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REVIEW AND SYNTHESIS OF THE ENVIRONMENTAL IMPACTS OF AQUACULTURE

CHAPTER TWO THE DISCHARGE OF WASTE NUTRIENTS AND THEIR INTERACTION IN THE WIDER MARINE ENVIRONMENT

SOLID WASTES FROM CAGE FARMS AND EFFECTS ON SEDIMENTS

2.1 The major particulate effluent from a cage farm consists of faecal material and uneaten fish feed. The amount of faeces and feed will depend not only on the digestibility of the food, but also on a range of other environmental and husbandry factors such as temperature and disease status. Feeds are fish meal/oil based, but they also contain a wide range of components including wheat, soya meal, crustacean meal, vitamins, amino acids, minerals and pigments.

2.2 Modern diets are easily assimilated and give good feed conversion ratios (FCR: product produced per unit feed), which has reduced waste inputs to the environment per unit production. Economics are also important, as overfeeding is most likely when the value of the product is high and the cost of the feed is low, with greater care being taken of an expensive feed product. In the early years of the Atlantic salmon farming industry, feed losses were thought to be up to 20% of total feed input. It is now generally accepted that feed losses have been reduced to less than 5% in well-run farms. This is important, as fish feed is extremely energy-rich, causing much greater organic enrichment than faeces on a weight for weight basis.

2.3 The solids emanating from cage farms consist of a range of particle sizes and densities, with a range of settling velocities. These particles are affected by water currents that may vary with depth. The resulting dispersion may cause settlement well away from the farm, but usually the highest deposition rates are in the immediate vicinity. The eventual site of deposition will depend on local bathymetry, water movement, and flocculation (clumping of finer particles to form larger, more rapidly settling particles). Bacteria may break down slow settling particles, leading to the release of nutrients into solution. A variety of computer models have been used to track particles to the bed in an effort to predict the zone of organic enrichment. On reaching the seabed, these particles may become incorporated into the sediment or may be resuspended by near-bed currents, thus further dispersing them away from the cages.

2.4 Addition of organic wastes to sediments immediately causes an oxygen drain as bacteria degrade them. The dissolved oxygen concentration at any point in the sediment is dependent on the rate of its uptake, either to fuel aerobic metabolism, or to re-oxidise reduced products released by anaerobic bacteria deeper in the sediment. When the oxygen demand caused by the input of organic matter exceeds the oxygen diffusion rate from overlying waters, sediments become anoxic and anaerobic processes dominate.

2.5 Animals burrowing in sediments that receive normal detrital inputs have a diverse fauna with many species and include a wide range of higher taxa, body sizes and functional types. As organic inputs increase, this diversity also initially increases as the enhanced food supply provides opportunities for the expansion of existing populations and the immigration of new species. However, deterioration of the physical and chemical conditions in the sediments progressively eliminates the larger, deeper-burrowing and longer-lived forms favouring smaller, rapidly growing opportunist species. With increasing inputs, the surface sediments become anoxic and only a small number of specialist taxa can survive, mainly small annelid and nematode worms, which may flourish in huge numbers. Where anaerobic processes occur close to the sediment surface, this may become covered in dense white mats of sulphide oxidising bacteria Beggiatoa sp. High flow rates, bringing a continuous supply of oxygen to the sediment surface, do allow the survival of infauna even when the sedimentary surface layer is anoxic but, where sediments suffer oxygen deficiency for even relatively short periods of a few hours, e.g. caused by slack water, large sections of the benthic macrofauna are eliminated. Ultimately, increasing levels of sedimentary oxygen demand bring about anoxia in the lower levels of the overlying water column leading to the elimination of all higher life.

2.6 Organic degradation rates for labile materials such as are present in waste feed ( e.g. lipids and protein) are broadly similar in both anaerobic and aerobic sediments but less labile organic material degrades much more slowly in aerobic sediments. The small worms that dominate enriched sediments significantly enhance the degradation rate of organic materials by mechanisms that are not yet fully understood. Thus, if these are excluded by a severe lack of oxygen in the sediment the rate of organic breakdown is reduced. This enhances organic accumulation through negative feedback.

2.7 The rate at which sedimentary ecosystems recover following the removal of cages or the cessation of farming is of considerable interest, particularly as the fallowing of sites and rotation of cages has now become recommended practice in many areas. In a Scottish study of benthic recovery, communities adjacent to the cages returned to near-normal (with respect to unimpacted stations) 21-24 months after farming ceased, but to date no study has looked at recovery processes over a sufficiently long period to be certain about recovery times.

Summary

2.8 Particulate organic wastes from cage farms have a profound effect on the benthic environment and recovery, on cessation of farming, may take several years. Impact on the sea bed is the most obvious pollution effect from fish farms and measures of this effect are the main method of regulating and controlling the size of fish farms such that the local environment is not overwhelmed. However, severe effects are generally confined to the local area (a few hundred metres at most) and the total area of seabed used for this purpose is insignificant in terms of the total coastal resource. Recovery of the seabed after farming is variable, but in Scottish waters may take around 2 years.

