Estuaries and Coasts

, Volume 39, Issue 6, pp 1746–1761 | Cite as

Quantifying the Effects of Commercial Clam Aquaculture on C and N Cycling: an Integrated Ecosystem Approach

  • Anna E. MurphyEmail author
  • Kyle A. Emery
  • Iris C. Anderson
  • Michael L. Pace
  • Mark J. Brush
  • Jennie E. Rheuban


Increased interest in using bivalve cultivation to mitigate eutrophication requires a comprehensive understanding of the net carbon (C) and nitrogen (N) budgets associated with cultivation on an ecosystem scale. This study quantified C and N processes related to clam (Mercenaria mercenaria) aquaculture in a shallow coastal environment (Cherrystone Inlet, VA) where the industry has rapidly increased. Clam physiological rates were compared with basin-wide ecosystem fluxes including primary production, benthic nutrient regeneration, and respiration. Although clam beds occupy only 3 % of the ecosystem’s surface area, clams filtered 7–44 % of the system’s volume daily, consumed an annual average of 103 % of the phytoplankton production, creating a large flux of particulate C and N to the sediments. Annually, N regenerated and C respired by clam and microbial metabolism in clam beds were ∼3- and ∼1.5-fold higher, respectively, than N and C removed through harvest. Due to the short water residence time, the low watershed load, and the close vicinity of clam beds to the mouth of Cherrystone Inlet, cultivated clams are likely subsidized by phytoplankton from the Chesapeake Bay. Consequently, much of the N released by mineralization associated with clam cultivation is “new” N as it would not be present in the system without bivalve facilitation. Macroalgae that are fueled by the enhanced N regeneration from clams represents a eutrophying process resulting from aquaculture. This synthesis demonstrates the importance of considering impacts of bivalve aquaculture in an ecosystem context especially relative to the potential of bivalves to remove nutrients and enhance C sinks.


Clam Aquaculture Nitrogen Carbon Bivalve Ecosystem budget 



We are grateful to the aquaculturists for providing access to their farms as well as information regarding harvest and cultivation practices. Thank you to Willy Reay for providing historical light attenuation data and Michael Kuschner for modeling the system. Feedback from Mark Luckenbach, Liz Canuel, Anne Giblin, and Lisa Kellogg greatly improved this manuscript. This work was supported by Virginia Sea Grant (NA10OAR4170085, #R/71515 W, #R/715168), the NSF GK12 Fellowship (DGE-0840804), the Strategic Environmental Research and Development Program – Defense Coastal/Estuarine Research Program Project SI-1413, and NSF Virginia Coast Reserve LTER Project (DEB 0080381, DEB 0621014). This manuscript is contribution No. 3551 from the Virginia Institute of Marine Science, College of William and Mary.

Supplementary material

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Supplementary Fig. S1 (DOC 69 kb)
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Supplementary Fig. S2 (DOC 87 kb)
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Supplementary Fig. S3 (DOC 48 kb)
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Supplementary Table S1 (DOC 121 kb)
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Supplementary Table S2 (DOC 31 kb)


