Sea lice infestation rates on wild and escaped farmed Atlantic salmon (Salmo salar L.) entering the Magaguadavic River, New Brunswick

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1 doi:1.1111/j x Sea lice infestation rates on wild and escaped farmed Atlantic salmon (Salmo salar L.) entering the Magaguadavic River, New Brunswick Jonathan Carr & Frederick Whoriskey Atlantic Salmon Federation, St Andrews, NB, Canada Correspondence: J Carr, Atlantic Salmon Federation, PO Box 5, St Andrews, NB, Canada E5B 3S8. Abstract A monitoring program for the prevalence and of sea lice infestations of wild and escaped farmed salmon has been underway on the Magaguadavic River since. Fish are screened in a sh ladder trap located in freshwater a short distance above the head of tide. No trends with time were evident in observed sea lice burdens, and in all years the majority of salmon, both wild and escapees, had no or low levels of infestation with sea lice. In the spring of 2, 23 landlocked salmon moving to sea from the Magaguadavic River were acoustically tagged. Two sh returned to the river after a brief period of residence in Passamaquoddy Bay, with signi cant dermal damage from sea lice. These sh were tracked to areas close to commercial salmon farms. Keywords: sea lice, wild and escaped farmed and landlocked salmon Introduction Sea lice, Lepeophtheirus salmonis Kryer, are natural parasites of salmonids, and generally occur in low numbers on wild sh (Boxshall 1974; Berland ). Occasionally, epidemics erupt in wild salmon populations (White 19; Johnson, Blaylock, Rlphick & Hyatt ). In many areas where the farming of Atlantic salmon (Salmo salar, Linnaus) occurs, sea lice have become a signi cant problem for the farmed salmon, and there is concern that the parasite could be spreading from infected farmed sh to wild salmonid populations (Bjorn & Finstad 2). In the late 197s, the development of the Atlantic salmon farming industry began along Canada s east coast in the Bay of Fundy region. Sea lice infestations have been problematic for the farms in this region, and lice reached epidemic levels in the industry in, resulting in high sh mortality and signi cant economic losses (Hogans ; MacKinnon ). Various treatments are used to attempt to control lice numbers in the industry. Wild Atlantic salmon populations in the Bay of Fundy region are severely depressed (DFO 3), and there is concern that mortalities caused by lice could be contributing to the declines. Since, we have conducted a lice-monitoring program on adult wild and escaped farmed salmon entering the Magaguadavic River, New Brunswick. Our objectives were to: (1) document the prevalence and of sea lice burdens (chalimus to adult stages of Lepeophtheirus salmonis as described by Johnson & Albright 1991) on wild, escaped farmed and landlocked salmon returning to freshwater in the Magaguadavic River; (2) document positions lice occupied on the bodies of the salmon and what damage the lice did to the sh; (3) investigate a possible link between lice prevalence/ and the age or size of wild and farmed salmon. Materials and methods Study area The Magaguadavic River is the sixth largest river in New Brunswick with a drainage area of 1812 km 2.It r 4 Blackwell Publishing Ltd 723

2 originates in Magaguadavic Lake in the southwest part of the province and ows southeasterly 88 km to a head of tide hydroelectric dam. Its tidal water drains an additional 9 km before emptying into Passamaquoddy Bay (Fig. 1). A pool and weir sh ladder bypasses the 13.4 m high head of tide dam for all upstream sh passage (Fig.1). The sh ladder consists of 43 pools (including two resting pools), each 3.5 cm higher than the one below. Wild salmon ascend the river from June until early November. Escaped farmed salmon ascend the river from May to December, with their numbers peaking during the fall (Carr ; Carr, Anderson,Whoriskey & Dilworth ). The Magaguadavic system formerly supported a sea run salmon shery, but this was closed in due to severe run declines. The river now supports a sport shery for brook trout (Salvelinus fontinalis, Mitchill), introduced smallmouth bass (Micropterus dolomieui, Lace pe' de), and landlocked Atlantic salmon. Landlocked salmon normally complete their entire life cycle in freshwater. Landlocked salmon are stocked annually to the Magaguadavic system by the Province for sport