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Marine Estate Research Report

Alternative marine sources of protein and oil for aquaculture feeds: State of the art and recommendations for future research

Alternative marine sources of protein and oil for aquaculture feeds: State of the art and recommendations for future research
Contract reference: AQU/06/02

Technical Report

December 2006 by Thomas A. Wilding, Maeve S. Kelly, Kenneth D. Black

SAMS Research Services Limited, Dunstaffnage Marine Laboratory, Oban, Argyll, Scotland. PA37 1QA

Wilding et al (2006)

Alternative marine sources of protein and oil for aquaculture

ADMINISTRATION PAGE Contract reference: AQU/06/02, period: January December 2006. Report version: Final. Queens Printer for Scotland, 2006.

ISBN (10): 0-9553427-4-0

ISBN (13): 978-0-9553427-4-5

Published by The Crown Estate on behalf of the Marine Estate. Dissemination statement: This publication (excluding the logos) may be re-used free of charge in any format or medium. It may only be re-used accurately and not in a misleading context. The material must be acknowledged as Crown Estate copyright and use of it must give the title of the source publication. Where third party copyright material has been identified, further use of that material requires permission from the copyright holders concerned. This report is available from The Crown Estate website www.thecrownestate.co.uk Disclaimer: The opinions expressed in this report do not necessarily reflect the views of The Crown Estate and The Crown Estate is not liable for the accuracy of the information provided or responsible for any use of the content.

Suggested citation: Wilding, T. A., Kelly, M. S. and Black, K. D. (2006) Alternative marine sources of protein and oil for aquaculture feeds: state of the art and recommendations for further research. The Crown Estate, 63 pages, December 2006. ISBN (10): 09553427-4-0, ISBN (13): 978-0-9553427-4-5.

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Alternative marine sources of protein and oil for aquaculture

CONTENTS ADMINISTARATION PAGE ................................................................................ i CONTENTS.........................................................................................................ii LIST OF ABBREVIATIONS................................................................................ iv LIST OF TABLES ...............................................................................................iv LIST OF FIGURES.............................................................................................iv EXECUTIVE SUMMARY.................................................................................... 1 1. INTRODUCTION............................................................................................ 3 2. FEEDING FARMED FISH: THE UK IN A GLOBAL CONTEXT...................... 4 2.1 Fishmeal and fish-oil .............................................................................. 4 2.2 UK fish-farming industry in context .................................................... 10 2.3 Fish-feed requirements and constituents........................................ 11 3. ALTERNATIVE SOURCES OF PROTEIN AND OIL .................................... 12 3.1 Higher plants......................................................................................... 12 3.1.1 Rape / canola ................................................................................... 13 3.1.2 Peas and lupins................................................................................ 15 3.1.3 Linseed............................................................................................. 15 3.1.4 Soya ................................................................................................. 16 3.1.5 Maize gluten meal ............................................................................ 17 3.2 By-products........................................................................................... 18 3.3 Single cell culture (including marine algae)....................................... 18 3.4 Marine sources ..................................................................................... 20 3.4.1 Copepods......................................................................................... 21 3.4.2 Krill ................................................................................................... 22 3.4.3 Fisheries by-products ....................................................................... 24 3.4.4 Mussels............................................................................................ 26 3.4.5 Marine worms................................................................................... 28 3.4.6 Marine plants.................................................................................... 29 4. REALISTIC POSSIBILITIES FOR THE UK INDUSTRY............................... 34 5. IMPLICATIONS FOR THE UK FISH FARMING INDUSTRY........................ 35 5.1 Product quality - taste, texture, appearance and shelf life................ 35 5.2 Nutritive value and implications for human health............................ 37 ii

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5.3 Fish husbandry and welfare ................................................................ 39 5.4 Implications for organic producers..................................................... 39 6. RECOMMENDED RESEARCH AVENUES AND PRIORITIES.................... 43 7. REFERENCES............................................................................................. 45 8. APPENDICES .............................................................................................. 53 Annex 1 Annex 2 Annex 3 Predicted changes in fishmeal usage in aquaculture diets .. 53 Predicted changes in fish-oil usage in aquaculture diets ..... 54 Plant derived anti-nutritional compounds, their sources,

effects and remediative methods (Francis et al. 2001).......................... 55 Annex 4 Annex 5 Dry weight (DW %), protein, lipid, fiber, ash and starch Crude nutrient profile of the polychaete Nereis virens (data content of various pea products............................................................. 58

from Dragon Feeds Limited) .................................................................. 58 Annex 6 Organisations contacted ...................................................... 59

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LIST OF ABBREVIATIONS Abbreviation/ acronym BTA DEFRA Meaning British Trout Association Department of Environment, Fisheries and Rural Affairs EFA FIN HUFA IFFO MSC OFF POC POP PUFA SOFIA SSPO LIST OF TABLES Table 1 Projected Scottish aquaculture output and fishmeal consumption .. 9 Table 2 Production of farmed finfish, by species, in the UK ....................... 10 Table 3 Crude breakdown (protein and oil) in various feed formulations.... 12 Table 4 - Example studies using seaweeds in fish diets. .............................. 32 LIST OF FIGURES Figure 1 - Proportions of fishmeal and fish-oil used in different agricultural and industrial sectors ...................................................................................... 5 Figure 2 The proportions of fishmeal and fish-oil used in different aquaculture sectors (for 2003, from Tacon 2005) ........................................................ 5 Figure 3 Global trends in fishmeal and fish-oil usage in salmon feed over the period 1992 2003 (from Tacon 2005) .................................................... 7 essential fatty-acid Fishmeal information network highly unsaturated fatty acid International fishmeal and fish-oil organisation Marine Stewardship Council Organic Food Federation protein omega concentrate persistent organic pollutant polyunsaturated fatty acid State of world fisheries and aquaculture (report by the FAO; Anon, 2006) Scottish Salmon Producers Organisation

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EXECUTIVE SUMMARY Fish-farming, particularly of salmon, forms an important part of the Scottish rural economy and makes an important fiscal contribution to The Crown Estate. Scottish fish-farmers currently feed their fish a diet that is predominantly derived from fishmeal and fish-oil. There is growing concern regarding the ecological sustainability and concomitant price stability of these commodities and, consequently, many of the UKs competitors in salmon production are increasing the proportion of terrestrial plant oil and protein in their fish-feeds. There is currently resistance from the UK retailing sector to follow suit and certain markets, particularly the French, pay a premium for fish fed on natural diets. There is, therefore, interest in sourcing alternative marine sources of protein and oil that will maintain the product price-premium without reliance on unsustainable industrial fisheries. Krill and copepods were identified as offering the most potential as a bulk source of marine oils and proteins for inclusion in aqua-feeds. However, there are issues regarding the ecological impacts of new fisheries for krill and copepods and their economic and technological viability. The existing krill, and inchoate copepod, fisheries are currently limited by technological problems in harvesting (copepods) and post-catch processing and fluoride contamination (krill). These issues need to be resolved before the fisheries can make a substantial contribution to existing aqua-feed supplies. There is potential for improved utilisation of waste from other sectors of the aquaculture and capture industries particularly in relation to prawn and shrimp waste. The effectiveness of mussel meal and polychaete worms in fish diets should also be further investigated as the rising price of fishmeal and recent advances in culture methods (polychaetes) means they might become more financially realistic options in the future. The organic sector essentially faces the same challenges as the mainstream producers, and there is recognition from the certifiers that organic fish diets will ultimately contain ingredients from a greater diversity of sources and they do not rule out the possibility of including vegetable products and adding EPA/DHA or proteins from microbial fermentation, providing no GM organisms are involved in their production. The future direction of the UK fish-farming industry is dependent on both fishmeal and fish-oil commodity prices and on competition from other producers - both these variables are highly unpredictable. Fishmeal and fish-oil prices may stabilise as the majority of the industry moves to non-marine ingredients or may continue to increase as aquaculture expands in the Far East. This will, in turn, dictate when, and the extent to which, the UK industry utilises vegetable components in fish diets. In the meantime, further research into marine alternatives remains key to the development of more natural diets with the capacity to provide the essential fatty acids essential to the marketing of salmon. 1

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Recommendations 1) that the industry should finalise standards that guarantee minimum EFA content to assure consumers that the health benefits of farmed salmon remain, regardless of diet 2) establish the minimal fishmeal and fish-oil content for use in salmonid diets that maintain product quality including EFA levels 3) that profitability projections be made to establish the cost threshold at which marine alternatives to fish-oil and fishmeal become viable 4) concurrently (with 2 and 3) assess consumer acceptability of fish reared using alternative marine and non-marine feed sources 5) determine if a sustainable brand is a marketing tool, both in terms of a switch to plant-based alternatives and sustainably sourced fishmeal and fish-oil 6) determine the consumer attitudes towards genetically modified salmon and salmon feed constituents If it is found that the consumer is willing to pay a considerable premium for fish fed natural diets then it may be economic to utilise alternative marine source of oil and protein. We recommend that research into the following areas be conducted, in order of priority: 7) establish the broader ecological implications of developing/ increasing copepod and krill fisheries including methods of preservation and contamination-minimisation 8) the determination of whether zooplankton oil is equally effective at all developmental stages of salmon 9) methods of maximising the utilisation of waste from other fishing and aquaculture industries 10) the economics, logistics and environmental compatibility of utilising cultured mussels and worms

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1. INTRODUCTION Aquaculture makes an important contribution to global fish supplies, currently standing at 24 % of the total landed tonnage and increasing at 8.9 % per annum since 1970 (FAO). It is estimated that aquacultural production will meet 50% of the worlds fish demand by 2030 (FAO). Some sectors of the aquaculture industry are highly dependent on wild-caught fish (forage-fish) as they form the basis of the feed-stocks. Growth in the forage-fish dependent sector has contributed to an increasing demand on the forage-fish stocks and there are now concerns regarding their sustainability. These concerns were addressed in a recent review by the Royal Commission on Environmental Pollution (RCEP) (Anon 2005) which identified the feeding of forage fish to farmed fish (fishing down the food-web Pauly et al. 2002) as potentially unsustainable and identified a number of alternative fish-feed constituents. Research into sourcing alternatives to fishmeal and fish-oil has been ongoing for over 20 years (Trushenski et al. 2006) in the expectation of a rise in fishcommodity prices. The predicted rise in fishmeal and fish-oil price has certainly occurred, particularly during 2006, where prices have already (January to June) increased by 30% predominantly as a consequence of a buoyant Chinese market (FIN, 2006). A review of the ongoing research into alternatives is, therefore, both pertinent and timely.

In order to assess the likely vulnerability of the UK fish-farming industry to increased feed costs we firstly review the current global trends in fishmeal and fish-oil utilisation/price and the status of the forage-fish stocks from which these commodities are derived. Following this, we establish the main dietary requirements of farmed fish and comment on how these are currently being met. We then review the current knowledge with regard to terrestrial and, particularly, marine alternatives to fishmeal and fish-oil. A synthesis of this information, derived from both academic sources and industry contacts, was used to identify research needs and make recommendations.

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2. FEEDING FARMED FISH: THE UK IN A GLOBAL CONTEXT The UK is one among many nations that hosts a fish-farming industry. This industry, once small-scale and operated by numerous small companies, is now largely operated by a small number of multinational companies. The fish-feed used in UK operations is sourced from large multinational companies and their subsidiaries (BioMar, EWOS, Skretting; (Huntington 2004) many of which produce feeds for a range of farmed animals and who are significant buyers on the international feedstock market. These manufacturers have a commercial interest in maximising the cost-effectiveness of their products and are at the forefront of research into fishmeal and fish-oil replacement. 2.1 Fishmeal and fish-oil Fishmeal and fish-oil are commodities derived from processed whole-fish, fish trimmings or offal. The bulk of the world's fish meal and oil is manufactured by the wet pressing method which involves various cooking and separation stages to yield a press-cake containing 60-80% of the oil-free dry matter (protein, bones), an oil and an aqueous liquid phase which is concentrated and added to the meal. Fishmeal and fish-oil are both variable products with a specification that is dependent inter alia on source, season and location (FAO 1986). In 2003, it was estimated that around 22% (29 million tonnes) of the total global wild-fishery catch (of 103 million tonnes) was used in the manufacture of fish meal and fish oil (Anon 2004).

Fishmeal and fish-oil are primarily used in the manufacture of feed stocks for a wide range of farmed animals including fish. The global aquacultural feed sector uses 46 and 81% of the available fishmeal and fish-oil respectively (Pike, 2005 cited in Tacon 2005) (Figure 1).

