Diseases of wild sea trout in Scotland in relation to fish population decline

Fisheries Research, 17 (1993) 175-185 0 1 6 5 - 7 8 3 6 / 9 3 / $ 0 6 . 0 0 © 1993 - Elsevier Science Publ ishers B.V. All rights reserved

175

Diseases of wild sea trout in Scotland in relation to fish population decline

A.H. McVicar a,*, L.A. Sharp a'c, A.F. Walker b, A.W Pike c aSOAFD Marine Laboratory, Aberdeen, UK

bSOAFD Freshwater Fisheries Laboratory, Pitlochry, UK cZoology Department, Aberdeen University, Aberdeen, UK

Abstract

Sea trout catches have been unusually low in recent years in some areas of Scotland, particularly parts of the west coast, coincident with a decline in sea trout catches and stocks in parts of western Ireland. The causes of the widespread decline are at present unknown and are being investigated but climatic as well as biological influences are likely to be involved. A wide variety of pathologies has been detected in sampled sea trout, particularly in the kidney, liver, and heart but with no overall consistency in occurrence between areas or within individual rivers. In some fish the lesions were sufficiently extensive to be considered to be possibly threatening to organ function, but no correlation was established between severity and loss of fish condition. Juvenile trout sampled in seawater, in estuaries and lower rivers were mainly in good condition. However, some obtained in rivers in northwestern Scotland during early summer had cranial lesions and dorsal fin damage associated with sea lice. The prevalence and intensity of infection varied between and within sites with high intensities being found on both west and east coast rivers. There was no clear relationship between lice burden and the extent of fin damage on individual fish. Samples obtained in the late summer and autumn were clear of lice and showed no lesions. A wide range of other metazoan parasites was recorded, with no indication of correlation with host condition. No significant bacterial infection was detected, but infectious pancreatic necrosis ( IPN) virus was detected in fish from two west coast rivers. The significance of the pathologies and occurrence of metazoan parasite and other infections is being studied but with the data currently available no cause-effect relationship between disease and decline of sea trout populations could be established.

Introduction

Concern has been expressed in recent years by fishery owners and fish bi- ologists about the low level of stocks of sea trout (Salmo trutta) in parts of Scotland. The questions have to be asked (a) whether this perception is real and can be supported by scientific evidence, (b) whether the reasons for any changes can be determined and (c) whether there are any management or other strategies which can be introduced to improve the situation. Each of these questions is, by itself, sufficiently large and complex to provide the sub-

*Corresponding author.

176 A.H. Mc Vicar et al. /Fisheries Research 17 (1993) 175-185

stance of an extended research programme and consequently it is unrealistic to expect to provide definitive answers to all or even any of them in the short term. However, it is important that the significant underlying principles of the subject area are established and well understood at an early stage to provide a solid base for further focused research. This paper reports the prelimi- nary results of an ongoing study designed to evaluate the extent of the problem in Scotland and whether there is evidence of parasite or disease involvement. It also attempts to highlight some of the dangers in premature interpretation of incomplete data.

Scottish sea trout stocks

Accurate data on the state of sea trout stocks are difficult to obtain, but it is clear from catch returns, even with all their inadequacies, that there is a recent trend. Angling catches of sea trout have been unusually low in several areas of Scotland in recent years, the national catches reported for both 1990 and 1991 being less than at any t ime since the statutory catch series began in 1952. Widespread low catches were also a feature during the late 1960s and the 1970s (Fig. 1 (a ) ) . It is notable that over the same period, a sharp decline in sea trout catches occurred in mid-western Ireland and evidence from trapping and other studies indicated that spawning stocks were severely depleted in both 1989 and 1990 (Tully and Whelan, 1993). The Irish trapping data indicate a long-term decline in sea trout stocks, particularly in the mid 1970s, but with a further unprecedented steep reduction beginning in 1987 (Tully and Whelan, 1993). Current angling catches for Scotland as a whole are only slightly lower than in the 1970s. However, northwestern rivers have experi- enced a particularly severe decline in angling catches, with 1989, 1990 and 1991 being unprecedentedly low (Fig. 1 (b ) ) . Statistics also show that com- mercial netting catches of sea trout have been falling progressively over the last 10 years but these data are less valuable for evaluation because the sea trout are taken largely as a by-catch to salmon and there has been a substantial decline in the salmon netting effort during the same period (Anonymous, 1992a). The general perception of a long-term gradual decline of some sea trout stocks with a steeper decline since the late 1980s, particularly in the rivers of the west coast of Scotland, is borne out by the currently available scientific data (Walker et al., 1991 ).