Research Gaps

2.9 Although the gross effects of fish farming on sediments are relatively well understood, much remains to be done regarding the dynamics of waste input, responses from the sediments in terms of the interactions between microbial and macrobiological processes, how these influence the chemistry of the sediments, and the physical processes of oxygen supply, sediment resuspension and mixing by water currents. These interactions take place against a background of seasonal changes and the 2 year farming cycle that results in great variation in the supply of organic materials to sediments. In addition, interannual variability in biological factors, such as the supply of invertebrate larvae, probably has effects that are not as yet well understood. These aspects are important as they affect: 1) our understanding of the assimilative capacity of sediments with respect to farm wastes; 2) the ways in which chemical contaminants in sediments are redistributed to the wider environment and; 3) the ways sediments consume oxygen and release dissolved nutrients into the water column.

DISSOLVED NUTRIENT INPUTS AND EFFECTS ON PHYTOPLANKTON

Introduction

2.10 Fish farms undoubtedly contribute to the pool of plant nutrients in seawater. Fish excreta and decaying food contain or release ammonia and salts of nitrate and phosphate. In pristine coastal waters the nutrients are typically present only in small amounts, but are important because they support the growth of seaweeds and the much smaller floating algae that comprise the phytoplankton and which can be properly seen and identified only with microscopes. Additional nutrients enter the sea from acid rain and from rivers enriched with (treated) urban sewage, farmyard waste and drainage from fertilised soils. In the north and west of Scotland, however, fish farms are the most important extra source of nutrients in most lochs and voes.

2.11 Phytoplankton, it has been said, are "the grass of the sea", the basic food on which animal life and fisheries depend. Whenever there is sufficient light, planktonic algae increase in numbers by absorbing mineral nutrients and converting solar energy into organic matter. They are eaten by equally microscopic single celled creatures, the protozoa, as well as by pelagic crustaceans, the size of seeds, termed zooplankton. In turn these zooplankton provide food for larger animals and thus for fish. Live and dead plankton sinks towards the seabed and provides the main source of food for animals living there.

2.12 However, nutrient enrichment can have negative consequences. Most of these are comprehended by the widely accepted EU definition of eutrophication, which is "the enrichment of water by nutrients especially compounds of nitrogen and phosphorus, causing an accelerated growth of algae and higher forms of plant life to produce an undesirable disturbance to the balance of organisms and the quality of the water concerned".

2.13 The undesirable consequences of eutrophication include:

• Increased abundance of micro-algae, perhaps sufficient to discolour the sea and be recognised as a bloom or "Red Tide";
• Foaming of seawater;
• Killing of free-living or farmed fish, or sea-bed animals;
• Poisoning of shellfish;
• Changes in marine food chains;
• Removal of oxygen from deep water and sediments as a consequence of the sinking and decay of blooming algae.

2.14 The main concerns relating to the marine aquaculture industry in Scotland are that the discharge of plant nutrients from finfish farms:

• Has led to an increased occurrence of algal blooms.
• Has disturbed the natural ratios of nutrient elements in seawater so favouring the occurrence of toxic species over harmless algae.
• Has made potentially toxic algae more poisonous.

2.15 This part of the report presents the scientific background and reviews the evidence relating to these charges. Our conclusion is that, except perhaps in a few enclosed waters, enrichment by fish farm nutrients is too little, relative to natural levels, to have the alleged effects. However, we cannot, as we would wish, support this conclusion with data from series of measurements of nutrients, phytoplankton, algal blooms, and the presence and toxicity of harmful species, made at key sites over the several decades that span the development of the current fish farming industry. The future collection of such data, and its scientific analysis, should be made a priority.

Phytoplankton growth and harmful algal blooms

2.16 Under conditions of plentiful light and nutrient supply, many types of planktonic algae reproduce at an increased rate, potentially doubling their abundance every few days. The peaty waters of many sea-lochs, and the turbid sea in regions of strong tidal streams, are too dark for algal growth except near the sea surface. In many lochs, however, river discharges lower near-surface salinity and create a distinct and well-illuminated upper layer. Adding nutrients to this layer, either in river water or by way of fish excreta, can create ideal conditions for algal blooms. Even here, however, algal population increase can be offset by zooplankton grazing or by dilution with seawater containing less phytoplankton.

