Aquaculture International8: 543–549, 2000.© 2000Kluwer Academic Publishers. Printed in the Netherlands.

Short Communication

Size heterogeneity can reduce aggression and promotegrowth in Atlantic salmon parr

COLIN ADAMS, FELICITY HUNTINGFORD1, JIMMY TURNBULL 2,STEVE ARNOTT1 and ALY BELLFish Biology Group, University Field Station, University of Glasgow, Glasgow G63 0AW,UK; 1Fish Biology Group, Division of Evolutionary and Environmental Biology, Institute ofBiological and Life Sciences, Graham Kerr Building, University of Glasgow, Glasgow G128QQ, UK;2Institute of Aquaculture, University of Stirling, Stirling FK9 4LA, UK

(Received 1 March 1999; accepted 19 June 2000)

Abstract. Aggression in groups of 0+ Atlantic salmon (Salmo salar) was monitored at weeklyintervals in two tanks containing 100 fish each. Three 1 + salmon parr were added to one ofthese. After 5 weeks, fish weights were measured in both tanks and the conditions reversed.At ten weeks, weights of fish in both tanks were measured again. In both populations, levelsof aggression among the smaller fish were significantly lower and growth rates significantlyhigher when the large fish were present. Although the large fish attacked the small ones,the rate at which they did so was an order of magnitude lower that the rate at which smallfish attacked each other in the absence of larger conspecifics. This raises the possibility thatlevels of aggression among farmed salmon might be reduced by the addition of a few largeconspecifics.

Key words: aggression, Atlantic salmon (Salmo salar), dominance, growth

Intraspecific aggression is recognised as a problem in aquaculture becauseit may lead to uneven distribution of food (e.g. Jobling and Reinsnes, 1986;McCarthy et al., 1992; Alanära and Brännäs, 1996; Kadri et al., 1996), stress(Ejike and Schreck, 1980), impaired immune function (Pottinger and Pick-ering, 1992), unequal growth (e.g. Jobling and Reinsnes, 1986; Jobling et al.,1995) and increased injury and infection (Abbott and Dill, 1989; Siikavuopioet al., 1996; Turnbull et al., 1996). Thus there is interest in developinghusbandry systems that result in reduced levels of aggression.

Aggression is a flexible behaviour, modified according to the costs andbenefits of fighting over resources (Archer, 1987; Huntingford and Turner,1987), so one mechanism, through which aggression could be reduced wouldbe to limit the benefits that fish gain from fighting. For example, aggressionis reduced when food is not limiting (e.g. Brännäs and Alanärä, 1994) andthe frequency of attacks within groups of fish can be reduced by increasing

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the energetic costs of aggression via an increase in current speed (Grant andNoakes, 1988; Christiansen et al., 1992; Adams et al., 1995).

One important determinant of the costs of fighting is the behaviour of otherfish, because the responses of conspecifics influence an individual’s positionin a hierarchy (Adams et al., 1998) and because retaliation is a commonresponse to attack and can result in injury (e.g. Neat et al., 1998). In groupsof salmonids, a small proportion of the fish often dominate their compan-ions, performing the majority of attacks and monopolising food (e.g. Abbottand Dill, 1989; Metcalfe et al., 1989). Such dominant fish are often largerthan their companions (e.g. Jenkins, 1969; Hughes, 1992), either becauselarger size inhibits aggression in smaller fish or because fish that are able tomonopolise food through aggression grow faster (Huntingford et al., 1990).Adams et al. (1998) found that when dominants were removed from smallgroups of Atlantic salmon, there was increased aggressiveness among theremaining fish. This suggests that the presence of a large dominant fish maysuppress aggression among its smaller companions. We report here on asmall-scale experiment designed to test this possibility with Atlantic salmon(Salmo salar).

