The role of social learning in conservation and fisheries reintroductions

The plight of the world fish stocks is all too well documented. As part of an ongoing attempt to bolster fish stocks for both commercial and conservation purposes, many fish are reared in captivity and released into the wild. It is well known that hatchery‐reared fish have low post‐release survival compared with wild fish of similar age. Part of the reason for this high mortality is that hatchery fish show deficits in virtually all aspects of their behaviour, including prey selection and predator avoidance. Much behaviour requires repeated experience so that it may become fine‐tuned to prevailing circumstances via learning during development. It has been suggested that inappropriate behaviour is encouraged when fish are reared in the unnatural surroundings of the hatchery. However, hatchery fish can be taught to recognise live, novel prey items and predators and the rate of learning is increased in the presence of a more knowledgeable conspecifics. Here we present data showing how social learning protocols can be used to dramatically increase foraging success in juvenile Atlantic salmon. We also outline related aspects of our ongoing research and discuss some of the possibilities for altering hatchery practices to maximize post‐release survival.     

Environmental enrichment and prior experience of live prey improve foraging behaviour in hatchery‐reared Atlantic salmon

Atlantic salmon salmo salar L. parr were reared for 3 months under standard hatchery conditions or in a structurally enriched tank (containing plants, rocks and novel objects). Half of each of these fish had prior exposure to live prey in the form of live bloodworm while the other half were fed hatchery‐pellets. After 12 days all fish were tested on a novel live prey item (brine shrimp). A significant interaction between the two factors (prior exposure to live prey and rearing condition) revealed that foraging performance was only enhanced in fish that had been reared in a complex environment and exposed to live prey. It appears that the ability to generalize from one live prey type to another is only enhanced in fish that had been reared in an enriched environment. The findings support the assertion that the provision of enriched environments in combination with exposure to live prey prior to release may significantly improve the post‐release survival rates of hatchery‐reared fishes. As both the environmental enrichment and the prior foraging experience procedures were comparatively simple, the provision of such pre‐release experiences are likely to prove cost effective to hatcheries.     

The relationship between dominance behaviour and growth as a function of habitat stability and community complexity: a test using salmon and trout

Predation shortly after release is the main source of mortality among hatchery‐reared fish used to restore or enhance endangered salmonid populations. We found, that hatchery‐reared salmonid young originating from endangered stocks have weak innate responses to their natural fish predators. The ability to avoid predation in fish can be improved through social learning from experienced to naïve individuals. Huge benefits would be achieved, if social learning processes could be successfully applied on a large scale to enhance viability of hatchery fish prior to release into the wild. By using model predators together with chemical cues from real predators we tested if social learning could be used to train hatchery‐reared salmonid young to avoid fish predators. As there are clear differences in social behaviour among the salmonid species, we first examined whether these differences affect the probability and efficiency of learning anti‐predator skills from trained demonstrators. We compared anti‐predator responses of observers (fish trained by using experienced fish as demonstrators) with those of control fish, which had been 'trained' by untrained naïve conspecifics. We also examined how the efficiency of social learning depends on the ratio of experienced to naïve fish involved in social transmission trials. The results of these experiments will give guidelines how social learning could be utilized in developing hatchery scale training protocols.     

Fish cognition: what can we learn, and what do they need to learn?

Fish provide a wonderful opportunity to explore processes that shape and select cognitive ability. In this presentation, I will illustrate three aspects of work that my colleagues and I have used to investigate fish learning and memory over the last decade. First, I will discuss how comparing different populations sampled from contrasting habitats allows differences in cognitive ability to be related to the evolutionary ecology of the fish. I will use examples that have investigated how differences in learning ability between populations of the same species can arise. Here, the examples will be taken from the ubiquitous three‐spined stickleback, and a Panamanian poecilid, Brachyraphis .
The second approach has used fish cognition as a tool to quantify behaviour to enable assessment of different aspects of fish welfare. For example, the recent work investigating pain perception in trout required the use of a learning task to quantify how fish behaviour was modified after noxious stimulation. Ways in which these, and similar, processes can be used in future studies of fish welfare will be discussed.
The final part of the presentation will consider recent work that addresses the problems of releasing hatchery‐reared fish for restocking purposes. Although a common practice, most of the hatchery‐reared fish die shortly after they are released. Much of the observed mortality apparently stems from the fishes' inexperience with a variable environment. Experiments with juvenile cod and brown trout suggest that both age, and the early rearing environment, have profound effects on fish learning and behaviour. I will discuss how simple modifications to current rearing practices may have large beneficial effects on the post‐release survival of hatchery‐reared fish.     

