Compound-specific δ15N amino acid measurements in littoral mussels in the California upwelling ecosystem: A new approach to generating baseline δ15N isoscapes for coastal ecosystems

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Vokhshoori, Natasha L ^a   McCarthy, Matthew D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; NITRATE; NITROGEN 15; PHENYLALANINE; NITROGEN;

ANIMAL TISSUE; ARTICLE; COASTAL WATERS; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ISOTOPE SPATIAL GRADIENT; ISOTOPE TRACING; LITTORAL; MYTILUS; MYTILUS CALIFORNIANUS; NITROGEN CONCENTRATION; NONHUMAN; PHYTOPLANKTON; PRIMARY PRODUCTION (BIOMASS); SEAWATER UPWELLING; UNITED STATES; WATER FLOW; WATER TRANSPORT; ANIMAL; AQUATIC SPECIES; BIVALVE; ECOSYSTEM; FOOD CHAIN; GEOGRAPHY; METABOLISM;

AMINO ACIDS; ANIMALS; AQUATIC ORGANISMS; BIVALVIA; CALIFORNIA; ECOSYSTEM; FOOD CHAIN; GEOGRAPHY; NITROGEN ISOTOPES;

EID: 84902338479     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0098087     Document Type: Article

References (60)

1. Graham BS, Koch PL, Newsome SD, McMahon KW, Aurioles D (2009) Using Isoscapes to Trace the Movements and Foraging Behavior of Top Predators in Oceanic Ecosystems Dordrecht: Springer Netherlands. pp. 299-318. doi:10.1007/978-90-481-3354-3-14.
2. McMahon KW, Ling Hamady L, Thorrold SR (2013) A review of ecogeochemistry approaches to estimating movements of marine animals. Limnol Oceangr 58: 697-714. doi:10.4319/lo.2013.58.2.0697.
3. Sigman DM, Kash KL, Casciotti KL (2009) Ocean process tracers: nitrogen isotopes in the ocean. Encyclopedia of ocean science, 2nd edn Elsevier, Amsterdam.
4. Liu Z, Altabet MA, Herbert TD (2008) Plio-Pleistocene denitrification in the eastern tropical North Pacific: Intensification at 2.1 Ma. Geochem Geophys Geosyst 9: n/a-n/a. doi:10.1029/2008GC002044.
5. Sherwood OA, Guilderson TP, Batista FC, Schiff JT, McCarthy MD (2013) Increasing subtropical North Pacific Ocean. Nature: 1-26.
6. Jackson JBC (2001) Historical Overfishing and the Recent Collapse of Coastal Ecosystems. Science 293: 629-637. doi:10.1126/science.1059199.
7. Ware DM, Thomson RE (2005) Bottom-up ecosystem trophic dynamics determine fish production in the Northeast Pacific. Science 308: 1280-1284. (Pubitemid 40746119)
8. DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. GEOCHIMICA ET COSMOCHIMICA ACTA 42: 495-506.
9. Vander Zanden M, Rasmussen JB (2001) Variation in δ15N and δ13C trophic fractionation: implications for aquatic food web studies. Limnol Oceangr 46: 2061-2066. (Pubitemid 34009955)
10. Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83: 703-718.
11. McCutchan JH, Lewis WM, Kendall C, McGrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102: 378-390. (Pubitemid 36914279)
12. Vanderklift MA, Ponsard S (2003) Sources of variation in consumer-diet ?15N enrichment: a meta-analysis. Oecologia 136: 169-182. doi:10.1007/s00442- 003-1270-z. (Pubitemid 36933250)
13. Chikaraishi Y, Ogawa NO, Kashiyama Y, Takano Y, Suga H, et al. (2009) Determination of aquatic food-web structure based on compound-specific nitrogen isotopic composition of amino acids. Limnology and Oceanography: Methods 7: 740-750.
