The role of particle associated microbes in remineralization of fecal pellets in the upper mesopelagic of the Scotia Sea, Antarctica

Limnology and Oceanography

Volumn 61, Issue 3, 2016, Pages 1049-1064

  Belcher, Anna ^a,b   Iversen, Morten ^c,d   Manno, Clara ^e   Henson, Stephanie A ^a   Tarling, Geraint A ^e   Sanders, Richard ^a  

^a NATIONAL OCEANOGRAPHY CENTRE   (United Kingdom)

^b UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^c ALFRED WEGENER INSTITUTE FOR POLAR AND MARINE RESEARCH   (Germany)

^d UNIVERSITY OF BREMEN   (Germany)

^e BRITISH ANTARCTIC SURVEY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ABUNDANCE; BOUNDARY LAYER; CARBON FLUX; FRAGMENTATION; GRAZING; MESOPELAGIC ZONE; MICROORGANISM; OXYGEN; PARTICULATE ORGANIC CARBON; REMINERALIZATION; RESPIRATION; ZOOPLANKTON;

ANTARCTICA; ATLANTIC OCEAN; SCOTIA SEA;

EUPHAUSIACEA;

EID: 84958259146     PISSN: None     EISSN: 19395590     Source Type: Journal    
DOI: 10.1002/lno.10269     Document Type: Article

References (74)

