contraceptive pill, ethinyl estradiol, are known to have feminizing effects in many fish species. Natural estrogenic chemicals, known as phytoestrogens, are found in some plant species and may be released into the environment through pulp and paper-mill processing. Male fish exposed to these compounds in the water may develop intersex reproductive organs that demonstrate the characteristics of both testes and ovaries. A commonly used indicator of estrogenic exposure in male fish is the
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production of vitellogenin, an egg-yolk precursor protein. Vitellogenin is normally only produced in female fish where high concentrations of the female hormone estro gen cause the liver to produce vitellogenin, which is then transported in the blood stream to the ovaries and pack aged into eggs. Synthetic estrogens have the capacity to induce a similar effect in male fish, resulting in unchar acteristically high levels of plasma vitellogenin. Exposure to these feminizing chemicals also has the potential to alter male reproductive behavior. Effects of endocrine disruptors on reproductive behavior have been particularly studied in fathead minnows, Pimephales promelas. Reproductively mature male fathead minnows develop secondary sexual characteristics, such as a fat pad on their head and tubercles on their snout, which aid in attracting a mate. Following courtship behaviors, these fish form pairs, and the female lays eggs, which the male then fertilizes. Exposure to estrogenic chemicals, such as nonylphenol, has been shown to reduce fat-pad size and the number of face tubercles in male fathead minnows, reducing their chances of attracting a mate and success fully reproducing. In three-spined sticklebacks, Gasterosteus aculeatus, males build a nest to attract a female to lay eggs in and use elaborate courtship behaviors to attract females to their nest (see Social and Reproductive Behaviors: Sexual Behavior in Fish). Exposure to estrogenic endocrine-disrupting chemicals has been shown to reduce courtship success and nest building behavior in male sticklebacks. Other pollutants may interfere with reproductive behavior without necessarily disrupting endocrine function. Many fish use sexual pheromones to attract mates (see Hormones in Communication: Hormonal Pheromones). As mentioned previously, there are many chemicals that can interfere with olfactory function and thus disrupt courtship behaviors that depend on olfac tory cues. For example, female Atlantic salmon, Salmo salar, release prostaglandin F2� as an olfactory cue that has a priming influence on males, resulting in eleva tions of male hormones and sperm availability. Exposure of male Atlantic salmon to many insecticides and pesticides, including carbofuran, atrazine, cyperme thrin, and diazinon, reduces the ability of males to detect prostaglandin F2� and, therefore, their ability to beha viorally and physiologically respond to female cues.
Future Studies The ways in which human activity can and has disrupted the fragile link that exists between fish behavior and phy siology are vast and, here, I have only scraped the surface of the detrimental effects that we know we have exerted on fish biology. However, there are many areas where we are still lacking in knowledge. For example, a plethora of
research has focused on chemicals that interfere with the functioning of reproductive hormones but little considered are chemicals that might interfere with other hormonal systems, such as stress hormones and thyroid hormones. Many fish species undergo sex change during their life history (see Social and Reproductive Behaviors: Socially Controlled Sex Change in Fishes), what impacts do estrogenic or androgenic chemicals have on this process? Also lacking is our understanding of how laboratory toxicity studies translate into field exposures. For example, labora tory exposure to toxicants can affect the ability to both detect predators and forage for food. In the field, these behaviors do not occur in isolation and it is likely that both prey and predator will be exposed to toxicants at the same time. It is imperative that we continue to strive to understand the anthropogenic influences on fish behavior and physiology and to add ecological relevance to our understanding of these issues.
See also: Behavioral Responses to the Environment: A Survival Guide for Fishes: How to Obtain Food While Avoiding Being Food; Behavioral Responses to Hypoxia. Brain and Nervous System: Physiology of the Mauthner Cell: Discovery and Properties. Fish Migrations: The Biology of Fish Migration. Hearing and Lateral Line: Effects of Human-Generated Sound on Fish; Lateral Line Structure; Physiology of the Ear and Brain: How Fish Hear. Hormones in Communication: Hormonal Pheromones. Sensory Systems, Perception, and Learning: Communication Behavior: Visual Signals; How Fishes Use Sound: Quiet to Loud and Simple to Complex Signalling. Smell, Taste, and Chemical Sensing: Chemoreception (Smell and Taste): An Introduction; Morphology of the Olfactory (Smell) System in Fishes. Social and Reproductive Behaviors: Dominance Behaviors; Sexual Behavior in Fish; Socially Controlled Sex Change in Fishes. Toxicology: The Toxicology of Metals in Fishes; The Toxicology of Organics in Fishes.
