Eastern oyster (Crassostrea virginica) δ15N as a bioindicator of nitrogen sources: Observations and modeling

Marine Pollution Bulletin

Volumn 60, Issue 8, 2010, Pages 1288-1298

  Fertig, B ^a   Carruthers, T J B ^a   Dennison, W C ^a   Fertig, E J ^b   Altabet, M A ^c  

^a UNIVERSITY OF MARYLAND CENTER FOR ENVIRONMENTAL SCIENCE   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c UNIVERSITY OF MASSACHUSETTS DARTMOUTH   (United States)

Author keywords

Biological indicators; Chesapeake Bay; Crassostrea virginica; Nitrogen sources; Stable nitrogen isotopes; Temporal integration

Indexed keywords

BIOLOGICAL INDICATORS; CHESAPEAKE BAY; CRASSOSTREA VIRGINICA; NITROGEN SOURCES; STABLE NITROGEN ISOTOPE; TEMPORAL INTEGRATION;

AIR POLLUTION CONTROL; BIOMARKERS; ISOTOPES; LOCATION; MUSCLE;

NITROGEN;

NITROGEN; NITROGEN 15; WATER POLLUTANT;

BIOINDICATOR; MARINE POLLUTION; MODELING; MOLLUSC; NITROGEN ISOTOPE; OBSERVATIONAL METHOD; STABLE ISOTOPE;

ANIMAL TISSUE; ARTICLE; BIOLOGICAL MONITORING; CRASSOSTREA VIRGINICA; MARINE ENVIRONMENT; NONHUMAN; OBSERVATIONAL STUDY; OYSTER; SEASONAL VARIATION; TISSUE DISTRIBUTION; ANIMAL; CHEMICAL MODEL; CRASSOSTREA; ENVIRONMENTAL MONITORING; GILL; METABOLISM; MUSCLE; OBSERVATION; PROCEDURES; WATER POLLUTANT;

ANIMALS; CRASSOSTREA; ENVIRONMENTAL MONITORING; GILLS; MODELS, CHEMICAL; MUSCLES; NITROGEN ISOTOPES; OBSERVATION; WATER POLLUTANTS, CHEMICAL;

CHESAPEAKE BAY; UNITED STATES;

CRASSOSTREA VIRGINICA; OSTREIDAE;

EID: 77955415513     PISSN: 0025326X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.marpolbul.2010.03.013     Document Type: Article

References (93)