  1. Adams, Charles M., E. Sandra Shumway, Robert B. Whitlatch, and Tessa Getchis. 2011. Biofouling in marine molluscan shellfish aquaculture: a survey assessing the business and economic implications of mitigation. Journal of the World Aquaculture Society 42: 242–252. Wiley Online Library.CrossRefGoogle Scholar
  2. Bartoli, M., D. Nizzoli, P. Viaroli, E. Turolla, G. Castaldelli, E.A. Fano, and R. Rossi. 2001. Impact of Tapes philippinarum farming on nutrient dynamics and benthic respiration in the Sacca di Goro. Hydrobiologia 455: 203–212.CrossRefGoogle Scholar
  3. Bass, A.E., R.E. Malouf, and S.E. Shumway. 1990. Growth of northern quahogs (Mercenaria mercenaria (Linnaeus, 1758)) fed on picoplankton. Journal of Shellfish Research 9(2): 299–307.Google Scholar
  4. Bauer, James E., Wei-Jun Cai, Peter A. Raymond, Thomas S. Bianchi, Charles S. Hopkinson, and Pierre A.G. Regnier. 2013. The changing carbon cycle of the coastal ocean. Nature 504: 61–70. doi: 10.1038/nature12857.CrossRefGoogle Scholar
  5. Bendell, L.I. 2015. Favored use of anti-predator netting (APN) applied for the farming of clams leads to little benefits to industry while increasing nearshore impacts and plastics pollution. Marine Pollution Bulletin 91: 22–28. doi: 10.1016/j.marpolbul.2014.12.043. Elsevier Ltd.CrossRefGoogle Scholar
  6. Beseres, Pollack, Jennifer David Yoskowitz, Kim Hae-Cheol, and Paul A. Montagna. 2013. Role and value of nitrogen regulation provided by oysters (Crassostrea virginica) in the Mission-Aransas Estuary, Texas, USA. Edited by Simon Thrush. PLoS ONE 8: e65314. doi: 10.1371/journal.pone.0065314.t003.CrossRefGoogle Scholar
  7. Bouillon, S., R.M. Connolly, and D.P. Gillikin. 2011. 7.07 Use of stable isotopes to understand food webs and ecosystem functioning in estuaries. Treatise on Estuarine and Coastal Science. Vol. 7. Treatise on Estuarine and Coastal Science. doi: 10.1016/B978-0-12-374711-2.00711-7.
  8. Bricker, Suzanne B., Karen C. Rice, and Owen P. Bricker. 2014. From headwaters to coast: influence of human activities on water quality of the Potomac River Estuary. Aquatic Geochemistry 20: 291–323. doi: 10.1007/s10498-014-9226-y.CrossRefGoogle Scholar
  9. Brush, M.J. 2002. Development of a numerical model for shallow marine ecosystems with application to Greenwich Bay, R.I. PhD Dissertation, University of Rhode Island, Kingston, RI, USA.Google Scholar
  10. Brush, Mark J., and John W. Brawley. 2009. Adapting the light biomass (BZI) models of phytoplankton primary production to shallow marine ecosystems. Journal of Marine Systems 75: 227–235. doi: 10.1016/j.jmarsys.2008.10.003. Elsevier B.V.CrossRefGoogle Scholar
  11. Brush, M.J., J.W. Brawley, and S.W. Nixon. 2002. Modeling phytoplankton production: problems with the Eppley curve and an empirical alternative. Marine Ecology Progress Series.Google Scholar
  12. Cai, Wei-Jun. 2011. Estuarine and coastal ocean carbon paradox: CO2 sinks or sites of terrestrial carbon incineration? Annual Review of Marine Science 3: 123–145. doi: 10.1146/annurev-marine-120709-142723.CrossRefGoogle Scholar
  13. Carmichael, R., 2004. The effects of eutrophication on Mya arenaria and Mercenaria mercenaria: growth, survival, and physiological responses to changes in food supply and habitat across estuaries receiving different N loads. PhD dissertation, Boston University.Google Scholar
  14. Castagna, M. 2001. Aquaculture of the hard clam, Mercenaria mercenaria. In Biology of the hard clam, ed. J.N. Kraeuter and M. Castagna, 675–697. The Netherlands: Elsevier Science B.V. Amsterdam.CrossRefGoogle Scholar