1. Alldredge, A. L. 1998. The carbon, nitrogen and mass content of marine snow as a function of aggregate size. Deep Sea Res. Part I Oceanogr. Res. Pap. 45: 529-541. doi:10.1016/S0967-0637(97)00048-4
2. Atkinson, A., K. Schmidt, S. Fielding, S. Kawaguchi, and P. A. Geissler . 2012. Variable food absorption by Antarctic krill: Relationships between diet, egestion rate and the composition and sinking rates of their fecal pellets. Deep Sea Res. Part II Top. Stud. Oceanogr. 59-60: 147-158. doi:10.1016/j.dsr2.2011.06.008
3. Berggren, M., J.-F. Lapierre, and P. A. del Giorgio . 2012. Magnitude and regulation of bacterioplankton respiratory quotient across freshwater environmental gradients. ISME J. 6: 984-93. doi:10.1038/ismej.2011.157
4. Borrione, I., and R. Schlitzer . 2013. Distribution and recurrence of phytoplankton blooms around South Georgia, Southern Ocean. Biogeosciences 10: 217-231. doi:10.5194/bg-10-217-2013
5. Boyd, P. W., and T. W. Trull . 2007. Understanding the export of biogenic particles in oceanic waters: Is there consensus? Prog. Oceanogr. 72: 276-312. doi:10.1016/j.pocean.2006.10.007
6. Broecker, W. S., and T. H. Peng . 1974. Gas exchange rates between air and sea. Tellus 26: 21-35. doi:10.1111/j.2153-3490.1974.tb01948.x
7. Buesseler, K. O., and P. W. Boyd . 2009. Shedding light on processes that control particle export and flux attenuation in the twilight zone of the open ocean. Limnol. Oceanogr. 54: 1210-1232. doi:10.4319/lo.2009.54.4.1210
8. Cavan, E. L., and others. 2015. Attenuation of particulate organic carbon flux in the Scotia Sea, Southern Ocean, controlled by zooplankton fecal pellets. Geochim. Cosmochim. Acta 42: 821-830. doi:10.1002/2014GL062744
9. Cnudde, C., C. Sanchez Clavano, T. Moens, A. Willems, and M. De Troch . 2013. Structural and functional patterns of active bacterial communities during aging of harpacticoid copepod fecal pellets. Aquat. Microb. Ecol. 71: 25-42. doi:10.3354/ame01663
10. Ebersbach, F., T. W. Trull, D. M. Davies, and S. G. Bray . 2011. Controls on mesopelagic particle fluxes in the Sub-Antarctic and Polar Frontal Zones in the Southern Ocean south of Australia in summer-perspectives from free-drifting sediment traps. Deep. Res. Part II 58: 2260-2276. doi:10.1016/j.dsr2.2011.05.025
11. Emerson, C., and J. Roff . 1987. Implications of fecal pellet size and zooplankton behaviour to estimates of pelagic-benthic carbon flux. Mar. Ecol. Prog. Ser. 35: 251-257. doi:10.3354/meps035251
12. Fielding, S., J. L. Watkins, M. A. Collins, P. Enderlein, and H. J. Venables . 2012. Acoustic determination of the distribution of fish and krill across the Scotia Sea in spring 2006, summer 2008 and autumn 2009. Deep. Res. Part II 59-60: 173-188. doi:10.1016/j.dsr2.2011.08.002
13. Fischer, G., and G. Karakas . 2009. Sinking rates and ballast composition of particles in the Atlantic Ocean: Implications for the organic carbon fluxes to the deep ocean. Biogeosciences 6: 85-102. doi:10.1007/s00531-007-0234-7
14. Giering, S. L. C., and others. 2014. Reconciliation of the carbon budget in the ocean's twilight zone. Nature 507: 480-483. doi:10.1038/nature13123
15. González, H. E. 1992. The distribution and abundance of krill faecal material and oval pellets in the Scotia and Weddell Seas (Antarctica) and their role in particle flux. Polar Biol. 12: 81-91. doi:10.1007/BF00239968
16. Hamner, W., P. Hamner, and B. Obst . 1989. Field observations on the ontogeny of schooling of Euphausia superba furciliae and its relationship to ice in Antarctic waters. Limnol. Oceanogr. 34: 451-456. doi:10.4319/lo.1989.34.2.0451
17. Hansen, B., F. L. Fotel, N. Jjensen, and S. D. Madsen . 1996. Bacteria associated with a marine planktonic copepod in culture. II. Degradation of fecal pellets produced on a diatom, a nanoflagellate or a dinoflagellate diet. J. Plankton Res. 18: 275-288. doi:10.1093/plankt/18.2.275
18. Henson, S. A., R. Sanders, E. Madsen, P. J. Morris, F. Le Moigne, and G. D. Quartly . 2011. A reduced estimate of the strength of the ocean's biological carbon pump. Geophys. Res. Lett. 38: L04606. doi:10.1029/2011GL046735
