© 2006 International Council for the Exploration of the Sea
Monitoring the incidence of escaped farmed Atlantic salmon, Salmo salar L., in rivers and fisheries of the United Kingdom and Ireland: current progress and recommendations for future programmes
a Centre for Fisheries and Aquaculture Science Pakefield Road, Lowestoft, Suffolk NR33 0HT, England, UK
b FRS Freshwater Laboratory Faskally, Pitlochry, Perthshire PH16 5LB, Scotland, UK
c Department of Agriculture and Rural Development (DARD), Agriculture and Food Science Centre Newforge Lane, Belfast BT9 5PX, Northern Ireland, UK
d Marine Institute Abbotstown Laboratory Complex, Snugboro Road, Abbotstown, Dublin 15, Ireland
e National Fisheries Technical Team, Environment Agency, Institute of Environmental Science, University of Bangor Robinson Building, Deiniol Road, Bangor, Gwynedd LL57 2UW, Wales, UK
*Correspondence to A. M. Walker: tel: +44 1502 524351; fax: +44 1502 526351. e-mail: alan.walker{at}cefas.co.uk.
An inevitable consequence of the development of the Atlantic salmon, Salmo salar L., farming industry in coastal waters of the British Isles has been the loss of farmed salmon to the wild, their occurrence in inshore waters and rivers, and their appearance in coastal and freshwater fisheries. Monitoring programmes have been developed throughout the British Isles, variously using scientific sampling, catch records from coastal or freshwater fisheries or both, and scientific sampling of catches from in-river traps. We compare the results of these monitoring programmes with regional production and the numbers of escapees reported from marine fish farms. We also consider the effectiveness of the programmes for assessing the prevalence of farmed salmon that escape from marine cages. Finally, we make recommendations for improvements to these programmes and for the development of best practice, including the scientific sampling of in-river spawning stocks through fishery-independent sources, identification of fish origin based on at least two methods, assessment of the degree of incorrect classification, and the timely and accurate reporting of all escapes.
Keywords: aquaculture, Atlantic salmon, escapee, monitoring programmes, stock assessment, wild stocks
Received 28 October 2005; accepted 15 April 2006.
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Introduction |
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Atlantic salmon, Salmo salar L., aquaculture in the coastal waters of the British Isles began in Scotland in the late 1960s and extended to Ireland in the 1980s. Production increased exponentially from the 1980s onward, reaching a total of approximately 170 000 t in 2004 (ICES, 2005; Figure 1). Currently, there are approximately 50 times as many farmed salmon harvested from coastal waters as wild salmon returning to UK and Irish rivers each year (ICES, 2005).
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Typically, farmed salmon are lost to the surrounding environment through damage to the nets, during routine handling, e.g. grading, treatments, and the transfer of fish to or between cages and at harvesting, or as the result of vandalism (Beveridge, 2004). Escapee adult salmon may spawn with other escapees and wild salmon (Lura and Saegrov, 1991; Webb et al., 1991, 1993a, b; Fleming et al., 1996; Crozier, 1998; Butler et al., 2005). Evidence clearly demonstrates the risks posed to wild stocks by escaped farmed fish (see Naylor et al., 2005 and references therein) and, therefore, the importance of assessing the prevalence of escaped farmed salmon in in-river spawning stocks of the British Isles. Escaped farmed salmon may inflate catch-based spawning stock estimates to such an extent that the stock appears either to be healthy or recovering, the consequences of which are that conservation measures are either relaxed or not strengthened, or new measures not being introduced.
The incidence of escapees in salmon catches in the British Isles has been reported previously: for various coastal and freshwater fisheries in Scotland between 1981 and 1996 (Youngson et al., 1997); for coastal fisheries and an in-river trap in the River Bush in Northern Ireland between 1991 and 1995 (Crozier, 1998); and for English and Welsh freshwater fisheries in 2001 (Milner and Evans, 2003). In this paper, "coastal fishery" refers to fixed (e.g. bag nets or trapnets) and mobile nets (drift, excluding Scotland, and estuary seine nets), whereas "freshwater fishery" refers to rod-and-line fisheries and fish sampled in traps for scientific or management purposes.