Further Reading Abrahams M (2006) The physiology of antipredator behavior: What you do with what you’ve got. In: Sloman KA, Wilson RW, and Balshine S (eds.) Behaviour and Physiology of Fish, 1st edn., vol. 24, pp. 79–108. San Diego, CA: Elsevier. Allin CJ and Wilson RW (1999) Behavioural and metabolic effects of chronic exposure to sublethal aluminium in acidic soft water in juvenile rainbow trout (Oncorhynchus mykiss). Canadian Journal of Fisheries and Aquatic Sciences 56: 670–678. Baker CF and Montgomery JC (2001) Sensory deficits induced by cadmium in banded kokopu, Galaxias fasciatus, juveniles. Environmental Biology of Fishes 62: 455–464. Bardach JE, Fujiya M, and Holl A (1965) Detergents: Effects on the chemical senses of the fish Ictalurus natalis (le Sueur). Science 148: 1605–1607. Borg-Neczak K and Tjalve H (1996) Uptake of 203Hg2þ in the olfactory system in pike. Toxicology Letters 84: 107–112.
Behavioral Responses to the Environment | Anthropogenic Influences on Fish Behavior Brewer SK, Little EE, De Lonay AJ, et al. (2001) Behavioural dysfunctions correlate to altered physiology in rainbow trout (Oncorhynchus mykiss) exposed to cholinesterase-inhibiting chemicals. Archives of Environmental Contamination and Toxicology 40: 70–76. De Boeck G, Nilsson GE, Elofsson U, Vlaeminck A, and Blust R (1995) Brain monoamine levels and energy status in common carp (Cyprinus carpio) after exposure to sublethal levels of copper. Aquatic Toxicology 33: 265–277. Harries JE, Runnalls T, Hill E, et al. (2000) Development of a reproductive performance test for endocrine disrupting chemicals using pairbreeding fathead minnows (Pimephales promelas). Environmental Science and Technology 34: 3003–3011. Johnson A, Carew E, and Sloman KA (2007) The effects of copper on the morphological and functional development of zebrafish embryos. Aquatic Toxicology 84: 431–438. Knudsen FR, Schreck CB, Knapp SM, Enger PS, and Sand O (1997) Infrasound produces flight and avoidance responses in Pacific juvenile salmonids. Journal of Fish Biology 51: 824–829. Maes J, Turnpenny AWH, Lambert DR, et al. (2004) Field evaluation of a sound system to reduce estuarine fish intake rates at a power plant cooling water inlet. Journal of Fish Biology 64: 938–946. McKenzie DJ, Shingles A, Claireaux G, and Domenici P (2009) Sublethal concentrations of ammonia impair performance of the teleost faststart escape response. Physiological and Biochemical Zoology 82: 353–362.
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Moore A and Waring CP (1996) Sublethal effects of the pesticide Diazinon on olfactory function in mature male Atlantic salmon parr. Journal of Fish Biology 48: 758–775. Niyogi S, Kamunde CN, and Wood CM (2006) Food selection, growth and physiology in relation to dietary sodium chloride content in rainbow trout (Oncorhynchus mykiss) under chronic waterborne Cu exposure. Aquatic Toxicology 77: 210–221. Scott GR and Sloman KA (2004) The effects of environmental pollutants on complex fish behaviour: Integrating behavioural and physiological indicators of toxicity. Aquatic Toxicology 68: 369–392. Scott GR, Sloman KA, Rouleau C, and Wood CM (2003) Cadmium disrupts behavioural and physiological responses to alarm substance in juvenile rainbow trout (Oncorhynchus mykiss). Journal of Experimental Biology 206: 1779–1790. Sloman KA (2007) Effects of trace metals on salmonid fish: The role of social hierarchies. Applied Animal Behaviour Science 104: 326–345. Sloman KA, Scott GR, Diao Z, et al. (2003) Cadmium affects the social behaviour of rainbow trout, Oncorhynchus mykiss. Aquatic Toxicology 65: 171–185. Sloman KA and Wilson RW (2006) Anthropogenic impacts upon behaviour and physiology. In: Sloman KA, Wilson RW, and Balshine S (eds.) 1st edn., Behaviour and Physiology of Fish, vol. 24, pp. 413–468. San Diego, CA: Elsevier. Wardle CS, Carter TJ, Urquhart GG, et al. (2001) Effects of seismic air guns on marine fish. Continental Shelf Research 21: 1005–1027.
