Colin E. Adams

Behavioural syndromes in farmed fish: implications for production and welfare

Consistent individual differences in behaviour have been described for several species of salmonid fish, the group that has been most intensively farmed. In particular, fish accept different levels of risk when competing for limited resources and, in nature, the different behavioural phenotypes seem to perform better in different environmental conditions. Studies of the behaviour of farmed fish can provide insights into the genetic basis of such differences and into their consequences for some components of fitness. Both deliberate selection for fast growth in farmed fish and inadvertent selection of fish that flourish in intensive aquaculture systems have generated inherited behavioural differences between farmed fish and the wild stocks from which they originated. Thus, fish from farmed stocks tend to be bolder and to take greater risks when foraging; they may also be more aggressive, depending both on conditions during selection and the environment used to screen aggressiveness. Such results indicate the existence of inherited variation in risk-taking and aggression in the populations from which todays farmed stocks were derived. They also suggest that fish from the risk-avoiding/non-aggressive end of the behavioural spectrum may fail to flourish in conditions that usually prevail in intensive husbandry systems. The implications of these findings for production and welfare in aquaculture are discussed.

Alternative competitive strategies and the cost of food acquisition in juvenile Atlantic salmon (Salmo salar)

Aggressive interactions were recorded for 3 h per day in 11 groups of 10, 1+, juvenile Atlantic salmon given access to a limited food supply. Observations were made over nine-day periods in which the dominant (most aggressive) fish on each day was identified and removed. In all groups at the start of the study, one (usually relatively large) fish performed most (67% overall) of the aggressive acts. Feeding activity was also polarised, though less strongly so, with the two most actively feeding fish taking on average 41% of the food supplied. Behavioural polarisation was also marked at a later stage in the study, when five fishes remained in each group, but rates of aggression per fish increased markedly over successive days. Food intake was positively related to aggression, but not to relative size once the size/aggression relationship was corrected statistically. The relationship between aggression and food intake on the first day of testing was weak (R2=8%); in particular, 30% gained no food in spite of behaving aggressively, while 11% obtained food even though they showed no aggression. The proportion of attacks received was positively, but weakly (R2=5%) related to feeding rates, but not to level of aggression. As a consequence, fishes that engaged in neither feeding nor fighting were attacked less frequently than others in the group. These results, which suggest that the risk of injury may act as a counter-selection against some strategies for food acquisition, are discussed in the context of previous work on resource competition in salmonid fishes.

Population genetic structure of Arctic Charr, Salvelinus alpinus from northwest Europe on large and small spatial scales

To examine the population genetic structure of lake‐resident Arctic charr, Salvelinus alpinus from northwest Europe on multiple spatial scales, 2367 individuals from 43 lakes located in three geographical regions (Iceland, the British Isles and Scandinavia) were genotyped at six microsatellite loci. On a large scale, data provided little evidence to support clustering of populations according to geographical region. Hierarchical analysis of molecular variance indicated that, although statistically significant, only 2.17% of the variance in allelic frequencies was partitioned at the among‐region level. Within regions, high levels of genetic differentiation were typically found between lakes regardless of the geographical distance separating them. These results are consistent with the hypothesis of rapid postglacial recolonization of all of northwest Europe from a single charr lineage, with subsequent restriction of gene flow. On a smaller scale, there was evidence for close genetic relationships among lakes from within common drainage basins in Scotland. Thus, interlake genetic structure reflects localized patterns of recent (or contemporary) gene flow superimposed onto a larger scale structure that is largely a result of historical processes. There was also evidence for widespread genetic structuring at the within‐lake level, with sympatric populations detected in 10 lakes, and multilocus heterozygote deficits found in 23 lakes. This evidence of the Wahlund effect was found in all lakes known to contain discrete phenotypic morphs, as well as many others, suggesting that morphs may often represent separate breeding populations, and also that the phenomenon of polymorphism in this species may be more widespread than is currently realized.

Exercise, agonistic behaviour and food acquisition in Arctic charr, Salvelinus alpinus

SynopsisAlthough swimming is energetically costly, a number of studies on salmonid species have demonstrated increased growth rates in fishes forced to swim for prolonged periods at moderate speeds (typically 1–2 body lengths per sec). This suggests that additional energetic costs of swimming are more than met by alternative compensatory gains. The mechanisms underlying such effects are not fully understood. In this paper, we describe an experiment designed to examine one possible mechanism, namely a swimming-induced inhibition of aggression, with consequent beneficial effects on growth. The study used Arctic charr,Salvelinus alpinus, a species for which a positive relationship between exercise and growth has been clearly established. Using direct behavioural observations on small groups, we demonstrate that individuals displaying high levels of aggressive behaviour are able to monopolise access to food and that enforced swimming at a moderate speed (1 body length per sec) reduces the incidence of aggression although not the degree of monopolisation of food shown by aggressive individuals. These results suggest that the enhanced growth rates accompanying enforced swimming may reflect lower energetic costs of reduced aggressive activity rather than improved access to food by subordinates.

Photoperiod and temperature effects on early development and reproductive investment in Atlantic salmon (Salmo salar L.)

