Midwater zooplankton and suspended particle dynamics in the North Pacific Subtropical Gyre: A stable isotope perspective

Limnology and Oceanography

Volumn 58, Issue 6, 2013, Pages 1931-1946

  Hannides, Cecelia C S ^a,b   Popp, Brian N ^a   Anela Choy, C ^a   Drazen, Jeffrey C ^a  

^a UNIVERSITY OF HAWAII   (United States)

^b CYPRUS INSTITUTE   (Cyprus)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; FOOD WEB; FRACTIONATION; GYRE; HETEROTROPHY; ISOTOPIC ANALYSIS; MESOPELAGIC ZONE; NUTRIENT ENRICHMENT; SURFACE WATER; SUSPENDED PARTICULATE MATTER; TROPHIC LEVEL; WATER DEPTH; ZOOPLANKTON;

PACIFIC OCEAN; PACIFIC OCEAN (SUBTROPICAL);

EID: 84884550623     PISSN: 00243590     EISSN: None     Source Type: Journal    
DOI: 10.4319/lo.2013.58.6.1931     Document Type: Article

References (74)

1. ABRAMSON, L., C. LEE, Z. LIU, S. G. WAKEHAM, and J. SZLOSEK. 2010. Exchange between suspended and sinking particles in the northwest Mediterranean as inferred from the organic composition of in situ pump and sediment trap samples. Limnol. Oceanogr. 55: 725-739. doi:10.4319/lo.2009.55.2. 0725.
2. Al-Mutairi, H., and M. R. LANDRY. 2001. Active export of carbon and nitrogen at Station ALOHA by diel migrant zooplankton. Deep-Sea Res. II 48: 2083-2103. doi:10.1016/ S0967-0645(00)00174-0.
3. Alonso-Gonzalez, I. J., and OTHERS. 2010. Role of slowly settling particles in the ocean carbon cycle. Geophys. Res. Lett. 37: L13608. doi:10.1029/2010GL043827.
4. Alonso-Saez, L., and OTHERS. 2012. Role for urea in nitrification by polar marine Archaea. Proc. Natl. Acad. Sci. USA 109: 17989-17994. doi:10.1073/pnas.1201914109.
5. ALTABET, M. A. 1990. Organic C, N, and stable isotopic composition of particulate matter collected on glass-fiber and aluminum-oxide filters. Limnol. Oceanogr. 35: 902-909. doi:10.4319/lo.1990.35.4.0902.
6. ALTABET, M. A, W. G. DEUSER, S. HONJO, and C. STEINEN. 1991. Seasonal and depth-related changes in the source of sinking particles in the North Atlantic. Nature 354: 136-139. doi:10.1038/ 354136a0.
7. ALTABET, M. A, and J. J. MCCARTHY. 1986. Vertical patterns in 15N natural abundance in PON from the surface waters of warmcore rings. J. Mar. Res. 44: 185-201. doi:10.1357/002224086 788460148.
8. AMON, R. M. W., and R. BENNER. 1996. Bacterial utilization of different size classes of dissolved organic matter. Limnol. Oceanogr. 41: 41-51. doi:10.4319/lo.1996.41.1.0041.
9. AMON, R. M. W, H. P. FITZNAR, and R. BENNER. 2001. Linkages among the bioreactivity, chemical composition, and diagenetic state of marine dissolved organic matter. Limnol. Oceanogr. 46: 287-297. doi:10.4319/lo.2001.46.2.0287.
10. ANGEL, M. V., and A. C. BAKER. 1982. Vertical distribution of the standing crop of plankton and micronekton at three stations in the northeast Atlantic. Biol. Oceanogr. 2: 1-29.
11. ANGEL, M. V, P. HARGREAVES, P. KIRKPATRICK, and P. DOMANSKI. 1982. Low variability in planktonic and micronektonic populations at 1,000 m depth in the vicinity of 42uN, 17uW; evidence against diel migratory behavior in the majority of species. Biol. Oceanogr. 2: 287-319.
12. BACON, M. P., and R. F. ANDERSON. 1982. Distribution of thorium isotopes between dissolved and particulate forms. J. Geophys. Res. Oceans Atmos. 87: 2045-2056. doi:10.1029/ JC087iC03p02045.
13. BACON, M. P, C. A. HUH, A. P. FLEER, and W. G. DEUSER. 1985. Seasonality in the flux of natural radionuclides and plutonium in the deep Sargasso Sea. Deep-Sea Res. 32: 273-286. doi:10.1016/0198-0149(85)90079-2.
