NOT TO BE CITED WITHOUT PRIOR REFERENCE TO THE AUTHORS

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1 NOT TO BE CITED WITHOUT PRIOR REFERENCE TO THE AUTHORS International Council for the Exploration of the Sea Theme session T: Salmon Aquaculture, Enhancement, and Ranching: are they a Threat to Wild Salmonid Stock. ICES CM 2002/T:06 Planktonic distribution of sea lice Lepeophtheirus salmonis larvae in inter-tidal plankton samples in Loch Shieldaig, Western Scotland in relation to local salmon farm production cycles. M. A. McKibben 1 & D. W. Hay 2 1 FRS Freshwater Laboratory, Shieldaig Field Station, Shieldaig, Strathcarron, Wester Ross, Scotland 2 FRS Freshwater Laboratory, Faskally, Pitlochry, Scotland. Abstract Sea trout, Salmo trutta, numbers on the west coast of Scotland have fallen over the last thirty years. This decline is linked to reduced survival in the marine phase. Sea lice infection may potentially have a detrimental impact on the survival of wild smolts soon after seawater transfer. This study examines the levels of planktonic sea lice larvae in the inter-tidal areas of Loch Torridon close to river mouths where sea trout are known to congregate in the first few days after going to sea, with concurrent sampling of wild fish in the lower Shieldaig river Planktonic copepodids were present in high numbers, peak minimum densities of larval sea lice of 71 and 94 m -3 respectively were recorded at the mouth of the rivers Balgy and Shieldaig. Within 5 m of the shore, close to the mouth of the River Shieldaig, a peak minimum density of larval sea lice of 423 m -3 was detected. These values exceed the highest densities reported in the literature so far. This study showed a marked inter-annual difference between the samples taken in 2000 and 2001 in Loch Torridon with sea lice copepodids only being found in 2001 when gravid female sea lice were present on local fish farms. Wild fish sampling also showed a inter-annual difference in sea lice levels which was related to fish farm production cycles. Early returning sea trout smolts with high levels of sea lice are only seen in the second year of the production cycle but are scarce in the first year of production when ovigerous sea lice levels are zero. The alternate year presence/absence information suggests that the source of sea lice found in Loch Torridon is not from wild fish but is of fish farm origin.

2 Introduction The sea louse Lepeophtheirus salmonis is a parasite of salmonid fishes, which include, in Scottish waters, the Atlantic salmon Salmo salar and the anadromous trout Salmo trutta. The salmon louse has become an important parasite in the Scottish salmon farming industry with losses of fish and growth potential associated with the parasite estimated to cost the industry 30 million pounds per year (Anon., 1999). It has also been linked to the decline of sea trout stocks in Ireland (Tully et al., 1993; Anon 1994; 1995), Norway (Birkeland, 1995) and Scotland (Northcott & Walker, 1996; Butler et al., 2001) Epizootics have occurred in wild sea trout in Ireland (Tully et al., 1993) and Norway (Grimnes & Jakobsen, 1996) and have been associated with significant host pathology. Studies in the wild have shown that liced sea trout return to rivers sooner than uninfected sea trout (Birkeland & Jakobsen, 1997). Early returning sea trout, sometimes within days of running to sea have been recorded on the west coast of Ireland (Tully et al., 1993; Anon 1994; 1995), Norway (Birkeland 1995) and Scotland (Northcott & Walker, 1996; Butler et al., 2001). In Ireland and Norway they have linked this phenomenon with salmon farming activities (Tully & Whelan 1993; Tully et al., 1999). In Scotland there is some correlation between finding these early returning post smolts and the presence of fish farming activity (Northcott et al., 2001). The larval distributions and densities of L. salmonis in Ireland and Norway have been studied for some time (Costelloe et al., 1995; 1996; 1998a; 1998b; O Donoghue et al., 1998), and the presence of these marine ecto-parasites has been recorded close inshore in areas where sea trout smolts first congregate on entering the sea. This study continues and extends the observations made by Northcott et al. (2001) by examining levels of larval sea lice in the inter-tidal areas of Loch Torridon close to river mouths where sea trout are known to congregate in the first few days after going to sea (Johnstone, Walker, Urquhart & Thorne, 1995). This study also looked at the presence and absence of early returning post smolt sea trout (Salmo trutta) and the seasonal activities of the local salmon farms in the Loch Torridon system. A pilot study in 1999 (Northcott et al., 2001) showed that early returning sea trout were present in the lower part of the River Shieldaig within a week of sea trout heading to sea.

