Individual behaviour and growth of halibut (Hippoglossus hippoglossus L.) fed sinking and floating feed: Evidence of different coping styles

Individual behaviour and growth of halibut

(Hippoglossus hippoglossus L.) fed sinking and

floating feed: Evidence of different coping styles

Tore S. Kristiansen a,*, Anders Ferno b

a Institute of Marine Research, Austevoll, N-5392 Storebø, Norwayb University of Bergen, Department of Biology, P.O. Box 7800, N-5020 Bergen, Norway

Available online 2 October 2006

Abstract

A crucial problem in halibut farming is low and variable growth during the on-growing phase. Individual

halibut may have different abilities to adapt to different aspects of the farming environment, including the

feed distribution mode. In this study, 30 individually tagged halibut (mean weight 1.5 kg) were moved from

a larger tank and kept for 3 months in six 7 m3 tanks with five fish in each tank. Individual feed intake and

behaviour were compared in two periods, when either sinking or floating food was offered. Individual fish

within a tank showed large variations in behaviour and feed intake, but both individual swimming behaviour

and feed intake were positively correlated between periods. On the basis of differences in stereotypic surface

swimming activity and feed intake, the halibut were classified in four behaviour categories that were

suggested to reflect reactive or proactive stress coping styles. Floating food seemed to be an additional

stressor and decreased feeding and increased stereotypic swimming activity. When floating food was

replaced by sinking food, proactive fish that exhibited frequent surface swimming turned into ‘‘well-

adapted’’ fish. The indication of different coping styles in individual halibut and the ability of fish applying a

stress coping style to adapt when the situation changes suggests the possibility of improving halibut farming

by both selective breeding and tailoring the tank environment to the demands of the fish.

# 2006 Elsevier B.V. All rights reserved.

Keywords: Adaptive capacity; Fish welfare; Coping strategy; Aquaculture

1. Introduction

The Atlantic halibut (Hippoglossus hippoglossus L.) is highly valued in northern Europe and

North America and since the early 1980s has been a selected ‘‘new species’’ candidate for

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Applied Animal Behaviour Science 104 (2007) 236–250

* Corresponding author. Tel.: +47 55238500; fax: +47 56182222.

E-mail address: [email protected] (T.S. Kristiansen).

0168-1591/$ – see front matter # 2006 Elsevier B.V. All rights reserved.

doi:10.1016/j.applanim.2006.09.007

mailto:[email protected]

http://dx.doi.org/10.1016/j.applanim.2006.09.007

aquaculture in Norway (Haug, 1990). Halibut have a very long and vulnerable larval stage, and

it has taken much effort to establish stable high production of high-quality juveniles.

Production of farmed halibut in Norway was only 400 tonnes in 2003, but rose sharply to

1300 tonnes in 2004 (Harboe and Adoff, 2005). Large investments have recently been made in

halibut ongrowing farms, and a further increase is expected if the remaining problems in halibut

farming are solved.

The success of domestication of wild animals depends on the flexibility and capability of the

species to adapt to the farming environment, but also on our ability to create a farming

environment within the range of the adaptive capacity of the species concerned (Price, 1999). As

an undomesticated ‘‘new species’’, the Atlantic halibut broodstock still consists for the most part

of individuals of wild origin or first-generation farmed fish, and basic knowledge of the adaptive

capacity of halibut to farming conditions is generally lacking. Halibut are ongrown in tanks

originally constructed for salmon production, or in sea-cages with trampoline bottoms (Tuene

et al., 1999). Attempts have been made to adapt the rearing environment to the species, e.g. by

using shelves to increase bottom area, but there has been little scientific evaluation of these

modifications. Experimental trials have shown that it should be possible to grow halibut to 5 kg

average weight in 3–4 years (Bjornsson, 1995; Bjornsson and Tryggvadottir, 1996; Nortvedt and

Tuene, 1995; Norberg et al., 2001). However, in commercial farms the growth rates are usually

far lower, leading to a much longer and more expensive production cycle (Holm et al., 1993;

Sparboe, 2000). Various suboptimal farming conditions have been identified, such as temperature

(Hallaraker et al., 1995; Bjornsson and Tryggvadottir, 1996; Jonassen et al., 2000), the tank/cage

environment (Holm et al., 1998), crowding (Bjornsson, 1994; Kristiansen et al., 2004), feed

(Nortvedt and Tuene, 1995; Helland and Grisdale-Helland, 1998), low juvenile quality

(Kristiansen and Harboe, 2004), and early sexual maturation and slow growth in males (Norberg

et al., 2001).

Behavioural problems such as aggression and stereotypical and abnormal behaviour are

regularly observed in halibut farms and research facilities. During the juvenile stage, aggressive

behaviour causes physical injuries to eyes and fins (Ottesen and Strand, 1996; Holm et al., 1998;

Greaves, 2001). The frequency of aggressive acts declines markedly with fish size and is rarely

observed between halibut larger than 500 g (Greaves and Tuene, 2001). Stereotyped surface

swimming behaviour is observed in all stages and have found to be negative correlated with

individual growth rate (Kristiansen et al., 2004). When performing this behaviour the halibut is

swimming almost vertical in the surface, with repeated lifting of the head above water.

