Occurrence of canthaxanthin in Atlantic salmon, Salmo salar L., fry in Irish rivers as an indicator of escaped farmed salmon

The rapid growth of Atlantic salmon, Salmo salar L., culture in north-western Europe has given rise to concerns regarding the biological consequences of fish farm escapes on wild salmonid populations. Canthaxanthin, a carotenoid pigment additive to farmed salmon feed which is passed from females to their progeny, may be used as an indicator of the numbers of escaped farmed salmon which spawn in the wild. In the present study, thin-layer chromatography and high-performance liquid chromatography (HPLC) were used to screen emergent Atlantic salmon fry sampled from seven river catchments in Ireland for canthaxanthin. The incidence of fry containing canthaxanthin at greater than trace levels (<5% of total carotenoid pigment) was 0–4%, with an average of 1.7%, among the seven rivers sampled, indicating that the progeny of farmed salmon were present at similarly low frequencies. Canthaxanthin was detected at trace levels in an unexpectedly high proportion (35%) of salmon fry. Canthaxanthin was present at levels exceeding trace amounts in 24% of 21 non-anadromous brown trout, Salmo trutta L., sampled from six Irish rivers and present at trace levels in a further 57% of the fish, indicating that dietary canthaxanthin is freely available to salmonids in Irish rivers. The widespread presence of trace levels in salmon fry may be attributable, at least in part, to the increased sensitivity of the HPLC methods and to rapid dietary uptake during early post-emergence feeding.     

Spawning of farmed Atlantic salmon, Salmo salar L., in the second year after their escape

Abstract. The frequency of escaped farmed salmon in the River Polla, Scotland was estimated at spawning in 1990, the second year after the escape of 184000 fish from a sea-cage site nearby. Fourteen of 73 spawners examined were of farmed origin. In only six of these fish were scale growth patterns consistent with their being part of the documented escape. All of these fish carried the pigment canthaxanthin. Fifty-nine redds were constructed at spawning. Five of 54 redds sampled contained embryos or alevins bearing canthaxanthin. The frequency of fry bearing canthaxanthin was determined in samples obtained from the neighbouring Rivers Hope and Dionard following spawning in both 1989 and 1990. There was no evidence of substantial returns of salmon from the documented escape to these rivers. These findings and those of a previous study suggest that more than 95% of those fish which returned to rivers near the site of the documented loss did so in the first year after escape and that fewer than 0·5% of those fish which escaped returned within the 2 years of study.     

ON THE WILLINGNESS-TO-PAY FOR RECREATIONAL FISHING—ESCAPED FARMED VERSUS WILD ATLANTIC SALMON

This article explores to what extent escaped farmed salmon from fish farms affect the willingness-to-pay for recreational fishing of Atlantic salmon in Norwegian rivers. This is a first attempt to explore the economic consequences of escaped farmed species in terms of the anglers’ willingness-to-pay for fishing permits working through the relationship between the price of fishing permits and the share of escaped farmed salmon. The empirical analysis is based on the results from a contingent valuation survey conducted in Norway. It is found that the presence of escaped farmed salmon in Norwegian rivers may have severe economic consequences on the willingness-to-pay for recreational fishing with a reduction of up to 85% compared to a situation with a ‘pure’ wild salmon stock.     

Incidence and timing of wild and escaped farmed Atlantic salmon (Salmo salar) in Norwegian rivers inferred from video surveillance monitoring

Run timing of escaped farmed Atlantic salmon Salmo salar vs. wild fish was compared by the use of video camera surveillance in 15 rivers over several years, covering 1600 km of the Norwegian coastline (from 58°N to 69°N). Annual runs of wild salmon varied among rivers from <200 fish to more than 10 000. During the surveillance period that for most rivers extended from late May to early October, larger‐sized salmon (fish ≥ 65 cm) generally entered the rivers earlier than small fish. The percentage of salmon identified as escaped farmed fish ranged from 0.1% to 17% across rivers with an average of 4.3%. Estimates of escapees are, however, assumed to represent minimum values because an unknown number of farmed fish passing the video cameras may have been misclassified as wild fish. By the use of a linear mixed model and generalised additive mixed models, it was found that the relationship between run timing and fish length differed significantly between farmed and wild salmon. While small‐sized farmed and wild fish (<65 cm) entered the river at about the same time, wild large salmon returned on average 1–2 weeks earlier than similarly sized escapees. The proportion of large‐sized farmed escapees also increased until late August and decreased thereafter. In contrast, there was a relatively constant and lower proportion of small‐sized escapees throughout the season. Within the surveillance period, there was no evidence of any exceptionally late runs of fish classified as escaped farmed salmon.     

