Copepod carcasses as microbial hot spots for pelagic denitrification

Limnology and Oceanography

Volumn 60, Issue 6, 2015, Pages 2026-2036

  Glud, Ronnie N ^a,b,c,d   Grossart, Hans Peter ^e,f   Larsen, Morten ^a,b   Tang, Kam W ^g,h   Arendt, Kristine E ^c   Rysgaard, Søren ^c,d,i   Thamdrup, Bo ^a   Nielsen, Torkel Gissel ^j  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b SCOTTISH MARINE INSTITUTE   (United Kingdom)

^c GREENLAND INSTITUTE OF NATURAL RESOURCES   (Greenland)

^d AARHUS UNIVERSITY   (Denmark)

^e LEIBNIZ INSTITUTE OF FRESHWATER ECOLOGY AND INLAND FISHERIES   (Germany)

^f UNIVERSITY OF POTSDAM   (Germany)

^g VIRGINIA INSTITUTE OF MARINE SCIENCE   (United States)

^h SWANSEA UNIVERSITY   (United Kingdom)

ⁱ UNIVERSITY OF MANITOBA   (Canada)

^j TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ANOXIC CONDITIONS; BIOAVAILABILITY; BIODIVERSITY; CRUSTACEAN; DENITRIFICATION; GENE EXPRESSION; MICROBIAL ACTIVITY; MORTALITY; OXIC CONDITIONS; OXYGEN; OXYGEN MINIMUM LAYER; SEAWATER; WATER COLUMN;

CALANUS FINMARCHICUS; COPEPODA;

EID: 84945944148     PISSN: None     EISSN: 19395590     Source Type: Journal    
DOI: 10.1002/lno.10149     Document Type: Article

References (61)