Consideration of the nature of the sea trout populations in different areas of Scotland may give some clues as to why their stock performance apparently differs over the same period. Sea trout from the western Highlands and Is- lands fisheries are based largely on slow-growing, potentially long-lived and multiple-spawning fish. In contrast, the rivers of eastern Scotland and those of Ayrshire and the Solway Firth in the southwest, tend to contain faster growing, shorter-lived sea trout (Nail, 1930; Walker, 1984). The wider spread

,4. H. Mc Vicar et al./Fisheries Research 17 (1993) 175-185

SCOTTISH SEA TROUT ANGLING CATCHES (I 952 -91 )

177

8o~

70' I] ('~}i .........................

::i .......... ,

30 i . . . . . .

zO I I0 i ........

52 56 60 64 68 72 76 80 84 88

NORTH WEST SEA TROUT ANGLING CATCHES (I 952-91 )

lziL -- 1

? "" i

4 i . . . . . . . . . . . . . . . . . . . . . . . .

52 56 60 64 68 72 76 80 84 88

Fig. 1. Scottish sea trout angling catches for the period 1952-1991.

of year classes may confer more inherent stability on northwestern stocks; conversely, however, they would also be expected to take longer to recover from any prolonged reductions in recruitment, or periods when mortality rates were unusually high.

Possible contributory factors to sea trout population decline

The complexity of factors which could be involved in the regulation and consequently in the variations of sea trout populations was highlighted by the published reports of several recent reviews of this subject; namely the meeting

178 A.H. McVicar et aL /Fisheries Research 17 (1993) 175-185

of the UK Coordinator of Fisheries Research and Development (CFRD) Re- port (Anonymous, 1992b), by the National Rivers Authority (NRA) Fish- eries Technical Report (Anonymous, 1992c) and The Sea Trout Action Group (STAG) Report (Anonymous, 1992d). Because of this complexity it is not surprising that none of these reports were able to pinpoint a single biological or environmental component which could be conclusively identified as the only cause of sea trout population decline.

Some major changes have occurred in recent years in areas where sea trout populations have declined. For example, drought conditions have undoubt- edly affected catches in some parts of the country and may also have reduced stocks. The growth of the salmon farming industry in sea cages on the west coasts of Scotland and Ireland has led to the speculation (particularly in Ire- land) that parasites, notably sea lice, may be transferred from the fish farms to wild stocks with adverse affect. However, in Scotland, no direct association with fish farming has been proven as survey data show that there has been a decline in sea trout catches in areas where there are no salmon farms, e.g. the Ayrshire and Solway rivers.

The CFRD Report (Anonymous, 1992b) considered factors affecting ju- veniles in fresh water and/or increased mortality in the marine phase of their life cycle as causes for the apparent reduction in sea trout numbers. Particu- larly highlighted as possible contributing factors were possibly changed conditions in inshore waters, drought conditions, a shortage of prey species and possible exposure to diseases and parasites. Direct links could not be dem- onstrated with the data available. The STAG Report (Anonymous, 1992d) stated that the weight of available evidence indicated that the increase in the number of lice emanating from salmon farms was a major contributory factor in the decline in sea trout populations. This focus on disease as one possible factor affecting sea trout populations makes it particularly appropriate to in- troduce a note of caution at this stage in the investigations. The cause of disease and/or mortality in fish is frequently not attributable to infectious agents and the possible role of other extraneous factors should not be lightly dis- missed without exhaustive investigations. Also, when infection is known to be involved, experience has shown that, even in the relatively clearly defined situation of an aquarium or a fish farm, overt disease frequently results from simultaneous infection by more than one type of organism, often with an associated husbandry fault (McVicar and Richards, 1981; McVicar, 1988 ). Consequently, the source (or more likely sources ) of a problem on such a vast scale as the open environment will probably be considerably more difficult to determine; the complex interaction of many different factors (e.g. genetics, nutrition, environment, disease organisms) which can be involved in causing disease in fish, will make it very difficult to attribute the contribution being made to the problem in sea trout by any single component. At the early stage of any study, it is tempting for the non-specialist and the media to seize on