19. Henson, S. A., A. Yool, and R. Sanders . 2015. Variability in efficiency of particulate organic carbon export: A model study. Global Biogeochem. Cycles 29: 33-45. doi:10.1002/2014GB004965
20. Hewitt, R. P., and others. 2004. Biomass of Antarctic krill in the Scotia Sea in January/February 2000 and its use in revising an estimate of precautionary yield. Deep Sea Res. Part II Top. Stud. Oceanogr. 51: 1215-1236. doi:10.1016/S0967-0645(04)00076-1
21. Hilton, J., J. P. Lishman, S. Mackness, and S. I. Heaney . 1986. An automated method for the analysis of "particulate" carbon and nitrogen in natural waters. Hydrobiologia 141: 269-271. doi:10.1007/BF00014221
22. Iversen, M. H., and L. Poulsen . 2007. Coprorhexy, coprophagy, and coprochaly in the copepods Calanus helgolandicus, Pseudocalanus elongatus, and Oithona similis. Mar. Ecol. Prog. Ser. 350: 79-89. doi:10.3354/meps07095
23. Iversen, M. H., N. Nowald, H. Ploug, G. A. Jackson, and G. Fischer . 2010. High resolution profiles of vertical particulate organic matter export off Cape Blanc, Mauritania: Degradation processes and ballasting effects. Deep Sea Res. Part I Oceanogr. Res. Pap. 57: 771-784. doi:10.1016/j.dsr.2010.03.007
24. Iversen, M. H., and H. Ploug . 2013. Temperature effects on carbon-specific respiration rate and sinking velocity of diatom aggregates-potential implications for deep ocean export processes. Biogeosciences 10: 4073-4085. doi:10.5194/bg-10-4073-2013
25. Jing, H., L. Shek, W. Yung, X. Jin, and H. Liu . 2012. Dynamics of bacterial community composition during degradation of copepod fecal pellets. J. Plankton Res. 34: 700-710. doi:10.1093/plankt/fbs043
26. Köster, M., G. A. Paffenhöfer, R. Schluter, and A. Meuche . 2014. Time-series observations of prokaryotic colonization of zooplankton fecal pellets. J. Plankton Res. 36: 1461-1475. doi:10.1093/plankt/fbu060
27. Kwon, E. Y., F. Primeau, and J. L. Sarmiento . 2009. The impact of remineralization depth on the air-sea carbon balance. Nat. Geosci. 2: 630-635. doi:10.1038/ngeo612
28. Lam, P. J., and J. K. B. Bishop . 2007. High biomass, low export regimes in the Southern Ocean. Deep Sea Res. Part II Top. Stud. Oceanogr. 54: 601-638. doi:10.1016/j.dsr2.2007.01.013
29. Lampitt, R. S., T. Noji, and B. Von Bodungen . 1990. What happens to zooplankton faecal pellets? Implications for material flux. Mar. Biol. 104: 15-23. doi:10.1007/BF01313152
30. Laurenceau-Cornec, E. C., and others. 2015. The relative importance of phytoplankton aggregates and zooplankton fecal pellets to carbon export: Insights from free-drifting sediment trap deployments in naturally iron-fertilised waters near the Kerguelen Plateau. Biogeosciences 12: 1007-1027. doi:10.5194/bg-12-1007-2015
31. Manno, C., G. Stowasser, P. Enderlein, S. Fielding, and G. A. Tarling . 2015. The contribution of zooplankton faecal pellets to deep-carbon transport in the Scotia Sea (Southern Ocean). Biogeosciences 12: 1955-1965. doi:10.5194/bg-12-1955-2015
32. Marsay, C. M., R. J. Sanders, S. A. Henson, K. Pabortsava, E. P. Achterberg, and R. S. Lampitt . 2015. Attenuation of sinking particulate organic carbon flux through the mesopelagic ocean. Proc. Natl. Acad. Sci. U. S. A. 112: 1089-1094. doi:10.1073/pnas.1415311112
33. Martin, J. H., G. A. Knauer, D. M. Karl, and W. W. Broenkow . 1987. VERTEX: Carbon cycling in the northeast Pacific. Deep Sea Res. Part I Oceanogr. Res. Pap. 34: 267-285. doi:10.1016/0198-0149(87)90086-0
34. Mayor, D. J., R. Sanders, S. L. C. Giering, and T. R. Anderson . 2014. Microbial gardening in the ocean's twilight zone: Detritivorous metazoans benefit from fragmenting, rather than ingesting, sinking detritus. Bioessays 36: 1132-1137. doi:10.1002/bies.201400100
35. McDonnell, A. M. P., P. W. Boyd, and K. O. Buesseler . 2015. Effects of sinking velocities and microbial respiration rates on the attenuation of particulate carbon fluxes through the mesopelagic zone. Global Biogeochem. Cycles 29: 175-193. doi:10.1002/2014GB004935