In this paper, we extend these time-series to 2004 and summarize new data on the prevalence of escapees from catches reported by Scottish coastal and freshwater fisheries (1994–2004), from the coastal fisheries of the Republic of Ireland (1991–2004), and from coastal fisheries and in-river traps in England and Wales (2003–2004). We consider how effective the various monitoring programmes are for assessing the prevalence of farmed salmon that escape after transfer to marine cages, and how these programmes could be improved through an examination of, first, how escapes are reported from marine fish farms and second, how escapees are monitored in coastal waters and rivers. We also examine current data sets with regard to the regional prevalence of escapees and suggest priority areas for future programmes.
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Reporting of escapes by fish farms |
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Marine salmon farms are sited along the west coast of mainland Scotland, around the Western, Orkney, and Shetland Isles, and along the west and north coasts of Ireland (Figure 1), while wild salmon are present in rivers throughout these countries, apart from the Orkney and Shetland Isles. Wild salmon inhabit rivers in the northeast, south, and west of England, and throughout Wales.
Fish farm operators in the Republic of Ireland have been required by law to report losses of salmon from their sites since 1996. Information is provided to the Department of Communications, Marine and Natural Resources (DCMNR) about the site location; the number, age, time at sea, and average weight of escaped fish; the reason for the escape; and measures taken to reduce the impact of the escape (Anon., 2004a). Official statistics indicate that approximately 415 000 salmon were reported to have escaped from salmon farms in coastal waters of the Republic of Ireland in the period 1996–2004 (Table 1) with an annual range of 0–160 000. Typically, the numbers of fish lost in an escape event will be an estimate because farms rarely know exactly how many fish were in a sea cage before the event.
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Scottish salmon farmers have been required to report escapes to the Scottish Executive Environment and Rural Affairs Department (SEERAD) since 2002, providing similar information to farmers in the Republic of Ireland (Anon., 2002a). As with the Irish reports, however, the number of salmon declared may be an estimate.
Before the introduction of mandatory reporting by Scottish farms, the increased Fisheries Inspectorate monitoring, in response to the outbreak of Infectious Salmon Anaemia (ISA) among Scottish marine farms in the late 1990s, facilitated improved voluntary reporting of losses. Consequently, SEERAD data are considered to have provided a reasonably accurate indication of losses from Scottish farms since 1998 (D. Pendrey, pers. comm.), with the total loss from 1998 to 2004 estimated at almost 1.4 million salmon (Table 1) and an annual range of between 67 000 and 430 000 in this case. Some escape incidents were also voluntarily reported by fish farm operators to some local District Salmon Fishery Boards, e.g. from Loch Ewe in 1993 and 1997 (Butler, 2000; Butler et al., 2005; Table 1). Scottish national data are published annually (Anon., 2001a, 2002b, 2003a, 2005a, b), but have been disaggregated and are presented here (Table 1) by adult salmon Production Areas (Anon., 2001a; Figure 1).
In Northern Ireland, it has always been a condition of the operating licence that marine salmon farms report escape incidents to the Fisheries Division of the Department of Agriculture and Rural Development (DARD). However, these data may be commercially sensitive and, therefore, are not available to the public. There are no salmon farms operating in the coastal waters of England and Wales.
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Monitoring of escapees in coastal waters and rivers |
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Table 2 lists the escapee monitoring programmes coordinated by government agencies and others throughout the British Isles and provides summary details of the regions sampled, methods of capture and identification of fish origin, those responsible for scanning catches, whether scanning is of whole catch or subsamples, and sources of published data.
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In Scotland, Fisheries Research Services (FRS) personnel have sampled catches from coastal and freshwater fisheries for the presence of escapees since 1981 (Youngson et al., 1997). Daily catches are sampled periodically throughout the fishing season, from late spring to the beginning of the close seasons, the end of August for the netting operations, and typically the end of October for freshwater fisheries. In addition, since 1994, fishery proprietors throughout Scotland have been required to report their catches of escapee salmon through statutory catch returns to FRS.
Catches from coastal fisheries in the Republic of Ireland have been examined routinely since 1991 as part of microtag recovery programmes. Catch sampling focuses principally on the fisheries off Donegal, Mayo, Galway, and Limerick, and the Southwest region (Cork and Kerry), but also some fisheries from the South and East region (Figure 1). These fisheries operate between March and August, with extensions into September in some years. In Northern Ireland, catches have been sampled from the coastal fishery off County Antrim (Figure 1), which extends for approximately 70 km along the north and northeast coasts and operates between March and September. Crozier (1998) provides further details of the study area, fishery, and sampling regime. There is no systematic reporting of escapees in riverine catches throughout Ireland, but data are presented here from the daily sampling of fish caught in an adult trap on the River Bush (Northern Ireland: as described in Crozier and Kennedy, 1991).
