Fish Nutrition, Aquafeeds and Companion Animal Nutrition in Ontario: Building on Half a Century of Tradition and Cutting-Edge R&D

Over the past 50 years, the University of Guelph has gained an enviable reputation, nationally and internationally, for its innovative research programs in aquaculture nutrition and expertise in aquaculture feed formulation. The history of fish nutrition research at the University of Guelph is intimately related to history of fish culture by governmental hatcheries in Ontario. The need for feeds from these hatcheries combined with sustained support from the Ontario and Canadian Governments over a period of four decades has created a dynamic ecosystem that have allowed University of Guelph fish nutrition researchers to become pioneers and references in the field of aquaculture nutrition. The influence of these researchers on global aquaculture nutrition community has greatly exceeded that would have been expected/justified by the small size of our local fish culture and fish feed industry.

Companion animal food manufacturing is an increasingly important sector of the economy in Ontario. The significant development of this industry also largely linked to the "ecosystem" created in the region by the Ontario Veterinary College and, perhaps strangely, to the existence of the fish nutrition program at the University of Guelph.

The paper provides a short historical account of the development of fish culture, feed formulations and nutrition research in Ontario. It highlights the key accomplishments of University of Guelph researchers in the science of fish nutrition and feeding. The origin of veterinary medical diets is also briefly highlighted and the growing importance of companion animal nutrition research and development efforts at the University of Guelph and in the region is also reviewed.

The earliest fish culture efforts in Ontario are attributed to Mr. Samuel Wilmot who reared Atlantic salmon and many other native fish species (whitefish, lake trout, walleye and bass) at a small private facility on Wilmot creek near Newcastle around 1865. In 1868, the Canadian government provided funding to construct a permanent hatchery and initiate full-scale production. Research done by Samuel Wilmot led to the development of many culture techniques for trout and salmon. These techniques included techniques for fish spawning and egg fertilization, incubation and rearing techniques, as well as, different approaches to stocking fish in water bodies (Kerr, 2006). A display of the fish culture techniques and installations of Samuel Wilmot was presented at the Great International Fisheries Exhibition in London England in 1883 and this display won several medals, including a gold medal (Kerr, 2006).

The federal government invested significant effort in fish culture activities starting in 1876 and established many fish hatcheries. Most efforts were devoted to species of importance for commercial fisheries, such as whitefish, walleye, lake herring, and lake trout (Kerr, 2006). There was high level of public interest in the fish culture and it was reported that tens of thousands of people were visiting the hatcheries every year.

The government of the province of Ontario became involved in fish culture around 1910 when it reached an agreement with the federal government. Under this agreement, the province assumed responsibility for culturing fish destined to provide recreational fisheries (sport fishing) and federal government retained the fish culture activities related to commercial fisheries. By 1920, there were more than 45 main hatcheries and sub-stations operated by the Ontario Government. Today, the Ontario Ministry of Natural Resources operates 10 fish culture stations that rear 12 species of fish and produce the millions of eggs required to meet production targets. The provincial hatcheries currently stock about 7 million fish annually in more than 1,000 water bodies.

Feeding aquatic animals in captivity under intensive conditions represented a major challenge in the early days of fish culture. During the 1920’s and 30’s, salmon and trout were fed a variety of items available in the vicinity of hatcheries. These ingredients included salmon eggs, fresh or frozen fish, oilseed meals, brewer’s yeast combined with beef liver, horse meat, chicken eggs, and cottage cheese. “Wet mixtures” made of one third beef liver, one third hog liver, and one third salmon viscera were commonly used. The organs were chopped and mixed at the hatchery together with salt which helped congeal the mixture. The wet mixture was delivered to fish using a spoon or a scoop. This process was labor intensive and the wet mixtures resulted in poor water quality and disease transmission. Feed conversion ratio (feed:gain) ranged from 2 to more than 8 (Hardy and Barrows, 2002).