Improving anti‐predator responses of hatchery reared salmonids by social learning

Predation shortly after release is the main source of mortality among hatchery‐reared fish used to restore or enhance endangered salmonid populations. We found, that hatchery‐reared salmonid young originating from endangered stocks have weak innate responses to their natural fish predators. The ability to avoid predation in fish can be improved through social learning from experienced to naïve individuals. Huge benefits would be achieved, if social learning processes could be successfully applied on a large scale to enhance viability of hatchery fish prior to release into the wild. By using model predators together with chemical cues from real predators we tested if social learning could be used to train hatchery‐reared salmonid young to avoid fish predators. As there are clear differences in social behaviour among the salmonid species, we first examined whether these differences affect the probability and efficiency of learning anti‐predator skills from trained demonstrators. We compared anti‐predator responses of observers (fish trained by using experienced fish as demonstrators) with those of control fish, which had been ‘trained’ by untrained naïve conspecifics. We also examined how the efficiency of social learning depends on the ratio of experienced to naïve fish involved in social transmission trials. The results of these experiments will give guidelines how social learning could be utilized in developing hatchery scale training protocols.     

Effects of Hatchery Rearing on Brain Structures of Rainbow Trout, Oncorhynchus mykiss

In this study, we contrast brain morphology from hatchery and wild reared stocks to examine the hypothesis that in salmonid fishes, captive rearing produces changes in brain development. Using rainbow trout, Oncorhynchus mykiss, as a model, we measured eight regions of the salmonid brain to examine differences between wild and hatchery reared fish. We find using multiple analysis of covariance (MANCOVA), analysis of covariance (ANCOVA) and discriminant function analysis (DFA) that the brains of hatchery reared fish are relatively smaller in several critical measures than their wild counterparts. Our work may suggest a mechanistic basis for the observed vulnerability of hatchery fish to predation and their general low survival upon release into the wild. Our results are the first to highlight the effects of hatchery rearing on changes in brain development inbreak fishes.     

Physiological and behavioural differences of hatchery and wild‐reared steelhead Oncorhynchus mykiss smolts of the same genetic origin

In many parts of the world release of hatchery‐reared smolts has long been used to mitigate for the deleterious effects of habitat loss and overfishing on salmonid populations. Of increasing concern is whether this may cause harm by spreading non‐native stocks and potentially releasing incompetent smolts. The objective of this study was to determine if smolt physiology and behavior of juveniles produced from a recently founded native broodstock differ from their wild (naturally‐reared) counterparts. In the fall of 2002 and 2003 juvenile wild steelhead were captured, PIT tagged, and returned ( n  = 1360 in 2002 and n  = 2708 in 2003) to Abernathy Creek. In winter of 2003 and 2004 hatchery‐reared fish were PIT tagged and later released ( n  = 1100 in 2003 and n  = 1400 in 2004) into Abernathy Creek. Gill biopsies were collected from wild and hatchery fish throughout the rearing and out‐migration season. The timing and speed of outmigration was assessed using two stationary PIT tag antennas (92–97% efficient). Hatchery migrants in 2003 were larger, had significantly lower gill Na⁺, K⁺‐ATPase activities, and migrated slower than wild fish. Results from the 2004 migratory season will also be presented. This study shows that hatchery rearing can result in smolts which are physiologically and behaviourally different from genetically similar wild fish. Whether these differences are critical enough to affect the rate of adult returns will be determined in future years.     

