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BEHAVIORAL RESPONSES TO THE ENVIRONMENT | Effects of Compensatory Growth on Fish Behavior
Effects of Compensatory Growth on Fish Behavior D A´lvarez, Universidad de Oviedo, Oviedo, Spain ª 2011 Elsevier Inc. All rights reserved.
Introduction Behavioral Changes during Compensation Deferred Costs of Compensatory Growth
Glossary Compensatory growth A faster-than-normal growth that some species exhibit after a period of resource deprivation. Dominance The state of being dominant where dominant individuals obtain a high status within a social group. Hormone A chemical substance, often a peptide or steroid, released from endocrine glands that controls and regulates a range of physiological activities.
Introduction Fish are capable of reacting after a period of resource depri vation by increasing their growth rates to higher-than normal levels. This implies that animals under normal con ditions are growing at a rate below their physiological potential and therefore they are able, to some extent, to adjust their growth. The main question regarding compen satory growth is why fish do not usually grow as fast as they can, since it is well known that the risk of predation reduces with increased body size (see also Behavioral Responses to the Environment: A Survival Guide for Fishes: How to Obtain Food While Avoiding Being Food). There is some evidence that indicates that there is a trade-off between growth and fitness such that rapid growth can produce deleterious effects compromising further survival. Growth compensation will be favored if the benefits of catching up in size outweigh these costs. Many consequences of accelerated growth rates are related to behavioral changes that animals show during and after compensation, particularly associated with changes in feeding habits and the trade-off between accelerated growth and the increased risks than the fish must take foraging for the extra food. These changes in behavior can be grouped into two different classes depending on whether these changes occur during the period of compen sation or are a consequence of increased growth rates (Figure 1). The main mechanism involved in the compensatory growth response is hyperphagia, an increased rate of food consumption, although increased conversion efficiencies or
752
Summary Further Reading
Hyperphagia Rate of food consumption significantly higher than that shown by animals that have been feeding continuously on an ad libitum ration. Smolting Behavioral and physiological changes crucial to the successful rapid entry of fish that were born in freshwater and are migrating to the marine environment.
behavioral adjustments can play a role. Hyperphagia implies various behavioral changes, mainly an increase in the bold ness and reduction in the use of shelters. During the period of compensation, fish increase their feeding activity and spend more time searching for food in open waters where the chances to be preyed upon are higher than in normal cir cumstances. The need to grow at a higher rate also affects intra-specific behavior, increasing aggressiveness and com petition between fish. However, in the majority of studies on compensatory growth, study animals are held individually and therefore the behavioral changes that they experience during compensation are very difficult to evaluate due to the absence of social interactions (Figure 2). After full growth compensation, fish can show deferred physiological and behavioral effects as a consequence of the rapid growth experienced. There is evidence in a variety of taxa that rapid growth can affect locomotor performance, possibly because of its effects on muscle cellularity and development, and therefore the benefits of growth accel eration should be matched against the locomotor costs. Swimming performance is strongly related to many fish behaviors, such as anti-predator behavior or breeding per formance via sexual displays or offspring care.
Behavioral Changes during Compensation Hyperphagia can result from increasing meal frequency, food consumption per session, or the combination of both. There is significant inter-specific variation in the
Behavioral Responses to the Environment | Effects of Compensatory Growth on Fish Behavior Risk-taking behavior
Agressiveness +
753
Shelter use –
+ Hyperphagia + –
Muscular development – Burst swimming –
Escape response
Growth rate
–
Life span
– Swimming stamina
–
Feeding
behavior
–
Breeding behavior
Courtship
Offspring care
Figure 1 Schematic representation of the direct and indirect effects of compensatory growth on fish behavior where hyperphagia indicates the elevated rate of food consumption associated with compensatory growth. Above the blue line: behavioral changes during compensation; under the blue line: deferred effects of compensatory growth on fish behavior. +, positive relationship; –, negative relationship.
Figure 2 Three-spined sticklebacks (Gasterosteus aculeatus) held in groups of five fish during the phase of growth compensation. Many fish species live in shoals as juveniles, and isolation of individuals during laboratory experiments could affect growth performance. The majority of studies investigating compensatory growth separate fish into individual tanks making it impossible to study additional effects on social behavior. Photo: David A´ lvarez.