14. BALTAR, F., J. ARISTEGUI, J. M. GASOL, E. SINTES, and G. J. HERNDL. 2009. Evidence of prokaryotic metabolism on suspended particulate organic matter in the dark waters of the subtropical North Atlantic. Limnol. Oceanogr. 54: 182-193. doi:10.4319/lo.2009.54.1.0182.
15. BEMAN, J. M., B. N. POPP, and C. A. FRANCIS. 2008. Molecular and biogeochemical evidence for ammonia oxidation by marine Crenarchaeota in the Gulf of California. ISME J. 2: 429-441. doi:10.1038/ismej.2007.118.
16. BISHOP, J. K., J.M. EDMOND, D.R. KETTEN, M.P. BACON, and W. B. SILKER. 1977. The chemistry, biology, and vertical flux of particulate matter from the upper 400m of the equatorial Atlantic Ocean. Deep-Sea Res. 24: 511-548. doi:10.1016/ 0146-6291(77)90526-4.
17. BÖTTGER, R. 1987. The vertical distribution of micro- and small mesozooplankton in the central Red Sea. Biol. Oceanogr. 4: 383-403.
18. Böttger-Schnack, R. 1994. The microcopepod fauna in the eastern Mediterranean and Arabian Seas: A comparison with the Red Sea fauna. Hydrobiologia 292-293: 271-282. doi:10.1007/BF00229951.
19. BRODEUR, R. D., and O. YAMAMURA. 2005. Micronekton of the North Pacific. North Pacific Marine Science Organization (PICES) Scientific Report 30. Available from https://www.pices.int/publications/scientific_reports/
20. CALLEJA, M. L., F. BATISTA, M. PEACOCK, R. M. KUDELA, and M. D. MCCARTHY. 2013. Changes in compound specific d15N amino acid signatures and D/L ratios in marine dissolved organic matter induced by heterotrophic bacterial reworking. Mar. Chem. 149: 32-44. doi:10.1016/j.marchem.2012.12.001.
21. CASCIOTTI, K. L., T. W. TRULL, D. M. GLOVER, and D. DAVIES. 2008. Constraints on nitrogen cycling at the subtropical North Pacific Station ALOHA from isotopic measurements of nitrate and particulate nitrogen. Deep-Sea Res. II 55: 1661-1672. doi:10.1016/j.dsr2.2008.04.017.
22. CHIKARAISHI, Y., and OTHERS. 2009. Determination of aquatic food-web structure based on compound-specific nitrogen isotopic composition of amino acids. Limnol. Oceanogr.: Methods 7: 740-750. doi:10.4319/lom.2009.7.740.
23. CHIKARAISHI, Y, N. O. OGAWA, and N. OHKOUCHI. 2010. Further evaluation of the trophic level estimation based on nitrogen isotopic composition of amino acids, p. 37-51. In N. Ohkouchi, I. Tayasu, and K. Koba [eds.], Earth, life and isotopes. Kyoto Univ. Press.
24. CLARKE, T. A. 1978. Diel feeding patterns of 16 species of mesopelagic fishes from Hawaiian waters. Fish. Bull. 76: 495-513.
25. DALE, J. J., N. J. WALLSGROVE, B. N. POPP, and K. N. HOLLAND. 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.
26. DAUWE, B., J. J. MIDDELBURG, P. M. J. HERMAN, and C. H. R. HEIP. 1999. Linking diagenetic alteration of amino acids and bulk organic matter reactivity. Limnol. Oceanogr. 44: 1809-1814. doi:10.4319/lo.1999.44.7.1809.
27. DELONG, E. F., and D. M. KARL. 2005. Genomic perspectives in microbial oceanography. Nature 437: 336-342. doi:10.1038/ nature04157.
28. DILLING, L., and A. L. ALLDREDGE. 2000. Fragmentation of marine snow by swimming macrozooplankton: A new process impacting carbon cycling in the sea. Deep-Sea Res. I 47: 1227-1245. doi:10.1016/S0967-0637(99)00105-3.
29. DORE, J. E., and D. M. KARL. 1996. Nitrification in the euphotic zone as a source for nitrite, nitrate, and nitrous oxide at Station ALOHA. Limnol. Oceanogr. 41: 1619-1628. doi:10. 4319/lo.1996.41.8.1619.
30. EMEIS, K.-C., and OTHERS. 2010. External N inputs and internal N cycling traced by isotope ratios of nitrate, dissolved reduced nitrogen, and particulate nitrogen in the eastern Mediterranean Sea. J. Geophys. Res. Biogeosci. 115: G04041. doi:10.1029/2009JG001214.
