AQUACULTURE ENVIRONMENT INTERACTIONSAquacult Environ Interact

Vol. 6: 151174, 2015doi: 10.3354/aei00122

Published online February 4

INTRODUCTION

The marine finfish aquaculture industry is expand-ing as demand for seafood rises but cannot be met bywild catch fisheries (Halwart et al. 2007). Technologi-cal innovations have made the aquaculture productionof seafood possible in coastal and open ocean areasand these industries are now reliably providing in-

creasing amounts of marine protein. Marine aquacul-ture production has reached 20.1 million metric tons(t) per year and global food fish production has ex-panded almost 12 times in the past 30 yr at an annualrate of 8.8% (FAO 2012). However, along with thiseconomic opportunity comes environmental risk.

The United States (U.S.) and other countries en -dorse a modern marine aquaculture industry that is

The authors 2015. Open Access under Creative Commons byAttribution Licence. Use, distribution and reproduction are un -restricted. Authors and original publication must be credited.

Publisher: Inter-Research www.int-res.com

*Corresponding author: carol.price@noaa.gov

REVIEW

Marine cage culture and the environment: effectson 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, UK3561 Balmy Beach Road, Owen Sound, Ontario N4K 5N4, Canada

ABSTRACT: Increasing human population and reliance on aquaculture for seafood will lead toexpansion 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 craftscience-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 impactsof individual fish farms on marine water quality. Effects on dissolved oxygen and turbidity arelargely 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 isminimized. 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 foradvances in integrated multi-trophic aquaculture (IMTA) to assimilate waste nutrients. Althoughmodern farm management practices have decreased environmental effects of marine fish farms,we conclude that questions remain about the additive impacts of discharge from multiple farmspotentially leading to increased primary production and eutrophication. Research results on sec-ondary effects upon primary production are highly variable. In some locations, nutrient loadinghas little or no trophic impact, while at others there is evidence that nutrients are assimilated byprimary producers. Research on far-field and regional processes, especially in intensively farmedareas and over longer time scales, will refine understanding of the full ecological role of fish farmsin marine environments.

KEY WORDS: Marine aquaculture Environmental impacts Dissolved nutrients Oxygen Nitrate Phosphorus Harmful algal blooms Mitigation strategies

OPENPEN ACCESSCCESS

Aquacult Environ Interact 6: 151174, 2015

both profitable and environmentally responsible(NOAA 2011, Subasinghe et al. 2012, National Sci-ence and Technology Council Committee on ScienceInteragency Working Group on Aquaculture 2014).It is necessary to balance the benefits that this indus-try bringsa safe, nutritious and consistent supplyof seafood, jobs and economic opportunitywith acommitment to marine stewardship. To best managemarine resources, coastal stakeholders require toolsto evaluate the risks that aquaculture poses in themarine environment and to implement measureswhich safeguard marine and coastal ecosystems. Toachieve an industry that is both profitable and envi-ronmentally responsible, the most current knowl-edge must be readily available to support industrialexpansion, guide regulatory processes, inform andreassure the public and strategically direct research.

The real, perceived and potential environmentaleffects of marine finfish cage aquaculture on waterquality are a primary concern of those interested indeveloping an ecologically responsible industry, andseveral reviews have broadly addressed this topic(Wu 1995, Goldburg et al. 2001, Pearson & Black 2001,Hargrave 2003, Goldburg & Naylor 2005, Braaten2007, Pittenger et al. 2007, Holmer 2010, Grigorakis& Rigos 2011). Regional efforts, many sponsored bygovernmental entities, are also underway to addressenvironmental issues at varying scales (Nash 2001,Wildish et al. 2004, Nash et al. 2005, Huntington et al.2006, Costa-Pierce et al. 2007, Halwart et al. 2007,IUCN 2007, Olsen et al. 2008).

Waste discharge from marine fish farms can poten-tially have negative environmental effects that couldlimit growth of the industry in some areas. Past mar-ine aquaculture practices resulted in environmentaldegradation, yet in high production areas like north-ern Europe the industry has largely learned fromthose mistakes and reduced environmental impactsper unit production largely through a combination ofimproved feeds and proper siting of farms (Grttum& Beveridge 2007). Taken together, lessons learnedcan be used to develop a framework for siting andoperating fish farms that maximize production whileminimizing the impact on water quality. However,we lack a comprehensive analysis of how fish farms,as currently operated with modern managementpractices, have changed in the last 2 decades withregard to reducing potential negative environmentalimpacts, as well as what issues remain problematic orin need of more research and development efforts.This need for a global, scientific assessment of effectsof finfish cage aquaculture prompted us to reviewrecent literature regarding dissolved nutrient load-

ing from marine fish farms, direct impacts on waterquality, and secondary impacts on primary pro -duction, including the formation of harmful algalblooms. Our first goal for this undertaking was tosummarize worldwide results from marine fish farmresearch and monitoring projects that investigatedpredominant water quality effects including dis-solved nitrogen and phosphorus loading, dissolvedoxygen depletion, turbidity and lipids, and measura-ble secondary impacts to primary production. Fur-ther, we provide a qualitative analysis of the latestinformation and scientific research on effects of marine finfish cage culture on water quality and pri-mary production in coastal and ocean environments.Finally, this global perspective supports develop-ment of a framework for siting and operating ecolog-ically sustainable fish farms in the USA and world-wide. Effects of particulate waste discharges fromfish farms on sediment biogeochemistry, benthic fau-nal communities, marine biodiversity and sensitivehabitats will be reviewed separately in forthcomingpapers.

METHODS

Papers for this review were collected, beginning inearly 2011 through 2014, through keyword searchesof electronic databases, primarily Aquatic Sciencesand Fisheries Abstracts (ProQuest, LLC) and GoogleScholarTM. Our aim was to ensure comprehensivecoverage, so initial searches included broad keywordcombinations such as marine aquaculture + nitro-gen and marine fish farming + water quality whichwere then narrowed down by carefully reviewingabstracts and full text for direct relevance. Col-leagues and early reviewers additionally providedrecommendations for relevant publications. To pro-vide the needed modern perspective, we limited ourreview primarily to papers published after 2000 inpeer-reviewed journals. We paid particular attentionto the peer-reviewed journal literature, but alsoincluded material from books and key reports (grayliterature) generated by government agencies, aca-demic or research institutions, and private organiza-tions. Only reports with scientific citations and pub-lished in English were included. Excluded from ourreview are opinion pieces, magazine articles, reportswithout scientific references and papers for whichonly the abstracts, and not the full manuscripts, weretranslated into English.

The collected literaturetotaling over 180 titlesoriginates from research around the world, covers a

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Price et al.: Marine cage culture and the environment

range of cultured fish species, includes many newfarm management approaches, and addresses eco-logical processes at many scales. The studies hereinclude those that used measurements and changesin concentration as indicators (including bioassays)and studies using modeling approaches to under-stand interactions between fish farms, water qualityand ecological impacts.

FARM NUTRIENT DISCHARGE AND WATERQUALITY

Nitrogen

The trend of increasing nitrogen levels in coastalwaters due to anthropogenic sources is a concernworldwide, especially because it may cause algalblooms and contribute to nutrient enrichment oreutrophication (Cloern 2001, Galloway et al. 2004,Anderson et al. 2008, Holmer et al. 2008, Tett2008, Karydis & Kitsiou 2012). Marine cage aqua-culture operations are a recognized source of nitro -genous discharge released both in the form of par-ticulate matter (uneaten food and feces containingundigested food