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Others 7% Poultry 22% Ruminants 1%

Industrial 5% Edible 14%

Pigs 24%

Aquaculture 46%

Aquaculture 81%

Fishmeal

Fish-oil Edible - dietary supplements Industrial refers to commodities such as lubricants

Figure 1 - Proportions of fishmeal and fish-oil used in different agricultural and industrial sectors

Of the total fishmeal used in aquaculture diets, 27% goes for crustacean feeds, equal parts (20%) go to salmon and marine fish and the remainder goes to carp, trout, eel, milkfish, tilapia and catfish (Figure 2; from Tacon (2005)). Of the oil, 51% and 15% goes into salmon and trout feeds respectively (Figure 2).
Catfish 1% Marine fish 20% Tilapia 3% Milkfish 1% Other 18% Carp 15% Eel 6% Trout 7%

Trout 15%

Salmon 20%

Marine fish 14%

Crustaceans 9% Catfish 1%

Other 20%

Tilapia 2% Carp 6%

Crustaceans 27%

Salmon 51%

Milkfish 1% Eel 1%

Fishmeal sectors (for 2003, from Tacon 2005)

Fish-oil

Figure 2 The proportions of fishmeal and fish-oil used in different aquaculture

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The status of forage-fish stocks is currently under considerable scrutiny as the resource is an important part of the human-food supply chain (Figure 1) and any unsustainable exploitation of the stocks has considerable economic and ecological implications. Forage fish tend to be short lived, highly fecund pelagic species that are low in the food chain (Huntington 2004). Such species are able to sustain large fisheries and show large natural population fluctuations under climatic drivers such as the North Atlantic- and El Nino-Southern-Oscillations. Forage-fish species in the NE Atlantic include capelin, blue whiting, sandeel, sprat, herring and Norway pout and, from South America, anchovy, jack mackerel, horse mackerel and sardines (Shepard et al. 2005). A majority of forage-fish are caught in the waters around South America (IFFO).

Of the forage-fish stocks, the blue whiting is considered particularly threatened (Huntington 2004; Shepard et al. 2005) and, whilst the long-term consequences to the marine mammals and seabirds that depend on these species for food remain uncertain (Huntington 2004), current fisheries models indicate that forage-fishing may be significantly reducing higher trophic level (more valuable) capture-fisheries (Hannesson 2003). Although forage -fisheries are closely monitored and a majority are sustainably fished, according to the International Fishmeal and Fish-oil Organisation (Shepard et al. 2005), Naylor et al (2000) concluded that aquaculture must move away from marine-sourced feeds if it is to remain a useful net contributor to global fish protein supplies.

Sustained growth in the aquaculture sector has seen the amount of fishmeal utilised in salmon feeds increase from approximately 200,000 tonnes in 1992 to a maximum of around 600,000 tonnes in 2001. The demand for fishmeal for use in salmon feeds appears to have stabilised and is currently approximately 550,000 tonnes per year (Figure 3). The demand for fish-oil has shown an even greater rise over the same period, increasing more than six-fold from approximately 60,000 to 400,000 tonnes, over the same period, with no

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apparent stabilisation in demand (Figure 3).


700

Thousand tonnes

600 500 400 300 200 100 0

Fishmeal Fish-oil

1992 1994 1995 1998 1999 2000 2001 2002 2003

Year
Figure 3 Global trends in fishmeal and fish-oil usage in salmon feed over the period 1992 2003 (from Tacon 2005) Much of the observed trend in fishmeal and fish-oil use has occurred as the industry has moved towards a higher inclusion rate of oil in salmonid diets. This has occurred because oil is a superior source of energy, promoting faster growth (Tacon 2005). This trend has now reversed, over the salmonid diet sector as a whole such that Huntington (2004) predicts a decrease in fishmeal and fish-oil inclusion in salmon feeds over the period 2000 - 2010 to 75% and 80% of their current levels respectively. However, despite the reductions in the proportion of fishmeal and fish-oil used in salmon feed, both Huntington (2004) and Tacon (2005) predict overall increases in the demand for both fishmeal and fish-oil primarily as a consequence of the growth in carp aquaculture along with the expansion of a broad range of marine species including bass, bream, grouper, yellow tail, carangids, mullet, flounder, turbot, halibut, cod, sole and hake. This is projected to result, by 2010, in the aquaculture sector taking 85% of global fish-oil production (Huntington 2004).

In the UK, aquaculture production (predominantly Atlantic salmon) has been projected to increase to 116% of current levels into the next decade (Table 1), but with an overall decrease in the reliance on fishmeal. The increased 7

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production and decreased utilisation of fishmeal stems from a projected 10% decrease in the fishmeal content present in aquacultural feed including that for salmon.

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Table 1 Projected Scottish aquaculture output and fishmeal consumption (all units in thousand tonnes unless otherwise specified, from Huntington 2004). Year Species Fish production Feed consumption

2003
Fishmeal Content Fishmeal consumption Fish production Feed

2010
Fishmeal content Fishmeal consumption

consumption

Atlantic salmon Rainbow trout Marine fish Freshwater fish Total

177.6 6.5 0.4 0.4 183.9

215.4 18.7 2.8 1.1 238.0

45% 45% 55% 45%

96.9 8.4 1.6 0.5 107.3

180.0 10.0 3.0 20.0 213.0

250.1 22.3 17.5 2.5 292.4

35% 30% 40% 40%

87.5 6.7 7.0 1.0 102.2

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On the basis of 80% of fish-oil being directed to aquacultural feeds (Figure 1) of which 50% is used for salmon (Figure 2) of which 10% are farmed in the UK, the UK aquaculture sector accounts for 4% of fish-oil consumption. This indicates that reductions in fish-oil utilisation within the UK fish-farming sector will have only a marginal effect on the global demand and price of fish-oil. However, the UK fish-farming industry is still vulnerable to externally driven fluctuations in the price of fish-oil. Circumstances resulting in shortages of fish-oil, for example, following El Nino events (Naylor et al. 2000), have already caused substantial price fluctuations (rises) in fish-based commodities and, more recently (2006), price rises have occurred through increased demand from the rapidly growing economies of the Far East, particularly China. Whatever the reasons, the dependence of the UK fish farming industry on fish-commodity based feeds threatens its viability and it is responding by developing substitute ingredients for use in salmonid feeds. 2.2 UK fish-farming industry in context The UK finfish aquaculture business, which produces ca 30% of the total European output, is dominated by marine-based salmon culture (Table 2; The Crown Estate, pers. comm., 2006 unless otherwise specified) contributing 10% of world salmon production. Fresh-water trout production adds an additional 17,000 tonnes to this total (D. Basset, BTA, pers. comm., 2006). Table 2 Production of farmed finfish, by species, in the UK Species Salmon Halibut Cod Sea trout Trout (seawater) Trout (freshwater)** Total Production (tonnes) *112,000.00 34.43 58.56 1.72 783.53 17,000.00 129,878.24 Percentage 86.23 0.03 0.05 <0.01 0.60 13.09 100

* - estimated maximum tonnage, this excludes fresh-water trout. ** -data from the British Trout Association 10

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The UK fish-farming industry supplies both the home market and Europe, particularly France, where Scottish salmon can attract a premium price. The marketing strategy adopted by Scottish fish-farming industry has been to promote the naturalness of the product. This has resulted in the establishment of a number of standards that guarantee, inter alia, minimum fish-inclusion in dietary formulations. These standards currently limit the degree to which UK salmon farmers can accept alternatives to fishmeal and fish-oil in their salmon feeds. A large part of the challenge in reducing the reliance on fish-oil in the UK salmon industry is to re-educate retailers in order that they accept salmon fed a diet containing fish-replacements and to develop quality assurance schemes that assure the consumer base. This would enable the UK industry to adopt the fish-commodity substituted diets that are already used in other major salmon producing countries, such as Norway, Chile and Canada, and reduce their reliance on fishmeal and fish-oil. Resolution of these issues is central to the ongoing success of the UK fishfarming sector and is further discussed in Section 5. 2.3 Fish-feed requirements and constituents Salmon and trout are predators and, in the wild, prey upon a range of crustacea and fish. Early attempts at farming salmonids utilised feeds made using ground fish, a formulation which continues in the UK, albeit with changes in production techniques. Such diets are highly palatable, supply all the nutrients (possibly to excess) and result in both the rapid growth of the cultured stock and excellent product quality. In addition, fish-based feeds are amenable to automated feed systems and can be designed to benefit fish culture in both recirculating and open systems.

The bulk of salmon food, used in the UK, consists of fishmeal and fish-oil. Fishmeal is mostly protein but also contains the trace micro-nutrients, essential amino acids, vitamins and minerals required for fish health. The most efficient source of energy, for fish such as salmon, is oil and a large proportion of the oil in commercial feeds is simply catabolysed to provide energy for growth (Bell 2005). Salmon feeds must contain an adequate 11

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supply of essential polyunsaturated fatty acids (PUFAs) and, in particular, eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), as the fish have limited ability to synthesise these de novo, particularly post-smolting (Sargent et al. 1995; Bell et al. 2001; Tocher et al. 2003). These essential fatty acids are prevalent in fish-oil but are lacking in vegetable based alternative oils. The effect of dietary deficiencies in fatty acids are particularly apparent during stressful phases of the life-cycle of salmon, including smolting (Sargent et al. 1997) and pathogenic challenge, and are characterised by increased mortality rates. Table 3 Crude breakdown (protein and oil) in various feed formulations (from Huntington 2004). FCR feed conversion ratio (feed weight to fresh weight). Feed type Salmon starter diets Salmon grower diets Trout starter diets Trout grower diets Other marine Other freshwater % protein 50 55 34 50 50 57 38 50 50 60 31 55 % oil 14 23 22 38 14 22 8 33 12 24 7 18 FCR 0.90 1.00 1.20 1.30 0.80 0.95 0.90 1.30 1.10 1.40 1.10 1.40

From the UK feed producers perspective, the challenge is to increase the marketability of feeds that contain alternative ingredients. 3. ALTERNATIVE SOURCES OF PROTEIN AND OIL Several research avenues are currently being investigated to find fish-feed formulations that reduce their reliance on fishmeal and fish-oil. The main candidate substitute ingredients are terrestrial plants, single celled sources and alternative marine animals and plants. 3.1 Higher plants Plant derived proteins and oils, for use in feed-stocks, are produced in quantities that far exceed that derived from fisheries. There is widespread 12

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acceptance of the use of such materials as a feedstock and, already, plant derived proteins and oils are extensively used in salmon feeds outside the UK (I. Carr, EWOS, pers. comm., 2006). Plants are under continuous grazing pressure from herbivores and, as a consequence, have evolved a variety of defence mechanisms. Of the range of defence mechanisms adopted the chemical deterrents are most relevant to this review. These secondary plant products are designed to reduce grazing by a broad-spectrum of herbivores and many of them are effective in this role against fish (Annex 3). Despite this, there are currently a number of terrestrial plants which are either increasingly being used, or show considerable potential for use, as alternative sources of protein and oil for use in fish feeds. These include rape, peas and lupins, linseed, soya and maize. A majority of the problematic secondary plant products are present in the meal, rather than the oil, and these vary between species (Annex 3). For the purposes of this review, each source is considered separately, although it should be noted that a majority of existing aqua-feed formulations contain a blend of meals and oils dependent on their price, specification and availability. 3.1.1 Rape / canola Oilseed rape (Cruciferae) is widely grown for the seeds, which are pressed to produce a filtercake and oil both of which are highly useful and valuable commodities. Canola is simply a variety of rape that contains low amounts of glucosinolate, the group of antinutrients that characterise the Crucificerae family (Annex 3). Canola meal has an essential amino acid profile that makes it ideal for inclusion in a range of agrifoods including fish-feeds. Whilst many aquafeeds already contain considerable quantities of canola meal and oil, particularly those destined for freshwater fish, further research is required to resolve problems stemming from the presence of antinutrients, in particularly phytic acid. Phytic acid is a phosphorous-containing compound considered to have some beneficial effects in human diets, but which acts to reduce digestive 13

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absorption of some minerals and amino acids in fish, such as salmon, by binding to them and thus removing them from solution (Annex 3). Salmon, lacking the enzyme phytase, are unable to digest phytic acid and it is egested with other faecal material into the surrounding water. The resultant elevated phosphorous concentrations have major implications for water quality, particularly in re-circulating systems such as hatcheries (Satoh et al. 2003). There are several avenues being pursued to address the phytic acid problem in canola. This includes plant breeding programmes to reduce the phytate concentration at source, supplementing diets with the enzyme phytase and the maximisation of the efficacy of processing and production techniques in order to eliminate as much of the phytic acid as possible.