In the 1930s and 1940s, significant advances in fish culture techniques were made which included better methods for controlling diseases and parasites. The demand for ingredients used in wet mixture feeds increased due to increasing number of hatcheries in North America. To extend these traditional ingredients, "meat-meal mixtures" were developed in 1940s and 1950s. These “meat-meal mixtures” were blends of slaughter house by-products and dry, commercially available feed ingredients. The most famous was the “Cortland Dry Feed Mixture No 6”. This mixture was blended with an equal weight of beef liver and pig spleen, water was added, and the mixed material was squeezed through a potato ricer to feed small fish or made into stands (pellets) using a meat grinder for larger fish (Hardy and Barrows, 2002). These mixtures allowed relatively good growth rates but were relatively expensive, quite highly polluting, and very tedious to prepare. In addition, they were not heat-treated and, thus, were often vectors of diseases.

The Cortland Laboratory in New York State (USA) was apparently the first to successfully use dry pellets for trout rearing in the early 1950s. The Cortland station worked for three decades on development of feeds and on studying nutrient requirements and metabolism of fish. Their annual report series “Fisheries Research Bulletin”, was first published in the 1930s, report the results of dozens of very interesting and progressive studies on feed formulation, mineral metabolism, protein and energy nutrition, effects of environmental factors with various salmonid species.

Researchers at the Cortland Station found that production could be increased by 60% and feed cost reduced by 40% with the use of dry pelleted feeds. Because the initial formulations did not include any vitamin supplements, it was necessary to feed beef liver once every three weeks to provide some vitamins. The trout grew from 10 cm to a stocking length of 18 cm after 7 months. Around 1960, Philips and his colleagues added vitamins to the feed formulations permitted the successful rearing of trout to spawning and subsequent rearing of fry entirely on manufactured pellets (Philips et al. 1964). The Cortland Laboratory played a decreasingly important role in fish feed formulation in the late 1960s. Research and development efforts in the US were picked up by Fowler and Burrows in 1971 and these US government scientists started formulating the “Abernathy” dry diets used for many years by US Fish and Wildlife hatcheries.

At about the same time (1969), the Department of Lands and Forests (now the Ontario Ministry of Natural Resources, OMNR) approached Prof. Stanley Slinger, was well-known poultry nutritionist with the Department of Nutritional Science, University of Guelph for help to formulate Canadian-made dry fish diets which could replace imported feeds from the U.S. and Europe. These feeds were very expensive and did not support good growth performance. At that time, the old “meat-meal mixtures” made with beef and pig liver and spleen were still used widely as diet in the Government of Ontario hatcheries with marginally better results than imported diets.

Prof. Slinger recruited Mr. C. Young Cho, a graduate student from the Dept. of Nutritional Sciences and a dairy and swine nutritionist by training. The two worked in collaboration to develop practical dry fish feed formulae based on principles of land animal nutrition and feed formulation. These researchers arguably were the first to formulate fish feeds on the same principles used poultry and swine feed formulation. These first feeds were, in fact, very similar in composition of turkey starter feed used in Ontario at the time. Results achieved at the hatcheries with these feeds were very impressive right from the start, to the great pleasure of hatchery personnel.

In 1973, the OMNR decided to publically tender the production of the feed required to supply all of the Ontario Government fish hatcheries and the few private fish farmers of the province. The feeds were formulated by Young Cho and Stanley Slinger but the production of these feeds were tendered for production by private feed manufacturers in Canada. Since the expertise in fish feed production did not exist in the industry in Canada, Cho and Slinger introduced the concept of “Open Feed Formula”. Several "open formulae" (e.g. Table 1) were developed and information on key issues, such as ingredient quality criteria, feed manufacturing equipment and process, feed handling and storage, and feeding practices was included in an annual "provincial feed tender package". This package was widely distributed, without limitations, over a span of about three decades to all feed manufacturers requesting the information. This package proved to be a very effective technology transfer tool.