shery purposes, and some wild reproduction occurs. In recent years, we have detected movements of landlocked salmon to the sea.this is a signi cant shift in their life history strategy. Sonic tracking studies revealed that some landlocked salmon behaved similar to wild sea trout, with movements to sea in the spring and subsequent returns to the river in later months. Escaped farmed salmon have been detected entering the river in every year since systematic monitoring began in. The escapees have been either one sea winter (1SW) sh, two sea winter (2SW) sh or post smolts. Post smolts are sh that have spent less than 1 year at sea before returning to the river. Generally, they are precociously maturing males. Seawater salinity is 26.4 ppt (2-m depth) at low tide 5-m downriver from the bottom of the sh ladder. Downstream of this point salinity levels are 4 ppt at all water depths. Upstream of this area, the river rises steeply to a dam and its associated sh ladder. At the base of the ladder, is a freshwater pool in which sh can hold before continuing their upstream migration. Fish can access the sh ladder onlyat high tides. We have limited information on the amount of time the sh spend in the pool at the base of the ladder, or in the ladder itself, during the upstream migration. Three sonically tagged sh took from a few hours to 3 days to clear the ladder once they entered it. Other sh have been observed to remain in the chamber immediately below the sh ladder s collection trap for more than 7 days before moving into the trap. Lice monitoring Since, all salmonids that ascended the river were captured in the trap of the sh ladder.wild salmon were distinguished from farmed escapees using external morphology and scale circuli characteristics (Carr;Carr et al. ). Landlocked salmon were identi ed on the basis of n clips for recently stocked sh, and/or scale analysis. Fork length was recorded to the nearest mm, and a sample of scales was taken from all sh. Scales were also used to age the sh. Sea lice counts Figure 1 Map showing the tidal portion of the Magaguadavic River and the location of the head of tide sh ladder. The locations of the Canadian commercial salmon sea cages (shaded) are shown for Passamaquoddy Bay and the Bay of Fundy. From to 2, 43 sh entering the shway trap were screened for the presence of sea lice (chalimus to adult stages of Lepeophtheirus salmonis as described by Johnson & Albright 1991). Fish were anesthetized using Marinol (1 mg L 1 )from to, and clove oil ( mg L 1 ) from to 2. To ensure consistency in the screening standards, all 724 r 4 Blackwell Publishing Ltd, Aquaculture Research, 35, 723^729

3 personnel were trained at the start of the annual monitoring period. In most years, the same experienced individual performed counts. Prevalence was determined, and intensities were scored as: I, no lice; II, lice; III, 21^5 lice; IV 45 lice. In 1, all lice (chalimus to adult stages) on 69 sh were counted, and the body damage resulting from sea lice was systematically recorded. Damage noted in sea lice infested areas included: open wounds, loss of epidermal tissue, and bleeding and hemorrhaging. These wounds, and their locations on the sh, are characteristic of lice infections (Bjorn & Finstad ). The location of attachment of sea lice (preadults and adults) on 219 salmon was assessed in,, and. We did not include chalimus stages for this assessment. The attachment regions included anterior, middle and posterior zones on both the dorsal and ventral surface of the salmon. The anterior zone extended from the snout to the posterior side of the pectoral n. The posterior zone extended from the tail to the anterior side of the anal n. The middle zone encompassed the rest of the sh. While lice levels tend to be correlated with environmental variables such as water temperature, we did not attempt to associate lice burdens of wild and farmed sh with local temperatures for the following reasons: we did not know what temperature regimes the wild sh had encountered during their extended ocean migration and farmed salmon would have been subjected to lice control programs prior to their escapement. Statistical analysis Due to small sample sizes and non-normality of data, statistical comparisons were made with non-parametric tests (Mann^Whitney, Kruskal^Wallis). Di erences in sea lice intensities between the dorsal and