Canola oil contains high concentrations of 18:1 (n-9) and 18:2(n-6) fatty acids (in proportions that make it considered beneficial for human health) but low concentrations of the longer chain 20:5(n-3) and 22:6(n-3) highly unsaturated fatty acids (HUFA; see 5.2) (Opsahl-Ferstad et al. 2003). Despite the deficiencies in HUFAs, Wonnacott et al. (2004) has demonstrated similar growth and survival rates between seabass fed on canola oil diets compared to fish-oil based controls and Bell et al. (2003) comments that canola oil should be sufficient for salmonid well-being (growth and survival) provided the essential fatty acids (EPA and DHA) are supplied, potentially as oil-residues associated with fishmeal. More recently Higgs et al. (2006) has demonstrated, in salmon, that a blend of canola oil and poultry fat (1:1) can be used to replace 60% of fish-oil with no loss of product quality (except in the important issue of HUFAs content in the end product, see 5.1) while Carter et al. (2003) has shown that essential fatty acid requirements of salmon parr could be entirely met by canola oil. The change in flesh fatty acid content where fish are grown on diets containing high concentrations of vegetable oil has also been observed in red seabream (Glencross et al. 2003) and reductions of these important fatty 14

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acids in the final product will be a recurrent research theme in vegetable oilbased diets in marine fish. This has important implications for product marketing (see sections 4. and 5.1). However, a finishing diet containing increased concentrations of fish-oil results in the recovery of the beneficial oils in the flesh of seabream (Glencross et al. 2003) and salmon.

3.1.2 Peas and lupins Peas and lupins (Leguminosae) both offer considerable potential for inclusion in salmonid feeds. Peas contain high levels of starch and protein and can be variously processed to produce a range of meals with protein concentrations up to 76%. Whilst the protein fraction is suitable for use in fish-feeds salmonids cannot digest the starch unless the pea is treated. In terms of salmonid feedstocks, the concentrated protein product shows greatest potential. Indeed, it has been shown that it can replace at least 33% of fishmeal with no discernible effects of fish quality parameters in salmon (Carter and Hauler 2000). Lupin protein concentrates also offer considerable potential in fish-feeds, for example, Glencross et al. (2006) has shown that lupin protein concentrate, at up to 40%, can be used to replace fishmeal protein in trout diets, while Allan and Booth (2004) demonstrated, for silver perch, that crude lupin protein was more digestible than either peas, soya or oilseed proteins. 3.1.3 Linseed Linseed (Linaceae) oil is currently extensively used as a fish-oil replacement. It contains high proportions of 18:3 (n-3) fatty acids which have consumer health benefits and which accumulate in the flesh of salmon (Sargent and Tacon 1999). In addition, salmon are able, at least to some extent, to convert these to the more health-beneficial longer chain HUFAs (Sargent and Tacon 1999). Whilst diets containing linseed oil have been shown to improve protein digestibility, at least at low temperatures (Bendiksen et al. 2003b), it has also been associated with decreased growth during seawater acclimation as a

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consequence of either a deficiency in essential fatty-acids or dietary energy (Bendiksen et al. 2003a). In other studies the inclusion of linseed oil has been shown to result in growth comparable with fish-oil fed control fish (Menoyo et al. 2005). 3.1.4 Soya Soya (Leguminosae) is a widely cultivated forage crop, the seeds of which, like canola, are used to produce a cake and an oil. The cake and oil are currently being used as a replacement for fishmeal and fish-oil in fish feeds following research that has been ongoing for over 20 years with mixed, and occasionally contradictory, results. Some of these differences may occur as the soya plant changes through selective breeding or genetic modification, or as a consequence of how the raw bean protein and oil products are processed (the flour, defatted flour and protein concentrates are all referred to in the literature). Processing can substantially reduce the potency of several of the antinutrients present in the raw product (Annex 3).

The inclusion of soyabean oil in salmon diets has been shown to result in negligible differences compared to fish-oil controls in terms of flesh firmness (Regost et al. 2004), water retention in either the raw or smoked product (Rora et al. 2003) or growth rates (Grisdale-Helland et al. 2002). However, soya lecithins (phospholipids) have been shown to reduce astaxanthin adsorption in salmon resulting in a deterioration in product colour. This may be as a consequence of the reduced solubility of the pigment in the soya oil compared with fish-oil (Olsen et al. 2005), although this was not observed in fish fed a linseed/palm/rapeseed blend (Torstensen et al. 2005).

The use of soya protein appears more problematic than the oil primarily as a consequence of the presence of anti-nutrients (Annex 3). Soya protein inclusion in salmonid feeds (65% replacement of fish protein) has been shown to reduce growth rates by 13% (Mundheim et al. 2004) although this was not found by Kaushik et al. (1995) in work on rainbow trout. The presence of trypsin inhibitors, and the foul tasting isoflavone genistein, in soya proteins 16

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may account for the reduced digestibility or acceptability of a soya based diet reported by Refstie et al. (2000) and Arndt et al. (1999). There are concerns regarding the transmission of the isoflavone to the final product although (D'Souza et al. 2005) reported that a taste panel were unable to detect any difference in the taste between fish fed a standard diet and one based on soya (see section 5.1). The feed-palatability issue may be overcome, perhaps through the inclusion of krill meal (see 3.4.2). In addition to the isoflavones present in soya meal, it also contains antigens that may cause allergic reactions in fish (Rumsey et al. 1993; Kaushik et al. 1995). Soyabean oil and protein have also been trialled in cod diets. In terms of the oil, the initial results are encouraging, with growth rates and some flesh characteristics being unaffected by the inclusion of soya-oil (Morkore et al. 2005). Soymeal, as an alternative to fishmeal, also performed well, with cod being considered to have a flexible digestion system well able to cope with the change from fish- to soymeal (Refstie et al. 2005a). The antinutrients found in soya products can, according to Refstie et al. (2005b), be removed through lactic acid fermentation so, despite the problems associated with soya protein as a fishmeal replacement, it offers considerable potential as a source of protein (Carter and Hauler 2000). 3.1.5 Maize gluten meal Maize gluten is a high protein ingredient formed as a co-product during the wet milling of maize. It typically contains between 60% and 62% protein and less than 5% oil. Compared to fish meal, maize gluten contains relatively low amounts of lysine, methionine, arginine and tryptophan. Maize gluten is also used as a source of carotene and xanthophyll. Whilst there is relatively little published on the use of this ingredient in Atlantic salmon diets, it has potential as a partial replacement (up to 50%) for fish meal (Mente et al. 2003).

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3.2 By-products A broad-range of by-products have been trialled as substitutes for inclusion in aquaculture diets but most are based on either meat render products or feather-meal. In the light of concerns surrounding bovine spongiform encephalopathy (BSE) and scrapie, animal proteins were largely banned from inclusion in animal feeds, by the European Union, in 2001. However, in 2003 restrictions on the incorporation of blood products into animal feeds were lifted (Hoetink 2005). Blood products are considered to offer an excellent and highly digestible source of protein, are not contaminated by persistent organic pollutants, are sustainably produced and contain high concentrations of the essential amino acid histidine (Hoetink 2005) making them ideal candidates for inclusion in fish-diets.

Feather meal has been considered as having some potential as a partial replacement for fish meal in trout feeds (Bureau et al. 1999; Rahnema et al. 2005). Feather meal contains low concentrations of phosphorus making it a preferable source of protein where water quality issues are paramount. In this role it has been shown to be a useful component in trout (Hernandez et al. 2005) and carp (Jahan et al. 2003) feeds. In Chile and Canada feather and blood-meal are currently extensively used in salmon diets (N. Bradbury, pers. comm., 2006). 3.3 Single cell culture (including marine algae) The biosynthesis of a range of food- and pharmaceutical-related commodities, using fermentation technology, is well established. In terms of aquaculture feed-stocks there are two main routes by which single cell culture could be used to reduce reliance on forage fish. These are firstly using fermentationderived essential fatty acids to bolster concentrations in vegetable oils, thereby reducing reliance of fish-oil and, secondly, by the bulk production of proteins to replace fishmeal. The primary driving force in the development of species and techniques for producing high quality essential fatty acids is the dietary supplement sector. 18

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Although crude fish-oil is an excellent source of EFA, it has a complex fattyacid profile meaning that it requires purification before it can be used in dietary supplements. The purification process is costly and there is, therefore, considerable interest in finding cost-effective fermentation methods of production (Lewis et al. 1999; Harel et al. 2002).

A number of algal groups, including diatoms, crysophytes, cryptophytes, dinoflagellates and others, produce long chain PUFAs. In the sea these algae form the base of the food chain and, ultimately, the PUFAs they synthesise are concentrated in forage fish stocks. It should be of no surprise then, that the culture of algae has been considered as a source for PUFAs. Algae that have been proposed for essential fatty acid production include Nitzschia spp., Nannochloropsis sp, Navicula sp, Phaeodactylum sp and Porphyridium species (Vazhappilly and Chen 1998). However, whilst Bullis et al. (2005) demonstrated the potential for algae to make up HUFA shortfalls in vegetable based shrimp diets, this is yet to be demonstrated on a commercial scale or with a broad range of species. The problem with culturing autotrophs is that the maximum culture-vessel cell density is relatively low and heating/lighting costs are very high, meaning that such processes tend to be cost-prohibitive on industrial scales (Vazhappilly and Chen 1998; Harel et al. 2002). These disadvantages can be overcome by growing heterotrophic algae in conventional fermentators where energy for cell growth is supplied by glucose or other utilizable carbon sources in the medium. Heterotrophic algae used in aquaculture include Chlorella, Nitzschia, Cyclotella and Tetraselmis species (Wen and Chen 2002) while Zaslavskaia et al. (2001) reported that the EFA synthesising photoautotrophic diatom Phaeodactylum tricornutum could be converted to a heterotroph by genetic engineering allowing it to be grown more cost-effectively. The commercial potential of genetic engineering has been demonstrated by the modification of the microalgae Crypthecodinium cohnii and Schizochytrium sp , on an industrial scale, to produce EFAs by the Marteck Biosciences Corporation, US (Vazhappilly and Chen 1998)

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Another group of micro-organisms offering considerable potential are the thraustochytrids (Leman 1997). Thraustochytrids are marine microheterotrophs that contain both a high lipid content and extremely high concentrations of the essential fatty acid DHA. Thraustochytrids have considerable potential for industrial-scale production of essential fatty acids, beyond that of many autotrophs, because their culture is relatively straightforward (Carter et al. 2003). Oil derived from thraustochytrids has been used in experimental aquaculture feeds, at an inclusion rate of 10%, to double DHA concentrations in canola-oil based diets with no adverse effects in the growth or performance of the fish (Carter et al. 2003). Recent research has suggested that methanogenic bacteria can be grown to produce a protein product having a very similar amino-acid profile to highquality fishmeal. This has been shown to be usable by salmon, both pre- and post-smolt, but its inclusion in feeds has been linked to decreases in fishgrowth attributable to its reduced digestibility (ca. 80%) compared with fishderived proteins (Berge et al. 2005; Berge and Barnathan 2005). However, the presence of essential amino-acids has meant that it can be included in some UK salmon feed formulations (I. Carr, EWOS, pers. comm., 2006). Single cell proteins are well established in the market place, examples include the meat alternative Quorn (produced by the fungus Fusarium gramineurum) The existing market acceptance of biotech foods, such as Quorn, is likely to increase consumer acceptance of salmon fed similar products. 3.4 Marine sources Feeding salmon and trout marine-based foods has a number of marketing advantages primarily by maintaining a degree of naturalness as far as the consumer is concerned. There are a number of non-fish marine sources that have potential as salmonid feed stocks. These are copepods, krill, fisheries by-products, mussels and marine worms and plants.

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3.4.1 Copepods Copepods are a diverse group of crustaceans with over 12,000 marine species having been described. They constitute the biggest source of animal protein in the oceans and provide food for many fishery species (Olsen et al. 2004). They have a range of lifestyles with some being parasitic, commensal and others free-living. The free living types are mostly planktivorous and include the pelagic calanoid- and benthic harpacticoid- copepods that are of most relevance to the current review.