There is no formal requirement for fisheries to report escapees in England and Wales. A Cefas/Environment Agency study in 2003 targeted coastal fishing operations with large annual catches (Northeast coast and Severn Estuary) and fish caught in Environment Agency (EA) traps on four monitored rivers (Lune, Dee, Tamar, and Tyne). Coastal catches are examined by netsmen or fish merchants and trap-caught salmon by EA scientists. This programme was extended to include additional coastal fisheries (Northwest) and all other EA traps in 2004 (Figure 1).
Putative escapees are identified in all monitoring and reporting programmes according to abnormalities of the snout, opercula and fins (Lund et al., 1989). Typically, origin is authenticated by scale reading for all FRS samples (wild and escapees) and, for England and Wales, of suspect escapees plus five wild salmon sampled from the same catch, following the approach of Lund and Hansen (1991). Irish samples are not subject to secondary examination of fish origin.
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Prevalence of escapees in spawning stocks |
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The results of the various monitoring programmes are summarized in Tables 3 and 4, which provide the average, maximum, and minimum incidences of escapee salmon in coastal and freshwater fisheries, across years, summarized by region. Scottish data are analysed and presented for SEERAD adult salmon Production Areas (Anon., 2001a). However, as much of the Southwest Production Area has no marine farms, fisheries statistics for this area have been disaggregated to allow analyses appropriate to those subareas with (Strathclyde) and without (Solway, East) farms. There is only one marine farm site in Northern Ireland, so the data are presented for Northern Ireland as a whole. For the Republic of Ireland, the prevalence of escapees in catches is presented separately for Fishery Regions, but marine farm production and the number of escapees reported from farms are presented for the nation as a whole.
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Escapees have occurred, though at varying frequencies and intervals, in coastal and freshwater fisheries throughout Scotland and Ireland and in northwest Wales and England during the study period (Tables 3 and 4). When compared across Scottish Farm Production Areas, escapees occur, on average, at low to very low frequencies in coastal and freshwater fisheries: <5% in the Northwest and <1% in the Western Isles and Southwest Areas. Note, however, that escapees have been reported at far higher frequencies in the Northwest Area in some years, both in coastal (22%) and freshwater (19%) fisheries. Furthermore, when data for the Southwest Area are disaggregated to subareas, it is apparent that escapees occur at higher frequencies in the coastal fisheries of Strathclyde, where farms are sited, than those of Solway and the East where there are no farms. A similar pattern is shown for freshwater fisheries, with the exception of the FRS study in the Solway subarea (Table 3).
In Northern Ireland, escapees have occurred in coastal catches across years at an average level of 4.2% and at a maximum of 13.8% (Table 4). In contrast, escapees occur at very low frequencies in the coastal fisheries of all regions in the Republic of Ireland, with the average ranging from <0.1% to 0.6% and a maximum frequency of 2.2% (Table 4). No escapees were reported from surveyed fisheries in England and Wales in 2003 or 2004, but were reported at up to 19.4% in coastal and 30% in freshwater fisheries in 2001 (Table 4) following an escape in Northern Ireland (Milner and Evans, 2003).
Pearson Product Moment Correlation (PPMC) was used to test for any association across years between farm production and the numbers of escaped salmon reported by farms, farm production and the incidence of escapees in coastal or freshwater fisheries, and the numbers of escaped farmed salmon reported by farms and the incidence of escapees in coastal or freshwater fisheries. These analyses were applied to data for Scottish regions separately, but to the data for the Republic of Ireland as a whole, where only national production and reported numbers of escaped farmed salmon were available. PPMC was also used to test for any association within regions between the incidences of escapees in Scottish coastal and freshwater fisheries.
Comparison between the average incidence of escapees in coastal and freshwater fisheries within regions was analysed by paired t-test. Before statistical analysis, data were normalized by log (salmon production), log(x+1) (escapees reported), or arcsine (proportions of escapees in catches) transformation. Statistical analyses were conducted using SigmaStat for Windows, version 3.10.