Interactions between Physiology and Behavior Disruption of Sensory Information Neurotoxins and Interference with Brain Function Toxicants that Interfere with Respiration
Glossary Acetylcholine A neurotransmitter particularly associated with motor control. Acetylcholinesterase An enzyme that degrades the neurotransmitter acetylcholine. Alarm substance A chemical or group of chemicals released in some species of fish from the skin of injured individuals. Cholinesterase An enzyme (technically a group of enzymes) that degrades acetylcholine and butyrylcholine. Endocrine disruptor An exogenous substance that causes adverse health effects in an organism or its
Interactions between Physiology and Behavior The physiology and behavior of fish are closely related and as such represent a fragile link vulnerable to anthropogenic disturbances. There are a myriad of ways in which humans have altered the aquatic environment, including chemical pollution, acoustic disturbances, physical disturbances, such as habitat destruction, and the release of invasive or transgenic species. The effects of human disturbance on fish behavior and physiology have been most studied in relation to chemical contaminants, including organic pol lutants (e.g., some pesticides; see also Toxicology: The Toxicology of Organics in Fishes), pharmaceuticals, inor ganic pollutants (e.g., metals; see also Toxicology: The Toxicology of Metals in Fishes), and radionuclides. Many types of anthropogenic disturbance target specific physio logical systems and may exert their effects on fish behavior via physiological pathways. The performance of behaviors by individual fish generally follows specific physiological sequences acting as a link between physiological and eco logical processes. Indeed, the use of fish behavior as a sensitive and ecologically relevant tool for monitoring anthropogenic effects in the aquatic environment is widely accepted. This article considers the main ways in which
Reproductive Impairment Future Studies Further Reading
progeny, subsequent to changes in endocrine function. Monoamine neurotransmitter A group of neurotransmitters that contain one amino group in their chemical structure. Neurotransmitters A group of chemicals that are released from nerve endings that transmit information to neighboring cells. Ototoxin A chemical that causes damage to hair cells of the ear or lateral line. Rheotaxis Orientation in a water current; most fish orientate to face into the water current.
human activities are known to affect the fragile link that exists between behavior and physiology, focusing particu larly on the effects of chemical contaminants.
Disruption of Sensory Information Olfaction The sense of smell is a key factor in allowing a fish to gain information about its surrounding environment and to behaviorally respond in an appropriate way. Olfaction is important in a plethora of behaviors. For example, salmo nids rely on their sense of smell to find their way back to natal streams during migration (see also Fish Migrations: The Biology of Fish Migration). Many fish species, when injured by a predator, release a chemical known as ‘alarm substance’ into the water, sending olfactory warning signals to neighboring individuals that there is a predator present (see also Behavioral Responses to the Environment: A Survival Guide for Fishes: How to Obtain Food While Avoiding Being Food). Reproductive pheromones play a vital role in courtship behaviors of many fish species (see also Social and Reproductive Behaviors: Sexual Behavior in Fish and Hormones in Communication: Hormonal Pheromones). Therefore, any chemicals that
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damage or interfere with the olfactory system in fish could disrupt a vast array of behavioral processes. The olfactory system of fish consists of an olfactory rosette in direct contact with the external environment. Receptors in the rosette send information about olfactory stimuli via the olfactory nerve to the olfactory bulb located in the brain (see also Smell, Taste, and Chemical Sensing: Chemoreception (Smell and Taste): An Introduction and Morphology of the Olfactory (Smell) System in Fishes). Direct contact between the olfactory rosette and the environment of the fish can allow damage of the olfactory rosette by waterborne contaminants and some may actually be transported along the olfactory nerve to the brain. In pike, Esox lucius, mercury is transported along olfactory nerves, and, in salmonids (e.g., salmon and trout), cadmium has been found to accumulate in the
olfactory rosette, olfactory nerve, and the anterior part of the olfactory bulb of the brain of fish held in cadmiumcontaminated water, as illustrated in Figure 1. Figure 1(a) shows a cross section through a rainbow trout, Oncorhynchus mykiss, that has been exposed to waterborne radiolabeled cadmium. The olfactory system can be clearly seen. Figure 1(b) shows exactly the same section of fish but viewed using whole body phosphor screen autoradiogra phy, which highlights the areas where radiolabeled cadmium has accumulated. From this, it is possible to see that cadmium has accumulated in the olfactory rosette, olfactory nerve, and olfactory bulb. Accumulation of tox icants in the olfactory rosette may also lead to a decrease in the number of functional receptors. Contaminant accumulation in the olfactory system and the knock-on effects they have on cellular and
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Figure 1 (a) Cross section through a rainbow trout showing a variety of tissues, including the olfactory bulb (OB), the olfactory nerve (ON), and the olfactory rosette (OR). (b) The same cross section of a rainbow trout viewed using phosphor screen autoradiography showing accumulation of radiolabeled cadmium following a waterborne exposure. Reproduced from Scott GR, Sloman KA, Rouleau C, and Wood CM (2003) Cadmium disrupts behavioural and physiological responses to alarm substance in juvenile rainbow trout (Oncorhynchus mykiss). Journal of Experimental Biology 206: 1779–1790, with permission from The Company of Biologists.