ventral surface of the sh were compared using a w 2 test. Results A total of 957 wild salmon, 3119 farmed salmon, 116 landlocked salmon and 11 rainbow trout were screened for the presence of sea lice from to 2. Sea lice occurred on 21%, 17%, and 23%, respectively, of the wild, farmed and landlocked salmon caught ascending the sh ladder over the 11-year monitoring period. The prevalence of sea lice on wild salmon was signi cantly higher than on escaped farmed sh in (Po.5, see Fig. 2). Sea lice prevalence on wild and farmed salmon trended upward from to, before starting to decline (Fig. 2). Sea lice prevalence on landlocked salmon ranged from % to 67% during the study period (Fig.2). Sea lice were found on only1 of 11 rainbow trout screened during the 11-year period. Sea lice infections were signi cantly higher on 1SW than on 2SW wild salmon in (Po.1, see Fig. 3a). For farmed salmon, the prevalence of sea lice on 1SW sh was signi cantly greater than that of 2SW or post smolt during 6 years (Po.5, see Fig. 3b). The proportion of highly infected sh (categories III and IV) was signi cantly higher on wild salmon than farmed salmon in (Po.5). Lower sea lice intensities (category II, lice per sh) for farmed salmon were found in more than % of the samples during 9 years (Fig.4). Sea lice levels in wild salmon began decreasing in, reaching their lowest values in the time series in 2 (all sh had lice per sh, see Fig. 4). For landlocked salmon, sea lice intensities varied, with high intensities (levels III and IV) occurring in 3 of 6 years (Fig. 4). Average sea lice counts by infection level, were similar between wild and farmed salmon in the 1year in which we have complete counts from 69 sh (Table 1). For level II ( lice per sh), the average counts were and for wild and farmed salmon respectively (Table 1). For level III (21^5 lice per sh), average counts were (one sh) and for wild and farmed salmon respectively (Table 1). For level IV (45 lice per sh), average counts were 7 (one sh) and for % Sealice prevalence Wild Farmed Landlocked Figure 2 The sea lice (chalimus to adult stages of L. salmonis) prevalence levels (% of sh of all ages infected) in wild salmon, farmed salmon and landlocked salmon recorded at the head of tide sh ladder on the Magaguadavic River from to 2. No landlocked salmon were captured in. The indicates a signi cant di erence (Po.5) between wild and farmed salmon sea lice prevalence in a given year. 1 2 r 4 Blackwell Publishing Ltd, Aquaculture Research, 35, 723^

4 (a) % Sealice prevalence on wild salmon (b) % Sealice prevalence on farmed salmon wild and farmed salmon respectively (Table 1). None of the eight wild salmon screened had sea lice damage. However, for farmed salmon, lice damage was recorded on12% (sea lice level II), % (level III), and 57% (level IV) of the sh screened for total lice counts (Table 1). Damage included hemorrhaging, open sores and loss of epidermal layer of tissue on sea lice infested areas. Lice were more common on the dorsal than ventral surface of the salmon. Of the 219 sh examined, 59% had lice on both the dorsal and ventral surfaces, 37% had lice only on the dorsal surface and 4% had lice only on the ventral surface. The levels of sea lice were signi cantly greater on the dorsal than ventral surface (Po.1, see Fig. 5). The middle and posterior regions on the dorsal surface were the most infested (Fig. 5). No signi cant di erences (P.5, see Fig. 5) were found between infestations of adult and pre-adult lice in each of the regions on the dorsal and ventral surfaces of the sh. Discussion 1SW We found that lice were present on o25% of the wild and farmed salmon we screened at the Magaguadavic River sh ladder trap, and prevalence was in general higher for wild sh than for farmed escapees. 