Marine Cage Culture and the Environment: Effects on Water Quality and Primary Production
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Vol. 6: 151–174, 2015 AQUACULTURE ENVIRONMENT INTERACTIONS Published online February 4 doi: 10.3354/aei00122 Aquacult Environ Interact OPENPEN ACCESSCCESS REVIEW Marine cage culture and the environment: effects on water quality and primary production Carol Price1,*, Kenneth D. Black2, Barry T. Hargrave3, James A. Morris Jr.1 1Center for Coastal Fisheries and Habitat Research, National Centers for Coastal Ocean Science, National Ocean Service, NOAA, 101 Pivers Island Rd., Beaufort, North Carolina 28516, USA 2SAMS, Scottish Marine Institute, Oban, Argyll, PA37 1QA, UK 3561 Balmy Beach Road, Owen Sound, Ontario N4K 5N4, Canada ABSTRACT: Increasing human population and reliance on aquaculture for seafood will lead to expansion of the industry in the open ocean. To guide environmentally sustainable expansion, coastal stakeholders require tools to evaluate the risks that marine aquaculture poses and to craft science-based policies and practices which safeguard marine ecosystems. We summarized cur- rent knowledge regarding dissolved nutrient loading from marine fish farms around the world, direct impacts on water quality and secondary impacts on primary production, including forma- tion of harmful algal blooms. We found that modern operating conditions have minimized impacts of individual fish farms on marine water quality. Effects on dissolved oxygen and turbidity are largely eliminated through better management. Nutrient enrichment of the near-field water col- umn is not detectable beyond 100 m of a farm when formulated feeds are used, and feed waste is minimized. We highlight the role of siting fish farms in deep waters with sufficient current to dis- perse nutrients and prevent water quality impacts. We extensively discuss the potential for advances in integrated multi-trophic aquaculture (IMTA) to assimilate waste nutrients. Although modern farm management practices have decreased environmental effects of marine fish farms, we conclude that questions remain about the additive impacts of discharge from multiple farms potentially leading to increased primary production and eutrophication. Research results on sec- ondary effects upon primary production are highly variable. In some locations, nutrient loading has little or no trophic impact, while at others there is evidence that nutrients are assimilated by primary producers. Research on far-field and regional processes, especially in intensively farmed areas and over longer time scales, will refine understanding of the full ecological role of fish farms in marine environments. KEY WORDS: Marine aquaculture · Environmental impacts · Dissolved nutrients · Oxygen · Nitrate · Phosphorus · Harmful algal blooms · Mitigation strategies INTRODUCTION creasing amounts of marine protein. Marine aquacul- ture production has reached 20.1 million metric tons The marine finfish aquaculture industry is expand- (t) per year and global food fish production has ex- ing as demand for seafood rises but cannot be met by panded almost 12 times in the past 30 yr at an annual wild catch fisheries (Halwart et al. 2007). Technologi- rate of 8.8% (FAO 2012). However, along with this cal innovations have made the aquaculture production economic opportunity comes environmental risk. of seafood possible in coastal and open ocean areas The United States (U.S.) and other countries en- and these industries are now reliably providing in- dorse a modern marine aquaculture industry that is © The authors 2015. Open Access under Creative Commons by *Corresponding author: [email protected] Attribution Licence. Use, distribution and reproduction are un - restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 152 Aquacult Environ Interact 6: 151–174, 2015 both profitable and environmentally responsible ing from marine fish farms, direct impacts on water (NOAA 2011, Subasinghe et al. 2012, National Sci- quality, and secondary impacts on primary pro - ence and Technology Council Committee on Science duction, including the formation of harmful algal Interagency Working Group on Aquaculture 2014). blooms. Our first goal for this undertaking was to It is necessary to balance the benefits that this indus- summarize worldwide results from marine fish farm try brings—a safe, nutritious and consistent supply research and monitoring projects that investigated of seafood, jobs and economic opportunity—with a predominant water quality effects including dis- commitment to marine stewardship. To best manage solved nitrogen and phosphorus loading, dissolved marine resources, coastal stakeholders require tools oxygen depletion, turbidity and lipids, and measura- to evaluate the risks that aquaculture poses in the ble secondary