Marked variations in the behaviour of individual fish within a species are often observed

(Magurran, 1993). Within a single environment, multiple optima can exist and be enhanced by

frequency-dependent selection (Sih et al., 2004). Such variation may result from genetic,

environmental or ontogenetic factors, as well as interactions of these factors (Caro and Bateson,

1986; Sneddon, 2003). There are wide individual variations in how halibut adapt to different

rearing environments (e.g. Tuene and Nortvedt, 1995; Nortvedt and Tuene, 1995; Kristiansen

et al., 2004). Individual halibut may have different ways of coping with environmental

challenges. Coping strategies refer to the specific efforts, both behavioural and psychological,

that animals employ to master, tolerate, reduce, or minimize stressful events. The two main

coping strategies described are proactive (fight-flight response) and reactive (conservation-

withdrawal response, Koolhaas et al., 1999). The predominance of one type of strategy over

another is partly determined by personality or coping style. A coping style can be defined as a

coherent set of behavioural and physiological stress responses which is consistent over time and

which is characteristic of a certain group of individuals (Koolhaas et al., 1999). Coping styles are

T.S. Kristiansen, A. Ferno / Applied Animal Behaviour Science 104 (2007) 236–250 237

characterized by consistent behavioural and neuroendocrine characteristics, some of which seem

to be causally linked to each other. Distinct behavioural/physiological coping styles have

previously been observed in fish (van Raaij et al., 1996; Øverli et al., 2004).

A characteristic behavioural response to stress in fish is reduction in feed intake. In addition to

its appetite-suppressing effect, stress can disrupt other aspects of feeding behaviour such as food

searching, finding or capture (Beitinger, 1990). Several stressors including environmental, social

and physical challenges have been shown to inhibit food consumption in fish (Schreck et al.,

1997; Wendelaar Bonga, 1997; Bernier and Peter, 2002). The way in which food is presented

could have a strong influence on feeding activity and the social environment. In this study, we

focus on variations in behaviour of individual halibut in two different feeding situations, using

sinking and floating food. Floating food supplied from the bottom is only available in the water

column for a few seconds, which should give proactive fish an advantage and also increase any

scramble competition for feed. Sinking food fed at the bottom is more easily available to fish

lying on the bottom, which should favour more reactive individuals. In order to try to identify

individual coping styles, we studied the behaviour of individual halibut during two feeding

periods. In the first period, the groups of fish were presented either floating or sinking food, and in

the second period we switched feed type in all groups to challenge adaptive flexibility in the

foraging behaviour of halibut.

2. Materials and methods

2.1. Experimental fish and tagging

The 30 halibut used in the experiment were taken from a group of 2.5 year-old reared halibut of mixed

origin kept in a 7 m diameter glass-fibre tank (water depth 1 m) since the previous year and fed sinking food

from the surface. The 30 fish were anaesthetised with Benzocaine (10 g in 100 ml 96% ethanol; 5 ml

Benzocaine solution per 10 l oxygenated sea water; fish kept in 3–5 min until immobilisation), PIT-tagged

(TrovanTM Passive Implant Transponder tags PIT; Type ID100A placed in the muscle on the dorsal side

behind the head), measured and weighed (Day 0, August 30, 2001, Table 1), and put into a 3 m diameter

glass fibre tank with green floor and walls (outside tanks with natural light), water depth 1.5 m, for recovery

after handling and acclimation to the new experimental tank environment (Table 1). In this period the fish

were fed ad lib with sinking food once a day around 01:00 p.m. After 4 weeks (Day 27, Table 1), the halibut

were carefully netted from the tank, anaesthetised and individually tagged with T-bar tags with a plastic flag,

at one of five different positions on the body rim to enable individual identification from video recordings.

The fish were not measured and weighed at this stage, in order to reduce handling stress. Five fish (with tags

T.S. Kristiansen, A. Ferno / Applied Animal Behaviour Science 104 (2007) 236–250238

Table 1

Overview of the experiment (Day 0 is 30 August 2001)

Day Action

0 Measuring, weighing, PIT-tagging 30 fish, all in one tank. Start feeding

with sinking food. Acclimation period to day 27.

27 External tagging and allocating five fish to each of six tanks

33 Start feeding three tanks with sinking food and three tanks with floating food

82–93 Video recording of behaviour – Period 1 (2 � 5 days)

98 Measuring and weighing after Period 1

103 Switch of food type

103–114 Video recording of behaviour – Period 2 (2 � 5 days)

147 Measuring and weighing at termination of experiment

in five different positions) were then allocated to one of six identical 3 m diameter tanks of the same type as

above (Table 2). The tanks were supplied with 50 l min�1 seawater pumped from a depth of 140 m, with

stable temperature around 7.8 8C (�0.5 8C) and identical oxygen content (90–96% saturation), and covered

with shade-nets (70%) to reduce sunlight intensity.

