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Behavioural responses in wild cod (Gadus morhua L.) exposed to fish holding water
Aquaculture 262 (2007) 260 – 267 www.elsevier.com/locate/aqua-online
Behavioural responses in wild cod (Gadus morhua L.) exposed to fish holding water Bjørn-Steinar Sæther ⁎, Pål-Arne Bjørn, Trine Dale Norwegian Institute of Fisheries and Aquaculture Research (Fiskeriforskning), Breivika, 9291 Tromsø, Norway Received 28 July 2006; received in revised form 21 November 2006; accepted 22 November 2006
Abstract Local fishermen in several areas of Norway assert that salmon farms have caused the wild migrating cod to change their migratory behaviour, so that they no longer enter their natural spawning grounds in the fjords. If the asserted changes in behaviour of wild cod populations can be linked to establishment of salmon farms, water-soluble odorants are then possible candidates to explain such a connection. Chemical stimulants are important to the individual fish's conception of the surrounding environment. High density stocks of fish in a farm are expected to release large amounts of waterborne information. The present laboratory experiments were conducted to test behavioural responses in Atlantic cod exposed to water containing metabolites and waste from farmed salmon. The trials were conducted on single fish in a multiple chamber preference system. The results show that migrating wild Atlantic cod chose to spend more time in chambers without addition of water from the salmon tank, regardless of their maturation status, and even at very low concentrations (0.2%). The avoidance is probably due to presence of chemical compounds with olfactory properties from salmon, since anosmic cod did not elicit such response. Farmed cod, on the other hand, does not avoid water from the salmon tank, and stationary wild cod caught nearby a fish farm had a less pronounced response as compared to wild migrating cod. The response seen is not species specific, as wild migrating cod responded similar to water from a tank holding farmed cod as to water from salmon. These results do not preclude fishermen's observations that cod change their behaviour in areas with fish farming activity. Such a change in behaviour could be a response to water-soluble odorants, but needs to be validated and detailed in further laboratory experiments as well as in nature before any conclusions can be made. © 2006 Elsevier B.V. All rights reserved. Keywords: Chemosensory stimulants; Wild cod; Fishfarms; Interaction; Behaviour
1. Introduction Norwegian coastal waters host spawning grounds for the commercially important Atlantic cod (Gadus morhua L.). The Atlantic cod is divided into different
⁎ Corresponding author. Tel.: +47 77 62 90 00. E-mail address: [email protected] (B.-S. Sæther). 0044-8486/$ - see front matter © 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.aquaculture.2006.11.020
stocks having different life-history characteristics and migration patterns (Brander, 1994). The north-east Arctic cod (NAC) migrate from feeding areas in the Barents Sea to spawning areas in coastal waters (Hylen, 1964; Bergstad et al., 1987; Brander, 1994). The most important areas are near the Lofoten Islands and off Møre, although minor spawning areas and areas with occasional spawning are identified along the coast from Møre to Finnmark (Brander, 1994). The coastal cod (CC) inhabit coastal areas and fjords. They have shorter
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feeding migrations and spawn in a number of fjords (Rollefsen, 1954; Jakobsen, 1987; Maurstad and Sundet, 1998). Details about their life history are still relatively limited (Berg and Pedersen, 2001), but new research imply that they consist of both stationary and migrating sub populations (Svein Fevolden, Norwegian College of Fishery Science, personal communications). The regularity of the spawning in some fjords, however, indicates that they have populations that to a large extent are self sustainable (Jakobsen, 1987). Local fjord fishermen have harvested from these fish populations in generations (Maurstad and Sundet, 1998). However, the same fjord areas are well suited for fishfarming, and along the coastline more than 850 licences to farm salmonids have been granted. Over the last two decades the biomass of salmonids produced in Norwegian coastal waters has increased from less than 25,000 to more than 600,000 tonnes per year. In several areas along the Norwegian coast local fishermen asserts that wild migrating cod have changed their migratory behaviour following establishment of salmon farms, and no longer enters their natural spawning grounds in the fjords (Maurstad et al., in press). To the best of our knowledge, no long-term studies on the effect of salmon farming on wild cod populations have been conducted, and the causerelationship within the fjord systems may be very complex. This is complicated by observations made by fish farmers, who report that wild cod aggregate around the fish cages rather than avoiding them. Aggregation of wild fish around fish cages is earlier described by Carss (1990), and is also in agreement with several recent papers describing fish farms as “Fish Aggregating Device”, especially in the Mediterranean (Dempster et al., 2002; Boyra et al., 2004; Machias et al., 2005). The chemosensory systems in fish are extremely well developed, and mediate behaviours of fundamental importance, such as e.g. food finding, recognition/ location of familiar/preferred habitats, predator avoidance, and intraspecific communication (Sorensen and Caprio, 1998). Since chemical stimulants are important to the individual fish's conception of the surrounding environment, high density stocks of fish in a farm may then be expected to release significant amounts of waterborne information. If the asserted change in behaviour of migrating wild cod populations can be linked to establishment of salmon farms, water-soluble odorants are then likely candidates to explain such a connection. The present experiments were therefore conducted to test behavioural responses in wild Atlantic cod exposed to water containing metabolites and waste from farmed salmon.
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2. Materials and methods The experiment consists of several sets of trials that, due to availability of wild mature fish were conducted during different time periods. Fish for runs 1 (spring 2003) and 2 (spring 2004) were wild migrating Atlantic cod from a farm free area off Sørøya (70°30′ N 22°30′ E) in Northern Norway. The fish were caught using purse seine by a local fishing vessel in an area where they have captured coastal cod on spawning migration for generations. The fish was transported to the Tromsø Aquaculture Research Station, and stored in a circular tank (2 m diameter, 1 m water depth) with flow-through water at natural ambient temperature (6–8 °C), salinity (33 ppt) and natural photoperiod (transparent roof) before the trials. The reported aggregation of wild cod around fish cages was addressed in run 3 (autumn 2004) on cod caught at approximately 100 m distance from a salmon fish farm, located nearby Sørøya, using fish pots. These fish, later referred to as wild stationary, were stored in a small cage (5 × 5 × 5 m) in the sea nearby the Tromsø Aquaculture research station before trials, located in the same basin that supply the research station with sea water. Wild migrating cod for the 4th run (spring 2005) were caught at Malangsgrunnen (69°55′ N 18°29′ E), a fishing area absent of fishfarms used by coastal fishermen in the Tromsø region. These fish were caught by angling and special care was taken to reduce damages to the fish. No wild caught fish was stored at the research station for more than 1 month before trials started. During storage they were fed whole thawed capelin 3 times per week, approximately 5% of bodyweight per meal. Two year old farmed cod, originating from a commercial cod hatchery, Troms Marin Yngel, Tromsø, were also used in the third run during autumn 2004. These fish were fed commercial feed at a daily ration based on expected growth calculated from a fish size and temperature relationship provided by the feed manufacturer (Ewos). A preference-chamber system consisting of three tanks, each holding 1.7 m3 of water was used in all trials (Fig. 1). The tanks were interconnected by two 40 cm diameter 43 cm long plastic pipes. This allowed the fish to move freely between the tanks, still efficiently separating the water bodies between tanks (tested with Rhodamine). Each tank had a separate water supply via a vertical perforated pipe, delivering 20 l min− 1 , producing a circular water current speed of approximately 5 cm s− 1. The tanks were drained through the whole water column via a vertical perforated pipe in the tank centre, and water levels were held identical between tanks by a common external standpipe. The
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Fig. 1. Scematic view of a three-cell preference system used with large (mature) fish. Each tank has a water inlet (vertical spray) controlling the flow independently of the others, producing a circular waterflow (arrows) within each tank with very limited mixing of water between them. Fish can swim freely between tanks. Additional treatment water can be added to either of the side tanks.
