Innovative behaviour in fish: Atlantic cod can learn to use an external tag to manipulate a self-feeder.

This study describes how three individual fish, Atlantic cod (Gadus morhua L.), developed a novel behaviour and learnt to use a dorsally attached external tag to activate a self-feeder. This behaviour was repeated up to several hundred times, and over time these fish fine-tuned the behaviour and made a series of goal-directed coordinated movements needed to attach the feeder's pull string to the tag and stretch the string until the feeder was activated. These observations demonstrate a capacity in cod to develop a novel behaviour utilizing an attached tag as a tool to achieve a goal. This may be seen as one of the very few observed examples of innovation and tool use in fish.

Environmental enrichment promotes neural plasticity and cognitive ability in fish.

Different kinds of experience during early life can play a significant role in the development of an animal's behavioural phenotype. In natural contexts, this influences behaviours from anti-predator responses to navigation abilities. By contrast, for animals reared in captive environments, the homogeneous nature of their experience tends to reduce behavioural flexibility. Studies with cage-reared rodents indicate that captivity often compromises neural development and neural plasticity. Such neural and behavioural deficits can be problematic if captive-bred animals are being reared with the intention of releasing them as part of a conservation strategy. Over the last decade, there has been growing interest in the use of environmental enrichment to promote behavioural flexibility in animals that are bred for release. Here, we describe the positive effects of environmental enrichment on neural plasticity and cognition in juvenile Atlantic salmon (Salmo salar). Exposing fish to enriched conditions upregulated the forebrain expression of NeuroD1 mRNA and improved learning ability assessed in a spatial task. The addition of enrichment to the captive environment thus promotes neural and behavioural changes that are likely to promote behavioural flexibility and improve post-release survival.

A Standardized Protocol for Preference Testing to Assess Fish Welfare.

Animal welfare assessment techniques try to take into consideration the specific needs and wants of the animal in question. Providing enrichment (the addition of physical objects or conspecifics in the housing environment) is often a way to give captive animals the opportunity to choose who or what they interact with and how they spend their time. A fundamental component of the aquatic environment that is often overlooked in captivity, however, is the ability for the animal to choose to engage in physical exercise. For many animals, including fish, exercise is an important aspect of their life history, and is known to have many health benefits, including positive changes in the brain and behavior. Here we present a method for assessing habitat preferences in captive animals. The protocol could easily be adapted to look at a variety of environmental factors (e.g., gravel versus sand as a substrate, plastic plants versus live plants, low flow versus high flow of water) in different aquatic species, or for use with terrestrial species. Statistical assessment of preference is carried out using Jacob's preference index, which ranks the habitats from -1 (avoidance) to +1 (most preferred). With this information, it can be determined what the animal wants from a welfare perspective, including their preferred location.

Habitat stability and predation pressure affect temperament behaviours in populations of three-spined sticklebacks.

1. There is growing interest in the causes and consequences of animal temperaments. Temperament behaviours often have heritable components, but ecological variables can also affect them. Numerous variables are likely to differ between habitats, and these may interact to influence temperament behaviours. 2. Temperament behaviours may be correlated within populations (behavioural syndromes), although the underlying causes of such correlations are currently unclear. 3. We analysed three different temperament behaviours and learning ability in three-spined sticklebacks, Gasterosteus aculeatus, to determine how different ecological variables influence them both within and between populations. We selected populations from four ponds and four rivers that varied naturally in their exposure to predators. 4. High-predation river populations were significantly less bold than a high-predation pond and low-predation river populations, and low-predation pond populations were significantly less bold than a high-predation pond population. Within populations, temperament behaviours were correlated in one high-predation river population only. 5. These results suggest that multiple ecological factors can interact to affect temperament behaviours between populations, and also correlations in those behaviours within populations.

Brain differences in ecologically differentiated sticklebacks.