36. Menden-Deuer, S., and E. J. Lessard . 2000. Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnol. Oceanogr. 45: 569-579. doi:10.4319/lo.2000.45.3.0569
37. Møller, E., P. Thor, and T. Nielsen . 2003. Production of DOC by Calanus finmarchicus, C. glacialis and C. hyperboreus through sloppy feeding and leakage from fecal pellets. Mar. Ecol. Prog. Ser. 262: 185-191. doi:10.3354/meps262185
38. Murphy, E. J., and others. 2007. Spatial and temporal operation of the Scotia Sea ecosystem: A review of large-scale links in a krill centred food web. Philos. Trans. R. Soc. B Biol. Sci. 362: 113-148. doi:10.1098/rstb.2006.1957
39. Nielsdóttir, M. C., and others. 2012. Seasonal and spatial dynamics of iron availability in the Scotia Sea. Mar. Chem. 130-131: 62-72. doi:10.1016/j.marchem.2011.12.004
40. Ploug, H. 2001. Small-scale oxygen fluxes and remineralization in sinking aggregates. Limnol. Oceanogr. 46: 1624-1631. doi:10.4319/lo.2001.46.7.1624
41. Ploug, H., M. Kühl, B. Buchholz-Cleven, and B. B. Jergensen . 1997. Anoxic aggregates-an ephemeral phenomenon in the pelagic environment? Aquat. Microb. Ecol. 13: 285-294. doi:10.3354/ame013285
42. Ploug, H., and B. B. Jorgensen . 1999. A net-jet flow system for mass transfer and microsensor studies of sinking aggregates. Mar. Ecol. Prog. Ser. 176: 279-290. doi:10.3354/meps176279
43. Ploug, H., and H.-P. Grossart . 2000. Bacterial growth and grazing on diatom aggregates: Respiratory carbon turnover as a function of aggregate size and sinking velocity. Limnol. Oceanogr. 45: 1467-1475. doi:10.4319/lo.2000.45.7.1467
44. Ploug, H., M. H. Iversen, M. Koski, and E. T. Buitenhuis . 2008. Production, oxygen respiration rates, and sinking velocity of copepod fecal pellets: Direct measurements of ballasting by opal and calcite. Limnol. Oceanogr. 53: 469-476. doi:10.4319/lo.2008.53.2.0469
45. Ploug, H., A. Terbruggen, A. Kaufmann, D. Wolf-gladrow, and U. Passow . 2010. A novel method to measure particle sinking velocity in vitro, and its comparison to three other in vitro methods. Limnol. Oceanogr.: Methods 8: 386-393. doi:10.4319/lom.2010.8.386
46. Poulsen, L., and T. Kiørboe . 2005. Coprophagy and coprorhexy in the copepods Acartia tonsa and Temora longicornis: Clearance rates and feeding behaviour. Mar. Ecol. Prog. Ser. 299: 217-227. doi:10.3354/meps299217
47. Poulsen, L., and M. H. Iversen . 2008. Degradation of copepod fecal pellets: Key role of protozooplankton. Mar. Ecol. Prog. Ser. 367: 1-13. doi:10.3354/meps07611
48. Prairie, J., and others. 2013. Delayed settling of marine snow at sharp density transitions driven by fluid entrainment and diffusion-limited retention. Mar. Ecol. Prog. Ser. 487: 185-200. doi:10.3354/meps10387
49. Reigstad, M., C. W. Riser, and C. Svensen . 2005. Fate of copepod faecal pellets and the role of Oithona spp. Mar. Ecol. Prog. Ser. 304: 265-270. doi:10.3354/meps304265
50. Rembauville, M., I. Salter, N. Leblond, A. Gueneugues, and S. Blain . 2015. Export fluxes in a naturally iron-fertilized area of the Southern Ocean-part 1: Seasonal dynamics of particulate organic carbon export from a moored sediment trap. Biogeosciences 12: 3153-3170. doi:10.5194/bg-12-3153-2015
51. Revsbech, N. P. 1989. An oxygen microsensor with a guard cathode. Limnol. Oceanogr. 34: 474-478. doi:10.4319/lo.1989.34.2.0474
52. Riley, J. S., R. Sanders, C. Marsay, F. Le Moigne, E. P. Achterberg, and A. J. Poulton . 2012. The relative contribution of fast and slow sinking particles to ocean carbon export. Global Biogeochem. Cycles 26: GB1026. doi:10.1029/2011GB004085
53. Roe, H. S. J., and D. M. Shale . 1979. A new multiple rectangular midwater trawl (RMT 1+8M) and some modifications to the institute of oceanographic sciences' RMT 1+8. Mar. Biol. 50: 283-288. doi:10.1007/BF00394210
54. Saborowski, R., S. Bröhl, G. A. Tarling, and F. Buchholz . 2002. Metabolic properties of Northern krill, Meganyctiphanes norvegica, from different climatic zones. I. Respiration and excretion. Mar. Biol. 140: 547-556. doi:10.1007/s00227-001-0730-4