3 Study Area Loch Shieldaig (Fig 1) is part of the larger Loch Torridon system (Fig 2) and is exposed to the north west. The loch was chosen because of the existing sea trout trap at the mouth of the River Shieldaig which would provide information on the number and timing of sea trout smolts running to sea during the study period. The nearest salmon farm is at Aird, 4.6km from the mouth of the river. Materials and Methods. Field sampling procedure. The initial study ran from March to June 2000, covering the period when sea trout smolts enter the sea. The sampling period was extended in 2001 from March until September. Surface water was sampled using a 1metre long cone-shaped net with a mesh of 140 µm and a mouth diameter of 30 cm. A flow meter could not used to estimate net efficiency as the areas sampled included substantial weed cover. Larval densities are taken to be minimum values for the area sampled. The net was towed at constant speed either from a small boat or by wading. All samples were taken on the surface with the net just breaking the surface layer close to shore in water depths between 1 3 metres. Three main areas (called sweeps) were sampled (Figure 1). The volume of water sampled was calculated by multiplying the mouth area of the net by the distance towed, measured between marks on the shore. In general, tows were taken within one hour of high tide, constrained by daylight conditions. After each tow was completed, the plankton net was washed down with seawater and the residue stored in 500ml jars of seawater with 50 ml of 40% formalin added. To further localise the presence of sea lice larvae in the inter-tidal zone, a series of samples were taken perpendicular to the shoreline. Samples were taken from 15 metres offshore to 10metres offshore (sweep 15), from 10 metres offshore to 5 metres offshore (sweep 10) and from 5 metres offshore to the shoreline (sweep 5). As well as repeating the samples taken in 2000, extra sampling sites were added in Samples were collected from the River Balgy in Upper Loch Torridon (Figure 2). Where a 60 metre shore sweep on the east shore was taken. The presence or absence of early returning post smolts was examined by electrofishing for post smolts from Apr - June in 2001 and An area approximately 1100m 2, from close to the high water mark to the fish trap approximately 120 metres upstream was fished. The trap created an upstream barrier for the fish. The presence of a number of pools (less than 1.5metres deep) allow good habitat for sea trout to rest in upon returning to freshwater. In the present study the hypothesis that there was no significant difference in early returning sea trout numbers between the first and second year in the production cycle of the local fish farms is tested. Electrofishing allowed the fish to be captured live, photographed and tagged and their subsequent recaptures studied.

4 The study area was electrofished between the 12/04/01 and the 22/07/01, on 9 occasions and between the 02/05/02 and the 19/07/02 on 5 occasions. The presence or absence of post smolts and liced post smolts was recorded. Results River Shieldaig 2000 In 2000, samples were taken weekly from the 22 nd of March until the 19 th of June A sample was taken at high tide on each sampling date from sweeps one, two and three. All results for the 2000 sampling programme were negative with no larval stages of sea lice found in any of the samples. After the 2000 Shieldaig river-mouth sea lice samples had been collected and analysed, the formation of a local Area Management Group (AMG) permitted the exchange of sea lice data between fish farms and wild fish interests. Although it had been assumed that sea lice levels would be low on the local fish farms during 2000 because they were in the first year of production, the supply of the fish farm sea lice data allowed a direct comparison to be made. Over the period when no sea lice copepodids were found on the shoreline of Loch Shieldaig, there were no gravid female sea lice present on any of the farms in Loch Torridon. Figure 3 details the results of sweep three and the gravid lice information from the nearest fish farm in Aird, 4.6 km away. River Shieldaig 2001 In Loch Shieldaig in 2001, the spring sea lice sampling regime was extended compared with Samples were collected weekly from the 15 th of March until the 10 th of September 2001 (Fig. 4). The maximum sea lice density recorded from the sweeps was 94 lice m -3. The only larval sea lice stage found in the samples was the copepodid, no naupliar stages were found. The period of the smolt run from the River Shieldaig is also detailed. During the period of peak sea lice shoreline densities in spring 2001, additional sampling was carried out towards the shore to localise the copepodid distribution in relation to the shoreline (Fig. 5). When present, sea lice copepodids were invariably found in the 5-metre strip closest to the shore. The results were highly variable with a maximum density of 423 lice m - ³ being recorded. Throughout 2001 the potential production of sea lice eggs in the Loch Torridon system was substantial. The numbers of gravid female sea lice on the 5 fish farms in the area are shown in Figure 6. One of the fish farms, Camas, ceased production during 2001 after the stock was killed by jellyfish. Two of the fish farms, Torridon and Diabeg, treated with Slice which resulted in a substantial lowering of the number of gravid female sea lice at these sites. However, despite this, there remained substantial numbers of gravid female sea lice in the loch in all weeks throughout 2001.

