Effects of the rearing environment on average behaviour and behavioural variation in steelhead

In the context of conservation hatcheries that seek to bolster wild populations by releasing captively-reared fishes into the wild, steelhead Oncorhynchus mykiss were used to test the hypothesis that naturalistic rearing environments promote adaptive behaviour that might otherwise not develop in typical hatchery environments. When comparisons were made among fish reared in barren, structured or structurally variable environments ( i.e. the location of the structure was repositioned every 2–3 days), structure in the rearing environment increased future exploratory behaviour, but only if the structure was stable. Under conditions of high perceived predation risk, the fish no longer exhibited increased exploratory behaviour, suggesting that it is expressed in an adaptive, context-dependant manner. Another concern with hatcheries is that relaxed selection over multiple generations in captivity can increase maladaptive behavioural variation. Compared to rearing in hatchery-typical barren environments, rearing in structured-stable environments decreased behavioural variation. This effect, which occurred during development and did not involve selection, demonstrates a different mechanism for change in behavioural variation in captivity. These experiments show that effects of structure and structural stability occur at the level of both average behaviour and behavioural variation, and suggest that these effects should be considered when fishes are reared in hatcheries for later release into the wild.     

Environmental effects on behavioural development consequences for fitness of captive‐reared fishes in the wild

Why do captive‐reared fishes generally have lower fitness in natural environments than wild conspecifics, even when the hatchery fishes are derived from wild parents from the local population? A thorough understanding of this question is the key to design artificial rearing environments that optimize post‐release performance, as well as to recognize the limitations of what can be achieved by modifying hatchery rearing methods. Fishes are generally very plastic in their development and through gene–environment interactions, epigenetic and maternal effects their phenotypes will develop differently depending on their rearing environment. This suggests that there is scope for modifying conventional rearing environments to better prepare fishes for release into the wild. The complexity of the natural environment is impossible to mimic in full‐scale rearing facilities. So, in reality, the challenge is to identify key modifications of the artificial rearing environment that are practically and economically feasible and that efficiently promote development towards a more wild‐like phenotype. Do such key modifications really exist? Here, attempts to use physical enrichment and density reduction to improve the performance of hatchery fishes are discussed and evaluated. These manipulations show potential to increase the fitness of hatchery fishes released into natural environments, but the success is strongly dependent on adequately adapting methods to species and life stage‐specific conditions.     

Implications of domestication and rearing conditions for the behaviour of cultivated fishes

Farmed fishes are often selectively bred for desirable production traits, such as rapid growth, that brings with them behavioural differences. In addition, the striking differences in the environment experienced by wild and cultured fishes offers considerable scope both for unplanned, natural selection for different inherited behavioural phenotypes and for behavioural differences arising from differential experience. In this paper, the evidence that such processes have produced behavioural differences between wild and cultured fishes is reviewed in relation to feeding, antipredator responses, aggression and reproductive behaviour. The reported findings are discussed in relation to the concept of 'behavioural syndromes', or suites of co‐varying behavioural traits that adapt individuals of the same population to spatial and temporal variation in selection regimes. The implications of the behaviour of cultured fishes for their welfare in production cages, for the environmental impact of escapees on wild stocks and for the success of hatchery‐based restocking programmes are considered. The review inevitably concentrates on salmonids, in which such phenomena have been intensively researched.     

A short hatchery history: does it make a difference to aggressiveness in European grayling?

The level of aggressive behaviour in three populations of grayling Thymallus thymallus was lower in the hatchery strains than in the wild strains at the age of 0+ years. Due to similar rearing conditions, genetic divergence of the strains was most likely. As the hatchery fish used were second generation hatchery fish, this suggested that genetic changes in the hatchery can be very rapid. Therefore, it would be beneficial to use the progeny of wild fish for re-introductions. Differences in aggressiveness between the strains still existed at the age of 1+ years, when the strains had been reared under common hatchery conditions for a year. A relatively short period in the hatchery may maintain the original behavioural characteristics of the fish and thus give the best possible basis for survival in the natural environment.     