Analyses of the data do not support any association between the prevalence of escapees in coastal or freshwater fisheries and the reported number of salmon that have escaped from farms. Evidence for any association between escapee prevalence and farm production is weak, with significant positive correlations only for the Republic of Ireland, County Mayo coastal fishery survey data (r = 0.605, n = 14, p = 0.022) and for the reported coastal fishery data from the Scottish Southwest Production Area (r = 0.817, n = 11, p < 0.01). Indeed, comparisons between farm production in the Scottish Northwest Area and the incidence of escapees in fisheries, obtained from FRS studies, yielded significant negative correlations for both coastal (r = –0.842, n = 13, p < 0.001) and freshwater (r = –0.874, n = 13, p < 0.01) fisheries.
The only significant correlations between the incidence of escapees in coastal and adjacent freshwater fisheries arose from data reported by fishery proprietors in the Scottish Solway Subarea (r = 0.910, n = 11, p < 0.001) and from FRS data for the Scottish Northwest Area (r = 0.842, n = 9, p < 0.01). Escapees were present at significantly greater frequencies in coastal than freshwater fisheries in the Scottish Northwest Area (t = 4.225, d.f. = 10, p < 0.01) and Strathclyde Subarea (t = 2.637, d.f. = 10, p = 0.03), based on data from fishery proprietors, and in Northern Ireland (t = 2.539, d.f. = 13, p = 0.03). In contrast, the FRS study of fisheries in the Southwest Area yielded significantly greater escapee frequencies in fresh water than in coastal fisheries (t = –2.713, d.f. = 13, p = 0.02).
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Discussion |
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Our data and those reported previously (Youngson et al., 1997; Crozier, 1998) indicate that escapee salmon are rare in regions of the British Isles without salmon farms, occurring irregularly and typically at frequencies <0.5% and occurring, on average, at relatively low frequencies in fisheries in regions with farms (typically <5%). As such, the impact of escapees on wild populations is not currently considered in catch-based assessment of stock status. However, the limited impact of such low background levels on both the management and conservation of the stocks throughout a region may be of relatively little importance compared with the occasional high incidence of escapees contributing to single river stocks (Crozier, 1998), especially those with small spawning stocks. Escapees have been reported by fishery proprietors at much higher annual frequencies (up to 86%) in some freshwater fisheries of western Scotland (SEERAD, unpublished data) and in northwest England and Wales for short periods (Milner and Evans, 2003).
Our analyses yielded only weak evidence for any association between the incidence of escaped farmed salmon in fisheries and the numbers of salmon being reared in marine cage sites in Scotland and Ireland. However, the analysis of data averaged across a region may obscure significant relationships apparent at more local levels, e.g. if escapes occur at considerable distances from the nearest monitored river. As such, data should be collected and analysed at a finer spatial scale, i.e. for rivers. This, and the ability to instigate ad hoc monitoring in response to escape incidents, would facilitate analyses designed to answer questions such as, given an escape of X salmon of Y age in season Z, what spawning contribution would the farmed salmon be expected to make to a stock of A fish in a river B km from the farm site.
Although the results presented here provide rudimentary support but little statistical evidence to maintain the hypothesis, presumably because of the limited availability of data and perhaps because the analyses were applied at the regional scale, it is commonly assumed that escapees are more prevalent in fisheries in regions where farms are sited and, therefore, monitoring should be focused primarily in these regions. Probability of river entry must be related a priori to the availability of escapees, notwithstanding other factors. The incidence of escapee salmon in coastal and freshwater fisheries of Wales and northwest England was related (p = 0.035) to distance from the farm site in Northern Ireland from which the fish were lost (Milner and Evans, 2003). This was probably the result of the scale of the escape and the comparatively long distance over which their incidence was recorded.
There are a number of issues with current monitoring programmes that may prevent them from being fully effective as tools with which to assess the frequency of escapees among spawning salmon and, hence, egg deposition, which is a key index of risk to the wild stocks. These issues, which are more or less important for the various programmes around the nations of the British Isles, concern the methods used to identify escapee salmon and the reliance, to a greater or lesser extent, on data derived from fisheries.
