Becoming a better swimmer: structural complexity enhances agility in a captive-reared fish.

To test whether swimming skills can be improved by exposure to structurally complex environments, juvenile rainbow trout Oncorhynchus mykiss were reared in either physically enriched or plain tanks for 2 months and were then screened to test their ability to swim along a channel while avoiding obstructions. The results show that even a relatively short exposure period to enrichment improves O. mykiss swimming agility.

The influence of complex and threatening environments in early life on brain size and behaviour.

The ways in which challenging environments during development shape the brain and behaviour are increasingly being addressed. To date, studies typically consider only single variables, but the real world is more complex. Many factors simultaneously affect the brain and behaviour, and whether these work independently or interact remains untested. To address this, zebrafish (Danio rerio) were reared in a two-by-two design in housing that varied in structural complexity and/or exposure to a stressor. Fish experiencing both complexity (enrichment objects changed over time) and mild stress (daily net chasing) exhibited enhanced learning and were less anxious when tested as juveniles (between 77 and 90 days). Adults tested (aged 1 year) were also less anxious even though fish were kept in standard housing after three months of age (i.e. no chasing or enrichment). Volumetric measures of the brain using magnetic resonance imaging (MRI) showed that complexity alone generated fish with a larger brain, but this increase in size was not seen in fish that experienced both complexity and chasing, or chasing alone. The results highlight the importance of looking at multiple variables simultaneously, and reveal differential effects of complexity and stressful experiences during development of the brain and behaviour.

Learning rate and temperament in a high predation risk environment.

Living in challenging environments can influence the behavior of animals in a number of ways. For instance, populations of prey fish that experience frequent, nonlethal interactions with predators have a high proportion of individuals that express greater reaction to risk and increased activity and exploration-collectively known as temperament traits. Temperament traits are often correlated, such that individuals that are risk-prone also tend to be active and explore more. Spatial learning, which requires the integration of many sensory cues, has also been shown to vary in fish exposed to different levels of predation threat. Fish from areas of low predation risk learn to solve spatial tasks faster than fish from high predation areas. However, it is not yet known whether simpler forms of learning, such as learning associations between two events, are similarly influenced. Simple forms of associative learning are likely to be affected by temperament because a willingness to approach and explore novel situations could provide animals with a learning advantage. However, it is possible that routine-forming and inflexible traits associated with risk-prone and increased exploratory behavior may act in the opposite way and make risk-prone individuals poorer at learning associations. To investigate this, we measured temperament in Panamanian bishop fish (Brachyrhaphis episcopi) sampled from a site known to contain many predators. The B. episcopi were then tested with an associative learning task. Within this population, fish that explored more were faster at learning a cue that predicted access to food, indicating a link between temperament and basic learning abilities.

Pain and stress responses in farmed fish.

Farming fish for human consumption continues to expand as an industry and, with this increasing interaction with captive fish populations, there is now a growing interest in determining how to create good welfare for the fish we farm. This article summarises recent advances in our understanding of pain and stress responses in fish and how these relate to farmed fish welfare. Over the last decade several studies have examined whether or not fish feel pain, how aversive the experience is, and how such experiences may be mitigated through the use of analgesics. The basic neural mechanisms that enable the detection of tissue damage, i.e. nociceptive mechanisms, appear to be broadly conserved from fish through to birds and mammals, however, there is debate about the extent of the negative feelings associated with pain and whether these are truly experienced by fish. The stress response that helps fish to cope with various challenges also appears to be largely conserved across vertebrates, and the physiological changes that occur in response to acute and chronic stress in fish are similar to those described for mammals. Therefore, fish appear to have the innate ability to experience negative states such as pain and stress in a way analogous to that experienced by other vertebrates. There are multiple situations in which farmed fish may experience pain and stress and there is now a growing recognition that, to deliver appropriate welfare, on-farm practices and procedures will have to change. It is also the case that the welfare requirements of the different fish species that we farm vary, with some species coping better in captive rearing environments than others. The topic of fish welfare is relatively new and more research on stress responses, allostasis, pain thresholds and analgesics is required to help promote good fish welfare.

