Isotopic invisibility of protozoan trophic steps in marine food webs

Limnology and Oceanography

Volumn 59, Issue 5, 2014, Pages 1590-1598

  Gutiérrez Rodríguez, Andrés ^a,c   Décima, Moira ^a   Popp, Brian N ^b   Landry, Michael R ^a  

^a INTEGRATIVE OCEANOGRAPHY DIVISION   (United States)

^b UNIVERSITY OF HAWAII   (United States)

^c SORBONNE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84905038016     PISSN: 00243590     EISSN: None     Source Type: Journal    
DOI: 10.4319/lo.2014.59.5.1590     Document Type: Article

References (46)

1. AZAM, F., T. FENCHEL, J. FIELD, J. GRAY, L. MEYER-REIL, AND F. THINGSTAD. 1983. The ecological role of water-column microbes in the sea. Mar. Ecol. Prog. Ser. 10: 257-263, doi:10. 3354/meps010257
2. BEHRENFELD, M. J., AND OTHERS. 2006. Climate-driven trends in contemporary ocean productivity. Nature 444: 752-755, doi:10. 1038/nature05317
3. BODE, A., AND OTHERS. 2007. Stable nitrogen isotope studies of the pelagic food web on the Atlantic shelf of the Iberian Peninsula. Prog. Oceanogr. 74:115-131, doi:10. 1016/j. pocean. 2007. 04. 005
4. BOECKLEN, W. J., C. T. YARNES, B. A. COOK, AND A. C. JAMES. 2011. On the use of stable isotopes in trophic ecology. Ann. Rev. Ecol. Syst. 42:411-440, doi:10. 1146/annurev-ecolsys-102209-144726
5. BRANCH, T. A., AND OTHERS. 2010. The trophic fingerprint of marine fisheries. Nature468:431-435, doi:10. 1038/nature09528
6. CABANA, G., AND J. B. RASMUSSEN. 1996. Comparison of aquatic food chains using nitrogen isotopes. Proc. Nat. Acad. Sci. U. S. A. 93:10844-10847, doi:10. 1073/pnas. 93. 20. 10844
7. CALBET, A., AND M. R. LANDRY. 1999. Mesozooplankton influences on the microbial food web: Direct and indirect trophic interactions in the oligotrophic open ocean. Limnol. Oceanogr. 44:1370-1380, doi:10. 4319/lo. 1999. 44. 6. 1370
8. CALBET, A., AND M. R. LANDRY. 2004. Phytoplankton growth, microzooplankton grazing, and carbon cycling in marine systems. Limnol. Oceanogr. 49:51-57, doi:10. 4319/lo. 2004. 49. 1. 0051
9. CALLEJA, M. L., F. BATISTA, M. PEACOCK, R. KUDELA, AND M. D. MCCARTHY. 2013. Changes in compound specific d15N amino acid signatures andD/Lratios in marine dissolved organic matter induced by heterotrophic bacterial reworking. Mar. Chem. 149:32-44, doi:10. 1016/j. marchem. 2012. 12. 001
10. CAMPBELL, L., H. LIU, H. A. NOLLA, AND D. VAULOT. 1997. Annual variability of phytoplankton and bacteria in the subtropical North Pacific Ocean at Station ALOHA during the 1991-1994 ENSO event. Deep-Sea Res. Part I 44: 167-192, doi:10. 1016/S0967-0637(96)00102-1
11. CHIKARAISHI, Y., AND OTHERS. 2009. Determination of aquatic food-web structure based on compound-specific nitrogen isotopic composition of amino acids. Limnol. Oceanogr.: Meth. 7:740-750, doi:10. 4319/lom. 2009. 7. 740
12. CHOUVELON, T., AND OTHERS. 2012. Revisiting the use of d15Nin meso-scale studies of marine food webs by considering spatiotemporal variations in stable isotopic signatures-the case of an open ecosystem: The Bay of Biscay (North-East Atlantic). Prog. Oceanogr. 101:92-105, doi:10. 1016/j. pocean. 2012. 01. 004
13. DALE, J., N. WALLSGROVE, B. POPP, AND K. HOLLAND. 2011. Nursery habitat use and foraging ecology of the brown stingray Dasyatis latadetermined from stomach contents, bulk and amino acid stable isotopes. Mar. Ecol. Prog. Ser. 433:221-236, doi:10. 3354/meps09171