  15. CBP. 2012. Chesapeake Bay program data hub. (Accessed 29 May 2013).
  16. Chauvaud, L., J.K. Thompson, and J.E. Cloern. 2003. Clams as CO2 generators: the Potamocorbula amurensis example in San Francisco Bay. Limnol. Oceanogr. Google Scholar
  17. Cloern, James E. 1982. Does the benthos control phytoplankton biomass in South San Francisco Bay. Marine Ecology Progress Series 9: 191–202.CrossRefGoogle Scholar
  18. Cloern, J.E. 1987. Turbidity as a control on phytoplankton biomass and productivity in estuaries. Continental Shelf Research 7: 1367–1381.CrossRefGoogle Scholar
  19. Cohen, Ronald R.H., Paul V. Dresler, Elizabeth J.P. Phillips, and Robert L. Cory. 1984. The effect of the Asiatic clam, Corbicula fluminea, on phytoplankton of the Potomac River, Maryland. Limnology and Oceanography 29: 170–180.CrossRefGoogle Scholar
  20. Condon, Elizabeth Darrow. 2005. Physiological ecology of the cultured hard clam, Mercenaria mercenaria: a case study in Cherrystone Inlet, Virginia. MS Thesis, College of William and Mary, Williamsburg, VA.Google Scholar
  21. Cranford, P.J., P.M. Strain, M. Dowd, B.T. Hargrave, J. Grant, and M. Archambault. 2007. Influence of mussel aquaculture on nitrogen dynamics in a nutrient enriched coastal embayment. Marine Ecology Progress Series 347: 61–78.CrossRefGoogle Scholar
  22. Dame, R.F. 2011. Ecology of marine bivalves: an ecosystem approach, second edition.Google Scholar
  23. Dame, Richard F., and Theo C. Prins. 1998. Bivalve carrying capacity in coastal ecosystems. Aquatic Ecology 31: 409–421.CrossRefGoogle Scholar
  24. Doering, P.H., and C.A. Oviatt. 1986. Application of filtration rate models to field populations of bivalves: an assessment using experimental mesocosms. Marine Ecology Progress Series 31: 265–275.CrossRefGoogle Scholar
  25. Doering, P.H., J.R. Kelly, C.A. Oviatt, and T. Sowers. 1987. Effect of the hard clam Mercenaria mercenaria on benthic fluxes of inorganic nutrients and gases. Marine Biology 94: 377–383. Springer.CrossRefGoogle Scholar
  26. Doney, Scott C. 2010. The growing human footprint on coastal and open-ocean biogeochemistry. Science 328: 1512–1516. doi: 10.1126/science.1185198.CrossRefGoogle Scholar
  27. Dumbauld, Brett R., Jennifer L. Ruesink, and Steven S. Rumrill. 2009. The ecological role of bivalve shellfish aquaculture in the estuarine environment: a review with application to oyster and clam culture in West Coast (USA) estuaries. Aquaculture 290: 196–223. Elsevier.CrossRefGoogle Scholar
  28. Emery, Kyle A. 2015. Coastal bivalve aquaculture carbon cycling, spatial distribution and resource use in Virginia, USA and Baja California, Mexico. MS Thesis, University of Virginia, Charlottesville, Virginia, USA.Google Scholar
  29. Emery, Kyle A, Grace M Wilkinson, Victor F Camacho-Ibar, Michael L Pace, Karen J McGlathery, Jose M Sandoval-Gil, and Julieta Hernández-López. 2015. Resource use of an aquacultured oyster (Crassostrea gigas) in the reverse estuary Bahia San Quintin, Baja California, Mexico. Estuaries and Coasts. Estuaries and Coasts: 1–9. doi: 10.1007/s12237-015-0021-9.
