Differential responses to environmental challenge by common carp Cyprinus carpio highlight the importance of coping style in integrative physiology.

Common carp Cyprinus carpio displaying proactive or reactive stress coping styles were acclimated to two environmental regimes (low oxygen and low temperature), and selected groups were tested for response to an inflammatory challenge (Escherichia coli lipopolysaccharide, LPS). Plasma glucose and lactate levels were measured, as were selected C. carpio-specific messenger (m)RNA transcript abundance, including cortisol receptor (CR), enolase (ENO), glyceraldehyde 3-phosphate dehydrogenase (GAPDH) and interleukin-1-beta (IL1ß) was measured in individual whole brain samples. Basal levels (in sham injected fish held in normoxic conditions at 25° C) of plasma lactate and glucose differed between coping styles, being significantly lower in proactive individuals. Both variables increased in response to LPS challenge, with the exception of plasma glucose in reactive fish held in hypoxia. Baseline levels of gene expression under control conditions were significantly different for GAPDH between behavioural phenotypes. The responses to experimental challenge were sometimes diametrically opposed between stress-coping styles in a transcript-specific manner. For CR and GAPDH, for example, the response to LPS injection in hypoxia were opposite between proactive and reactive animals. Proactive fish showed decreased CR and increased GAPDH, whereas reactive showed the opposite response. These results further highlight that screening for stress-coping styles prior to experiments in adaptive physiology can significantly affect the interpretation of data obtained. Further, this leads to a more finely tuned analytical output providing an improved understanding of variation in individual responses to both environmental and inflammatory challenge.

Defining, assessing and promoting the welfare of farmed fish.

As currently practised, the culture of fish for food potentially raises concerns about the welfare of farmed fish, and this is a topic that has received considerable attention. As vertebrates, fish share a number of features with the birds and mammals that are more commonly farmed, so many welfare principles derived from consideration of these groups may also be applied to fish. However, fish have a long, separate evolutionary history and are also adapted to a very different, aquatic environment. For these reasons, they have a number of special features that are relevant to how welfare is defined, assessed and promoted and these are discussed. The various methods that are available to researchers for identifying and assessing good and bad welfare in fish are considered, including assessment of physical health and physiological, behavioural and genomic status. The subset of practical welfare indicators that can be used on working farms is also reviewed. Various aspects of intensive aquaculture that can potentially compromise fish welfare are outlined, as are some strategies available for mitigating such adverse effects. Finally, the paper ends by looking briefly to the future, identifying likely changes in aquaculture practices and how these might affect the welfare of farmed fish.

Identifying individual common carp Cyprinus carpio using scale pattern.

Volunteers were able to match photographs of the same common carp Cyprinus carpio taken on two occasions. Images were identified correctly on 95·76% of occasions. Thus, scale patterns can be used for non-invasive identification of C. carpio over a period of time.

The physiology of fish behaviour: a selective review of developments over the past 40 years(§).

During the past 40 years many new techniques have emerged that have been pivotal in furthering understanding of the physiology of fish behaviour. Behavioural studies have been enhanced by video recording systems and software for computerized event recording analysis, fine scale anatomical studies by fluorescence confocal microscopy, neurophysiological studies by visualisation and neuroendocrinology with techniques for identifying, localizing and quantifying many neurochemicals within the central nervous system. This array of approaches has been complemented by developments in molecular biology that include the ability to monitor expression profiles for known genes in specific neural structures and within the whole transcriptome. This article explores how the deployment of new techniques during the last four decades has advanced the understanding of two extensively studied systems. The first of these is the fast-start escape response, concentrating on work on goldfish Carassius auratus and zebrafish Danio rerio. The second is the link between social experience and neuroendocrinology and how this relates to life-history traits in the cichlid Burton's mouthbrooder Astatotilapia burtoni. These two case studies are then used to explore the extent to which the behaviour of animals can be explained in terms of underlying physiological mechanisms.

Boldness and aggressiveness in early and late hatched three-spined sticklebacks Gasterosteus aculeatus.