5 River Balgy 2001 The results from the Shieldaig and Balgy (Fig. 7) show a similar pattern of sea lice abundance in spring 2001 at the river-mouths with substantial densities of sea lice copepodids present before and during the period of the smolt migration, which in the Shieldaig extended from 03/04/01 to 28/06/02. A comparison of the Balgy shoreline data and the Torridon fish farm data over the same period in spring 2001 reveals a pattern of progressive development of sea louse stages. Firstly the shoreline data show a rise in copepodids followed by the progressive appearance of chalimus, pre-adult and gravid females on the fish farm. As the levels of gravid female sea lice on the fish farm were low prior to this occurrence it is not likely that this fish farm was the source of the infection. The observations at upper Loch Torridon fish farm and on the Balgy shore (Fig. 8) are consistent with a pulse of sea lice copepodids entering upper Loch Torridon from Loch Shieldaig, where fish farms had substantial levels of gravid sea lice, then passing through the only fish farm in upper Loch Torridon, which at that time had very low gravid sea lice levels. (This was at the same time as substantial numbers of copepodids also arrived at the mouth of the River Shieldaig.). Sea Trout post-smolts In 2001, a total of 155 fish were examined from electrofishing below the fish trap. Thirty nine 39 sea trout post smolts had different lice stages present. In 2002 only 34 fish were collected with only five of them having sea lice present (fig 9). As none of the sea trout collected in 2001 were tagged in the Shieldaig River they were probably strays from other river systems.

6 Discussion The importance of sea lice infestations on sea trout post-smolts can not be overestimated. A serious decline in sea trout numbers in north western Scotland since the 1970 s has been observed (Butler et al., 2001). In a study in Ireland, Tully et al. (1999) found that infestations of post-smolt sea trout by L. salmonis occurred in bays that contained lice-infested farmed salmon. During the sampling period in 2000, when gravid female sea lice levels on the local fish farm were zero, not even background levels of sea lice were found at the shore. Either wild fish populations are currently too low to support sea lice populations or the levels were below the detection range of the sampling regime (Fig 3). Costelloe et al. (1996) found sea lice larvae consistently at a station close to a salmon farm but only sporadically close to a river mouth. The maximum lice level found close to the river mouth was 16 lice m -3. These findings led to the conclusion that there was a very high retention of sea lice within fish farms and that lice found at river mouths came from wild salmon and sea trout (Costelloe et al., 1996; Gravil 1995). Donoghue et al. (1998) claimed that it was highly probable that as the larvae develop to the copepodid stage, they immediately attach to the available reservoir of hosts present in the cage. This view was also supported by Gravil (1995). In the course of this study planktonic sea lice were found regularly close to river mouths and in high concentrations at a time when sea trout smolts were going to sea (fig. 4). This figure also shows that the major concentrations of sea lice are primarily located close to the river mouth rather than being dispersed along the shores of Loch Shieldaig with the highest levels being observed in late March and again in late April The high levels taken perpendicular to the shore (fig. 5) might represent copepodids that have accumulated on the shore but are not still viable. Figure 7 details the comparison between sea lice copepodids at the mouth of both the Shieldaig and the Balgy rivers in spring 2001, the similarities between the peaks at both rivers in late April is striking. O Donoghue et al. (1998) found that although sea lice spawning occurred throughout their study on a salmon farm in Ireland, distinct peaks were observed suggesting that there may be some synchronicity in spawning behaviour. The relationship between sea lice levels at the Balgy shore and the upper Loch Torridon fish farm shown in Figure 8, suggests that sea lice could be dispersed over substantial distances around sea lochs. In the absence of synchronised sea lice treatments on all fish farms within a loch system, farms could be re-infected by larval sea lice circulating from elsewhere, reducing any long-term advantage from treatment. This finding emphasises the need for integrated fish farm area management. The samples of post smolts may only represent the proportion of the population returning to freshwater rather than the entire population (Tully et al., 1998). No comparison of the distributions of sea lice in fish returning to freshwater and those remaining at sea has been undertaken. Lice larvae infecting sea trout post-smolts originate either from wild salmon or sea trout or farmed salmon as this parasite is specific to salmonids (Tully et al., 1998). As our fish were taken in freshwater and