2.17 Some types of algae, usually slow growing, deter their potential predators by means such as the formation of jelly-like masses, or the making of chemicals that make the algae taste or smell bad to their potential consumers. Should nutrient enrichment coincide with certain physical conditions, and other, poorly understood factors, it may be the growth of a noxious species that is stimulated, leading to a failure of this grazing control and the creation of a Harmful Algal Bloom. According to the editorial in the scientific journal Limnology and Oceanography (Volume 42, 1997). "The last two decades have been marked by an extraordinary expansion in the nature and extent of the marine phenomena we now call "harmful algal blooms". For years, the term "red tide" was used to describe many of these outbreaks, but in time, that term became less and less appropriate ... Not all red tides are harmful, and many blooms that cause negative impacts are not red and in fact, do not discolour the water at all. Some blooms are associated with potent toxins in the causative algae, while others cause problems simply because of high algal biomass. Some are of concern at exceedingly low cell densities .... Blooms of seaweeds or macroalgae also cause harm, in many cases as a result of the same environmental forcing that regulate microalgal blooms. The search for a term that encompasses these diverse phenomena was doomed to fail, but, for better or worse, "harmful algal bloom" is now used by scientists and government officials throughout the world, with HAB the obligatory acronym."

2.18 In most Scottish waters, the increase in daylight during spring stimulates phytoplankton to make a Spring Bloom with the aid of mineral nutrients formed during the winter from the decay of the previous year's plankton. The algae, termed "diatoms", are normally the most important members of this bloom, which is in some places sufficiently dense to make the sea brown in colour. Even when the Spring Bloom is enhanced by nutrient enrichment, it is not normally harmful, because the diatoms get eaten and thus provide food to fuel the pelagic ecosystem for much of the rest of the year. In addition to the nitrates and phosphates needed by all algae, diatoms also need dissolved silica to make the glassy material that forms the walls of their cells. When the supply of this nutrient becomes exhausted, diatoms cease to grow, and, if nitrates and phosphates remain, other algae may succeed the diatoms. Amongst these are flagellates, characterised by one or more whiplash-like organelles named from the Latin, flagellum. The tiny flagellate Chrysochromulina polylepis formed extensive and persistent blooms that caused widespread fish kills in Scandinavian waters in 1988.

2.19 Dinoflagellates have two flagella, arranged in characteristic fashion: one circles the waist of the cell, and spins it, the other trails lengthways and acts as a propulsive screw or propeller. The dinoflagellate formerly called Gyrodinium aureolum, but recently renamed as Gymnodinium mikimotoi, typifies harmfully blooming algae. G. mikimotoi seems to have been introduced into European waters in the 1960s. Where dinoflagellates are abundant, typically in late summer, the sea becomes dark brown or red-brown and sometimes appears oily - the classic signs of a Red Tide. These have sometimes been associated with the death of seabed animals. In Loch Fyne in September 1980, a Red Tide of the dinoflagellate G. mikimotoi killed salmon in ponds supplied with water from the loch.

2.20 Other harmful algae are associated with 'shellfish poisoning', in which toxins produced by the algae are accumulated in mussels, oysters, scallops, etc., that feed by filtering phytoplankton from water. Paralytic shellfish poisoning (PSP) is caused by a dinoflagellate formerly called Gonyaulax tamarensis and now Alexandrium tamarense. Humans eating intoxicated shellfish suffer numbness, headache, nausea, and diarrhoea, leading to paralysis and death in extreme cases. PSP has been known in south-eastern Scotland for several centuries. Species of the dinoflagellate genus Dinophysis are responsible for Diarrhetic Shellfish Poisoning (DSP), which involves rapid onset diarrhoea and vomiting (but is not fatal). Finally, Amnesic Shellfish Poisoning (ASP) has been known to science and medicine only since its discovery in 1987 in eastern Canada. Nausea and diarrhoea occur when humans eat intoxicated shellfish, leading in extreme cases to hallucinations, short-term memory loss, and death. The toxin seems especially persistent in scallops in Scotland. The causative algae are diatoms, mainly species of the genus Pseudo-nitzschia, and thus disprove the general rule that 'diatoms are good and flagellates are bad'. A common feature of all the shellfish poisonings is that potentially harmful levels of toxin can be found in mussels or scallops even when the causative algae are not abundant.

Harmful algal blooms in Scottish waters

2.21 Current HAB problems in Scottish waters are summarised in Table 2.1 (Both Tables 2.1 and 2.2 are largely taken from: Tett, P. & Edwards, E. (2002) Review of Harmful Algal Blooms in Scottish coastal waters, forthcoming report to SEPA, Stirling).

Table 2.1 Main Scottish HAB problems, circa 2000.

2.22 A summary of the recent history of harmful algal blooms in Scottish waters is given below in Table 2.2.

Table 2.2 Main HABs in Scotland, by decades.