Levels of boldness and the degree of aggressiveness were compared in juvenile three-spined sticklebacks Gasterosteus aculeatus that had hatched early and late in the breeding season. The most striking result found in this study was that early hatched individuals were bolder when exploring a novel environment than were late-hatched individuals. No differences in levels of aggression between early and late hatchlings were found, but a relationship between boldness and aggressiveness was present regardless of hatching date. The implications of these findings are discussed in the light of research on individual variation in behaviour and the development of behavioural syndromes.

Coping strategies in a strongly schooling fish, the common carp Cyprinus carpio.

Individual common carp Cyprinus carpio were screened repeatedly for risk taking (rate of exploration of a novel, potentially dangerous environment) and for competitive ability (success in gaining access to a spatially restricted food source). Marked differences in behaviour were evident, and significant consistency in individual responses across trials was found for both risk taking and competitive ability. In addition, there was a significant positive relationship between individual performance in these two contexts, with fish that explored more quickly in the novel environment tending to be among the first to gain access to restricted food. In two follow-up studies, resting metabolic rate, blood lactate and glucose and the expression of the cortisol receptor gene in the head kidney and brain were compared in fish from the two extremes of the risk-taking spectrum. Mass-specific metabolic rate was significantly higher in risk-taking than in risk-avoiding fish, while plasma lactate and glucose concentrations and expression of the cortisol receptor gene were lower. It was concluded that a behavioural syndrome based on boldness and aggression exists in C. carpio, as it does in many other animals, and that this is associated with differences in metabolic and stress physiology (down to the genomic level) similar to those described in animals with different coping strategies.

Taking account of fish welfare: lessons from aquaculture.

This paper explores the possibility that lessons learned from aquaculture might contribute to current debate on welfare and fisheries. After looking briefly at the history of research interest in the welfare of farmed fishes, some implications of using different definitions of and approaches to the concept of welfare are discussed. Consideration is given to the way in which the aquaculture industry has responded to public concern about fish welfare and, for cases where these responses have been effective, why this might be the case. Finally, possible cross-over points between aquaculture and fisheries in the context of fish welfare, as well as experience and expertise that might be shared between these two areas, are identified.

Three-spined sticklebacks Gasterosteus aculeatus as a model for exploring behavioural biology.

Niko Tinbergen chose the three-spined stickleback Gasterosteus aculeatus for his classic behavioural studies because they are small, robust, common and easy to house in the laboratory under reasonably natural conditions and also because their behaviour, while sufficiently simple to be tractable, is still sufficiently complex to be interesting. An analysis of citation records shows that this was an inspired choice. Research on these small fish has addressed all four of Tinbergen's famous questions (causation, development, functions and evolution) and has contributed to the understanding of many different behavioural systems. The G. aculeatus literature is used here to explore several themes in fundamental behavioural biology (diet choice, shoaling, behavioural syndromes and sexual signalling) and the extent to which research using G. aculeatus has informed both fundamental and applied behavioural biology, the latter in the context of aquaculture research.

Parasite-associated growth enhancement in a fish-cestode system.

Parasites impose an energetic cost upon their hosts, yet, paradoxically instances have been reported in which infection is associated with enhanced, rather than diminished, host growth rates. Field studies of these parasite effects are problematic, since the pre-infection condition of the hosts is generally unknown. Here, we describe a laboratory experiment in which the growth rate and body condition of 76 laboratory-reared three-spined stickleback fishes were examined before, during and after each fish was fed the infective stage of the parasitic cestode Schistocephalus solidus. Twenty-one of these fishes went on to become infected by the cestode. Fishes were individually housed and provided with an abundant food supply to eliminate the potentially masking effects of variable competitive ability. Infection occurred independently of fish gender, size, body condition or pre-exposure growth rate. After exposure to the cestode, infected fishes grew faster (excluding parasite weight) and maintained a similar or better body condition compared with uninfected fishes, despite developing enlarged spleens. The accelerated growth could not be explained by reduced gonadal development. This result, one of few demonstrations of parasite-associated growth enhancement in fishes, is discussed with respect to other such parasite systems.

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.

How sticklebacks learn to avoid dangerous feeding patches.