Populations that have recently diverged offer a powerful model for studying evolution. Ecological differences are expected to generate divergent selection on multiple traits, including neurobiological ones. Animals must detect, process, and act on information from their surroundings and the form of this information can be highly dependent on the environment. We might expect different environments to generate divergent selection not only on the sensory organs, but also on the brain regions responsible for processing sensory information. Here, we test this hypothesis using recently evolved reproductively isolated species pairs of threespine stickleback fish Gasterosteus aculeatus that have well-described differences in many morphological and behavioral traits correlating with ecological differences. We use a state-of-the-art method, magnetic resonance imaging, to get accurate volumetric data for 2 sensory processing regions, the olfactory bulbs and optic tecta. We found a tight correlation between ecology and the size of these brain regions relative to total brain size in 2 lakes with intact species pairs. Limnetic fish, which rely heavily on vision, had relatively larger optic tecta and smaller olfactory bulbs compared with benthic fish, which utilize olfaction to a greater extent. Benthic fish also had larger total brain volumes relative to their body size compared with limnetic fish. These differences were erased in a collapsed species pair in Enos Lake where anthropogenic disturbance has led to intense hybridization. Together these data indicate that evolution of sensory processing regions can occur rapidly and independently.

The long-term benefits of human generosity in indirect reciprocity.

Among the theories that have been proposed to explain the evolution of altruism are direct reciprocity and indirect reciprocity. The idea of the latter is that helping someone or refusing to do so has an impact on one's reputation within a group. This reputation is constantly assessed and reassessed by others and is taken into account by them in future social interactions. Generosity in indirect reciprocity can evolve if and only if it eventually leads to a net benefit in the long term. Here, we show that this key assumption is met. We let 114 students play for money in an indirect and a subsequent direct reciprocity game. We found that although being generous, i.e., giving something of value to others, had the obvious short-term costs, it paid in the long run because it builds up a reputation that is rewarded by third parties (who thereby themselves increase their reputation). A reputation of being generous also provided an advantage in the subsequent direct reciprocity game, probably because it builds up trust that can lead to more stable cooperation.

Environmental variability in the early rearing environment generates behaviourally flexible cod: implications for rehabilitating wild populations.

The release of hatchery-reared fishes for restoring threatened and endangered populations is one of the most controversial issues in applied ecology. A central issue has been to determine whether releases cause extinction of local wild populations. This may arise either through domesticated or non-local fishes hybridizing with wild fishes, or through inappropriate behavioural interactions; for example, many hatchery fishes show exaggerated aggressive and competitive behaviour and out-compete wild counterparts. The impact of the impoverished hatchery environment in shaping behaviour is only now receiving attention. Attempts to counteract hatchery-related behavioural deficiencies have utilized intensive training programmes shortly before the fishes are released. However, we show here that simple exposure to variable spatial and foraging cues in the standard hatchery environment generates fishes with enhanced behavioural traits that are probably associated with improved survival in the wild. It appears that fishes need to experience a varying and changeable environment to learn and develop flexible behaviour. Using variable hatchery rearing environments to generate suitable phenotypes in combination with a knowledge of appropriate local genotypes, rehabilitation of wild fishes is likely to succeed, where to date it has largely failed.

Changing tides: ecological and historical perspectives on fish cognition.

The capacity for specialization and radiation make fish an excellent group in which to investigate the depth and variety of animal cognition. Even though early observations of fish using tools predates the discovery of tool use in chimpanzees, fish cognition has historically been somewhat overlooked. However, a recent surge of interest is now providing a wealth of material on which to draw examples, and this has required a selective approach to choosing the research described below. Our goal is to illustrate the necessity for basing cognitive investigations on the ecological and evolutionary context of the species at hand. We also seek to illustrate the importance of ecology and the environment in honing a range of sensory systems that allow fish to glean information and support informed decision-making. The various environments and challenges with which fish interact require equally varied cognitive skills, and the solutions that fish have developed are truly impressive. Similarly, we illustrate how common ecological problems will frequently produce common cognitive solutions. Below, we focus on four topics: spatial learning and memory, avoiding predators and catching prey, communication, and innovation. These are used to illustrate how both simple and sophisticated cognitive processes underpin much of the adaptive behavioral flexibility exhibited throughout fish phylogeny. Never before has the field had such a wide array of interdisciplinary techniques available to access both cognitive and mechanistic processes underpinning fish behavior. This capacity comes at a critical time to predict and manage fish populations in an era of unprecedented global change.