A.H. Mc Vicar et al./Fisheries Research 17 (1993) 175-185 1 7 9

the first association found and to blame the whole problem on that, ignoring other possible interactions and the different role each may play in the total scene.

Because of the emphasis of the current symposium, the disease aspects of the current studies on sea trout in Scotland will be concentrated on in this paper.

Disease conditions of sea trout

An immediate problem in disease studies in the natural environment is the difficulty in finding fish which are dead or dying with a disease. This is particularly the case in the large marine environment where predation pressures are great and any sick, abnormally behaving fish would rapidly be eaten. In survey work it is therefore a case of searching, in individual fish, for the occurrence of diseases which are known to be pathogenic and to extrapolate these observations to the population level. Fish which are being subjected to natural stress incidents such as smolting and spawning make particularly good subjects for disease investigation as they tend to be more susceptible to infection and consequently are more likely to reveal endemic diseases occurring at low levels in the environment. As was indicated by McVicar (1988), it is important to note that a low number of fish found with a highly pathogenic disease could be highly significant and that commonly occurring diseases may be of lesser significance unless there is an epidemic situation. It is therefore important to have a good understanding of the dynamics and pathogenicity of a disease before making comment on the possible impact it may have on a wild fish population. Any field observations should be supported by experimental studies.

The approach taken in the present study was to sample nationwide from as wide a range of situations as possible; from the east and west of Scotland, including locations associated with successful netting operations, in the vicin- ity of and far from salmon farming sea cage sites, and from rivers which had generated greater or lesser concern over catches. Sampling has been under- taken both in fresh water, in estuaries and at sea in an attempt to study all the different life cycle stages of sea trout. A particular problem with sea trout is that fish which will ultimately migrate to sea cannot be distinguished as fry or parr from those which will remain in fresh water. Also there are consider- able practical difficulties in obtaining sufficient samples from the sea phase of the life cycle. Disease aspects under investigation include pathology, bac- teriology, virology, parasitology, immunology and experimental epidemiology. This study is still in its early stages and the current results are from 1990 and 1991 only. It is being fully integrated with parallel studies on sea trout populations and the environment in both fresh water and seawater. The study in 1990 was based on 52 fish from east coast rivers and 110 from west coast

1 80 A.H. Mc Vicar et al./Fisheries Research 17 (1993) 175-185

rivers. Most fish were caught in the estuary, or immediately above the estuary, and emphasis was placed on the pathology of fish which had returned from the sea. In the 1991 sampling programme, over 220 fish were tested for viral and bacterial infections, in addit ion to pathology and parasitology. All samples were taken to comply with standard practices for pathology and disease analysis. Because the question has been raised whether fish farming has introduced new disease conditions to the environment or has elevated existing naturally occurring diseases to a level where wild stocks become heavily infected, diseases known to occur in salmon farming were particularly studied.

Disease of unknown aetiology

Fish pathology has been recognised (McVicar, 1986 ) as a potentially useful index for adverse environmental effects. Because it represents the end point of an often long sequence of changes within the body of fish it may also give a clue as to the occurrence of disease long after the disappearance of the caus- ative agent. Consequently, some emphasis was placed on pathology in the early part of this study, particularly as this could give an indication of differences between areas, some of which were suffering apparent declines in sea trout populations. Evaluation of the literature revealed remarkably little published information available on disease in this species of fish.