Three-spined sticklebacks from sites with a high and a low predation risk were subjected to a passive avoidance test using a simulated attack from an overhead predator to provide negative reinforcement. All the subjects learned to avoid a feeding patch that had been strongly preferred when they received a simulated predatory attack whenever they entered this patch. The fish varied in the way in which they learned this task, in how quickly they did so and in the cues used to discriminate between the safe and the dangerous feeding patch. Some of this variation is related to the predation risk of their site of origin.

Relative size and agonistic behaviour in the female velvet swimming crab, Necora puber (L.) (Brachyura, Portunidae).

Female velvet swimming crabs (Necora puber) fight readily in the laboratory, with interactions being initiated equally often by the larger and smaller of the two opponents, but with the larger usually being victorious. In 17 out of 65 interactions, however, a smaller crab won against a larger one, and possible reasons for this are discussed. In two respects our results are surprising in the context of insights gained from games theory: firstly, the fights do not show a gradual pattern of escalation through display to overt physical violence; and secondly, fights do not become more costly in terms of either potential for injury (intensity) or duration as the contestants became more evenly matched; indeed, as the contestants became more evenly matched, fight duration decreased.

The ecology of endoparasitic helminth infections of brown trout (Salmo trutta) and rainbow trout (Oncorhynchus mykiss) in Scotland.

Two hundred and forty brown trout (Salmo trutta) and 49 rainbow trout (Oncorhynchus mykiss), obtained from 21 locations in Central Scotland between October 1990 and August 1993, were examined for endoparasitic helminth infections. Crepidostomum farionis (Digenea) was the most widely distributed helminth species, followed by Eubothrium crassum (Cestoda), Diphyllobothrium dendriticum and D. ditremum (Cestoda), Neoechinorhynchus rutili (Acanthocephala), Echinorhynchus truttae (Acanthocephala), Eustrongylides sp. (Nematoda), Capillaria salvelini (Nematoda), Cyathocephalus truncatus (Cestoda), Raphidascaris acus (Nematoda) and Cystidicola farionis (Nematoda), in that order. The prevalences and intensities of each helminth infection were recorded. No evidence was found to indicate that even fish with the highest worm burdens (e.g. 339 plerocercoids of Diphyllobothrium spp.) were experiencing any obvious morbidity. An analysis of pairs of associations between species of helminths revealed a significantly positive association between N. rutili and C. farionis (P < 0.01). The results are discussed in terms of patterns in helminth communities in freshwater fish.

Reproductive ecology of a neotropical cichlid fish, Cichla monoculus (Osteichthyes: Cichlidae).

The reproductive ecology of the freshwater fish Cichla monoculus Spix, 1831 (Osteichthyes: Cichlidae) was investigated in the Campo Grande Reservoir, Northeast Brazil. Rainfall, temperature, pH, dissolved oxygen and electrical conductivity of the water were recorded monthly. Fish collected on a monthly basis were measured, weighted, dissected, sexed and the stage of maturation of the gonads were assessed by macro and microscopic means. The semi-arid study region has short spells of rain of 2-3 months duration interspersed with dry seasons. A positive correlation was observed between rainfall and air and water temperatures and conductivity of the water. The study population had an extended spawning season, with peak reproductive activity coinciding with low water temperatures. Males were longer and heavier than females on average and were larger at onset of sexual maturity. The size frequency distributions of the oocytes indicate that C. monoculus is a multiple spawner with an estimated batch fecundity of 3100. Condition factor showed an inverse relationship in relation to gonad size during maturation in both sexes and spent fish were in poor condition. In mature males, lipid stores in the post-occipital cephalic protuberance, a secondary sexual characteristic developed during the reproductive phase, which depleted in spent individuals. The success of this fish is attributed to its reproductive capacity and to the phenotypic plasticity that allows it to adapt to the harsh ecological conditions that prevail in the semi-arid region of Northeast Brazil.

Consistent boldness behaviour in early emerging fry of domesticated Atlantic salmon (Salmo salar): Decoupling of behavioural and physiological traits of the proactive stress coping style.