14. DÉCIMA, M., M. R. LANDRY, AND B. N. POPP. 2013. Environmental perturbation effects on baseline15N values and zooplankton trophic flexibility in the southern California Current Ecosystem. Limnol. Oceanogr. 58:624-634, doi:10. 4319/lo. 2013. 58. 2. 0624
15. DENIRO, M. J., AND S. EPSTEIN. 1981. Influence of diet on the distribution of nitrogen isotopes in animals. Geochim. Cosmochim. Acta45: 341-351, doi:10. 1016/0016-7037 (81)90244-1
16. DROOP, M. R. 1959. Water-soluble factors in the nutrition of Oxyrrhis marina. J. Mar. Biol. Assoc. U. K. 38:605-620, doi:10. 1017/S0025315400007037
17. FRY, B., AND R. B. QUIÑONES. 1994. Biomass spectra and stable isotope indicators of trophic level in zooplankton of the northwest Atlantic. Mar. Ecol. Prog. Ser. 112: 201-204, doi:10. 3354/meps112201
18. GARCIA, S. M., A. ZERBI, C. ALIAUME, T. DO CHI, AND G. LASSERRE. 2003. The ecosystem approach to fisheries. Issues, terminology, principles, institutional foundations, implementation and outlook. FAO Fish. Tech. Pap. Nu 443 Rome FAO.
19. GOLDMAN, J. C., D. A. CARON, O. K. ANDERSEN, AND M. R. DENNETT. 1985. Nutrient cycling in a microflagellate foodchain: I. Nitrogen dynamics. Mar. Ecol. Prog. Ser. 24: 231-242, doi:10. 3354/meps024231
20. HANNIDES, C. C. S., B. N. POPP, M. R. LANDRY, AND B. S. GRAHAM. 2009. Quantification of zooplankton trophic position in the North Pacific Subtropical Gyre using stable nitrogen isotopes. Limnol. Oceanogr. 54:50-61, doi:10. 4319/ lo. 2009. 54. 1. 0050
21. HOCH, M. P., R. A. SNYDER, AND L. A. CIGUENTES. 1996. Stable isotope dynamics of nitrogen recycled during interactions among marine bacteria and protists. Mar. Ecol. Prog. Ser. 132:229-239, doi:10. 3354/meps132229
22. ISAACS, J. D. 1972. Unstructured marine food webs and "pollutant analogues. " U. S. Natl. Mar. Fish. Serv. Fish. Bull. 70: 1053-1059.
23. KARL, D. M. 2002. Nutrient dynamics in the deep blue sea. Trends Microbiol. 10:410-418, doi:10. 1016/S0966-842X(02)02430-7
24. KAUNZINGER, C. M. K., AND P. J. MORIN. 1998. Productivity controls food-chain properties in microbial communities. Nature395:495-497, doi:10. 1038/26741
25. LEGENDRE, L., AND F. RASSOULZADEGAN. 1996. Food-web mediated export of biogenic carbon in oceans: Hydrodynamic control. Mar. Ecol. Prog. Ser. 145: 179-193, doi:10. 3354/ meps145179
26. MACKO, S. A., M. E. UHLE, M. H. ENGEL, AND V. ANDRUSEVICH. 1997. Stable nitrogen isotope analysis of amino acid enantiomers by gas chromatography/combustion/isotope ratio mass spectrometry. Anal. Chem. 69:926-929, doi:10. 1021/ ac960956l
27. MCCLELLAN, J. W., AND J. P. MONTOYA. 2002. Trophic relationships and the nitrogen isotopic composition of amino acids in plankton. Ecology83:2173-2180, doi:10. 1890/0012-9658(2002)083[2173:TRATNI]2. 0. CO;2
28. METGES, C. C., K. PETZKE, AND U. HENNIG. 1996. Gas chromatography/combustion/isotope ratio mass spectrometric comparison of N-acetyl-and N-pivaloyl amino acid esters to measure 15 N isotopic abundances in physiological samples: A pilot study on amino acid synthesis in the upper gastrointestinal tract of minipigs. J. Mass. Spectrom. 31:367-376, doi:10. 1002/(SICI)1096-9888(199604)31:4, 367::AIDJMS310. 3. 0. CO;2-V
29. MINAGAWA, M., AND E. WADA. 1984. Stepwise enrichment of 15N along food chains: Further evidence and the relation between d15 N and animal age. Geochim. Cosmochim. Acta48: 1135-1140, doi:10. 1016/0016-7037(84)90204-7
30. PAULY, D., V. CHRISTENSEN, J. DALSGAARD, R. FROESE, AND F. TORRES, JR. 1998. Fishing down marine food webs. Science 279:860-863, doi:10. 1126/science. 279. 5352. 860