The technology for the rearing and capture of copepods, on scales necessary to make significant contributions to the global aquaculture feeds, has still to be developed. However, on smaller scales there is currently considerable interest in the potential for intensively culturing copepods as a living food source for larval fish. This stems, primarily, from the advantages of live prey over pellets in initiating larval feeding. Whilst harpacticoid copepods are able to synthesise EFA their laboratory culture is accelerated by including animal derived EFA in their diets. This suggests that de-novo synthesis of EFA is a rate limiting stage in their own growth (Cutts 2003). Harpacticoid copepods, being benthic, require a substratum on which to grow and production is limited more by surface area than volume making their mass culture difficult (Cutts 2003). Harpacticoid copepods have been used, on experimental scales, as a food source for turbot larvae but questions remain as to whether the additional cost of including intensively reared copepod larvae in fishlarval diets is cost effective (Stottrup 2000). It seems questionable, therefore, that intensively reared copepods will make a cost-effective contribution to bulk aquaculture feeds. The calanoid copepod Calanus finmarchicus is the main food of post-smolt wild juvenile salmon and also feature in the natural diet of older salmon feeding in the North Atlantic (Olsen et al. 2004). North Atlantic copepods have an annual production of several hundred million tonnes (Melle (2004) cited in Olsen et al. 2004) and there is considerable interest in developing a fishery targeting them. 21

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Copepods such as C. finmarchicus are an excellent source of oil. However, unlike fish-oils it is rich (37.5%) in wax-esters (Olsen et al. 2004). Despite these differences copepods appear well suited for inclusion in fish diets; Olsen et al. (2004) and Sountama et al. (2005) have shown that copepod-derived oils are efficiently digested by salmon and that, despite containing only twothirds of the n-3 PUFAs compared with fish oil, they deliver similar flesh characteristics compared with fish-oil controls. Like most oil sources from the lower part of the trophic chain, Calanus oil can be expected to have a lower content of PCBs and dioxins compared with fishoil (see 5.2), compounds that are undesirable in food for human consumption. However, this needs further research as elevated heavy metal concentrations, derived from copepod oil, have been implicated in larval cod deformities (Opstad et al. 2006) 3.4.2 Krill Krill are swarming pelagic euphausids (Crustacea), similar in appearance to shrimp, that are important members of the food chain in temperate and polar waters. They are relatively low in the trophic food-web and form an essential part of the diet of species as diverse as fish, seabirds and whales. There are currently six krill species that are fished (Nicol and Endo 1997); two will be considered here Nyctiphanes australis and, particularly, the Antarctic krill Euphausia suberba, Dana) on the basis of their prevalence in relevant literature. The Antarctic krill fishery is the largest extending to about 100,000 tonnes per annum. This catch represents only about 1/40th of the total allowable catch where the standing stock is estimated to be between 55 and 160 million tonnes (Nicol and Foster 2003).

The development of the market for krill as an aquaculture feedstock source is limited by technical difficulties, associated with catching and processing, and issues pertaining to its suitability of inclusion in the human food chain. The 22

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astaxanthins (Storebakken 1988), proteins and oils (Anon 2006) that are present in high concentations in krill, degrade rapidly once captured meaning that krill must be immediately processed once on board. The extreme environment characteristic of a majority of oceans where krill are found increase the cost of exploiting this resource.

Krill contain high concentrations of fluoride (up to 6000 mg/kg dry-weight) which, through interference with calcium metabolism, is considered toxic to humans above 150 mg/kg. However, krill derived fluoride has been shown to have a very low retention time in both salmon and cod (Moren et al. 2005) and, where it is retained, it is largely stored in the fish skeleton (Virtue et al. 1995).

Krill is highly palatable, as far as salmon are concerned, and it has considerable potential for inclusion in feeds that are otherwise distasteful, perhaps as a consequence of the inclusion of a high proportion of plant protein. Arnd et al. (1999) have shown that 5% krill inclusion increased the palatability of highly fish oil/meal substituted feeds to levels comparable with more traditional diets while Suontama et al. (2005) demonstrated excellent performance of both salmon and halibut fed diets based on krill protein and copepod oil.

Nyctiphanes australis has been shown to offer considerable potential as a basis of aquacultural feed stocks, containing, on a dry weight basis, an average of 52% crude protein and 5.0 to 9.5% lipid. The fatty acid profile of N. australis is markedly unsaturated, with a mean total omega 3 fatty acid content of 48.62.4% of total fatty acids. N. australis contains high levels of the essential long-chain polyunsaturated fatty acids eicosapentaenoic (EPA) and docosahexaenoic (DHA), ranging from 16.6 to 36.5% and 11.1 to 24.8%, respectively. The concentration of total carotenoids (79.5% astaxanthin and 20.5% canthaxanthin) ranged from 137 to 302 g/g dry wt, with no significant differences in concentrations found with season or life stage indicating product reliability. Euphasia superba exhibits a similar nutrient profile to N. australis 23

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though some variation in fat quantity is present as a function of season and sex (Storebakken 1988).

Although krill have been successfully cultured in extensive ponds (Hirano et al. 2003) there is currently no research to suggest that intensive culturing methods may serve as a potential source of protein or oil for aquaculture. 3.4.3 Fisheries by-products Fish by-products are currently used to produce 17% of global fishmeal and fish-oil supplies and represents a common-sense usage option for fish offal. There is also interest in the conversion of by-catch into fishmeal and fish-oil. However, this proposal has the potential to increase the amount of bycatching and may, therefore, not be viable. The use of fish by-products in the production of fishmeal and fish-oil is predicted to expand in the future (2010), but only to 18% (Huntington 2004). There are a variety of fish waste-streams, including offal (blood, heads, tails, skins, entrails etc) and shellfish heads and carapaces, that offer potential as a source of fishmeal and fish-oil. Each waste-stream is likely to offer very different properties dependent on its nature and source (species). Some fish by-products, particularly when derived from oily fish, can be processed in the same way as forage fish in the generation of fishmeal and fish-oil. However, other techniques are being trialled. For example, Hevroy (2004) describes a new product Sea Grain which is produced from fish-waste by grinding, emulsification and drying of the fish material thus omitting the cooking, pressing and separation steps of traditional fish meal production. Using herring as the main stock ingredient in the production of such a feed resulted in good growth, protein retention and normal fish health in Atlantic salmon (Hevroy et al. 2004). Further work has shown the potential for Sea Grain made from a variety of different sources. The admixture of fish by-products into salmon feed may also confer advantages by the stimulation of the innate immune system (Murray et al. 2003).

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Waste water from shrimp/ prawn processing contains high levels of organic compounds and nutrient salts. It is anticipated that environmental legislation will soon impose stricter limits on the amounts of particulate matter, organic matter, nitrogen and phosphorous dischargeable from processing units to receiving waters. Researchers in the EU funded consortium project BYPROFEED have demonstrated an effective method of extracting good quality raw Protein Omega Concentrate (POC) from this waste water. The valuable pigment astaxanthin can also be recovered from the waste water. The POC can be dried to a stabilised material ready for incorporation to fish feeds. Extensive trials have already been carried out on a range of target species (salmon, Arctic charr, trout, cod and lobster) and indicated that the POC acted as a significant attractant. Further analysis showed the POC was effective as a source of protein and fatty acids and the astaxanthin content conferred redness on the target species. The research concluded that POC had significant commercial potential as a source of organic astaxanthin and as an alternative to high cost synthetic sources. The geographical source of the shrimp had implications for its suitability as a feed ingredient as when the levels of PCBs, dioxins and brominated flame retardants were monitored they were found to vary between harvest areas (BYPROFEED project code Q5CR2001-70626). UK king scallop ( Pecten maximus) landings are in the order of 15,000 tonnes p.a., and the inedible soft tissues (all remaining tissue after removal of the adductor mussel and gonad) comprise over 40% of the total soft tissue weight (Campbell, unpublished). This material, normally disposed of as waste, has been considered to have potential as fish feed. However, extreme caution is required over its inclusion as a feed ingredient as this material could be a source of domoic acid (DA) the amnesic shellfish poison (ASP). Scallops acquire the DA from the naturally occurring diatom Pseudonitzchia spp.; the scallop hepatopancreas is the location of 99% of the scallops DA burden (Campbell et al. 2001). Given that the king scallop is peculiarly slow to depurate DA, the DA burden may not be lost between one years diatom blooms and the next. As a result a residual DA level is found in the 25

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hepatopancreas of most scallops in UK waters (Cousins 2006). Before scallop waste could be used in fish diets a study on the potential of the water soluble DA toxin to accumulate and move up the food chain would be required. Given the low oil (1%) and high water (90%) content (C. Bavington, GlycoMar Ltd., pers comm.) the scallop waste may not be a prime candidate for conversion to fish feed, however, as the DA toxin is water soluble and can be effectively removed from the edible parts of the scallop by careful shucking and washing (Campbell et al. 2003), it may also be possible to devise a relatively simple process to separate DA from scallop waste tissue. Similarly it may be worth investigating the quantity of scallop waste available from the scallop fishery and cultivation sectors in other countries (where ASP may not prevalent) and its potential to meet global fish feed demands. SOFIA (2004) lists pectinids among the top ten animal species-groups in aquaculture production with some 1.2 million tonnes cultured in 2002. In China, a major producer of scallops, the processing waste is bought by Japanese companies although for what purpose is uncertain (H. Liu, pers. comm. 2006). Whereas ASP is not ubiquitous, the presence of other harmful algal toxins in scallop waste should be monitored. 3.4.4 Mussels The flesh of the blue mussel ( Mytilus edulis) and green-lipped mussel Pernia canaliculus has also been considered as a raw material in fish feed (Sigholt et al. 2003; Williams et al. 2005). Sigholt et al. (2003) suggested that, as a primary consumer, the mussel may be an ecologically appropriate species to use as a protein source for aquaculture, and trialled the effect of 3 different inclusion levels of mussel protein (8, 12 and 15%) on feed intake, feed conversion and growth of approximately 160g Atlantic salmon. The mussel protein was prepared from cooked mussel meat ensiled with 1.5% formic acid and contained 23% dry matter. The dry matter contained 11.5% lipid, 65.5% protein and 15% nitrogen free extracts and 8% ash. Although the inclusion of the mussel ensilage at the two higher rates (12 and 15%) did have a negative impact on specific growth rates (SGR), even at the highest inclusion levels acceptable commercial SGR and food conversion ratios were found. They 26

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concluded that the palatability of the diets may have been affected by the formic acid used in the ensiling process, but that mussels may provide an alternative source of protein for small salmon. Unlike scallops, there is no waste tissue from processing mussels, the entire shell contents being destined for the consumer. However, there is a proportion of waste in the form of small, cracked or heavily fouled mussels. The Scottish mussel industry produces over 4,000 tonnes of premium quality rope grown mussels p.a., the total production in the UK being 26,000 tonnes, a large proportion of which comes from the dredge fishery of managed beds. UK mussel production would have to expand massively to provide commercially relevant quantities of mussels for fishmeal. Such an expansion would be limited by site availability. Recent research in the Bay of Fundy (S. Robinson pers. comm. 2006) has shown that mussels, positioned in the trajectory of particulate waste from salmon cages showed enhanced growth rates of up to 60%. Integrating salmon and mussel culture would provide more sites for mussel cultivation, although whether economics would allow mussel production for fishmeal is debateable. However, in Galicia, Spain some 300,000 tonnes of mussels are produced p.a. The potential use of waste mussels from the larger producing nations or the potential to grow mussels specifically for fishmeal should be evaluated following further trials as to their suitability for use in fish diets. Economic evaluation should take into consideration the range of prices found in the mussel cultivation industry, for example rope grown mussels, produced in Ireland, currently fetch 500 per tonne, live in shell, (N. OBoyle pers. comm. 2006). Mussel meal is known to be an acceptable partial replacement for fish meal in diets for laying hens, but despite enquiries within the industry, a recent price for mussel meal has not been obtainable.

However, as with scallops the occurrence of harmful algal toxins would have to be considering in assessing the commercial viability of utilising waste mussels in fish feed. In the UK, as in other European producing countries, there are significant annual closures on harvesting because of the presence of 27

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the diarrhetic shellfish poison (DSP) and other harmful algal toxins in mussels. This may simply be a matter of ensuring the mussels are not harvested when containing toxins, as is currently the practice with shellfish for human consumption. Further research is required to ensure these toxins do not move up the food chain were they to be incorporated into fish diets. 3.4.5 Marine worms The culture of marine worms, including the native species of ragworm Nereis virens and the lugworm Arenicola marina is now well established in the UK by companies such as Seabait Limited (Northumberland) and Dragon Feeds (Port Talbot). These companies initially supplied the sport-angling live-bait market but have expanded into aquaculture feeds. The main aquacultural feed markets are shrimp and finfish broodstocks where quality is paramount. In the UK this has, over the past 12 years, included Dover sole (Solea solea) and, more recently, seabream, bass, mullet, cod, haddock and halibut (Seabait Ltd, www.seabait.com).