1. Alldredge, A. L., and Y. Cohen. 1987. Can microscale chemical patches persist in the sea? Microelectrode study of marine snow and fecal pellets. Science 235: 689-691. doi:10.1126/science.235.4789.689
2. Berner, R. A. 1971. Principles of chemical sedimentology, 240 p. McGrave-Hill.
3. Bickel, S. L., J. D. M. Hammond, and K. Tang. 2011. Boat-generated turbulence as a potential source of mortality among copepods. J. Exp. Mar. Bio. Ecol. 410: 105-109. doi: 10.1016/j.jembe.2011.02.038
4. Borisov, S. M., T. Mayr, G. Mistlberger, K. Waich, K. Koren, P. Chojnacki, and I. Klimant. 2009. Precipitation as a simple and versatile method for preparation of optical nano-chemosensors. Talanta 79: 1322-1330. doi:10.1016/j.talanta.2009.05.041
5. Bottger-Schnack, R. 1996. Vertical structure of small metazoan plankton, especially non-calaniod copepods. I. Deep Arabian Sea. J. Plankton Res. 18: 1073-1101. doi:10.1093/plankt/18.7.1073
6. Braman, R. S., and S. A. Hendrix. 1989. Nanogram nitrite and nitrate determination in environmental and biological materials by vanadium (III) reduction with chemilumi-nescence detection. Anal. Chem. 61: 2715-2718. doi:10.1021/ac00199a007
7. Braun, S. T., L. M. Proctor, S. Zani, M. T. Mellon, and J. P. Zehr. 1999. Molecular evidence for zooplankton-associated nitrogen-fixing anaerobes based on amplification of the nifH gene. FEMS Microb. Ecol. 28: 273-279. doi:10.1111/j.1574-6941.1999.tb00582.x
8. Calbet, A. 2001. Mesozooplankton grazing impact on primary production: A global comparative analysis in marine ecosystems. Limnol. Oceanogr. 46: 1824-1830. doi: 10.4319/lo.2001.46.7.1824
9. Carter, K., C. M. Woodley, and R. S. Brown. 2011. A review of tricaine methanesulfonate for anesthesia of fish. Rev. Fish. Biol. Fish. 21: 51-59. doi:10.1007/s11160-010-9188-0
10. Daase, M., O. Varpe, and S. Falk-Petersen. 2014. Non-consumptive mortality in copepods: Occurrence of Calanus spp. Carcasses in the Arctic Ocean during winter. J. Plankton Res. 36:129-144. doi:10.1093/plankt/fbt079
11. Dalsgaard, T., B. Thamdrup, L. Farias, and N. P. Revsbech. 2012. Anammox and denitrification in the oxygen minimum zone of the eastern South Pacific. Limnol. Ocean-ogr. 57: 1331-1346. doi:10.4319/lo.2012.57.5.1331
12. Dalsgaard, T., and others. 2014. Oxygen nanomolar levels reversibly suppress process rates and gene expression in anammox and denitrification in the oxygen minimum zone. Mbio 5: e01966-14. doi:10.1128/mBio.01966-14
13. DeAngelis, M. A., and C. Lee. 1994. Methane production during zooplankton grazing on marine phytoplankton. Limnol. Oceanogr. 39: 1298-1308.
14. De Brabandere, L., D. E. Canfield, T. Dalsgaard, G. E. Friederich, N. P. Revsbech, O. Ulloa, and B. Thamdrup. 2014. Verticalpartitioning of nitrogen-loss processes across the oxic-anoxic interface of an oceanic oxygen minimum zone. Environ. Microb. 16: 3041-3054. doi:10.1111/1462-2920.12255
15. Devol, A. H. 2015. Denitrification, Anammox, and N-2 production in marine sediments. In C. A. Carlson, and S. J. Giovannoni [eds] Annual Review of Marine Science, vol 7. Annual Reviews Publishers. doi:10.1146/annurev-marine-010213-135040
16. Dziallas, C., H. P. Grossart, K. W. Tang, and T. G. Nielsen. 2013. Distinct communities of free-living and copepod associated microorganisms along a salinity gradient in Godthabsfjord, West Greenland. Arct. Antarct. Alp. Res. 45: 471-480. doi: 10.1657/1938-4246.45.4.471
17. Elliot, D. T., and K. W. Tang. 2011a. Spatial and temporal distribution of live and dead copepods in the lower Chesapeak Bay (Virginia, USA). Estuar. Coast. 34: 1039-1048. doi: 10.1007/s12237-011-9380-z
18. Elliot, D. T. and K.W. Tang. 2011b. Influence of carcass abundance on estimates of mortality and assessment of population dynamics in Acartia tonsa. Mar.Ecol. Prog.Ser. 427: 1-12. doi:10.3354/meps09063
19. Frederiksen, M. S., and R. N. Glud. 2006. Oxygen dynamics in the rhizosphere of Zostera marina: A two-dimensional planar optode study. Limnol. Oceanogr. 51: 1072-1083. doi:10.4319/lo.2006.51.2.1072
20. Genin, A., G. Gal, and L. Haury. 1995. Copepod carcasses in the Ocean. II. Nera Coral Reefs. Mar. Ecol. Prog. Ser. 123: 65-71. doi:10.3354/meps123065