A number of feed manufacturers were involved in the production of the open feed formulae in the early days. However, Martin Feed Mill a feed manufacturer from Elmira, Ontario whose roots date back to 1923 was the most successful and produced the open feed formulation for about two decades. These governmental contracts allowed Martin Feed Mills to develop its expertise in fish feed manufacturing and be able to supply quality feeds to support the development of commercial fish culture in the province. Martin Mills is the only fish feed manufacturer in Ontario today and a cornerstone of commercial aquaculture in Ontario. The company provided quality inputs to commercial fish culture operations, as well as, short and medium term credits to the enterprises, many of which would have problems financing themselves through traditional means.

The open feed formula concept developed by Cho and Slinger also played a highly influential for the development of commercial feeds, in Scandinavia (Denmark, Sweden, Norway), notably through an informal association with Astra-Ewos (Mississauga, Ontario), the ancestor of EWOS, one of the leading salmon feed manufacturers today. In the late 70s, EWOS feed formulators from Denmark started adopting the experimental high fat feed formulas developed by C. Young Cho. These high fat diets were considered the original low pollution diets as they allowed reduction of nitrogenous waste outputs from land-based operations. High-fat diets have become the norm in salmon production in Norway, Chile and Canada.

The landscape evolved very significantly since the 70's and seven corporations currently produce aquaculture feeds in Canada, namely Skretting North America, EWOS Canada, Martin Mills, Corey Feed Mills, Northeast Nutrition, Taplow Feeds and Viterra Feed Products. These corporation are operating a total of nine (9) aquaculture feed mills in British Columbia, Ontario, New Brunswick, and Nova Scotia. Canadian aquaculture feed manufacturers are producing an estimated 150,000 to 200,000 tonnes of feed annually (Tacon and Metian, 2004).

In the wake of early success, the Government of Ontario decided to support a research and development program on fish nutrition and feeding at the University of Guelph. This support was very long lasting since the UG Fish Nutrition Research Laboratory (UG FNRL) virtually operated as a "joint venture" between the University of Guelph and the OMNR for 44 years, from 1969 until 2013.

As the first phase of the project, the UG FNRL constructed a wet laboratory with a recirculation system and initiated what was to be the first fish nutrition research project in Canada. The initial objectives of the experiments were to formulate salmonid diets using ingredients available in Canada. A large grant from the Canada's Department of Fisheries and Oceans through the Federal-Provincial Fisheries Industrial Development Program, and a National Research Council (NRC) grant in 1973, made possible a major expansion of the facilities and of the scope of the research efforts.

In the mid 1970's, the Department of Nutritional Sciences sought approval from the Ontario Ministry of Agriculture and Food (OMAF). The granting of this approval was the beginning of funding of commercial (private) aquaculture research at the University of Guelph by the Ontario Government, an endeavor that has still important today. A number of faculty, graduate students and technicians from the Dept. of Nutritional Sciences were recruited or became involved in the research efforts on fish nutrition and feeding with support of OMAF and the OMNR. Some of these scientists included Dr. John Hilton, Dr. Bill Woodward, Dr. Bruce Holub, Dr. Jim Atkinson, Dr. Henry Bayley and Dr. Colin Cowey.

The scientists invested significantly in the development of novel and better-adapted research equipment and protocols for basic and applied fish nutrition research. The infrastructure, equipment, tools, protocol and a progressive "eco-system" made it possible to carry out innovative studies in the fields of nutrient requirements (protein/amino acids, lipid/fatty acids and vitamins) at the cutting-edge of the field. The estimates of vitamin requirements derived from studies carried out in Guelph in the 70's and 80's are a cornerstone of the requirements established by the NRC today (NRC,2011).

The researchers pioneered what is now referred to as the "Guelph system of fecal collection" that has led to reliable estimate of apparent digestibility for feedstuffs commonly used in fish feeds. The research infrastructure also was set-up to enable examination of the effect of various biotic and abiotic factors (e.g. species, water temperature, light, dissolved oxygen levels, etc.) on nutritional regimes. Finally, the work on bioenergetics of fish carried out by C.Young Cho in the late 70's and early 80's was highly innovative and remains the gold standard in the field to this day (NRC, 2011).