2.2. Food and feeding

After the last tagging three of the groups were fed 12 mm floating dry fish feed and the other three

groups 12 mm sinking feed (Table 2). Both feed types were specially made for the experiment by a

manufacturer of dry feed. The chemical composition of the feed types was identical (mainly high-quality

fish meal and fish oil). The feed was fed through a water hose with the outlet on the bottom, one pellet at a

time at intervals of a few seconds, in two batches of about 15 pellets with an interval of about 5 min

between batches. The fish were fed in excess a fixed ration 5 days a week (Monday–Friday, ration 30–

35 g, approximately 0.4% of biomass per feeding). The floating food rose from the bottom to the surface

in a few seconds, so the fish had to react very rapidly to catch the pellets. The sinking food pellets moved

slowly along the bottom towards the drain, and were therefore easier to catch and available for a longer

time then the floating food. Regrettably, the tanks were not equipped with feed collectors, so uneaten

pellets could not be collected without disturbing the fish too much. Uneaten floating pellets sunk when

they became sufficiently soaked with water (after more than half an hour; such wet pellets are usually

eaten). At the end of Period 1 (Day 98, Table 1) the fish were starved for four days, anaesthetized,

measured and weighed, returned to the same tanks and fed for another 6 weeks. In order to challenge the

fish, we then switched feed type. The fish in the tanks fed sinking food were given floating food, which

was assumed to be a more difficult task, while the fish in the remaining tanks were given what was

assumed to be easier task (change from floating to sinking food). At the end of the period, the fish were

again measured and weighed.

2.3. Video recordings

After 50 days acclimatization to the tanks and feeding, all groups were filmed from 10 min before

feeding until 10 min after feeding with an underwater colour video camera (Sony DCR-VX-1000 DV

Camcorder camera) mounted in underwater housing and connected to a JVC HM-DR10000 D-VHS

recorder, 5 days a week (Monday–Friday) for 2 weeks (Period 1, Days 82–93, Table 1). The camera was

placed close to the tank wall at the opposite side of the feeding area and the camera view covered

approximately 70% of the tank. After the types of feed had been switched the feeding periods were filmed

for another 2 weeks (2 � 5 days; Period 2, Days 103–114, Table 1).

2.4. Behavioural analysis

The 30 fish were observed for 20 days, giving a total of 600 individual observation sessions with an

average length 28 min. Two recording periods in tank 1 and one in tank 2 had to be excluded due to technical


Table 2

Mean size of the six groups of five halibut at Day 0 (see Table 1) allocated to the six different tanks (1–6)

Floating food in P1 Sinking food in P1

1 3 5 2 4 6

Mean weight (g) 1313 1470 1605 1406 1573 1750

S.D. weight (g) 453 511 563 494 549 800

Mean length (cm) 48.2 48.6 50.6 48.2 50 51.4

S.D. length (cm) 5.6 5.5 7.3 6.6 6.5 7.4

errors, reducing the numbers of observations to 585. Positions in the tank, postures and behaviours of all

individuals were registered for the whole of each recording period using The Observer video analysis

program (Noldus Information Technology, Wageningen, The Netherlands). All positions, postures, and

behaviours were recorded as states, with the exception of ‘‘eating’’, which was recorded as an event. A

number of different postures and behaviours were recorded, but in this paper we focus on two behaviours

that are relevant for identifying different coping styles and where wide individual variations in activity were

found: feeding behaviour (pellets eaten) and stereotypical surface swimming behaviour. A bout of surface

swimming was defined as a short period (seconds to a few minutes) where the fish swam with the body in

upright position (inclined at over 308 to the surface), with the head frequently breaking the surface.

Interactions between fish were seldom seen and only recorded on paper.

3. Results

3.1. Feed intake and growth

In general, there were wide variations in feed intake between the individual fish in a tank, with

some fish eating in almost all feeding sessions and others almost never observed eating in the

video recordings (Fig. 1). An exception was tank 2, where all individuals had very low feed intake

in both observation periods. There was a significant positive correlation in individual feed intake

between the two observation periods (Fig. 2). Of the six fish, which were observed to take most

pellets in Period 1, four also took most pellets in Period 2. The remaining two fish were ranked as

second in Period 1. Similarly, the six lowest-ranking fish in Period 1 were lowest ranked in Period

2. However, there were also individuals, which coped better or worse after a change in feed type

(Fig. 2). The shift from floating to sinking food generally resulted in increased feed intake and

growth rate (from an average SGR of 0.09 to 0.13% day�1), whereas the change from sinking to

floating food produced the opposite result (SGR from 0.13 to 0.06% day�1, Table 3). The halibut

were not seen catching pellets floating on the surface, but some pellets started to sink after some

minutes and could have been eaten later. However, at this time the pellets were very moist and

unattractive for the halibut.