Behavioral Responses to the Environment | Anthropogenic Influences on Fish Behavior
physiological processes can ultimately affect the behavior of the fish. Alarm substance is a chemical or group of chemicals that is released when a fish is injured and its skin cells are ruptured. For example, in rainbow trout, individuals will demonstrate freezing behaviors and an overall decrease in activity when alarm substance is added to the water – characteristic behaviors seen in response to a potential predation threat. However, in rainbow trout that have been exposed to waterborne cadmium prior to the addition of alarm substance, no changes in behavior are seen. In contrast, exposure to dietary cadmium does not affect the behavioral response of fish to alarm substance. The effects of waterborne cadmium on the ability of fish to respond to alarm sub stance can be seen at relatively low concentrations that do not cause mortality or major physiological distur bances. However, the inability to detect and respond to alarm substance when a predator is present is a poten tially lethal situation for the fish. Toxicants that interfere with detection of olfactory stimuli can also disrupt other behaviors, including courtship, prey capture, migration, and social interaction.
Mechanoreception The lateral line functions to detect vibrations and water movement and allows fish to orientate themselves in a water current (rheotaxis), gain information about their spatial environment, and also plays a vital role in school ing (see also Hearing and Lateral Line: Lateral Line Structure). The sensory cells within the lateral line are known as hair cells and are also present in the ear. In the lateral line, hair cells are contained in sensory units known as neuromasts. Toxicants that interfere with hair-cell function, therefore, have the potential to disrupt behaviors reliant on hearing and the lateral line. Ototoxins are contaminants known to specifically affect hair-cell function and include the pharmaceuticals such as gentamicin sulfate, streptomycin, and amiloride.
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Trace metals may also interfere with lateral line func tion. For example, banded kokopu (Galaxius fasciatus) exposed to waterborne cadmium show a reduced ability to orientate in a water current. Waterborne copper expo sure in zebrafish larvae reduces the number of functional neuromasts in the lateral line. In control zebrafish larvae, functional neuromasts can be visualized by staining with the fluorescent dye, 2-(4-dimethylaminostyryl)-N-ethyl pyridinium iodide) (DASPEI). Figure 2(a) shows control zebrafish larvae with functional neuromasts running along either side of the body in the lateral line stained with DASPEI. Figure 2(b) shows zebrafish larvae exposed to waterborne copper before staining with DASPEI; a clear reduction in functional neuromasts can be seen. In con sequence, zebrafish larvae exposed to waterborne copper during development have a reduced ability to orientate and maintain their position within a water current. Sound Sound plays a major role in many fish behaviors, includ ing social communication and mating (see also Sensory Systems, Perception, and Learning: How Fishes Use Sound: Quiet to Loud and Simple to Complex Signalling). In species with planktonic dispersal, for example many coral reef fish, sound also plays a vital role in locating a suitable habitat. Studies using artificial reefs with audio recordings of reef sounds have demon strated how important sound is for settlement and habitat choice. In addition to ototoxins that can damage the hair cells of the ear, anthropogenic noise pollution can be problematic for fish although not all noise pollution has been found to have an effect on fish beha vior (see also Hearing and Lateral Line: Effects of Human-Generated Sound on Fish). Marine fish from an inshore reef in Loch Ewe, Scotland, displayed a startle response to deployment of seismic air guns; however, there was little effect on day-to-day behavior of the fish. In the laboratory, initial exposure of Chinook salmon, Oncorhynchus tshawytscha, and rainbow trout to
Figure 2 (a) Control and (b) copper-exposed zebrafish larvae stained with DASPEI illustrating the presence (in (a)) and absence (in (b)) of DASPEI-stained neuromasts. Scale ¼ 0.25 mm. Reproduced from Johnson A, Carew E, and Sloman KA (2007) The effects of copper on the morphological and functional development of zebrafish embryos. Aquatic Toxicology 84: 431–438, with permission from Elsevier.