  30. FAO. 2014. The state of world fisheries and aquaculture. Food and Agriculture Organizationo f the United Nations: 1–243.Google Scholar
  31. Ferreira, J.G., A.J.S. Hawkins, and S.B. Bricker. 2007. Management of productivity, environmental effects and profitability of shellfish aquaculture—the Farm Aquaculture Resource Management (FARM) model. Aquaculture 264: 160–174.CrossRefGoogle Scholar
  32. Filgueira, R., T. Guyondet, L.A. Comeau, and J. Grant. 2014. A fully-spatial ecosystem-DEB model of oyster (Crassostrea virginica) carry capacity in the Richibucto Estuary, Eastern Canada. Journal of Marine Systems 136: 42–54. doi: 10.1016/j.jmarsys.2014.03.015. Elsevier B.V.CrossRefGoogle Scholar
  33. Filgueira, R., C.J. Byron, L.A. Comeau, B. Costa-Pierce, P.J. Cranford, J.G. Ferreira, J. Grant, et al. 2015. An integrated ecosystem approach for assessing the potential role of cultivated bivalve shells as part of the carbon trading system. Marine Ecology Progress Series 518: 281–287. doi: 10.3354/meps11048.CrossRefGoogle Scholar
  34. Foreman, K.H. 1985. Regulation of benthic algal and meiofaunal productivity and standing stock in a salt marsh ecosystem: the relative importance of resources and predation. Pp 224. Ph.D. Thesis, Boston University.Google Scholar
  35. Frankignoulle, M., and C. Canon. 1994. Marine calcification as a source of carbon dioxide: positive feedback of increasing atmospheric CO2. Limnology and Oceanography 39: 458–462.CrossRefGoogle Scholar
  36. Giles, Hilke, and Conrad A. Pilditch. 2006. Effects of mussel (Perna canaliculus) biodeposit decomposition on benthic respiration and nutrient fluxes. Marine Biology 150: 261–271. doi: 10.1007/s00227-006-0348-7.CrossRefGoogle Scholar
  37. Gillikin, David P., Anne Lorrain, Li Meng, and Frank Dehairs. 2007. A large metabolic carbon contribution to the δ13C record in marine aragonitic bivalve shells. Geochimica et Cosmochimica Acta 71: 2936–2946. doi: 10.1016/j.gca.2007.04.003.CrossRefGoogle Scholar
  38. Giordano, J.C.P., M.J. Brush, and I.C. Anderson. 2011. Quantifying annual nitrogen loads to Virginia’s coastal lagoons: sources and water quality response. Estuaries and Coasts 34: 297–309.CrossRefGoogle Scholar
  39. Grant, J., C. Bacher, P.J. Cranford, T. Guyondet, and M. Carreau. 2008. A spatially explicit ecosystem model of seston depletion in dense mussel culture. Journal of Marine Systems 73(1–2): 155–168.CrossRefGoogle Scholar
  40. Grizzle, R.E., V.M. Bricelj, and S.E. Shumway. 2001. Physiological ecology of Mercenaria mercenaria. In Biology of the hard clam, ed. J.N. Kraeuter and M. Castagna. Amsterdam: Elsevier Science B.V.Google Scholar
  41. Gruber, Nicolas. 2015. Ocean biogeochemistry: carbon at the coastal interface. Nature 517: 148–149. doi: 10.1038/nature14082.CrossRefGoogle Scholar
  42. Guyondet, T., R. Sonier, and L.A. Comeau. 2013. Spatially explicit seston depletion index to optimize shellfish culture. Aquaculture Environment Interactions 4: 175–186. doi: 10.3354/aei00083.CrossRefGoogle Scholar
  43. Hammen, Carl Schlee. 1980. Marine invertebrates. University Press of New England.Google Scholar
  44. Herman, Julie, Jian Shen, and Jie Huang. 2007. Tidal flushing characteristics in Virginia’s tidal embayments. Virginia Coastal Zone Management Program: 1–25.Google Scholar
  45. Hily, Christian, Jacques Grall, Laurent Chauvaud, Morgane Lejart, and Jacques Clavier. 2013. CO2 generation by calcified invertebrates along rocky shores of Brittany, France. Marine and Freshwater Research 64: 91. doi: 10.1071/MF12146.CrossRefGoogle Scholar