2.23 The major concern relates to algal toxins accumulating in shellfish. Although toxicity monitoring prevents harmful consequences to humans, the occurrence of toxicity results in substantial economic loss through closure of shellfisheries. At first glance, it indeed seems that these types of HAB have grown more common and widespread during recent years, but this may be the result of greater spread and intensity of toxin monitoring rather than a real increase in the frequency of occurrences of HABs. It is unfortunate that there are no sites in fish farming regions that have been regularly and continuously sampled for phytoplankton amount and type since the 1960s, as this would allow a sound judgment to be made concerning whether toxic organisms had increased. However, information about phytoplankton is available from various sources and for particular places and years. This evidence, sporadic as it is, does not show conclusively that there has been a widespread increase in the abundance of most of the types of organisms responsible for harmful blooms. Despite increased numbers of fish-farms, which might be expected to provide a better detection network for harmful blooms of Gyrodinium aureolum and flagellates, there would seem to have been a decline in reports of such blooms.

2.24 On the east coast, present-day PSP levels seem to be no worse than those reported for 1968-1990. The apparent spread of toxicity (as opposed to that of the organism) to the Northern isles and the West-North-Hebrides region may have been a result of wider monitoring, a genuine spread of the causative organism, or a spread of toxicity or of toxic strains amongst existing populations. There is no evidence that Alexandrium tamarense is becoming more abundant either at new or traditional sites: it remains an organism that can give rise to significant toxin in shellfish at low concentrations of the dinoflagellate.

2.25 Dinophysis acuminata and other DSP-causing species have always been widely distributed in Scottish waters, and, with the exception of a Red Tide in Loch Long in 1994, there seems no evidence of an increase in abundance. As with Alexandrium tamarense, D. acuminata and related species can cause DSP when present in relatively small numbers, although the occurrence of outbreaks of DSP seems to be more sporadic and localised than that of ASP. DSP may have been endemic in Scottish waters for much longer than revealed by systematic monitoring for the toxin.

2.26 The greatest puzzle relates to ASP. Pseudo-nitzschia spp., formerly known as Nitzschia spp., have been common, and sometimes abundant, in Scottish waters for as long as records exist. Widespread toxicity was discovered soon after the commencement of extensive monitoring in 1999. Common sense suggests that this is too much of a coincidence, and that toxicity likely existed in years prior to 1999, an argument supported by sporadic records from occasional sampling in 1997 and 1998. But did ASP occur in Scottish waters long before 1997? If it did not, what has changed within the populations of Pseudo-nitzschia spp.? If it did, why are there no records of occurrences of the signs and symptoms of ASP amongst either Scottish or other European consumers of Scottish scallops?

2.27 Experience elsewhere may be relevant. In Mexico, although Red Tides have been known to occur in coastal waters for a long time, it is only in the last decade that ASP, DSP and PSP have become a cause for concern. A lack of regular monitoring of these waters - PSP analysis only taking place regularly in shellfish destined for export to the USA - suggests that where shellfish poisonings occurred in the past, they may have either been ignored, tolerated without permanent remark, or ascribed to bacterial contamination of the shellfish rather than to the effects of algal toxins.

2.28 On the one hand, then, the available data can be read as 'no change'. On the other hand, it must also be said that these data do not conclusively exclude the possibility of a real increase in the frequency of Scottish HABs, and especially in ASP, generally, and PSP in the Northern Isles. What could account for such increases? Table 2.3 lists several possibilities.

Table 2.3 Possible causes of a real increase in HABs in Scotland.

2.29 We now turn to three specific hypotheses commonly espoused regarding finfish aquaculture in relation to eutrophication and harmful blooms.

Hypothesis 1: plant nutrients from fin-fish farms have led to an increased occurrence of algal blooms

2.30 Scientists would prefer to address this charge with extensive data obtained in fish farming regions before and during the development of the industry. In Japan, for example, many years of observations in the Inland Sea have documented an increase and then decrease in the number of Red Tides as urban and industrial discharges first increased and then were controlled. In Scotland we do not have such time-series. Instead, there are two main sorts of indirect evidence.

2.31 The first derives from many site-specific studies carried out for purely scientific reasons and largely before the main growth of salmonid farming. These studies give a good picture of seasonal changes and spatial variation in coastal phytoplankton, either under natural conditions or under nutrient enriched conditions in the Firth of Clyde and its lochs. A study of Loch Hourn between 1988 and 1990, during the establishment of a farm in the inner part of the loch, showed a small but detectable increase in nutrient but no significant effect on the biomass or the 'balance of species' of the phytoplankton. A comparison between the nutrient-poor Loch Creran between 1972 and 1982 (before local fish farming) and in the nutrient-enriched Loch Striven circa 1980, shows that human-generated nutrients do cause larger blooms. The extra nutrients in Loch Striven derive largely from waste water and agricultural inputs to the Clyde and associated rivers, and greatest winter concentrations in Striven were more than twice those in Creran. Although phytoplankton abundance was highly variable in both lochs, and sometimes less in Striven than in Creran, the largest blooms in Striven were much larger than those in Creran at the same time of year.