In the late 1980's, the UG FNRL made a significant contribution in terms of transfer of technology to the feed and aquaculture industry in Canada, Asia and Latin America. It has provided support for the design of aquatic systems and research protocols used by fish nutrition laboratories in more than 15 countries. Moreover, the framework and mathematical models developed by University of Guelph researchers in the 1970's, 80's and 90's underpin many of the models and production management tools used by aquaculture operations around the World. The most famous example may be the thermal-unit growth coefficient model (TGC model, also known as "GF3") which is now used by virtually all salmon culture operations on the planet and gaining wide acceptance for other fish species.

The University of Guelph gained an enviable reputation, nationally and internationally, for the quality and innovative aspects of its research programs in aquaculture nutrition. Scientists from the University participated to the Subcommittee for Fish Nutrition of U.S. National Research Council (NRC) for the 1981, 1993 and 2011 editions of “Nutrient Requirement of Fish”, which are very influential reference documents for the global aquaculture nutrition community. Guelph scientists also played a very active role internationally, notably by leading the International Union of Nutritional Sciences (IUNS) Committee for Production of Fish and Shellfish for over a decade.

Right for the start, in the early 70's, one of first goals of fish nutrition research program at the University of Guelph was the reduction of the high fish meal levels used in fish feeds, through the use of local rendered animal proteins, such as meat and blood meal, and with plant protein ingredients, such as soybean and corn gluten meal. For decades, Guelph feed formulations were always at leading edge of the field through their focus on cost-effectiveness and on maximizing the use of feed ingredients commonly used in other livestock feeds.

Globally, the aquaculture feed industry was a lot more refractive to reducing fish meal levels and relying more on terrestrial animal and plant feedstuffs. Up until about 20 years ago, fish meal still represented about 50% of the weight of most commercial salmon, trout and marine fish species feeds sold around the World. However, the very significant and sustained growth (approximately 9% per year) of the global aquaculture feed industry resulted in the price of fish meal (Fair average quality (FAQ) basis 65 percent protein, FOB Peru) surging from about $500 to more than $1,500 per tonne over the past two decades. The price of fish oil also increased by more than 400% over the same period (Tacon and Metian, 2008). The heavy reliance of the aquaculture industry on marine-derived resources also drew critics among environmentalists regarding the impacts of fish meal and oil demand on reduction fisheries specifically and marine ecosystems in general (Naylor et al. 2009). The volatility of the commodities market, the economic recession, increasing competition, and slim profit margins have added to the complexity of the situation.

These issues have created a strong incentive to reduce the reliance on marine-derived resources for aquaculture feed manufacturing. Aquaculture feed manufacturers have had to progressively decrease fish meal and fish oil levels in their feeds, and correspondingly increase their reliance on suitable alternative feedstuffs of plant, terrestrial animal or microbial origins. Canadian fish feed manufacturers have been among the first to aggressively modify their feed formulation practices in response to these challenges (Sarker et al. 2013). Practically speaking, this is where the contribution of the University of Guelph fish nutrition research programs has had the greatest global impacts and this impact is still seen today. Formulation of lower fish meal feeds through the use of common, more economical, ingredients requires reliable estimates of digestibility of nutrients of ingredients and on the nutrient and energy requirements of the animals. The research tools and protocols developed at the University of Guelph have been instrumental to generating this type of information.

Perhaps, one of the most important contributions of C. Young Cho and colleagues at UG FNRL and the OMNR has been on the management of the organic matter, phosphorus, and nitrogen discharges from fish culture operations. Fish production is carried out in a wide variety of production systems (marine or freshwater net pens, land-based flow-through facilities, recirculation systems, ponds, etc.). Many aquaculture operations release their wastes directly (or indirectly) in the environment with relatively limited capability to recover wastes which is in part due to the high capital and operating cost required to implement waste removal technologies. The release of wastes by aquaculture operations may result in nutrient enrichment of the receiving environment which, in turn, may result in environmental changes (Cho et al, 1994, Cho and Bureau, 2001, Bureau and Hua, 2010). In certain regions of the country, ongoing tensions with some stakeholder groups (environmental non-governmental agencies, cottage owners, tourism operators, etc.) have lead to intense scrutiny and questioning about the potential environmental impacts of aquaculture operations. This issue has hindered the development of the sector for many years. The effective and meaningful management of waste outputs is a complex issue that can, in broad terms, be simplified to the management of the release of solid wastes (mainly organic wastes) and that of “elemental” wastes (e.g. nitrogenous or phosphorus containing compounds) in forms which may stimulate primary productivity (algae and plant) and eutrophication processes in the receiving water body (Bureau and Hua, 2010). Despite divergences of opinion, there is a general consensus that long-term sustainability of many aquaculture operations in Canada and many other regions is very much related to how these can minimize or better manage their release of solid and dissolved wastes in the environment (Cho et al., 1991; Bureau and Hua, 2010).