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10-Hz-frequency sound causes a flight response away from the source; however, upon repeated exposure, this behavior changes to a less-dramatic avoidance response. This kind of sound avoidance by fish is well documen ted. Indeed, sound is often used as a fish repellent. For example, an acoustic deterrent system producing 20– 600 Hz sound resulted in a 60% avoidance of a power station cooling water inlet by estuarine fishes. The clu peiod species, Atlantic herring, Clupea harengus, and European sprat, Sprattus sprattus, were most affected; a characteristic feature of the Clupeidae family is their advanced hearing capacity (see Hearing and Lateral Line: Physiology of the Ear and Brain: How Fish Hear).
Taste Feeding behavior of fish depends on taste with many fish being able to distinguish between different food sources and display food preferences. Fish may also rely on taste to alter their diet in response to environmental change; for example, there may be potential for them to select a highsodium diet, which is known to counteract the toxicity of some trace metals. In yellow bullheads, Ictalurus natali, detergents cause disintegration of taste buds and reduce the ability of individuals to chemically detect food. In catfish, such as yellow bullheads, taste buds, known as barbels, are located on whisker-like projections from the mouth, which are used for probing the sediment and searching for food. Damage to these sensory receptors may reduce the ability of individuals to detect potential prey.
Vision The major anthropogenic influence affecting the vision of fish is increased turbidity through increased suspended material in the water column. Dredging, soil erosion, and sewage output are just a few examples of activities that can increase turbidity. The variety of bright colors utilized by fish indicates the importance of vision in fish communication for a myriad of reasons, including indivi dual recognition and mate attraction (see also Sensory Systems, Perception, and Learning: Communication Behavior: Visual Signals). A reduction in visibility in the surrounding environment can disrupt fish visual commu nication and, in extreme cases, can lead to constraints in color vision. Some toxicants, including methylmercury, may also interfere directly with the eye. Optic nerve function can be affected by the drug ethambutol, which is used to treat tuberculosis, and signal processing in the eye may be disrupted by the herbicide thiobencarb and the insecti cide dichlorodiphenyltrichloroethane (DDT).
Neurotoxins and Interference with Brain Function Neurotransmitters are chemicals that transmit signals both within the nervous system and from the nervous system to other cells. These chemicals play a vital role in many physiological and behavioral processes and, in order to function as reliable signals, they must be effec tively degraded to give the signal a temporal property. Production and breakdown of the neurotransmitter allow transmission of a signal from one cell to another. A vast array of different neurotransmitters exists and several have been closely associated with behavioral patterns. Acetylcholine (ACh) is a neurotransmitter particularly involved with motor coordination and is broken down after release by the enzyme acetylcholinesterase (AChE). Total brain cholinesterase (ChE) activity is often measured as an indicator of AChE activity. Many studies have considered the impact of toxicants on fish brain ChE activity. The insecticides malathion and diazinon are known to inhibit ChE activity, resulting in a buildup of ACh and subsequent effects on motor function. Studies on rainbow trout found that exposure to both of these insecticides resulted in fish swimming shorter dis tances at slower speeds. Other chemicals known to affect ChE activity include the organophosphate insecticides chloropyrifos and fenitrothion and several carbamate pes ticides and herbicides, including thiobencarb and diuron. A group of monoamine chemicals, which includes serotonin (5-hydroxytryptamine, 5-HT) and dopamine, also function as neurotransmitters. These monoamines are associated with the stress response and social beha viors. Elevated concentrations of serotonin and dopamine have been linked to submissive and aggressive behaviors, respectively. Methylmercury, the organochlorine pesti cide lindane, polychlorinated biphenyls (PCBs), and copper can disrupt levels of these monoamines and, there fore, have the potential to impact behaviors associated with these neurotransmitters. Toxicants may also inter fere with brain function through direct damage to brain tissue, including the formation of vacuoles within cell body layers and decreases in antioxidant enzymes, which function to break down free radicals and protect tissues from DNA damage. Disruption of neurotransmitters and damage to brain tissue have many implications for behavior. The vital role of ChE activity in motor control means that chemicals, such as organophosphate pesticides that inhibit ChE activity, have profound effects on the myriad of behaviors that are dependent on locomotion. In particular, the decrease in swimming speeds associated with impaired ChE activity has implications for predator avoidance and prey capture. The escape response in most fish in response to a predatory threat occurs via the Mauthner