end tanks (1 and 3) had modified water inlets, allowing treatment water to be added to the regular water flow. The amount of water added could be controlled between 45 and 925 ml min− 1 by an adjustable peristaltic pump, enabling controlled manipulation of treatment water concentrations in the preference system. Each tank in the preference system was videotaped, and positioning of the fish was also monitored by radio antennas mounted beneath the pipes connecting the tanks (Trovan ANT 612 HP combined with 650/655 LID decoders). These antennas registered passage of a Trovan ID 100 passive integrated transponder (PIT) attached to the fish, recording date and time for each time the fish passed through the pipe. Results from the PIT-tag system were compared with results from videotapes in the first run, and no difference in distribution of time spent in the different tanks was revealed (3 trials compared, highest Chi-square test value = 0.18, critical value at P < 0.05 = 5.991). All results reported here are based on data from the automated PIT-tag system. The treatment water used to test behavioural responses came from a 500 l tank holding salmon of 500 g average weight at a density of approximately 20 kg m− 3. The salmon were fed in excess during light hours, and treatment water was always collected during feeding periods. The feed used was commercially available salmon feed mainly based on fish meal and fish oil, but also contained some oil of vegetable origin. The treatment water was collected through a mesh sieve (1 mm) in the middle of the water column. The sieve prevented large particles to enter, but smaller particles, soluble metabolites and other odour factors could be introduced from the salmon tank. The water supplied to the salmon tank was from the same source as the water supplying the preference system, and had a high flow through so that oxygen tension typically was near 100% and never below 90%. The volume added to the
preference system in runs 1, 3 and 4 constituting about 4.6% of the water flow to the tank it was added (920 ml min− 1 to 20 l min− 1), temperature or oxygen tension were not affected. Tests where seawater from a tank without fish was added via the same system did not elicit any behavioural changes in cod, and both immature and mature migrating coastal cod responded similar to salmon treatment water (Sæther et al., unpublished results). Prior to trials in runs 1 and 3, individual fish was always acclimated to the preference system overnight without any treatment water added, and fish were tested separately. Fish that did not move between tanks during the acclimation period was replaced. Treatment water was first added to tank 1 for 1h after which the system was left to clean without addition of treatment water for 2 h. Given the water flow and tank volumes this supersedes the theoretical average water residence time, calculated as T = V × Q− 1, where T is time in minutes, V is tank volume in m3 and Q is water flow in m3 min− 1. Then treatment water was added to tank 3 for 1h, and the trial terminated. Positioning of the fish in each experiment was based on the last 30 min of the two treatment periods, and the response to the treatment is calculated as the percentage of these 60 min that the fish spends in each tank. The last 30 min was chosen to let the system stabilise, and allow the fish time to learn the new situation after the changes. Run 2 differed from this protocol as the same fish was used in a series of 5 trials over 5 days, stepwise reducing the concentration of treatment water between trials according to Table 1. Responses in wild cod were also tested towards water from a tank holding farmed cod. The protocol used in these trials was as previously described for runs 1 and 3. Comparisons of time spent in each tank before trials were based on data from the last 30 min before treatment started.
B.-S. Sæther et al. / Aquaculture 262 (2007) 260–267 Table 1 Proportion of time spent (% of 30 min) in a three-cell preference system by wild migrating Atlantic cod, with addition of treatment water from a tank holding Atlantic salmon Concentration −1
4.6% (925 ml min ) 3.5% (695 ml min− 1) 2.3% (463 ml min− 1) 1.2% (231 ml min− 1) 0.2% (45 ml min− 1)
n
Treatment
Intermediate No treatment
4 5 5 4 4
6.5 (5.1) 23.2 (28.8) 17.4 (24.5) 16.7 (21.9) 8.7 (14.4)
42.3 (19.8) 44.3 (27.1) 40.1 (22.8) 30.2 (16.5) 51.8 (29.3)
51.2 (18.8) 32.5 (27.1) 42.5 (27.4) 53.1 (24.3) 39.5 (37.7)
Numbers in brackets indicate variability as standard deviation. The addition of treatment water was changed as indicated in the first column, where 4.6% represents the same volume added as in the other trials reported in this paper. n is the number of trials for each concentration.
The contribution of olfaction to the response was tested in the 4th run, with a modified protocol. Each fish went through two trials on consecutive days. The first trial followed the same protocol as in runs 1 and 3. Immediately after the first trial, where any response to the treatment was established, the fish was anaesthetised again and the nostrils blocked using a fast setting hydroactive impression material (3rd Generation Affinity Light Body RF Vinyl Poly Siloxane, from Clinician's choice Dental Products Inc.), similar material and method as described in Vrieze and Sorensen (2001). The material was injected into the nasal cavity through the anterior opening until the pouch was filled up, indicated by a flow of impression material out through the posterior opening. It resulted in a complete blocking of the sensory epithelium in the lining of the cavity, avoiding passage of water to the olfactory nerve cells. After injection the material was left to set for 2–3 min before the fish was returned to the preference tank. The trial was repeated the following day according to the same protocol as the day before. After each trial on nostril-blocked fish, the nasal cavity was opened and the impression material plug checked.
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3. Results 3.1. Runs 1 and 2: wild migrating cod Before treatment started the migrating cod showed a general browsing behaviour by swimming continuously and regularly between the tanks, spending an equal share of the time in all three tanks (χ2 = 1.44; ν = 1). This behaviour changed during treatment periods, and, based on data from 15 trials in 2003 (average fish weight approximately 2.5 kg; run 1), wild migrating cod spent more time in the tank without addition of treatment water from the salmon tank with some short and irregular visits to the treated tank; 67.5 vs. 13.5% with 19% of the time spent in the intermediate tank (χ2 = 72.58; ν = 1; P < 0.001; Fig. 2a). In one of these trials, the cod showed a preference towards the tank that
2.1. Statistical analyses The proportion of time that the fish spent in tanks 1 and 3 was combined during treatment and no treatment periods and compared using Chi-square (χ2) analysis on contingency data. If the use of a tank during treatment differed significantly from a theoretic random use (i.e. 50%), the fish was considered to respond to the treatment. Responses to treatment between different groups of fish, e.g. wild migrating, wild stationery and farmed fish, were compared using Chi-square analysis on contingency data. Significant differences were assumed when p < 0.05.