temporal pattern of hyperphagia. However, fish, like other vertebrates, can regulate their hyperphagic response according to the quality of the food and the energy needed. Animals that are compensating in growth have a greater food intake than fish that have continuous access to food but which have not undergone a growth depression. This suggests that the maximum daily rates observed during hyperphagia represent a rate close to the maximum possible rate at which the gut can process food. Although the mechanisms that allow compensatory growth are physiological, behavioral adjustments must be involved as high growth rates require an increase in food intake. Hyperphagia imposes several behavioral costs. Increased foraging to obtain the extra ration of food
needed to increase their growth rate may expose the animals to a greater risk of predation. Compensating fish are bolder in the presence of a potential predator than the fish growing at normal rates, and fish exhibiting hyperphagic behavior can increase the number of feeding attempts by more than 50% compared to fish of the same age growing at normal rates. Risk-Taking Behavior Feeding activity can increase the risk of being eaten, since foraging often decreases vigilance. Moreover, after a period of growth depression, a hungry fish may have difficulties avoiding an attack if it is weakened by its poor body condition. For the fish, this is a behavioral
754
Behavioral Responses to the Environment | Effects of Compensatory Growth on Fish Behavior
dilemma: on the one hand, a high growth rate will reduce the time that a fish spends in smaller, more vulnerable stages, but on the other hand to have a high growth rate, a fish has to take more risks and obtain more food. The search for the food necessary to increase their intake rates implies that fish have to use open waters more frequently than fish growing at normal rates and, therefore, they will have a greater chance of being captured. Studies carried out with coho salmon (Oncorhynchus kisutch) showed unequivocally that catch-up growth after a period of growth depression involves a change in the trade-off between food consumption and risk of mortality due to predation. In a study carried out with reef fish ambon damsel (Pomacentrus amboinensis), Monica Gagliano and her collaborators demonstrated that young fish with an intense selective pressure to grow at a faster rate during their benthic life had a high feeding motivation, and were willing to take a greater predation risk as a cost of gaining more resources. Shelters are commonly used by inactive fish to give security against predators but usually imply a cost of reduced feeding opportunities. Fish experiencing com pensatory growth after a period of growth depression change their habits and are more likely to spend increased time out of refuges than fish growing at normal rates. Studies carried out with three-spined sticklebacks demonstrate that the recovery time taken for a fish to emerge from a refuge after a predator attack is less in fish that are compensating than in normal growing fish. In Atlantic salmon (Salmo salar), after a simulated threat of predation, juvenile fish growing at normal rates are reluc tant to move away from refuges to intercept prey items drifting past in the current. In contrast, fish that are displaying hyperphagic behavior after a period of food shortage spend less time in refuges after a simulated predation attack and assume more risks. This behavior increases the time spent for feeding but at the same time increases the risks of being preyed upon since they are more exposed to predatory attacks. Treatment of fish with growth hormone (GH) can be used to evaluate the behavioral consequences of rapid growth. GH stimulates tissue growth by increasing deox yribose nucleic acid (DNA) synthesis and the rate of cell multiplication and differentiation, increasing the meta bolic demands of the animal and the hunger level it experiences. In brown trout (Salmo trutta), GH-treated fish increased their growth rate and also reduced their anti-predator responses. Fish treated with GH spent more time swimming and in the upper part of the water column where they were more accessible to predators. Various studies suggest that GH increases feeding motivation. Similar results are obtained with transgenic Atlantic salmon bred to contain and transmit a GH transgene (see also Cellular, Molecular, Genomics, and Biomedical Approaches: Growth Hormone
Overexpression in Transgenic Fish): they grow faster than control fish but spend more time foraging in risky environments. Although it has not been exhaustively investigated, some authors suggest that fish that experi ence a phase of compensatory growth produce more GH which could increase growth rates above normal levels. Aggressiveness and Risk of Aggression Hyperphagia may induce higher levels of intra-specific aggression as individuals compete for food, with associated costs in terms of higher rates of energy expenditure and increased risk of mortality. Intra-specific aggression can result in the formation of dominance hierarchies (see also Social and Reproductive Behaviors: Dominance Behaviors) and lead to a trade-off between increased resource acquisition and energy losses associated with ago nistic encounters. Growth rates of subordinate fish can be depressed as a consequence of dominant aggression but aggression also involves energetic costs and loss of feeding opportunities during time spent in territory defense. Studies carried out with Atlantic salmon have demon strated links between growth bimodality, aggressiveness, and compensatory growth with food-deprived Atlantic salmon juveniles showing increased levels of aggression during the compensatory growth phase. In salmonids, lifehistory pathways are not fixed and life-history decisions depend on growth rates or size during specific decision windows. For example, several months prior to smolting and migration to sea, juveniles must decide whether to migrate to sea or whether to postpone seaward migration until the subsequent year. Slow-developing fish from the initially poorer competitive fraction of the population are likely to postpone migration, whereas fast-developing fish from the more competitive fraction of the population are likely to migrate to sea at least 1 year before slow-growing individuals. Fish that adopt the faster development path way show compensatory growth and may experience higher aggression than slower-growing fish. Aggression arises over competition for food and fish that are com pensating for growth are more likely to receive attacks from other competing fish. Fish that postpone migration initiate less aggressive actions needing only to maintain their energy reserves above a critical level with a further year in the river to grow; competition for food with the faster-growing fish is not necessary. These different growth strategies in Atlantic salmon result in the fastgrowing juvenile Atlantic salmon that are more aggressive than slow-growing fish, but are also more vulnerable to receiving attacks from other conspecifics. Activity Patterns Some fish species become nocturnal to reduce the risk from diurnal predators, and shelters may be used by
Behavioral Responses to the Environment | Effects of Compensatory Growth on Fish Behavior
inactive animals to give security against predation risk. However, fish that compensate in growth need to eat more than normal and changes in foraging habits can affect diel activity patterns. Individuals that are nocturnal in normal circumstances can increase their diurnal activ ity and hence the risk of predation. In contrast, in species such as Atlantic salmon where nocturnal fish tend to be subordinates that could not find a secure foraging place during the daylight, it may be more risky to feed at night. If energy demand increases as a consequence of compen satory growth, fish will be forced to eat during the hours when they would normally reduce their activity, there fore succumbing to a greater risk of predation. Time–Place Learning Animals organize their daily activities, particularly fora ging, by associating different places with food availability at different times of the day; this is called time–place learning (TPL) (see also Sensory Systems, Perception, and Learning: Fish Learning and Memory). In rats it has been observed that animals that were fed ad libitum lost their ability to learn time-of-day discriminating tasks, whereas food-restricted rats were able to acquire associa tions between two different places and two different times of day. Experiments carried out with Nile tilapia (Oreochromis niloticus) demonstrated that fish that were fed ad libitum failed to learn the time and place synchro nization task, but when the experiment was repeated with fish that had experienced a period of 17 days of starvation, those fish were able to switch places at the correct period of the day to get food, suggesting that food restriction facilitates TPL discrimination.
