1.0 INTRODUCTION
Outbreaks of harmful algal blooms ( HAB) have occurred in Scottish coastal waters causing Amnesic Shellfish Poisoning ( ASP), Diarrhetic Shellfish Poisoning ( DSP) and Paralytic Shellfish Poisoning ( PSP). These shellfish-borne illnesses compromise human health, resulting in fishery closures, commercial losses, and concerns over seafood safety and environmental quality. They have also stimulated local debate over the causes of HABs and whether they have increased in frequency. Shellfish producers and other parties have concluded that marine fish farming is the most probable primary cause of these HAB events. Staniford (2002a) has stated: " the evidence pointing to a causal link, in certain areas, between toxic algal blooms and salmon farming is surely now beyond reasonable doubt". Berry (1999) has claimed a clear link exists between blooms of domoic acid ( ASP causative) producing species (and other HAB species) and nutrient wastes discharged from fish farms, particularly in nitrogen, an essential nutrient required by HAB species and phytoplankton generally. He has argued that aquacultural nitrogenous wastes in altering natural nitrogen concentrations, their seasonal and annual cycles, and ratios with other essential phytoplankton nutrients, stimulate harmful blooms. The evidence adduced in support of aquacultural stimulation of HABs is based on estimates of the amount of waste nutrients discharged at fish farms, and the controversial view that anthropogenically facilitated increases in nutrient supply is a primary and direct trigger of harmful blooms. The magnitude of aquacultural wastes discharged into Scottish coastal waters and their potential impact on altered phytoplankton behaviour and HAB events is a legitimate cause for concern. MacGarvin (2000) reported that in year 2000 Scottish aquaculture released ca. 7,500 tonnes N and 1,240 tonnes P, amounts comparable to the annual sewage input of ca. 3.2 million and 9.4 million people, respectively. In 1997, Scotland's population was 5.1 million. The evidence mustered by adherents to support the aquacultural stimulation hypothesis combines MacGarvin-type estimations, circumstantial evidence and extrapolations based on insights obtained from the scientific literature. Although the approach followed is primarily anecdotal, the concern is nonetheless a legitimate one.
Tett and Edwards (2002) and SE (2002), based on more rigorous scientific analysis of historical bloom patterns, including application of ecophysiological data and ecological principles, came to the opposing view. They concluded that there is no causative correlation between nutrient enrichment of Scottish coastal waters, estuaries, sea lochs and voes, and HAB occurrences and effects. Some stakeholders, including shellfish producers and environmentalists, have resisted extrapolation of this conclusion to aquacultural impacts on HABs, which has spawned intensifying debate over the impact of marine fish farming on HAB occurrences in Scottish coastal waters. This disagreement may not be surprising, since it applies different methodology in seeking to resolve whether less desirable ecosystem responses that can occur in parallel with anthropogenic activities are unconnected behavior, or are cause-and-effect responses amenable to mitigation and environmental engineering practises, should cessation of the presumed anthropogenic activity be impractical.
In response to this controversy, and to obtain an impartial analysis of the data, the SE Water Division commissioned two independent, external reviews of whether there is a linkage between Scottish aquaculture and algal blooms. Dr. Lars Rydberg and his group from the University of Gothenburg, Sweden, and Dr. Ted Smayda of the University of Rhode Island, U.S., were commissioned as external reviewers. Neither has been funded previously by industry or government sources from within Scotland. The report by Dr. Rydberg and colleagues is found in Rydberg et al. (2002). Seven primary questions were assigned to Dr. Smayda for review, and are the subject of this report:
• Review current knowledge on the occurrence of algal blooms (harmful or otherwise) in Scottish coastal waters.
• Assess the impact of nutrient inputs from fish farms on the algal communities of the Scottish coastal zone in comparison with regional seas.
• Evaluate the primary factors controlling the occurrence of algal blooms in the coastal waters of Scotland.
• Assess whether fish farming contributes to algal blooms in Scottish coastal waters, and if so, how.