Effects of hatchery rearing on Florida largemouth bass Micropterus floridanus resource allocation and performance under semi‐natural conditions

This study examined the growth, activity, metabolism and post‐release survival of three groups of Florida largemouth bass Micropterus floridanus: wild‐caught fish, hatchery fish reared according to standard practice (hatchery standard) and hatchery fish reared under reduced and unpredictable food provisioning (hatchery manipulated). Hatchery‐standard fish differed from wild‐caught fish in all measured variables, including survival in semi‐natural ponds. Hatchery‐standard and hatchery‐manipulated fish showed higher activity levels, faster growth and lower standard metabolic rates than wild‐caught fish in the hatchery. Fish reared under the manipulated feeding regime showed increased metabolic rates and increased post‐release growth, similar to wild‐caught fish. Their activity levels and post‐release survival, however, remained similar to those of hatchery‐standard fish. Activity was negatively correlated with post‐release survival and failure of the feed manipulation to reduce activity may have contributed to its failure to improve post‐release survival. Activity and post‐release survival may be influenced by characteristics of the rearing environment other than the feeding regime, such as stock density or water flow rates.     

Differences in the pattern of antipredator behaviour between hatchery‐reared and wild European sea bass juveniles

Shoals of hatchery‐reared and wild sea bass juveniles Dicentrarchus labrax were tested for differences in their antipredator responses towards a potential live predator, the eel Anguilla anguilla . Eight experimental shoals ( i.e . replicates), each composed of 15 individuals from the same stock of juveniles ( i.e . wild or hatchery), were video recorded for 5 min before and after predator exposure. A set of behavioural variables were measured during the pre‐stimulus and stimulus phases of each test and compared between the two groups of replicates. Results showed that in both hatchery‐reared and wild juveniles predator exposure elicited a significant increase in the mean level of shoal cohesiveness and mean shoal distance from the predator, and a significant decrease in the mean shoal distance from the bottom. Shoals of wild juveniles, however, aggregated more quickly and reached higher shoal cohesiveness within the first 20 s of the stimulus period than shoals of hatchery‐reared fish. During this period, the wild fish also reached the highest peak in shoal cohesiveness, which then decreased gradually towards the levels observed before predator exposure. Another component of the antipredator response, the predator inspection behaviour, was fully developed in both wild and hatchery fish. Wild fish, however, tended to inspect the predator at a closer distance than hatchery fish.     

Lack of trophic competition among wild and hatchery juvenile chum salmon during early marine residence in Taku Inlet,Southeast Alaska

Early marine trophic interactions of wild and hatchery chum salmon (Oncorhynchus keta) were examined as a potential cause for the decline in harvests of adult wild chum salmon in Taku Inlet, Southeast Alaska. In 2004 and 2005, outmigrating juvenile chum salmon were sampled in nearshore habitats of the inlet (spring) and in epipelagic habitat at Icy Strait (summer) as they approached the Gulf of Alaska. Fish were frozen for energy density determination or preserved for diet analyses, and hatchery stocks were identified from the presence of thermal marks on otoliths. We compared feeding intensity, diets, energy density, and size relationships of wild and hatchery stocks (n = 3123) across locations and weeks. Only hatchery fish feeding intensity was negatively correlated with fish abundance. In both years, hatchery chum salmon were initially larger and had greater energy density than wild fish, but lost condition in early weeks after release as they adapted to feeding on wild prey assemblages. Diets differed between the stocks at all inlet locations, but did not differ for hatchery salmon between littoral and neritic habitats in the outer inlet, where the stocks overlapped most. Both diets and energy density converged by late June. Therefore, if density-dependent interactions affect wild chum salmon, these effects must be very rapid because survivors in Icy Strait showed few differences. Our study also demonstrates that hatchery release strategies used near Taku Inlet successfully promote early spatial segregation and prey partitioning, which reduce the probability of competition between wild and hatchery chum salmon stocks.     

A comparison of prey capture kinematics in hatchery and wild Micropterus salmoides floridanus: effects of ontogeny and experience

Analysis of high‐speed videography demonstrated that juvenile wild Florida largemouth bass Micropterus salmoides floridanus captured live prey with very rapid movements and large excursions. Hatchery fish of the same age, raised on pelleted feed, however, used slower kinematics with smaller excursions, yielding strikes with a higher degree of 'suction'. Capture events of hatchery Florida largemouth bass fed live prey for the first time were characterized by movements that had smaller excursion measurements than wild fish and resulted in a decreased level of capture success. After five exposures to elusive mosquitofish Gambusia holbrooki , hatchery Florida largemouth bass adapted their behaviour to capture prey at the kinematic level of wild fish.     