Fig. 2. Proportion of time spent (% of 30 min) in a three-cell preference system by (a) wild migrating (n = 15), (b) wild stationary (n = 13) and (c) farmed Atlantic cod (n = 9), with addition of treatment water from a tank holding Atlantic salmon. Treatment water was alternately added to the end tanks in two consecutive periods. The bar in the middle shows proportion of time spent in the intermediate tank. Variation indicated as standard deviation.
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Fig. 3. Proportion of time spent (% of 30 min) in a three-cell preference system by wild migrating Atlantic cod, responding to treatment water from a tank holding farmed Atlantic cod (n = 4). Treatment water was alternately added to the end tanks in two consecutive periods. The bar in the middle shows the percentage of time spent in tank 2. Variation indicated as standard deviation.
received water from the salmon tank. Six of these 15 had running milt (5) or ovulated eggs (1), but this did not affect their behaviour as compared to the remaining maturing fish in this group (χ2 = 0.34; ν = 1). The findings from run 1 were confirmed in a new run of trials in 2004 (Table 1; 4.6%; run 2) on wild migrating cod from the same area (average weight 1.7 kg, 0.6 SD). Reduced addition of treatment water did not significantly change the resulting behaviour, even at 0.2% addition of water from the salmon tank (Table 1).
5 h period the trial lasted. This means that we do not know whether they did not respond, or did not know how to respond, i.e. not aware of the opportunity to move between tanks, and thus the results were omitted. Of the 9 trials where the fish did move between tanks, 2 fish avoided the treatment water and 2 fish were attracted to it. The other 5 showed no response to the treatment. The farmed cod differed in behaviour from wild cod as they were less mobile than their wild counterparts. The responses shown by the different groups of cod, wild migrating, wild aggregating and farmed cod (Fig. 2a–c) were compared. There was a highly significant difference in distribution pattern between these groups (χ2 = 40.93; ν = 2; P < 0.001), with increased aversion towards water from the salmon tank in farmed, wild aggregating and wild migrating cod, respectively. The difference between wild aggregating and farmed cod was only just significant (χ2 = 3.93 vs. critical value 3.84). In a series of 4 trials wild migrating cod responded to water from a tank holding farmed cod by spending significantly less time in the treated tank (χ2 = 53.1; ν = 1; P < 0.001; Fig. 3; prior to treatment fish spent an
3.2. Run 3: wild aggregating cod, farmed cod and cod– cod interactions In a series of totally 13 trials (average fish weight 1.3 kg, 1.1 SD), 9 wild aggregating cod responded with avoidance to addition of treatment water (4.6% addition). In 2 of the remaining 4, the cod showed a positive response to addition of water from the salmon holding tank, whereas the last two seemed indifferent to the treatment. Prior to trials, the fish spent an equal share of the time in each tank (χ2 = 0.53; ν = 2). All trials taken together, there was a significant effect of adding treatment water, as the time the cod occupied the treated tank was significantly reduced (χ 2 = 7.23; ν = 1; P < 0.05; Fig. 2b). However, the difference between times spent in tanks was not as obvious as in trials on wild migrating cod. From a total of 14 trials, farmed cod (average weight 1.4 kg, 0.3 SD) did not respond to addition of water from the salmon tank by avoiding the tank that was treated (χ2 = 0.163; ν = 1; Fig. 2c). Prior to trials, the fish spent an equal share of the time in each tank (χ2 = 2.192; ν = 2). From the 14 trials, 5 fish stayed in one tank regardless of treatment throughout the whole
Fig. 4. Proportion of time spent (% of 30 min) in a three-cell preference system by wild migrating Atlantic cod, responding to treatment water from a tank holding Atlantic salmon. The fish were exposed in two consecutive trials, first intact (a) and then anosmic (b), repeated 13 times with different fish (n = 13). Treatment water was alternately added to the end tanks in two consecutive periods. The bars in the middle show the percentage of time spent in tank 2. Variation indicated as standard deviation.
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equal share of the time in each tank χ2 = 4.43; ν = 2). This response was not different to what was observed in wild migrating cod exposed to salmon holding water (2003 data; χ2 = 0.025; ν = 1). 3.3. Run 4: behavioural responses in olfactory blocked (anosmic) fish Prior to trials the fish spent an equal share of the time in each tank (χ2 = 2.12; ν = 2). During a total number of 13 trials, 12 of the fish showed a negative response to the treatment water when intact (χ2 = 66.65; ν = 1; P < 0.001; Fig. 4). The last fish had a slight reduction, but not significantly so, in time spent in tanks with addition of treatment water. The results from the trials after blocking of the nasal cavity looked completely different, with the overall result including all 13 trials showing no difference in time spent between treated and untreated tanks (χ2 = 0.017; ν = 1; Fig. 4). Only one fish responded negatively after blocking, and dissections after the second trial revealed that one of the plugs had a poor fit to the nasal cavity and probably let water pass to the olfactory nerves. From the other 12 trials, 3 fish actually shifted preference when olfaction was blocked and showed a preference towards treated tanks in the second trial. 4. Discussion Results from the first run (spring 2003), showed that migrating wild mature cod reduce their time spent in a given area of the preference system when water from a tank holding salmon is added. The variation between individuals is relatively low, indicating a consistent response in all individuals. Results from the second run (spring 2004) confirmed these findings, and there seem to be limited effects of reducing the amount of water added between 4.6 and 0.2% of the total water flow per tank. However, teleost fishes in general have a sensitive olfaction system that mediate functions basic to survival of individuals and species, i.e. predator avoidance, feeding and reproduction (Hara, 1994; Sorensen and Caprio, 1998). Four classes of compounds have been identified as specific olfactory stimulants in fish, with their stimulatory effectiveness characterised: amino acids (especially L-amino acids), bile acids/salts, prostaglandins and sex steroids (Hara, 1994; Sorensen and Caprio, 1998). The detection thresholds for at least some of these compounds are at concentrations found in natural waters (Hara, 1994). From more than 30 species, Hara (1994) demonstrated electrophysiological thresholds from 10− 9 to 10− 7 M for the most stimulatory