Behavioral Responses to the Environment | Anthropogenic Influences on Fish Behavior
system, consisting of two large nerve fibers located on either side of the brainstem with connections to hair cells of the lateral line (see also Brain and Nervous System: Physiology of the Mauthner Cell: Discovery and Properties). Activation of these nerve fibers in response to detecting pressure waves on one side of the body results in a classic reflex response away from the potential predator. This response occurs within milliseconds and is an extremely effective predator-avoidance mechanism. Exposure to the broad-spectrum insecticide, carbaryl or the chemical phenol, affected Mauthner cell function in medaka, Oryzias latipes. Sublethal concentrations of ammonia also affect the fast-start escape response in fish by interfering with the function of the Mauthner cells, and, additionally, by exerting toxic effects on white mus cle. Exposures to sublethal levels of contaminants that impair swimming ability and reduce the effectiveness of the escape response can become lethal situations for the fish if they are unable to escape predation. Likewise, if fish are unable to catch their prey, then sublethal exposure to a toxicant can soon lead to starvation. Neurotoxins are also known to interfere with fish social behavior. Exposure of rainbow trout to the neuro toxic metal, cadmium, decreased their ability to form social hierarchies and socially compete with nonexposed fish. Social hierarchies are known to form among groups of juvenile salmonid fish over resources such as food and shelter (see also Social and Reproductive Behaviors: Dominance Behaviors). The ability to win dominance contests can, therefore, translate into increased food acquisition and better territories. Initial competitions between pairs of juvenile trout often involve chases and bites by each fish, and occasionally mouth fighting until dominance is ascertained. In cadmium-exposed fish, it has been noted that individuals have difficulty making accu rate judgments of the exact location of their competitor, resulting in aggressive chases that fail to make physical contact with their opponent. Consequently, hierarchy formation is either delayed where both competitors have been exposed to this neurotoxin, or cadmium-exposed fish are at a disadvantage when paired with a nonexposed fish.
Toxicants that Interfere with Respiration There are two major ways in which fish gills or respira tory organs come into direct contact with contaminants. Some toxicants dissolve directly in the water column and thus are passed over the gills during ventilation. Other immiscible toxicants, such as oil, form layers on top of the water surface and can be inhaled by fish coming to the water surface to breathe air (Behavioral Responses to the Environment: Behavioral Responses to Hypoxia). Fish coughing has been observed as a general behavioral
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response to many waterborne toxicants. Aluminum is a trace metal that has been particularly associated with respiratory toxicity in fish, causing changes in gill mor phology and impaired respiratory function. Fish exposed to waterborne aluminum reduce metabolically costly fast swimming behavior, suggesting a decrease in respiratory efficiency and, therefore, available energy. Other trace metals that can negatively impact on the energetic capa city of fish include copper and nickel. Many fish species show adaptations to low oxygen levels in the water which involve moving to the water surface either to ventilate their gills in the thin layer of water in immediate contact with the air (aquatic surface respiration) or to actually breathe air (see Behavioral Responses to the Environment: Behavioral Responses to Hypoxia). When a contaminant forms a thin layer on the water surface, such as in the case of oil spills, there can be severe consequences for fish that rely on access to the water surface. Some fish, such as the piraracu, Arapaima gigas, are obligate air breathers and will die when denied access to air, regardless of levels of dissolved oxygen in the water. These fish are particularly susceptible to pol lutants, such as oil, which can enter their air-breathing organs causing respiratory distress and suffocation.