Abstract By manipulating the growth opportunity of underyearling Atlantic salmon parr, via photoperiod and temperature control, Thorpes (1986) model of growth, smoltification and maturity was tested. Under relatively good conditions for growth during the maturation “window” in February, male parr subsequently became sexually mature as underyearlings. Females, exposed to good growth conditions, did not become mature but they increased their reproductive investment by increasing oocyte size.

Attack site and resultant damage during aggressive encounters in Atlantic salmon (Salmo salar L.) parr

Fin rot is a term used to describe a range of changes in fins, from splitting and erosion to nodular thickening. It is common among farmed Atlantic salmon (Salmo salar) parr and is of considerable economic and welfare importance. Fin rot is known to commence when fins become damaged, for example, following attacks by conspecifics; however, not all fins are equally affected, the dorsal fin being much more frequently damaged. This study examined the hypothesis that fin rot is more prevalent in the dorsal fin because it is more frequently attacked during aggressive encounters with conspecifics. Behavioural observations showed that the dorsal and caudal fin areas are much more frequently attacked than other areas of the body and significantly more attacks directed at the dorsal fin area resulted in physical contact than attacks directed at other parts of the body. Fin damage, scored as the total amount of fin splitting was highest in the dorsal and pectoral fins despite the pectoral fins being attacked less frequently than the dorsal or caudal fins. This suggests that pectoral fins may have sustained damage through contact with the tank as well as through attacks. We conclude that at least one reason for the observed prevalence of fin rot in the dorsal fin of Atlantic salmon in aquaculture systems is that it is a preferred site of attack by conspecifics and because attacks are more likely to end in physical contact than attacks on other areas of the body and, thus, they sustain more damage.

The functional significance of inherited differences in feeding morphology in a sympatric polymorphic population of Arctic charr

Artificially fertilised eggs from wild-caught Arctic charr parents of two sympatric morphs (benthivorous and planktivorous) from Loch Rannoch, Scotland were reared in the laboratory under identical conditions. During the subsequent 2 years, aspects of their trophic anatomy and feeding behaviour were compared. As previously described for wild-caught fish, charr derived from the benthivorous morph had an increasingly wider mouth gape for a given body length than those derived from the planktivorous morph. The functional significance of these differences in gape was tested by comparing the maximum size of prey that could be handled by each of the two morphs. In both forms, a larger gape enabled larger food particles to be eaten, but the elevation of the regression of maximum prey size on gape was higher in the benthivorous form, indicating the existence of additional morphological and/or behavioural differences influencing the size of prey consumed. When offered a choice between a typical benthic prey item and a typical pelagic food item, charr of benthivorous origin were more likely to feed on the former, whereas those of planktivorous origin were more likely to feed on the latter. Thus inherited differences in gape place constraints on foraging ability and are associated with inherited differences in dietary preference. We conclude that the functional significance of the foraging specialisations indicate a strong selection pressure for the evolution of the divergence and propose that heterochronic growth is the mechanism resulting in the divergence of tropic anatomy.

Some influences of photoperiod and temperature on opportunity for growth in juvenile Atlantic salmon, Salmo salar L.

Abstract The greater the opportunity for growth (represented by °C-daylight h as a thermal sum index) in mid- to late-summer, especially July, the greater the proportion of young Atlantic salmon populations that maintained rather than arrested growth. Under experimental photoperiods out of phase with the natural cycle, the effect was also evident in the fishs ‘perceived’ May–July, indicating growth regulation by change in photoperiod as well as by temperature.

Does breeding site fidelity drive phenotypic and genetic sub-structuring of a population of Arctic charr?

There is now increasing acceptance that divergence of phenotypic traits, and the genetic structuring that underlie such divergence, can occur in sympatry. Here we report the serendipitous discovery of a sympatric polymorphism in the upper Forth catchment, Scotland, in a species for which high levels of phenotypic variation have been reported previously, the Arctic charr, Salvelinus alpinus. Attempting to determine the proximate mechanisms through which this pattern of phenotypic variation is maintained, we examine the use of the available feeding resource and the genotypic and phenotypic structure of charr in this system. We show clear differences in head morphology between charr from three very closely connected lakes with no barrier to movement (Lochs Doine, Voil and Lubnaig) and also differences in muscle stable isotope signatures and in stomach contents. There were significant differences at 6 microsatelite loci (between Lubnaig and the other two lochs) and very low estimates of effective migration between populations. We conclude that, despite living in effective sympatry, strong genetic and phenotypic sub-structuring is likely maintained by very high levels of site fidelity, especially during spawning, resulting in functional allopatric divergence of phenotype.

Size heterogeneity can reduce aggression and promote growth in Atlantic salmon parr

Aggression in groups of 0+ Atlantic salmon (Salmo salar) was monitoredat weekly intervals in two tanks containing 100 fish each. Three 1 + salmonparr were added to one of these. After 5 weeks, fish weights were measuredin both tanks and the conditions reversed. At ten weeks, weights of fish inboth tanks were measured again. In both populations, levels of aggressionamong the smaller fish were significantly lower and growth ratessignificantly higher when the large fish were present. Although the largefish attacked the small ones, the rate at which they did so was an order ofmagnitude lower that the rate at which small fish attacked each other in theabsence of larger conspecifics. This raises the possibility that levels ofaggression among farmed salmon might be reduced by the addition of a fewlarge conspecifics.