7 only sampled every two weeks some sea lice may have been lost. A study in 1990 found that a large proportion of the sea lice attached to fish held in freshwater were lost during the first 48hrs. The few remaining lice remained attached for up to 144hrs (McLean et al., 1990). Birkeland (1996) indicated that the catch rate of post smolts in systems where the level of infestation is high is greater than in systems where the infestation rate is low. If sea lice induce fish to return prematurely to freshwater then there should be a positive relationship between catch per unit effort sampling in estuaries and the level of infestation on those fish. Therefore the high numbers of liced sea trout caught in 2001 in comparison to 2002 should indicate higher levels of infestation in 2001 (fig 9) This study showed that the infectious stage of the sea louse Lepeophtheirus salmonis can be successfully located close to river mouths by plankton sampling. Copepodids were present in high numbers over a sustained period and were particularly abundant in the early spring at times when salmon and sea trout smolts enter the sea. Plankton samples only contained sea lice copepodids when the local fish farms were in the second year of their production cycle. Early returning post smolt sea trout were more commonly found when the local fish farms were in the second year of their production cycle. The alternate year presence or absence information suggests that the source of sea lice found in Loch Torridon in the plankton and on sea trout post smolts is not from wild fish but is of fish farm origin.

8 Bibliography Anon. (1994) Report of the Sea Trout Working Group (1993). Department of the Marine, Dublin. 127pp. Anon. (1995) Report of the Sea Trout Working Group (1994). Department of the Marine, Dublin. 254pp. Anon. (1999) Trouw Outlook No. 11. Special Edition Sea Lice. Trouw Aquaculture, 16pp. Birkeland, K. (1995) Salmon lice, Lepeophtheirus salmonis Krøyer, infestations and implications for anadromous brown trout, Salmo trutta L. PhD thesis, University of Bergen, Norway. Birkeland, K. (1996). Consequences of premature return by sea trout (Salmo trutta) infested with the salmon louse (Lepeophtheirus salmonis Krøyer): migration, growth and mortality. Canadian Journal of Fish and Aquatic Sciences. 53, Birkeland, K. & Jakobsen, P. (1997) Salmon lice, Lepeophtheirus salmonis, infestation as a causal agent of premature return to rivers and estuaries by sea trout Salmo trutta L., post smolts. Environmental Biology of Fishes 49, Butler, J.A., Marshall, S., Watt, J., Kettlewhite, A., Bull, C., Bilsby, M., Bilsby, H., Ribbens, J., Sinclair, C.A., Stoddart, R.C., & Crompton, D.W.T. (in review). Pattern of sea lice infestations on Scottish west coast sea trout: survey results, Costelloe, J., Costelloe, M. & Roche, N. (1995). Variation in sea lice infestation on Atlantic salmon smolts in Killary Harbour, West Coast of Ireland. Aquaculture International. 3, Costelloe, M., Costelloe, J. & Roche, N. (1996) Planktonic dispersion of larval salmon lice, Lepeophtheirus salmonis, associated with cultured salmon, Salmo salar, in western Ireland. Journal of the Marine Biological Association of the United Kingdom 76, Costelloe, M., Costelloe, J., Coghlan, N., O Donohoe, G., & O Connor, B. (1998a) Distribution of the larval stages of Lepeophtheirus salmonis in three bays on the west coast of Ireland. ICES Journal of Marine Science 55, Costelloe, M., Costelloe, J., O Donohoe, G., Coghlan, N.J., Oonk, M. & Van Der Heijden, Y. (1998b). Planktonic distributions of sea lice larvae, Lepeophtheirus salmonis, in Killary Harbour, West Coast of Ireland. Journal of Marine Biological Association U.K. 78, Gravil, H.R. (1996). Studies of the biology and ecology of the free swimming larval stages of Lepeophtheirus salmonis (Krøyer, 1838) and Caligus elongatus