14. Chikaraishi Y, Kashiyama Y, Ogawa NO, Kitazato H, Ohkouchi N (2007) Metabolic control of nitrogen isotope composition of amino acids in macroalgae and gastropods: implications for aquatic food web studies. Mar Ecol Prog Ser 342: 85-90. (Pubitemid 47300560)
15. Popp BN, Graham BS, Olson RJ, Hannides C, Lott MJ, et al. (2007) Insight into the Trophic Ecology of Yellowfin Tuna, Thunnus albacares, from Compound-Specific Nitrogen Isotope Analysis of Proteinaceous Amino Acids. Terrestrial Ecology 1: 173-190. (Pubitemid 351734482)
16. Hannides CC, Popp BN, Landry MR, Graham BS (2009) Quantification of zooplankton trophic position in the North Pacific Subtropical Gyre using stable nitrogen isotopes. Limnol Oceangr 54: 50.
17. Dale JJ, Wallsgrove NJ, Popp BN, Holland KN (2011) Nursery habitat use and foraging ecology of the brown stingray Dasyatis lata determined from stomach contents, bulk and amino acid stable isotopes. Mar Ecol Prog Ser 433: 221-236. doi:10.3354/meps09171.
18. Germain LR, Koch PL, Harvey J, McCarthy MD (2013) Nitrogen isotope fractionation in amino acids from harbor seals: implications for compound-specific trophic position calculations. Mar Ecol Prog Ser 482: 265-277.
19. Ruiz-Cooley RI, Ballance LT, McCarthy MD (2013) Range Expansion of the Jumbo Squid in the NE Pacific: d15N Decrypts Multiple Origins, Migration and Habitat Use. PLoS ONE 8: e59651. doi:10.1371/journal.pone.0059651.g003.
20. Hannides CCS, Popp BN, Anela Choy C, Drazen JC (2013) Midwater zooplankton and suspended particle dynamics in the North Pacific Subtropical Gyre: A stable isotope perspective. Limnol Oceangr 58: 1931-1946. doi:10.4319/lo.2013.58.6.1931.
21. Choy CA, Davison PC, Drazen JC, Flynn A, Gier EJ, et al. (2012) Global Trophic Position Comparison of Two Dominant Mesopelagic Fish Families (Myctophidae, Stomiidae) Using Amino Acid Nitrogen Isotopic Analyses. PLoS ONE 7: e50133. doi:10.1371/journal.pone.0050133.s005.
22. McCarthy MD, Lehman J, Kudela R (2013) Compound-specific amino acid Î15N patterns in marine algae: Tracer potential for cyanobacterial vs. eukaryotic organic nitrogen sources in the ocean. GEOCHIMICA ET COSMOCHIMICA ACTA 103: 104-120. doi:10.1016/j.gca.2012.10.037.
23. Sigman DM, DiFiore PJ, Hain MP, Deutsch C, Karl DM (2009) Sinking organic matter spreads the nitrogen isotope signal of pelagic denitrification in the North Pacific. 36: L08605. doi:10.1029/2008GL035784.
24. McCarthy MD, Benner R, Lee C, Fogel ML (2007) Amino acid nitrogen isotopic fractionation patterns as indicators of heterotrophy in plankton, particulate, and dissolved organic matter. GEOCHIMICA ET COSMOCHIMICA ACTA 71: 4727-4744. doi:10.1016/j.gca.2007.06.061. (Pubitemid 47560049)
25. Seminoff JA, Benson SR, Arthur KE, Eguchi T, Dutton PH, et al. (2012) Stable Isotope Tracking of Endangered Sea Turtles: Validation with Satellite Telemetry and d15N Analysis of Amino Acids. PLoS ONE 7: e37403. doi:10.1371/journal.pone.0037403.s002.
26. Kahru M, Mitchell BG (2000) Influence of the 1997-98 El Nifio on the surfacechlorophyll in. Geophys Res Lett 27: 2937-2940. Available: http://onlinelibrary.wiley.com/store/10.1029/2000GL011486/asset/grl13695.pdf?v= 1&t=hj1w7gpw&s=1ed5d0f26e9b4f694f3c377a2f099c51154a2858.
27. Ford HL, Schellenberg SA, Becker BJ, Deutschman DL, Dyck KA, et al. (2010) Evaluating the skeletal chemistry of Mytilus californianusas a temperature proxy: Effects of microenvironment and ontogeny. Paleoceanography 25: PA1203. doi:10.1029/2008PA001677.