Aluminum exposure impacts brain plasticity and behavior in Atlantic salmon (Salmo salar).

Aluminum (Al) toxicity occurs frequently in natural aquatic ecosystems as a result of acid deposition and natural weathering processes. Detrimental effects of Al toxicity on aquatic organisms are well known and can have consequences for survival. Fish exposed to Al in low pH waters will experience physiological and neuroendocrine changes that disrupt homeostasis and alter behavior. To investigate the effects of Al exposure on both the brain and behavior, Atlantic salmon (Salmo salar) kept in water treated with Al (pH 5.7, 0.37±0.04 µmol 1(-1) Al) for 2 weeks were compared with fish kept in under control conditions (pH 6.7, <0.04 µmol 1(-1) Al). Fish exposed to Al and acidic conditions had increased Al accumulation in the gills and decreased gill Na(+), K(+)-ATPase activity, which impaired osmoregulatory capacity and caused physiological stress, indicated by elevated plasma cortisol and glucose levels. Here we show for the first time that exposure to Al in acidic conditions also impaired learning performance in a maze task. Al toxicity also reduced the expression of NeuroD1 transcript levels in the forebrain of exposed fish. As in mammals, these data show that exposure to chronic stress, such as acidified Al, can reduce neural plasticity during behavioral challenges in salmon, and may impair the ability to cope with new environments.

Environmental effects on fish neural plasticity and cognition.

Most fishes experiencing challenging environments are able to adjust and adapt their physiology and behaviour to help them cope more effectively. Much of this flexibility is supported and influenced by cognition and neural plasticity. The understanding of fish cognition and the role played by different regions of the brain has improved significantly in recent years. Techniques such as lesioning, tract tracing and quantifying changes in gene expression help in mapping specialized brain areas. It is now recognized that the fish brain remains plastic throughout a fish's life and that it continues to be sensitive to environmental challenges. The early development of fish brains is shaped by experiences with the environment and this can promote positive and negative effects on both neural plasticity and cognitive ability. This review focuses on what is known about the interactions between the environment, the telencephalon and cognition. Examples are used from a diverse array of fish species, but there could be a lot to be gained by focusing research on neural plasticity and cognition in fishes for which there is already a wealth of knowledge relating to their physiology, behaviour and natural history, e.g. the Salmonidae.

Increased exposure to predators increases both exploration and activity level in Brachyrhaphis episcopi.

Two temperament traits, tendency to explore and activity level, were measured in a tropical poeciliid fish, the Panamanian bishop Brachyrhaphis episcopi. Open-field arena tests were used to quantify how predation pressure shapes activity levels and exploratory behaviours. Fish behaviour differed between high and low-predation populations. Fish that experienced higher levels of predation were both more explorative and more active. There were also some individual differences within populations; fish varied in their levels of exploration and activity in a novel open arena, but these differences were not related to sex or size. Together with previous studies on this species, these results indicate that there is a behavioural syndrome associated with predation pressure. Fish from high-predation populations are bolder, more explorative and more active than those from low-predation populations.

Stressed mothers - troubled offspring: a study of behavioural maternal effects in farmed Salmo salar.

Mature female Atlantic salmon Salmo salar were given intraperitoneal cortisol implants 1 week prior to stripping to examine the influence of simulated maternal stress on offspring boldness and social dominance. Behavioural tests originally designed to investigate stress responsiveness and coping styles in salmonids (i.e. feeding in isolation, dominance tests and acute confinement) were carried out on the offspring 1·5 years after hatching. In the feeding test, there were no differences between the two treatment groups in total feeding score or number of pellets eaten, but offspring from the cortisol-implanted females made more unsuccessful feeding attempts than offspring from control females. In dominance tests, there was no difference between controls and cortisol-treated fish regarding propensity to become socially dominant. A higher proportion of individuals with bite marks, however, was observed in the cortisol group when compared to controls. Cortisol-treated offspring that gained dominant rank in the dominance tests performed more aggressive acts after stable dominance-subordinate relationships were established compared to control winners. During acute confinement stress, offspring from cortisol-implanted females showed a reduction in the proportion of time they were moving compared to the controls. These results indicate that the maternal endocrine state at spawning affects several aspects of progeny behaviour potentially related to subsequent success and survival in farmed S. salar.