University of Guelph researchers, under the leadership of C. Young Cho, has worked under the premise that since most of the wastes released by aquaculture operations are ultimately from biological and dietary origins, effective management of waste outputs can be achieved through management of the nutrient composition of feeds (Bureau and Hua, 2010). Under this impetus, numerous stakeholders in the sector have been proactive in the evaluation and adoption of nutritional strategies to reduce or manage the waste outputs from commercial aquaculture operations. The invested efforts have resulted in very significant reduction of waste outputs (per unit of fish produced) by fish culture operations in Canada over the past four decades (Bureau and Hua, 2010). In the late 1970’s and 1980’s, for example, commercial trout feeds were relatively low in protein (e.g. 35%) and lipids (e.g. 8%) but rich in starch (30-40%) (Table 2). The finding by researchers at the University of Guelph (Hilton et al., 1982) that starch was of limited nutritive value (net energy) to these fish has led to reduction in the level of grains and high carbohydrate grain by-products in feed formulations. This has resulted in the production of feed with higher digestible/useful nutrient (mostly protein and fat) density and significant reduction in the amount of feed required to produce 1 kg of fish as well as very significant decrease in waste outputs (Cho et al., 1994). These feeds supported feed conversion ratio (FCR, feed/gain) of 2 to 2.5 for market size rainbow trout (1 kg). Today, the use of higher digestible nutrient density feeds allows a FCR of about 1.1 to 1.2 for the same fish with substantially lower waste outputs (Tables 2). University of Guelph played a key role in this transition.

Today, the UG FNRL has good research facilities inherited in large part from investments made in the 1970's and 80's, as well as, a grant from the Canada Foundation for Innovation (CFI) in 2002. The UG FNRL currently has a dynamic research team composed of about 30 graduate students, post-docs, visiting scientists, and research assistants. It collaborates with researchers, feed manufacturers, feed ingredient suppliers, aquaculture producers, consultants, and governmental agencies in more than 10 countries on four continents.

The UG FNRL maintains the trajectory and carries out innovative research programs solidly anchored in the long tradition of research excellence established by the predecessors. The long-term goal of this research program is to develop a more complete understanding of nutrients utilization by fish, and then use this greater understanding to devise solutions and tools (feed formulae, production strategies, models, software) to improve the economic and environmental sustainability of aquaculture operations. This progressive research program can be divided in three major themes as follows:

1) Improved understanding of nutrient utilization and requirements of fish
2) Evaluation of the nutritive value of economical feed ingredients
3) Nutritional management of waste outputs.

This research program is supported by the National Science and Engineering Research Council (NSERC), OMNR, OMAF, MITACS, as well as, numerous industrial partners.

The past two decades have seen a rapid expansion of "premium" pet food production in the region. This is especially the case for highly specialized "veterinary" or "prescription" diets which have become an extremely important segment of the pet food industry. The "ecosystem" created in the region by the Ontario Veterinary College is not foreign to this emergence but the existence of the fish nutrition program at the University of Guelph has serendipitously contributed to the development of the industry.