Dragon Feeds has just entered a new phase of development and are producing feeds from a pilot mill with commercial capabilities. This is a forerunner to a project between Dragon Feeds and G.E. Energy, a USA corporation, to develop a new feed mill with a capacity of 500,000 tons per year using surplus steam heat and power from a revolutionary gas turbine power station based in South Wales. Their aim is to process 100,000 tons p.a. of polychaetes produced from farms in Europe. The polychaetes are grown in seawater, in shallow sand beds, and are fed on trimmings from a fish processing plant. Polychaete yields are 5 kg m-2. The diets contain the worms as a paste mixed with fishmeal, mussels and squid meal. One formulation of the diet has been used as a 100% replacement broodstock maturation diet for the prawn Penaeus vannamei. The company believe this is the first time a dry feed alone has been successful in a shrimp maturation trial. Dragon Feeds have also commenced feed trials with cod using polychaete meal as both a partial and as a complete replacement for fish meal. Trials are 28

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also being conducted on trout and with cobia (in the USA). The company report serious interest from one large salmon producer and believe they have the capacity to produce polychaete meal on a scale and at a price that will make them competitive. The aim is not to replace all the fishmeal in fish diets, but to replace increasingly large amounts as production is scaled up (M. Owen, pers. comm., 2006). While the manufacturers of the polychaete meal have clear aspirations to scale up production to levels commercially relevant to the UK salmon industry, the performance of salmonids on diets containing polychaete meal diets is untested and more research is required urgently. 3.4.6 Marine plants Both the wild harvest and cultivation of seaweeds are long established traditions in many countries. World aquatic plant production in 2002 was 11.6 million tonnes, 76% of which originated from China (SOFIA, 2004). The production of the kelp (Laminaria japonica 4.7 million tonnes) is the highest production by weight of any aquaculture species. Seaweeds are collected and cultured for a wide range of purposes including direct human consumption, alginate extraction and fertilisers. However, information on the potential for seaweeds as raw material in fish diets is quite scarce although some information exists for tilapia, sea bream, snakehead (Channus striatus), thick lipped grey mullet and European sea bass and rainbow trout (Table 4). The biochemical content of seaweeds varies markedly with season, species and culture conditions; growing seaweeds in nitrogen rich environments increases their protein content and has led to more recent investigations of the potential of this high-nitrogen seaweed to enhance growth rates in marine macroalgivores (Shpigel et al. 1999; Neori et al. 2000). The increasing use of seaweeds to absorb dissolved nitrogen in both sea and land-based aquaculture systems means that more protein enriched seaweed is available. A recent study (Valente et al. 2006) evaluated the inclusion of three seaweeds Gracilaria bursa-pastoris (GP), Ulva rigida (UR) and Gracilaria cornea (GC) as

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dietary ingredients on the performance, nutrient utilisation and body composition of European sea bass juveniles. Six experimental diets were formulated to replace 5% and 10% fish protein hydrolysate by each of the three seaweeds. Diets were fed to European sea bass ( Dicentrarchus labrax) juveniles. Growth performance was only significantly reduced in fish fed the GC-10% diet. The authors considered that as inclusion of GP and UR, up to 10%, had no negative consequences on growth performance, nutrient utilization or body composition, that macroalgae have great potential as alternative ingredients in diets for juvenile European sea bass. They also comment that a comparison of the cost of seaweed meal compared to fish meal would be required to determine if low inclusion levels would be cost effective. Soler Vila et al. (2006) recently presented results from a study on the nutritional value of 3 species of seaweeds Ascophyllum nodosum, Porphyra dioica and Ulva lactuca, in a series of feed trials with 200g rainbow trout (Oncorhyncus mykiss ). The feeds contained up to 8% A. nodosum and up to 15% of the other species. While the trout fed the highest inclusion level (15%) of P. dioica were the only group to display a significant decrease in FCR, they also displayed a distinct pigmentation of the flesh. The relatively low nutritive value of seaweeds could explain their deleterious effects on growth and performance when used at higher inclusion levels (Valente et al. 2006). In addition some species of macroalgae have reported amino acid deficiencies; Ulva lactuca for example lacks cysteine (Wahbeh 1997). In the last three decades the discovery of metabolites with biological activities from macroalgae has increased significantly. Substances with antifouling activity as well as those for the possible treatment human viral infections and cancers have been described (Smit 2004). There is also a growing literature on the immunostimulatory effects of seaweeds in both terrestrial and aquatic farmed animals (Turner et al. 2002; Felix et al. 2004; Felix et al. 2005). Some consider that the use of such naturally occurring compounds is safer than the 30

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use of other chemotherapeutics in fish and shrimp and that their range of efficacy is wider than vaccination (Sakai 1999). Gabrielsen and Austeng (1998) suggested higher lysozyme activity in Atlantic salmon fed diets containing Ascophyllum nodosum meal was attributable to the immunostimulating effect of the alginate. The potential of alginates as immunostimulants is a current area of research in fish feed producers (N. Bradbury, pers. comm. 2006).

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Table 4 - Example studies using seaweeds in fish diets. (from Valente et al. 2006)
Fish species Life history stage Tilapia Oreocromis niloticus, Tilapia zillii Snakehead Channa striatus Fry Ulva spp. Hydrodictyon reticulatum (freshwater) 5% inclusion did not alter growth or protein utilisation efficiency, but increasing inclusion level reduced growth. Incorporation of 5% Ulva resulted in increased growth, feed efficiency and consumption. Gracilaria spp. Silver sea bream Rhabdosargus sarba Red sea bream Pagrus major fingerlings Spirulina meal (microalga) fingerlings Ascophyllum nodosum, Porphyra yezeoensis, Ulva pertusa Thick lipped grey mullet Chelon labrosus Porphrya purpurea Inclusion at 9% and 18% suppressed growth and feed utilisation efficiency Davies et al. 1997 5% inclusion had no significant effect. Used to replace 75% of protein source without adverse effect. 5% inclusion increased body weight, feed utilisation and muscle protein deposition. Mustafa et al. 1995 El-Sayed 1994 Hashim and Mat Saat 1992 Appler 1985 Seaweed species Percentage replacement of fish meal component by seaweed and benefit. Authors Year

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Atlantic salmon, Salmo salar

Ascophyllum nodosum

Used as a binder to produce a wet feed from fish offal. Higher lysozyme levels in wet feed group indicative of an immunostimulating effect of alginate,

Gabrielsen and Austreng

1998

European sea bass Dicentrarchus labrax

4.7g juveniles

Gracilaria bursapastoris, Ulva rigida, Gracilaria cornea

5 and 10% inclusion rate, no depression in performance except with 10% G. cornea A = 3, 5, 8% B = 5, 10, 15% C = work in progress. No decrease in growth except with B 15% but this diet also positively influenced flesh colour.

Valente et al.

2006

Rainbow trout Oncorhynchus mykiss

200g

A = Ascophyllum nodosum, B = Porphyra dioica,C = Ulva lactuca

Soler-Vila, Couglan and Kraan

2006

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4. REALISTIC POSSIBILITIES FOR THE UK INDUSTRY There is currently very limited fish oil replacement within the UK salmon farming sector. This is in marked contrast to other major salmon producing countries (Norway and Chile) where the industry is increasing its reliance on vegetable based alternatives to fish oil and meal. Whilst the overall fishcommodity demand from the salmon-farming sector is declining this is more than outweighed by the increasing demand from the Far East and, consequently, fish-commodity prices continue to rise. As a consequence, at some point in the future, the UK salmon farming industry will either have to move to alternative dietary formulations or establish a (highly specialised) market able to withstand feed-cost increases. The Soil Association and large retailers (Supermarkets) may give the lead in altering consumer expectations and demand through the promotion of a sustainable salmon standard where salmon are fed non-fish based alternatives diets. The UK salmon export sector is currently dominated by the French market (56% of exports going to France; data communicated by the SSPO (2006), modified from 'Business & Trade Statistics (2005)), a market more concerned with naturalness issues compared with many others. French consumers can purchase Scottish salmon under a number of categories which guarantee, among other things, the proportion of the fishs diet that was of natural (marine) origin. For example, under the prestigious Label Rouge scheme a minimum of 45% dietary fishmeal is specified (I. Carr, EWOS, pers. comm., 2006). Accreditation under such schemes can result in a considerable premium on the wholesale price (SSPO) potentially offsetting the increasing price of fish-based feeds. The non Franco-Italian markets are more likely to accept a product reared using non-marine diets and the UK sector must be prepared to compete in the global market place for this consumer. This includes the US which, in 2005, accounted for approximately 10% of the Scottish salmon export market (data communicated by the SSPO (2006), modified from 'Business & Trade Statistics (2005)).

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Concerns regarding the long-term security of fishmeal and fish-oil supply has led some researchers to speculate about long-term solutions. The UK fishfarming sector may benefit from the genetic selection of salmon to enhance their ability to synthesise long-chain HUFA which would reduce or eliminate the need to include these EFAs in the diet (Sargent and Tacon 1999) or from the genetic modification of plants so that they produce the HUFAs and PUFAs that are currently sourced from fish-oil (Opsahl-Ferstad et al. 2003). Such strategies, even if not directly adopted by the UK industry, would reduce the demand, and therefore cost, of fish-based commodities allowing the UK sector to continue to utilise fish-based feeds. The actual strategy adopted by the UK sector depends on the degree to which the consumer is prepared to pay a premium for fish-fed fish and the price of fish-based commodities. Such problems will be addressed by the industry as it evolves in response to changing market conditions. The main threat to the UK salmon farming industry may stem from increasing competition with South American producers, particularly those based in Chile, where labour is cheaper and the regulatory framework less restrictive. 5. IMPLICATIONS FOR THE UK FISH FARMING INDUSTRY The change in diet formulations that may occur in the UK fish-farming industry have a number of potential implications with regard to product quality (taste and texture), human health, fish welfare and organic production. While the implications associated with a change to alternative marine supplies, such as krill or copepods, are considerably less, such a change is not immediately foreseeable in the current economic climate. The following part of this review focuses on the most realistic (and ongoing) change in the industry, where fishbased feeds are increasingly being substituted with higher plant products. 5.1 Product quality - taste, texture, appearance and shelf life The taste, texture and appearance of many food items is dependent, inter alia , on its growing conditions including the diet. This axiom has led to the recent growth in free-range and organic production and sales. Diet associated changes in the taste and texture of farmed fish is a pivotal consideration in 35

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terms of marketing and has considerable implications for the UK fish-farming industry.

The influence of diet on taste and texture has been assessed in a range of marine species. In salmon, Torstensen et al.(2005) showed that vegetable oil feeds resulted in flesh that was favourably considered being less rancid and less marine, when compared with fish fed a fish-oil based diet, by a professional taste-panel. In addition, no difference was noted between fish grown on vegetable oils with a fish-oil based finishing diet compared with those grown throughout their life using standard feeds (Torstensen et al. 2005) with similar findings where bacterial protein meal was used to replace up to 20 % of the ingredients (Berge et al. 2005). Soya protein contains a range of antinutrients (Section 3.1.4 and Annex 3), one of which, genistein has an off flavour which has the potential to be transmitted to the product. However, DSouza et al. (2005) have shown that this off-flavour cannot be detected, by taste-panelists, in the flesh of fish fed at 3000 ppm genistein. Rora et al. (2005) concludes that soya-oil can be used to completely replace fish-oil in salmon diets with no loss of product quality in terms of texture, liquid holding capacity and consumer preference. These findings have been replicated by Regost et al. (2004) who, however, note that rapeseed oil fed fish were inferior in terms of flesh firmness. The negligible influence of oil source on flesh characteristics have also been found in gilthead seabream and seabass where cooked vegetable-oil-fed-fish has been reported, by trained tasters, to be indistinguishable from the fish-oil based control (Izquierdo et al. 2003). However, in turbot the effect of dietary oil source was more pronounced with vegetable oils resulting in significant changes in the taste, texture and colour of fresh fillets (Regost et al. 2003). In a broader study, involving alternative protein sources (render by-products and soybean meal) as well as oil, Allan and Rowland (2005) showed that silver perch products were comparable to control (fish-oil) diets on the basis of flavour, smell and freshness.

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The influence of dietary oil source on flesh colour (vividness and hue) is widely reported with contradictory results. Effects on flesh colour are considered most likely mediated through differential solubility of the main dietary pigment, astaxanthin, in fish- versus vegetable oils. Research indicating an effect includes that by Izquierdo et al. (2005) where chroma values, in seabream flesh, were affected by diet, but at a level undetectable by the human eye. In salmon muscle Rora et al. (2005) reports pigment concentrations as being significantly lower (5.6 mg/kg) compared with those fed on a fish-oil based diet (7.9 mg/kg), a trend also reported in Regost et al. (2004) The replacement of dietary fish-oils with vegetable oils, and the resultant change in fatty acid profile in the flesh has the potential to influence the shelf life of the resultant products. Research into this field is, however, often contradictory (Rora et al. 2003). For example, Menoyo et al. (2005) has shown that replacement of fish-oil by linseed oil did not adversely affect the oxidative stability of salmon muscle whereas Regost et al. (2004) showed that flesh lipids were less liable to oxidation in salmon fed a vegetable-oil based diet. A significant proportion (13%) of exported salmon of UK produced salmon is marketed as smoked (data communicated by the SSPO (2006), modified from 'Business & Trade Statistics (2005)). The smoking yield (smoked weight/fresh weight) from vegetable oil fed fish has been reported to be greater compared with fish-oil controls (Rora et al. 2003). 5.2 Nutritive value and implications for human health The use of alternatives to fishmeal and fish-oil in fish feeds has two main implications for human health. These relate to the positive health benefits of essential fatty acids, normally present in oily fish, and the negative effects of fat-soluble pollutants that may be also be present.