A wide variety of pathologies has been detected in the sea trout sampled in this study, particularly in the kidney, liver, heart and pancreas. Kidney lesions consisted of glomerular shrinkage and fluid accumulation in the Bow- man's capsule, proximal kidney tubule wall degeneration and occasionally ne- phrocalcinosis with partial or complete blockage of the tubule lumen. Renal blood vessel walls sometimes showed extensive inflammation without evidence of focal localisation. The livers of several fish showed exceptionally high levels of lipid vacuolation in hepatocytes with evidence in some areas of localised degeneration. The hearts of a low number of sea trout showed extensive pericardial inflammation, and foci of myocardial degeneration of the ventricle and auricle. An unidentified microsporian (Protozoa) was also recorded infecting the heart muscle of one fish.

In some fish the lesions were so extensive that if they had been found in a fish farm stock they would have been considered as being potentially damag- ing to organ function and possibly the general health and performance of the fish. However, no correlation was established between lesion severity and loss offish condition in the sea trout. Also, there was no overall consistency in the occurrence of lesions between areas and within even one river sample. At the moment no conclusions can be made on the effect of these lesions on individual fish or on sea trout populations as a whole.

Some research effort was directed at the condition of post-smolts because it has been noted (Tully and Whelan, 1993 ) that particular features of the sea

A.H. Mc Vicar et al./Fisheries Research 17 (1993) 175-185 1 8 1

trout problem in mid-western Ireland has been the premature return of smolts and the presence of severely emaciated fish. There have been similar reports from fishery owners of some northwestern Scottish rivers, but few sick-look- ing fish were observed in the present study. However, the description of a problem in the immediate post-smolt stage of the life cycle possibly bears some resemblance to the condition popularly known as 'failed smolt syndrome' observed in some salmon farms in Scotland and Norway. At these farms, 50% or more of salmon smolts show loss of condition, poor feeding response and high mortality rates in the period 2-4 months after transfer to seawater. The syndrome is not well characterised and the cause is currently unknown. It may be associated with feeding problems following smolting compounded by secondary problems, e.g. diseases such as infectious pancreatic necrosis ( IPN). Until the results of further research currently in prog- ress are available, the relevance of this to sea trout must remain speculative.

Known infectious disease

The emaciated condition reported particularly in the Irish sea trout post- smolts was very reminiscent of a condition in farmed Atlantic salmon known as pancreas disease (PD). This is an infectious disease, probably viral in, aetiology, which is known to have a natural distribution in seawater on the west coast of Scotland and Ireland (McVicar, 1987, 1990). It is therefore probable that sea trout will be exposed to the disease when they migrate into seawater. The only diagnostic criterion currently available for PD is total necrosis of the exocrine pancreas and associated loss of fish condition. Patho- logical changes can persist in a recognisable form in affected salmon for up to several months. The sea trout pancreases examined so far showed no pathology similar to that of PD. However, it is now known that PD can affect salmon without actually destroying the pancreas so the possibility of this disease being present in sea trout cannot yet be totally excluded. Experiments will be car- ried out on this disease in sea trout.

Of over 220 fish sampled for viruses in 1991, 16 sampled in July from two different sites were positive for IPN virus. Subsequent samples from the same locations and repeat samples at the same time of year the following season were all negative. The significance to sea trout populations of this isolated occurrence is not fully understood at present. However, IPN infection was believed by Smail et al. ( 1992 ) to be closely associated with clinical disease and associated mortalities in farmed Atlantic salmon post-smolts and consequently the effects of this disease in sea trout is the subject of planned experimental transmission trials with sea trout post-smolts.

To date, no significant bacterial pathogens have been detected in kidney samples from any fish. This contrasts with the report of furunculosis in Irish sea trout and the suggestion by McArdle et al., 1993 ) that furunculosis (Aero-

182 A.H. Mc Vicar et aL/Fisheries Research 17 (1993) 175-185

monas salnonicida) may have had a role in the collapse in sea trout numbers in some rivers in Ireland in 1989 and 1990.