Content of synthetic astaxanthin in escaped farmed Atlantic salmon, Salmo salar L., ascending Norwegian rivers

Abstract  Isomeric ratios of astaxanthin in eggs and alevins of Atlantic salmon, Salmo salar L., have proven useful in identifying female spawners of farmed origin, but the method underestimates the proportion of fish of farmed origin. The rate of underestimation was studied by analysing astaxanthin content in tissue of 55 farmed Atlantic salmon ascending two Norwegian rivers in the autumn of 1991. The astaxanthin content fell into two distinct classes. Fifty-one per cent of the adult escaped salmon had isomeric ratios similar to salmon fed synthetic astaxanthin, whereas all the remaining fish had ratios similar to wild fish. Discriminant analysis classified 96.4% of the fish with known astaxanthin content into the correct astaxanthin class on basis of tail-fin erosion, length, weight and gill-cover damage. This discriminant function was used to estimate the astaxanthin classification of 1017 farmed salmon caught in nine rivers during 1989–1991. The classification success varied among years from 52 to 64%. Corresponding numbers for females and males were 45–48% and 54–70%, respectively. Thus, estimates of spawning rates of farmed female salmon via astaxanthin content in eggs or alevins from redds should be adjusted accordingly. The observed isomeric ratios of astaxanthin in the escaped farmed salmon and the relationship with morphology indicates that a significant proportion of the escapees ascending rivers have spent more than 1 year in the wild after escape.     

Reared Atlantic salmon, Salmo salar L., in the catches of a salmon fishery on the western coast of Scotland

Abstract. Atlantic salmon, Salmo salar L., of reared origin were distinguished from putative wild fish In the catch of a single salmon fishery in western Scotland. Fish in seven day-catches made in 1990 totalling 403 individuals were assessed formally for the presence of residual fin damage resulting from culture. Fifty-eight (22%) were classed as being of reared origin, on the basis of previously established criteria. Additional examination of 54 of these fish showed the pigment canthaxanthin to be detectable in the tissues of 35 (65%), which were therefore classed as having escaped from sea cages. Among the fish in which canthaxanthin could not be detected, a further 17 individuals (31% of the total) were classed as having escaped from sea cages on the basis of scale growth patterns. Scale growth patterns in the remaining two fish (4% of the total) were consistent with their having grown in a hatchery before escape or release.     

Migratory behaviour of adult wild and escaped farmed Atlantic salmon, Salmo salar L., before, during and after spawning in a Norwegian river

The migratory behaviour of adult wild and escaped farmed Atlantic salmon, Salmo salar L., before, during after spawning in the River Namsen, Norway, was analysed using radio telemetry. The fish were caught, radio tagged and released into the fjord between 7 and 25 km from the river mouth. A significantly higher proportion of wild (74%) than farmed (43%) salmon was subsequently recorded in the river. Wild salmon (33%) were more frequently captured in the sea and in rivers than farmed salmon (14%). The migration speed from release to passing a data logger 11 km upstream from the river mouth was not significantly different between wild (20.6 km day^?1) and farmed (19.8 km day^?1) salmon. Wild salmon tagged when water flow in the river was increasing had a significantly higher migration speed than wild salmon tagged when water flow was decreasing. This was not true for farmed salmon. Farmed salmon were distributed significantly higher up the river than wild salmon during spawning, although both types of fish were found together in spawning areas. Thus, there was no geographical isolation to prevent spawning between wild and escaped farmed salmon. Farmed salmon had significantly more and longer up- and downstream movements than wild salmon during the spawning period. Unlike farmed salmon, the number of riverine movements by wild salmon increased significantly when variation in water flow increased. A smaller proportion of wild (9%) than farmed (77%) salmon survived through the winter after spawning.     

The effect of feed pigment type on flesh pigment deposition and colour in farmed Atlantic salmon, Salmo salar L.