• Assess whether the postulated link between fish farming and harmful algal bloom occurrences is supported by the available evidence.
• Assess whether fish farming is a factor in the presence of ASP/ PSP, even where eutrophication is not an issue, and
• Where there is insufficient knowledge to answer the above questions, recommend additional steps to determine whether or not the potential link exists.
Dr. Rydberg's group also reviewed these questions (Rydberg et al., 2002), except that in addressing the 2 nd question they were to focus on individual sea lochs, while Dr. Smayda was to follow a regional seas approach.
The present review was carried out partially utilizing published and unpublished material provided by the SE Environment Protection Unit and scientists who have researched Scottish coastal waters (see Acknowledgments). More than 850 papers published in refereed journals were reviewed; of these, ca. 650 have been cited and referenced in this report. Relevant papers were identified using standard bibliographic search instruments. It is believed that the essential documents available in the "open" scientific literature relevant to this review were consulted. The excellent review of Tett and Edwards (2002) is sometimes cited as the "authority" in lieu of the primary literature where duplication of effort would have made analysis of the topic redundant. Following completion of the review of the aquacultural impacts on HAB behaviour and environmental conditions in Scottish coastal waters, an organismal approach was applied in the regional HAB analyses and in dealing with the utilization of aquacultural nutrient wastes by harmful algal species. Since blooms of ASP, DSP, PSP and ichthyotoxic species are species-specific events, the autecology of the individual species falling within these groups, and found in Scottish waters, were focused on. The regional comparison was interpreted broadly to include global bloom occurrences of the harmful species in question whether, for example, they occurred in Norwegian or New Zealand coastal waters. Although the associations between HABs and aquaculture have site-specific features, the generic relationships between HABs and aquaculture transcend local behavior. Associations between HAB events and aquacultural activities in distant regions are analogues of events that can occur elsewhere. For example, potential HAB responses to nitrogenous waste discharge at a given site reasonably can be expected to occur elsewhere once similar thresholds are reached. This axiom holds since the basic nutrient requirements and biochemical pathways of nutrient physiology are common traits among HAB species. The relationship between aquaculture and HABs in northern European waters was the focus in the regional comparison.
I have applied a general principles approach in evaluating the observed and expected behavior of HAB species in Scottish coastal waters. This perspective was followed because phytoplankton have evolved and adapted to oceanic conditions in general, and not to a specific location, such as Loch Linnhe. I have also applied the view that Scottish waters, as elsewhere, are "open systems"; i.e. oceanographic processes and climate influence the long-term patterns and episodic blooms of both HAB species and phytoplankton generally. The confluence of such natural phenomena with aquacultural initiatives can make it difficult to distinguish anthropogenically induced changes from natural behaviour and events. This ambiguity has partly fueled the debate over the hypothesized aquacultural stimulation of HABs in Scottish coastal waters. The "open systems" concept is applied as a baseline to assess the extent to which HAB events and aquacultural activites in Scottish coastal waters may be linked. The analyses consider the spatial and temporal heterogeneity of harmful blooms, and the variability in toxicity found among strains of the same species.
This report is submitted as a scientifically based evaluation restricted to the issues specifically assigned for review by the SE Environment Protection Unit. It is not offered, nor should be perceived as an evaluation of fish farming and shellfish aquaculture as an industry, or an assessment of the environmental and public health issues currently under debate in Scotland or elsewhere (see Staniford, 2002b).
Acknowledgements
I acknowledge the generous help of Dr. Liam Kelly, Project Officer, during all phases of this study, and his considerable patience extended to me when unforeseen circumstances delayed earlier completion of this report. Dr. Paul Tett kindly provided reprints of his published and unpublished reports, as did Dr. Richard Gowen. This report also benefitted from very helpful discussions with Dr. Tett, Dr. Gowen, Dr. Lars Rydberg, and Dr. Richard Parke at an ICES Workshop on Eutrophication convened in The Hague. Dr. Ian Davies provided information on fish farm nutrient inputs into sea lochs.