Identification and authentication of farm origin
Except for most FRS samples, escapees were identified using external morphology alone, either because of the practicalities of examining large numbers of fish (Ireland) or of relying on anglers and netsmen to examine their own catches (Scotland: reported catches). Although the origin of putative escapees caught in England and Wales is validated by scale reading, no assessment is made of how many escapees are wrongly classified as wild fish and, therefore, not sampled. External morphology is an effective identification criterion for recently escaped fish (Crozier, 1998), but is less suitable for fish that escaped long enough before capture to allow regeneration of the fins and operculae. For example, 36% of salmon escapees caught in waters north of the Faroes bore no fin damage (Hansen et al., 1993), and three of ten escapees caught in the River Ewe, Scotland, were identified by anglers as wild fish (Butler et al., 2005). In contrast, assessments based solely on eroded fins can classify wild salmon as farmed (Hansen et al., 1993): two putative escapee salmon caught in the coastal fishery of Northeast England were subsequently classified as wild fish based on scale reading. Furthermore, the use of external morphological criteria does not allow an assessment of the spawning contribution of those farm fish that escape as juveniles from freshwater facilities: more than 76 000 juvenile salmon were reported to have escaped from Scottish freshwater farms during the period 2000–2004 (Anon., 2001a, 2002b, 2003a, 2005a, b). The origin of such fish might be confirmed using molecular genetics, image analysis techniques (Stokesbury et al., 2001), or trace-metals–stable-isotopes analysis (C. Trueman, pers. comm.), and the contribution of these fish should be better understood.
In addition to mistaken identity, fish may be wrongly classified on purpose, either to allow the retention of salmon from a fishery where wild fish must be returned to the water alive, or where less obvious farmed fish might be classed as wild to increase their market value. In Ireland, escapees are generally regarded as damaged fish and, before the introduction of mandatory carcass tags and logbooks, may have been retained or sold privately. These fish may not have been included in the catch being examined, leading to some underestimation of the actual number of these fish in catches.
Reliance on fisheries data
In-river trap catches are monitored throughout the British Isles, but most of the fish scanned for the presence of escapee salmon are caught by coastal or freshwater rod-and-line fisheries. Unfortunately, this reliance on fisheries for data introduces potential problems of geographical and seasonal bias in the collection of appropriate data.
Geographical bias, stemming from the mismatch between the distribution of farming and fisheries, is likely to have the greatest influence in the FRS studies, which have relied, to a large extent, on sampling coastal fisheries. The decline in net fishing effort in recent years as netting stations closed, especially on the north and west coasts of Scotland, means that FRS sampling is numerically dominated by fisheries on the east coast, farthest from marine fish farms. For example, even in 2004, when FRS sampling included rod catches from the southwest coast round to the east coast, and coastal catches from the north and east coasts, 77% of sampled salmon had been caught in east coast fisheries. This limitation extends to the catch reports made by the coastal fisheries themselves, although the reports from rod fisheries go some way to addressing this bias. However, the use of fishery catch statistics is not ideal for the present purpose, owing to the concerns highlighted above regarding reliance on identifications that are not subject to later confirmation.
Geographical mismatch between fisheries and farms may also be significant in Ireland. Typically, escapees are far less common in the coastal fisheries of the Republic of Ireland than in those of Northern Ireland, although salmon farming in Northern Ireland accounts for less than 1.5% of the total Irish production (ICES, 2005). The Republic of Ireland catch, however, is derived primarily from driftnets set up to 9.7 km offshore (19.3 km before 1997). Perhaps escapees from farms on the west coast of Ireland migrate northward closer inshore and are less susceptible to the driftnets, but do not survive to return to Irish rivers, or enter Scottish or Norwegian rivers instead (L. P. Hansen, pers. comm.).
Another concern is whether or not the presence of escapee salmon coincides with seasonal fisheries. Examination of the SEERAD Record of Escapes (unpublished data) for the period July 1998–March 2003 indicates that 76% of the 1.2 million fish lost from marine cage sites escaped during November–March. Most escapees do not enter rivers immediately (Webb et al., 1993a), and their subsequent survival is relatively poor (Gausen and Moen, 1991). It is possible, therefore, that fish lost from farms during the closed seasons for fisheries will disperse widely and die or just die per se, and that relatively few become available to fisheries.