2.32 The second sort of evidence derives from the application of mathematical models, which allow the theoretical effect of adding nutrients to sea-lochs or coastal waters to be estimated. Two types of model have been employed:

• simple 'screening' models that represent the contents of a loch or voe or coastal water as a box or bath full of water, exchanging contents slowly with the outside sea;
• sophisticated and complex models that aim to represent more accurately the water flows in coastal seas and some of the variety of organisms that make up the marine community.

2.33 Both types of models are sets of equations. The equations of screening models are simple, and can be solved 'on the back of an envelope'. The equations of the sophisticated models are complex and difficult, and can only be solved by computers, using programmes that require years of effort to render error-free. Additionally, both types of model make assumptions about some of the numbers used in the calculations and about the best way to describe the processes represented in the model. Because of such assumptions, the models are best viewed as sets of hypotheses about the workings of marine ecosystems, rather than completely realistic descriptions thereof. In general, it is wise not to rely too much on results obtained from a single model.

2.34 Prediction of the bulk effect of human-generated nutrients on phytoplankton in small water-bodies - those of the size of a sea-loch - involves calculation of the Equilibrium Concentration Enhancement (ECE) of nutrients. The ECE is the extra concentration that would occur if a steady input of nutrients were to be balanced by steady removal by seawater exchange. Use by algae is ignored. The procedure used by the Fisheries Research Service (FRS) then compares the ECE with concentrations of total nutrients at a reference site (Loch Linnhe). The procedure of the Comprehensive Studies Task Team (CSTT) considers the potential for conversion of the ECE plus background nutrients into phytoplankton: lack of light, or losses caused by dilution or grazing, can prevent such conversion. The reliability with which the yield of phytoplankton from nutrients can be predicted is improved by results from a recent SNIFFER-funded study carried out by Napier and DML and by ongoing work in the EC project OAERRE. An unresolved issue is how to take account of the dissolved organic nutrients naturally present in seawater. Both procedures depend on good estimates of the flushing rates of water in lochs and voes, and a number of Scottish and European projects aim at improving methods for such estimation. Application of the FRS procedure shows that a few sea-lochs and voes are strongly enriched with nutrients to a level where they may exceed Environmental Quality Standards. At most sites, however, relative levels of enrichment are low.

2.35 The ECE procedure can also be applied to larger water bodies, such as the Minch, and allows apportioning of observed nutrient concentrations to known sources. Depending on assumptions made about flow in offshore water, nutrients from west coast fish farms may contribute between 1 and 10% of summer concentrations in the Minch, which is one of the regions most impacted by ASP. However, nutrient levels here are most strongly influenced by inputs from the Atlantic Ocean, human-controlled discharges into the Irish Sea, and poorly understood loss processes. More sophisticated ecosystem models also predict that nutrients from fish farms make a relatively minor contribution to algal production in Scottish coastal waters.

2.36 All told, it may be concluded that the present level of fish farming is having a small effect on the amount and growth rate of Scottish coastal phytoplankton, but that this effect should not be a cause for concern, except in a few, heavily-loaded, sea-lochs.

Hypothesis 2: plant nutrients from fin-fish farms have disturbed the natural ratios of nutrient elements in sea water so favouring the occurrence of toxic species over harmless algae.

2.37 Despite many studies of algal growth in the laboratory, science is still far from understanding what controls the 'balance of organisms' in the plankton. Some broad aspects of the balance can be predicted. Those algae associated with eutrophication, Red Tides, and substantial blooms ( G. mikimotoi, Phaeocystis pouchetii, and toxic flagellates) do seem to be stimulated by nutrient enrichment and favoured by increases in ratios of nitrogen or phosphorus to silicon, but suitable physical conditions and lack of grazing must also be invoked to explain their blooms. In contrast, explanations for the fluctuations in abundance of the species of Alexandrium, Dinophysis and Pseudo-nitzschia causing the shellfish poisonings, remain speculative. The scientific literature contains little unequivocal evidence that the populations of these algae are stimulated, relative to other species, by nutrient inputs or by changes in nutrient ratios. In addition, as already mentioned, there is no clear evidence that their populations have increased in Scottish waters. Of course, absence of evidence is not the same as evidence of absence of effect.

2.38 The perturbing effect of fish farm wastes on nutrient element ratios can in most Scottish cases be shown to be small. Typical farm waste has a ratio of nitrogen (N) and phosphorus (P) of about 11:1, close to natural ratios in seawater and well within the acceptable range of ratios of 7:1 to 30:1. Thus, even where farms substantially enrich lochs or voes, they should not dangerously disturb the N:P ratio. However, farm waste contains little or no silicon (Si), so can increase N:Si ratios, especially during summer when background levels of nutrients are often low and the Spring Bloom has already drawn down silicate. Therefore, there may be some heavily enriched lochs or voes where the "safe" N:Si limit of 2.5:1 is exceeded locally, especially in the waters of the Northern Isles where nitrate is enriched by inflow from the North Atlantic. However, ECE calculations show that broad-area effects should be small and more sophisticated models show that the ratio of flagellates to diatoms is not much increased by the addition of fish farm nutrients. The concept of safe nutrient ratios is examined in Tett, P. & Edwards, E. (2002) Review of Harmful Algal Blooms in Scottish coastal waters, forthcoming report to SEPA, Stirling.