The characteristic pink colour of salmonid flesh is a result of deposition of naturally occurring carotenoid pigments. Achieving successful pigmentation in farmed salmonids is a vital aspect of fish farming and commercial feed production. Currently commercial diets for farmed salmonids contain either or both of the synthetic pigments commercially available, astaxanthin and canthaxanthin. Atlantic salmon, Salmo salar L. ( = 220 g initial weight) were given feeds where the pigment source was astaxanthin only, canthaxanthin only or a astaxanthin/canthaxanthin mix. The rearing environment was 12 × 3 m tanks supplied with sea water at the EWOS research farm Lønningdal, near Bergen, Norway. As the proportion of dietary canthaxanthin increased, flesh pigment levels also showed an increase; the pigment content in the muscle of canthaxanthin‐only fed fish was 0.4 mg kg^?1 (or 14%) higher than that of the astaxanthin‐only fed fish, with the mixed pigment fed fish being intermediate between the two extremes. Results of cross‐section assessment for Minolta colorimeter redness (a*) values and Roche Salmofan^TM scores also showed an increase in colour with increasing proportions of canthaxanthin in the feed. The data reported clearly indicates that S. salar ( = 810 g final weight) of this size deposit canthaxanthin more efficiently than they do astaxanthin. These results contrast with those obtained by other authors with rainbow trout, Oncorynchus mykiss (Walbaum), and imply that the absorption or utilization of the pigments differs between species.     

High numbers of farmed Atlantic salmon. Salmo salar L., observed in oceanic waters north of the Faroe Islands

Abstract. To estimate the proportion of escaped fanned Atlantic salmon. Salmo salar L., at the feeding grounds in the north-east Atlantic Ocean, samples of salmon caught with long-lines north of the Faroe Islands were examined. Identification of reared fish was carried out using scale analysis. The proportion of fanned fish was estimated to range from 25 to 48% in the different samples, suggesting that high numbers of escaped farmed salmon occur in the Norwegian Sea. The farmed fish were significantly smaller in size than the wild salmon. Although it is suggested that most of the farmed fish are of Norwegian origin, farmed fish of Scottish, Faroese and Irish origin are also believed to be present. If not accounted for, high numbers of reared salmon in fisheries and stocks will seriously affect the assessments of fisheries and stocks of wild salmon.     

Potential disease interaction reinforced: double-virus-infected escaped farmed Atlantic salmon,Salmo salar L., recaptured in a nearby river

The role of escaped farmed salmon in spreading infectious agents from aquaculture to wild salmonid populations is largely unknown. This is a case study of potential disease interaction between escaped farmed and wild fish populations. In summer 2012, significant numbers of farmed Atlantic salmon were captured in the Hardangerfjord and in a local river. Genetic analyses of 59 of the escaped salmon and samples collected from six local salmon farms pointed out the most likely source farm, but two other farms had an overlapping genetic profile. The escapees were also analysed for three viruses that are prevalent in fish farming in Norway. Almost all the escaped salmon were infected with salmon alphavirus (SAV) and piscine reovirus (PRV). To use the infection profile to assist genetic methods in identifying the likely farm of origin, samples from the farms were also tested for these viruses. However, in the current case, all the three farms had an infection profile that was similar to that of the escapees. We have shown that double-virus-infected escaped salmon ascend a river close to the likely source farms, reinforcing the potential for spread of viruses to wild salmonids.     

Incidence of hybridization between Atlantic salmon, Salmo salar L., and brown trout, Salmo trutta L., in Ireland

The substantial growth of the farmed salmon industry in Europe since the 1970s has highlighted concerns regarding the genetic impact of escaped farmed salmon on wild salmonid stocks. High incidences of salmon × trout hybrids have been recorded in rivers situated near intensive salmon farming in Norway and Scotland, which may be indicative of a breakdown in reproductive isolation between salmon, Salmo salar L., and brown trout, Salmo trutta L. In the present study, salmonid fry and 0+ parr were collected from rivers in western Ireland. Allozyme and minisatellite DNA analysis were carried out on fry to determine the frequency of F1 hybrids from 10 rivers located within 38 km of salmon farms and three rivers at least 80 km from salmon farms. A total of 49 hybrids were recorded from 4135 salmonid fry (frequency = 1.2%). Mitochondrial DNA analysis showed that all hybrids arose from Atlantic salmon female × brown trout male crosses. Hybrid parr were recorded from one of the low-risk rivers (1.0%), but were present in seven out of the 10 catchments located within 38 km of salmon farms, with frequencies ranging from 0.7% to 3.1%. The results of the present survey, which represents the first extensive record of the levels of salmon-trout hybridization in Ireland, are discussed in relation to the continued growth of salmon farming in this country.     