Deferred Costs of Compensatory Growth Effects on Predator Avoidance Rapid growth can affect locomotor performance, prob ably through effects on muscle cellularity and development. In some species of fish, fast-growing indi viduals have a higher percentage of small-diameter white muscle fibers and greater numbers of similar-diameter red muscle fibers than the slow-growing individuals, which could detrimentally influence fish swimming ability. In the case of compensatory growth, the benefits of growth acceleration can be matched against the locomotor costs. Many fish species use burst swimming as a response to evade predators, and the speed of this response is directly related with the probability of surviving predation attempts. In a study on Atlantic silversides (Menidia meni dia) faster-growing fish had poorer prolonged and burst swimming performances, suggesting a trade-off between growth rate and swimming performance.
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In three-spined sticklebacks, fish that had undergone compensatory growth after a period of food deprivation had a reduced burst swimming speed compared to fish growing at normal rates. Interestingly, there was a strong interhabitat difference in the impact of compensatory growth on swimming performance. Following compensa tory growth, fish from stream populations showed impaired escape speeds, but this was not seen in the pond populations. The explanation for this habitat differ ence appears to lie in the nonlinear nature of the trade-off curve. Small but sustained increases in growth rate (as observed in the pond populations of sticklebacks) had relatively little effect on burst swimming, whereas the greater growth acceleration seen in the stream popula tions of sticklebacks incurred a much greater cost. Lakes and ponds are structured environments in which fish need to be able to dart quickly into a refuge and then remain still; burst swimming is a key factor in determining like lihood of escape and may be too important a trait to be traded off against growth. In contrast, in rivers and streams the importance of burst swimming in evading predators is less important and fish can assume the cost of impaired swimming ability to achieve a larger size in a shorter period of time. Many fish species possess a defensive morphology that protects them from predators (see also Behavioral Responses to the Environment: A Survival Guide for Fishes: How to Obtain Food While Avoiding Being Food). For example, in three-spined sticklebacks there is an interesting potential trade-off in resource allocation between investment in body growth and investment in defensive morphology. In this species, there is marked intra- and interpopulation variation in the average extent of their anti-predator defensive structures (the pelvic and dorsal spines, pelvic girdle and lateral plates), which is linked to the intensity of predation and the willingness of the fish to take risks when foraging. Fish from populations without predatory fish tend to have fewer lateral plates and spines than the fish from populations with intense predation. This reduction of spines and plates has been interpreted as an evolutionary regression of defensive structures in populations from small lakes and streams that lack predatory fish. Due to the phenotypic plasticity of these structures, individual sticklebacks that experi ence compensatory growth after a period of growth depression may compromise on allocation of resources to defensive armor in order to increase their skeletal growth rate. Hence, these fish will be less protected than the fish that have grown at normal rates. Effects on Breeding Behavior Fish and other animals have to reach a minimum size to have the opportunity of finding mates and breeding. A further dimension is the fact that the cost of being small
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Behavioral Responses to the Environment | Effects of Compensatory Growth on Fish Behavior
during the breeding season differs between the sexes. In three-spined sticklebacks, an increase in body length has a positive effect on reproductive success in both the sexes. However, the cost of a small size is greater for males, because females can breed when as small as 32 mm, whereas even a 40-mm male will likely never breed. Moreover, while an increase in body size from 40 to 50 mm doubles the clutch size of a female, the same increase in body size leads to an approximately 15-fold increase in reproductive success in males. This necessity to achieve a minimum size is complicated by the need to allocate resources to other external characteristics that affect the sexual attractiveness of an individual. As with predator avoidance, a large body size at the time of breeding is clearly a fitness advantage, but the rapid growth needed to achieve it may be costly.
obtained from the diet. Thus, fast growth may result in more resources being allocated to growth at the expense of sexual ornaments, which could negatively affect female preference. Some authors suggest that males that have experienced compensatory growth early in life after a period of food restriction could be unable to develop phenotypic traits associated with mate attraction when older. They predict that such males may suffer a more severe decline in phenotypic traits than males that have not undergone growth compensation. This would result in females choosing males with normal growth trajectories over the growth-compensating males because the general appearance of the latter could be interpreted as an indi cator of lower genetic quality.