Hypothesis 3: plant nutrients from fin-fish farms have made potentially toxic algae more poisonous

2.39 Laboratory experiments show that providing algal populations with an unbalanced mixture of nutrient elements can result in an increase in the toxin content of individual cells. However, some papers report more toxin under nitrogen starvation, others, more under phosphorus starvation. A wise precaution, until more is known, would be to avoid exposing potentially toxic algae to additional nutrient stress, defined as any substantial perturbation of nutrient element ratios. The N:P ratio of fish-farm waste is typically about 11:1, close to optimal, and thus fish-farm perturbation of N:P ratios in Scottish waters is unlikely to stress algae. In contrast, the N:Si ratio may be substantially increased during summer in lochs and voes that are heavily loaded. Would this change stress cells of Pseudo-nitzschia spp. brought into the loch in natural exchange of seawater, causing them to increase their content of the domoic acid responsible for ASP? Or might it instead suppress the diatom in favour of flagellates or dinoflagellates? In any case, the effects should be local and uncommon, and the ECE calculations reported above suggest that fish farm nutrients should not result in nutrient stress in coastal waters in general.

2.40 The FRS monitoring programme allows toxin levels in shellfish to be compared with the abundance of the causative algae in water taken nearby. The ratio is highly variable for all three kinds of shellfish poisoning. Variation might be caused by changes in the toxin content of the algal cells, or result from differences in rate of capture of the cells, and accumulation of their toxins, by mussels and scallops. Algal populations might differ genetically between locations. Toxicity might change from year to year as a result of genetic re-assortment during sexual reproduction at intervals of several years. Although these suggestions can help explain apparent changes in levels of toxicity, and although fish farm nutrients seem unlikely to have a widespread effect on algal toxin content, only the development of new methods will allow the claim to be convincingly refuted. Such methods would ideally demonstrate the presence of the toxin in single algal cells.

The influence of fish farm nutrient discharges on sea loch assimilative capacity

2.41 One critical factor determining the carrying capacity of the coastal zone is oxygen availability. Oxygen is supplied through the sea surface and is transported throughout the water column by turbulent diffusion. The activities of the animals and plants and bacteria within the water column and sediments consume oxygen by the process of respiration. If respiratory demand exceeds turbulent supply, oxygen concentrations will fall and may become depleted. Even a modest reduction in oxygen concentration can effect fish and other marine animals. At most sites in Scotland, oxygen supply in surface waters is not a limiting factor. Those sites with problems tend to be located at the head of lochs where tidal currents are lowest. Such sites may experience oxygen problems during warm calm periods.

2.42 Oxygen demand is controlled, amongst other things, by the rate of supply of organic matter, some of which is provided by production of phytoplankton. Nutrients may influence oxygen demand by stimulating primary production, which in turn may be ultimately consumed by bacteria and grazing animals. Whether nutrient inputs have an influence on the carrying capacity of a coastal system depends, therefore, on whether environmental conditions exist for the phytoplankton to uptake and make use, photosynthetically, of the nutrients. In many sea lochs, because of dissolved and suspended material, light cannot penetrate to more than 10-15 m or so. Consequently the zone within the water column where phytoplankton can photosynthesise is relatively shallow and the average illumination experienced by phytoplankton is low. Modelling studies suggest that phytoplankton production is relatively insensitive to changes in nutrient supply as in many areas, production is limited by light rather than by nutrients. Thus, except where special conditions exist, i.e. where nutrients are introduced into a shallow and well-illuminated surface layer, nutrient discharges are unlikely to have a significant effect on capacity for fish farming.

Summary

2.43 Modelling studies have shown that a few sea loch sites are strongly enriched with nutrients to such a level that they might exceed environmental quality standards but, in the main, enrichments are low. It is concluded that the present level of fish farming is having a small effect on the amount and growth rate of Scottish coastal phytoplankton and that this effect should not be a cause for concern except in a few, heavily loaded sealochs.

2.44 The perturbing effect of fish farm waste on nutrient element ratios in most Scottish cases can be shown to be small. Typical farm waste has a ratio of nitrogen to phosphorus that is close to natural ratios. However, there is a possibility that because of the absence of silicate in fish foods there may be a danger of exceeding the "safe" N:Si limit of 2.5 locally at heavily enriched sites in summer when background nutrient levels are low and silicate has been drawn down by the Spring Bloom. However, modelling studies suggest that broad area effects should be small. Similarly there is no convincing evidence to suggest that changes in nutrients as a result of fish farm inputs ratios is likely to stress potentially toxic species to cause them to increase their toxicity.