Reproductive Impairment Research into the effects of contaminants on fish repro duction has focused in recent years on compounds that can act as endocrine disruptors. An endocrine disruptor is an exogenous substance that causes adverse health effects in an organism or its progeny subsequent to alterations in endocrine function. Many endocrine disruptors mimic endogenous hormones, while others may interfere with the production of endogenous hormones or block their effects. In particular, a vast array of estrogenic endocrine disruptors have been identified, chemicals that mimic the natural hormone estrogen with potentially more potent effects. Androgenic endocrine disruptors also exist along with known anti-androgens and anti-estrogens that inter fere with the functioning or production of male or female hormones, respectively. Estrogenic chemicals, such as nonylphenol, used as a surfactant in detergents, bisphenol A, an important com ponent of many plastics and the synthetic estrogen found in the contraceptive pill, ethinyl estradiol, are known to have feminizing effects in many fish species. Natural estrogenic chemicals, known as phytoestrogens, are found in some plant species and may be released into the environment through pulp and paper-mill processing. Male fish exposed to these compounds in the water may develop intersex reproductive organs that demonstrate the characteristics of both testes and ovaries. A commonly used indicator of estrogenic exposure in male fish is the
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production of vitellogenin, an egg-yolk precursor protein. Vitellogenin is normally only produced in female fish where high concentrations of the female hormone estro gen cause the liver to produce vitellogenin, which is then transported in the blood stream to the ovaries and pack aged into eggs. Synthetic estrogens have the capacity to induce a similar effect in male fish, resulting in unchar acteristically high levels of plasma vitellogenin. Exposure to these feminizing chemicals also has the potential to alter male reproductive behavior. Effects of endocrine disruptors on reproductive behavior have been particularly studied in fathead minnows, Pimephales promelas. Reproductively mature male fathead minnows develop secondary sexual characteristics, such as a fat pad on their head and tubercles on their snout, which aid in attracting a mate. Following courtship behaviors, these fish form pairs, and the female lays eggs, which the male then fertilizes. Exposure to estrogenic chemicals, such as nonylphenol, has been shown to reduce fat-pad size and the number of face tubercles in male fathead minnows, reducing their chances of attracting a mate and success fully reproducing. In three-spined sticklebacks, Gasterosteus aculeatus, males build a nest to attract a female to lay eggs in and use elaborate courtship behaviors to attract females to their nest (see Social and Reproductive Behaviors: Sexual Behavior in Fish). Exposure to estrogenic endocrine-disrupting chemicals has been shown to reduce courtship success and nest building behavior in male sticklebacks. Other pollutants may interfere with reproductive behavior without necessarily disrupting endocrine function. Many fish use sexual pheromones to attract mates (see Hormones in Communication: Hormonal Pheromones). As mentioned previously, there are many chemicals that can interfere with olfactory function and thus disrupt courtship behaviors that depend on olfac tory cues. For example, female Atlantic salmon, Salmo salar, release prostaglandin F2� as an olfactory cue that has a priming influence on males, resulting in eleva tions of male hormones and sperm availability. Exposure of male Atlantic salmon to many insecticides and pesticides, including carbofuran, atrazine, cyperme thrin, and diazinon, reduces the ability of males to detect prostaglandin F2� and, therefore, their ability to beha viorally and physiologically respond to female cues.
Future Studies The ways in which human activity can and has disrupted the fragile link that exists between fish behavior and phy siology are vast and, here, I have only scraped the surface of the detrimental effects that we know we have exerted on fish biology. However, there are many areas where we are still lacking in knowledge. For example, a plethora of
research has focused on chemicals that interfere with the functioning of reproductive hormones but little considered are chemicals that might interfere with other hormonal systems, such as stress hormones and thyroid hormones. Many fish species undergo sex change during their life history (see Social and Reproductive Behaviors: Socially Controlled Sex Change in Fishes), what impacts do estrogenic or androgenic chemicals have on this process? Also lacking is our understanding of how laboratory toxicity studies translate into field exposures. For example, labora tory exposure to toxicants can affect the ability to both detect predators and forage for food. In the field, these behaviors do not occur in isolation and it is likely that both prey and predator will be exposed to toxicants at the same time. It is imperative that we continue to strive to understand the anthropogenic influences on fish behavior and physiology and to add ecological relevance to our understanding of these issues.
See also: Behavioral Responses to the Environment: A Survival Guide for Fishes: How to Obtain Food While Avoiding Being Food; Behavioral Responses to Hypoxia. Brain and Nervous System: Physiology of the Mauthner Cell: Discovery and Properties. Fish Migrations: The Biology of Fish Migration. Hearing and Lateral Line: Effects of Human-Generated Sound on Fish; Lateral Line Structure; Physiology of the Ear and Brain: How Fish Hear. Hormones in Communication: Hormonal Pheromones. Sensory Systems, Perception, and Learning: Communication Behavior: Visual Signals; How Fishes Use Sound: Quiet to Loud and Simple to Complex Signalling. Smell, Taste, and Chemical Sensing: Chemoreception (Smell and Taste): An Introduction; Morphology of the Olfactory (Smell) System in Fishes. Social and Reproductive Behaviors: Dominance Behaviors; Sexual Behavior in Fish; Socially Controlled Sex Change in Fishes. Toxicology: The Toxicology of Metals in Fishes; The Toxicology of Organics in Fishes.