Restoring depleted coral-reef fish populations through recruitment enhancement: a proof of concept.

To determine whether enhancing the survival of new recruits is a sensible target for the restorative management of depleted coral-reef fish populations, settlement-stage ambon damsel fish Pomacentrus amboinensis were captured, tagged and then either released immediately onto small artificial reefs or held in aquaria for 1 week prior to release. Holding conditions were varied to determine whether they affected survival of fish: half the fish were held in bare tanks (non-enriched) and the other half in tanks containing coral and sand (enriched). Holding fish for this short period had a significantly positive effect on survivorship relative to the settlement-stage treatment group that were released immediately. The enrichment of holding conditions made no appreciable difference on the survival of fish once released onto the reef. It did, however, have a positive effect on the survival of fish while in captivity, thus supporting the case for the provision of simple environmental enrichment in fish husbandry. Collecting and holding settlement-stage fish for at least a week before release appear to increase the short-term survival of released fish; whether it is an effective method for longer-term enhancement of locally depleted coral-reef fish populations will require further study.

Pain perception, aversion and fear in fish.

There is now compelling evidence that teleost fish possess similar nociceptive processing systems to those found in terrestrial vertebrates. Noxious stimulation of these nociceptors--specialised pain receptors -in the skin around the snout of fish generates neural activity that can be electrophysiologically recorded, and induces a number of behavioural and physiological changes. To determine whether changes in behaviour are more than simple responses to the noxious stimulation it is necessary to demonstrate that higher order cognitive processes such as mental state or 'affective state' are involved. However, quantifying the 'motivational affected state' of an animal--a concept encompassing not just pain but also fear, hunger, thirst and pleasure - is difficult owing to its subjectivity. Recent empirical work is beginning to test these concepts in fish, and we review a number of these studies and suggest how these general methodologies could be used to further our understanding of fish cognition and the capacity for fish to experience mental states such as fear or suffering.

Can personality predict individual differences in brook trout spatial learning ability?

While differences in individual personality are common in animal populations, understanding the ecological significance of variation has not yet been resolved. Evidence suggests that personality may influence learning and memory; a finding that could improve our understanding of the evolutionary processes that produce and maintain intraspecific behavioural heterogeneity. Here, we tested whether boldness, the most studied personality trait in fish, could predict learning ability in brook trout. After quantifying boldness, fish were trained to find a hidden food patch in a maze environment. Stable landmark cues were provided to indicate the location of food and, at the conclusion of training, cues were rearranged to test for learning. There was a negative relationship between boldness and learning as shy fish were increasingly more successful at navigating the maze and locating food during training trials compared to bold fish. In the altered testing environment, only shy fish continued using cues to search for food. Overall, the learning rate of bold fish was found to be lower than that of shy fish for several metrics suggesting that personality could have widespread effects on behaviour. Because learning can increase plasticity to environmental change, these results have significant implications for fish conservation.

Chronic unpredictable stress during adolescence causes long-term anxiety.

Exposure to stress during adolescence can cause long-term changes in behavior and cognition. Anxiety diagnoses rise during adolescence and are increased by adverse experiences. Currently, it is unknown how long stress during adolescence alters anxiety in adulthood. We found that rats exposed to chronic unpredictable stress during adolescence expressed altered behavior 6.5 months later; showing increased anxiety in a feeding test in a novel environment. Although behavioral changes indicative of anxiety were detected in late adulthood, the basal levels of fecal corticoid metabolites in prior-stressed rats did not differ from unstressed, control rats.

