Non-consumptive mortality in copepods: Occurrence of Calanus spp. Carcasses in the Arctic Ocean during winter

Journal of Plankton Research

Volumn 36, Issue 1, 2014, Pages 129-144

  Daase, Malin ^a   Varpe, Oystein ^b,c   Falk Petersen, Stig ^a,b,d  

^a NORWEGIAN POLAR INSTITUTE   (Norway)

^b NORWEGIAN INSTITUTE FOR WATER RESEARCH   (Norway)

^c UNIVERSITY CENTRE IN SVALBARD   (Norway)

^d UNIVERSITY OF TROMSØ   (Norway)

Author keywords

carcasses; life history; marine copepods; non predatory mortality; population dynamics; review

Indexed keywords

CRUSTACEAN; LITERATURE REVIEW; MORTALITY; POPULATION DYNAMICS; SAMPLING; SPATIOTEMPORAL ANALYSIS; SPECIES OCCURRENCE; WINTER;

ARCTIC OCEAN;

EID: 84892734041     PISSN: 01427873     EISSN: 14643774     Source Type: Journal    
DOI: 10.1093/plankt/fbt079     Document Type: Article

References (96)

1. Aksnes, D. L. and Giske, J. (1990) Habitat profitability in pelagic environments. Mar. Ecol. Prog. Ser., 64, 209-215.
2. Aksnes, D. L., Miller, C. B., Ohman, M. D. et al. (1997) Estimation techniques used in studies of copepod population dynamics-A review of underlying assumptions. Sarsia, 82, 279-296.
3. Arnkværn, G., Daase, M. and Eiane, K. (2005) Dynamics of coexisting Calanus finmarchicus, Calanus glacialis and Calanus hyperboreus populations in a high-Arctic fjord. Polar Biol., 28, 528-538.
4. Auel, H., Klages, M. and Werner, I. (2003) Respiration and lipid content of the Arctic copepod Calanus hyperboreus overwintering 1 m above the seafloor at 2,300 m water depth in the Fram Strait. Mar. Biol., 143, 275-282.
5. Bamber, R. N. and Seaby, R. M. H. (2004) The effects of power station entrainment passage on three species of marine planktonic crustacean, Acartia tonsa (Copepoda), Crangon crangon (Decapoda) and Homarus gammarus (Decapoda). Mar. Environ. Res., 57, 281-294.
6. Beckmann, W. (1988) The zooplankton community in the deep bathyal and abyssal zones of the eastern North Atlantic. Preliminary results and data lists from MOCNESS hauls during cruise 08 of the RV 'Polarstern'. Ber. Polarforsch., 42, 1-57.
7. Beyer, F. (1992) Meganyctiphanes norvegica (M Sars) (Euphausiacea) a voracious predator on Calanus, other copepods and ctenophores in Oslofjorden, southern Norway. Sarsia, 77, 189-206.
8. Bickel, S. L., Hammond, J. D. M. and Tang, K. W. (2011) Boat-Generated turbulence as a potential source of mortality among copepods. J. Exp. Mar. Biol. Ecol., 401, 105-109.
9. Bottger-Schnack, R. (1996) Vertical structure of small metazoan plankton, especially non-Calanoid copepods. 1. Deep Arabian Sea. J. Plankt. Res., 18, 1073-1101.
10. Carlotti, F., Giske, J. and Werner, F. (2000) Modelling zooplankton dynamics. In Harris, R., Wiebe, P., Lenz, J., Skjodal, H. and Huntley, M. (eds), ICES Zooplankton Methodology Manual. Academic Press, London, pp. 571-667.
11. Chambers, J. M., Cleveland, W. S., Kleiner, B. et al. (1983) Graphical Methods for Data Analysis.Wadsworth, Belmont, CA.
12. Checkley, D. M. (1982) Selective feeding by Atlantic herring (Clupea harengus) larvae on zooplankton natural assemblages. Mar. Ecol. Prog. Ser., 9, 245-253.
13. Conover, R. J. (1988) Comparative life histories in the genera Calanus and Neocalanus in high latitudes of the northern hemisphere. Hydrobiologia, 167, 127-142.
14. Daase,M. and Eiane, K. (2007) Mesozooplankton distribution in northern Svalbard waters in relation to hydrography. Polar Biol., 30, 969-981.
15. Daase, M., Falk-Petersen, S., Varpe, V. et al. (2013) Timing of reproductive events in the marine copepod Calanus glacialis: A pan-Arctic perspective. Can. J. Fish. Aquat. Sci., 70, 871-884.
16. Deevey, G. B. and Brooks, A. L. (1971) Annual cycle in quantity and composition of zooplankton of Sargasso Sea off Bermuda 2. Surface to 2,000 m. Limnol. Oceanogr., 16, 927-943.