  46. Hofmann, E.E., J.M. Klinck, J.N. Kraeuter, E.N. Powell, R.E. Grizzle, S.C. Buckner, and V.M. Bricelj. 2006. A population dynamics model of the hard clam, Mercenaria mercenaria: development of the age- and length-frequency structure of the population. Journal of Shellfish Research 25(2): 417–444.CrossRefGoogle Scholar
  47. Hondula, K.L., and M.L. Pace. 2014. Macroalgal support of cultured hard clams in a low nitrogen coastal lagoon. Marine Ecology Progress Series 498: 187–201. doi: 10.3354/meps10644.CrossRefGoogle Scholar
  48. Kellogg, Lisa M., Ashley R. Smyth, Mark W. Luckenbach, Ruth H. Carmichael, Bonnie L. Brown, Jeffrey C. Cornwell, Michael F. Piehler, Michael S. Owens, D. Dalrymple Joseph, and Colleen B. Higgins. 2014. Use of oysters to mitigate eutrophication in coastal waters. Estuarine, Coastal and Shelf Science 151: 156–168. doi: 10.1016/j.ecss.2014.09.025. Elsevier Ltd.CrossRefGoogle Scholar
  49. Kuo AY, Butt AJ, Kim SC, Lin J. 1998. Application of a tidal prism water quality model to Virginia small coastal basins: Poquoson River, Piankatank River, Cherrystone Inlet, and Hungars Creek. Special report in applied marine science and ocean engineering no. 348.Virginia Institute of Marine Sciences.Google Scholar
  50. Kuschner, M.A. 2015. A model of carrying capacity and ecosystem impacts in a large-scale, bivalve-dominated agro-ecosystem: hard clam aquaculture in Cherrystone Inlet, VA. MS Thesis, Virginia Institute of Marine Science, The College of William and Mary, Gloucester Point, Virginia, USA.Google Scholar
  51. Lake, Samuel J., and Mark J. Brush. 2015. Contribution of nutrient and organic matter sources to the development of periodic hypoxia in a tributary estuary. Estuaries and Coasts. doi: 10.1007/s12237-015-9954-2.Google Scholar
  52. Laruelle, Goulven G., Ronny Lauerwald, Benjamin Pfeil, and Pierre Regnier. 2014. Regionalized global budget of the CO2 exchange at the air-water interface in continental shelf seas. Global Biogeochemical Cycles 28: 1199–1214. doi: 10.1002/(ISSN)1944-9224.CrossRefGoogle Scholar
  53. Laws, E.A., and T.T. Bannister. 1980. Nutrient- and light-limited growth of Thalassiosira fluviatilis in continuous culture, with implications for phytoplankton growth in the ocean. Limnology and Oceanography 25: 457–473.CrossRefGoogle Scholar
  54. Lindahl, Odd, Rob Hart, Bodil Hernroth, Sven Kollberg, Lars-Ove Loo, Lars Olrog, Ann-Sofi Rehnstam-Holm, Jonny Svensson, Susanne Svensson, and Ulf Syversen. 2005. Improving marine water quality by mussel farming: a profitable solution for Swedish society. Ambio 34: 131–138.CrossRefGoogle Scholar
  55. Luckenbach, M W, and H V Wang. 2004. Linking watershed loading and basin-level carrying capacity models to evaluate the effects of land use on primary production and shellfish aquaculture. Bull. Fish. Res. Agen.: 123–132.Google Scholar
  56. Madden, C.J., and J.W. Day. 1992. An instrument system for high-speed mapping of chlorophyll a and physico-chemical variables in surface waters. Estuaries 15: 421–427.CrossRefGoogle Scholar
  57. Mayzaud, P., and R.J. Conover. 1988. O:N atomic ratio as a tool to describe zooplankton metabolism. Marine Ecology Progress Series 45: 289–302.CrossRefGoogle Scholar
  58. McGlathery, Karen J., Iris Cofman Anderson, and Anna Christina Tyler. 2001. Magnitude and variability of benthic and pelagic metabolism in a temperate coastal lagoon. Marine Ecology Progress Series 216: 1–15.CrossRefGoogle Scholar