1. Adams T.S., Sterner R.W. The effect of dietary nitrogen content on trophic level N-15 enrichment. Limnology and Oceanography 2000, 45:601-607.
2. Altabet M. Isotopic tracers of the marine nitrogen cycle: present and past. Handbook of Environmental Chemistry. Marine Organic Matter: Biomarkers, Isotopes and DNA 2006, Vol. 2N:251-293. Springer-Verlag, Berlin, Heidelberg, New York.
3. Anderson W.T., Fourqurean J.W. Intra- and interannual variability in seagrass carbon and nitrogen stable isotopes from south Florida, a preliminary study. Organic Geochemistry 2003, 34:185-194.
4. Apple J.K., Del Giogio P.A., Kemp W.M. Temperature regulation of bacterial production, respiration, and growth efficiency in a temperate salt-marsh estuary. Aquatic Microbial Ecology 2006, 43:243-254.
5. Aravena R., Evans M.L., Cherry J.A. Stable isotopes of oxygen and nitrogen in source identification of nitrate from septic systems. Ground Water 1993, 31:180-186.
6. Bebianno M.J., Geret F., Hoarau P., Serafim M.A., Coelho M.R., Gnassia-Barelli M., Romeo M. Biomarkers in Ruditapes decussatus: a potential bioindicator species. Biomarkers 2004, 9:305-330.
7. Benson E.R., O'Neil J.M., Dennison W.C. Using the aquatic macrophyte Vallisneria americana (wild celery) as a nutrient bioindicator. Hydrobiologia 2008, 596:187-196.
8. Boag B., Neilson R., Scrimgeour C.M. The effect of starvation on the planarian Arthurdendyus triangulatus (Tricladida: Terricola) as measured by stable isotopes. Biology and Fertility of Soils 2006, 43:267-270.
9. Bosley K.L., Witting D.A., Chambers R.C., Wainright S.C. Estimating turnover rates of carbon and nitrogen in recently metamorphosed winter flounder Pseudopleuronectes americanus with stable isotopes. Marine Ecology - Progress Series 2002, 236:233-240.
10. Bros W.E., Cowell B.C. A technique for optimizing sample size (replication). Journal of Experimental Marine Biology and Ecology 1987, 114:63-71.
11. Carmichael R.H., Hattenrath T., Valiela I., Michener R.H. Nitrogen stable isotopes in the shell of Mercenaria mercenaria trace wastewater inputs from watersheds to estuarine ecosystems. Aquatic Biology 2008, 4:99-111.
12. Chesapeake Bay Program, 2004. Chesapeake Bay Program Analytical Segmentation Scheme: Revisions, Decisions and Rationales 1983-2003. Chesapeake Bay Program Monitoring and Analysis Subcommittee Tidal Monitoring and Analysis Workgroup. Annapolis, Maryland, 72 pp.
13. Cline J.D., Kaplan I.R. Isotopic fractionation of dissolved nitrate during denitrification in the eastern tropical North Pacific Ocean. Marine Chemistry 1975, 3:271-299.
14. Cohen R.A., Fong P. Using opportunistic green macroalgae as indicators of nitrogen supply and sources to estuaries. Ecological Applications 2006, 16:1405-1420.
15. Cole M.L., Valiela I., Kroeger K.D., Tomasky G.L., Cebrian J., Wigand C., McKinney R.A., Grady S.P., da Silva M.H.C. Assessment of a delta N-15 isotopic method to indicate anthropogenic eutrophication in aquatic ecosystems. Journal of Environmental Quality 2004, 33:124-132.
16. Cole M.L., Kroeger K.D., McClelland J.W., Valiela I. Effects of watershed land use on nitrogen concentrations and delta (15) nitrogen in groundwater. Biogeochemistry 2006, 77:199-215.
17. Coleman D.C., Fry B. Carbon Isotope Techniques 1991, Academic Press, San Diego. first ed.
18. Costanzo S.D., O'Donohue M.J., Dennison W.C., Loneragan N.R., Thomas M. A new approach for detecting and mapping sewage impacts. Marine Pollution Bulletin 2001, 42:149-156.
19. Dame R.F. The ecological energies of growth, respiration and assimilation in the intertidal American oyster Crassostrea virginica. Marine Biology 1972, 17:243-250.
20. Daskin J.H., Calci K.R., Burkhardt W.I., Carmichael R.H. Use of N stable isotope and microbial analyses to define wastewater influence in Mobile Bay, AL. Marine Pollution Bulletin 2008, 56:860-868.
21. Dattagupta S., Bergquist D.C., Szalai E.B., Macko S.A., Fisher C.R. Tissue carbon, nitrogen, and sulfur stable isotope turnover in transplanted Bathymodiolus childressi mussels: relation to growth and physiological condition. Limnology and Oceanography 2004, 49:1144-1151.
22. D'Elia C.F., Steudler P.A., Corwin N. Determination of total nitrogen in aqueous samples using persulfate digestion. Limnology and Oceanography 1977, 22:760-764.
23. Elliott E.M., Brush G.S. Sedimented organic nitrogen isotopes in freshwater wetlands record long-term changes in watershed nitrogen source and land use. Environmental Science and Technology 2006, 40:2910-2916.