Interaction between hatchery and wild Pacific salmon in the Far East of Russia: A review

We review studies of interactions between hatchery and wild Pacific salmon in the Russian Far East. This includes the role of hatchery practices that result in premature migration to the sea and increased mortality, and data on feeding and territorial competition between juveniles of hatchery and wild origin. In the course of downstream migration many juvenile hatchery salmon are eliminated by wild salmon predation. During the marine period, Japanese hatchery chum salmon (Oncorhynchus keta) distribution overlaps the distribution of Russian wild salmon. Consequently, replacement of wild populations by hatchery fishes, as a result of abundant juvenile hatchery releases combined with extensive poaching in spawning grounds, is apparent in some Russian rivers. Interactions between the populations occur in all habitats. The importance of conservation of wild salmon populations requires a more detailed study of the consequences of interactions between natural and artificially reared fishes.     

Social learning and life skills training for hatchery reared fish

With the stress placed on our natural resources, many fisheries increasingly rely on restocking from hatchery-reared sources in an attempt to maintain commercially viable populations. However, the mortality rates of hatchery-reared fishes during the period directly following release are very high. The successful development of restocking programs is consequently dependent upon production and release strategies that lead to improved migratory, antipredator and feeding behaviour in hatchery fish. While relevant individual experience prior to release might improve performance, social learning potentially provides a process whereby fish can acquire locally adaptive behaviour rapidly and efficiently. It is now well over a decade since Suboski & Templeton (1989) raised the possibility of using social learning processes to improve the post-release survival of hatchery-reared fishes. This period has witnessed considerable progress in the understanding of how social learning operates in fish populations. We review new methods and recent findings that suggest how social learning protocols could realistically be applied on a large scale to enhance the viability of hatchery fish prior to their release into the wild. We also suggest a practical pre-release training protocol that may be applied at the hatchery level.     

The importance of genetic cluster recognition for the conservation of migratory fish species: the example of the endangered European huchen Hucho hucho (L.)

European huchen Hucho hucho (L.) is an endangered flagship species, which is endemic to the Danube drainage in central Europe. To date, no genetic information has been available as a basis for ongoing conservation and breeding programmes for the species. It is suspected that most populations in the wild share one common gene pool and that they exclusively depend on stocking with hatchery fish. In this study, highly variable microsatellite markers were established and the genetic diversity and differentiation from four important hatchery-reared stocks were compared with that of eight H. hucho populations sampled in the wild. Overall, eight genetic clusters with a moderate to very great degree of genetic differentiation and high assignment rates were identified. Each cluster contained individuals from two to 10 different populations and 9–100% of specimens from hatchery stocks. It is proposed that genetic cluster-based management in the conservation of European huchen is advantageous compared with the consideration of single local populations. A combined approach of maintaining the evolutionary potential of wild populations and genetically variable hatchery stocks can maximize the conservation of the species' evolutionary potential.     

Comparison of maturation timing,egg size and fecundity between hatchery lines of chinook salmon and their wild donor stocks

Increasing concern has been expressed about the genetic effects of cultured salmonid fishes on natural populations. Avoidance of extreme negative outcomes was one reason for the establishment of a genetic management policy for the State of Alaska. However, domestication within the hatchery may still cause divergence from the wild donor population. This divergence could potentially lead to adverse impacts on wild stocks through straying and introgression. This study examines potential domestication in two Alaskan chinook salmon stocks. The Little Port Walter (LPW) Hatchery Chickamin River stock resulted from a small collection of wild broodstock in 1976. The LPW Unuk stock was founded with a larger number of individuals in 1976 and has had subsequent infusion of wild gametes. These lines have been maintained at LPW through ocean ranching of tagged smolts. Comparisons are made between the hatchery lines, progeny of wild chinook collected from the Chickamin and Unuk Rivers, and hybrids between the hatchery and wild groups. Mature ocean‐ranched female chinook salmon returning to the facility were periodically graded for ripeness and spawned. Body size and meristic measurements were collected from these mature spawners. Maturation timing, fecundity, and individual egg size of these fourth generation hatchery fish are compared with that of offspring of wild fish from the same donor stock. Stock of origin is confirmed for all spawners and offspring using microsatellite DNA analysis.     