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amino acids. The sensitivity towards bile salts is even higher and lies between 10− 12 and 10− 10 M (Døving et al., 1980; Hara et al., 1984). For further information on compounds and responses see also Smith (1997). The added water was unlikely to reduce the water quality per se to such an extent that it elicited the observed behavioural changes. The fish did not respond to addition of “un-used” water during tests previous to the experiments. This is further strengthened by the absence of response in olfactory-blocked (anosmic) fish. Gills of teleosts, including cod, have sensory neurons that respond to environmental changes in concentrations of O2 and CO2/pH (Evans et al., 2005). These are factors known to be affected by high biological activity and, thus, expected to be amongst the first that elicit behavioural changes in fish. Although the variety of functions of the gills are still not known (Evans et al., 2005), it is clear that anosmic fish did not change their behaviour, despite having access to some environmental information via the sensory systems located in the gills as well as the gustatory system located in the mouth/ head region. It seems therefore that the observed changed behaviour in wild migrating cod is based on presence of chemical compounds with olfactory properties. Cod of different origin responded differently to the salmon water. Farmed fish seemed in general indifferent to the treatment, although inconsistent aversion and attractant behaviour was observed in some fish as indicated by the high variability. The farmed fish may generally have a higher threshold for responding to changes in their chemosensory environment. Cod caught nearby a fish farm, most likely of a stationary coastal cod population, did respond negatively to salmon water, but the magnitude of the response was reduced and variability increased as compared to the wild migrating cod. These were stored in a cage before trials, as the only group of fish included. However, the basin in which they were stored did not hold any other cages, and all cage based research activity had been abandoned the last two years before this fish was stored there. Thus, there seem to be some population based differences in the response under experimental conditions. This is probably an effect of accommodation more than populations as such, as the farmed cod that did not respond was offspring from wild fish. Aggregation of wild fish, including cod, around fish farms are commonly observed by fish farmers and has also been subject to more detailed studies (Carss, 1990; Bjordal and Skar, 1992; Nøstvik and Pedersen, 1999; Dempster et al., 2002; Boyra et al., 2004). Fish cages seem to work as “Fish Aggregating Device” or “Artificially created
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ecosystems”, providing the wild fish shelter and easy access to food supplying increased growth rate and condition factor (Carss, 1990; Skog et al., 2003). According to fishermen, the cod that they follow and harvest during mating season belong to a migratory subpopulation different to those found around fish cages, and rather than being attracted to them they avoid areas with fish farming activity (Maurstad et al., in press). Thus, there may be two different responses amongst wild coastal cod to the same sort of stimuli, since some fish seem to be attracted and some seem to shy away. It is known from studies on alarm substances, initiating avoidance behaviour in fish, that learning is involved before the stimuli elicit the expected response (Chivers and Smith, 1995). Learning could explain the described difference in behaviour amongst cod; the stationary cod may connect the “fishfarm odours” with something positive (food) whereas naive cod with something unknown or negative. In habitat selection theory, the number of animals in a habitat may influence the profitability of the area (Kramer et al., 1997). Foraging profitability, for instance, will be reduced with increasing number of competitors foraging on the same prey. Waterborne olfactory substances are likely to be important indicators of frequency of competitors. An increase in fish density, as in the case of fish farms, may increase concentrations above levels that trigger changes in behaviour in wild fish. The signals could be perceived as “high concentration of predators” or simply “crowded”, which in both cases could make naive migrating wild cod avoid the area. Aversion towards water from a tank holding farmed cod indicates that the response seen in wild migrating cod is not species specific. This could mean that the observed response is caused by more general waterborne factors. In a recent study on tadpole larvae, Manteifel and co-workers (2005) describe avoidance to appearance of excreta in the water, and this response was repeated with added ammonia. The increased ammonia concentration is suggested to play a role as a non specific pheromone signal for amphibian tadpoles indicating the presence of predators. The experimental designs employed will not mimic all chemical stimulants found in nearby fish farms. For instance, flow-through tanks will not aggregate any waste, and neither will there be aggregation of any other species (fish, benthic feeders, shellfish etc.) that benefit from the “artificially created ecosystems” induced by fish farming. In nature, migrating cod have a strong incentive to go to the spawning areas. The experimental set-up does not offer any reward, but simply a choice of similar alternative places to stay.
This could mean that even the slightest disadvantages of one place, i.e. smell of other fish, could lead to reluctance to stay and therefore less time spent there. In nature, selection and preference of habitats is often considered as a trade-off between costs and benefits to the best long term interest (fitness) of the animal (Kramer et al., 1997). This would imply that the preference system used is too sensitive to generalise conclusions, since water from salmon may represent a cost of staying but no loss of leaving. The present paper provides results that do not preclude fishermen's observations that cod change their behaviour in areas with fish farming activity, further that the olfactory sense is still a strong candidate to mediate such a response. However, the responses seen in the present study need to be validated and detailed in further laboratory experiments as well as in nature, before conclusions as to any effect of fish farms on wild cod populations can be made. Identification of what waterborne olfactory stimulants that elicit the observed behaviour would give an opportunity to work with concentrations, and later correlate this to farming sites, hydrodynamic conditions and dilution distances, and migratory behaviour of coastal cod in fjord systems. The apparent difference between cod that are stationary around fish farms and cod that avoids them seems contradictory. Basic studies of the ecology of coastal cod are, however, relatively scarce. These need to be addressed in future work, and all available knowledge must be assembled and used in the management of aquaculture and its role in the coastal zone (Stead et al., 2002). References Berg, E., Pedersen, T., 2001. Variability in recruitment, growth and sexual maturity of coastal cod (Gadus morhua L.) in a fjord system in northern Norway. Fish. Res. 52, 179–189. Bergstad, O.A., Jørgensen, T., Dragesund, O., 1987. Life history and ecology of the gadoid resources of the Barents Sea. Fish. Res. 5, 11–161. Bjordal, A.A., Skar, A.B., 1992. Tagging of saithe (Pollachius virens L.) at a Norwegian fish farm: preliminary results on migration. ICES council meeting papers. ICES, Copenhagen (Denmark). ICES-CM-1992/G:35, 8 pp. Boyra, A., Sanches-Jerez, P., Tuya, F., Espino, F., Haroun, R., 2004. Attraction of wild coastal fishes to Atlantic subtropical cage fish farms. Gran Canaria Islands. Environ. Biol. Fishes 4, 39–401. Brander, K., 1994. Spawning and life history information for North Atlantic cod stocks. ICES Coop. Res. Rep., vol. 205. Copenhagen, 150 pp. Carss, D.N., 1990. Concentrations of wild and escaped fishes immediately adjacent to fish farm cages. Aquaculture 90, 29–40. Chivers, D.P., Smith, R.J.F., 1995. Free-living fathead minnows rapidly learn to recognize pike as predators. J. Fish Biol. 46, 949–954.