Piscine reovirus (PRV) in wild Atlantic salmon,Salmo salar L., and sea‐trout,Salmo trutta L., in Norway

This is the first comprehensive study on the occurrence and distribution of piscine reovirus (PRV) in Atlantic salmon, Salmo salar L., caught in Norwegian rivers. PRV is a newly discovered reovirus associated with heart and skeletal muscle inflammation (HSMI), a serious and commercially important disease affecting farmed Atlantic salmon in Norway. A cross‐sectional survey based on real‐time RT‐PCR screening of head kidney samples from wild, cultivated and escaped farmed Atlantic salmon caught from 2007 to 2009 in Norwegian rivers has been conducted. In addition, anadromous trout (sea‐trout), Salmo trutta L., caught from 2007 to 2010, and anadromous Arctic char, Salvelinus alpinus (L.), caught from 2007 to 2009, were tested. PRV was detected in Atlantic salmon from all counties included in the study and in 31 of 36 examined rivers. PRV was also detected in sea‐trout but not in anadromous Arctic char. In this study, the mean proportion of PRV positives was 13.4% in wild Atlantic salmon, 24.0% in salmon released for stock enhancement purposes and 55.2% in escaped farmed salmon. Histopathological examination of hearts from 21 PRV‐positive wild and one cultivated salmon (Ct values ranging from 17.0 to 39.8) revealed no HSMI‐related lesions. Thus, it seems that PRV is widespread in Atlantic salmon returning to Norwegian rivers, and that the virus can be present in high titres without causing lesions traditionally associated with HSMI.     

The prevalence of escaped farmed salmon, Salmo salar L., in the River Ewe, western Scotland, with notes on their ages, weights and spawning distribution

Abstract  The prevalence of escaped farmed Atlantic salmon, Salmo salar L., in the River Ewe, western Scotland, was assessed. After the establishment of smolt cages in the catchment and marine cages near the river mouth during 1986–1987, approximately 425 000 parr and smolts, and 122 000 growers have escaped. Between 1987 and 2001, farmed salmon occurred in the rod fishery in 13 of the 15 years, contributing at least 5.8% of the total catch, with a maximum annual frequency of 27.1%. It was estimated that <1% of fish escaping from the marine cages entered the river, but contributed at least 27% of potential anadromous spawners in 1997. Radiotagged, farmed fish in 2001 probably spawned in three subcatchments also used by tagged wild fish. Despite the likelihood of hybridisation there was no change in the median weight or marine age of wild fish, but smolt age decreased significantly ( P  < 0.02). The Ewe has a depleted wild salmon population (≤900 anadromous adults), and further genetic introgression by escapees should be prevented.     

An ecological–economic model on the effects of interactions between escaped farmed and wild salmon (Salmo salar)

This study explores the ecological and economic impacts of interactions between escaped farmed and wild Atlantic salmon (Salmo salar, Salmonidae) over generations. An age‐ and stage‐structured bioeconomic model is developed. The biological part of the model includes age‐specific life‐history traits such as survival rates, fecundity and spawning successes for wild and escaped farmed salmon, as well as their hybrids, while the economic part takes account of use and non‐use values of fish stock. The model is simulated under three scenarios using data from the Atlantic salmon fishery and salmon farming in Norway. The social welfare is derived from harvest and wild salmon while the economic benefits of fishing comprise both sea and river fisheries. The results reveal that the wild salmon stock is gradually replaced by salmon with farmed origin, while the total social welfare and economic benefit decline, although not at the same rate as the wild salmon stock.     

An investigation into the prevalence of Renibacterium salmoninarum in farmed rainbow trout, Oncorhynchus mykiss (Walbaum), and wild fish populations in selected river catchments in England and Wales between 1998 and 2000

A cross-sectional survey of Renibacterium salmoninarum infection in farmed rainbow trout (RBT) and wild fish populations was carried out in 10 farms and six river catchments, respectively, in England and Wales. The majority of the wild fish were sampled in 1998 and the farmed fish in 2000. Grayling, Thymallus thymallus, and brown trout, Salmo trutta, were the main wild species sampled. Two fish, one grayling and one salmon, Salmo salar, were R. salmoninarum culture-positive, compared with 40 confirmed polymerase chain reaction-positive wild fish. The highest prevalence of R. salmoninarum infection was found in grayling in rivers with RBT farms with a history of R. salmoninarum infection. One hundred and fifty fish were sampled from each RBT farm, but none of the fish was found to be R. salmoninarum-positive. Evidence was found, for the first time, for the presence of R. salmoninarum in an eel, Anguilla anguilla.     