Consequences to fitness‐related traits of hybridization between farmed and wild Atlantic salmon, Salmo salar

Increasing concern has been expressed about the genetic effects of cultured salmonid fishes on natural populations. Avoidance of extreme negative outcomes was one reason for the establishment of a genetic management policy for the State of Alaska. However, domestication within the hatchery may still cause divergence from the wild donor population. This divergence could potentially lead to adverse impacts on wild stocks through straying and introgression. This study examines potential domestication in two Alaskan chinook salmon stocks. The Little Port Walter (LPW) Hatchery Chickamin River stock resulted from a small collection of wild broodstock in 1976. The LPW Unuk stock was founded with a larger number of individuals in 1976 and has had subsequent infusion of wild gametes. These lines have been maintained at LPW through ocean ranching of tagged smolts. Comparisons are made between the hatchery lines, progeny of wild chinook collected from the Chickamin and Unuk Rivers, and hybrids between the hatchery and wild groups. Mature ocean‐ranched female chinook salmon returning to the facility were periodically graded for ripeness and spawned. Body size and meristic measurements were collected from these mature spawners. Maturation timing, fecundity, and individual egg size of these fourth generation hatchery fish are compared with that of offspring of wild fish from the same donor stock. Stock of origin is confirmed for all spawners and offspring using microsatellite DNA analysis.     

Strong divergence in trait means but not in plasticity across hatchery and wild populations of sea-run brown trout Salmo trutta

There is ample evidence that organisms adapt to their native environment when gene flow is restricted. However, evolution of plastic responses across discrete environments is less well examined. We studied divergence in means and plasticity across wild and hatchery populations of sea-run brown trout (Salmo trutta) in a common garden experiment with two rearing environments (hatchery and a nearly natural experimental stream). Since natural and hatchery environments differ, this arrangement provides an experiment in contemporary adaptation across the two environments. A Q(ST) - F(ST) approach was used to investigate local adaptation in survival and growth over the first summer. We found evidence for divergent selection in survival in 1 year and in body length in both years and rearing environments. In general, the hatchery populations had higher survival and larger body size in both environments. Q(ST) in body size did not differ between the rearing environments, and constitutive divergence in the means was in all cases stronger than divergence in the plastic responses. These results suggest that in this system, constitutive changes in mean trait values are more important for local adaptation than increased plasticity. In addition, ex situ rearing conditions induce changes in trait means that are adaptive in the hatchery, but potentially harmful in the wild, suggesting that hatchery rearing is likely to be a suboptimal management strategy for trout populations facing selection in the stream environment.     

Predator avoidance behaviour in wild and hatchery‐reared brown trout: the role of experience and domestication

Juvenile brown trout Salmo trutta from natural populations reacted to the presence of piscivorous brown trout by increasing the use of refuges. In contrast, second‐generation hatchery fish and the offspring of wild fish raised under hatchery conditions were insensitive to predation risk. The diel pattern of activity also differed between wild and hatchery brown trout. Second‐generation hatchery fish were predominantly active during daytime regardless of risk levels. Wild fish, however, showed a shift towards nocturnal activity in the presence of predators. These findings emphasize the potential role of domestication in weakening behavioural defences. They support the idea that the behavioural divergence between wild and domesticated individuals can arise from a process of direct or indirect selection on reduced responsiveness to predation risk, or as a lack of previous experience with predators.     