The impetus given by the provincial fish feed tender discussed earlier allowed Martin Feed Mills to develop an expertise in the production of high value animal feeds produced through advanced feed manufacturing techniques (extrusion) and on the nutritive value of high quality ingredients (e.g. fish meal, fish oil, poultry by-products meal, etc.). In the mid-70's, Martin Feed Mills initiated the production of pet food and started developing their pet food brands, including Doc Kennedy, named after the staff veterinarian, Dr. Al Kennedy, in their plant in Elmira, Ontario. Business thrived and in 1979 the Elmira facility started shipping a super premium pet food to compete directly against well established American brands. As sales grew the company continued to reinvest back into their manufacturing plant to meet increased production requirements and quality expectations. The strong quality and performance reputation of the brands produced in Elmira caught the attention of private label accounts. Soon top tier private label brands were being developed and produced in Elmira with great success. In 1988, the first export shipment was sent to Japan. This was the beginning of a long and successful international presence.

In 1990, four entrepreneurs, Drs. John Hilton, Brent Matthew, Donald McKeown and James Patterson benefited from the feed production expertise of Martin Feed Mills and developed a pet food company, Veterinary Medical Diets (VMD), focused on producing therapeutic diets. The Medi-Cal™ brand was launched in October 1990 by VMD. There are nine different diets for dogs and cats, available exclusively from veterinary hospitals. VMD truly revolutionized diets for companion animals and rapidly went on to become a leading brand within the veterinary channel.

Interestingly, one of the founders of VMD, Dr. John W. Hilton was one of the early, and highly productive, fish nutrition researchers at the Dept. of Nutritional Sciences in the 70 and 80's. The great expertise Dr. Hilton developed at the University of Guelph, notably in the nutritional requirements of "carnivorous" animal species (e.g. rainbow trout), feed ingredient quality and feed manufacturing, was likely highly complementary to that of his three other partners who were veterinary clinicians and instrumental to the success of the company.

VMD products found wide acceptance in virtually every companion animal veterinary clinic across this country. The success made the company highly attractive to large players in the food business. In 1996 the business was sold to the H.J. Heinz Company of Canada Ltd. This acquisition allowed Heinz to be rated as 1 of the top 5 pet food companies in the world. In 2002 Heinz sold the North American Pet Food and Pet Snacks business to Del Monte foods. In 2004 Del Monte sold select brands to Royal Canin, a subsidiary of Mars Inc., who was looking to enter the veterinary channel. These products continued to be made in Elmira for 6 years under an agreement with a new corporation, Elmira Pet Products, which took over the production plant in Elmira.

Since 2005, Elmira Pet Products invested over $7M in infrastructure and equipment and now produces about 76,000 t of cat and dog food per year, mostly premium quality pet foods for private label customers and for specialty accounts. The company has plan to ramp up production to more than 100,000 t within a few years.

Royal Canin also opted to keep their feed production in the immediate vicinity of Guelph and invested the building of a $60M state-of-the-art pet food plant in Aberfoyle (Ontario). This plant manufactures the comprehensive veterinary exclusive line of diets sold across North America (Canada/USA/Mexico) under the Medi-Cal/Royal Canin Veterinary Diet brand name. Today, volume of production stands at about 50,000 t of dry petfood per year and is expected to increase to 70,000 t within a few years.

In 2008, the University of Guelph received a $3-million commitment from Royal Canin Canada Company to establish the Royal Canin Veterinary Diet Endowed Chair in Canine and Feline Clinical Nutrition and support independent research and graduate scholarships at the Ontario Veterinary College (OVC).

The major goals of this position are:
1. to enhance companion animal nutrition education within the DVM curriculum at OVC and provide a graduate program focussing on companion animal nutrition
2. to provide a referral clinical nutrition service (only service in Canada). I have attached our service card if you need more info about what we do in the clinic.
3. to start and maintain a companion animal nutrition research program current research is mainly focused on all aspects above in companion animal obesity and cancer.

The University conducted an international search and Dr. Adronie Verbrugghe, a companion animal veterinarian originating from Belgium and board-certified from the European College of Veterinary and Comparative Nutrition joined the Ontario Veterinary College as Assistant Professor and Royal Canin Endowed Chair in Canine and Feline Clinical Nutrition. Dr. Verbrugghe research interests are mainly in obesity, diabetes and other metabolic diseases in cat and dogs.