A framework for investigating animal consciousness.

An assessment of consciousness in nonverbal animals requires a framework for research that extends testing methods beyond subjective report. This chapter proposes a working definition of consciousness in terms of temporal representation that provides the critical link between internal phenomenology and external behavior and neural structure. Our claim is that consciousness represents the present moment as distinct from the past and the future in order to flexibly respond to stimuli. We discuss behavioral and neural evidence that indicates the capacity for both flexible response and temporal representation, and we illustrate these capacities in fish, a taxonomic group that challenges human intuitions about consciousness.

Can we understand how developmental stress enhances performance under future threat with the Yerkes-Dodson law?

Recently we have shown that adult rats exposed to chronic stress during adolescence increase foraging performance in high-threat conditions by 43% compared to rats reared without stress. Our findings suggest that stress during adolescence can prepare rats to better function under future threat, which supports hypotheses describing an adaptive role for the long-term consequences of early stress (e.g. the thrifty phenotype and maternal mismatch hypotheses). These hypotheses often predict that early stress will impair performance in low-threat conditions later in life. However, we did not find any difference in performance under low-threat conditions between adolescent-stressed and unstressed adult animals. To understand why stress during adolescence may affect performance in high-threat but not in low-threat conditions, we discuss our findings in the framework of the Yerkes-Dodson law, a key precept of psychology that has been used for over a century to describe how stress affects performance.

Does Chronic Unpredictable Stress during Adolescence Affect Spatial Cognition in Adulthood?

Spatial abilities allow animals to retain and cognitively manipulate information about their spatial environment and are dependent upon neural structures that mature during adolescence. Exposure to stress in adolescence is thought to disrupt neural maturation, possibly compromising cognitive processes later in life. We examined whether exposure to chronic unpredictable stress in adolescence affects spatial ability in late adulthood. We evaluated spatial learning, reference and working memory, as well as long-term retention of visuospatial cues using a radial arm water maze. We found that stress in adolescence decreased the rate of improvement in spatial learning in adulthood. However, we found no overall performance impairments in adult reference memory, working memory, or retention caused by adolescent-stress. Together, these findings suggest that adolescent-stress may alter the strategy used to solve spatial challenges, resulting in performance that is more consistent but is not refined by incorporating available spatial information. Interestingly, we also found that adolescent-stressed rats showed a shorter latency to begin the water maze task when re-exposed to the maze after an overnight delay compared with control rats. This suggests that adolescent exposure to reoccurring stressors may prepare animals for subsequent reoccurring challenges. Overall, our results show that stress in adolescence does not affect all cognitive processes, but may affect cognition in a context-dependent manner.

Chronic Stress During Adolescence Impairs and Improves Learning and Memory in Adulthood.

HIGHLIGHTS This study tested the effects of adolescent-stress on adult learning and memory.Adolescent-stressed rats had enhanced reversal learning compared to unstressed rats.Adolescent-stress exposure made working memory more vulnerable to disturbance.Adolescent-stress did not affect adult associative learning or reference memory. Exposure to acute stress can cause a myriad of cognitive impairments, but whether negative experiences continue to hinder individual as they age is not as well understood. We determined how chronic unpredictable stress during adolescence affects multiple learning and memory processes in adulthood. Using male Sprague Dawley rats, we measured learning (both associative and reversal) and memory (both reference and working) starting 110 days after completion of an adolescent-stress treatment. We found that adolescent-stress affected adult cognitive abilities in a context-dependent way. Compared to rats reared without stress, adolescent-stressed rats exhibited enhanced reversal learning, an indicator of behavioral flexibility, but showed no change in associative learning and reference memory abilities. Working memory, which in humans is thought to underpin reasoning, mathematical skills, and reading comprehension, may be enhanced by exposure to adolescent-stress. However, when adolescent-stressed animals were tested after a novel disturbance, they exhibited a 5-fold decrease in working memory performance while unstressed rats continued to exhibit a linear learning curve. These results emphasize the capacity for stress during adolescence to transform the cognitive abilities of adult animals, even after stress exposure has ceased and animals have resided in safe environments for the majority of their lifespans.