The observation that Inuit people, who traditionally consumed large quantities of oily fish, suffered much less from coronary thrombosis compared with similar populations consuming a western diet led, in the 1970s, to 37

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considerable interest in the role of fish in healthy living (Dyerberg et al. 1975). Subsequent research has shown that the beneficial components of oily fish are the (n-3) highly unsaturated fatty acids (HUFAs), specifically eicosapentaenoic acid (EPA) [20:5(n-3)] and docosahexaenoic acid (DHA) [22:6(n-3)] (Din et al. 2004). Salmon have only a very limited capacity to synthesise these EFAs and most is derived from their diet. Fish-oil based diets, which contain high concentrations of EFA, result in high-levels in the fish produced. This forms a critical component of the marketing strategy for salmon. In broad terms salmon flesh EFA profiles reflect those present in the diets of the growing fish so that where fish-oil is replaced by alternatives, containing lower levels of EFAs, such as vegetable oils, concomitantly lower concentrations are found in the product. The lipids present in the flesh of salmon are under continuous, but varying, flux. The accumulation of nonEFAs, occurring following replacement of fish-oil based diets by vegetable oils can, therefore, by overcome by the use of a finishing fish-oil based diet during the final four - six months of the life of the salmon. Over this period the EFA profile for the product adopts that of the feed thereby regaining the high EFA content. This has been shown for salmon (Bell et al. 2004) and seabass (Mourente et al. 2005). Persistent organic pollutants (POPs) are those that, by way of their organic nature, preferentially dissolve and accumulate in oils and fats. When they are sufficiently persistent they are transferred and concentrated up the food chain. Oily fish are contaminated with a range of POPs which include polychlorinated biphenyls (PCBs), organochlorine pesticides, dioxins and polybrominated diphenyl ethers (PBDEs). The concentration of pollutants present in oily fish reflects those in the body of water in which they have grown. This means that forage-fish from the NE Atlantic and North Sea tend to exhibit higher pollution loads compared with those from the south Atlantic and the resultant feeds, made using these respective forage species, show different levels of contamination (Jacobs et al. 2002). Once in the fish food (predominantly in the oil) a high proportion of the pollutant is transferred to the feeding fish, 95% in the case of PBDEs in salmon (Isosaari et al. 2005). Vegetable oils and oils 38

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derived from lower-trophic-level marine sources are less contaminated with POPs and their inclusion in fish-feeds results in fish-products that are concomitantly less contaminated (Bell et al. 2005) (but note that Opstad (2006) suggested elevated Cd and Hg, present in copepod oil, was responsible for increased mortality and deformity among cultured cod). The presence of POPs in both farmed and wild fish has attracted considerable media attention; the increased use of vegetable oils may offer a sustainable method of reassuring consumers regarding this important issue. 5.3 Fish husbandry and welfare The major driving force in the fish-farming industry is to maximise growth rates of the fish whilst minimising costs. One mechanism of achieving this goal is to ensure optimal fish welfare through fish-husbandry. This means that the industry is very unlikely to adopt fish-feeds that results in poor fish welfare as these are likely to result in poor growth performance thereby adversely affecting profitability.

The large-scale replacement of fish-oil with vegetable alternatives has been linked to the increased incidence of eye cataracts in salmon and an increase in stress as measured using a number of blood parameters (Bell 2005). Whilst Rumsey (1994) showed, in rainbow trout, that soya diets resulted in increased leukocyte density and immunoglobulins in the blood, characteristic of increased stress, this can be attributed to the antigenic nature of certain soya-proteins which can be removed by processing. 5.4 Implications for organic producers The Compendium of UK Organic Standards defines organic farming as: production systems designed to produce optimum quantities of food of high nutritional quality by using management practices which aim to avoid the use of agro-chemical inputs and which minimise damage to the environment and wildlife.

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Currently, almost all organic salmon produced in the UK is grown in Scotland (there is one farm in Northern Ireland) and accounts for the vast majority of organic salmon sold in the U.K. Organic producers are generally the smaller, independent growers, based in the Western Isles, Orkney and Shetland, although there are a number of mainland salmon producers in the process of applying for organic certification. There is also a cod-farming venture in Shetland and a cod hatchery on the Scottish mainland, both of which have recently been certified as organic. The Soil Associations annual Organic Market Report (2006) reports that organic salmon production increased to approximately 3,000 tonnes in 2005 (from 2,500 tonnes in 2004), and is expected to increase considerably in 2006 as newly certified farms begin their first harvests. The organic producers aim to niche market a high-value product. The farm gate value for organic salmon in 2005 was approximately 7 million, and the average price per kilogram was around 3.40. Approximately 60 per cent of organic salmon are sold fresh, mainly within the UK, with the balance going for smoking and other forms of processing usually within Scotland. There is currently only a small amount of organic trout being produced on the Scottish mainland. The first certified farm began production in 2005 and is currently in its start up phase. However the demand for organic salmon and trout is currently high and greatly exceeds supply. If organic salmon production expands in accordance with the prediction for all organic sales of 30% per annum (H. Raven, Soil Association) then production levels could reach 9,000 tonnes equivalent to 7.8 % of the total production figures in the next 5 years.

There are currently two bodies certifying organic aquaculture producers in the UK: The Soil Association and the Organic Food Federation (OFF). A jointlyproduced organic salmonid standard was approved by DEFRA in 1998, since which time the Soil Association has continued developing its own salmon 40

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standard (under its internal interim status) and OFF has produced its own standard for cod. The standards require organic growers to use feeds where at least 50% of the aquatic ingredients are by-products of wild fish caught for human consumption, the remainder must be from wild marine sources independently certified as sustainable by a recognised body such as the Marine Stewardship Council (MSC). As there are currently no MSC certified fisheries, in effect all fishmeal for organic fish feeds comes from trimmings. Not all fish oil comes from trimmings at present, due to the practical limitations of the production process, however the Soil Association has set a target date of 2010, by which all fish meal and fish oil incorporated into Soil Association organic fish diets should come exclusively from MSC-certified sources, and has entered into a partnership with MSC to encourage the certification of suitable fisheries. Components of agricultural (terrestrial origin) are permitted, providing they are certified organic, however in practice, their inclusion rate is limited by the price and availability of feed-grade certified ingredients and the major retailers concerns that their customers do not want vegetable ingredients in organic salmon. As with mainstream producers, who foresee meeting their oil needs by part substitution with plant oils, the Soil Association and OFF acknowledge that organic fish diets will ultimately contain ingredients from a greater diversity of sources and do not rule out the possibility of including vegetable products and adding EPA/DHA or proteins from microbial fermentation (providing no GM organisms are involved in their production). Partial substitution of fish oil with organic vegetable oil to reduce dependency on capture fisheries meets with their ethos for sustainability and may also reduce the level of environmental contaminants. Although the Soil Association standard specifies oil inclusion rates must not exceed 28%, neither certifier has yet specified a maximum permissible level of replacement with vegetable oil.

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OFF have recently given organic certification to the cod producer Johnson Seafarms, Shetland. Farmed cod have a lower oil requirement (< 20%) but a higher protein requirement (> 50%) than farmed salmon and trout. Currently organic cod diets are produced by BioMar (UK), and contain trimmings from fish captured for human consumption and plant raw materials (wheat, beans, soya and sunflower) from certified organic sources. Fish oil and meal from MSC certified sources will be included once available. However, fish meal contains approximately 68% protein and the plant materials available contain much lower levels (< 35%) protein, unless a solvent extraction process is performed to remove the oil and increase the protein content, which is not allowable in the organic standard. Therefore it is impossible to replace a large percentage of the fishmeal in cod diets with plant-sources of protein and still achieve the high-protein low-oil formulation required (N. Bradbury, BioMar pers comm. 2006). Synthetic sources of minerals and vitamins are permitted, providing they are non-GM. The accumulation of environmental contaminants is not such an issue for farmed cod, as it is fed, and contains, lower levels of oil. In summary, the production or organic diets for all fish species face the same challenges as those for conventional farmed stocks in terms of the need to find replacement sources of fish meal and fish oil. Organic standards do not prohibit the use of plant protein and vegetable oil provided they are from certified organic sources. However, if the pressure from retailers for organic salmon to be fed diets containing only fish oil and fish meal continues, then price rises for these commodities will have a proportionally greater impact on organic growers. The restriction on the inclusion of plant proteins attained by a solvent extraction will limit the percentage of fishmeal which can be replaced by plant protein in organic cod diets. Therefore organic, more so than, conventional farmed cod production is vulnerable to increases in price and / or decreases in availability of fishmeal.

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Both organic certifiers remain very interested in the potential for marine and therefore more natural sources of replacement fish oil and fishmeal.

6. RECOMMENDED RESEARCH AVENUES AND PRIORITIES There are several possible approaches to addressing the sustainability, and long-term future, of the UK fish-farming industry in relation to the supply of fish-feeds. These different approaches may be adopted simultaneously by the industry as market conditions and commodity prices dictate. The amount of any component in future fish-feeds will be dependent on its cost, market acceptability and the product quality it delivers. These factors are likely to operate along a continuum, waxing and waning as commodity prices and consumer fashions change, making predictions difficult.

The first mechanism by which the UKs fish-farming reliance on fish-oil and fishmeal could be reduced is to increase the utilisation of terrestrially derived feed sources in fish-diets, thereby emulating other major producers. In this regard we make the following recommendations, in order of priority, in relation to the market and consumer: 1) that the industry should finalise standards that guarantee minimum EFA content to assure consumers that the health benefits of farmed salmon remain, regardless of diet 2) establish the minimal fishmeal and fish oil content for use in salmonid diets that maintain product quality including EFA levels 3) that profitability projections be made to establish the cost threshold at which marine alternatives to fish-oil and fishmeal become viable 4) concurrently (with 2 and 3) assess consumer acceptability of fish reared using alternative marine and non-marine feed sources 5) determine if a sustainable brand is a marketing tool, both in terms of a switch to plant-based alternatives and sustainably sourced fishmeal and fish-oil 6) determine the consumer attitudes towards genetically modified salmon and salmon feed constituents 43

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If it is found that the consumer is willing to pay a considerable premium for fish fed natural diets then it may be economic to utilise alternative marine source of oil and protein. We recommend that research into the following areas be conducted, in order of priority: 7) establish the broader ecological implications of developing/ increasing copepod and krill fisheries including methods of preservation and contamination-minimisation 8) the determination of whether zooplankton oil is equally effective at all developmental stages of salmon 9) methods of maximising the utilisation of waste from other fishing and aquaculture industries 10) the economics, logistics and environmental compatibility of utilising cultured mussels and worms

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7. REFERENCES Allan GL, Booth MA (2004) Effects of extrusion processing on digestibility of peas, lupins, canola meal and soybean meal in silver perch Bidyanus bidyanus (Mitchell) diets. Aquaculture Research 35: 981-991 Allan GL, Rowland SJ (2005) Performance and sensory evaluation of silver perch (Bidyanus bidyanus Mitchell) fed soybean or meat meal-based diets in earthen ponds. Aquaculture Research 36: 1322-1332 Anon (2004) State of world fisheries and aquaculture (SOFIA). FAO Fisheries Department, ISBN: 9251051771 Anon (2005) Turning the tide - addressing the impact of fisheries on the marine environment. Royal Commission on Environmental Pollution, Published by The Stationery Office, Norwich, UK Anon (2006) Norway: research underway on krill as salmon food Fish Farmer Arndt RE, Hardy RW, Sugiura SH, Dong FM (1999) Effects of heat treatment and substitution level on palatability and nutritional value of soy defatted flour in feeds for Coho Salmon, Oncorhynchus kisutch. Aquaculture 180: 129-145 Bell G (2005) Vegetable oil over fish oil - researching alternatives to fish oil in aquaculture Aquaculture News, pp 13 Bell JG, Henderson RJ, Tocher DR, Sargent JR (2004) Replacement of dietary fish oil with increasing levels of linseed oil: Modification of flesh fatty acid compositions in Atlantic salmon (Salmo salar) using a fish oil finishing diet. Lipids 39: 223-232 Bell JG, McGhee F, Dick JR, Tocher DR (2005) Dioxin and dixon-like polychlorinated biphenyls (PCBS) in Scottish farmed salmon (Salmo salar): effects of replacement of dietary marine fish oil vegetable oils. Aquaculture 243: 305-314 Bell JG, Tocher DR, Henderson RJ, Dick JR, Crampton VO (2003) Altered fatty acid compositions in Atlantic salmon (Salmo salar) fed diets containing linseed and rapeseed oils can be partially restored by a subsequent fish oil finishing diet. Journal of Nutrition 133: 2793-2801 Bell MV, Dick JR, Porter AEA (2001) Biosynthesis and tissue deposition of docosahexaenoic acid (22 : 6n-3) in rainbow trout (Oncorhynchus mykiss). Lipids 36: 1153-1159 Bendiksen EA, Arnesen AM, Jobling M (2003a) Effects of dietary fatty acid profile and fat content on smolting and seawater performance in Atlantic salmon (Salmo salar L.). Aquaculture 225: 149-163 Bendiksen EA, Berg OK, Jobling M, Arnesen AM, Masoval K (2003b) Digestibility, growth and nutrient utilisation of Atlantic salmon parr (Salmo salar L.) in relation to temperature, feed fat content and oil source. Aquaculture 224: 283-299 Berge GM, Baeverfjord G, Skrede A, Storebakken T (2005) Bacterial protein grown on natural gas as protein source in diets for Atlantic salmon, Salmo salar, in saltwater. Aquaculture 244: 233-240 Berge JP, Barnathan G (2005) Fatty acids from lipids of marine organisms: Molecular biodiversity, roles as biomarkers, biologically active