impacts to primary production. Fur- marine environment and to implement measures ther, we provide a qualitative analysis of the latest which safeguard marine and coastal ecosystems. To information and scientific research on effects of achieve an industry that is both profitable and envi- marine finfish cage culture on water quality and pri- ronmentally responsible, the most current knowl- mary production in coastal and ocean environments. edge must be readily available to support industrial Finally, this global perspective supports develop- expansion, guide regulatory processes, inform and ment of a framework for siting and operating ecolog- reassure the public and strategically direct research. ically sustainable fish farms in the USA and world- The real, perceived and potential environmental wide. Effects of particulate waste discharges from effects of marine finfish cage aquaculture on water fish farms on sediment biogeochemistry, benthic fau- quality are a primary concern of those interested in nal communities, marine biodiversity and sensitive developing an ecologically responsible industry, and habitats will be reviewed separately in forthcoming several reviews have broadly addressed this topic papers. (Wu 1995, Goldburg et al. 2001, Pearson & Black 2001, Hargrave 2003, Goldburg & Naylor 2005, Braaten 2007, Pittenger et al. 2007, Holmer 2010, Grigorakis METHODS & Rigos 2011). Regional efforts, many sponsored by governmental entities, are also underway to address Papers for this review were collected, beginning in environmental issues at varying scales (Nash 2001, early 2011 through 2014, through keyword searches Wildish et al. 2004, Nash et al. 2005, Huntington et al. of electronic databases, primarily Aquatic Sciences 2006, Costa-Pierce et al. 2007, Halwart et al. 2007, and Fisheries Abstracts (ProQuest, LLC) and Google IUCN 2007, Olsen et al. 2008). ScholarTM. Our aim was to ensure comprehensive Waste discharge from marine fish farms can poten- coverage, so initial searches included broad keyword tially have negative environmental effects that could combinations such as ‘marine aquaculture + nitro- limit growth of the industry in some areas. Past mar- gen’ and ‘marine fish farming + water quality’ which ine aquaculture practices resulted in environmental were then narrowed down by carefully reviewing degradation, yet in high production areas like north- abstracts and full text for direct relevance. Col- ern Europe the industry has largely learned from leagues and early reviewers additionally provided those mistakes and reduced environmental impacts recommendations for relevant publications. To pro- per unit production largely through a combination of vide the needed modern perspective, we limited our improved feeds and proper siting of farms (Grøttum review primarily to papers published after 2000 in & Beveridge 2007). Taken together, lessons learned peer-reviewed journals. We paid particular attention can be used to develop a framework for siting and to the peer-reviewed journal literature, but also operating fish farms that maximize production while included material from books and key reports (gray minimizing the impact on water quality. However, literature) generated by government agencies, aca- we lack a comprehensive analysis of how fish farms, demic or research institutions, and private organiza- as currently operated with modern management tions. Only reports with scientific citations and pub- practices, have changed in the last 2 decades with lished in English were included. Excluded from our regard to reducing potential negative environmental review are opinion pieces, magazine articles, reports impacts, as well as what issues remain problematic or without scientific references and papers for which in need of more research and development efforts. only the abstracts, and not the full manuscripts, were This need for a global, scientific assessment of effects translated into English. of finfish cage aquaculture prompted us to review The collected literature—totaling over 180 titles— recent literature regarding dissolved nutrient load- originates from research around the world, covers a Price et al.: Marine cage culture and the environment 153 range of cultured fish species, includes many new due to advances in feeding efficiency. Olsen et al. farm management approaches, and addresses eco- (2008) constructed a mass balance estimate of nitro- logical processes at many scales. The studies here gen flow from a hypothetical Norwegian salmon farm include those that used measurements and changes producing 1000 t per year. The estimated annual in concentration as indicators (including bioassays) loading rate of 44 kg of nitrogen per metric ton of fish and studies using modeling approaches to under- produced was comparable to rates measured in