Other regional organizations are also playing an increasingly important role by offering services to the global companion animal nutrition industry. For example, a private research facility, Ontario Nutri Lab Inc. (ONL) performs digestibility, feeding behaviour and palatability studies and minimally invasive testing, such as weight-loss studies, urinary tract health information, glycemic index to a very large number of national and international clients.

An emerging expertise in companion animal nutrition at the University of Guelph combined to growth in companion animal food manufacturing and testing in the region are creating a dynamic ecosystem that is probably unique in the World. This ecosystem has offered excellent growth opportunities for many of the stakeholders of the agri-food industry in Ontario (e.g., grain farmers, animal protein producers, feed additive manufacturers, etc.) in recent years and many other opportunities exist.

Bureau, D.P. and K. Hua. 2010. Towards effective nutritional management of waste outputs in aquaculture, with particular reference to salmonid aquaculture operations. Aquaculture Research, 41: 777-792.

Cho, C.Y., J.D. Hynes, K.R. Wood and H.K. Yoshida. 1994. Development of high nutrient-dense, low pollution diets and prediction of aquaculture wastes using biological approaches. Aquaculture 124: 293-305.

Cho, C.Y, and Bureau, D.P. 2001. A review of diet formulation strategies and feeding systems to reduce excretory and feed wastes in aquaculture. Aquaculture Research 32: 349-360.

Committee on Nutrient Requirement of Fish and Shrimp (Hardy RW, Gatlin DM, Bureau DP, Dabramo L, Davis DA, Halver JE, Krogdahl, A, Medale F, Shiau SY, Tocher D.), National Research Council. 2011. Nutrient Requirements of Fish and Shrimp. Animal Nutrition Series. National Academies Press, Washington, DC.

Hardy, R.W. and F.T. Barrows. 2002. Diet formulation and manufacture. Pp. 505-600. In: Halver, J.E. and R.W. Hardy.(Eds.). Fish Nutrition, 3rd Edition, Academic press, Amsterdam.

Hilton, J. W. and J. L. Atkinson, 1982. Response of rainbow trout Salmo gairdneri to increased levels
of available carbohydrate in practical trout diets. British J. Nutr., 47: 597-607.

Kerr, S. 2006. An historical review of fish culture, stocking and fish transfers in Ontario, 1865-2004. Fish and Wildlife Branch, Ontario Ministry of Natural Resources, Peterborough, Ontario, Canada.

Naylor, R.L., Hardy R.W., Bureau D.P., Chiu, A., Elliott M., Farrell A.P. , Forster I, Gatlin D.M., Goldburg R.J., Hua K, Nichols P.D. 2009. Aquaculture in an era of finite resources. Proceedings of the National Academy of Science (PNAS) 106 15103-15110.

Phillips, A.M., H.A. Podoliak, H.A. Poston, D.L. Livingston. 1964. The nutrition of trout. Fisheries Research Bulletin No. 27, Cortland, New York.

Sarker, P.K., D.P. Bureau, K. Hua, M. D. Drew, I Forster, K. Were, B. Hicks and G.W. Vandenberg. 2013. Sustainability issues related to feeding salmonids: a Canadian perspective. Reviews in Aquaculture 5: 1–21.

Tacon A.G.J. 2004. Estimated major finfish and crustacean aquafeed markets: 2000 to 2003. International Aquafeed 7 37-41.

Tacon A.G. and Metian M. 2008. Global overview on the use of fish meal and fish oil in industrially compounded aquafeeds: trends and future prospects. Aquaculture 285 146-158.

Table 1. Ontario Ministry of Natural Resources Open Feed Formulae developed by C.Y. Cho from 1973 to 2002.

Table 2. Theoretical waste outputs¹ associated with different historical feed formulae.

¹ based on an estimated digestible energy requirement of 21.5 MJ to grow a rainbow trout from 10 g to 1000 g.

² estimated using the biological method presented by Cho and Bureau (2001).