Effect of hatchery environment on cranial morphology and developmental stability of Atlantic salmon (Salmo salar L.) from North‐West Russia

The study addresses the effect of hatchery rearing on morphological variation and developmental stability of Atlantic salmon parr from North‐West Russia. Totally, we collected nine samples. Four wild samples were collected from each of the rivers Kola, Umba, Keret’ and Shuia. Five samples of hatchery‐reared parr were the first‐generation progeny of wild adults from these rivers reared separately at the four hatcheries (one hatchery was represented by two samples). Ten meristic and 48 morphometric cranial characters were analysed. We studied the morphological divergence between wild and hatchery fishes of the same river of origin. To analyze developmental stability we used fluctuating asymmetry (random deviations from perfect bilateral symmetry). It was found that hatchery‐reared parr significantly differ from wild parr in both meristic characters and the shape of cranial bones. Different hatcheries caused similar effect on morphological variation in all populations. Fluctuating asymmetry in morphometric characters was significantly higher in hatchery fish than in wild from the Shuia River, indicating a higher level of developmental instability. However, wild parr from the Keret’ River had significantly higher fluctuating asymmetry than cultivated parr of the same origin, possible due to a high infection pressure of the parasite Gyrodactylus salaris Malmberg which has led to significant decline of the wild salmon population in this river, or from genetic changes caused by cultivation. The obtained results indicate a notable effect of hatchery environment on Atlantic salmon’s phenotype.     

Identifying footprints of selection in stocked brown trout populations: a spatio‐temporal approach

Studies of interactions between farmed and wild salmonid fishes have suggested reduced fitness of farmed strains in the wild, but evidence for selection at the genic level is lacking. We studied three brown trout populations in Denmark which have been significantly admixed with stocked hatchery trout (19–64%), along with two hatchery strains used for stocking. The wild populations were represented by contemporary samples (2000–2006) and two of them by historical samples (1943–1956). We analysed 61 microsatellite loci, nine of which showed putative functional relationships [expressed sequence tag (EST)‐linked or quantitative trait loci]. F_ST‐based outlier tests provided support for diversifying selection at chromosome regions marked by three loci, two anonymous and one EST‐linked. Patterns of differentiation suggested that the loci were candidates for being under diversifying hitch‐hiking selection in hatchery vs. wild environments. Analysis of hatchery strain admixture proportions showed that in one wild population, two of the loci showed significantly lower admixture proportions than the putatively neutral loci, implying contemporary selection against alleles introduced by hatchery strain trout. In the most strongly admixed population, however, there was no evidence for selection, possibly because of immigration by stocked trout overcoming selection against hatchery‐derived alleles or supportive breeding practices allowing hatchery strain trout to escape natural selection. To our knowledge, this is the first study demonstrating footprints of selection in wild salmonid populations subject to spawning intrusion by farmed fish.     

Effects of habitat enrichment and food availability on the foraging behaviour of juvenile Atlantic Cod (<Emphasis Type="Italic">Gadus morhua L</Emphasis>)

The environment can play an important role in shaping how an animal behaves, and how well the animal performs in a particular environment can be influenced by early experiences. The tradition of releasing captive-reared juveniles into the wild in an effort to strengthen wild fish populations has often had little success owing to high post-release mortality. Fish reared under standard hatchery conditions are provided with fewer stimuli and they receive excess quantities of pellet food that are easy to handle and consume. Captive reared fish therefore appear to be under-stimulated and overfed. Several studies have demonstrated that simple structural enrichment in the rearing facilities promotes flexible behaviour compared to fish reared in plain, standard hatchery tanks. Less attention has been given to the effects of the diet. Here we use a cross-factored design to test the relative role of food ration and spatial enrichment on foraging behaviour. Our results show that fish from enriched environments, regardless of previous food-ration size, were more reluctant to start feeding on the first day in a novel arena. On day two and three, however, fish with prior experience of a low food ration showed greater foraging activity and efficiency than fish fed on full rations. On the second and third day, prior experience with enrichment was less important. We discuss how early feeding experience in combination with structural enrichment may contribute in producing fish that are better suited for release into the wild.     