9 Nordmann, 1832 (Copepoda: Caligidae). Unpub. Ph.D. thesis, University of Stirling. 299pp. Grimnes, A. & Jacobsen, P.J., The physiological effects of salmon lice (Lepeophtheirus salmonis Krøyer) infection on post smolt of Atlantic salmon (Salmo salar). Journal of Fish Biology 48, Johnstone, A.D.F., Walker, A.F., Urquhart, G.G. and Thorne, A.E. (1995) The movements of sea trout smolts, Salmo trutta L., in a Scottish west coast sea loch determined by acoustic tracking. Scottish Fisheries Research Report No. 56, Scottish Office Agriculture, Environment and Fisheries Department 21pp. McLean, P.H., Smith, G.W. & Wilson, M.J. (1990) Residence time of the sea louse, Lepeophtheirus salmonis K., on Atlantic salmon, Salmo salar L., after immersion in fresh water. Journal of Fish Biology 37, Northcott, S.J. & Walker, A.F. (1996). Farming salmon, saving sea trout; a cool look at a hot issue. In Aquaculture and Sea Lochs, ed. K. Black, The Scottish Association for Marine Science, 93pp. Northcott, S.J., Bresnan, E.M., McKibben, M.A. & Walker, A.F. (2001). The primary location of infection of sea trout, Salmo trutta L., post-smolts by sea lice, Lepeophtheirus salmonis (Kryer), in a Scottish sea loch. FRS report Freshwater Fisheries Laboratory. 20pp. O Donoghue, G., Costelloe, M. & Costelloe, J. (1998). Development of a Management Strategy for the Reduction/Elimination of Sea Lice Larvae, Lepeophtheirus salmonis, parasites of salmon and trout. Marine Resource Series. No. 6. The marine Institute, Dublin, Ireland. 51pp. Tully, O., Whelan, K.F. (1993). Production of nauplii of Lepeophtheirus salmonis (Krøyer) (Copepoda: Caligidae) from farmed and wild salmon and its relation to the infestation of wild sea trout (Salmon trutta L.) off the west coast of Ireland in 1991). Fisheries Research. 17, Tully, O., Poole, W.R., Whelan, K.F. & Merigoux, S. (1993) Parameters and possible causes of epizootics of Lepeophtheirus salmonis (Krøyer) infesting sea trout (Salmo trutta L.) off the west coast of Ireland. In: G.A. Boxshall and D. Defaye (eds) Pathogens of Wild and Farmed Fish: Sea Lice. Ellis Horwood Ltd., London, Tully, O., Gargan, P., Poole, W.R. & Whelan, K.F. (1999) Spatial and temporal variation in the infestation of sea trout (Salmo trutta L.) by the caligid copepod Lepeophtheirus salmonis (Krøyer) in relation to sources of infection in Ireland. Parasitology 119,

10 Figure 1: Loch Shieldaig, showing the three shore sweeps taken in 2000 and 2001.

11 Figure 2: The Loch Torridon system showing the rivers and the salmon farms in the system. Figure 3: Planktonic sea lice levels and local fish farm levels Mean gravid L.salmonis Mar May Jul Sep Nov Date Gravids Copepodids

12 Figure 4: Sea lice levels Loch Shieldaig shore Sweeps 1,2 and 3, Period of smolt run 100 Minimun lice m Mar Apr May Jun Jul Aug Sep Date Figure 5: Distribution of planktonic lice in Sweeps 5,10 and Minimum lice m Sweep /03/ /04/01 16/05/2001 Date 11/06/2001

13 Figure 6: Gravid female sea lice numbers in the 5 fish farms in the Loch Torridon area in Mean gravid females Jan Apr Aug Dec 2001 Aird Kenmore Camas Diabeg Torridon Figure 7: Comparison of sea lice copepodid levels at the mouth of the Shieldaig and Balgy in spring/summer Minimum lice m Mar Apr May Jun Jul Aug Months Balgy Shieldaig

14 Figure 8: The relationship between Balgy shoreline sea lice copepodid levels and sea lice levels on the Loch Torridon fish farm in spring Balgy Copepodids Torridon Pre-Ad Torridon Chalimus Torridon Gravids Figure 9: Post smolt incidence 2001 and 2002, electrofishing results from the Shieldaig River. No. of fish caught Year Liced Unliced