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compounds, and economical aspects Marine Biotechnology I, pp 49125 Bullis RA, Davis DA, Samocha TM, Patnaik S, Browdy CL, Stokes AD, Atwood HL (2005) The use of algal meals for fishmeal and fish oil replacment. In: Howell B, Flos R (eds) Lesson from the past to optimise the future. European Aquaculture Society, Aquaculture Europe 2005, pp 153 Bureau DP, Harris AM, Cho CY (1999) Apparent digestibility of rendered animal protein ingredients for rainbow trout (Oncorhynchus mykiss). Aquaculture 180: 345-358 Campbell DA, Kelly MS, Busman M, Bolch CJ, Wiggins E, Moeller PDR, Morton SL, Hess P, Shumway SE (2001) Amnesic shellfish poisoning in the king scallop, Pecten maximus, from the west coast of Scotland. Journal of Shellfish Research 20: 75-84 Campbell DA, Kelly MS, Busman M, Wiggins E, Fernandes TF (2003) Impact of preparation method on gonad domoic acid levels in the scallop, Pecten maximus (L.). Harmful Algae 2: 215-222 Carter CG, Bransden MP, Lewis TE, Nichols PD (2003) Potential of thraustochytrids to partially replace fish oil in Atlantic salmon feeds. Marine Biotechnology 5: 480-492 Carter CG, Hauler RC (2000) Fish meal replacement by plant meals in extruded feeds for Atlantic salmon, Salmo salar L. Aquaculture 185: 299-311 Cousins S (2006) An investigation of the processes involved in Pecten maximus contamination by amnesic shellfish poisons. University of Dundee, Dundee Cutts CJ (2003) Culture of harpacticoid copepods: Potential as live feed for rearing marine fish Advances in Marine Biology, Vol 44, pp 295-316 D'Souza N, Skonberg DI, Camire ME, Guthrie KE, Malison J, Lima L (2005) Influence of dietary genistein levels on tissue genistein deposition and on the physical, chemical, and sensory quality of rainbow trout, Oncorhynchus mykiss. Journal of Agricultural and Food Chemistry 53: 3631-3636 Din JN, Newby DE, Flapan AD (2004) Science, medicine, and the future Omega 3 fatty acids and cardiovascular disease - fishing for a natural treatment. British Medical Journal 328: 30-35 Dyerberg J, Bang HO, Hjorne N (1975) Fatty-Acid Composition of PlasmaLipids in Greenland Eskimos. American Journal of Clinical Nutrition 28: 958-966 FAO (1986) The production of fish mean and oil, FAO, Fishery Industries Division, Rome, Italy. ISBN 92-5-102464-2 Felix S, Robins PH, Rajeev A (2004) Immune enhancement assessment of dietry incorporated marine alga Sargassum wightii (Phaeophyceae/Punctariales) in tiger shrimp Penaeus monodon (Crustacia/Penaeidae) through prophenoloxidase (proPO) systems. Indian Journal of Marine Sciences 33: 361-364 Felix S, Robins PH, Rajeev A (2005) Immune enhancement in Indian white, shrimp by addition of seaweed. Indian Veterinary Journal 82: 13271328 46

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Isosaari P, Lundebye AK, Ritchie G, Lie O, Kiviranta H, Vartiainen T (2005) Dietary accumulation efficiencies and biotransformation of polybrominated diphenyl ethers in farmed Atlantic salmon (Salmo salar). Food Additives and Contaminants 22: 829-837 Izquierdo MS, Montero D, Robaina L, Caballero MJ, Rosenlund G, Gines R (2005) Alterations in fillet fatty acid profile and flesh quality in gilthead seabream (Sparus aurata) fed vegetable oils for a long terin period. Recovery of fatty acid profiles by fish oil feeding. Aquaculture 250: 431444 Izquierdo MS, Obach A, Arantzamendi L, Montero D, Robaina L, Rosenlund G (2003) Dietary lipid sources for seabream and seabass: growth performance, tissue composition and flesh quality. Aquaculture Nutrition 9: 397-407 Jacobs MN, Covaci A, Schepens P (2002) Investigation of selected persistent organic pollutants in farmed Atlantic salmon (Salmo salar), salmon aquaculture feed, and fish oil components of the feed. Environmental Science & Technology 36: 2797-2805 Jahan P, Watanabe T, Kiron V, Satoh S (2003) Balancing protein ingredients in carp feeds to limit discharge of phosphorus and nitrogen into water bodies. Fisheries Science 69: 226-233 Kaushik SJ, Cravedi JP, Lalles JP, Sumpter J, Fauconneau B, Laroche M (1995) Partial or Total Replacement of Fish-Meal by Soybean Protein on Growth, Protein-Utilization, Potential Estrogenic or Antigenic Effects, Cholesterolemia and Flesh Quality in Rainbow-Trout, OncorhynchusMykiss. Aquaculture 133: 257-274 Leman J (1997) Oleaginous microorganisms: An assessment of the potential Advances in Applied Microbiology, pp 195-243 Lewis TE, Nichols PD, McMeekin TA (1999) The biotechnological potential of thraustochytrids. Marine Biotechnology 1: 580-587 Menoyo D, Lopez-Bote CJ, Obach A, Bautista JM (2005) Effect of dietary fish oil substitution with linseed oil on the performance, tissue fatty acid profile, metabolism, and oxidative stability of Atlantic salmon. Journal of Animal Science 83: 2853-2862 Mente E, Deguara S, Santos MB, Houlihan D (2003) White muscle free amino acid concentrations following feeding a maize gluten dietary protein in Atlantic salmon (Salmo salar L.). Aquaculture 225: 133-147 Moren M, Olsen RE, Hemre G, Malde M, Dahl L, Karlsen O, Julshamn K (2005) Krill meal as a replacement of fish meal in deits to salmon and cod, limitations and possibilities in relation to fluorine as a possible risk factor. In: Howell B, Flos R (eds) Lesson from the past to optimise the future. European Aquaculture Society, Aquaculture Europe 2005, pp 338 - 339 Morkore T, Netteberg C, Olsen B (2005) Product quality of Atlantic Cod fed diets supplemented with soybean oil. In: Howell B, Flos R (eds) Lesson from the past to optimise the future. European Aquaculture Society, Aquaculture Europe 2005, pp 334 - 335 Mourente G, Good JE, Bell JG (2005) Partial substitution of fish oil with rapeseed, linseed and olive oils in diets for European sea bass (Dicentrarchus labrax L.): effects on flesh fatty acid composition, 48

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plasma prostaglandins E-2 and F-2 alpha, immune function and effectiveness of a fish oil finishing diet. Aquaculture Nutrition 11: 25-40 Mundheim H, Aksnes A, Hope B (2004) Growth, feed efficiency and digestibility in salmon (Salmo salar L.) fed different dietary proportions of vegetable protein sources in combination with two fish meal qualities. Aquaculture 237: 315-331 Murray AL, Pascho RJ, Alcorn SW, Fairgrieve WT, Shearer KD, Roley D (2003) Effects of various feed supplements containing fish protein hydrolysate or fish processing by-products on the innate immune functions of juvenile coho salmon (Oncorhynchus kisutch). Aquaculture 220: 643-653 Naylor RL, Goldburg RJ, Primavera JH, Kautsky N, Beveridge MCM, Clay J, Folke C, Lubchenco J, Mooney H, Troell M (2000) Effect of aquaculture on world fish supplies. Nature 405: 1017-1024 Neori A, Shpigel M, Ben-Ezra D (2000) A sustainable integrated system for culture of fish, seaweed and abalone. Aquaculture 186: 279-291 Nicol S, Endo Y (1997) Krill fisheries of the world. FAO, Rome Nicol S, Foster J (2003) Recent trends in the fishery for Antarctic krill. Aquatic Living Resources 16: 42-45 Olsen RE, Henderson RJ, Sountama J, Hemre G, Ringo E, Melle W, Tocher DR (2004) Atlantic salmon, Salmo salar, utilizes wax ester-rich oil from Calanus finmarchicus effectively. Aquaculture 240: 433-449 Olsen RE, Kiessling A, Milley JE, Ross NW, Lall SP (2005) Effect of lipid source and bile salts in diet of Atlantic salmon, Salmo salar L., on astaxanthin blood levels. Aquaculture 250: 804-812 Opsahl-Ferstad HG, Rudi H, Ruyter B, Refstie S (2003) Biotechnological approaches to modify rapeseed oil composition for applications in aquaculture. Plant Science 165: 349-357 Opstad I, Suontama J, Langmyhr E, Olsen RE (2006) Growth, survival, and development of Atlantic cod (Gadus morhua L.) weaned onto diets containing various sources of marine protein. Ices Journal of Marine Science 63: 320-325 Pauly D, Christensen V, Guenette S, Pitcher TJ, Sumaila UR, Walters CJ, Watson R, Zeller D (2002) Towards sustainability in world fisheries. Nature 418: 689-695 Rahnema S, Borton R, Shaw E (2005) Determination of the effects of fish vs plant vs meat protein-based diets on the growth and health of rainbow trout. Journal of Applied Animal Research 27: 77-80 Refstie S, Korsoen OJ, Storebakken T, Baeverfjord G, Lein I, Roem AJ (2000) Differing nutritional responses to dietary soybean meal in rainbow trout (Oncorhynchus mykiss) and Atlantic salmon (Salmo salar). Aquaculture 190: 49-63 Refstie S, Krogdahl A, Forde O, Ringo E, Shearer K (2005a) Nutrient digestion and absorption along the intestinal tract of Atlantic cod (Gadus morhua) fed standard or bioprocessed soybean meal. In: Howell B, Flos R (eds) Lesson from the past to optimise the future. European Aquaculture Society, Aquaculture Europe 2005, pp 384 - 385 Refstie S, Sahlstrom S, Brathen E, Baeverfjord G, Krogedal P (2005b) Lactic acid fermentation eliminates indigestible carbohydrates and 49

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antinutritional factors in soybean meal for Atlantic salmon (Salmo salar). Aquaculture 246: 331-345 Regost C, Arzel J, Cardinal M, Rosenlund G, Kaushik SJ (2003) Total replacement of fish oil by soybean or linseed oil with a return to fish oil in Turbot (Psetta maxima) 2. Flesh quality properties. Aquaculture 220: 737-747 Regost C, Jakobsen JV, Rora AMB (2004) Flesh quality of raw and smoked fillets of Atlantic salmon as influenced by dietary oil sources and frozen storage. Food Research International 37: 259-271 Rora AMB, Regost C, Lampe J (2003) Liquid holding capacity, texture and fatty acid profile of smoked fillets of Atlantic salmon fed diets containing fish oil or soybean oil. Food Research International 36: 231-239 Rora AMB, Ruyter B, Skorve J, Berge RK, Slinning KE (2005) Influence of high content of dietary soybean oil on quality of large fresh, smoked and frozen Atlantic salmon (Salmo salar). Aquaculture International 13: 217-231 Rumsey GL, Hughes SG, Winfree RA (1993) Chemical and NutritionalEvaluation of Soya Protein Preparations as Primary Nitrogen-Sources for Rainbow-Trout (Oncorhynchus-Mykiss). Animal Feed Science and Technology 40: 135-151 Rumsey GL, Siwicki AK, Anderson DP, Bowser PR (1994) Effect of Soybean Protein on Serological Response, Nonspecific Defense-Mechanisms, Growth, and Protein-Utilization in Rainbow-Trout. Veterinary Immunology and Immunopathology 41: 323-339 Sakai M (1999) Current research status of fish immunostimulants. Aquaculture 172: 63-92 Sargent JR, Bell JG, Bell MV, Henderson RJ, Tocher DR (1995) Requirement criteria for essential fatty acids. Journal of Applied IchthyologyZeitschrift Fur Angewandte Ichthyologie 11: 183-198 Sargent JR, McEvoy LA, Bell JG (1997) Requirements, presentation and sources of polyunsaturated fatty acids in marine fish larval feeds. Aquaculture 155: 117-127 Sargent JR, Tacon AGJ (1999) Development of farmed fish: a nutritionally necessary alternative to meat. Proceedings of the Nutrition Society 58: 377-383 Satoh S, Hernandez A, Tokoro T, Morishita Y, Kiron V, Watanabe T (2003) Comparison of phosphorus retention efficiency between rainbow trout (Oncorhynchus mykiss) fed a commercial diet and a low fish meal based diet. Aquaculture 224: 271-282 Shepard CJ, Pike IH, Barlow SM (2005) Sustainable feed resources of marine origin. In: Howell B, Flos R (eds) Lesson from the past to optimise the future. European Aquaculture Society, Aquaculture Europe 2005, pp 59 - 66 Shpigel M, Ragg NL, Lupatsch I, Neori A (1999) Protein content determines the nutritional value of the seaweed Ulva lactuca L for the abalone Haliotis tuberculata L. and H. discus hannai Ino. Journal of Shellfish Research 18: 227-233 Sigholt T, Nielsen BG, Bendiksen EA, Oppedal F (2003) Blue mussel protein ensilage in feed for Altantic salmon ( Salmo salar) European 50