3.2. Surface swimming and feeding behaviour

By looking closer at the individual feed intake and other behaviour patterns, we could identify

individuals with similar behaviour styles. The most characteristic differences between

individuals were found in feed intake and swimming activity, especially with regard to how

often the fish performed stereotypical surface-swimming behaviour (Fig. 3). Also in this

behaviour there were large individual variation, and also clear differences between tanks and

between periods with different feed types. Of the 585 individual feeding sessions observed, 214

sessions included periods where the fish displayed one or more bouts of stereotypic surface

swimming. The numbers of bouts per session varied from 1 to 141, with an average of 20, where

each bout lasted for an average of 4.4 s. Typical behaviour was several short surface-swimming

bouts lasting a few seconds, interrupted by a few seconds of normal swimming near the surface.

Of the total time the surface swimmers were observed in the camera view, an average of 41% was

spent on swimming (average 6.6 min). The surface swimming bouts occupied on average 22% of

this time. There was a significant positive correlation between the time spent swimming and the

time spent surface swimming (RS = 0.57, p < 0.0001, n = 214). In the 371 feeding sessions when

the fish were not surface swimming, they only spent an average of 15% of the observed time

swimming.


By plotting the sum of pellets eaten in P1 against the sum of bouts of surface swimming

behaviour in the same period for each fish, we could identify clusters of individuals with similar

behavioural characteristics (Fig. 4). Based on these clusters, the individuals were classified in

four categories using the following category names and definitions:


Fig. 1. Cumulative numbers of pellets eaten by the five individual halibut in each tank, in the two 10 feeding-days

observational periods (see Table 1). Tanks 1, 3 and 5 were given floating food in the first period and sinking food in the last,

while tanks 2, 4 and 6 were given sinking food in the first period.

� Reactive: <5 pellets eaten and <40 surface swimming

� Proactive non-feeders: <5 pellets eaten and �40 surface swimming

� Proactive feeders: �5 pellets eaten and �40 surface swimming

� Well-adapted: �5 pellets eaten and <40 surface swimming

The two first categories consisted of fish that seemed to adapt badly to the rearing and feeding

conditions and ate almost nothing (Fig. 4) and grew slowly or not at all (Fig. 5, Table 3). While

the ‘‘Reactive’’ group seemed to have a ‘‘wait and see’’ strategy, the ‘‘Proactive non-feeders’’ had

high surface activity. Based on their relatively high feed intake, the next two categories were

regarded as adapting better. The ‘‘Proactive feeders’’ still did a lot of surface swimming, which

may suggest problems of adaptation. ‘‘Well-adapted’’ fish were (by definition) fish that did very

little surface swimming and had a relatively high feed intake.


Table 3

Average numbers of pellets eaten in the 2-week observation periods and average specific growth rate in the whole feeding

periods (in brackets) by the groups defined by their behavioural categories in observation Period 1

Well-adapted Proactive feeders Proactive non-feeders Reactive All

Period 1, Sinking food 36 (0.19) 20 (0.18) 2 (0.00) 0 (0.10) 15 (0.13)

Period 2, Floating food 23 (0.05) 11 (0.12) 0 (�0.06) 0 (0.06) 9 (0.06)

Numbers of fish in P1 3 6 3 3 15

Period 1, Floating food 25 (0.16) 21 (0.06) 0 (0.01) 1 (0.01) 16 (0.09)

Period 2, Sinking food 27 (0.21) 28 (0.16) 2 (�0.04) 6 (0.05) 20 (0.13)

Numbers of fish in P1 6 4 2 3 15

Fig. 2. Correlation between individual feed intakes in the two observation periods, shown as the sum of pellets eaten in

each period (floating to sinking: RS = 0.86, p < 0.001, n = 15, sinking to floating: RS = 0.80, p < 0.001, n = 15). The

figure also shows a general increase in food consumption when changing from floating food to sinking food (almost all

points above the 1:1 line), and vice versa.

When they were transferred from the more demanding floating food to the more easily

available sinking food, all ‘‘Proactive feeders’’ in P1 fell within the definition of ‘‘Well-

adapted’’ in Period 2, and two of three ‘‘Reactive’’ fish in P1 also changed category to ‘‘Well-

adapted’’ (Fig. 4). Only 2 of the 15 fish given floating food in P1 were classified as


Fig. 3. Cumulative numbers of stereotypic surface swimming bouts of the five individual halibut in each tank in the two

observational periods. Tanks 1, 3 and 5 were given floating food in the first period and sinking food in the last, while tanks

2, 4 and 6 were given sinking food in the first period.

‘‘Proactive non-feeders’’ in P1 and were never observed to eat, and both fish remained in the

same category in P2.