55. Shek, L., and H. Liu . 2010. Oxygen consumption rates of fecal pellets produced by three coastal copepod species fed with a diatom Thalassiosira pseudonana. Mar. Pollut. Bull. 60: 1005-1009. doi:10.1016/j.marpolbul.2010.02.001
56. Smayda, T. J. 1970. The suspension and sinking of phytoplankton in the sea. Oceanogr. Mar. Biol. Annu. Rev. 8: 353-414. ISBN: 0080345085.
57. Steinberg, D. K., B. A. S. Van Mooy, K. O. Buesseler, P. W. Boyd, and D. M. Karl . 2008. 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
58. Suzuki, H., H. Sasaki, and M. Fukuchi . 2001. Short-term variability in the flux of rapidly sinking particles in the Antarctic marginal ice zone. Polar Biol. 24: 697-705. doi:10.1007/s003000100271
59. Suzuki, H., H. Sasaki, and M. Fukuchi . 2003. Loss processes of sinking fecal pellets of zooplankton in the mesopelagic layers of the Antarctic marginal ice zone. J. Oceanogr. 59: 809-818. doi:10.1023/B:JOCE.0000009572.08048.0d
60. Svensen, C., and J. C. Nejstgaard . 2003. Is sedimentation of copepod faecal pellets determined by cyclopoids? Evidence from enclosed ecosystems. J. Plankton Res. 25: 917-926. doi:10.1093/plankt/25.8.917
61. Svensen, C., C. Wexels Riser, M. Reigstad, and L. Seuthe . 2012. Degradation of copepod faecal pellets in the upper layer: Role of microbial community and Calanus finmarchicus. Mar. Ecol. Prog. Ser. 462: 39-49. doi:10.3354/meps09808
62. Svensen, C., N. Morata, and M. Reigstad . 2014. Increased degradation of copepod faecal pellets by co-acting dinoflagellates and Centropages hamatus. Mar. Ecol. Prog. Ser. 516: 61-70. doi:10.3354/meps10976
63. Thiele, S., B. M. Fuchs, R. Amann, and M. H. Iversen . 2014. Colonization in the photic zone and subsequent changes during sinking determines bacterial community composition in marine snow. Appl. Environ. Microbiol. 81: 1-34. doi:10.1128/AEM.02570-14
64. Thor, P., H. Dam, and D. Rogers . 2003. Fate of organic carbon released from decomposing copepod fecal pellets in relation to bacterial production and ectoenzymatic activity. Aquat. Microb. Ecol. 33: 279-288. doi:10.3354/ame033279
65. Thornton, D. C. O. 2002. Diatom aggregation in the sea: Mechanisms and ecological implications. Eur. J. Phycol. 37: 149-161. doi:10.1017/S0967026202003657
66. Turner, J. T. 2002. Zooplankton fecal pellets, marine snow and sinking phytoplankton blooms. Aquat. Microb. Ecol. 27: 57-102. doi:10.3354/ame027057
67. Turner, J. T. 2015. Zooplankton fecal pellets, marine snow, phytodetritus and the ocean's biological pump. Prog. Oceanogr. 130: 205-248. doi:10.1016/j.pocean.2014.08.005
68. Urban-Rich, J. 1999. Release of dissolved organic carbon from copepod fecal pellets in the Greenland Sea. J. Exp. Mar. Bio. Ecol. 232: 107-124. doi:10.1016/S0022-0981(98)00104-X
69. Urban-Rich, J., D. A. Hansell, and M. R. Roman . 1998. Analysis of copepod fecal pellet carbon using a high temperature combustion method. Mar. Ecol. Prog. Ser. 171: 199-208. doi:10.3354/meps171199
70. 2 changes, p. 99-110. In E. T. Sundquist and W. S. Broecker [eds.], The carbon cycle and atmospheric CO2: Natural variations Archean to Present. American Geophysical Union.
71. Ward, P., A. Atkinson, and G. Tarling . 2012a. Mesozooplankton community structure and variability in the Scotia Sea: A seasonal comparison. Deep Sea Res. Part II Top. Stud. Oceanogr. 59-60: 78-92. doi:10.1016/j.dsr2.2011.07.004
72. Ward, P., and others. 2012b. Food web structure and bioregions in the Scotia Sea: A seasonal synthesis. Deep Sea Res. Part II Top. Stud. Oceanogr. 59-60: 253-266. doi:10.1016/j.dsr2.2011.08.005
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. Part II Top. Stud. Oceanogr. 55: 1636-1647. doi:10.1016/j.dsr2.2008.04.019
74. Wilson, S. E., H. A. Ruhl, and K. L. Smith . 2013. Zooplankton fecal pellet flux in the abyssal northeast Pacific: A 15 year time-series study. Limnol. Oceanogr. 58: 881-892. doi:10.4319/lo.2013.58.3.0881