24. 15N in Maryland's Coastal Bays. Estuaries and Coasts 2009, 32:773-786.
25. Fila L., Carmichael R.H., Shriver A., Valiela I. Stable N isotopic signatures in bay scallop tissue, feces, and pseudofeces in Cape Cod estuaries subject to different N loads. Biological Bulletin 2001, 201:294-296.
26. Finlay J.C., Kendall C. Stable isotope tracing of temporal and spatial variability in organic matter sources to freshwater ecosystems. Stable Isotopes in Ecology and Environmental Science 2007, 283-333. Blackwell Publishing. R.H. Michener, K. Lajtha (Eds.).
27. Ford S.E., Smolowitz R. Infection dynamics of an oyster parasite in its newly expanded range. Marine Biology 2007, 151:119-133.
28. Ford S.E., Cummings M.J., Powell E.N. Estimating mortality in natural assemblages of oysters. Estuaries and Coasts 2006, 29:361-374.
29. Fourqurean J.W., Moore T.O., Fry B., Hollibaugh J.T. Spatial and temporal variation in C:N:P ratios, del15N, and del13C of eelgrass Zostera marina as indicators of ecosystem processes, Tomales Bay, California, USA. Marine Ecology Progress Series 1997, 157:147-157.
30. 15N of Thalassia testudinum from South Florida and its implications for ecosystem studies. Estuaries and Coasts 2005, 28:447-461.
31. Fourqurean J.W., Marba N., Duarte C.M., Diaz-Almela E., Ruiz-Halpern S. Spatial and temporal variation in the elemental and stable isotopic content of the seagrasses Posidonia oceanica and Cymodocea nodosa from the Illes Balears, Spain. Marine Biology 2007, 151:219-232.
32. Frazer T.K., Ross R.M., Quetin L.B., Montoya J.P. Turnover of carbon and nitrogen during growth of larval krill, Euphausia superba Dana: a stable isotope approach. Journal of Experimental Marine Biology and Ecology 1997, 212:259-275.
33. Fry B. Stable Isotope Ecology 2006, Springer, New York. first ed.
34. Fry B., Allen Y.C. Stable isotopes in zebra mussels as bioindicators of river-watershed linkages. River Research and Applications 2003, 19:683-696.
35. Fry B., Gace A., McClelland J.W. Chemical indicators of anthropogenic nitrogen-loading in four Pacific estuaries. Pacific Science 2003, 57:77-101.
36. Fuller B.T., Fuller J.L., Sage N.E., Harris D.A., O'Connell T.C., Hedges R.E.M. Nitrogen balance and delta N-15: why you're not what you eat during nutritional stress. Rapid Communications in Mass Spectrometry 2005, 19:2497-2506.
37. 15N signatures of different functional forms of macroalgae and filter-feeders to reveal temporal and spatial patterns in sewage dispersal. Marine Ecology Progress Series 2002, 235:63-73.
38. Garton D.W., Payne C.D., Montoya J.P. Flexible diet and trophic position of dreissenid mussels as inferred from stable isotopes of carbon and nitrogen. Canadian Journal of Fisheries and Aquatic Sciences 2005, 62:1119-1129.
39. Gaye-Siessegger J., Focken U., Abel H., Becker K. Individual protein balance strongly influences delta N-15 and delta C-13 values in Nile tilapia, Oreochromis niloticus. Naturwissenschaften 2004, 91:90-93.
40. Grant M., Kopple R.V. A stable isotope investigation into the feeding behavior of Brychius hungerfordi Spangler (Coleoptera: Haliplidae), a federally endangered crawling water beetle. The Coleopterists Bulletin 2009, 63:71-83.
41. Griffin M.P.A., Valiela I. Delta N-15 isotope studies of life history and trophic position of Fundulus heteroclitus and Menidia menidia. Marine Ecology Progress Series 2001, 214:299-305.
42. Haubert D., Langel R., Scheu S., Ruess L. Effects of food quality, starvation and life stage on stable isotope fractionation in Collembola. Pedobiologia 2005, 49:229-237.
43. 13C of coral tissue show significant inter-reef variation. Coral Reefs 2000, 19:189-193.
44. Hobson K.A., Clark R.G. Assessing avian diets using stable isotopes. 2. Factors influencing diet-tissue fractionation. Condor 1992, 94:189-197. (Heikoop).
45. Hobson K.A., Alisauskas R.T., Clark R.G. Stable-nitrogen isotope enrichment in avian-tissues due to fasting and nutritional stress - implications for isotopic analyses of diet. Condor 1993, 95:388-394.
46. Hoch M.P., Fogel M.L., Kirchman D.L. Isotope fractionation associated with ammonium uptake by a marine bacterium. Limnology and Oceanography 1992, 37:1447-1459.
47. Hübner H. Isotope effects of nitrogen in the soil and biosphere. Handbook of Environmental Isotope Geochemistry. The Terrestrial Environment 1986, Vol. 2B:361-425. Elsevier, Amsterdam.