In the groups that were given sinking food in P1 and floating food in P2 (which they had never

experienced before), two of six ‘‘Proactive feeders’’ changed category to ‘‘Proactive non-

feeders’’ and in all but one case, surface swimming activity increased and feed intake decreased

(Fig. 5). The ‘‘Proactive non-feeders’’ in P1 completely stopped feeding and increased their

surface swimming activity. Interestingly, one of the ‘‘Reactive’’ fish also displayed frequent

bouts of surface swimming on several days in P2, and thus changed to proactive non-feeder

behaviour. Of the three ‘‘Well-adapted’’ fish in P1, one almost went into the ‘‘Reactive’’

category, whereas the other two still adapted well (one fish slightly increased surface

swimming).

There was a significant, but relatively weak, positive correlation between specific growth rate

and the observed numbers of pellets eaten in both observation periods (Spearman Rank

Correlation P1: RS = 0.51, p = 0.004, n = 30; P2: RS = 0.58, p < 0.001, n = 30, all individuals

pooled).

No aggressive interactions between individuals were observed, and the relationship between

size and growth rate gave no indications of size hierarchies, as the largest fish grew most slowly

(Fig. 6). Surface swimming activity was significantly higher in the groups fed floating food

( p < 0.012, Mann–Whitney U-test), but the surface activity of individual fish was positively

correlated at a significant level in the two observation periods (Fig. 7), indicating a degree of

permanence in individual coping styles.


Fig. 4. The relationship between surface swimming activity and pellets eaten in the feeding periods of all individuals. The

defined borders between the different behavioural categories are indicated by thin lines. Classification of individuals in

different categories was based on Period 1, with individuals given the same symbol in Period 2 as in Period 1.

4. Discussion

In this study, we have demonstrated marked individual variations in behaviour and growth in

halibut reared in tanks, with clear differences in feeding activity and surface swimming

behaviour. The fish with very low feeding motivation were unable to adapt, or adapted very

slowly, to the rearing conditions and showed a sub-optimal coping strategy, since in the long run,

low or no feed intake will weaken the animal and in the end be life threatening. The introduction

of floating food as an extra challenge for the fish decreased food intake and increased the

frequency of stereotyped swimming activity, indicating an increased stress level. On the other

hand, the change from floating to sinking food, which made feeding easier, led to better feed

intake and less stereotyped behaviour, with more individuals able to adapt.

The group of individuals that adapted badly and were seldom or never seen feeding in the first

observation period (P1) were divided into two behavioural categories named ‘‘Proactive non-

feeders’’ and ‘‘Reactive’’. While the first group displayed a high frequency of stereotyped

swimming activity, the latter lay apathetically on the bottom during most of the observed feeding

sessions. If we interpret the behaviour of the two categories of fish as representing the two basic

coping styles in a stressful environment, the fish in these two groups choose to cope with the

rearing conditions in either a reactive (‘‘wait and see’’) or proactive (‘‘try to get out of here’’) way

(Koolhaas et al., 1999).

Although fish that do not feed and grow in a tank are unsuccessful in their present

environment, their behaviour may be adaptive in the longer time perspective of their natural

environment. ‘‘Reactive’’ (non-feeding) fish appear to have gone into an apathetic state with


Fig. 5. Relationship between surface swimming activity and individual growth rates.

generally low activity and slow growth. This seems to be maladaptive behaviour in the tanks, but

under natural conditions it may reflect a strategy of staying alive until environmental conditions

improve. The halibut is a species with large metabolic reserves and a long life span, which is

capable of tolerating long periods of starvation (Haug, 1990), and a reactive behaviour may be

beneficial under certain conditions. The ‘‘Proactive non-feeders’’ also seemed to be poorly

adapted to the rearing environment, but their high swimming activity could be seen as attempts to

leave a suboptimal environment and their low feeding intake to be a result of change to a

‘‘migration mode’’, where feeding motivation is turned off.


Fig. 6. Correlation between start length and specific growth rate during the first 3 months (Days 0–103, see Table 1)

(Spearman Rank Correlation RS = �0.51, p < 0.01, n = 30).

Fig. 7. Correlation between individual surface swimming activity in periods with sinking and floating food (Spearman

Rank Correlation RS = 0.67, p < 0.001, n = 30). The points below the 1:1 line show individuals that displayed less surface

swimming activity in the period with sinking food.

The group of individuals that fed relatively well and seemed to adapt quite well in P1, was also

divided into two categories, which we named ‘‘Well-adapted’’, with little stereotyped surface

swimming activity, and ‘‘Proactive feeders’’, that displayed relatively high levels of stereotyped

swimming activity. Since stereotyped surface swimming wild halibut to our knowledge has never

been observed in the sea, the ‘‘Well-adapted’’ fish must be assumed to have been displaying the

most normal halibut behaviour. Our knowledge of halibut behaviour in the field is very limited,

but the excellent camouflage ability of halibut (by changing skin patterns) and the prey species

consumed by small halibut (benthic crustaceans and small fish, Haug, 1990), indicate that they

often employ a ‘‘sit-and-wait’’ feeding strategy. The ‘‘Well-adapted’’ fish in the present study

actually showed this feeding strategy, and mostly responded to the food when they observed a

moving pellet from their position on the bottom. They were never observed swimming around

searching for food on the bottom.