  59. Mesnage, Valérie, Sylvie Ogier, Gabriel Bally, Jean-Robert Disnar, Nathalie Lottier, Karine Dedieu, Christophe Rabouille, and Yoann Copard. 2007. Nutrient dynamics at the sediment–water interface in a Mediterranean lagoon (Thau, France): influence of biodeposition by shellfish farming activities. Marine Environmental Research 63: 257–277. doi: 10.1016/j.marenvres.2006.10.001.CrossRefGoogle Scholar
  60. Metzger, E., C. Simonucci, E. Viollier, G. Sarazin, F. Prévot, and D. Jézéquel. 2007. Benthic response to shellfish farming in Thau lagoon: pore water signature. Estuarine, Coastal and Shelf Science 72: 406–419. doi: 10.1016/j.ecss.2006.11.011.CrossRefGoogle Scholar
  61. Mirto, S., R. Danovaro, and A. Mazzola. 2000. Microbial and meiofaunal response to intensive mussel-farm biodeposition in coastal sediments of the western Mediterranean. Marine Pollution Bulletin 40: 244–252.CrossRefGoogle Scholar
  62. Mistri, Michele, and Munari Cristina. 2012. Marine pollution bulletin. Marine Pollution Bulletin 64: 2261–2264. doi: 10.1016/j.marpolbul.2012.07.010. Elsevier Ltd.CrossRefGoogle Scholar
  63. Munari, C., E. Rossetti, and M. Mistri. 2013. Shell formation in cultivated bivalves cannot be part of carbon trading systems: a study case with Mytilus galloprovincialis. Marine Environmental Research 92: 264–267.CrossRefGoogle Scholar
  64. Murphy, A.E., I.C. Anderson, and M.W. Luckenbach. 2015. Enhanced nutrient regeneration at commercial hard clam (Mercenaria mercenaria) beds and the role of macroalgae. Marine Ecology Progress Series 530: 135–151. doi: 10.3354/meps11301.CrossRefGoogle Scholar
  65. Murphy, A.E., I.C. Anderson, A.R. Smyth, B. Song, M.W. Luckenbach. 2016. Microbial nitrogen processing in hard clam (Mercenaria mercenaria) aquaculture sediments: the relative importance of denitrification and dissimilatory nitrate reduction to ammonium (DNRA). Limnology and Oceanography. Google Scholar
  66. Newell, Roger I.E. 2004. Ecosystem influences of natural and cultivated populations of suspension-feeding bivalve molluscs: a review. Journal of Shellfish Research 23: 51–62. [Sl: National Shellfisheries Association.Google Scholar
  67. Newell, R.I.E., and E.W. Koch. 2004. Modeling seagrass density and distribution in response to changes in turbidity stemming from bivalve filtration and seagrass sediment stabilization. Estuaries 27: 793–806.CrossRefGoogle Scholar
  68. Newell, Roger I.E., Jeffry C. Cornwell, and S. Owens. 2002. Influence of simulated bivalve biodeposition and microphytobenthos on sediment nitrogen dynamics: a laboratory study. Limnology and Oceanography 47: 1367–1379.CrossRefGoogle Scholar
  69. Nixon, Scott W. 1995. Coastal marine eutrophication: a definition, social causes, and future concerns. Ophelia 41: 199–219. Taylor & Francis.CrossRefGoogle Scholar
  70. Nizzoli, D., D.T. Welsh, E.A. Fano, and P. Viaroli. 2006. Impact of clam and mussel farming on benthic metabolism and nitrogen cycling, with emphasis on nitrate reduction pathways. Marine Ecology Progress Series 315: 151–165.CrossRefGoogle Scholar
  71. Nizzoli, D., D.T. Welsh, and P. Viaroli. 2011. Seasonal nitrogen and phosphorous dynamics during benthic clam and suspended mussel cultivation. Marine Pollution Bulletin 62: 1276–1287.CrossRefGoogle Scholar
  72. NRC. 2010. Ecosystem concepts for sustainable bivalve mariculture. National Research Council of the National Academies. Washington: The National Academies Press.Google Scholar
  73. Officer, C.B., T.J. Smayda, and R. Mann. 1982. Benthic filter feeding: a natural eutrophication control. Marine Ecology Progress Series 9: 203–210.CrossRefGoogle Scholar
  74. Orth, Robert J., Scott R. Marion, Kenneth A. Moore, and David J. Wilcox. 2010. Eelgrass (Zostera marina L.) in the Chesapeake Bay Region of Mid-Atlantic Coast of the USA: challenges in conservation and restoration. Estuaries and Coasts 33: 139–150. doi: 10.1007/s12237-009-9234-0.CrossRefGoogle Scholar