48. Jin Z.F., Chen Y.X., Wang F., Ogura N. Detection of nitrate sources in urban groundwater by isotopic and chemical indicators, Hangzhou City, China. Environmental Geology 2004, 45:1017-1024.
49. Kemp W.M., Boynton W.R., Adolf J.E., Boesch D.F., Boicourt W.C., Brush G., Cornwell J.C., Fisher T.R., Glibert P.M., Hagy J.D., Harding L.W., Houde E.D., Kimmel D.G., Miller W.D., Newell R.I.E., Roman M.R., Smith E.M., Stevenson J.C. Eutrophication of Chesapeake Bay: historical trends and ecological interactions. Marine Ecology Progress Series 2005, 303:1-29.
50. Kendall C. Tracing nitrogen sources and cycling in catchments. Isotope Tracers in Catchment Hydrology 1998, 519-576. Elsevier Science B.V., Amsterdam. C. Kendall, J.J. McDonnell (Eds.).
51. Kennedy V.S., Shaw K.S., Newell R.I.E. Discriminatory predation by three invertebrates on eastern oysters (Crassostrea virginica) compared with non-native Suminoe oysters (C. ariakensis). Invertebrate Biology 2009, 128:16-25.
52. Kerouel R., Aminot A. Procédure optimisée hors-contaminations pour l'analyze des éléments nutritifs dissous dans l'eau de mer. Marine Environmental Research 1987, 22:19-32.
53. Kimbrough K.L., Johnson W.E., Lauenstein G.G., Christensen J.D., Apeti D.A. An Assessment of Two Decades of Contaminant Monitoring in the Nation's Coastal Zone 2008, NOAA, Silver Spring, MD, USA.
54. Knowles R., Blackburn T.H. Nitrogen Isotope Techniques 1993, Academic Press, Inc., Harcourt Brace Jovanovich, San Diego.
55. Lake J.L., McKinney R.A., Osterman F.A., Pruell R.J., Kiddon J., Ryba S.A., Libby A.D. Stable nitrogen isotopes as indicators of anthropogenic activities in small freshwater systems. Canadian Journal of Fisheries and Aquatic Science 2001, 58:870-878.
56. Langdon C.J., Newell R.I.E. Digestion and nutrition in larvae and adults. The Eastern Oyster Crassostrea virginica 1996, 231-260. Maryland Sea Grant, College Park, MD, USA. V.S. Kennedy, R.I.E. Newell, A.F. Eble (Eds.).
57. Lefebvre S., Clement J.-C., Pinay G., Thenail C., Durand P., Marmonier P. 15N-Nitrate signature in low-order streams: effects of land cover and agricultural practices. Ecological Applications 2007, 17:2333-2346.
58. Lorrain A., Paulet Y.M., Chauvaud L., Savoye N., Donval A., Saout C. Differential delta C-13 and delta N-15 signatures among scallop tissues: implications for ecology and physiology. Journal of Experimental Marine Biology and Ecology 2002, 275:47-61.
59. Macko S.A., Ostrom N.E. Pollutions studies using nitrogen isotopes. Stable Isotopes in Ecology and Environmental Science 1994, 45-62. Blackwell Scientific Publishers, Oxford. K. Lajtha, R.M. Michener (Eds.).
60. Mariotti A., Germon J.C., Leclerc A. Nitrogen isotope fractionation associated with the NO2-→N2O step of denitrification in soils. Canadian Journal of Soil Science 1982, 62:227-241.
61. Matthews B., Mazumder A. Consequences of large temporal variability of zooplankton delta N-15 for modeling fish trophic position and variation. Limnology and Oceanography 2005, 50:1404-1414.
62. McClelland J.W., Valiela I. Linking nitrogen in estuarine producers to land-derived sources. Limnology and Oceanography 1998, 43:577-585.
63. McClelland J.W., Valiela I., Michener R.H. Nitrogen-stable isotope signatures in estuarine food webs: a record of increasing urbanization in coastal watersheds. Limnology and Oceanography 1997, 42:930-937.
64. McIlvin M.R., Altabet M.A. Chemical conversion of nitrate and nitrite to nitrous oxide for nitrogen and oxygen isotopic analysis in freshwater and seawater. Analytical Chemistry 2005, 77:5589-5595.
65. McKinney R.A., Nelson W.G., Wigand C., Charpentier M.A. Ribbed mussel nitrogen isotope signatures reflect nitrogen sources in coastal salt marshes. Ecological Applications 2001, 11:203-214.
66. McKinney R.A., Lake J.L., Charpentier M.A., Ryba S.A. Using mussel isotope ratios to assess anthropogenic nitrogen inputs to freshwater ecosystems. Environmental Monitoring and Assessment 2002, 74:167-192.
67. Millero F.J. Chemical Oceanography 2005, CRC Press. third ed.
68. 15N and animal age. Geochimica et Cosmochimca Acta 1984, 48:1135-1140.
69. Montoya J.P., McCarthy J.J. Isotopic fractionation during nitrate uptake by phytoplankton grown in continuous culture. Journal of Plankton Research 1995, 17:439-464.
70. Moore, K.B., 2003. Uptake dynamics and sensitivity of oysters to detect sewage-derived nitrogen. University of the Sunshine Coast, p. 114.