While the ‘‘Proactive feeders’’ appeared to be relatively well adapted to the environment

based on their feeding behaviour and growth, they also frequently displayed stereotyped

swimming behaviour. Supported by their wide range of feeding activity and growth rates, and the

fact that they were observed to change their behaviour when switching food type (to ‘‘Proactive

non-feeders’’ when given floating food, and to ‘‘Well-adapted’’ when given sinking food), this

category may represent a transitional state between adaptation and proactive stress coping

behaviour when the stress level is moderate.

The relative weak correlations between pellets seen eaten and growth indicate that feeding

behaviour differed in the weeks with and without observations, and the weaker correlations in P1

could be caused by the relatively shorter observation period compared to P2 (2 of 12 weeks

relative to 2–6 weeks). Less than 50% of the pellets were seen to be eaten, and some of the pellets

remaining in the tanks after the observation session may have also have been eaten, and

contributed to the low correlation.

In a previous study, we have shown surface swimming to be negatively correlated with growth

rate, and suggested that such behaviour may be a useful indicator of sub-optimal rearing

conditions and impaired welfare in halibut farms (Kristiansen et al., 2004). However, when the

level of individual welfare is being assessed, this indicator is more uncertain, since individual

growth rates may also be relatively high in fish with high surface swimming activity (like the

‘‘Proactive feeders’’), while fish without surface swimming activity could be ‘‘Reactive’’

(apathetic) stress copers. Surface swimming is probably a stereotyped behaviour that develops

when fish are swimming in a limited volume, and is caused by the frustration of not being able to

leave. The stereotyped behaviour itself is not necessarily an indication of lack of well being, since

the performance of the behaviour may be self-stimulating and make the animal ‘‘feel’’ better

(Broom and Johnson, 1993), but should probably be seen as a way of compensating for

unsatisfied demands. In other species, stereotypes are found in stimulus-poor environments

where the animals are not able to perform natural behavioural actions, or in situations in which

fear, social challenges, or strong anticipation lead to directed behaviour as a result of not being

able to deal with the situation (Broom and Johnson, 1993).

A crucial question is that of why some fish adapted to the environment, whereas others

employed different stress coping strategies. Individual variation in feed intake in small groups of

fish is often explained by dominance hierarchies caused by aggressive interactions (Huntingford

et al., 1990; Adams et al., 1998). Although subtle ways of acquiring dominance may have been

overlooked, we observed no aggressive interactions or other signs of dominance in this study.

While halibut may be very aggressive at the small juvenile stage, they seldom show aggression

when they have reached the size used in this experiment (Greaves and Tuene, 2001). If


dominance hierarchies do occur, the largest halibut in the tanks might be expected to be dominant

and to have the most rapid growth, but in fact there was a significant negative correlation between

size and growth rate. Also when taking into account the decreasing growth rate with increasing

size normally found in halibut (Bjornsson and Tryggvadottir, 1996), the results gave no

indication of size hierarchies. Other studies indicate that large halibut prefer a relatively larger

rearing space (Holm et al., 1996), so the larger fish may have perceived the experimental tanks as

being relatively smaller than the smaller fish, and thereby been given an additional stressor when

moved from a larger to a smaller tank.

One intention behind the shift between feed distribution modes was to study the adaptive

flexibility (Dill, 1983) of the foraging behaviour of halibut. Most fish that fed well in one feed

distribution mode seemed to cope directly with the new mode. These fish even tended to deal with

the change to floating food, which they had not earlier experienced, reasonably well. However,

some individuals adapted more slowly to a new regime, and they fed only seldom early in the

observation period and only gradually resumed feeding. Another aim was to compare an easy

feeding situation (sinking food with pellets available for a long time) and a more difficult one

(floating pellets available for a brief period of time, representing a new situation). As expected the

fish coped better with sinking food, with generally higher feeding activity, higher growth rate and

lower surface activity. An interesting observation was that fish given floating food before sinking

food in the experiment seemed to perform better (less surface swimming during the period with

sinking food), than fish given sinking food at the beginning of the experiment. Reward and

distress are important feedback mechanisms that facilitate or inhibit motivational systems

(Spruijt et al., 2001). One reason for this might be that reward-evaluating mechanisms respond

preferentially to changes and should then estimate a ‘‘normal’’ situation as more rewarding after

having experienced something worse. A third intention of the shifts in feed distribution mode was

to give fish with different coping styles an advantage in different situations, with proactive fish

expected to cope better with floating food and reactive fish better with sinking food. However,

fish that did well in one feed distribution mode also generally did well in the other mode. The

situations may therefore have been too similar to alter the relative success of particular coping

styles, and the proactive fish just seemed to have more or less advantage of the two feed

distribution modes.