21. Glud, R. N., N. B. Ramsing, J. K. Gundersen, and I. Klimant. 1996. Planar optodes, a new tool for fine scale measurements of two dimensional O2 distribution in benthic communities. Mar. Ecol. Prog. Ser. 140: 217-226. doi: 10.3354/meps140217
22. Grossart, H. P., C. Dziallas, F. Leunert, and K. Tang. 2010. Bacteria dispersal by hitchhiking on zooplankton. Proc. Natl. Acad. Sci. 107: 11959-11964. doi:10.1073/pnas.1000668107
23. Hansen, B., and G. Bech. 1996. Bacteria associated with a marine planktonic copepod culture. I. Bacterial genera in seawater, body surface, intestines and fecal pellets and sucession during fecal pellet degradation. J. Plankton Res. 18: 257-273. doi:10.1093/plankt/18.2.257
24. Harris, R. P. 1994. Zooplankton grazing on the coccolitho-phore Emiliania huxleyi and its role in inorganic carbon flux. Mar. Biol. 119: 431-439. doi:10.1007/BF00347540
25. Haury, L., C. Frey, G. Gal, A. Hobday, and A. Genin. 1995. Copepod carcasses in the Ocean. I. Over seamounts. Mar. Ecol. Prog. Ser. 123: 57-63. doi:10.3354/meps123057
26. Helaouet, P., G. Beugrand, and P. C. Reid. 2011. Macrophysiol-ogy of Calanus finmarchicus in the North Atlatic Ocean. Prog.Oceanogr. 91: 217-228. doi:10.1016/j.pocean.2010.11.003
27. Hirst, A. G., and T. Ki0rboe. 2002. Mortality of marine plank-tonic copepods: Global rates and patterns. Mar. Ecol. Prog. Ser. 230: 195-209. doi:10.3354/meps230195
28. Holst, G., and B. Grunwald. 2001. Luminescence lifetime imaging with transparent oxygen optodes. Sens. Actuators B-Chem. 74: 78-90. doi:10.1016/S0925-4005(00)00715-2
29. Holst, G., O. Kohls, I. Klimant, B. Konig, M. Kuhl, and T. Richter. 1998. A modular luminescence lifetime imaging system for mapping oxygen distribution in biological samples. Sens. Actuators B-Chem. 51: 163-170. doi:10.1016/S0925-4005(98)00232-9
30. Ivory, J. A., K. W. Tang, and K. Takahashi. 2014. Use of neutral red in short-term sediment traps to distinguish between zooplankton swimmers and carcasses. Mar. Ecol. Prog. Ser. 505: 107-117. doi:10.3354/meps/10775
31. Jansen, H., and D. A. Wolf-Gladrow. 2001. Carbonate dissolution in copepod guts: A numerical model. Mar. Ecol.Prog. Ser. 221: 199-207. doi:10.3354/meps221199
32. Juul-Pedersen, T., K. E. Arendt, J. Mortensen, M. E. Blicher, D. H. S0gaard, and S. Rysgaard. 2015. Seasonal and inter-annual phytoplankton production in a sub-Arctic tidewater outlet glacier fjord, SW Greenland. Mar. Ecol. Prog. Ser. 524: 27-38. doi:10.3354/meps11174
33. Karstensen, J., L. Starmma, and M. Visbeck. 2008. Oxygen minimum zones in the eastern tropical Atlantic and Pacific Oceans. Prog. Oceanogr. 77: 331-350. doi:10.1016/j.pocean.2007.05.009
34. King, C., R. Sanders, E. ShottsJr, and K. Porter. 1991. Differential survival of bacteria ingested by zooplankton from a stratified eutrophic lake. Limnol. Oceanogr. 36:829-845. doi:10.4319/lo.1991.36.5.0829
35. Klawonn, I., S. Bonaglia, V. Bruechert, and H. Ploug. 2015. Aerobic and anaerobic nitrogen transformation processes in N2-fixing cyanobacterial aggregates. ISME J. 9: 14561466. doi:10.1038/ismej.2014.232
36. Lehto, N., R. N. Glud, G. a Nordi, H. Zang, and W. Davison. 2014. Anoxic micronishes in marine sediments induced by aggregate settlement: Biogeochemical dynamics and implications. Biogeochemistry 119: 307-327. doi:10.1007/s10533-014-9967-0
37. Marty, D. G. 1993. Methanogenic bacteria in seawater. Lim-nol. Oceanogr. 38: 452-456. doi:10.4319/lo.1993.38.2.0452
38. Mortensen, J., K. Lennert, J. Bendtsen, and S. Rysgaard. 2011. Heat sources for glacial melt in the sub-Arctic fjord (Godthabsfjord) in contact with the Greenland Ice sheet. J. Geophys. Res. 116: C01913. doi:10.1029/2010JC006528
39. Nercessian, O., E. Noyes, M. G. Kalyuzhnaya, M. E. Lidstrom, and L. Christoserdova. 2005. Bacterial populations active in metabolism of C 1 compounds in the sediment of Lake Washington, a freshwater lake. Appl. Environ. Microbiol. 71: 6885-6899. doi:10.1128/AEM.71.11.6885-6899.2005
40. Nielsen, L. P. 1992. Denitrification in sediment determined from nitrogen isotope pairing. FEMS Microb. Ecol. 86:357-362. doi:10.1016/0378-1097(92)90800-4