Historically, a wide range of metazoan parasites has been recorded from sea trout and there are several extensive reviews on the subject (see Kennedy, 1974). The current study indicates a similar range of parasites, though the present list is still considered incomplete. A large variation in the intensity of parasitic infection has been observed, both between sites and within fish at individual sites. Patterns of parasite species distribution can be discerned, with particular differences between east and west coast Scottish rivers. The identification of Pomphorhynchus sp. (Phylum Acanthocephala) in a western Scottish river marks a new site record for the parasite and a new host record for Scotland. However, parasitic infection should not be considered as anything other than an entirely natural phenomenon and infections of mod- erate intensity are believed to have little effect on the condition of otherwise healthy hosts. There is no evidence in the present data to suggest that there has been any introduction of a new parasite species to the Scottish sea trout population; the catastrophic effects on the naive western Norwegian salmon stocks following the appearance of Gyrodactylus salaris is well documented (Halvorsen and Hartvigsen, 1989). It is also noteworthy that, as a general principle, fish which are compromised by, e.g. a poor environment or diseases often show an imbalance in their parasitic fauna in terms of species present or the intensity of infection of any one species. To date, no such imbalance has been detected in the data on endoparasites from sea trout in Scotland.

Sea trout, which tend to be coastal in habit, have frequently been found to be infected with sea lice when caught in, or newly returning from the sea. It is remarkable that, despite Caligus elongatus usually being considered to be a more coastal species, it was rarely found on sea trout during this investigation and most infections were of the calagid copepod Lepeophtheirus salmonis. As with other parasites, a large variation in infection intensity was evident, between individual fish and between sites. The majority of juvenile sea trout sampled in 1991 (and also in 1992) were in relatively good condition and none were recovered in a condition which could be described as emaciated. This contrasts with the situation in Ireland (Tully and Whelan, 1993 ) where the occurrence of high levels of L. salmonis infection of smolts and kelts was directly associated with severe emaciation. However, in both years in Scot- land, some juvenile trout were recovered which showed evidence of sea lice damage. This took the form of dorsal fin erosion, with the fin rays becoming separated as a result of the destruction of the soft connective tissue. More severe infection was associated with cranial lesions, although damage of this severity was seen more rarely than dorsal fin erosion. There were some indi- cations of differences in the stage of development and healing of lesions in fish sampled in different months from the same site; fish sampled in early June from a northwestern Scottish river showed both dorsal fin and cranial

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damage, in late June dorsal fin recovery and healing of cranial lesions was evident while in late summer and autumn, no lice and no lesions were recorded.

As has also been noted in western Ireland (Anonymous, 1992d), there ap- peared to be no correlation between intensity of infection with sea lice at the time of capture and the degree of sea lice associated damage. However, most of the fish sampled in the earlier part of this study had returned from the sea to brackish or flesh water and may have shed some or all of their lice. In addition there does not appear to be a strong correlation between the prox- imity of salmon farming sea cages and the intensity of sea lice infection. High intensities (a maximum of 54 parasites per fish) have been recorded on the east coast, though the highest intensity so far recorded in Scotland was on a fish found moribund in a west coast river, the Little Gruinard (194 parasites). It is noteworthy that salmon caught by line fishing approximately 100 miles off the Faroe Islands were found with significant numbers of sea lice and some evidence of associated cranial damage. It is also worth noting that, in salmon farming in Scotland, fish which are sick from other diseases such as furunculosis and pancreas disease are particularly susceptible to sea lice infection and can build up heavy infections compared with healthy fish living in the same cages. Consequently, it should not be assumed that heavy lice burdens are the primary disease and these should be considered to be symp- tomatic of a totally different problem. Demonstrating a simple correlation between disease symptoms such as emaciation and an infection does not establish a cause-effect relationship. Such associations should be further investigated, particularly experimentally to determine if they are primary, secondary or even coincidental.

The STAG Report (Anonymous, 1992d) from Ireland stated that they believed "the weight of available evidence indicates that the increase in the number of lice emanating from salmon farms was a major contributory factor in the sea trout collapse". Data so far available from Scottish studies are in- sufficient to support or deny this conclusion.

