Environ. Sci. Technol. 2008, 42, 3519–3523
Use of Terrestrial Based Lipids in Aquaculture Feeds and the Effects on Flesh Organohalogen and Fatty Acid Concentrations in Farmed Atlantic Salmon ERIN N. FRIESEN,† M I C H A E L G . I K O N O M O U , * ,‡ D A V E A . H I G G S , § K E N G P E E A N G , |,⊥ A N D CORY DUBETZ‡ Faculty of Land and Food Systems, University of British Columbia (UBC), 4160 Marine Drive, West Vancouver, Canada V7V 1N6, Department of Fisheries and Oceans (DFO), Institute of Ocean Sciences, 9860 West Saanich Road, Sidney, Canada V8L 4B2, DFO/UBC Centre for Aquaculture and Environmental Research, 4160 Marine Drive, West Vancouver, Canada V7V 1N6, and Stolt Sea Farm Inc., 1761 Redwood Street, Campbell River, Canada V9W 3K7
Received June 18, 2007. Revised manuscript received February 15, 2008. Accepted February 18, 2008.
Consumption of salmon, wild or farmed, has been encouraged by many scientists and by national and international health organizations due to the potential health benefits associated with their high contents of omega-3 (n-3) highly unsaturated fatty acids (n-3 HUFAs). In 2004, there was increased public concern regarding the safety of farmed Atlantic salmon following the publication of several studies that indicated higher levels of organohalogens in their flesh relative to those noted in the flesh of wild Pacific salmon. Farmed salmon obtain most of these contaminants from the consumption of marine fish oil (MFO) present in salmon feed. In both a laboratory feeding trial and an on-farm field study, partial replacement of MFO in aquaculture feeds with economical and abundant lipids of terrestrial origin resulted in farmed Atlantic salmon with reduced flesh polychlorinated biphenyl and polychlorinated dibenzodioxin and furan concentrations. Flesh levels of n-3 HUFAs (g/(100 g serving)) were lower in farmed Atlantic salmon fed diets with alternative lipids relative to farmed salmon fed more traditional MFO-based diets. However, the former salmon were found to have higher flesh levels of n-3 HUFAs and also similar or lower flesh levels of organic contaminants than some species of market-size wild Pacific salmon. These findings show that consumption of either farmed Atlantic salmon or wild Pacific salmon can meet recommended weekly n-3 HUFA levels with minimal concurrent intake of flesh organohalogens.
* Corresponding author e-mail:
[email protected]. † University of British Columbia. ‡ Institute of Ocean Sciences. § DFO/UBC Centre for Aquaculture and Environmental Research. | Stolt Sea Farm Inc. ⊥ Present address: Cooke Aquaculture Inc., 255 Metcalf St., St. John, New Brunswick, Canada E2K 1K7. 10.1021/es0714843 CCC: $40.75
Published on Web 04/15/2008
2008 American Chemical Society
Introduction In January of 2004, a highly publicized study indicated that farmed Atlantic salmon contained higher levels of organohalogen contaminants, e.g., polychlorinated biphenyls (PCBs), and polychlorinated dibenzodioxins and furans (PCDD/Fs) than wild Pacific salmon (1). Although the levels of contaminants in farmed Atlantic salmon flesh were not a human health concern according to several national food safety regulatory guidelines (2–4), importation of farmed Atlantic salmon to the United States decreased by 20% in the first quarter of 2004 (5) due to public concerns over the adverse effects of these toxicants. Globally, demand for farmed salmon products decreased despite the fact that many studies have previously shown positive effects of frequent fish consumption on cognitive development and reduced risk of some types of cancer, inflammatory diseases, and coronary heart disease (6–10). These human health benefits mostly result from the high content of eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) in salmon. EPA and DHA are often collectively called omega-3 (n-3) highly unsaturated fatty acids (n-3 HUFAs). Organohalogen contaminants are highly lipophilic compounds that are found at increased concentrations in organisms with elevated lipid contents (11, 12). Market-size farmed Atlantic salmon have greater flesh lipid content than farmed or wild Pacific salmon species (12) due to the high lipid contents in their grow-out diets (e40% lipid), excellent genetic propensity for lipid deposition, and their increased size. All salmon accumulate lipophilic contaminants through the ingestion of lipid from their diet. In the case of farmed salmon, fish feed is the largest source of organic contaminants with minimal uptake of these compounds from water sources (13). Traditionally, marine fish oil (MFO) has provided most of the lipid in salmon grower diets and is the largest source of contaminants in aquaculture feeds. Moreover, MFO is a finite global resource that is becoming increasingly scarce and expensive (14). Plant and rendered animal lipid sources are less contaminated than fish oils (15, 16) and have been examined as partial replacements for MFO in aquaculture feeds for over 25 years (17, 18). In particular, two studies have examined the use of vegetable oils as alternatives to fish oil with respect to their potential to lower flesh organohalogen concentrations in Atlantic salmon (19, 20). In a 115 week study, salmon fed a diet with 100% of the supplemental lipid as a 1:1 blend of linseed (flaxseed) oil and rapeseed (canola) oil had 66% lower levels of contaminants than salmon fed a MFO based diet (21). In another study, contaminants were lowered by 90% when the supplemental lipid was comprised of 55% rapeseed oil, 30% linseed oil, and 15% palm oil (22). Each of the aforementioned studies examined a 100% replacement of MFO with terrestrial vegetable oil sources in a controlled laboratory setting. In this study, a controlled laboratory feeding trial was also conducted, but unlike the other studies we additionally carried out a farm-based field study to examine the efficacy of dietary MFO replacement with terrestrial lipid sources to reduce flesh concentrations of PCBS and PCDD/Fs in market-size farmed Atlantic salmon. In studies of this kind, it should be borne in mind that alternative dietary lipid sources often do not contain EPA and DHA. Consequently, reductions in dietary MFO concentrations lower the n-3 HUFA levels in the flesh of fish that consume these diets. Hence, the present study not only examined flesh concentrations of organohalogens but also EPA and DHA in both wild and farmed salmon to ensure that VOL. 42, NO. 10, 2008 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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the latter fish remained a healthy food source from a fatty acid perspective when they ingested the alternate lipid diets.
Experimental Section Laboratory Feeding Trial. Atlantic salmon (Salmo salar) were held at the Department of Fisheries and Oceans (DFO)/ University of British Columbia Centre for Aquaculture and Environmental Research (CAER) in West Vancouver, BC and were fed a commercial feed prior to commencement of the feeding trial. Triplicate groups of 50 fish (average initial body mass, 84 g) were each fed twice daily, to satiation, one of seven experimental diets for 24 weeks (the results of two treatments are presented here). The fish were held in indoor 1100 L tanks supplied with running (11–15 L · min-1), oxygenated (dissolved oxygen, 7.2–10.7 mg · L-1), ambient temperature (7.9–13.2 °C) seawater (mean salinity, 29–32 g · L-1), and a natural photoperiod was in effect. During the 24 week feeding trial the fish gained approximately seven times their initial body mass. The experimental diets contained 46% protein and 27% lipid on a dry weight basis. The two diets examined in this study were identical in ingredient composition except for the supplemental lipid. Most of the lipid (81.4%) originated from the supplemental lipid source, while LT-anchovy fish meal provided 16% of the dietary lipid and minor constituents of the diet such as plant protein sources provided the remainder of the lipid (