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Aquaculture Society Conference (Poster presentation), Trondheim, Norway Smit AJ (2004) Medicinal and pharmaceutical uses of seaweed natural products: A review. Journal of Applied Phycology 16: 245-262 Soler Vila A, Coughlan S, Kraan S (2006) Nutritional value of Irish seaweeds and its application in fish-feed production 7th Symposium on fish-feed and nutrition in fish (Poster presentation), Biarritz Sountama J, Olsen RE, Kiessling A (2005) The use of krill from Antarctic and Barents Sea and copepod oils as replacements for fish meal and oil in diets for Atlantic salmon and Atlantic halibut. In: Howell B, Flos R (eds) Lesson from the past to optimise the future. European Aquaculture Society, Aquaculture Europe 2005, pp 437 - 438 Storebakken T (1988) Krill as a Potential Feed Source for Salmonids. Aquaculture 70: 193-205 Stottrup JG (2000) The elusive copepods: their production and suitability in marine aquaculture. Aquaculture Research 31: 703-711 Tacon AGJ (2005) State of information on salmon aquaculture feed and the environment. Web address: http://www.westcoastaquatic.ca/Aquaculture_feed_environment.pdf. Date accessed: November 2006 Tocher DR, Bell JG, McGhee F, Dick JR, Fonseca-Madrigal J (2003) Effects of dietary lipid level and vegetable oil on fatty acid metabolism in Atlantic salmon (Salmo salar L.) over the whole production cycle. Fish Physiology and Biochemistry 29: 193-209 Torstensen BE, Bell JG, Rosenlund G, Henderson RJ, Graff IE, Tocher DR, Lie O, Sargent JR (2005) Tailoring of Atlantic salmon (Salmo salar L.) flesh lipid composition and sensory quality by replacing fish oil with a vegetable oil blend. Journal of Agricultural and Food Chemistry 53: 10166-10178 Trushenski JT, Kasper CS, Kohler CC (2006) Challenges and opportunities in finfish nutrition. North American Journal of Aquaculture 68: 122-140 Turner JL, Dritz SS, Higgins JJ, Minton JE (2002) Effects of Ascophyllum nodosum extract on growth performance and immune function of young pigs challenged with Salmonella typhimurium. Journal of Animal Science 80: 1947-1953 Valente LMP, Gouveia A, Rema P, Matos J, Gomes EF, Pinto IS (2006) Evaluation of three seaweeds Gracilaria bursa-pastoris, Ulva rigida and Gracilaria cornea as dietary ingredients in European sea bass (Dicentrarchus labrax) juveniles. Aquaculture 252: 85-91 Vazhappilly R, Chen F (1998) Eicosapentaenoic acid and docosahexaenoic acid production potential of microalgae and their heterotrophic growth. Journal of the American Oil Chemists Society 75: 393-397 Verleyen T, Adams CA (2005) Effects fo fish oil quality on aquaculture feed stability. In: Howell B, Flos R (eds) Lesson from the past to optimise the future. European Aquaculture Society, Aquaculture Europe 2005, pp 457 - 458 Virtue P, Johannes RE, Nichols PD, Young JW (1995) BiochemicalComposition of Nyctiphanes Australis and Its Possible Use as an

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Aquaculture Feed Source - Lipids, Pigments and Fluoride Content. Marine Biology 122: 121-128 Wahbeh MI (1997) Amino acid and fatty acid profiles of four species of macroalgae from Aqaba and their suitability for use in fish diets. Aquaculture 159: 101-109 Wen ZY, Chen F (2002) Perfusion culture of the diatom Nitzschia laevis for ultra-high yield of eicosapentaenoic acid. Process Biochemistry 38: 523-529 Williams KC, Smith DM, Irvin SJ, Barclay MC, Tabrett SJ (2005) Water immersion time reduces the preference of juvenile tropical spiny lobster Panulirus ornatus for pelleted dry feeds and fresh mussel. Aquaculture Nutrition 11: 415-426 Wonnacott EJ, Lane RL, Kohler CC (2004) Influence of dietary replacement of Menhaden oil with canola oil on fatty acid composition of sunshine bass. North American Journal of Aquaculture 66: 243-250 Zaslavskaia LA, Lippmeier JC, Shih C, Ehrhardt D, Grossman AR, Apt KE (2001) Trophic obligate conversion of an photoautotrophic organism through metabolic engineering. Science 292: 2073-2075

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8. APPENDICES Annex 1 Predicted changes in fishmeal usage in aquaculture diets

(from Huntington 2004) Inclusion rate in feed Species Carp Tilapia Shrimp Salmon Marine fish A Trout Catfish Milkfish Marine fish B Eels TOTAL 2000 5% 7% 25% 40% 45% 30% 3% 12% 55% 50% 2010 3% 4% 20% 30% 40% 25% 0% 5% 45% 40% Change 60% 57% 80% 75% 89% 83% 0% 42% 82% 80% Fish meal use (thousand tonnes) 2000 350 55 372 491 508 189 15 36 127 173 2,316 2010 516 60 485 569 892 202 0 28 585 114 3,451 Change 147% 109% 130% 116% 176% 107% 0% 78% 461% 66% 149%

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Annex 2

Predicted changes in fish-oil usage in aquaculture diets

(from Huntington 2004) Inclusion rate in feed Fish-oil use (thousand tonnes) Species Carp Tilapia Shrimp Salmon Marine fish A Trout Catfish Milkfish Marine fish B Eel TOTAL 2000 0% 1% 2% 25% 20% 15% 1% 2% 10% 5% 2010 0.5% 0.5% 3% 20% 15% 15% 0% 2% 12% 8% Change 50% 150% 80% 75% 100% 0% 100% 120% 160% 2000 0 8 30 307 226 95 5 6 23 17 717 2010 103 9 73 379 335 121 0 11 156 23 1,210 Change High 113% 243% 123% 148% 127% 0% 183% 678% 135% 169%

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Annex 3

Plant derived anti-nutritional compounds, their sources, effects and remediative methods (Francis et al. 2001).
Description Widespread, diverse group of compounds. Potency depends on target enzyme. Source Soya Effects Inhibits enzymes such as trypsin but is compensated for by increased enzyme production Remeditive action and efficacy Heat treatment eliminates most of the inhibitors

Antinutritional group Protease inhibitors

Phytates/phytic acid

Hexaphosphates of myo-inositol (glucose derivatives).

Soya Rapeseed Sesame

Chelates bi-and tri-valent mineral ions (particularly zinc) and some proteins making them unavailable, also causes intestinal damage; both lead to reduced growth

Careful milling to remove endosperm and fermentation +/- heat treatment all reduce feed concentrations

Gossypols

Polyphenols contained in pigment glands of some seeds.

Cottonseed

Combine with proteins to reduce their digestability and reduce essential aminoacid uptake. Causes reproductive problems

Plant breeding and processing is effective at reducing gossypol levels to allow up to 50% inclusion in fish feed.

Glucosinolates

Sulphur containing grazing deterents characterising the cabbage family.

Rapeseed Mustard oil cake

Affects thyroid gland.

Plant breeding and wet-heat processing effective methods of reducing glucosinolate concentration

Saponins

Steroid or triterpenoid glycosides.

Most legumes including soya

Disrupt respiratory surfaces (gills) and intestinal mucosa resulting in poor growth

The effects of saponins in fish food is poorly researched. Possibly have potential

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beneficial effects by neutralising other antinutrients such as tannins Tanins Broad group of polymers consisting of either hydrolysable or condensed versions Lectins Proteins, also known as phytohaemagglutinins Most legumes Bind to cell membranes and, when ingested, cause damage to the small intestine reducing gut efficacy and subsequent growth Oligosaccharides These Include sugars such as sucrose and raffinose and nonstarch polysaccharides such as pectin, cellulose and lignin. Phytoestrogens Non-steroidal hormone analogues Soyabean cottonbean linseed safflower Alkaloids Diverse, nitrogen containing compounds derived from amino acids Lupins and many other legumes Wide ranging acute toxic effects, also teratogenic Plant breeding should continue to deliver products with reduced alkaloid content, extrusion (heat treatment) also beneficial in reducing content. Lupin meal is considered to Potentially wide ranging effects on reproduction Largely unknown Many legumes and cereals Bind to bile acids, disrupt the action of enzymes. Although ubiquitous, these compounds do not normally constitute a part of the diet of predatory fish. Research is ongoing into their effects and the degree to which they are utilised. Most, including rapeseed, pea, bean Bind to enzymes disrupting their action or to their substrates effectively isolating them from potential utilisation Careful milling to remove outer husk of seeds, autoclaving, fermentation and alkali treatment all effective in reducing the concentration of tannins but further research is required. Aqueous heat treatment or autoclaving is effective in removing lectins

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have high potential as a fish feed. Antigenic compounds Broad spectrum of compounds classified by their action Aflatoxins Complex organic molecule http://www.answers.co m/topic/aflatoxin Aspergillus flavus and Aspergillus parasiticus contamination of poorly stored grain Aflatoxins are highly carcinogenic and hepatotoxic Many legumes and cereals Cause intestinal lesions and trigger a range of immune responses Poorly researched but allergen concentrations considered safe in a majority of potential alternative fish feed meals Proper storage, to reduce opportunities for A. flavus/parasiticus growth, and screening is essential to ensure that no aflatoxins enter the fish meal chain.

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Annex 4

Dry weight (DW %), protein, lipid, fiber, ash and starch content

of various pea products Product Whole peas Whole extruded Micronized Dehulled peas Dehulled extruded Protein flour Protein concentrate DW (%) 93 92 91 92 92 90 93 Protein 21.3 21.8 22.0 23.7 23.3 50.0 76.0 Lipid 1.4 1.6 1.5 1.4 1.6 2.5 3.0 Fibre 6.3 6.5 7.2 1.5 1.6 2.1 1.0 Ash 3.0 2.3 3.2 3.1 3.0 4.8 4.0 Starch 59 58 61 60 59.5 23 0.4

Annex 5

Crude nutrient profile of the polychaete Nereis virens (data from

Dragon Feeds Limited) Component Water Crude Protein (dmb) Crude Fat/Lipid (dmb) Ash Content (dmb) Crude Fibre (dmb) % 78.88 56.47 24.80 5.32 1.00

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Annex 6

Organisations contacted Contact Dr Andrew Mearns-Spragg Dr Nick Bradbury Dr David Basset Mrs June Francis Dr Mike Owen, Mr Ian Carr and Dr Jose Vecino Ms Anne Chamberlain Dr Charles Bavington Dr Gordon Bell Dr Andrew Jackson

Organisation Aquafarm Limited BioMar British Trout Association The Crown Estate Commission, Edinburgh Dragon Feeds Ltd EWOS Fishmeal information network (FIN) GlycoMar Ltd. Institute of Aquaculture, Stirling University International fishmeal and fish-oil organisation (IFFO) Organic Food Federation Scottish Salmon Producers Organisation Seabait Ltd Soil Association Department of Fisheries and Oceans, St Andrews Biological Station, New Brunswick, Canada. Clew Bay Marine Forum, Ireland.Mr Yellow Sea Fisheries Research Institute Chinese Academy of fishery Sciences 106 Nanjing Road Qingdao 266071 P.R. China

Mr Julian Wade Dr John Webster and Ms Lesley Jenkins Mr Mike Owen Dr Peter Bridston Dr Shawn Robinson

Royal Commission on Environmental Pollution Dr Jonny Wentworth

Niall OBoyle Prof Hui Liu

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