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Maurstad, A., Sundet, J.H., 1998. The invisible cod. Fishermen's knowledge and scientists' knowledge. In: Jentoft, S. (Ed.), Commons in a Cold Climate: Coastal Fisheries and Reindeer Pastoralism in North Norway: The Co-Management Approach. The Parthenon Publishing Group, New York, pp. 167–185. Maurstad, A., Dale, T., Bjørn, P.A., in press. You wouldn't spawn in a septic tank, would you? Hum. Ecol. Nøstvik, F., Pedersen, T., 1999. Movement patterns and growth of wild cod (Gadus morhua L.) and hatchery-reared cod released as 1group. In: Howell, B., Moksness, E., Svåsand, T. (Eds.), Stock Enhancing and Sea Ranching. Fishing news books. Blackwell Science Ltd., Oxford, pp. 315–333. Rollefsen, G., 1954. Observations on the cod and cod fisheries of Lofoten. Rapp. P.-V. Reun. - Cons. Int. Explor. Mer 136, 40–47. Skog, T.-E., Hylland, K., Torsteinsen, B.E., Berntssen, M.H.G., 2003. Salmon farming affects the fatty acid composition and taste of wild saithe Pollachius virens L. Aquacult. Res. 34, 999–1007. Smith, R.J.F., 1997. Avoiding and deterring predators. In: Godin, J.E. (Ed.), Behavioural Ecology of Teleost Fishes. Oxford University Press Inc., New York, pp. 163–190. Sorensen, P.W., Caprio, J., 1998. Chemoreception, In: Evans, D.H. (Ed.), The Physiology of Fishes, 2nd ed. Marine Science Series. CRC Press, Boca Raton, Florida, pp. 375–406. Stead, S.M., Burnell, G., Goulletquer, P., 2002. Aquaculture and its role in Integrated Coastal Zone Management. Aquacult. Int. 10, 447–468. Vrieze, L.A., Sorensen, P.W., 2001. Laboratory assessment of the role of a larval pheromone and natural stream odor in spawning stream localization by migratory sea lamprey (Petromyzon marinus). Can. J. Fish Aquat. Sci. 58, 2374–2385.
Behavioural responses in wild cod (Gadus morhua L.) exposed to fish holding water Bjørn-Steinar Sæther ⁎, Pål-Arne Bjørn, Trine Dale Norwegian Institute of Fisheries and Aquaculture Research (Fiskeriforskning), Breivika, 9291 Tromsø, Norway Received 28 July 2006; received in revised form 21 November 2006; accepted 22 November 2006
Abstract Local fishermen in several areas of Norway assert that salmon farms have caused the wild migrating cod to change their migratory behaviour, so that they no longer enter their natural spawning grounds in the fjords. If the asserted changes in behaviour of wild cod populations can be linked to establishment of salmon farms, water-soluble odorants are then possible candidates to explain such a connection. Chemical stimulants are important to the individual fish's conception of the surrounding environment. High density stocks of fish in a farm are expected to release large amounts of waterborne information. The present laboratory experiments were conducted to test behavioural responses in Atlantic cod exposed to water containing metabolites and waste from farmed salmon. The trials were conducted on single fish in a multiple chamber preference system. The results show that migrating wild Atlantic cod chose to spend more time in chambers without addition of water from the salmon tank, regardless of their maturation status, and even at very low concentrations (0.2%). The avoidance is probably due to presence of chemical compounds with olfactory properties from salmon, since anosmic cod did not elicit such response. Farmed cod, on the other hand, does not avoid water from the salmon tank, and stationary wild cod caught nearby a fish farm had a less pronounced response as compared to wild migrating cod. The response seen is not species specific, as wild migrating cod responded similar to water from a tank holding farmed cod as to water from salmon. These results do not preclude fishermen's observations that cod change their behaviour in areas with fish farming activity. Such a change in behaviour could be a response to water-soluble odorants, but needs to be validated and detailed in further laboratory experiments as well as in nature before any conclusions can be made. © 2006 Elsevier B.V. All rights reserved. Keywords: Chemosensory stimulants; Wild cod; Fishfarms; Interaction; Behaviour
1. Introduction Norwegian coastal waters host spawning grounds for the commercially important Atlantic cod (Gadus morhua L.). The Atlantic cod is divided into different
⁎ Corresponding author. Tel.: +47 77 62 90 00. E-mail address: [email protected] (B.-S. Sæther). 0044-8486/$ - see front matter © 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.aquaculture.2006.11.020
stocks having different life-history characteristics and migration patterns (Brander, 1994). The north-east Arctic cod (NAC) migrate from feeding areas in the Barents Sea to spawning areas in coastal waters (Hylen, 1964; Bergstad et al., 1987; Brander, 1994). The most important areas are near the Lofoten Islands and off Møre, although minor spawning areas and areas with occasional spawning are identified along the coast from Møre to Finnmark (Brander, 1994). The coastal cod (CC) inhabit coastal areas and fjords. They have shorter
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feeding migrations and spawn in a number of fjords (Rollefsen, 1954; Jakobsen, 1987; Maurstad and Sundet, 1998). Details about their life history are still relatively limited (Berg and Pedersen, 2001), but new research imply that they consist of both stationary and migrating sub populations (Svein Fevolden, Norwegian College of Fishery Science, personal communications). The regularity of the spawning in some fjords, however, indicates that they have populations that to a large extent are self sustainable (Jakobsen, 1987). Local fjord fishermen have harvested from these fish populations in generations (Maurstad and Sundet, 1998). However, the same fjord areas are well suited for fishfarming, and along the coastline more than 850 licences to farm salmonids have been granted. Over the last two decades the biomass of salmonids produced in Norwegian coastal waters has increased from less than 25,000 to more than 600,000 tonnes per year. In several areas along the Norwegian coast local fishermen asserts that wild migrating cod have changed their migratory behaviour following establishment of salmon farms, and no longer enters their natural spawning grounds in the fjords (Maurstad et al., in press). To the best of our knowledge, no long-term studies on the effect of salmon farming on wild cod populations have been conducted, and the causerelationship within the fjord systems may be very complex. This is complicated by observations made by fish farmers, who report that wild cod aggregate around the fish cages rather than avoiding them. Aggregation of wild fish around fish cages is earlier described by Carss (1990), and is also in agreement with several recent papers describing fish farms as “Fish Aggregating Device”, especially in the Mediterranean (Dempster et al., 2002; Boyra et al., 2004; Machias et al., 2005). The chemosensory systems in fish are extremely well developed, and mediate behaviours of fundamental importance, such as e.g. food finding, recognition/ location of familiar/preferred habitats, predator avoidance, and intraspecific communication (Sorensen and Caprio, 1998). Since chemical stimulants are important to the individual fish's conception of the surrounding environment, high density stocks of fish in a farm may then be expected to release significant amounts of waterborne information. If the asserted change in behaviour of migrating wild cod populations can be linked to establishment of salmon farms, water-soluble odorants are then likely candidates to explain such a connection. The present experiments were therefore conducted to test behavioural responses in wild Atlantic cod exposed to water containing metabolites and waste from farmed salmon.