31. GAEBLER, O. H., T. G. VITTI, and R. VUKMIROV. 1966. Isotope effects in metabolism of 14N and 15N from unlabeled dietary proteins. Can. J. Biochem. 44: 1249-1257. doi:10.1139/o66-142.
32. GOWING, M. M., and K. F. WISHNER. 1992. Feeding ecology of benthopelagic zooplankton on an eastern tropical Pacific seamount. Mar. Biol. 112: 451-467. doi:10.1007/BF00356291.
33. HANNIDES, C. C. S., M. R. LANDRY, C. R. Benitez-Nelson, R. M. STYLES, J. P. MONTOYA, and D. M. KARL. 2009a. Export stoichiometry and migrant-mediated flux of phosphorus in the North Pacific Subtropical Gyre. Deep-Sea Res. I 56: 73-88. doi:10.1016/j.dsr.2008.08.003.
34. STYLES, J. P, B. N. POPP, M. R. LANDRY, and B. S. GRAHAM. 2009b. 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.
35. HERNDL, G. J., T. REINTHALER, E. TEIRA, H. VAN AKEN, C. VETH, A. PERNTHALER, and J. PERNTHALER. 2005. Contribution of Archaea to total prokaryotic production in the deep Atlantic Ocean. Appl. Environ. Microbiol. 71: 2303-2309. doi:10.1128/ AEM.71.5.2303-2309.2005.
36. INGALLS, A. E., S. R. SHAH, R. L. HANSMAN, L. I. ALUWIHARE, G. M. SANTOS, E. R. M. DRUFFEL, and A. PEARSON. 2006. Quantifying archaeal community autotrophy in the mesopelagic ocean using natural radiocarbon. Proc. Natl. Acad. Sci. USA 103: 6442-6447. doi:10.1073/pnas.0510157103.
37. KAISER, K., and R. BENNER. 2008. Major bacterial contribution to the ocean reservoir of detrital organic carbon and nitrogen. Limnol. Oceanogr. 53: 99-112. doi:10.4319/lo.2008.53.1.0099.
38. KAISER, K, and R. BENNER. 2012. Organic matter transformations in the upper mesopelagic zone of the North Pacific: Chemical composition and linkages to microbial community structure. J. Geophys. Res. Oceans 117: C01023. doi:10.1029/2011JC007141.
39. KARL, D. M., M. J. CHURCH, J. E. DORE, R. M. LETELIER, and C. MAHAFFEY. 2012. Predictable and efficient carbon sequestration in the North Pacific Ocean supported by symbiotic nitrogen fixation. Proc. Natl. Acad. Sci. USA 109: 1842-1849. doi:10.1073/pnas.1120312109.
40. KARNER, M. B., E. F. DELONG, and D. M. KARL. 2001. Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409: 507-510. doi:10.1038/35054051.
41. KAWASAKI, N., R. SOHRIN, H. OGAWA, T. NAGATA, and R. BENNER. 2011. Bacterial carbon content and the living and detrital bacterial contributions to suspended particulate organic carbon in the North Pacific Ocean. Aquat. Microb. Ecol. 62: 165-176. doi:10.3354/ame01462.
42. KEIL, R. G., and M. L. FOGEL. 2001. Reworking of amino acid in marine sediments: Stable carbon isotopic composition of amino acids in sediments along the Washington coast. Limnol. Oceanogr. 46: 14-23. doi:10.4319/lo.2001.46.1.0014.
43. KONNEKE, M., A. E. BERNHARD, J. R. DE LA TORRE, C. B. WALKER, J. B. WATERBURY, and D. A. STAHL. 2005. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437: 543-546. doi:10.1038/nature03911.
44. KOPPELMANN, R., R. Bottger-Schnack, J. MOBIUS, and H. WEIKERT. 2009. Trophic relationships of zooplankton in the eastern Mediterranean based on stable isotope measurements. J. Plankton Res. 31: 669-686. doi:10.1093/plankt/fbp013.
45. KOPPELMANN, R, and H. WEIKERT. 2000. Transfer of organic matter in the deep Arabian Sea zooplankton community: Insights from d15N analysis. Deep-Sea Res. II 47: 2653-2672. doi:10.1016/ S0967-0645(00)00043-6.