The wide individual variations in behaviour and growth rate of halibut in the present study as

well as the marked changes in behaviour after a relatively minor change in the farming

environment (feed type) suggest a potential for significant improvements in halibut farming

techniques. If the ability to adapt to the farming environment has a strong genetic basis, selective

breeding can produce fast-growing fish. If such behaviour is shaped during early ontogeny,

improving the rearing conditions of juvenile fish is crucial. Even if experiences in adulthood do

not seem to alter overall coping style (Koolhaas et al., 1999), we should also continuously try to

match the rearing environment to the requirements of the fish throughout the on-growth phase in

order to make the fish utilize their growth capacity and to secure acceptable fish welfare.

5. Conclusion

The present study indicates the existence of relatively distinct coping styles with some

stability across time and situations, but also suggests that an individual that employs a particular

strategy for coping with stress can develop into an adapted fish. We should thus attack the

problems of halibut farming both by selective breeding and optimisation of the environment at

different life stages.


Acknowledgements

We are most grateful to Dr. Jens Chr. Holm for initiating the project, Lucia Privitera for the

video analysis, Stine Bakke and Jan Erik Fosseidengen for technical assistance, and Hugh Allen

for correcting the English. The project was financed by The Research Council of Norway.

References

Adams, C.E., Huntingford, F.A., Turnbull, J.F., Beattie, C., 1998. Alternate competitive strategies and the cost of food

acquisition in juvenile Atlantic salmon (Salmo salar). Aquaculture 167, 17–26.

Beitinger, T.L., 1990. Behavioral reactions for the assessment of stress in fishes. J. Great Lakes Res. 16, 495–528.

Bernier, N.J., Peter, R.E., 2002. The hypothalamic–pituitary–interrenal axis and the control of food intake in teleost fish.

Comp. Biochem. Physiol. Part B: Biochem. Mol. Biol. 129 (2–3), 639–644.

Bjornsson, B., 1994. Effects of stocking density on growth rate of halibut (Hippoglossus hippoglossus L.) reared in large

circular tanks for 3 years. Aquaculture 123, 259–270.

Bjornsson, B., 1995. The growth pattern and sexual maturation of Atlantic halibut (Hippoglossus hippoglossus L.) reared

in large tanks for 3 years. Aquaculture 138, 281–290.

Bjornsson, B., Tryggvadottir, S.V., 1996. Effects of size on optimal temperature for growth and growth efficiency of

immature Atlantic halibut (Hippoglossus hippoglossus L.). Aquaculture 142, 33–42.

Broom, D.M., Johnson, K.G., 1993. Stress and Animal Welfare. Chapman and Hall, London, UK.

Caro, T.M., Bateson, P.P.G., 1986. Organisation and ontogeny of alternative tactics. Anim. Behav. 34, 1483–1499.

Dill, L.M., 1983. Adaptive flexibiolity in the foraging behaviour of fishes. Can. J. Fish. Aquat. Sci. 40, 398–408.

Greaves, K., Tuene, S., 2001. The form and context of aggressive behaviour in farmed Atlantic halibut (Hippoglossus

hippoglossus L.). Aquaculture 193, 139–147.

Greaves, K., 2001. Manipulating aggression among juvenile Atlantic halibut (Hippoglossus hippoglossus) in culture

conditions. PhD Thesis. Institute of Biomedical and Life Sciences, University of Glasgow, 240 pp.

Hallaraker, H., Folkvord, A., Stefansson, S., 1995. Growth of juvenile halibut (Hippoglossus hippoglossus L.) related to

temperature, day length and feeding regime. Netherlands J. Sea Res. 34, 139–147.

Harboe, T., Adoff, G., 2005. Oppdrett av kveite. Havbruksrapport 2005. Fisken og Havet, Særnummer 3, 2005.

Haug, T., 1990. Biology of the Atlantic halibut, Hippoglossus hippoglossus (L., 1758). Adv. Mar. Biol. 26, 1–69.

Helland, S.J., Grisdale-Helland, B., 1998. Growth, feed utilization and body composition of juvenile Atlantic halibut

(Hippoglossus hippoglossus) fed diets differing in the ratio between the macronutrients. Aquaculture 166, 49–56.

Holm, J.C.H., Hennø, J.S., Karlsen, Ø., Skiftesvik, A.B., Huse, I.J., 1993. Matfiskoppdrett av kveite. Faglig sluttrapport

Stolt Sea Farm AS. Havforskningsinstituttet, 21 pp.

Holm, J.C.H., Karlsen, Ø., Norberg, B., 1996. Vekst og kjønnsmodning hos kveite og torsk. Sluttrapport til Norges

Forskningsrad Pnr. 104835/110 og 1072225/100, 27 pp.

Holm, J.C., Tuene, S.A., Fosseidengen, J.E., 1998. Halibut behaviour as a means of assessing suitability of ongrowth

systems. ICES CM 1998, L:4.