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2. Materials and methods The experiment consists of several sets of trials that, due to availability of wild mature fish were conducted during different time periods. Fish for runs 1 (spring 2003) and 2 (spring 2004) were wild migrating Atlantic cod from a farm free area off Sørøya (70°30′ N 22°30′ E) in Northern Norway. The fish were caught using purse seine by a local fishing vessel in an area where they have captured coastal cod on spawning migration for generations. The fish was transported to the Tromsø Aquaculture Research Station, and stored in a circular tank (2 m diameter, 1 m water depth) with flow-through water at natural ambient temperature (6–8 °C), salinity (33 ppt) and natural photoperiod (transparent roof) before the trials. The reported aggregation of wild cod around fish cages was addressed in run 3 (autumn 2004) on cod caught at approximately 100 m distance from a salmon fish farm, located nearby Sørøya, using fish pots. These fish, later referred to as wild stationary, were stored in a small cage (5 × 5 × 5 m) in the sea nearby the Tromsø Aquaculture research station before trials, located in the same basin that supply the research station with sea water. Wild migrating cod for the 4th run (spring 2005) were caught at Malangsgrunnen (69°55′ N 18°29′ E), a fishing area absent of fishfarms used by coastal fishermen in the Tromsø region. These fish were caught by angling and special care was taken to reduce damages to the fish. No wild caught fish was stored at the research station for more than 1 month before trials started. During storage they were fed whole thawed capelin 3 times per week, approximately 5% of bodyweight per meal. Two year old farmed cod, originating from a commercial cod hatchery, Troms Marin Yngel, Tromsø, were also used in the third run during autumn 2004. These fish were fed commercial feed at a daily ration based on expected growth calculated from a fish size and temperature relationship provided by the feed manufacturer (Ewos). A preference-chamber system consisting of three tanks, each holding 1.7 m3 of water was used in all trials (Fig. 1). The tanks were interconnected by two 40 cm diameter 43 cm long plastic pipes. This allowed the fish to move freely between the tanks, still efficiently separating the water bodies between tanks (tested with Rhodamine). Each tank had a separate water supply via a vertical perforated pipe, delivering 20 l min− 1 , producing a circular water current speed of approximately 5 cm s− 1. The tanks were drained through the whole water column via a vertical perforated pipe in the tank centre, and water levels were held identical between tanks by a common external standpipe. The
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Fig. 1. Scematic view of a three-cell preference system used with large (mature) fish. Each tank has a water inlet (vertical spray) controlling the flow independently of the others, producing a circular waterflow (arrows) within each tank with very limited mixing of water between them. Fish can swim freely between tanks. Additional treatment water can be added to either of the side tanks.
end tanks (1 and 3) had modified water inlets, allowing treatment water to be added to the regular water flow. The amount of water added could be controlled between 45 and 925 ml min− 1 by an adjustable peristaltic pump, enabling controlled manipulation of treatment water concentrations in the preference system. Each tank in the preference system was videotaped, and positioning of the fish was also monitored by radio antennas mounted beneath the pipes connecting the tanks (Trovan ANT 612 HP combined with 650/655 LID decoders). These antennas registered passage of a Trovan ID 100 passive integrated transponder (PIT) attached to the fish, recording date and time for each time the fish passed through the pipe. Results from the PIT-tag system were compared with results from videotapes in the first run, and no difference in distribution of time spent in the different tanks was revealed (3 trials compared, highest Chi-square test value = 0.18, critical value at P < 0.05 = 5.991). All results reported here are based on data from the automated PIT-tag system. The treatment water used to test behavioural responses came from a 500 l tank holding salmon of 500 g average weight at a density of approximately 20 kg m− 3. The salmon were fed in excess during light hours, and treatment water was always collected during feeding periods. The feed used was commercially available salmon feed mainly based on fish meal and fish oil, but also contained some oil of vegetable origin. The treatment water was collected through a mesh sieve (1 mm) in the middle of the water column. The sieve prevented large particles to enter, but smaller particles, soluble metabolites and other odour factors could be introduced from the salmon tank. The water supplied to the salmon tank was from the same source as the water supplying the preference system, and had a high flow through so that oxygen tension typically was near 100% and never below 90%. The volume added to the
preference system in runs 1, 3 and 4 constituting about 4.6% of the water flow to the tank it was added (920 ml min− 1 to 20 l min− 1), temperature or oxygen tension were not affected. Tests where seawater from a tank without fish was added via the same system did not elicit any behavioural changes in cod, and both immature and mature migrating coastal cod responded similar to salmon treatment water (Sæther et al., unpublished results). Prior to trials in runs 1 and 3, individual fish was always acclimated to the preference system overnight without any treatment water added, and fish were tested separately. Fish that did not move between tanks during the acclimation period was replaced. Treatment water was first added to tank 1 for 1h after which the system was left to clean without addition of treatment water for 2 h. Given the water flow and tank volumes this supersedes the theoretical average water residence time, calculated as T = V × Q− 1, where T is time in minutes, V is tank volume in m3 and Q is water flow in m3 min− 1. Then treatment water was added to tank 3 for 1h, and the trial terminated. Positioning of the fish in each experiment was based on the last 30 min of the two treatment periods, and the response to the treatment is calculated as the percentage of these 60 min that the fish spends in each tank. The last 30 min was chosen to let the system stabilise, and allow the fish time to learn the new situation after the changes. Run 2 differed from this protocol as the same fish was used in a series of 5 trials over 5 days, stepwise reducing the concentration of treatment water between trials according to Table 1. Responses in wild cod were also tested towards water from a tank holding farmed cod. The protocol used in these trials was as previously described for runs 1 and 3. Comparisons of time spent in each tank before trials were based on data from the last 30 min before treatment started.
B.-S. Sæther et al. / Aquaculture 262 (2007) 260–267 Table 1 Proportion of time spent (% of 30 min) in a three-cell preference system by wild migrating Atlantic cod, with addition of treatment water from a tank holding Atlantic salmon Concentration −1
4.6% (925 ml min ) 3.5% (695 ml min− 1) 2.3% (463 ml min− 1) 1.2% (231 ml min− 1) 0.2% (45 ml min− 1)
n
Treatment
Intermediate No treatment
4 5 5 4 4
6.5 (5.1) 23.2 (28.8) 17.4 (24.5) 16.7 (21.9) 8.7 (14.4)
42.3 (19.8) 44.3 (27.1) 40.1 (22.8) 30.2 (16.5) 51.8 (29.3)
51.2 (18.8) 32.5 (27.1) 42.5 (27.4) 53.1 (24.3) 39.5 (37.7)
Numbers in brackets indicate variability as standard deviation. The addition of treatment water was changed as indicated in the first column, where 4.6% represents the same volume added as in the other trials reported in this paper. n is the number of trials for each concentration.
The contribution of olfaction to the response was tested in the 4th run, with a modified protocol. Each fish went through two trials on consecutive days. The first trial followed the same protocol as in runs 1 and 3. Immediately after the first trial, where any response to the treatment was established, the fish was anaesthetised again and the nostrils blocked using a fast setting hydroactive impression material (3rd Generation Affinity Light Body RF Vinyl Poly Siloxane, from Clinician's choice Dental Products Inc.), similar material and method as described in Vrieze and Sorensen (2001). The material was injected into the nasal cavity through the anterior opening until the pouch was filled up, indicated by a flow of impression material out through the posterior opening. It resulted in a complete blocking of the sensory epithelium in the lining of the cavity, avoiding passage of water to the olfactory nerve cells. After injection the material was left to set for 2–3 min before the fish was returned to the preference tank. The trial was repeated the following day according to the same protocol as the day before. After each trial on nostril-blocked fish, the nasal cavity was opened and the impression material plug checked.