Stocking hatchery‐reared brown trout in different densities into a wild population – a comparison of growth and movement

In spring 2001 and 2002 a small stream was stocked with tagged hatchery‐reared yearling brown trout ( Salmo trutta ), in order to study their influence on the resident brown trout population. The stream was separated into six sections: two sections without stocking, two sections where stocking doubled the trout population and two sections where the fish population was quadrupled. The working hypothesis was that due to food limitation (competition) growth of the wild fish will be negatively influenced by stocking, and wild fish will be displaced by the (possibly more aggressive) hatchery fish. Surprisingly, growth rate of wild and stocked fish of the same age was similar and independent of stocking density. Two main reasons may be responsible for this finding: only a low percentage of the stocked fish remained in the stream, and food was not limited during summer. Only 12–19% of the stocked fish were recaptured after six months, in contrats to 40–70% of one‐year old and up to 100% of older wild trout. The wild fish were not displaced by hatchery‐reared fish: During summer the wild fish remained more or less stationary, whereas most of the stocked trout had left their release site. The results indicate that in a natural stream stocking of hatchery reared brown trout does not influence negatively growth and movement of the wild fish independent of stocking density.     

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.     

Genetic versus Rearing-Environment Effects on Phenotype: Hatchery and Natural Rearing Effects on Hatchery- and Wild-Born Coho Salmon

With the current trends in climate and fisheries, well-designed mitigative strategies for conserving fish stocks may become increasingly necessary. The poor post-release survival of hatchery-reared Pacific salmon indicates that salmon enhancement programs require assessment. The objective of this study was to determine the relative roles that genotype and rearing environment play in the phenotypic expression of young salmon, including their survival, growth, physiology, swimming endurance, predator avoidance and migratory behaviour. Wild- and hatchery-born coho salmon adults (Oncorhynchus kisutch) returning to the Chehalis River in British Columbia, Canada, were crossed to create pure hatchery, pure wild, and hybrid offspring. A proportion of the progeny from each cross was reared in a traditional hatchery environment, whereas the remaining fry were reared naturally in a contained side channel. The resulting phenotypic differences between replicates, between rearing environments, and between cross types were compared. While there were few phenotypic differences noted between genetic groups reared in the same habitat, rearing environment played a significant role in smolt size, survival, swimming endurance, predator avoidance and migratory behaviour. The lack of any observed genetic differences between wild- and hatchery-born salmon may be due to the long-term mixing of these genotypes from hatchery introgression into wild populations, or conversely, due to strong selection in nature—capable of maintaining highly fit genotypes whether or not fish have experienced part of their life history under cultured conditions.     

Heart rate responses to predation risk in Salmo trutta are affected by the rearing environment

Both wild‐ and hatchery‐reared brown trout Salmo trutta , 18 months of age and of the same genetic origin, responded with increased heart rates (tachycardia) to a simulated predator attack on 2 consecutive days. Brown trout reared in the hatchery showed a more rapidly induced tachycardia compared with wild‐reared fish at day 1, but not day 2. During an undisturbed period several hours after attacks, hatchery‐reared brown trout maintained higher heart rates compared to wild‐reared fish on both days. Behavioural responses to the attack were very low for all fish, although hatchery‐reared fish tended to be more active than wild fish after the attack day 2. The observed differences may have had a genetic background caused by different selection regimes in the hatchery‐ and wild‐rearing environments, or could have been due to different phenotypic responses in the two environments.     