Population variation in lateralized eye use in the poeciliid Brachyraphis episcopi.

Differential use of each hemisphere of the brain for specific tasks is a widespread phenomenon that appears to have arisen in the early history of tetrapod lineage. Despite a high degree of conformity in the development of lateralization among the tetrapods, some variation exists. The mechanisms underlying this variation remain largely unresolved. We exposed fish from regions of high and low predation pressure to a series of visual experiences, including viewing an empty compartment, a novel object and a live predator. Fish from each region differed in their preferential use of each eye to view the scenes. For example, fish from high predation regions viewed a live predator by using their right eye, whereas fish from low predation sites showed no eye preference. These results suggest that the degree of lateralization varies between populations of the same species that have been exposed to different ecological/evolutionary pressures.

Spatial working memory in rats: no differences between the sexes.

In a number of mammalian species, males appear to have superior spatial abilities to females. The favoured explanations for this cognitive difference are hormonal, with higher testosterone levels in males than females leading to better spatial performance, and evolutionary, where sexual selection has favoured males with increased spatial abilities for either better navigational skills in hunting or to enable an increased territory size. However, an alternative explanation for this sex difference focuses on the role of varying levels of oestrogen in females in spatial cognition (the 'fertility and parental care' hypothesis). One possibility is that varying oestrogen levels result in variation in spatial learning and memory so that, when tested across the oestrous cycle, females perform as well as males on days of low oestrogen but more poorly on days of high oestrogen. If day in the oestrous cycle is not taken into account then, across an experiment, any sex differences found would always produce male superiority. We used a spatial working memory task in a Morris water maze to test the spatial learning and memory abilities of male and female rats. The rats were tested across a number of consecutive days during which the females went through four oestrous cycles. We found no overall sex differences in latencies to reach a submerged platform in a Morris water maze but, on the day of oestrus (low oestrogen), females took an extra swim to learn the platform's location (a 100% increase over the other days in the cycle). Female swim speed also varied across the oestrous cycle but females were no less active on the day of oestrus. These results oppose the predictions of the fertility and parental care hypothesis.

Indirect fitness consequences of mate choice in sticklebacks: offspring of brighter males grow slowly but resist parasitic infections.

'Good genes' models of sexual selection suggest that elaborate male sexual ornaments have evolved as reliable signals of male quality because only males of high genetic viability are able to develop and maintain them. Females benefit from choosing such individuals if quality is heritable. A key prediction is that the offspring of males with elaborate mating displays will perform better than those of less elaborate males, but it has proved difficult to demonstrate such an effect independently of the effects of differences in parental investment. We tested for 'good genes' linked to male ornamentation in the three-spined stickleback Gasterosteus aculeatus using in vitro fertilization to generate maternal half-siblings, which were raised without parental care. Maternal half-siblings sired by brightly coloured males grew less quickly than half-siblings sired by dull males but were more resistant to a controlled disease challenge. Among the offspring that became infected, those with brighter fathers had higher white blood cell counts. This suggests that highly ornamented males confer disease resistance on their offspring. The association with reduced growth suggests a mechanism for the maintenance of heritable variation in both disease resistance and male sexual coloration.

Social-psychological factors affecting help-seeking for emotional problems.

Predictors of the attitudinal measure of orientation toward help-seeking for emotional problems have been shown to include demographic, network, and personality variables. This research determined whether these same variables predict the behavioral outcome measure of help-seeking, both in general and from professional services in particular. Help-seeking in response to emotional problems was studied in a sample of Australian adolescents. General help-seeking was predicted by more symptoms of psychological distress, being female, availability of social support, knowing someone who had sought professional help, and the personality characteristics of high private self-consciousness and willingness to disclose mental health. When only those with evident emotional distress were considered, only gender and willingness to disclose remained significant predictors. These same variables did not account for those who sought professional help rather than relying upon their informal network. Level of psychological distress was the only significant predictor of professional consultation. Psychological symptoms and gender were shown to be more relevant predictors of the behavioral measure of help-seeking than network or personality characteristics.