41. Ploug, H., M. Kuhl, B. BuchholzCleven, and B. B. J0rgensen. 1997. Anoxic aggregates—an ephemeral phenomenon in the pelagic environment. Aquat. Microb. Ecol. 13: 285-294. doi:10.3354/ame013285
42. 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 opal and calcite. Limnol. Oceanogr. 53: 469476. doi:10.4319/lo.2008.53.2.0469
43. Proctor, L. M. 1997. Nitrogen-fixing, photosynthestic, anaerobic bacteria associated with pelagic copepods. Aquat. Microb. Ecol. 12: 105-113. doi:10.3354/ame012105
44. Risgaard-Petersen, N., and S. Rysgaard. 1995. Nitrate reduction in sediments and water logged soil measured by 15N techniques, p. 287-295. In K. Alef and P. Nannipieri [eds.], Methods in applied soil and microbiology. Academic.
45. Risgaard-Petersen, N., L. P. Nielsen, S. Rysgaard, T. Dalsgaard, and R. L. Meyer. 2003. Application of the isotope pairing techniques in sediments where anammoz and denitrifica-tion coexist. Limnol. Oceanogr. 1: 63-73.
46. Robertson, L. A., and J. G. Kuenen. 1984. Aerobic denitrification—old wine in new bottles? Antonie van Leeuwenhoek 50: 525-544. doi:10.1007/BF02386224
47. Rosel, S., A. Rychla, C. Wurzbacher, and H. P. Grossart. 2012. Effects of pollen leaching and microbial degradation on organic carbon and nutrient availability in lake water. Aquat. Sci. 74: 87-99. doi:10.1007/s00027-011-0198-3
48. Rysgaard, S., T. G. Nielsen, and B. Hansen. 1999. Seasonal variation in nutrients, pelagic primary production and grazing in a high-Arctic coastal marine ecosystem, Young Sound. Northeast Greenland. Mar. Ecol. Prog. Ser. 179: 13-25. doi:10.3354/meps179013
49. Rysgaard, S., and R. N. Glud. 2004. Anaerobic N2 production in Arctic sea-ice. Limnol. Oceanogr. 49: 86-94. doi:10.4319/lo.2004.49.1.0086
50. Tang, K., S. Bikel, C. Dziallas, and H. P. Grossart. 2009. Microbial activities accompanying decomposition of cla-doceran and copepod carcasses under different environmental conditions. Aquat. Microb. Ecol.. 57: 89-100. doi: 10.3354/ame01331
51. Tang, K. W., V. Turk, and H. P. Grossart. 2010. Linkage between crustacean zooplankton and aquatic bacteria. Aquat. Microb. Ecol. 61: 261-277. doi:10.3354/ame01424
52. Tang, K. W., R. N. Glud, A. Glud, S. Rysgaard, and T. G. Nielsen. 2011. Copepod guts as biogeochemical hotspots in the sea: Evidence from microelectrode profiling of Cal-anus spp. Limnol. Oceanogr. 56: 666-672. doi:10.4319/lo.2011.56.2.0666
53. Tang, K. W., and D. T. Elliott. 2014. Copepod carcasses: Occurrence, fate and ecological importance. p. 255-278. In L. Seuront [ed.] Copepods: Diversity, habitat and behaviour. Nova Science Publishers.
54. Tang, K. W., M. I. Gladyshev, O. P. Dubovskaya, G. Kirillin, and H. P. Grossart. 2014. Zooplankton carcasses and non-predatory mortality in freshwater and inland sea environments. J. Plankton Res. 36: 597-612. doi:10.1093/plankt/ fbu014
55. Terazaki, M., and M. Wada. 1988. Occurrence of large numbers of carcasses of the large grazing copepod Calanus cris-tatus from the Japan Sea. Mar. Biol. 97: 177-183. doi:10.1007/BF00391300
56. Thor, P., T. G. Nielsen, and P. Tiselius. 2008. Mortality rates of epipelagic copepods in the post-spring bloom period inDisko Bay, Western Greenland. Mar. Ecol. Prog. Ser. 359:151-160. doi:10.3354/meps07376
57. Verity, P. G., and V. Smetasek. 1996. Organism life cycles, predation and the structure of marine pelagic ecosystems. Mar. Ecol. Prog. Ser. 130: 277-293. doi:10.3354/meps130277
58. Ward, B. B., and others. 2009. Denitrification as dominant nitrogen loss process in the Arabian Sea. Nature 461: 78-U77. doi:10.1038/nature08276
59. Wheeler, E. H. 1967. Copepod detritus in the deep sea. Limnol. Oceanogr. 12: 697-701. doi:10.4319/lo.1967.12.4.0697
60. Yamaguchi, A., and others. 2002. Community and thropic structures of pelagic copepods down to greater depths in the western subarctic Pacific (West-COSMIC). Deep-Sea Res. 49: 1007-1025. doi:10.1016/S0967-0637(02)00008-0
61. Zumft, W. G. 1997. Cell biology and molecular basis of denitrification. Microbiol. Mol. Biol. Rev. 61: 533-616.