Artificial dietary regime may impair subsequent foraging behaviour of hatchery-reared turbot released into the natural environment

When offered a size range of shrimp Crangon crangon , fewer naïve reared turbot Scophthalmus maximus fed than did wild fish, and those that fed took smaller prey. Analysis of feeding behaviour indicated differences between wild and naïve reared fish in the motivation to feed on novel prey and in prey recognition and capture efficiency. Feeding efficiency and motivation increased with experience and reared fish achieved the feeding rate of wild fish within the 9 days of the experiment. The 'creep' style of approach to shrimp was innate to naïve reared turbot. A comparative feeding experiment confirmed that experienced reared fish ate more prey than naïve reared fish. Naïve reared turbot selected pellets and attacked stones preferentially to shrimp, in contrast to wild and experienced reared fish, which selected shrimp. Stones were attacked due to the memory of pellet-like visual characteristics and this behaviour persisted in some reared fish for at least 6 weeks, illustrating a cost of memory in which changing environmental conditions cause previously learnt information to become misleading. The experimental data also demonstrated that differences may arise in the prey and feeding behaviour of wild and naïve reared fish, but that such differences diminish with experience.     

Less is more: density influences the development of behavioural life skills in trout

Theory suggests that habitat structure and population density profoundly influence the phenotypic development of animals. Here, we predicted that reduced rearing density and increased structural complexity promote food search ability, anti-predator response and the ability to forage on novel prey, all behavioural skills important for surviving in the wild. Brown trout were reared at three densities (conventional hatchery density, a fourth of conventional hatchery density and natural density) in tanks with or without structure. Treatment effects on behaviour were studied on trout fry and parr, whereupon 20 trout from each of the six treatment groups were released in an enclosed natural stream and recaptured after 36 days. Fry reared at natural density were faster to find prey in a maze. Moreover, parr reared at natural density were faster to eat novel prey, and showed more efficient anti-predator behaviour than fish reared at higher densities. Furthermore, parr reared at reduced densities were twice as likely to survive in the stream as trout reared at high density. In contrast, we found no clear treatment effects of structure. These novel results suggest that reduced rearing densities can facilitate the development of behavioural life skills in captive animals, thereby increasing their contribution to natural production.     

Determination of body shape variation in Irish hatchery‐reared and wild Atlantic salmon

Discriminant function analysis was used to distinguish morphologically between samples of parr, smolts and adult Atlantic salmon Salmo salar from several hatchery and river systems in Ireland. The effect of habitat shift was investigated in Atlantic salmon parr. Parr grown from the eyed‐egg stage with a non‐sibling group in a hatchery environment, came to resemble the mean body shape of their host hatchery Atlantic salmon stock more closely than that of a full sibling group grown at their natal hatchery. Wild Atlantic salmon smolts differed in shape from hatchery‐reared smolts. This difference was less pronounced, but still statistically significant when wild adults were compared with hatchery‐reared adults captured in the coastal drift‐net fishery after a year spent at sea. Rearing conditions had a significant impact on the production and growth of fish body shape. This in turn may have affected adaptability and survivorship of ranched Atlantic salmon in the marine environment.     

Factors affecting the post‐release survival of cultured juvenile Pseudopleuronectes americanus

Laboratory experiments were performed with cultured and wild juvenile winter flounder Pseudopleuronectes americanus to evaluate differences in behaviour and adaptation affecting post‐release vulnerability to predation. Studies revealed that the cryptic abilities of cultured winter flounder increased over time. Sediment‐naïve, cultured fish required a minimum of 2 days to improve their burying skills and at least 90 days for colour adaptation to match the sediment. Cultured winter flounder selected sediments consisting of small grains and colours matching their own pigment. Cultured winter flounder, regardless of their colour, were significantly more vulnerable to predation by birds. Additionally, cultured fish reacted differently than wild winter flounder when exposed to cues from a potential predator.     

Impact of live food on survival and growth of hatchery‐reared sea trout (Salmo trutta trutta L.) parr in the wild

Survival rates and growth parameters of hatchery‐reared sea trout (Salmo trutta trutta L.) fry were determined after stocking in the wild. The larvae were hatchery‐reared for 12 weeks in two groups: fry were fed either on live zooplankton and live chironomidae larvae (LFG), or fed a pellet diet (PFG). The survival rate and specific growth rates were higher in the LFG than in the PFG group. Most effective for hatchery‐reared fish intended for stocking was the natural, live feed. The mean number of chironomid larvae found in the stomachs of fish that were initially captured in the wild was significantly higher in the LFG than in the PFG group. The live diet supplied in the rearing period had a positive impact on the foraging skills of the sea trout fry and their survival in the wild after their release on 24 April 2010.