2.45 Except perhaps in a few enclosed waters, enrichment by fish farm nutrients is too little, relative to natural levels, to have the various effects alleged. However, we cannot, as we would wish, always support this conclusion with data from series of measurements of nutrients, phytoplankton, algal blooms, and the presence and toxicity of harmful species, made at key sites over the several decades that span the development of the current fish farming industry.

Research Gaps

2.46 Further studies of phytoplankton abundance and species composition in some lochs originally studied before 1984 and now the site of major fish-farms;

2.47 A few key coastal sites should chosen to bring together long-term programmes of monitoring of nutrients, phytoplankton and algal toxins, and the historic and future data collected in this way should be subject to statistical analysis and compared with predictions from mathematical models; the sites should represent a range of loadings by fish farms;

2.48 Inflows of nutrients from the Atlantic Ocean and the Irish Sea should be monitored in winter and summer; such inputs are likely to change because of climate change as well as changes in nutrient enrichment of the Irish Sea;

2.49 Better understanding is needed of water movements within sea-lochs and voes, between them and coastal waters, and in coastal waters;

2.50 Studies of the biology, toxicology and ecology of Scottish populations of harmful algae, especially of Pseudo-nitzschia spp;

2.51 Development of methods capable of detecting the presence of toxins in small samples of phytoplankton - present methodology relies on analysis of shellfish tissues, and can thus provide only indirect information about toxic algae;

2.52 Better understanding of the role of pelagic protozoa in coastal waters, lochs and voes; these organisms may be crucial in preventing the development of algal blooms, yet especially sensitive to pollution with metals or pesticides;

2.53 More information on rates of loss of nutrients from Scottish continental shelf and sea-loch waters, especially concerning the process of denitrification which takes place in organically enriched sediments and which probably removes a substantial part of nutrient-N;

2.54 Continued development of simple, robust models that can predict 'undesirable disturbance to the balance of organisms and the quality of the water' as a result of inputs of nutrient and organic matter by fish farms.

ENVIRONMENTAL ASPECTS OF SHELLFISH CULTURE

2.55 Primarily small companies conduct shellfish cultivation in Scotland, the estimated first-sale value of the industry is around £5 million, not including the revenue from managed wild stocks. The recent trends are for increased overall production, an increase in the total number of operational businesses, but a slight decrease in the number of operational sites.

2.56 The main species cultivated, all bivalve molluscs, in descending order of tonnage produced are: the blue mussel, Mytilus edulis; the Pacific oyster, Crassostrea gigas; the queen scallop , Aequipecten opercularis; the king scallop, Pecten maximus and the native oyster, Ostrea edulis. Production is dominated by that of the blue mussel, both production levels and farm gate prices have risen over several consecutive years with a further substantive increase in production reported for 2001 with the expansion of cultivation in the Shetland Isles. Production of Pacific oysters has shown a smaller but consistent increase in recent years.

2.57 All these species are filter feeders, extracting the food they require naturally from the water column. Juveniles for on-growing are supplied from hatcheries (oysters) or collected from wild populations. For the blue mussel, spat can be collected in abundance and is not a limiting factor. During the grow-out phase the shellfish receive no additional feed or medication; as the cultivation processes are close to the natural mechanisms they are inherently sustainable.

2.58 There are, however, two major environmental considerations key to the sustainability of Scottish shellfish production. All bivalve mollusc production areas are classified under The Food Safety (Live Bivalve Molluscs and Other Shellfish) Regulations 1992, and areas are classified A, B or C depending on the number of faecal coliforms. The industry is, therefore, highly dependent on the maintenance of good water quality. The second major constraint on many businesses is the prevalence and duration of closures on harvesting caused by the presence of algal toxins. Most notably, with respect to mussel growers, prolonged closures caused by the presence of Diarrhetic Shellfish Poison (DSP), have threatened to close companies in north-west Scotland over the last two growing seasons. There have also been seasonal closures caused by the presence of Paralytic Shellfish Poisons (PSP). The scallop cultivation industry has been similarly effected by prolonged and widespread closures, since 1999, because of the detection of the toxin which can cause Amnesic Shellfish Poisoning (ASP). The first reports of AST (domoic acid) in king scallops from Scottish waters were coincident with the inclusion of ASP in the biotoxin monitoring programme, raising the possibility that it may in fact have been present prior to this. However, as 'shucking' or preparation of the scallop for table, leaving only the gonad and adductor mussel, removes 99% of the toxin burden in the scallop, it is unsurprising there were no reports of ASP illness.