Do fishes have nociceptors? Evidence for the evolution of a vertebrate sensory system.

Nociception is the detection of a noxious tissue-damaging stimulus and is sometimes accompanied by a reflex response such as withdrawal. Pain perception, as distinct from nociception, has been demonstrated in birds and mammals but has not been systematically studied in lower vertebrates. We assessed whether a fish possessed cutaneous nociceptors capable of detecting noxious stimuli and whether its behaviour was sufficiently adversely affected by the administration of a noxious stimulus. Electrophysiological recordings from trigeminal nerves identified polymodal nociceptors on the head of the trout with physiological properties similar to those described in higher vertebrates. These receptors responded to mechanical pressure, temperatures in the noxious range (more than 40 degrees C) and 1% acetic acid, a noxious substance. In higher vertebrates nociceptive nerves are either A-delta or C fibres with C fibres being the predominating fibre type. However, in the rainbow trout A-delta fibres were most common, and this offers insights into the evolution of nociceptive systems. Administration of noxious substances to the lips of the trout affected both the physiology and the behaviour of the animal and resulted in a significant increase in opercular beat rate and the time taken to resume feeding, as well as anomalous behaviours. This study provides significant evidence of nociception in teleost fishes and furthermore demonstrates that behaviour and physiology are affected over a prolonged period of time, suggesting discomfort.

The evolution of sex differences in spatial ability.

It is widely believed that male mammals have better spatial ability than females. A large number of evolutionary hypotheses have been proposed to explain these differences, but few species have been tested. The authors critically review the proposed evolutionary explanations for sex differences in spatial cognition and conclude that most of the hypotheses are either logically flawed or, as yet, have no substantial support. Few of the data exclusively support or exclude any current hypotheses. The hypothesis with the strongest support proposes that range size was the selection pressure that acted to increase spatial ability. The authors suggest ways in which these hypotheses could be tested by presenting explicit predictions and suggesting suitable test species or conditions.

Novel object test: examining nociception and fear in the rainbow trout.

This study aimed to assess fear responses to a novel object while experiencing a noxious event to determine whether nociception or fear will dominate attention in a fish in novel object testing paradigm. This experimentally tractable animal model was used to investigate (1) the degree of neophobia to a novel object while experiencing noxious stimulation, (2) the response of the fish after removing the fear-causing event by using a familiar object, and (3) the effects of removing the nociceptive response by morphine administration and examining the response to a novel object. Control animals displayed a classic fear response to the novel objects and spent most of their time moving away from this stimulus, as well as showing an increase in respiration rate when the novel object was presented. In contrast, noxiously stimulated animals spent most of their time in close proximity to the novel object and showed no additional increase in respiration rate to novel object presentation. There was evidence of a slight hypoalgesia in noxiously stimulated animals. The responses to familiar objects demonstrated that by familiarizing the animal with the object, fear was removed from the experiment. Both control and noxiously treated animals responded in similar ways to a novel object by spending the majority of their time in close proximity. Treatment with morphine reduced effects of noxious stimulation and appears to be an effective analgesic. After morphine administration, the acid-injected animals showed a neophobic response to a novel object and this was similar to the response of the control fish, with a similar amount of time spent moving away from the object and an increase in ventilation in response to the novel object. Morphine affected the fear response because both groups approached the novel object more quickly than the non-morphine controls. These results suggest that nociception captures the animal's attention with only a relatively small amount of attention directed at responding to the fear of the novel object.

Long-term changes in cognitive bias and coping response as a result of chronic unpredictable stress during adolescence.