  75. Petersen, J.K., K. Timmermann, M. Carlsson, M. Holmer, M. Maar, and O. Lindahl. 2012. Mussel farming can be used as mitigation tool—a reply. Marine Pollution Bulletin 64: 452–454.CrossRefGoogle Scholar
  76. Petersen, J.K., B. Hasler, K. Timmermann, and P. Nielsen. 2014. Mussels as a tool for mitigation of nutrients in the marine environment. Marine Pollution Bulletin 82: 137–143.CrossRefGoogle Scholar
  77. Peterson, B.J., and K.L. Heck. 1999. The potential for suspension feeding bivalves to increase seagrass productivity. Journal of Experimental Marine Biology and Ecology 240: 37–52.CrossRefGoogle Scholar
  78. Peterson, B.J., and K.L. Heck. 2001. An experimental test of the mechanism by which suspension feeding bivalves elevate seagrass productivity. Marin Ecology Progress Series 218: 115–125.CrossRefGoogle Scholar
  79. Piazza, B.P., P.D. Banks, and M.K. La Peyre. 2005. The potential for created oyster shell reefs as a sustainable shoreline protection strategy in Louisiana. Restoration Ecology 13: 499–506.CrossRefGoogle Scholar
  80. Pinckney, J., and R.G. Zingmark. 1993. Photophysiological responses of intertidal benthic microalgal communities to in situ light environments: methodological considerations. Limnology and Oceanography 38: 1373–1383.CrossRefGoogle Scholar
  81. Powers, M.J., C.H. Peterson, H.C. Summerson, and Sean P. Powers. 2007. Macroalgal growth on bivalve aquaculture netting enhances nursery habitat for mobile invertebrates and juvenile fishes. Marine Ecology Progress Series 339: 109–122.CrossRefGoogle Scholar
  82. Price, T.J., G.W. Thayer, M.W. LaCroix, and G.P. Montgomery. 1976. The organic content of shells and soft tissues of selected estuarine gastropods and pelecypods. Proceedings of the National Shellfisheries Association 65: 26–31.Google Scholar
  83. Prins, Theo C., A.C. Smaal, and Richard F. Dame. 1998. A review of the feedbacks between bivalve grazing and ecosystem processes. Aquatic Ecology 31: 349–359.CrossRefGoogle Scholar
  84. Reay, W.G., D.L. Gallagher, and G.M. Simmons. 1995. Sediment-water column oxygen and nutrient fluxes in nearshore environments of the lower Delmarva Peninsula, USA. Marine Ecology Progress Series 118: 215–215. INTER RESEARCH.CrossRefGoogle Scholar
  85. Rose, J., J.G. Ferreira, K. Stephenson, S.B. Bricker, M. Tedesco, and G.H. Wikfors. 2012. Comment on Stadmark and Conley. Marine Pollution Bulletin 64: 449–451.CrossRefGoogle Scholar
  86. Rose, Julie M., Suzanne B. Bricker, Mark A. Tedesco, and Gary H. Wikfors. 2014. A role for shellfish aquaculture in coastal nitrogen management. Environmental Science & Technology 48: 2519–2525. doi: 10.1021/es4041336.CrossRefGoogle Scholar
  87. Secrist, R.G. 2013. Food availability and utilization for cultured hard clams. Master’s Thesis, Virginia institute of marine science, The College of William and Mary, Gloucester Point, Virginia, USA.Google Scholar
  88. Shoaf, W T, and B W Lium. 1976. Improved extraction of chlorophyll a and b from algae using dimethyl sulfoxide. Limnology and Oceanography: 926–928.Google Scholar
  89. Souchu, P., André Vaquer, Y. Collos, S. Landrein, Deslous-Paoli Jean-Marc, and Bibent Bertrand. 2001. Influence of shellfish farming activities on the biogeochemical composition of the water column in Thau lagoon. Marine Ecology Progress Series 218: 141–152.CrossRefGoogle Scholar