Understanding the adaptive consequences of hatchery-wild interactions in Alaska salmon

About 31% of salmon harvested in Alaska comes from the hatchery production of hundreds of millions of pink and chum salmon and smaller numbers of sockeye, Chinook, and coho salmon. The numbers of hatchery-reared juveniles released in some areas are greater than the numbers of juveniles from wild populations. However, virtually nothing is known about the effects of hatchery fish on wild populations in Alaska. Possible effects of these interactions can be inferred from studies of salmonids in other areas, from studies of other animals, and from theory. Numerous studies show a complex relationship between the genetic architecture of a population and its environment. Adaptive responses to nature and anthropogenic selection can be influenced by variation at a single gene, or more often, by the additive effects of several genes. Studies of salmonids in other areas show that hatchery practices can lead to the loss of genetic diversity, to shifts in adult run timing and earlier maturity, to increases in parasite load, to increases in straying, to altered levels of boldness and dominance, to shifts in juvenile out-migration timing, and to changes in growth. Controlled experiments across generations show, and theory predicts, that the loss of adaptive fitness in hatchery salmon, relative to fitness in wild salmon, can occur on a remarkably short time scale. All of these changes can influence survival and impose selective regimes that influence genetically based adaptive traits. The preservation of adaptive potential in wild populations is an important buffer against diseases and climate variability and, hence, should be considered in planning hatchery production levels and release locations. The protection of wild populations is the foundation for achieving sustained harvests of salmon in Alaska.     

Genetic diversity and differentiation of the Korean starry flounder (Platichthys stellatus) between and within cultured stocks and wild populations inferred from microsatellite DNA analysis

The Korean starry flounder, Platichthys stellatus, is economically valuable coastal resident fish species. However, the annual catch of this fish has fluctuated and suffered major declines in Korea. We examined the genetic diversity and population structure for four wild populations and three hatchery stocks of Korean starry flounder to protect its genetic integrity using nine microsatellites. A group of 339 genotypes belonging to seven populations were screened. High degrees of polymorphism at the microsatellite loci were observed within both the wild and hatchery populations. Compared to the wild populations, genetic changes, including reduced genetic diversity and highly significant differentiation, have occurred in cultured stocks. Significant population differentiation was also observed in wild starry flounder populations. Similar degrees of inbreeding and significant Hardy–Weinberg equilibrium deviations were detected in both the wild and the hatchery populations. The genetic connectivity pattern identified four distinct metapopulations of starry flounder in Korea by clustering in the phylogenetic tree, Bayesian analyses, molecular variance analysis, PCA and multidimensional scaling analysis. A pattern of isolation-by-distance was not significant. This genetic differentiation may be the result of the co-effects of various factors, such as historic dispersal, local environment or anthropogenic activities. These results provide useful information for the genetic monitoring of P. stellatus hatchery stocks, for the genetic improvement of this species by selective breeding and for designing suitable management guidelines for the conservation of this species.     

The role of learning in fish behaviour

Summary The behavioural patterns of fish are the result of innate (built-in) patterns of maturation (developmental changes) and of learning processes (imprinting and trial-and-error learning). Innate behavioural patterns are considered to be hard-wired and inflexible. However, through learning, fish can adapt to environmental change. For instance, the homing behaviour of fish may be partly the result of the development of specific parts of the brain and partly because of changes in behaviour with experience. Similarly, one can assume that the feeding mode of fish involving snap-responses is innate, but learning enables fish to modify their foraging behaviour in response to a fluctuating environment. By reviewing these and other examples, such as the role of recognition learning and socially transmitted behaviour, one can illustrate the importance of learning in the everyday life of fishes. Although learning plays a large role in the behaviour of fishes, the learning capacity of fishes may also be useful to fisheries research and hatchery operations.     