28. Rykaczewski RR, Dunne JP (2010) Enhanced nutrient supply to the California Current Ecosystem with global warming and increased stratification in an earth system model. Geophys Res Lett 37: n/a-n/a. doi:10.1029/2010GL045019.
29. Rykaczewski RR, Checkley DM (2008) Influence of ocean winds on the pelagic ecosystem in upwelling regions. Proceedings of the National Academy of Sciences 105: 1965-1970. (Pubitemid 351439448)
30. Olson RJ, Popp BN, Graham BS, López-Ibarra GA, Galván-Magaña F, et al. (2010) Food-web inferences of stable isotope spatial patterns in copepods and yellowfin tuna in the pelagic eastern Pacific Ocean. Progress in Oceanography 86: 124-138. doi:10.1016/j.pocean.2010. 04.026.
31. Raikow DF, Hamilton SK (2001) Bivalve diets in a midwestern U.S. stream: A stable isotope enrichment study. Limnol Oceangr 46: 514-522. (Pubitemid 32434649)
32. Dobush GR, Ankney CD, Krementz DG (1985) The effect of apparatus, extraction time, and solvent type on lipid extractions of snow geese. Canadian Journal of Zoology 63: 1917-1920.
33. Asmus RM, Asmus H (1991) Mussel beds: limiting or promoting phytoplankton? Journal of Experimental Marine Biology and Ecology 148: 215-232.
34. Altabet MA, Pilskaln C, Thunell R, Pride C, Sigman D, et al. (1999) The nitrogen isotope biogeochemistry of sinking particles from the margin of the Eastern North Pacific. Deep-Sea Research Part I 46: 655-679. (Pubitemid 29147683)
35. Décima M, Landry MR, Popp BN (2013) Environmental perturbation effects on baseline δ15N values and zooplankton trophic flexibility in the southern California Current Ecosystem. Limnol Oceangr 58: 624-634. doi:10.4319/lo.2013.58.2.0624.
36. Voss M, Dippner JW, Montoya JP (2001) Nitrogen isotope patterns in the oxygen-deficient waters of the Eastern Tropical North Pacific Ocean. Deep-Sea Research Part I 48: 1905-1921. (Pubitemid 32507443)
37. Larsen T, Ventura M, Andersen N, O'Brien DM, Piatkowski U, et al. (2013) Tracing Carbon Sources through Aquatic and Terrestrial Food Webs Using Amino Acid Stable Isotope Fingerprinting. PLoS ONE 8: e73441. doi:10.1371/journal. pone.0073441.s010.
38. Vokhshoori NL, Larsen T, McCarthy MD (2014) Reconstructing δ13C isoscapes of phytoplankton production in a coastal upwelling system with amino acid isotope values of littoral mussels. Mar Ecol Prog Ser. doi:10.3354/ meps10746.
39. 13C isoscapes for the California Upwelling Ecosystem. Master's Thesis. Santa Cruz: University of California, Santa Cruz. 125 pp.
40. Gruber N, Sarmiento JL (1997) Global patterns of marine nitrogen fixation and denitrification. Global Biogeochem Cycles 11: 235-266.
41. Cline JD, Richards FA (1972) Oxygen deficient conditions and nitrate reduction in the eastern tropical North Pacific Ocean. Limnol Oceangr: 885-900.
42. Codispoti LA, Richards FA (1976) An analysis of the horizontal regime of denitrification in the eastern tropical North Pacific. Limnol Oceanogr 21: 379-388.
43. White AE, Foster RA, Benitez-Nelson CR, Masqué P, Verdeny E, et al. (2013) Nitrogen fixation in the Gulf of California and the Eastern Tropical North Pacific. Progress in Oceanography 109: 1-17. Available: http://www.sciencedirect.com/science/article/pii/S0079661112001115.
44. Sigman DM, Granger J, DiFiore PJ, Lehmann MM, Ho R, et al. (2005) Coupled nitrogen and oxygen isotope measurements of nitrate along the eastern North Pacific margin. Global Biogeochem Cycles 19: n/a-n/a. doi:10.1029/2005GB002458.