Effects on Clutch and Offspring Care Effects on Breeding Coloration and Sexual Attractiveness Numerous male fish develop secondary sexual traits when they reach maturity. These attributes could be hyper-developed fins or conspicuous appendices that males exhibit during sexual displays to attract females. As these attributes would be expected to impair swim ming performance, they are considered honest signals of the quality of the male because there is a trade-off between anti-predator escape responses and sexual attractiveness. This trade-off can be affected by a previous diet restriction and further resource allocation during compensatory growth. Green swordtails (Xiphophorus hel leri) are small, tropical, live-bearing fish whose males have developed a long sword which is an extension of the caudal fin that develops at sexual maturity. In an experi ment carried out to study the effects of compensatory growth on female selection, females did not visually dis criminate between males that had experienced poor early nutrition and a subsequent compensatory growth strategy and similar control males. However, physical aspect is not the only trait that female swordtails search for in a poten tial mate. Courtship displays are also very important in female selection, and male swordtails that have under gone a period of growth compensation have poorer swimming performance than control fish. Therefore, growth compensation following poor initial growth can indeed reduce the mating success of male swordtails much later in life. Other fish species swap the dull coloration that they exhibit during the majority of the year for a bright and colorful coloration during the breeding season (see also Sensory Systems, Perception, and Learning: Communication Behavior: Visual Signals). To achieve this, fish must quickly mobilize a large amount of resources to the skin. Some of these resources, such as the carotenoids, cannot be synthesized and must be
As shown previously in this article, compensatory growth may impair muscle development and swimming perfor mance. While this effect can be similar in males and females, there may be greater implications for males in terms of reproductive success as in many species females are the choosy sex and are likely to avoid males in poor condition or with reduced sexual attributes. However, in females compensatory growth can have a significant impact on reproductive investment (i.e., a reduced quality and number of eggs). Fast-growing males that show par ental care after egg laying may be poorer fathers due their reduced ability to swim, which will adversely affect their ability to fan the eggs and defend the nest against intru ders, but to demonstrate this potential effect, further experimental research is needed. Many salmonid fish spawn in rivers and streams where the female digs a nest in the gravel by lying on her side against the bottom and swimming forward energetically (Figure 3). These important movements might be impaired by the poor
Figure 3 A pair of brown trout spawning. The female uses her tail to dig out a hollow in the gravel using a fanning motion. This behavior could be impaired if muscle development is hindered after a period of growth compensation. Photo: David A´lvarez.
Behavioral Responses to the Environment | Effects of Compensatory Growth on Fish Behavior
development of her muscles after a period of growth compensation, and could affect nest structure and further egg development.
Summary The study of compensatory growth in fishes has received much recent attention, especially in relation to aquacul ture, but many behavioral consequences of this accelerated growth remain unexplored. The main beha vioral consequence of growth compensation is that fish have to take more risks to obtain the extra ration of food necessary to increase their growth rates. However, com pensatory growth also affects intra-specific relationships between individuals and may have consequences for breeding behavior and parental care through impaired muscle development after a period of rapid growth. Increased research efforts are now needed in the study of long-term effects of compensatory growth on fish behavior and the consequences of these behavioral changes for natural populations.
See also: Behavioral Responses to the Environment: A Survival Guide for Fishes: How to Obtain Food While Avoiding Being Food. Cellular, Molecular, Genomics, and Biomedical Approaches: Growth Hormone Overexpression in Transgenic Fish. Sensory Systems, Perception, and Learning: Communication Behavior: Visual Signals; Fish Learning and Memory. Social and Reproductive Behaviors: Dominance Behaviors.
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Further Reading Ali M, Nicieza A, and Wootton RJ (2003) Compensatory growth in fishes: A response to growth depression. Fish and Fisheries 4: 147–190. A´lvarez D and Metcalfe NB (2005) Catch-up growth and swimming performance in sticklebacks (Gasterosteous aculeatus): Seasonal changes in the cost of compensation. Canadian Journal of Fisheries and Aquatic Sciences 62: 2169–2173. A´lvarez D and Metcalfe NB (2007) The tradeoff between catch-up growth and escape speed: Variation between habitats in the cost of compensation. Oikos 116: 1144–1151. Billerbeck JM, Lankford TE, and Conover DO (2001) Evolution of intrinsic growth and energy acquisition rates. I. Tradeoffs with swimming performance in Menidia menidia. Evolution 55: 1863–1872. Damsga˚rd B and Dill LM (1998) Risk-taking behavior in weightcompensating coho salmon, Oncorhynchus kisutch. Behavioral Ecology 9: 26–32. Gagliano M, McCormick MI, and Meekan MG (2007) Survival against the odds: Ontogenetic changes in selective pressure mediate growth– mortality trade-offs in a marine fish. Proceedings of the Royal Society B 274: 1575–1582. Gotceitas V and Godin J-GJ (1991) Foraging under the risk of predation in juvenile Atlantic salmon (Salmo salar L.) – effects of social status and hunger. Behavioral Ecology and Sociobiology 29: 255–261. Jonsson E, Johnssonand JI, and Bjornsson BT (1996) Growth hormone increases predation exposure of rainbow trout. Proceedings of the Royal Society of London B 263: 647–651. Lima SL and Dill LM (1990) Behavioural decisions made under the risk of predation: A review and prospectus. Canadian Journal of Zoology 68: 619–640. Metcalfe NB and Monaghan P (2001) Compensation for a bad start: Grow now, pay later? Trends in Ecology and Evolution 16: 254–260. Nicieza AG and Metcalfe NB (1999) Costs of rapid growth: The risk of aggression is higher for fast-growing salmon. Functional Ecology 13: 793–800. Royle NJ, Lindstro¨m J, and Metcalfe NB (2006) Sexual selection, growth compensation and fast-start swimming performance in green swordtails Xiphophorus helleri. Functional Ecology 20: 662–669. Walling CA, Royle NJ, Metcalfe NB, and Lindstro¨m J (2007) Early nutritional conditions, growth trajectories and mate choice: Does compensatory growth lead to a reduction in adult sexual attractiveness? Behavioral Ecology and Sociobiology 61: 1007–1014.