Hatchery-reared Atlantic salmon, supplied by Stirling Aquaculture,Howietown, were held at the University Field Station, Loch Lomondside,Scotland (56◦ N). In July 1996, two groups, each of one hundred 0+ parr, wereweighed and placed in circular tanks (diameter 1m) with a circumferentialwater flow of approx. 7 cms/sec. Temperature and light regimes were ambient(temperature range 14.5–20◦C; photoperiod ambient for 56◦ N latitude).Food (BOCM-PAULS salmon diet of 1.3–2.1 mm diameter) was deliveredautomatically every 10 mins throughout daylight hours at 3% of total fishbiomass per day throughout the study. To aid food distribution, pellets weredelivered at a single point in the tank immediately in front of the water inletpipe. Three, 1+ parr (median weight = 6.46 g) were introduced into one ofthe tanks (designated Tank 1) at the beginning of the experiment. Five weekslater, the 0+ fish in both tanks were weighed and the three large fish weretransferred to the other tank (designated Tank 2). Each tank thus served as itsown control for comparison of the effects of the presence of the 1+ fish. The0+ fish in both groups were reweighed 5 weeks later. Daily specific growthrates for each tank for each 5 week period were calculated as:

(LnW2− LnW1)

t× 100

where W1 = mean weight at time 1, W2 = mean weight at time 2 and t = thenumber of days elapsing between weightings. There were no mortalities ineither tank during the experimental period.

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On 10 days during the experiment, at weekly intervals, both tanks werefilmed from above for 1 hour. The field of view of the camera (ca 0.75 m2)encompassed the area of the tank in which food was delivered. Ten, 5 minblocks of film all beginning with a delivery of food to the tank, were analysedto determine aggression rate. Each 5 min filming period was divided into five,1 min sub-periods. During each sub-period, a count was made of the numberof aggressive acts (mostly nips and short chases, Keenleyside and Yamamoto,1962) directed by 0+ fish towards other 0+ fish. The total numbers of fishwithin the camera’s field of view were counted at the beginning and end ofeach observation min. To correct for the varying number of fish within thefield of view, the number of aggressive acts seen in each 1 min sub-periodwas divided by the mean of the number of fish in view at the beginning andend of each 1 min observation period. Aggression rate (attacks per fish permin) for each of the 10, five min observation periods was calculated as themean aggression rate (attacks per fish per min) of the 5, one min sub-samplingperiods. Daily aggression rate was calculated as the mean of the 10, five minobservation periods on each observation day. A similar analysis was used todetermine the number of aggressive acts delivered to the 0+ fish by the 1+fish, again expressed as the number of attacks received per 0+ fish per min.Levels of aggression in each of the two tanks were compared on each day oftesting with t tests (not assuming equal variance). Daily levels of aggressionby 0+ fish in the presence and absence of 1+ fish were compared for each tankusing a Kruskal-Wallis non-parametric analysis of variance with Nemenyi’smultiple comparison of pooled data (Zar, 1996).

The 1+ fish dominated the 0+ fish, monopolising the region of the tanknearest to the feeder and gaining preferential access to food. The frequencyof attack by these fish towards 0+ fish was low (mean± SE aggressive actsreceived from the 1+ fish per 0+ fish per min = 0.013± 0.014). Subjectiveobservations made during each 5 min filming periods indicated that many ofthe 0+ fish in the field of view were feeding.

Mean aggressive interactions among the 0+ fish ranged from 0.04 to 0.46attacks per fish per min (Figure 1). In Tank 1, on the first five sampling days,there were 0.08–0.11 encounters per fish per min when the 1+ fish werepresent, but on sampling days 6–10, after the removal of the large parr, attackfrequency increased to 0.10–0.25 encounters per fish per min, with a sharpincrease on the last two sampling days. The reverse trend was seen in Tank2; the frequency of aggressive encounters on the first five sampling days was0.14–0.21 encounters per fish per min, but on sampling days 6–10, followingthe introduction of the 1+ parr, this declined to 0.08–0.13 encounters per fishper min.

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Figure 1. Mean (+ SE) aggression encounters per fish per min in Tank 1 and Tank 2 on eachsampling day. The bar indicates the period when the 1+ fish were present.