46. KOPPELMANN, R, and N. LAHAJNAR. 2003. Vertical distribution of mesozooplankton and its d15N signature at a deep-sea site in the Levantine Sea (eastern Mediterranean) in April 1999. J. Geophys. Res. Oceans 108: 8118. doi:10.1029/2002JC001351.
47. LAAKMANN, S., and H. AUEL. 2010. Longitudinal and vertical trends in stable isotope signatures (d13C and d15N) of omnivorous and carnivorous copepods across the South Atlantic Ocean. Mar. Biol. 157: 463-471. doi:10.1007/s00227-009-1332-9.
48. LARSEN, T., D. L. TAYLOR, M. B. LEIGH, and D. M. O'BRIEN. 2009. Stable isotope fingerprinting: A novel method for identifying plant, fungal, or bacterial origins of amino acids. Ecology 90: 3526-3535. doi:10.1890/08-1695.1.
49. LARSEN, T, M. J. WOOLLER, M. L. FOGEL, and D. M. O'BRIEN. 2012. Can amino acid carbon isotope ratios distinguish primary producers in a mangrove ecosystem? Rapid Commun. Mass Spectrom. 26: 1541-1548. doi:10.1002/rcm.6259.
50. LEE, C., S. G. WAKEHAM, and J. I. HEDGES. 2000. Composition and flux of particulate amino acids and chloropigments in equatorial Pacific seawater and sediments. Deep-Sea Res. I 47: 1535-1568. doi:10.1016/S0967-0637(99)00116-8.
51. LONGHURST, A. R., and W. G. HARRISON. 1989. The biological pump: Profiles of plankton production and consumption in the upper ocean. Prog. Oceanogr. 22: 47-123. doi:10.1016/ 0079-6611(89)90010-4.
52. MACKO, S. A., M. L. FOGEL ESTEP, M. H. ENGEL, and S. R. HARE. 1986. Kinetic fractionation of stable nitrogen isotopes during amino acid transamination. Geochim. Cosmochim. Acta 50: 2143-2146. doi:10.1016/0016-7037(86)90068-2.
53. MARIOTTI, A., J. C. GERMON, P. HUBERT, P. KAISER, R. LETOLLE, A. TARDIEUX, and P. TARDIEUX. 1981. Experimental determination of nitrogen kinetic isotope fractionation: some principles; illustration for the denitrification and nitrification processes. Plant Soil 62: 413-430. doi:10.1007/BF02374138.
54. MCCARTHY, M. D., R. BENNER, C. LEE, and M. L. FOGEL. 2007. Amino acid nitrogen isotopic fractionation patterns as indicators of heterotrophy in plankton, particulate, and dissolved organic matter. Geochim. Cosmochim. Acta 71: 4727-4744. doi:10.1016/j.gca.2007.06.061.
55. MCCARTHY, M. D., R. BENNER, C. LEE, J. I. HEDGES, and M. L. FOGEL. 2004. Amino acid carbon isotopic fractionation patterns in oceanic dissolved organic matter: An unaltered photoautotrophic source for dissolved organic nitrogen in the ocean? Mar. Chem. 92: 123-134. doi:10.1016/j.marchem.2004.06.021.
56. MCCLELLAND, J. W., and J. P. MONTOYA. 2002. Trophic relationships and the nitrogen isotopic composition of amino acids in plankton. Ecology 83: 2173-2180. doi:10.1890/0012- 9658(2002)083[2173:TRATNI]2.0.CO;2.
57. MINAGAWA, M., and E. WADA. 1984. Stepwise enrichment of 15N along food chains: Further evidence and the relation between d15N and animal age. Geochim. Cosmochim. Acta 48: 1135-1140. doi:10.1016/0016-7037(84)90204-7.
58. OUVERNEY, C. C., and J. A. FUHRMAN. 2000. Marine planktonic Archaea take up amino acids. Appl. Environ. Microbiol. 66: 4829-4833. doi:10.1128/AEM.66.11.4829-4833.2000.
59. POPP, B. N., and OTHERS. 2007. Insight into the trophic ecology of yellowfin tuna, Thunnes albacares, from compound-specific nitrogen isotope analysis of proteinaceous amino acids, p. 173-190. In T. D. Dawson and R. T. W. Siegwolf [eds.], Stable isotopes as indicators of ecological change. Elsevier.
60. R CORE TEAM. 2012. R: A language and environment for statistical computing. R Foundation for Statistical Computing.