Huntingford, F.A., Metcalfe, N.B., Thorpe, J.E., Graham, W.D., Adams, C.E., 1990. Social dominance and body size in

Atlantic salmon parr, Salmo salar L. J. Fish Biol. 36, 877–881.

Jonassen, T.M., Imsland, A.K., Kadowaki, S., Stefansson, S.O., 2000. Interaction of temperature and photoperiod on

growth of Atlantic halibut, Hippoglossus hippoglossus L. Aquacult. Res. 31, 219–227.

Koolhaas, J.M., Korte, S.M., De Boer, S.F., Van Der Vegt, B.J., Van Reenen, C.G., Hopster, H., De Jonga, I.C., Ruis,

M.A.W., Blokhuis, H.J., 1999. Coping styles in animals: current status in behaviour and stress-physiology. Neurosci.

Biobehav. Rev. 23 (7), 925–935.

Kristiansen, T.S., Ferno, A., Hjolm, J.C., Privitera, L., Bakke, S., Fosseidengen, J.E., 2004. Swimming behaviour as an

indicator of low growth rate and impaired welfare in Atlantic halibut (Hippoglossus hippoglossus L.) reared at three

stocking densities. Aquaculture 230, 137–151.

Kristiansen, T.S., Harboe, T. 2004. Oppdrett av kveite. In: Agnalt, A., Ervik, A., Kristiansen, T.S., Oppedal, F. (Eds.),

Havbruksrapport 2004, Fisken og havet, Særnummer 3-2004, pp. 72–75.

Magurran, A., 1993. Chapter 13. Individual differences and alternate behaviours. In: Pitcher, T.J. (Ed.), Behaviour of

Teleost Fishes. second ed. Chapman & Hall, London.

Norberg, B., Weltzien, F.-A., Karlsen, Ø., Holm, J.C., 2001. Effects of photoperiod on sexual maturation and somatic

growth in male Atlantic halibut (Hippoglossus hippoglossus L.). Comp. Biochem. Physiol. B 129, 357–365.


Nortvedt, R., Tuene, S., 1995. Multivariate evaluation of feed for Atlantic halibut. Chemom. Intell. Lab. Syst. 29,

271–282.

Ottesen, O.H., Strand, H.K., 1996. Growth, development, and skin abnormalities of halibut (Hippoglossus hippoglossus

L.) juveniles kept on different bottom substrates. Aquaculture 146, 17–25.

Øverli, Ø., Korzan, W.J., Hoglund, E., Winberg, S., Bollig, H., Watt, M., Forster, G.L., Barton, B.A., Øverli, E., Renner,

K.J., Summers, C.H., 2004. Stress coping style predicts aggression and social dominance in rainbow trout. Horm.

Behav. 45, 235–241.

Price, E.O., 1999. Behavioural development in animals undergoing domestication. Appl. Anim. Behav. Sci. 65, 255–271.

Schreck, C.B., Olla, B.L., Davis, M.W., 1997. Behavioral responses to stress. In: Iwama, G.W., Sumpter, J., Pickering,

A.D., Schreck, C.B. (Eds.), Fish Stress and Health in Aquaculture. Cambridge University Press, Cambridge, pp.

745–770.

Sih, A., Bell, A., Chadwick Johnson, J., 2004. Behavioural syndromes: an ecological and evolutionary overview. Trends

Ecol. Evol. 19 (7), 372–378.

Sneddon, L.U., 2003. The bold and the shy: individual differences in rainbow trout. J. Fish Biol. 62, 971–975.

Sparboe, L.O., 2000. Sluttrapport produksjonsoppfølging Kveitenett Nord April-99 til April-00. Akvaplan-Niva rapport

APN 630.1779, 10 pp.

Spruijt, B.M., Bos, R. van den, Pijlman, F.T.A., 2001. A concept of welfare based on reward evaluating mechanisms in the

brain: anticipatory behaviour as an indicator for the state of reward systems. Appl. Anim. Behav. Sci. 72, 145–171.

Tuene, S., Nortvedt, R., 1995. Feed intake, growth and feed conversion efficiency of Atlantic halibut. Aquacult. Nutr. 1,

27–35.

Tuene, S., Holm, J.C., Haugen, T., Fosseidengen, J.E., Mangor-Jensen, R., Bergh, Ø., Karlsen, Ø., Norberg, B., Kalvenes,

H., Rabben, H., 1999. Kveite i merd. Sluttrapport Norges forskningsrad (Final report to The Research Council of

Norway) nr 115690/122, 15 pp.

van Raaij, M.T.M., Pit, D.S.S., Balm, P.H.M., Steffens, A.B., van den Thillart, G.E.E.J.M., 1996. Behavioral strategy and

the physiological stress response in rainbow trout exposed to severe hypoxia. Horm. Behav. 30, 85–92.

Wendelaar Bonga, S.E., 1997. The stress response in fish. Physiol. Rev. 77, 591–625.


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Individual behaviour and growth of halibut (Hippoglossus hippoglossus L.) fed sinking and floating feed: Evidence of different coping styles