2SW Postsmolt 1SW 2SW Figure 3 The sea lice (chalimus to adult stages of L. salmonis) prevalence levels (% of sh infected) in: (a) wild one sea winter (1SW) and two sea winter (2SW) salmon, and (b) 1SW, 2SW and post smolt farmed salmon recorded at the head of tide sh ladder on the Magaguadavic River from to 2. The indicates a signi cant di erence (Po.5) in a given year between sh of di erent sea ages. 2 However, we recorded lice counts as high as 7 and per sh for wild and escaped farmed salmon, respectively, and these and some lower levels of infestation were associated with signi cant body damage to the farmed hosts. Lice burdens also tended to be higher on 1SW sh for both wild and farmed escapees. Wooten, Smith and Needham (1982) reported that Atlantic salmon might su er signi cant pathological damage from as few as ve adult lice per sh. Lice were found most frequentlyand in the greatest number on the dorsal surface of the sh. No di erence was found between the frequency of pre-adult and adult life stages among the body regions on the sh. Bjorn and Finstad () reported that pre-adult and adult life stages prefer the head and dorsal regions of sea trout and Arctic char, and caused severe skin damage. In infected Atlantic salmon and sea trout, mortalities increased exponentially when sea lice reached the pre-adult stage (Grimnes & Jakobsen ; Finstad, Bjorn, Grimnes & Huidsten ). There is little information available on the lice levels that wild salmon would normally bear in the open sea. Jacobsen and Gaard () have conducted the most complete study. They examined wild and escaped farmed salmon caught on long lines in the species European oceanic feeding grounds o the Faroe Islands. They found an overall prevalence of lice to be 99.2%, and an abundance of 25.9 lice per salmon, mostly adults, with a maximum infestation of 299 lice (L. salmonis and Caligus elongatus combined) on a farmed escapee. One sea winter escaped farmed salmon had more lice than wild salmon of the same age. However, there was no di erence in lice burdens between 2SW wild and farmed salmon. They postulated that the higher lice burdens of 1SW farmed sh could be due to their having picked up the lice in coastal waters prior to moving to the o shore feeding grounds, or to a higher susceptibility of the farmed sh to infection. Given the lice burdens we found, and their potential to cause far more signi cant damage than we observed (Table 1), it may suggest that the lice on sh that we screened were acquired relatively recently, perhaps back in coastal waters before entering the river. This is also consistent with the higher lice burdens we observed on the one sea winter sh compared with the two sea winter sh. One sea winter sh are believed to stay relatively close to their home rivers during their ocean migration (Ritter 1989). Exposure of sea lice to brackish and freshwater during the time it took to ascend into the shway trap may have also reduced lice levels on the sh (Finstad & 726 r 4 Blackwell Publishing Ltd, Aquaculture Research, 35, 723^729

5 Proportion of infected fish with various levels of lice Wild salmon 1 2 Farmed salmon 1 2 Landlocked salmon 1 2 > 5 Lice -5 Lice Lice > 5 Lice -5 Lice < Lice > 5 Lice -5 Lice < Lice Figure 4 Proportion of infected sh (wild, farmed and landlocked salmon) with speci ed levels of lice (chalimus to adult stages of L. salmonis) recorded at the head of tide sh ladder on the Magaguadavic River from to 2. Intensity levels were categorized as follows: lice per sh, 21^5 lice per sh, 45 lice per sh. Fish without sea lice were not included. Bjorn ). This may have resulted in an underestimation of prevalence, intensities, and abundance of sea lice on the sh we screened. However, sea lice can survive in fresh water for long periods. Studies with Arctic char demonstrated that % of the L. salmonis that they were infected with, survived in freshwater for 1 week, and some survived as many as 3 weeks (Finstad & Bjorn ). A second possibility is that the life stages of lice that the sh harboured were those that were the least damaging to the hosts. While a burden of 1 large adult lice could signi cantly hurt a sh, the impacts from 1 small chalimus would be limited, perhaps only to elevations in cortisol levels (Finstad et al. Dorsal Ventral > 5 Lice 21-5 Lice Lice > 5 Lice Ant. adult Ant. pre-adult Mid adult Mid pre-adult Post. adult Post. pre-adult Ant. adult Ant. pre-adult Mid adult Mid pre-adult Post. adult Post. pre-adult 21-5 Lice Lice Figure 5 Proportion of 219 sampled sh (wild and farmed salmon recorded at the head of tide sh ladder on the Magaguadavic River during, and) having sea lice (pre-adult and adult stages of L. salmonis) in speci ed regions on the dorsal and ventral surfaces. The regions included anterior, middle and posterior zones for both the dorsal and ventral surface of the salmon. Subdivisions within the histograms show the fractions of the sh with di ering lice levels ( lice per sh, 21^5 lice per sh, 