Individual variation in the way animals cope with stressors has been documented in a number of animal groups. In general, two distinct sets of behavioural and physiological responses to stress have been described: the proactive and the reactive coping styles. Some characteristics of stress coping style seem to be coupled to the time to emerge of fry from spawning redds in natural populations of salmonid fishes. In the present study, behavioural and physiological traits of stress coping styles were compared two and five months after emergence in farmed Atlantic salmon (Salmo salar), using individuals with an early or late time to emerge. Initially, compared to late emerging individuals, early emerging individuals showed a shorter time to resume feeding after transfer to rearing in isolation. Resumption of feeding after isolation was suggested to be related to boldness behaviour, rather than hunger, in the present study. This observation was repeated five months after emergence, demonstrating behavioural consistency over time in this trait. However, in other traits of proactive and reactive stress coping styles, such as social status, resting metabolism or post stress cortisol concentrations, early and late emerging individuals did not differ. Therefore, this study demonstrates that boldness in a novel environment is uncoupled from other traits of the proactive and reactive stress coping styles in farmed salmonids. It is possible that this decoupling is caused by the low competitive environment in which fish were reared. In natural populations of salmonids, however, the higher selection pressure at emergence could select for early emerging individuals with a proactive coping style.

Changes in metabolism and behaviour of the freshwater copepod Cyclops strenuus abyssorum infected with Diphyllobothrium spp.

In a population of copepods (Cyclops strenuus abyssorum), with a naturally high prevalence of infection with procercoids of Diphyllobothrium spp., no difference in body size was found between infected and uninfected hosts. However, a significant reduction in the reproductive capacity of infected females was observed, 87% of uninfected females having developed eggs in their gonads and sacs compared with 21% of infected females. The feeding rate of infected copepods was relatively high soon after infection occurred, but gradually decreased to less than half that of uninfected animals. Respiration rate was also lower in infected copepods. Infected copepods showed reduced motility and impaired escape responses, which is likely to make them more susceptible to predation.

Agonistic behaviour and biogenic amines in shore crabs Carcinus maenas.

To investigate the role of certain neurohormones in agonistic behaviour, fights were staged between pairs of size-matched male shore crabs Carcinus maenas, and blood samples were taken immediately after the contests had been resolved. Samples were also taken from these crabs at rest (before and after fighting) and after walking on a treadmill. A control group of crabs also had samples taken on each experimental day. Concentrations of tyramine, dopamine, octopamine, serotonin (5-HT) and norepinephrine were determined in each blood sample using a gas chromatography/mass spectrometry (GC-MS) system. Norepinephrine was not detectable in any of the samples, but the standards were recovered. Tyramine values were not significantly different between the control group and the fought group, so tyramine does not appear to be important in agonistic behaviour. A comparison between the control and fought groups shows that fighting had an effect on the concentrations of octopamine, dopamine and 5-HT, but exercise only had an effect on octopamine levels, which showed a reduction from resting values in both winners and losers. Resting and post-fight concentrations of octopamine, dopamine and 5-HT were higher in winners than in losers. 5-HT concentration increased in the blood of fought crabs from resting values, whereas dopamine concentration decreased. In winners, octopamine concentrations decreased from resting values, but in losers octopamine levels increased from resting concentrations. The escalatory behaviour or intensity of fighting performed by winners and losers was related to dopamine levels but not to those of octopamine or 5-HT. Therefore, there appears to be a link between relative concentrations of these three amines (dopamine, octopamine and 5-HT) and fighting ability; the effects are not simply a result of activity. The better competitors have higher concentrations of these three amines at rest and after fighting.

Early social status and the development of life-history strategies in Atlantic salmon.

Atlantic salmon have a variable life cycle. In good growing conditions, underyearling fish may metamorphose into the migratory smolt phase during their second spring, or delay at least a further year. The strategy adopted by particular fish appears to become fixed during their first summer. This paper examines whether either feeding efficiency or dominance in mid-summer correlates with the life-history strategy adopted. Eighty fish were individually marked and their feeding efficiency (= mean handling time for food items) and dominance rank measured under laboratory conditions in mid-July. Growth rates of the fish were then monitored over the next three months, until developmental strategies became apparent. Discriminant and logistic regression analyses revealed that both dominance rank and size attained by July were independent, significant predictors of future developmental pattern (the age at metamorphosis being correctly predicted on the basis of rank and size in 84% of cases) whereas feeding efficiency had no effect. Thus fish that were dominant or larger two months after first feeding or both had a greater probability of migrating after only one year in freshwater than those more subordinate or smaller or both.