Behavioural type in newly emerged steelhead Oncorhynchus mykiss does not predict growth rate in a conventional hatchery rearing environment

Behavioural assays were conducted on newly emerged steelhead Oncorhynchus mykiss to investigate the presence of behavioural syndromes and to determine whether behavioural type in young fish predicts growth rate in a conventional hatchery rearing environment. Individual fry were consistent in their position choice and activity behaviours across safe and unsafe contexts, as well as among assays conducted on different days. Position choice and activity behaviours, however, were not necessarily correlated to each other. Both behaviours predicted feeding rates during behavioural assays, but there was no relationship between fry behaviour and subsequent growth rate or survival during the first 3 months of hatchery rearing. These results support the hypothesis that selection in captivity may be relaxed with respect to behavioural type rather than directional, allowing for increased behavioural variance in domesticated populations. Modest magnitudes of correlations among fry behaviours, however, suggest that behavioural type may be unstable at the onset of the juvenile feeding stage.     

Microsatellite and mitochondrial DNA polymorphism reveals life-history dependent interbreeding between hatchery and wild brown trout (Salmo trutta L.)

The effects of stocking hatchery trout into wild populations were studied in a Danish river, using microsatellite and mitochondrial DNA (mtDNA) markers. Baseline samples were taken from hatchery trout and wild trout assumed to be unaffected by previous stocking. Also, samples were taken from resident and sea trout from a stocked section of the river. Genetic differentiation between the hatchery strain and the local wild population was modest (microsatellite FST = 0.06). Using assignment tests, more than 90% of individuals from the baseline samples were classified correctly. Assignment tests involving samples from the stocked river section suggested that the contribution by hatchery trout was low among sea trout (< 7%), but high (46%) among resident trout. Hybrid index analysis and a high percentage of mtDNA haplotypes specific to indigenous trout observed among resident trout that were assigned to the hatchery strain suggested that interbreeding took place between hatchery and wild trout. The latter result also indicated that male hatchery trout contributed more to interbreeding than females. We suggest that stronger selection acts against stocked hatchery trout that become anadromous compared to hatchery trout that become resident. As most resident trout are males this could also explain why gene flow from hatchery to wild trout appeared to be male biased. The results show that even despite modest differentiation at neutral loci domesticated trout may still perform worse than local populations and it is important to be aware of differential survival and reproductive success both between life-history types and between sexes.     

Long-term captive breeding does not necessarily prevent reestablishment: lessons learned from Eagle Lake rainbow trout

Captive breeding of animals is often cited as an important tool in conservation, especially for fishes, but there are few reports of long-term (<50 years) success of captive breeding programs, even in salmonid fishes. Here we describe the captive breeding program for Eagle Lake rainbow trout, Oncorhynchus mykiss aquilarum, which is endemic to the Eagle Lake watershed of northeastern California. The population in Eagle Lake has been dependent on captive breeding for more than 60 years and supports a trophy fishery in the lake. Nevertheless, the basic life history, ecological, and genetic traits of the subspecies still seem to be mostly intact. Although management has apparently minimized negative effects of hatchery rearing, reestablishing a wild population would ensure maintenance of its distinctive life history and its value for future use as a hatchery fish. An important factor that makes reestablishment possible is that the habitat in Eagle Lake is still intact and that Pine Creek, its major spawning stream, is recovering as habitat. With the exception of an abundant alien brook trout (Salvelinus fontinalis) population in Pine Creek, the habitat factors that led to the presumed near-extinction of Eagle Lake rainbow trout in the early twentieth century have been ameliorated, although the final stages of reestablishment (eradication of brook trout, unequivocal demonstration of successful spawning migration) have still not been completed. The Eagle Lake rainbow trout story shows that long-term captive breeding of migratory salmonid fishes does not necessarily prevent reestablishment of wild populations, provided effort is made to counter the effects of hatchery selection and that natural habitats are restored for reintroduction. Long-term success, however, ultimately depends upon eliminating hatchery influences on wild-spawning populations. Extinction of Eagle Lake rainbow trout as a wild species becomes increasingly likely if we fail to act boldly to protect it and the Eagle Lake watershed.