Introduction Behavioral Changes during Compensation Deferred Costs of Compensatory Growth
Glossary Compensatory growth A faster-than-normal growth that some species exhibit after a period of resource deprivation. Dominance The state of being dominant where dominant individuals obtain a high status within a social group. Hormone A chemical substance, often a peptide or steroid, released from endocrine glands that controls and regulates a range of physiological activities.
Introduction Fish are capable of reacting after a period of resource depri vation by increasing their growth rates to higher-than normal levels. This implies that animals under normal con ditions are growing at a rate below their physiological potential and therefore they are able, to some extent, to adjust their growth. The main question regarding compen satory growth is why fish do not usually grow as fast as they can, since it is well known that the risk of predation reduces with increased body size (see also Behavioral Responses to the Environment: A Survival Guide for Fishes: How to Obtain Food While Avoiding Being Food). There is some evidence that indicates that there is a trade-off between growth and fitness such that rapid growth can produce deleterious effects compromising further survival. Growth compensation will be favored if the benefits of catching up in size outweigh these costs. Many consequences of accelerated growth rates are related to behavioral changes that animals show during and after compensation, particularly associated with changes in feeding habits and the trade-off between accelerated growth and the increased risks than the fish must take foraging for the extra food. These changes in behavior can be grouped into two different classes depending on whether these changes occur during the period of compen sation or are a consequence of increased growth rates (Figure 1). The main mechanism involved in the compensatory growth response is hyperphagia, an increased rate of food consumption, although increased conversion efficiencies or
752
Summary Further Reading
Hyperphagia Rate of food consumption significantly higher than that shown by animals that have been feeding continuously on an ad libitum ration. Smolting Behavioral and physiological changes crucial to the successful rapid entry of fish that were born in freshwater and are migrating to the marine environment.
behavioral adjustments can play a role. Hyperphagia implies various behavioral changes, mainly an increase in the bold ness and reduction in the use of shelters. During the period of compensation, fish increase their feeding activity and spend more time searching for food in open waters where the chances to be preyed upon are higher than in normal cir cumstances. The need to grow at a higher rate also affects intra-specific behavior, increasing aggressiveness and com petition between fish. However, in the majority of studies on compensatory growth, study animals are held individually and therefore the behavioral changes that they experience during compensation are very difficult to evaluate due to the absence of social interactions (Figure 2). After full growth compensation, fish can show deferred physiological and behavioral effects as a consequence of the rapid growth experienced. There is evidence in a variety of taxa that rapid growth can affect locomotor performance, possibly because of its effects on muscle cellularity and development, and therefore the benefits of growth accel eration should be matched against the locomotor costs. Swimming performance is strongly related to many fish behaviors, such as anti-predator behavior or breeding per formance via sexual displays or offspring care.
Behavioral Changes during Compensation Hyperphagia can result from increasing meal frequency, food consumption per session, or the combination of both. There is significant inter-specific variation in the
Behavioral Responses to the Environment | Effects of Compensatory Growth on Fish Behavior Risk-taking behavior
Agressiveness +
753
Shelter use –
+ Hyperphagia + –
Muscular development – Burst swimming –
Escape response
Growth rate
–
Life span
– Swimming stamina
–
Feeding
behavior
–
Breeding behavior
Courtship
Offspring care
Figure 1 Schematic representation of the direct and indirect effects of compensatory growth on fish behavior where hyperphagia indicates the elevated rate of food consumption associated with compensatory growth. Above the blue line: behavioral changes during compensation; under the blue line: deferred effects of compensatory growth on fish behavior. +, positive relationship; –, negative relationship.
Figure 2 Three-spined sticklebacks (Gasterosteus aculeatus) held in groups of five fish during the phase of growth compensation. Many fish species live in shoals as juveniles, and isolation of individuals during laboratory experiments could affect growth performance. The majority of studies investigating compensatory growth separate fish into individual tanks making it impossible to study additional effects on social behavior. Photo: David A´ lvarez.