45 lice per sh). Separate histograms are provided for adult and pre-adult lice. Table 1 Mean sea lice (chalimus to adult stages of L. salmonis) counts from a sample of wild and escaped farmed salmon recorded at the head of tide sh ladder on the Magaguadavic River during 1 Fish showing lice damage Intensity level Origin Total fish Lice Mean count SD %fishshowing damage Mean lice count SD II Wild Farmed III Wild 1 Farmed IV Wild 1 7 Farmed Counts were done for each sea lice level. Intensity levels are as follows: II, lice per sh; III, 21^5 lice per sh; IV, 45 lice per sh. The per cent of salmon that had external damage from sea lice is also presented. r 4 Blackwell Publishing Ltd, Aquaculture Research, 35, 723^

6 ). The relatively low levels of body damage we observed on infested sh, given the lice counts we recorded (Table 1), could be due in whole or in part to the sh being infested with younger lice life stages. We did not systematically distinguish between early (chalimus) and later (pre-adult and adult) life stages of lice in our counting scheme. Sea lice reached epidemic levels in the Bay of Fundy salmon farming industry in (Hogans ; MacKinnon ), although few lice were reported on the sh at the sh ladder during the same year. This may have been related to high sh mortalities in the bay associated with the sea lice epidemic at the farms. Lice burdens on both wild and farmed sh increased over the course of our study until, at which point a precipitous decline was noted. The declining trend observed since for both farmed and wild sh suggests that the pool of larvae available to infect the sh is declining. This timing corresponds with the introduction of Slice (Emamectin benzoate, Schering-Plough Aquaculture, Union, NJ, USA) as a new and apparently e ective treatment for lice on the farms.the lice declines mayalso be related to lower farmed salmon production in the general area as a measure to combat recent outbreaks of Infectious Salmon Anemia. There is no centralized, publicly available, data registry reporting on the lice burdens and the e ectiveness of treatments for lice on the sh farms in the area. It is thus di cult to evaluate the e cacy of the treatment regimes being adopted in the industry. While the results we have presented suggest that wild adults during their return migration to the Magaguadavic River are not being severely injured by lice, the landlocked salmon data is troubling. Our tracking work showed that these sh frequented coastal areas in the vicinity of the Magaguadavic River, and we tracked some of them (six of 14 sh) into the vicinity of active sh farms. Bjorn and Finstad (2) and Gargan () reported strong correlations between lice in wild sea trout, and the proximity of salmon farms. Gargan () reported lethal infestations of lice on wild sea trout post smolts only near salmon farms. Two landlocked salmon that we tracked returned to the river in less than two months, and both sh had signi cant body damage from lice infestations. The damage caused to those sh suggests that levels of infestation that they bore would pose a mortality risk to out-migrant salmon smolts, which could contribute to wild salmon population declines in the region. This emphasizes the need for aggressive programs in farms that keep lice levels under tight control at low levels. As farmed salmon output continues to increase, more frequent treatment and lower acceptable lice levels on sh before treatment may be needed to insure the conservation of wild salmon populations (i.e. Heuch & Mo 1). Although some studies have suggested that sh farming activities may be linked to sea lice infestations on wild sh (Gargan ; Bjorn & Finstad 2), sh farming is not the only source of lice infestations. Marshall (3) reported no correlations between lice abundance on wild sea trout and farmed sh, and lice epidemics in wild sh have been reported in the past before the advent of salmon farming (White 19). More information is needed to determine the source of sea lice infestation levels on wild Atlantic salmon, in the open ocean and in coastal areas. Acknowledgments We wish to thank all those who participated in the eld data collection. Thanks to the following agencies for nancing this project: New Brunswick Environmental Trust Fund ^ Your Environmental Trust Fund at Work, New Brunswick Wildlife Trust Fund, Canada/New Brunswick Cooperation