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3. Results 3.1. Runs 1 and 2: wild migrating cod Before treatment started the migrating cod showed a general browsing behaviour by swimming continuously and regularly between the tanks, spending an equal share of the time in all three tanks (χ2 = 1.44; ν = 1). This behaviour changed during treatment periods, and, based on data from 15 trials in 2003 (average fish weight approximately 2.5 kg; run 1), wild migrating cod spent more time in the tank without addition of treatment water from the salmon tank with some short and irregular visits to the treated tank; 67.5 vs. 13.5% with 19% of the time spent in the intermediate tank (χ2 = 72.58; ν = 1; P < 0.001; Fig. 2a). In one of these trials, the cod showed a preference towards the tank that
2.1. Statistical analyses The proportion of time that the fish spent in tanks 1 and 3 was combined during treatment and no treatment periods and compared using Chi-square (χ2) analysis on contingency data. If the use of a tank during treatment differed significantly from a theoretic random use (i.e. 50%), the fish was considered to respond to the treatment. Responses to treatment between different groups of fish, e.g. wild migrating, wild stationery and farmed fish, were compared using Chi-square analysis on contingency data. Significant differences were assumed when p < 0.05.
Fig. 2. Proportion of time spent (% of 30 min) in a three-cell preference system by (a) wild migrating (n = 15), (b) wild stationary (n = 13) and (c) farmed Atlantic cod (n = 9), with addition of treatment water from a tank holding Atlantic salmon. Treatment water was alternately added to the end tanks in two consecutive periods. The bar in the middle shows proportion of time spent in the intermediate tank. Variation indicated as standard deviation.
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Fig. 3. Proportion of time spent (% of 30 min) in a three-cell preference system by wild migrating Atlantic cod, responding to treatment water from a tank holding farmed Atlantic cod (n = 4). Treatment water was alternately added to the end tanks in two consecutive periods. The bar in the middle shows the percentage of time spent in tank 2. Variation indicated as standard deviation.
received water from the salmon tank. Six of these 15 had running milt (5) or ovulated eggs (1), but this did not affect their behaviour as compared to the remaining maturing fish in this group (χ2 = 0.34; ν = 1). The findings from run 1 were confirmed in a new run of trials in 2004 (Table 1; 4.6%; run 2) on wild migrating cod from the same area (average weight 1.7 kg, 0.6 SD). Reduced addition of treatment water did not significantly change the resulting behaviour, even at 0.2% addition of water from the salmon tank (Table 1).
5 h period the trial lasted. This means that we do not know whether they did not respond, or did not know how to respond, i.e. not aware of the opportunity to move between tanks, and thus the results were omitted. Of the 9 trials where the fish did move between tanks, 2 fish avoided the treatment water and 2 fish were attracted to it. The other 5 showed no response to the treatment. The farmed cod differed in behaviour from wild cod as they were less mobile than their wild counterparts. The responses shown by the different groups of cod, wild migrating, wild aggregating and farmed cod (Fig. 2a–c) were compared. There was a highly significant difference in distribution pattern between these groups (χ2 = 40.93; ν = 2; P < 0.001), with increased aversion towards water from the salmon tank in farmed, wild aggregating and wild migrating cod, respectively. The difference between wild aggregating and farmed cod was only just significant (χ2 = 3.93 vs. critical value 3.84). In a series of 4 trials wild migrating cod responded to water from a tank holding farmed cod by spending significantly less time in the treated tank (χ2 = 53.1; ν = 1; P < 0.001; Fig. 3; prior to treatment fish spent an
3.2. Run 3: wild aggregating cod, farmed cod and cod– cod interactions In a series of totally 13 trials (average fish weight 1.3 kg, 1.1 SD), 9 wild aggregating cod responded with avoidance to addition of treatment water (4.6% addition). In 2 of the remaining 4, the cod showed a positive response to addition of water from the salmon holding tank, whereas the last two seemed indifferent to the treatment. Prior to trials, the fish spent an equal share of the time in each tank (χ2 = 0.53; ν = 2). All trials taken together, there was a significant effect of adding treatment water, as the time the cod occupied the treated tank was significantly reduced (χ 2 = 7.23; ν = 1; P < 0.05; Fig. 2b). However, the difference between times spent in tanks was not as obvious as in trials on wild migrating cod. From a total of 14 trials, farmed cod (average weight 1.4 kg, 0.3 SD) did not respond to addition of water from the salmon tank by avoiding the tank that was treated (χ2 = 0.163; ν = 1; Fig. 2c). Prior to trials, the fish spent an equal share of the time in each tank (χ2 = 2.192; ν = 2). From the 14 trials, 5 fish stayed in one tank regardless of treatment throughout the whole
Fig. 4. Proportion of time spent (% of 30 min) in a three-cell preference system by wild migrating Atlantic cod, responding to treatment water from a tank holding Atlantic salmon. The fish were exposed in two consecutive trials, first intact (a) and then anosmic (b), repeated 13 times with different fish (n = 13). Treatment water was alternately added to the end tanks in two consecutive periods. The bars in the middle show the percentage of time spent in tank 2. Variation indicated as standard deviation.