temporal pattern of hyperphagia. However, fish, like other vertebrates, can regulate their hyperphagic response according to the quality of the food and the energy needed. Animals that are compensating in growth have a greater food intake than fish that have continuous access to food but which have not undergone a growth depression. This suggests that the maximum daily rates observed during hyperphagia represent a rate close to the maximum possible rate at which the gut can process food. Although the mechanisms that allow compensatory growth are physiological, behavioral adjustments must be involved as high growth rates require an increase in food intake. Hyperphagia imposes several behavioral costs. Increased foraging to obtain the extra ration of food
needed to increase their growth rate may expose the animals to a greater risk of predation. Compensating fish are bolder in the presence of a potential predator than the fish growing at normal rates, and fish exhibiting hyperphagic behavior can increase the number of feeding attempts by more than 50% compared to fish of the same age growing at normal rates. Risk-Taking Behavior Feeding activity can increase the risk of being eaten, since foraging often decreases vigilance. Moreover, after a period of growth depression, a hungry fish may have difficulties avoiding an attack if it is weakened by its poor body condition. For the fish, this is a behavioral
754
Behavioral Responses to the Environment | Effects of Compensatory Growth on Fish Behavior
dilemma: on the one hand, a high growth rate will reduce the time that a fish spends in smaller, more vulnerable stages, but on the other hand to have a high growth rate, a fish has to take more risks and obtain more food. The search for the food necessary to increase their intake rates implies that fish have to use open waters more frequently than fish growing at normal rates and, therefore, they will have a greater chance of being captured. Studies carried out with coho salmon (Oncorhynchus kisutch) showed unequivocally that catch-up growth after a period of growth depression involves a change in the trade-off between food consumption and risk of mortality due to predation. In a study carried out with reef fish ambon damsel (Pomacentrus amboinensis), Monica Gagliano and her collaborators demonstrated that young fish with an intense selective pressure to grow at a faster rate during their benthic life had a high feeding motivation, and were willing to take a greater predation risk as a cost of gaining more resources. Shelters are commonly used by inactive fish to give security against predators but usually imply a cost of reduced feeding opportunities. Fish experiencing com pensatory growth after a period of growth depression change their habits and are more likely to spend increased time out of refuges than fish growing at normal rates. Studies carried out with three-spined sticklebacks demonstrate that the recovery time taken for a fish to emerge from a refuge after a predator attack is less in fish that are compensating than in normal growing fish. In Atlantic salmon (Salmo salar), after a simulated threat of predation, juvenile fish growing at normal rates are reluc tant to move away from refuges to intercept prey items drifting past in the current. In contrast, fish that are displaying hyperphagic behavior after a period of food shortage spend less time in refuges after a simulated predation attack and assume more risks. This behavior increases the time spent for feeding but at the same time increases the risks of being preyed upon since they are more exposed to predatory attacks. Treatment of fish with growth hormone (GH) can be used to evaluate the behavioral consequences of rapid growth. GH stimulates tissue growth by increasing deox yribose nucleic acid (DNA) synthesis and the rate of cell multiplication and differentiation, increasing the meta bolic demands of the animal and the hunger level it experiences. In brown trout (Salmo trutta), GH-treated fish increased their growth rate and also reduced their anti-predator responses. Fish treated with GH spent more time swimming and in the upper part of the water column where they were more accessible to predators. Various studies suggest that GH increases feeding motivation. Similar results are obtained with transgenic Atlantic salmon bred to contain and transmit a GH transgene (see also Cellular, Molecular, Genomics, and Biomedical Approaches: Growth Hormone
Overexpression in Transgenic Fish): they grow faster than control fish but spend more time foraging in risky environments. Although it has not been exhaustively investigated, some authors suggest that fish that experi ence a phase of compensatory growth produce more GH which could increase growth rates above normal levels. Aggressiveness and Risk of Aggression Hyperphagia may induce higher levels of intra-specific aggression as individuals compete for food, with associated costs in terms of higher rates of energy expenditure and increased risk of mortality. Intra-specific aggression can result in the formation of dominance hierarchies (see also Social and Reproductive Behaviors: Dominance Behaviors) and lead to a trade-off between increased resource acquisition and energy losses associated with ago nistic encounters. Growth rates of subordinate fish can be depressed as a consequence of dominant aggression but aggression also involves energetic costs and loss of feeding opportunities during time spent in territory defense. Studies carried out with Atlantic salmon have demon strated links between growth bimodality, aggressiveness, and compensatory growth with food-deprived Atlantic salmon juveniles showing increased levels of aggression during the compensatory growth phase. In salmonids, lifehistory pathways are not fixed and life-history decisions depend on growth rates or size during specific decision windows. For example, several months prior to smolting and migration to sea, juveniles must decide whether to migrate to sea or whether to postpone seaward migration until the subsequent year. Slow-developing fish from the initially poorer competitive fraction of the population are likely to postpone migration, whereas fast-developing fish from the more competitive fraction of the population are likely to migrate to sea at least 1 year before slow-growing individuals. Fish that adopt the faster development path way show compensatory growth and may experience higher aggression than slower-growing fish. Aggression arises over competition for food and fish that are com pensating for growth are more likely to receive attacks from other competing fish. Fish that postpone migration initiate less aggressive actions needing only to maintain their energy reserves above a critical level with a further year in the river to grow; competition for food with the faster-growing fish is not necessary. These different growth strategies in Atlantic salmon result in the fastgrowing juvenile Atlantic salmon that are more aggressive than slow-growing fish, but are also more vulnerable to receiving attacks from other conspecifics. Activity Patterns Some fish species become nocturnal to reduce the risk from diurnal predators, and shelters may be used by
Behavioral Responses to the Environment | Effects of Compensatory Growth on Fish Behavior
inactive animals to give security against predation risk. However, fish that compensate in growth need to eat more than normal and changes in foraging habits can affect diel activity patterns. Individuals that are nocturnal in normal circumstances can increase their diurnal activ ity and hence the risk of predation. In contrast, in species such as Atlantic salmon where nocturnal fish tend to be subordinates that could not find a secure foraging place during the daylight, it may be more risky to feed at night. If energy demand increases as a consequence of compen satory growth, fish will be forced to eat during the hours when they would normally reduce their activity, there fore succumbing to a greater risk of predation. Time–Place Learning Animals organize their daily activities, particularly fora ging, by associating different places with food availability at different times of the day; this is called time–place learning (TPL) (see also Sensory Systems, Perception, and Learning: Fish Learning and Memory). In rats it has been observed that animals that were fed ad libitum lost their ability to learn time-of-day discriminating tasks, whereas food-restricted rats were able to acquire associa tions between two different places and two different times of day. Experiments carried out with Nile tilapia (Oreochromis niloticus) demonstrated that fish that were fed ad libitum failed to learn the time and place synchro nization task, but when the experiment was repeated with fish that had experienced a period of 17 days of starvation, those fish were able to switch places at the correct period of the day to get food, suggesting that food restriction facilitates TPL discrimination.