In addition, the behaviour of the fish that escape from farm sites from spring to autumn indicates that they may be more or less susceptible to exploitation by different fishery types. Coastal netting operations typically cease fishing in August or September and will not intercept escapees returning to inshore waters thereafter. Escapees tend to enter rivers later than wild salmon (Gausen and Moen, 1991; Gudjonsson, 1991; Carr et al., 1997; Crozier, 1998), so some escapees may not enter rivers before the close of the freshwater fisheries (Carr et al., 1997; Youngson et al., 1997; Butler et al., 2005). This may explain, in part, the relatively low frequency of escapees in freshwater catches compared with those of some adjacent coastal fisheries in the UK and Ireland (Crozier, 1998; this paper). In Norwegian rivers, escapees occurred at similar frequencies (
29%) in summer coastal fisheries and among fish collected for broodstock in the autumn, but at far lower frequencies (5.8%) in summer freshwater catches (Lund et al., 1991). Data from the UK and Ireland showed few significant correlations between the frequencies of escapees in catches of coastal and freshwater fisheries. This topic requires further investigation, especially given the reliance on coastal fishery monitoring alone in the Republic of Ireland and the possibility of significant effort reductions in this fishery in the future.
Recommendations for future monitoring programmes
In this paper, we have examined the programmes designed to monitor the incidence of escaped farmed salmon in wild salmon stocks throughout the British Isles and considered their current limitations. As such, this paper could form the basis upon which to develop a guide to best practice for these and other monitoring programmes. Common use of best practice would facilitate better and more revealing comparison of results between areas and nations and, in turn, strengthen the scientific evidence base required to support improvements in farming practices designed to reduce the numbers of fish of all ages lost from production facilities. Elements of best practice would include the use of fishery-independent sources of data, identification of fish origin based on at least two methods, a quantitative assessment of the degree of incorrect classification, and the timely and accurate reporting of all escapes.
Given the issues raised above, we would recommend the following as the key principles by which to modify existing monitoring programmes and design future programmes in the British Isles:
- Scientific sampling of in-river stocks should be the principal method for collecting data and ideally be from fishery-independent sources. The identification of origin should be based on at least two methods, and a sample of "wild" fish should be examined using these methods to assess the rate of incorrect classification as wild. At present, it is unlikely that resources would allow additional validation of all catches throughout the UK and Ireland, and the low frequencies of escapees in many catches do not warrant greater accuracy. Nevertheless, it may be appropriate to validate subsamples and assess the rate of incorrect classification.
- Monitoring efforts should be targeted primarily in those regions where farms are sited. However, given the occurrence of escapee salmon in fisheries throughout Scotland and Ireland and occasionally England and Wales, programmes should also include a network of sampling in regions without farms. To broaden the geographical distribution of sampling, monitoring programmes should make better use of in-river traps not operated by Agencies (Figure 1) and the many broodstock collections, and should include rivers that have been designated as Special Areas of Conservation (SAC) with salmon listed as one of the primary reasons for this designation (Figure 1).
- The reporting of escapes should be a requirement for all production facilities, both in the freshwater and marine environments, and there should be better coordination between the timely and accurate reporting of escapes and ad hoc monitoring of in-river stocks within the area.
- There should be an increased awareness of the distribution of restocking programmes to highlight those fisheries where discrimination between reared fish that are purposefully or mistakenly released to the wild will be required.
In making these recommendations, we recognize that some would require considerable investment in resources. However, it should be noted that, although continuing efforts to minimize escapes, including the Code of Good Practice for Scottish Finfish Aquaculture, storm damage accounted for 74% of the losses from Scottish salmon farms between July 1998 and March 2003 (SEERAD, unpublished data). The frequency and severity of autumn/winter storms has increased during the past 50 years, and this trend is predicted to continue into the twenty-first century because of climate change (Hulme et al., 2002). Thus, numerically significant loss events from farms may become more frequent in the future.
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Acknowledgements |
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We thank those staff of the Fisheries Research Services, Marine Institute, Department of Agriculture and Rural Development, Environment Agency and Centre of Environment, Fisheries and Aquaculture Science who contributed to the various monitoring programmes, as well as anglers, netsmen and merchants who provided assistance in the sampling of fish. Our thanks also to Daniel Pendrey, Julian MacLean, and Gordon Smith of FRS and Rob Evans of the Environment Agency for their assistance in collating the data reported here. The manuscript benefited from the comments of two anonymous referees, to whom we are grateful.
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