Agreement on Recreational Fisheries and Development, and the Atlantic Fisheries Adjustment Program. References Berland B. () Salmon lice on wild salmon (Salmo salar L.) in western Norway. In: Pathogens ofwild and Farmed Fish: Sea Lice (ed. by G.A. Boxshall & D. Defaye), pp. 179^197. Ellis Horwood, London, UK. Bjorn P.A. & Finstad B. () The development of salmon lice (Lepeophtheirus salmonis) on arti cially infected post smolts of sea trout (Salmo trutta). CanadianJournal of Zoology 76,97^977. Bjrn P.A. & Finstad B. (2) Salmon lice, Lepeophtheirus salmonis (Kryer), infestation in sympatric populations of Arctic char, Salvelinus alpinus (L.), and sea trout, Salmo trutta (L.), in areas near and distant from salmon farms. ICES Journal of Marine Science 59,131^139. Boxshall G.A. (1974) Infections with parasitic copepods in North Sea marine shes. Journal of the Marine Biological Association UK 54,355^372. Carr J.W. () Interactions between wild and aquaculture Atlantic salmon in the Magaguadavic River, New Brunswick. MSc thesis, University of New Brunswick, Fredericton, Canada,77pp. 728 r 4 Blackwell Publishing Ltd, Aquaculture Research, 35, 723^729

7 Carr J.W., Anderson J.M.,Whoriskey F.G. & DilworthT. () The occurrence and spawning of cultured Atlantic salmon (Salmo salar) in a Canadian river. ICES Journal of Marine Science 54,164^173. DFO (3) Atlantic salmon maritime provinces overview for 2. Fisheries and Oceans Canada. Science Division, Gulf and Maritimes Regions Stock Status Report 3/ 26, 46pp. Federal Government, Halifax, NS, Canada. Finstad B. & Bjorn P.A. () Survival of salmon lice, Lepeophtheirus salmonis Kryer, on Arctic charr, Salvelinus alpinus (L.), in fresh water. Aquaculture Research 26, 791^795. Finstad B., Bjorn P.A., Grimnes A. & Huidsten N.A. () Laboratory and eld investigations of salmon lice (Lepeophtheirus salmonis) infestation on Atlantic salmon (Salmo salar L.) postsmolts. Aquaculture Research 31, 795^3. Gargan P. () The impact of the salmon louse (Lepeophtheirus salmonis) on wild salmonid stocks in Europe and recommendations for e ective management of sea lice on salmon farms. In: Proceedings of the Speaking for the Salmon Workshop: Aquaculture and the Protection of Wild Salmon (ed. by P. Gallaugher & C. Orr), pp. 37^45. Simon Fraser University, Burnaby, BC, Canada. Grimnes A. & Jakobsen P.J. () The physiological e ects of salmon lice infection on post-smolt of Atlantic salmon. Journal of Fish Biology 48,1179^1194. Heuch P.A. & Mo T.A. (1) A model of salmon louse production in Norway: e ects of increasing salmon production and public management issues. Diseases of Aquatic Organisms 45,145^152. Hogans W.E. () Infection of sea lice, Lepeophtheirus salmonis (Copepoda: Caligidae) parasitic on Atlantic salmon (Salmo salar) cultured in marine waters of the Lower Bay of Fundy. CanadianTechnical Report of Fisheries and Aquatic Sciences 67,1pp. Jacobsen J.A. & Gaard E. () Open-ocean infestation by salmon lice (Lepeophtheirus salmonis): comparison of wild and escaped farmed Atlantic salmon (Salmo salar L.). ICES Journal of Marine Science 54, 1113^1119. Johnson S.C. & Albright L.J. (1991) The developmental stages of Lepeophtheirus salmonis (Kryer, 1837) (Copepoda: Caligidae). CanadianJournal of Zoology 69, 929^95. Johnson S.C., Blaylock R.B., Rlphick J. & Hyatt K.D. () Disease induced by the salmon louse (Lepeophtheirus salmonis) (Copepoda: Caligidae) in wild sockeye salmon (Oncorhynchus nerka) stocks of Alberni Inlet, British Columbia. Canadian Journal of Fish and Aquatic Sciences 53, 2888^2897. MacKinnon B.M. () Sea lice: a review.world Aquaculture 28,5^1. Marshall S. (3) The incidence of sea lice infestations on wild sea trout compared to farmed salmon. Bulletin European Association of Fish Pathologists 23,72^79. Ritter J.A. (1989) Marine migration and natural mortality of North American Atlantic salmon (Salmo salar L.). Canadian Manuscript Report of Fisheries and Aquatic Sciences 41,136pp. White H.C. (19) Sea Lice (Lepeophtheirus) and death of salmon. Journal of the Fisheries Research Board of Canada 5,172^175. Wootten R., Smith J.W. & Needham E.A. (1982) Aspects of the biology of the parasitic copepods Lepeophtheirus salmonis and Caligus elongatus on farmed salmonids, and their treatment. Proceeding of the Royal Society of Edinburgh 81B, 185^197. r 4 Blackwell Publishing Ltd, Aquaculture Research, 35, 723^