2.59 There has been some speculation as to whether there is a link between the nutrient input from fish cultivation and the occurrence of the toxins causing DSP, PSP and ASP in shellfish from Scottish waters. There is no obvious spatial correlation between recent HAB events in Scotland and fish cultivation sites. For example AST (the Amnesic Shellfish Toxin) can be found in scallops from off-shore fishing areas as well as from those in sea lochs and the factors controlling the prevalence, duration and distribution of phytoplankton blooms, are clearly operating on a much larger scale. From laboratory study of toxin production in known AST-producing algal strains, it is clear that a change in nutrient ratios, or more specifically the limitation of a specific nutrient, can effect toxin production (see previous section).

2.60 The environmental impacts of shellfish farming in Scotland are generally considered to be minimal. Some studies on the impact of mussel culture have reported a build up of sediments, faecal and pseudo-faecal matter, which caused organic enrichment and a reduction in the diversity of macrobenthos beneath the farm. Other studies have concluded mussel culture had little impact and thus the extent of any impact is closely linked to the site-specific water movements. There are some objections to mussel cultivation on the basis of the visual impact of the floats supporting the culture ropes, although the widespread use of low profile, grey or black floats minimises the effect. Oyster culture, as conducted in Scotland, has to be considered benign, with a limited visual impact of trestles, only visible at low tides. The tonnage of the other species cultivated is still minimal.

2.61 There is awareness, however, of the need to monitor the carrying capacity of shellfish production waters, particularly in terms of phytoplankton availability. Well-documented studies from other countries have shown that intensive mussel cultivation can result in a significant negative correlation between mussel condition and the annual standing mussel stock, an indication the system is exploited to capacity. In such situations, intensive mussel cultivation will presumably be having an impact on other suspension feeders and throughout the food web. Current models for shellfish cultivation predict and optimise exploitation capacity but there is scope for studying nutrient flux, habitat degradation and deposition below suspended systems.

2.62 To avoid pronounced shifts in coastal processes, conversion, and not dilution, is promoted as the common sense solution to the issue of the additional nutrient loading that results from fish cultivation. By integrating 'fed' aquaculture with inorganic and organic extractive aquaculture (seaweed and shellfish), the wastes of one resource user become a resource (fertiliser or food) for the others. Asian countries, which account for more than two thirds of the world's aquaculture production, have been practising integrated aquaculture for centuries, whereas Western countries and the more rapidly expanding parts of the Asian aquaculture industry tend to focus on high value, high production monoculture.

2.63 The potential benefits of integrating seaweed / shellfish and finfish cultivation, with the aim of mitigating the effects of the latter are now recognised and being researched in Scotland. There have been several studies investigating the potential benefits of cultivating mussels alongside Atlantic salmon in Scottish sea lochs. Shell and tissue growth of mussels associated with salmon farms were found to be significantly augmented, but the variation of growth rates between lochs was greater than that within lochs, underlining the need for a better understanding of the interaction of site specific characteristics, primary productivity and carrying capacity at an ecosystem level.

2.64 There is now a consensus that at least 80% of the total nitrogen lost from fish farms is available for uptake by marine plants (both phytoplankton and macroalgae) and that fish excreta and waste fish food provide well-balanced nutrients for algal growth. As macroalgae can take up nitrogen from seawater at rates sufficient to support increases in biomass of up to 9-10% a day, they are regarded by some as important, renewable, biological nutrient scrubbers. As such, the potential benefits of their integration to fish cultivation sites is worthy of further attention.

2.65 The use of non-native species is one aspect of the cultivation of non-fish species that could potentially have negative environmental impacts. In some scenarios the risk of introducing disease to native species is of as much concern as any deleterious impacts of the species introduced.

Summary

2.66 The cultivation of non-fish species has few measured, negative environmental impacts, and those that have been recorded are restricted to the vicinity of the farm site. As this type of culture extracts nutrients from the marine system, carrying capacity considerations should be focussed on the extent to which the environment can supply these nutrients. It is likely that the cultivation of non-fish species can, to some extent, help reduce nutrient inputs from other activities including fish culture.

Research Gaps

2.67 A fuller understanding of the interaction of suspended-culture mussel populations with other components of the ecosystem, in terms of their scope for growth (phytoplankton availability), their impact on other suspension feeders in the food web and the potential for nutrient release from accumulated biodeposits is required.

2.68 Such studies should be linked to the development of models to assist in calculation of appropriate stocking densities for each bivalve cultivation area and the identification of sites where mussel cultivation could be practised to advantage.

2.69 Fuller study of the potential benefits of integrating aquaculture species is required, using a combination of nutrient extracting species on site with nutrient enriching species, with a view to increased productivity in the former and a net reduction in nutrient release from the latter.

2.70 There is a need to improve our understanding of the mechanism of toxification and depuration of AST in commercially valuable species such as the king scallop. There is little information at present on the levels and mechanisms of production of domoic acid in Pseudo-nitzschia species isolated locally, the reason for prolonged toxin retention in king scallops or the potential impact of the AST on shellfish physiology, fecundity and recruitment.

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