An exploratory study of poor adjustment styles among retirees.

This paper focuses on the one third of retirees who report difficulty in making the transition from work to retirement. On the basis of Levy's [16] research, it is hypothesized that there are different styles of poor adjustment that have different consequences for the retirees experiencing them. Data from 487 male and female retirees identify four poor adjustment styles--poor health, negativism, change adaptation and retirement reluctance. While the latter two responses to retirement tend to be problems only in the short term, the former two may have far reaching consequences. Health related retirement and negativism about retiring were linked with low activity and involvement, poor physical and mental health, inadequate income and low life satisfaction in the years following retirement.

Discrimination and recognition of photographs of places by homing pigeons.

Operant studies on pigeons using slide-projected images suggest that photographs of geographical locations might be used as a research tool to study the importance of visual landmarks in homing. Before using this method, however, it is necessary to show that pigeons do see photographic slides as representing real world locations. After reviewing the evidence for picture-to-object correspondence for geographical locations in pigeons, we report the results of an experiment designed to test whether outdoor experience at a location affected homing pigeons' ability to categorise slides of that versus another location displayed in an operant set-up. Four birds visited one location immediately before each experimental session; four birds visited an irrelevant location. No effect of outdoor experience was found on acquisition, or transfer to novel stimuli. The possible reasons for limitations on picture-to-object correspondence are discussed.

How ecology shapes prey fish cognition.

Fish exhibit diverse cognitive capacities: they cooperate, punish, develop cultural traditions, learn to map their environment and communicate their intentions to one another. Skills such as these have helped fish radiate to colonize the many and diverse aquatic niches available. Prey fish are no exception to this, and several recent studies have shown them to be a rich resource for understanding the evolutionary ecology of animal cognition. Many fish have to cope with the threat of predation, but some environments contain more predators than others. These environments deliver the opportunity to investigate how predation pressure shapes fish cognition and behaviour. Here we compared fish from two high and two low predation habitats in their ability to learn a sequential choice spatial task. We also investigated their ability to solve the maze after it was rearranged. Fish from high predation sites made more errors as they learned to navigate the maze than fish from low predation sites. The fish also varied in the cues that they learned to help them solve the task. These did not vary by levels of predation pressure, rather, they differed between rivers, with fish from one river learning to use landmark cues, and those from the other river learning the sequence of left and right turns. As the different populations varied in how well they learned to navigate through a reconfigured maze, it seems likely that predation pressure is not the only factor influencing spatial behavior in these fish.

Reproductive isolation in a threespine stickleback hybrid zone.

In many estuarine sites, morphological and genetic differences between anadromous and freshwater threespine sticklebacks are maintained despite breeding in sympatry. Here, we investigate the maintenance of this morphological divergence in a natural hybrid zone in the River Tyne, Scotland. We provide a morphological description of the hybrid zone, and using a Bayesian MCMC approach, identified distinct anadromous and freshwater genetic clusters. Anadromous and freshwater sticklebacks breed in spatial and temporal sympatry in the lower reaches of the River Tyne. The frequency of hybrids within these sites (33%) indicates prezygotic isolation is not complete, and suggests that assortative mating is not strong. However, significant heterozygote deficit and cytonuclear disequilibrium in juveniles collected from sympatric sites confirms that barriers to gene flow exist between the morphs in the wild. In addition, we found no evidence of a directional bias in hybridisation, although hybrids with anadromous mothers were more common because anadromous females outnumbered freshwater females within the hybrid zone. We discuss the potential contribution of temporal, spatial, and sexual prezygotic barriers to the observed reproductive isolation as well as postzygotic selection against hybrid zygotes or fry.