Deferred Costs of Compensatory Growth Effects on Predator Avoidance Rapid growth can affect locomotor performance, prob ably through effects on muscle cellularity and development. In some species of fish, fast-growing indi viduals have a higher percentage of small-diameter white muscle fibers and greater numbers of similar-diameter red muscle fibers than the slow-growing individuals, which could detrimentally influence fish swimming ability. In the case of compensatory growth, the benefits of growth acceleration can be matched against the locomotor costs. Many fish species use burst swimming as a response to evade predators, and the speed of this response is directly related with the probability of surviving predation attempts. In a study on Atlantic silversides (Menidia meni dia) faster-growing fish had poorer prolonged and burst swimming performances, suggesting a trade-off between growth rate and swimming performance.
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In three-spined sticklebacks, fish that had undergone compensatory growth after a period of food deprivation had a reduced burst swimming speed compared to fish growing at normal rates. Interestingly, there was a strong interhabitat difference in the impact of compensatory growth on swimming performance. Following compensa tory growth, fish from stream populations showed impaired escape speeds, but this was not seen in the pond populations. The explanation for this habitat differ ence appears to lie in the nonlinear nature of the trade-off curve. Small but sustained increases in growth rate (as observed in the pond populations of sticklebacks) had relatively little effect on burst swimming, whereas the greater growth acceleration seen in the stream popula tions of sticklebacks incurred a much greater cost. Lakes and ponds are structured environments in which fish need to be able to dart quickly into a refuge and then remain still; burst swimming is a key factor in determining like lihood of escape and may be too important a trait to be traded off against growth. In contrast, in rivers and streams the importance of burst swimming in evading predators is less important and fish can assume the cost of impaired swimming ability to achieve a larger size in a shorter period of time. Many fish species possess a defensive morphology that protects them from predators (see also Behavioral Responses to the Environment: A Survival Guide for Fishes: How to Obtain Food While Avoiding Being Food). For example, in three-spined sticklebacks there is an interesting potential trade-off in resource allocation between investment in body growth and investment in defensive morphology. In this species, there is marked intra- and interpopulation variation in the average extent of their anti-predator defensive structures (the pelvic and dorsal spines, pelvic girdle and lateral plates), which is linked to the intensity of predation and the willingness of the fish to take risks when foraging. Fish from populations without predatory fish tend to have fewer lateral plates and spines than the fish from populations with intense predation. This reduction of spines and plates has been interpreted as an evolutionary regression of defensive structures in populations from small lakes and streams that lack predatory fish. Due to the phenotypic plasticity of these structures, individual sticklebacks that experi ence compensatory growth after a period of growth depression may compromise on allocation of resources to defensive armor in order to increase their skeletal growth rate. Hence, these fish will be less protected than the fish that have grown at normal rates. Effects on Breeding Behavior Fish and other animals have to reach a minimum size to have the opportunity of finding mates and breeding. A further dimension is the fact that the cost of being small
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Behavioral Responses to the Environment | Effects of Compensatory Growth on Fish Behavior
during the breeding season differs between the sexes. In three-spined sticklebacks, an increase in body length has a positive effect on reproductive success in both the sexes. However, the cost of a small size is greater for males, because females can breed when as small as 32 mm, whereas even a 40-mm male will likely never breed. Moreover, while an increase in body size from 40 to 50 mm doubles the clutch size of a female, the same increase in body size leads to an approximately 15-fold increase in reproductive success in males. This necessity to achieve a minimum size is complicated by the need to allocate resources to other external characteristics that affect the sexual attractiveness of an individual. As with predator avoidance, a large body size at the time of breeding is clearly a fitness advantage, but the rapid growth needed to achieve it may be costly.
obtained from the diet. Thus, fast growth may result in more resources being allocated to growth at the expense of sexual ornaments, which could negatively affect female preference. Some authors suggest that males that have experienced compensatory growth early in life after a period of food restriction could be unable to develop phenotypic traits associated with mate attraction when older. They predict that such males may suffer a more severe decline in phenotypic traits than males that have not undergone growth compensation. This would result in females choosing males with normal growth trajectories over the growth-compensating males because the general appearance of the latter could be interpreted as an indi cator of lower genetic quality.