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In 8 of the 10 days of observation over the 10 weeks of the study, levelsof aggression in the two tanks differed significantly. The results of t testscomparing the two groups on each day are as follows: day 1,t = −15.83, df= 17, P = 0.0001; day 2,t = −7.68, df = 17,P = 0.0001; day 3,t = −8.36,df = 17, P = 0.0001; day 4,t = −6.02, df = 9,P = 0.001; day 5,t = −5.11,df = 13, P = 0.0001; day 6,t = −0.01, df = 14,P = 0.51; day 7,t = 3.03,df = 13, P = 0.005; day 8,t = −1.83, df = 16,P = 0.09; day 9,t = 8.51, df= 11, P = 0.0001; day 10,t = 4.30, df = 9,P = 0.001. When pooled datawere compared using a Kruskal-Wallis test (n = 50 periods for both groupsin both conditions), significantly differences between the treatment groupswere found (H3 = 103.05,p< 0.001. Multiple comparison tests (Nemenyi’smultiple comparison of pooled data; Zar, 1996) revealed that the fish in Tank1 were more aggressive than those in Tank 2 in the absence of 1+ fish (q =6.03,P < 0.03), but levels of attack were reduced to a uniformly (q = 2.64,P = 0.20) however, in the presence of 1+ parr (Tank 1:q = 8.67,P< 0.001;Tank 2:q = 10.34,P< 0.001).

For the 0+ parr in Tank 1 (initial mean weight = 0.63 g, SD = 0.232), dailyspecific growth rates based on mean weights were 4.7% day−1 over the first5 weeks (in the presence of 1+ parr) and 2.9% day−1 in the second 5 weeks(in the absence of 1+ parr). Equivalent figures for Tank 2 (initial mean weight= 0.91, SD = 0.266) were 2.8% day−1 (in the presence of 1+ parr) and 4.3%day−1 (in the absence of 1+ parr). Thus in both cases, growth rates were muchhigher when 0+ parr were held together with the 1+ fish than when the samefish were held on their own.

The presence of 1+ salmon reduced the frequency of aggressive interac-tions among 0+ fish at a ratio of three large to 100 small fish, and removal ofthe large fish resulted in an increase in aggression. This took several days todevelop, presumably because it took some time for the small fish to adapt tothe absence of the larger individuals. Further, the growth of the 0+ fish wasfaster in the presence of 1+ fish than in their absence, even though the 1+ fishappeared to dominate feeding.

These results are consistent with current understanding of aggressiveinteractions within animal groups. More-or-less stable social hierarchieshave been described in many animal species and levels of overt aggressionusually fall once dominance-subordinance relationships have been estab-lished (Archer, 1987; Huntingford and Turner, 1987). The destabilising effectof the removal of a dominant animal has also been reported; in primates, theeffect is particularly strong when the dominant animal has established domi-nance without resource to overt aggression (Gust and Gordon, 1993). Theaddition of the 1+ fish to the 0+ population may have resulted in the devel-opment of a despotic relationship without either the large or the small fish

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testing this through overt aggression; this might create a situation whereby‘benign despots’ generated conditions that were favourable for the smallerfish.

Our data may have implications for salmoid aquaculture, although it isby no means clear whether the effect identified in this small-scale studywould scale up to production conditions. Furthermore, above a certain sizethreshold this beneficial effect may be replaced by a risk of cannibalism bythe larger fish (see Amundsen et al., 1995). With these provisos, the presentresults suggest that the addition of larger conspecifics is worth considering asa means of reducing the adverse effect of aggression among farmed juvenileAtlantic salmon.

Acknowledgements

This work was funded by Biotechnology and Biological Science ResearchCouncil grant no. A01405. We are grateful to Vivien Cameron for care of thefish, to Caroline Askew for technical support, to Liz Denton for preparingthe figures and to an anonymous referee for detailed comments on an earlierversion of this manuscript.

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