31. PETERSON, B., AND B. FRY. 1987. Stable isotopes in ecosystem studies. Ann. Rev. Ecol. Syst. 18: 293-320, doi:10. 1146/ annurev. es. 18. 110187. 001453
32. POMEROY, L. R. 1974. The ocean's food web, a changing paradigm. BioScience24:499-504, doi:10. 2307/1296885
33. POPP, B. N., AND OTHERS. 2007. Insight into the trophic ecology of yellowfin tuna, Thunnus albacares, from compound-specific nitrogen isotope analysis of proteinaceous amino acids, p. 173. InT. Dawson and R. Siegwolf [eds.], Stable isotopes as indicators of ecological change. Terrestrial Ecology Series Elsevier Academic Press.
34. POST, D. M. 2002a. Using stable isotopes to estimate trophic position: Models, methods, and assumptions. Ecology 83: 703-718, doi:10. 1890/0012-9658(2002)083[0703:USITET]2. 0. CO;2
35. POST, D. M. 2002b. The long and short of food-chain length. Trends. Ecol. Evol. 17:269-277, doi:10. 1016/S0169-5347(02)02455-2
36. RAU, G. H., J. L. TEYSSIE, F. RASSOULZADEGAN, AND S. W. FOWLER. 1990. 13 C/12C and15 N/14 N variations among sizefractionated marine particles: Implications for their origin and trophic relationships. Mar. Ecol. Prog. Ser. 59:33-38, doi:10. 3354/meps059033
37. ROLFF, C. 2000. Seasonal variation in d13C andd15 N of sizefractionated plankton at a coastal station in the northern Baltic proper. Mar. Ecol. Prog. Ser. 203:47-65, doi:10. 3354/ meps203047
38. ROSE, J. M., AND D. A. CARON. 2007. Does low temperature constrain the growth rates of heterotrophic protists? Evidence and implications for algal blooms in cold waters. Limnol. Oceanogr. 52:886-895, doi:10. 4319/lo. 2007. 52. 2. 0886
39. SCHMIDT, K., A. ATKINSON, M. VOSS, AND D. W. POND. 2006. Protozoans as a food source for Antarctic krill, Euphausia superba:Complementary insights from stomach content, fatty acids, and stable isotopes. Limnol. Oceanogr. 51:2409-2427, doi:10. 4319/lo. 2006. 51. 5. 2409
40. SHERR, E. B., AND B. F. SHERR. 2002. Significance of predation by protists in aquatic microbial food webs. Antonie Leeuwenhoek81:293-308, doi:10. 1023/A:1020591307260
41. SHERWOOD, O. A., M. F. LEHMANN, C. J. SCHUBERT, D. B. SCOTT, ANDM. D. MCCARTHY. 2011. Nutrient regime shift in the western North Atlantic indicated by compound-specificd15N of deep-sea gorgonian corals. Proc. Natl. Acad. Sci. U. S. A. 108:1011-1015, doi:10. 1073/pnas. 1004904108
42. SIMÓ, R. 2001. Production of atmospheric sulfur by oceanic plankton: Biogeochemical, ecological and evolutionary links. Trends. Microbiol. 16:287-294.
43. STRAILE, D. 1997. Gross growth efficiencies of protozoan and metazoan zooplankton and their dependence on food concentration, predator-prey weight ratio, and taxonomic group. Limnol. Oceanogr. 42: 1375-1385, doi:10. 4319/ lo. 1997. 42. 6. 1375
44. STROM, S. 2002. Novel interactions between phytoplankton and microzooplankton: Their influence on the coupling between growth and grazing rates in the sea. Hydrobiologia 480: 41-54, doi:10. 1023/A:1021224832646
45. UEDA, K., S. L. MORGAN, A. FOX, J. GILBART, A. SONESSON, L. LARSSON, AND G. ODHAM. 1989. D-alanine as a chemical marker for the determination of streptococcal cell wall levels in mammalian tissues by gas chromatography/negative ion chemical ionization mass spectrometry. Anal. Chem. 61: 265-270, doi:10. 1021/ac00178a015
46. WASER, N. A. D., P. J. HARRISON, B. NIELSEN, S. E. CALVERT, AND D. H. TURPIN. 1998. Nitrogen isotope fractionation during the uptake and assimilation of nitrate, nitrite, ammonium, and urea by a marine diatom. Limnol. Oceanogr. 43:215-224, doi:10. 4319/lo. 1998. 43. 2. 0215