Conclusions

It has not been possible to establish a disease cause for the decline in sea trout populations from the data available in the present study, although it should be noted that the investigation is still in its early stages. Consequently, it is not possible to make meaningful comment from a disease point of view on strategies to improve the state of sea trout stocks in Scotland. A wide range of pathologies was found and some of these could be considered significant if found in farmed salmon stocks. However, their consequences to wild sea trout are speculative. There was no overall consistency in their occurrence which could point to a reason for the differences in sea trout catches in different

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areas. Some individual sea trout carry heavy burdens of lice with accompa- nying skin lesions. However, without comparative data for 'normal' lice levels it is not possible to state the significance of this observation.

This study has provided no evidence so far that fish farms could be having an effect on sea trout populations through transfer of disease to wild stocks, introduction of new diseases or the elevation of existing diseases to levels which are presenting danger to sea trout stocks. In the wider context, and with particular reference to salmonids, the ICES Working Group on Pathology and Diseases of Marine Organisms Report (Anonymous, 1992e) concluded that there was no evidence of a significant detrimental effect on wild fish stocks as a consequence of the occurrence of disease in mariculture in the North Atlan- tic/Baltic areas.

References

Anonymous, 1992a. Freshwater Fisheries Laboratory Pitlochry Annual Review 1990-1991. The Scottish Office Agriculture and Fisheries Department, Pitlochry, 64 pp.

Anonymous, 1992b. Research priorities for salmon and sea trout. A report of the UK Coordi- nator of Fisheries Research and Development. SOAFD Marine Laboratory, Aberdeen, pp. 1-27.

Anonymous, 1992c. Sea trout in England and Wales. National Rivers Authority Fisheries Tech. No. 1, NRA, Almondsbury, pp. 1-32.

Anonymous, 1992d. Sea Trout Action Group 1991 Report. Sea Trout News, 3: 1-24. Anonymous, 1992e. Report of the Working Group on Pathology and Diseases of Marine Orga-

nisms, Copenhagen. ICES C.M. 1992/f:2, 52 pp. Halvorsen, O. and Hartvigsen, R., 1989. A review of the biogeography and epidemiology of

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McVicar, A.H., 1987. Pancreas Disease of farmed Atlantic salmon, S a l m o salar+ in Scotland: epidemiology and early pathology. Aquaculture, 67:71-78.

McVicar, A.H., 1988. Epidemiology/epizootiology: a basis for control of disease in mariculture. In: F.O. Perkins and T.C. Cheng (Editors), Pathology in Marine Science. Academic Press, San Diego, CA, pp. 397-405.

McVicar, A.H., 1990. Infection as a primary cause of Pancreas Disease in farmed Atlantic salmon. Bull. Eur. Assoc. Fish Pathol., 10: 84-87.

McVicar, A.H. and Richards, R.H., 1981. Fish disease: its prevention, diagnosis and treatment. In: A.D. Hawkins (Editor), Aquarium Systems. Academic Press, London, pp. 279-301.

Nall, G.H., 1930. The Life of the Sea Trout. Seeley Service, London, 335 pp. Smail, D.A., Bruno, D.W., Dear, G., McFarlane, L.A. and Ross, K., 1992. Infectious pancreatic

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necrosis (IPN) virus Sp serotype in farmed Atlantic salmon, Salmo salar L., post-smolts associated with mortality and clinical disease. J. Fish Dis., 15: 77-83.

Tully, O. and Whelan, K.F., 1993. Production of nauplii of Lepeophtheirus sahnomis (Kroyer) (Copepoda: Caligidae) from farmed and wild salmon and its relation to the infestation of wild sea trout (Salmo trutta L.) offthe west coast of Ireland in 1991. Fish. Res., 17: 187- 200.

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Walker, A.F., Fryer, R.J. and Shanks, A.M., 1991. The decline in west coast Scottish sea trout, Sahno trutta L. angling catches. In: M.C. Lucas, I. Diack and L. Laird (Editors), Interactions between Fisheries and the Environment. University of Aberdeen, UK, pp. 47-54.

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Diseases of wild sea trout in Scotland in relation to fish population decline