  90. Stadmark, J., and D.J. Conley. 2011. Mussel farming as a nutrient reduction measure in the Baltic Sea: consideration of nutrient biogeochemical cycles. Marine Pollution Bulletin 62: 1385–1388. doi: 10.1016/j.marpolbul.2011.05.001.CrossRefGoogle Scholar
  91. Stadmark, J., and D.J. Conley. 2012. Response to Rose et al. and Petersen et al. Marine Pollution Bulletin 64: 455–456.CrossRefGoogle Scholar
  92. Strayer, David L, Nina F Caraco, Jonathan J Cole, Stuart Findlay, and Michael L Pace. 1999. Transformation of freshwater ecosystems by bivalves. BioScience 49. American Institute of Biological Sciences Circulation, AIBS, 1313 Dolley Madison Blvd., Suite 402, McLean, VA 22101. USA: 19–27.Google Scholar
  93. Sundbäck, K., A. Miles, and E. Goransson. 2000. Nitrogen fluxes, denitrification and the role of microphytobenthos in microtidal shallow-water sediments: an annual study. Marine Ecology Progress Series 200: 59–76.CrossRefGoogle Scholar
  94. Tang, Q., J. Zhang, and J. Fang. 2011. Shellfish and seaweed mariculture increase atmospheric CO2 absorption by coastal ecosystems. Marine Ecology Progress Series 424: 97–105. doi: 10.3354/meps08979.CrossRefGoogle Scholar
  95. Tenore, Kenneth R., Joel C. Goldman, and J. Phillip Clarner. 1973. The food chain dynamics of the oyster, clam, and mussel in an aquaculture food chain. Journal of Experimental Marine Biology and Ecology 12: 157–165. Elsevier.CrossRefGoogle Scholar
  96. Valiela, Ivan. 1995. Producers and processes involved in primary. In Marine ecological processes, 3–17. New York: Springer Science and Business Media.CrossRefGoogle Scholar
  97. Valiela, Ivan, James McClelland, Jennifer Hauxwell, Peter J. Behr, Douglas Hersh, and Kenneth Foreman. 1997a. Macroalgal blooms in shallow estuaries: controls and ecophysiological and ecosystem consequences. Limnology and Oceanography 42: 1105–1118.CrossRefGoogle Scholar
  98. Valiela, I., G. Collins, J. Kremer, K. Lajtha, M. Geist, B. Seely, J. Brawley, and C.H. Sham. 1997b. Nitrogen loading from coastal watersheds to receiving estuaries: new method and application. Ecological Applications 7(2): 358–380.CrossRefGoogle Scholar
  99. Vinogradov, A. P.: The elementary chemical composition of marine organisms, 647 pp. Sears Foundation for Marine Research Memoir II 1953Google Scholar
  100. Waldbusser, G.G., E.N. Powell, and R. Mann. 2013. Ecosystem effects of shell aggregations and cycling in coastal waters: an example of Chesapeake Bay oyster reefs. Ecology 94: 895–903.CrossRefGoogle Scholar
  101. Wiseman, H. 2010. Quantifying the ecosystem role of a suspension and a facultative deposit feeding bivalve in the New River Estuary, NC, with responses to changes in nutrient and sediment inputs. MS Thesis, Virginia Institute of Marine Science, The College of William and Mary, Gloucester Point, Virginia, USA.Google Scholar
  102. Woods H, 2001. An examination of potential conflict between SAV and hard clam aquaculture in the lower Chesapeake Bay. MS Thesis, College of William and Mary, Williamsburg, VA.Google Scholar

Copyright information

© Coastal and Estuarine Research Federation 2016

Authors and Affiliations

  • Anna E. Murphy
    • 1
    Email author
  • Kyle A. Emery
    • 2
    • 3
  • Iris C. Anderson
    • 1
  • Michael L. Pace
    • 3
  • Mark J. Brush
    • 1
  • Jennie E. Rheuban
    • 4
  1. 1.Virginia Institute of Marine ScienceCollege of William & MaryGloucester PointUSA
  2. 2.Marine Science InstituteUniversity of CaliforniaSanta BarbaraUSA
  3. 3.Department of Environmental SciencesUniversity of VirginiaCharlottesvilleUSA
  4. 4.Department of Marine Chemistry and GeochemistryWoods Hole Oceanographic InstitutionWoods HoleUSA

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