61. RAU, G. H., J. L. TEYSSIE, F. RASSOULZADEGAN, and S. W. FOWLER. 1990. 13C/12C and 15N/14N variations among sizefractionated marine particles: Implications for their origin and trophic relationships. Mar. Ecol. Prog. Ser. 59: 33-38. doi:10.3354/meps059033.
62. ROBINSON, C., and OTHERS. 2010. Mesopelagic zone ecology and biogeochemistry-a synthesis. Deep-Sea Res. II 57: 1504-1518. doi:10.1016/j.dsr2.2010.02.018.
63. SAINO, T., and A. HATTORI. 1980. 15N natural abundance in oceanic suspended particulate matter. Nature 283: 752-754. doi:10.1038/283752a0.
64. SAINO, T., and A. HATTORI. 1987. Geographical variation of the water column distribution of suspended particulate organic nitrogen and its 15N abundance in the Pacific and its marginal seas. Deep-Sea Res. I 34: 807-827.
65. SCOTT, J. H., D. M. O'BRIEN, D. EMERSON, H. SUN, G. D. MCDONALD, A. SALGADO, and M. L. FOGEL. 2006. An examination of the carbon isotope effects associated with amino acid biosynthesis. Astrobiology 6: 867-880. doi:10.1089/ ast.2006.6.867.
66. SHERIDAN, C. C., C. LEE, S. G. WAKEHAM, and J. K. B. BISHOP. 2002. Suspended particle organic composition and cycling in surface and midwaters of the equatorial Pacific Ocean. Deep- Sea Res. I 49: 1983-2008. doi:10.1016/S0967-0637(02)00118-8.
67. SHERWOOD, O. A., M. F. LEHMANN, C. J. SCHUBERT, D. B. SCOTT, and M. D. MCCARTHY. 2011. Nutrient regime shift in the western North Atlantic indicated by compound-specific d15N of deep-sea gorgonian corals. Proc. Natl. Acad. Sci. USA 108: 1011-1015. doi:10.1073/pnas.1004904108.
68. SILFER, J. A., M. H. ENGEL, and S. A. MACKO. 1992. Kinetic fractionation of stable carbon and nitrogen isotopes during peptide bond hydrolysis: Experimental evidence and geochemical implications. Chem. Geol. 101: 211-221.
69. SILFER, J. A., M. H. ENGEL, and E. J. JUMEAU. 1991. Stable carbon isotope analysis of amino-acid enantiomers by conventional isotope ratio mass-spectrometry and combined gas-chromatography isotope ratio mass-spectrometry. Anal. Chem. 63: 370-374. doi:10.1021/ac00004a014.
70. STEINBERG, D. K., J. S. COPE, S. E. WILSON, and T. KOBARI. 2008a. A comparison of mesopelagic mesozooplankton community structure in the subtropical and subarctic North Pacific Ocean. Deep-Sea Res. II 55: 1615-1635. doi:10.1016/j.dsr2. 2008.04.025.
71. STEINBERG, D. K, B. A. S. VAN MOOY, K. O. BUESSELER, P. W. BOYD, T. KOBARI, and D. M. KARL. 2008b. Bacterial vs. zooplankton control of sinking particle flux in the ocean's twilight zone. Limnol. Oceanogr. 53: 1327-1338. doi:10.4319/lo.2008.53.4.1327.
72. VINOGRADOV, M. E., and V. B. TSEITLIN. 1983. Deep-sea pelagic domain (aspects of bioenergetics), p. 123-165. In G. T. Rowe [ed.], Deep-sea biology. Wiley.WALKER, B. D., and M. D. MCCARTHY. 2012. Elemental and isotopic characterization of dissolved and particulate organic matter in a unique California upwelling system: Importance of size and composition in the export of labile material. Limnol. Oceanogr. 57: 1757-1774.
73. WILSON, S. E., D. K. STEINBERG, and K. O. BUESSELER. 2008. Changes in fecal pellet characteristics with depth as indicators of zooplankton repackaging of particles in the mesopelagic zone of the subtropical and subarctic North Pacific Ocean. Deep-Sea Res. II 55: 1636-1647. doi:10.1016/j.dsr2.2008.04. 019.
74. WILSON, S. E., D. K. STEINBERG, F. L. E. CHU, and J. K. B. BISHOP. 2010. Feeding ecology of mesopelagic zooplankton of the subtropical and subarctic North Pacific Ocean determined with fatty acid biomarkers. Deep-Sea Res. I 57: 1278-1294. doi:10.1016/j.dsr. 2010.07.005