Incidence of escaped farmed salmon, Salmo salar L., in commercial salmon catches and fresh water in Northern Ireland

External morphological characteristics were used to identify escaped farmed Atlantic salmon, Salmo salar L., in a coastal salmon fishery in County Antrim, Northern Ireland during four fishing seasons and at an adjacent freshwater location (R. Bush) during a 5-year period. Out of a total of 36 326 adult salmon examined in the fishery, 883 (2.4%) were identified as having escaped from sea cages. Annual average values ranged from 0.26% to 4.04% of the fish caught. Occurrence of escapees entering an adult trap in fresh water averaged 0.88%, with a range of 0.13–2.62%, depending on year. No correlation between presence in the marine fishery and in fresh water was evident, the latter year-round figures probably being more indicative of presence of escapees in spawning stocks. Entry to fresh water was significantly later on average for escaped farmed salmon, compared with wild salmon.     

Movements and spatiotemporal distribution of escaped farmed and local wild Atlantic cod (Gadus morhua L.)

Commercial farming of Atlantic cod (Gadus morhua L.) is now being developed in several countries. The ecological consequences of cod culture are poorly understood, but recent research suggests that Atlantic cod are more prone to escape from net pens than Atlantic salmon. Here, we describe the movements and the spatiotemporal distribution of farmed cod after escape relative to wild cod, both during and outside the natural spawning season. The experimental design included simulating escape incidents of farmed cod tagged with acoustic transmitters and using an array of automatic listening stations to monitor their dispersal and distribution. For comparison, local wild cod were monitored using the same array of receivers. The farmed cod dispersed rapidly after a simulated escape, they randomly distributed over large areas and their distribution overlapped with local wild cod. Moreover, escaped farmed fish were found at local cod spawning areas during the spawning season. The study also indicated that the recapture rate of escaped farmed cod was high compared with that of escaped farmed salmon. Thus, while our results showed that there is a considerable potential for ecosystem effects caused by escaped farmed cod, mitigating actions such as an efficient recapture fishery for escapees may be possible.     

FISHY FISH? THE ECONOMIC IMPACTS OF ESCAPED FARMED FISH

The escape of cultured fish from a marine aquaculture facility is a type of biological invasion that may lead to a variety of potential ecological and economic effects on native fish. This article develops a general invasive species impact model to capture explicitly both the ecological and economic effects of invasive species, especially escaped farmed fish, on native populations and harvests. First, the possible effects of escaped farmed fish on the growth and stock size of a native fish are examined. Next, a bioeconomic model to analyze changes in yield, benefit distribution, and overall profitability is constructed. Different harvesting scenarios, such as commercial, recreational, and joint commercial and recreational fishing are explored. The model is illustrated by a case study of the interaction between native and farmed Atlantic salmon in Norway. The results suggest that both the harvest and profitability of a native fish stock may decline after an invasion, but the total profits from the harvest of both native and farmed stocks may increase or decrease, depending on the strength of the ecological and economic parameters.     

Mercury comparisons between farmed and wild Atlantic salmon (Salmo salar L.) and Atlantic cod (Gadus morhua L.)

Wild and farmed Atlantic salmon ( Salmo salar L.) and Atlantic cod ( Gadus morhua L.) were collected to assess changes in mercury with size in wild vs. farmed fish. Mercury concentrations were compared with Health Canada and United States Environmental Protection Agency consumption guidelines. Lipid dilution of mercury was examined by comparing lipid-extracted (LE) and non-lipid-extracted (NLE) flesh samples in both farmed and wild fish. Mercury concentrations in the flesh and liver of farmed salmon were significantly lower than concentrations in wild salmon of similar fork length ( P <0.001), possibly due to growth dilution in rapidly growing farmed fish. Mercury concentrations were higher in LE tissue compared with NLE ( P <0.05), suggesting lipid dilution of mercury in farmed fish with a high lipid content. Farmed cod, which do not grow more rapidly than wild cod, did not have significantly different flesh and liver concentrations compared with wild cod of similar fork length ( P >0.05). Between species of farmed fish, cod had significantly higher mercury concentrations than salmon ( P <0.05), but neither farmed nor wild salmon mercury concentrations exceeded federal consumption guidelines. These results suggest that rapid growth rates and a high lipid content may play important roles in regulating concentrations of contaminants such as mercury.     

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

A monitoring program for the prevalence and intensity of sea lice infestations of wild and escaped farmed salmon has been underway on the Magaguadavic River since 1992. Fish are screened in a fish 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 2002, 23 landlocked salmon moving to sea from the Magaguadavic River were acoustically tagged. Two fish returned to the river after a brief period of residence in Passamaquoddy Bay, with significant dermal damage from sea lice. These fish were tracked to areas close to commercial salmon farms.