71. Moore S.K., Suthers I.M. Can the nitrogen and carbon stable isotopes of the pygmy mussel, Xenostrobus securis, indicate catchment disturbance for estuaries in northern New South Wales, Australia?. Estuaries 2005, 28:714-725.
72. Newell, R.I.E., 1988. Ecological changes in Chesapeake Bay: are they the result of overharvesting the eastern oyster (Crassostrea virginica)? In: Lynch, M.P., Krome, E.C. (Eds.), Understanding the Estuary: Advances in Chesapeake Bay Research. Chesapeake Bay Research Consortium, Publication 129 (CBP/TRS 24/88), Gloucester Point, VA, pp. 536-546.
73. Newell R.I.E., Alspach G.S., Kennedy V.S., Jacobs D. Mortality of newly metamorphosed eastern oysters (Crassostrea virginica) in mesohaline Chesapeake Bay. Marine Biology 2000, 136:665-676.
74. 15N dynamics under bloom conditions. Limnology and Oceanography 1996, 41:451-459.
75. Piola R.F., Moore S.K., Suthers I.M. Carbon and nitrogen stable isotope analysis of three types of oyster tissue in an impacted estuary. Estuarine Coastal and Shelf Science 2006, 66:255-266.
76. Powell E.N., Ashton-Alcox K.A. A comparison between a suction dredge and a traditional oyster dredge in the transplantation of oysters in Delaware Bay. Journal of Shellfish Research 2004, 23:803-823.
77. Sakano H., Fujiwara E., Nohara S., Ueda H. Estimation of nitrogen stable isotope turnover rate of Oncorhynchus nerka. Environmental Biology of Fishes 2005, 72:13-18.
78. Schlacher T.A., Liddell B., Gaston T.F., Schlacher-Hoenlinger M. Fish track wastewater pollution to estuaries. Oecologia 2005, 144:570-584.
79. Shearer G., Kohl D.H. Nitrogen isotopic fractionation and O-18 exchange in relation to the mechanism of denitrification of nitrite by Pseudomonas stutzeri. Journal of Biological Chemistry 1988, 263:13231-13245.
80. Smith G.F., Bruce D.G., Roach E.B., Hansen A., Newell R.I.E., McManus A.M. Assessment of recent habitat conditions of eastern oyster Crassostrea virginica bars in mesohaline Chesapeake Bay. North American Journal of Fisheries Management 2005, 25:1569-1590.
81. Strickland J.D.H., Parsons T.R. A Practical Handbook of Seawater Analysis 1972, Alger Press, Ottawa, Canada.
82. Sweeny R.E., Kaplan I.R. Tracing flocculent industrial and domestic sewage transport on San Pedro Shelf, southern California, by nitrogen and sulphur isotope ratios. Marine Environmental Research 1980, 3:215-224.
83. Sweeting C.J., Jennings S., Polunin N.V.C. Variance in isotopic signatures as a descriptor of tissue turnover and degree of omnivory. Functional Ecology 2005, 19:777-784.
84. Tieszen L.L., Boutton T.W., Tesdahl K.G., Slade N.A. Fractionation and turnover of stable carbon isotopes in animal tissues: implications for del13C analysis of diet. Oecologia 1983, 57:32-37.
85. Tucker J., Sheats N., Giblin A.E., Hopkinson C.S., Montoya J.P. Using stable isotopes to trace sewage-derived material through Boston Harbor and Massachusetts Bay. Marine Environmental Research 1999, 48:353-375.
86. Udy J.W., Dennison W.C. Physiological responses of seagrasses used to identify anthropogenic nutrient inputs. Marine and Freshwater Research 1997, 48:605-614.
87. Ventura M., Catalan J. Incorporating life histories and diet quality in stable isotope interpretations of crustacean zooplankton. Freshwater Biology 2008, 53:1453-1469.
88. Vitoria L., Otero N., Soler A., Canals A. Fertilizer characterization: isotopic data (N, S, O, C, and Sr). Environmental Science and Technology 2004, 38:3254-3262.
89. 15N abundance in nitrogen of naturally occurring substances and global assessment of denitrification from isotopic viewpoint. Geochemical Journal 1975, 9:139-148.
90. Waser N.A.D., Harrison P.J., Nielsen B., Calvert S.E. Nitrogen isotope fractionation during the uptake and assimilation of nitrate, nitrite, ammonium, and urea by a marine diatom. Limnology and Oceanography 1998, 43:215-224.
91. Witting D.A., Chambers R.C., Bosley K.L., Wainright S.C. Experimental evaluation of ontogenetic diet transitions in summer flounder (Paralichthys dentatus), using stable isotopes as diet tracers. Canadian Journal of Fisheries and Aquatic Sciences 2004, 61:2069-2084.
92. York J.K., Tomasky G., Valiela I., Repeta D.J. Stable isotopic detection of ammonium and nitrate assimilation by phytoplankton in the Waquoit Bay estuarine system. Limnology and Oceanography 2007, 52:144-155.
93. 14N (δ15NH4+) at natural abundance levels in fresh and saltwaters. Analytical Chemistry 2007, 79:5297-5303.