45. Somes CJ, Schmittner A, Altabet MA (2010) Nitrogen isotope simulations show the importance of atmospheric iron deposition for nitrogen fixation across the Pacific Ocean. Geophys Res Lett 37.
46. Schwing FB, O'Farrell M, Steger JM, Baltz K (1996) Coastal Upwelling indices west coast of North America. NOAA Tech Rep NMFS SWFSC 231: 144.
47. Sigman DM, Robinson R, Knapp AN, van Geen A, McCorkle DC, et al. (2003) Distinguishing between water column and sedimentary denitrification in the Santa Barbara Basin using the stable isotopes of nitrate. Geochem Geophys Geosyst 4: n/a-n/a. doi:10.1029/2002GC000384.
48. Checkley DM Jr, Barth JA (2009) Patterns and processes in the California Current System. Progress in Oceanography 83: 49-64. doi:10.1016/j.pocean.2009. 07.028.
49. Kienast SS, Calvert SE, Pedersen TF (2002) Nitrogen isotope and productivity variations along the northeast Pacific margin over the last 120 kyr: Surface and subsurface paleoceanography. Paleoceanography 17: 7-1-7-17. doi:10.1029/2001PA000650.
50. Grantham BA, Chan F, Nielsen KJ, Fox DS, Barth JA, et al. (2004) Upwelling-driven nearshore hypoxia signals ecosystem and oceanographic changes in the northeast Pacific. Nature 429: 749-754. (Pubitemid 38833124)
51. Brandes JA, Devol AH, Deutsch C (2007) New Developments in the Marine Nitrogen Cycle. Chem Rev 107: 577-589. doi:10.1021/cr050377t. (Pubitemid 46381034)
52. Waser N, Harrison PJ, Nielsen B, Calvert SE, Turpin DH (2010) Nitrogen isotope fractionation during the uptake and assimilation of nitrate, nitrite, ammonium, and urea by a marine diatom. Limnol Oceangr 43: 215-224. Available: http://www.jstor.org.oca.ucsc.edu/stable/pdfplus/2839209.pdf?acceptTC= true&acceptTC=true&jpdConfirm=true.
53. Behrenfeld MJ, O'Malley RT, Siegel DA, McClain CR, Sarmiento JL, et al. (2006) Climate-driven trends in contemporary ocean productivity. Nature 444: 752-755. doi:10.1038/nature05317. (Pubitemid 44949603)
54. Aksnes DL, Ohman MD (2009) Multi-decadal shoaling of the euphotic zone in the southern sector of the California Current System. Limnol Oceangr 54: 1272.
55. Polovina JJ, Howell EA, Abecassis M (2008) Ocean's least productive waters are expanding. Geophys Res Lett 35: L03618. doi:10.1029/2007GL031745.
56. McKinnell SM, Dagg MJ (2010) Marine ecosystems of the North Pacific Ocean, 2003-2008. PICES Special Publication 4: 393.
57. Rau GH, Ohman MD, Pierrot-Bults A (2003) Linking nitrogen dynamics to climate variability off central California: a 51 year record based on 15N/14N in CalCOFI zooplankton. Deep Sea Research Part II: Topical Studies in Oceanography 50: 2431-2447. doi:10.1016/S0967-0645(03)00128-0. (Pubitemid 37181377)
58. Duggins DO, Simenstad CA, ESTES JA (1989) Magnification of secondary production by kelp detritus in coastal marine ecosystems. Science 245: 170-173. (Pubitemid 20419197)
59. Bracken ME, Menge BA, Foley MM, Sorte CJ, Lubchenco J, et al. (2012) Mussel selectivity for high-quality food drives carbon inputs into open-coast intertidal ecosystems. Mar Ecol Prog Ser 459: 53-62. doi:10.3354/meps09764.
60. Lorrain A, Graham B, Ménard F, Popp B, Bouillon S, et al. (2009) Nitrogen and carbon isotope values of individual amino acids: a tool to study foraging ecology of penguins in the Southern Ocean. Mar Ecol Prog Ser 391: 293-306. doi:10.3354/meps08215.