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equal share of the time in each tank χ2 = 4.43; ν = 2). This response was not different to what was observed in wild migrating cod exposed to salmon holding water (2003 data; χ2 = 0.025; ν = 1). 3.3. Run 4: behavioural responses in olfactory blocked (anosmic) fish Prior to trials the fish spent an equal share of the time in each tank (χ2 = 2.12; ν = 2). During a total number of 13 trials, 12 of the fish showed a negative response to the treatment water when intact (χ2 = 66.65; ν = 1; P < 0.001; Fig. 4). The last fish had a slight reduction, but not significantly so, in time spent in tanks with addition of treatment water. The results from the trials after blocking of the nasal cavity looked completely different, with the overall result including all 13 trials showing no difference in time spent between treated and untreated tanks (χ2 = 0.017; ν = 1; Fig. 4). Only one fish responded negatively after blocking, and dissections after the second trial revealed that one of the plugs had a poor fit to the nasal cavity and probably let water pass to the olfactory nerves. From the other 12 trials, 3 fish actually shifted preference when olfaction was blocked and showed a preference towards treated tanks in the second trial. 4. Discussion Results from the first run (spring 2003), showed that migrating wild mature cod reduce their time spent in a given area of the preference system when water from a tank holding salmon is added. The variation between individuals is relatively low, indicating a consistent response in all individuals. Results from the second run (spring 2004) confirmed these findings, and there seem to be limited effects of reducing the amount of water added between 4.6 and 0.2% of the total water flow per tank. However, teleost fishes in general have a sensitive olfaction system that mediate functions basic to survival of individuals and species, i.e. predator avoidance, feeding and reproduction (Hara, 1994; Sorensen and Caprio, 1998). Four classes of compounds have been identified as specific olfactory stimulants in fish, with their stimulatory effectiveness characterised: amino acids (especially L-amino acids), bile acids/salts, prostaglandins and sex steroids (Hara, 1994; Sorensen and Caprio, 1998). The detection thresholds for at least some of these compounds are at concentrations found in natural waters (Hara, 1994). From more than 30 species, Hara (1994) demonstrated electrophysiological thresholds from 10− 9 to 10− 7 M for the most stimulatory
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amino acids. The sensitivity towards bile salts is even higher and lies between 10− 12 and 10− 10 M (Døving et al., 1980; Hara et al., 1984). For further information on compounds and responses see also Smith (1997). The added water was unlikely to reduce the water quality per se to such an extent that it elicited the observed behavioural changes. The fish did not respond to addition of “un-used” water during tests previous to the experiments. This is further strengthened by the absence of response in olfactory-blocked (anosmic) fish. Gills of teleosts, including cod, have sensory neurons that respond to environmental changes in concentrations of O2 and CO2/pH (Evans et al., 2005). These are factors known to be affected by high biological activity and, thus, expected to be amongst the first that elicit behavioural changes in fish. Although the variety of functions of the gills are still not known (Evans et al., 2005), it is clear that anosmic fish did not change their behaviour, despite having access to some environmental information via the sensory systems located in the gills as well as the gustatory system located in the mouth/ head region. It seems therefore that the observed changed behaviour in wild migrating cod is based on presence of chemical compounds with olfactory properties. Cod of different origin responded differently to the salmon water. Farmed fish seemed in general indifferent to the treatment, although inconsistent aversion and attractant behaviour was observed in some fish as indicated by the high variability. The farmed fish may generally have a higher threshold for responding to changes in their chemosensory environment. Cod caught nearby a fish farm, most likely of a stationary coastal cod population, did respond negatively to salmon water, but the magnitude of the response was reduced and variability increased as compared to the wild migrating cod. These were stored in a cage before trials, as the only group of fish included. However, the basin in which they were stored did not hold any other cages, and all cage based research activity had been abandoned the last two years before this fish was stored there. Thus, there seem to be some population based differences in the response under experimental conditions. This is probably an effect of accommodation more than populations as such, as the farmed cod that did not respond was offspring from wild fish. Aggregation of wild fish, including cod, around fish farms are commonly observed by fish farmers and has also been subject to more detailed studies (Carss, 1990; Bjordal and Skar, 1992; Nøstvik and Pedersen, 1999; Dempster et al., 2002; Boyra et al., 2004). Fish cages seem to work as “Fish Aggregating Device” or “Artificially created
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ecosystems”, providing the wild fish shelter and easy access to food supplying increased growth rate and condition factor (Carss, 1990; Skog et al., 2003). According to fishermen, the cod that they follow and harvest during mating season belong to a migratory subpopulation different to those found around fish cages, and rather than being attracted to them they avoid areas with fish farming activity (Maurstad et al., in press). Thus, there may be two different responses amongst wild coastal cod to the same sort of stimuli, since some fish seem to be attracted and some seem to shy away. It is known from studies on alarm substances, initiating avoidance behaviour in fish, that learning is involved before the stimuli elicit the expected response (Chivers and Smith, 1995). Learning could explain the described difference in behaviour amongst cod; the stationary cod may connect the “fishfarm odours” with something positive (food) whereas naive cod with something unknown or negative. In habitat selection theory, the number of animals in a habitat may influence the profitability of the area (Kramer et al., 1997). Foraging profitability, for instance, will be reduced with increasing number of competitors foraging on the same prey. Waterborne olfactory substances are likely to be important indicators of frequency of competitors. An increase in fish density, as in the case of fish farms, may increase concentrations above levels that trigger changes in behaviour in wild fish. The signals could be perceived as “high concentration of predators” or simply “crowded”, which in both cases could make naive migrating wild cod avoid the area. Aversion towards water from a tank holding farmed cod indicates that the response seen in wild migrating cod is not species specific. This could mean that the observed response is caused by more general waterborne factors. In a recent study on tadpole larvae, Manteifel and co-workers (2005) describe avoidance to appearance of excreta in the water, and this response was repeated with added ammonia. The increased ammonia concentration is suggested to play a role as a non specific pheromone signal for amphibian tadpoles indicating the presence of predators. The experimental designs employed will not mimic all chemical stimulants found in nearby fish farms. For instance, flow-through tanks will not aggregate any waste, and neither will there be aggregation of any other species (fish, benthic feeders, shellfish etc.) that benefit from the “artificially created ecosystems” induced by fish farming. In nature, migrating cod have a strong incentive to go to the spawning areas. The experimental set-up does not offer any reward, but simply a choice of similar alternative places to stay.
This could mean that even the slightest disadvantages of one place, i.e. smell of other fish, could lead to reluctance to stay and therefore less time spent there. In nature, selection and preference of habitats is often considered as a trade-off between costs and benefits to the best long term interest (fitness) of the animal (Kramer et al., 1997). This would imply that the preference system used is too sensitive to generalise conclusions, since water from salmon may represent a cost of staying but no loss of leaving. The present paper provides results that do not preclude fishermen's observations that cod change their behaviour in areas with fish farming activity, further that the olfactory sense is still a strong candidate to mediate such a response. However, the responses seen in the present study need to be validated and detailed in further laboratory experiments as well as in nature, before conclusions as to any effect of fish farms on wild cod populations can be made. Identification of what waterborne olfactory stimulants that elicit the observed behaviour would give an opportunity to work with concentrations, and later correlate this to farming sites, hydrodynamic conditions and dilution distances, and migratory behaviour of coastal cod in fjord systems. The apparent difference between cod that are stationary around fish farms and cod that avoids them seems contradictory. Basic studies of the ecology of coastal cod are, however, relatively scarce. These need to be addressed in future work, and all available knowledge must be assembled and used in the management of aquaculture and its role in the coastal zone (Stead et al., 2002). References Berg, E., Pedersen, T., 2001. Variability in recruitment, growth and sexual maturity of coastal cod (Gadus morhua L.) in a fjord system in northern Norway. Fish. Res. 52, 179–189. Bergstad, O.A., Jørgensen, T., Dragesund, O., 1987. Life history and ecology of the gadoid resources of the Barents Sea. Fish. Res. 5, 11–161. Bjordal, A.A., Skar, A.B., 1992. Tagging of saithe (Pollachius virens L.) at a Norwegian fish farm: preliminary results on migration. ICES council meeting papers. ICES, Copenhagen (Denmark). ICES-CM-1992/G:35, 8 pp. Boyra, A., Sanches-Jerez, P., Tuya, F., Espino, F., Haroun, R., 2004. Attraction of wild coastal fishes to Atlantic subtropical cage fish farms. Gran Canaria Islands. Environ. Biol. Fishes 4, 39–401. Brander, K., 1994. Spawning and life history information for North Atlantic cod stocks. ICES Coop. Res. Rep., vol. 205. Copenhagen, 150 pp. Carss, D.N., 1990. Concentrations of wild and escaped fishes immediately adjacent to fish farm cages. Aquaculture 90, 29–40. Chivers, D.P., Smith, R.J.F., 1995. Free-living fathead minnows rapidly learn to recognize pike as predators. J. Fish Biol. 46, 949–954.
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