Further Reading Abrahams M (2006) The physiology of antipredator behavior: What you do with what you’ve got. In: Sloman KA, Wilson RW, and Balshine S (eds.) Behaviour and Physiology of Fish, 1st edn., vol. 24, pp. 79–108. San Diego, CA: Elsevier. Allin CJ and Wilson RW (1999) Behavioural and metabolic effects of chronic exposure to sublethal aluminium in acidic soft water in juvenile rainbow trout (Oncorhynchus mykiss). Canadian Journal of Fisheries and Aquatic Sciences 56: 670–678. Baker CF and Montgomery JC (2001) Sensory deficits induced by cadmium in banded kokopu, Galaxias fasciatus, juveniles. Environmental Biology of Fishes 62: 455–464. Bardach JE, Fujiya M, and Holl A (1965) Detergents: Effects on the chemical senses of the fish Ictalurus natalis (le Sueur). Science 148: 1605–1607. Borg-Neczak K and Tjalve H (1996) Uptake of 203Hg2þ in the olfactory system in pike. Toxicology Letters 84: 107–112.
Behavioral Responses to the Environment | Anthropogenic Influences on Fish Behavior Brewer SK, Little EE, De Lonay AJ, et al. (2001) Behavioural dysfunctions correlate to altered physiology in rainbow trout (Oncorhynchus mykiss) exposed to cholinesterase-inhibiting chemicals. Archives of Environmental Contamination and Toxicology 40: 70–76. De Boeck G, Nilsson GE, Elofsson U, Vlaeminck A, and Blust R (1995) Brain monoamine levels and energy status in common carp (Cyprinus carpio) after exposure to sublethal levels of copper. Aquatic Toxicology 33: 265–277. Harries JE, Runnalls T, Hill E, et al. (2000) Development of a reproductive performance test for endocrine disrupting chemicals using pairbreeding fathead minnows (Pimephales promelas). Environmental Science and Technology 34: 3003–3011. Johnson A, Carew E, and Sloman KA (2007) The effects of copper on the morphological and functional development of zebrafish embryos. Aquatic Toxicology 84: 431–438. Knudsen FR, Schreck CB, Knapp SM, Enger PS, and Sand O (1997) Infrasound produces flight and avoidance responses in Pacific juvenile salmonids. Journal of Fish Biology 51: 824–829. Maes J, Turnpenny AWH, Lambert DR, et al. (2004) Field evaluation of a sound system to reduce estuarine fish intake rates at a power plant cooling water inlet. Journal of Fish Biology 64: 938–946. McKenzie DJ, Shingles A, Claireaux G, and Domenici P (2009) Sublethal concentrations of ammonia impair performance of the teleost faststart escape response. Physiological and Biochemical Zoology 82: 353–362.
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Moore A and Waring CP (1996) Sublethal effects of the pesticide Diazinon on olfactory function in mature male Atlantic salmon parr. Journal of Fish Biology 48: 758–775. Niyogi S, Kamunde CN, and Wood CM (2006) Food selection, growth and physiology in relation to dietary sodium chloride content in rainbow trout (Oncorhynchus mykiss) under chronic waterborne Cu exposure. Aquatic Toxicology 77: 210–221. Scott GR and Sloman KA (2004) The effects of environmental pollutants on complex fish behaviour: Integrating behavioural and physiological indicators of toxicity. Aquatic Toxicology 68: 369–392. Scott GR, Sloman KA, Rouleau C, and Wood CM (2003) Cadmium disrupts behavioural and physiological responses to alarm substance in juvenile rainbow trout (Oncorhynchus mykiss). Journal of Experimental Biology 206: 1779–1790. Sloman KA (2007) Effects of trace metals on salmonid fish: The role of social hierarchies. Applied Animal Behaviour Science 104: 326–345. Sloman KA, Scott GR, Diao Z, et al. (2003) Cadmium affects the social behaviour of rainbow trout, Oncorhynchus mykiss. Aquatic Toxicology 65: 171–185. Sloman KA and Wilson RW (2006) Anthropogenic impacts upon behaviour and physiology. In: Sloman KA, Wilson RW, and Balshine S (eds.) 1st edn., Behaviour and Physiology of Fish, vol. 24, pp. 413–468. San Diego, CA: Elsevier. Wardle CS, Carter TJ, Urquhart GG, et al. (2001) Effects of seismic air guns on marine fish. Continental Shelf Research 21: 1005–1027.