Effects on Clutch and Offspring Care Effects on Breeding Coloration and Sexual Attractiveness Numerous male fish develop secondary sexual traits when they reach maturity. These attributes could be hyper-developed fins or conspicuous appendices that males exhibit during sexual displays to attract females. As these attributes would be expected to impair swim ming performance, they are considered honest signals of the quality of the male because there is a trade-off between anti-predator escape responses and sexual attractiveness. This trade-off can be affected by a previous diet restriction and further resource allocation during compensatory growth. Green swordtails (Xiphophorus hel leri) are small, tropical, live-bearing fish whose males have developed a long sword which is an extension of the caudal fin that develops at sexual maturity. In an experi ment carried out to study the effects of compensatory growth on female selection, females did not visually dis criminate between males that had experienced poor early nutrition and a subsequent compensatory growth strategy and similar control males. However, physical aspect is not the only trait that female swordtails search for in a poten tial mate. Courtship displays are also very important in female selection, and male swordtails that have under gone a period of growth compensation have poorer swimming performance than control fish. Therefore, growth compensation following poor initial growth can indeed reduce the mating success of male swordtails much later in life. Other fish species swap the dull coloration that they exhibit during the majority of the year for a bright and colorful coloration during the breeding season (see also Sensory Systems, Perception, and Learning: Communication Behavior: Visual Signals). To achieve this, fish must quickly mobilize a large amount of resources to the skin. Some of these resources, such as the carotenoids, cannot be synthesized and must be
As shown previously in this article, compensatory growth may impair muscle development and swimming perfor mance. While this effect can be similar in males and females, there may be greater implications for males in terms of reproductive success as in many species females are the choosy sex and are likely to avoid males in poor condition or with reduced sexual attributes. However, in females compensatory growth can have a significant impact on reproductive investment (i.e., a reduced quality and number of eggs). Fast-growing males that show par ental care after egg laying may be poorer fathers due their reduced ability to swim, which will adversely affect their ability to fan the eggs and defend the nest against intru ders, but to demonstrate this potential effect, further experimental research is needed. Many salmonid fish spawn in rivers and streams where the female digs a nest in the gravel by lying on her side against the bottom and swimming forward energetically (Figure 3). These important movements might be impaired by the poor
Figure 3 A pair of brown trout spawning. The female uses her tail to dig out a hollow in the gravel using a fanning motion. This behavior could be impaired if muscle development is hindered after a period of growth compensation. Photo: David A´lvarez.
Behavioral Responses to the Environment | Effects of Compensatory Growth on Fish Behavior
development of her muscles after a period of growth compensation, and could affect nest structure and further egg development.
Summary The study of compensatory growth in fishes has received much recent attention, especially in relation to aquacul ture, but many behavioral consequences of this accelerated growth remain unexplored. The main beha vioral consequence of growth compensation is that fish have to take more risks to obtain the extra ration of food necessary to increase their growth rates. However, com pensatory growth also affects intra-specific relationships between individuals and may have consequences for breeding behavior and parental care through impaired muscle development after a period of rapid growth. Increased research efforts are now needed in the study of long-term effects of compensatory growth on fish behavior and the consequences of these behavioral changes for natural populations.
See also: Behavioral Responses to the Environment: A Survival Guide for Fishes: How to Obtain Food While Avoiding Being Food. Cellular, Molecular, Genomics, and Biomedical Approaches: Growth Hormone Overexpression in Transgenic Fish. Sensory Systems, Perception, and Learning: Communication Behavior: Visual Signals; Fish Learning and Memory. Social and Reproductive Behaviors: Dominance Behaviors.
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Further Reading Ali M, Nicieza A, and Wootton RJ (2003) Compensatory growth in fishes: A response to growth depression. Fish and Fisheries 4: 147–190. A´lvarez D and Metcalfe NB (2005) Catch-up growth and swimming performance in sticklebacks (Gasterosteous aculeatus): Seasonal changes in the cost of compensation. Canadian Journal of Fisheries and Aquatic Sciences 62: 2169–2173. A´lvarez D and Metcalfe NB (2007) The tradeoff between catch-up growth and escape speed: Variation between habitats in the cost of compensation. Oikos 116: 1144–1151. Billerbeck JM, Lankford TE, and Conover DO (2001) Evolution of intrinsic growth and energy acquisition rates. I. Tradeoffs with swimming performance in Menidia menidia. Evolution 55: 1863–1872. Damsga˚rd B and Dill LM (1998) Risk-taking behavior in weightcompensating coho salmon, Oncorhynchus kisutch. Behavioral Ecology 9: 26–32. Gagliano M, McCormick MI, and Meekan MG (2007) Survival against the odds: Ontogenetic changes in selective pressure mediate growth– mortality trade-offs in a marine fish. Proceedings of the Royal Society B 274: 1575–1582. Gotceitas V and Godin J-GJ (1991) Foraging under the risk of predation in juvenile Atlantic salmon (Salmo salar L.) – effects of social status and hunger. Behavioral Ecology and Sociobiology 29: 255–261. Jonsson E, Johnssonand JI, and Bjornsson BT (1996) Growth hormone increases predation exposure of rainbow trout. Proceedings of the Royal Society of London B 263: 647–651. Lima SL and Dill LM (1990) Behavioural decisions made under the risk of predation: A review and prospectus. Canadian Journal of Zoology 68: 619–640. Metcalfe NB and Monaghan P (2001) Compensation for a bad start: Grow now, pay later? Trends in Ecology and Evolution 16: 254–260. Nicieza AG and Metcalfe NB (1999) Costs of rapid growth: The risk of aggression is higher for fast-growing salmon. Functional Ecology 13: 793–800. Royle NJ, Lindstro¨m J, and Metcalfe NB (2006) Sexual selection, growth compensation and fast-start swimming performance in green swordtails Xiphophorus helleri. Functional Ecology 20: 662–669. Walling CA, Royle NJ, Metcalfe NB, and Lindstro¨m J (2007) Early nutritional conditions, growth trajectories and mate choice: Does compensatory growth lead to a reduction in adult sexual attractiveness? Behavioral Ecology and Sociobiology 61: 1007–1014.