Animals that experience adverse events in early life often have life-long changes to their physiology and behavior. Long-term effects of stress during early life have been studied extensively, but less attention has been given to the consequences of negative experiences solely during the adolescent phase. Adolescence is a particularly sensitive period of life when regulation of the glucocorticoid "stress" hormone response matures and specific regions in the brain undergo considerable change. Aversive experiences during this time might, therefore, be expected to generate long-term consequences for the adult phenotype. Here we investigated the long-term effects of exposure to chronic unpredictable stress during adolescence on adult decision-making, coping response, cognitive bias, and exploratory behavior in rats. Rats exposed to chronic unpredictable stress (e.g., isolation, crowding, cage tilt) were compared to control animals that were maintained in standard, predictable conditions throughout development. Unpredictable stress during adolescence resulted in a suite of long-term behavioral and cognitive changes including a negative cognitive bias [F (1, 12) = 5.000, P < 0.05], altered coping response [T (1, 14) = 2.216, P = 0.04], and accelerated decision-making [T (1, 14) = 3.245, P = 0.01]. Exposure to chronic stress during adolescence also caused a short-term increase in boldness behaviors; in a novel object test 15 days after the last stressor, animals exposed to chronic unpredictable stress had decreased latencies to leave a familiar shelter and approach a novel object [T (1, 14) = 2.240, P = 0.04; T (1, 14) = 2.419, P = 0.03, respectively]. The results showed that stress during adolescence has long-term impacts on behavior and cognition that affect the interpretation of ambiguous stimuli, behavioral response to adverse events, and how animals make decisions.

Food anticipatory behaviour as an indicator of stress response and recovery in Atlantic salmon post-smolt after exposure to acute temperature fluctuation.

In this study we evaluated Pavlovian conditioned food anticipatory behaviour as a potential indicator for stress in groups of Atlantic salmon, and compared this with the physiological stress responses of cortisol excretion into water and hyper-consumption of oxygen. We hypothesised that environmental stress would result in reduced feeding motivation. To assess this, we measured the strength of anticipatory behaviour during a period of flashing light that signalled arrival of food. Further, we expected that fish given a reduced food ration would be less sensitive to environmental stress than fish fed full ration. The fish responded to an acute temperature fluctuation with hyper-consumption of oxygen that decreased in line with the temperature, and elevated cortisol excretion up to 1h after the stressor. These physiological responses did not differ significantly between the food ration groups. The anticipatory behaviour was significantly reduced after the stressor and returned to control levels after 1 to 2 h in the reduced ration group, but not until after 3 to 4 h in the full ration group. Our results show that acute stress can be measured in terms of changes to feeding motivation, and that it is a more sensitive indicator of stress that influences the fish over a longer time period than measures of change in cortisol excretion.

Variation in aggressive behaviour in the poeciliid fish Brachyrhaphis episcopi: population and sex differences.

Aggression is often positively correlated with other behavioural traits such as boldness and activity levels. Comparisons across populations can help to determine factors that promote the evolution of such traits. We quantified these behaviours by testing the responses of wild-caught poeciliid fish, Brachyrhaphis episcopi, to mirror image stimuli. This species occurs in populations that experience either high or low levels of predation pressure. Previous studies have shown that B. episcopi from low predation environments are less bold than those that occur with many predators. We therefore predicted that fish from high predation populations would be more aggressive and more active than fish from low predation populations. However, we found the opposite - low predation fish approached a mirror and a novel object more frequently than high predation fish suggesting that 'boldness' and aggression were higher in low predation populations, and that population-level boldness measures may vary depending on context. When tested individually, low predation fish inspected their mirror image more frequently. Females, but not males, from low predation sites were also more aggressive towards their mirror image. Variation in female aggression may be driven by a trade-off between food availability and predation risk. This suggests that the relationship between aggression and boldness has been shaped by adaptation to environmental conditions, and not genetic constraints.

Trophic structure and community stability in an overfished ecosystem.

Since the collapse of the pelagic fisheries off southwest Africa in the late 1960s, jellyfish biomass has increased and the structure of the Benguelan fish community has shifted, making the bearded goby (Sufflogobius bibarbatus) the new predominant prey species. Despite increased predation pressure and a harsh environment, the gobies are thriving. Here we show that physiological adaptations and antipredator and foraging behaviors underpin the success of these fish. In particular, body-tissue isotope signatures reveal that gobies consume jellyfish and sulphidic diatomaceous mud, transferring "dead-end" resources back into the food chain.