17. Dunlap, D. S., Ng, T. F. F., Rosario, K. et al. (2013) Molecular and microscopic evidence of viruses in marine copepods. PNAS, 110, 1375-1380.
18. Elliott, D. T. and Tang, K. W. (2009) Simple staining method for differentiating live and dead marine zooplankton in field samples. Limnol. Oceanogr. Meth., 7, 585-594.
19. Elliott, D. T. and Tang, K. W. (2011a) Influence of carcass abundance on estimates of mortality and assessment of population dynamics in Acartia tonsa. Mar. Ecol. Prog. Ser., 427, 1-12.
20. Elliott, D. T. and Tang, K.W. (2011b) Spatial and temporal distributions of live and dead copepods in the lower Chesapeake Bay (Virginia, USA). Estuaries and Coasts, 34, 1039-1048.
21. Elliott, D. T., Pierson, J. J. and Roman, M. R. (2013) Copepods and hypoxia in Chesapeake Bay: Abundance, vertical position and nonpredatory mortality. J. Plankt. Res., 35, 1027-1034.
22. Falk-Petersen, S., Mayzaud, P., Kattner, G. et al. (2009) Lipids and life strategy of Arctic Calanus. Mar. Biol. Res., 5, 18-39.
23. Falk-Petersen, S., Timofeev, S., Pavlov, V. et al. (2007) Climate variability and possible effect on arctic food chains. The role of Calanus. In Orbaek, J. B., Tombre, T., Kallenborn, R., Hegseth, E., Falk-Petersen, S. and Hoel, A. H. (eds), Arctic-Alpine Ecosystems and People in a Changing Environment. Springer Verlag, Berlin, pp. 147-166.
24. Farran, G. P. (1926) Biscayan Plankton collected during a Cruise of H.M.S. ' Research,' 1900. - Part XIV. The Copepoda. J. Linn. Soc. London, Zoology, 36, 219-310.
25. Fiksen, V.. and Carlotti, F. (1998) A model of optimal life history and diel vertical migration in Calanus finmarchicus. Sarsia, 83, 129-147.
26. Fleming, J. M. and Coughlan, J. (1978) Preservation of vitally stained zooplankton for live-Dead sorting. Estuaries, 1, 135-137.
27. Forest, A., Sampei, M., Hattori, H. et al. (2007) Particulate organic carbon fluxes on the slope of the Mackenzie Shelf (Beaufort Sea): Physical and biological forcing of shelf-Basin exchanges. J. Mar. Syst., 68, 39-54.
28. Forest, A., Sampei, M., Makabe, R. et al. (2008) The annual cycle of particulate organic carbon export in Franklin Bay (Canadian Arctic): Environmental control and food web implications. J. Geophys. Res.-Oceans, 113, C3.
29. Frangoulis, C., Skliris, N., Lepoint, G. et al. (2011) Importance of copepod carcasses versus faecal pellets in the upper water column of an oligotrophic area. Estuar Coast Shelf Sci, 92, 456-463.
30. Gabrielsen, T., Merkel, B., Søreide, J. et al. (2012) Potential misidentifications of two climate indicator species of the marine arctic ecosystem: Calanus glacialis and C. finmarchicus. Polar Biol., 35, 1621-1628.
31. Gallienne, C. P. and Robins, D. B. (2001) Is Oithona the most important copepod in the world's oceans J. Plankt. Res., 23, 1421-1432.
32. Genin, A., Gal, G. and Haury, L. (1995) Copepod carcasses in the ocean 2. Near coral reefs. Mar. Ecol. Prog. Ser., 123, 65-71.
33. Gradinger, R. and Schnack-Schiel, S. B. (1998) Potential effect of ice formation on Antarctic pelagic copepods: Salinity induced mortality of Calanus propinquus and Metridia gerlachei in comparison to sympagic acoel turbellarians. Polar Biol., 20, 139-142.
34. Grebmeier, J. M. and Barry, J. P. (1991) The influence of oceanographic processes on pelagic-Benthic coupling in polar regions: A benthic perspective. J. Mar. Syst., 2, 495-518.
35. Hagen, W. and Auel, H. (2001) Seasonal adaptations and the role of lipids in oceanic zooplankton. Zoology, 104, 313-326.
36. Harding, G. C. H. (1973) Decomposition of marine copepods. Limnol. Oceanogr., 18, 670-673.
37. Haury, L., Fey, C., Gal, G. et al. (1995) Copepod carcasses in the Ocean 1. Over seamounts. Mar. Ecol. Prog. Ser., 123, 57-63.
38. Hirche, H. J. (1991) Distribution of dominant calanoid copepod species in the Greenland Sea during late fall. Polar Biol., 11, 351-362.
39. Hirche, H. J. (1998) Dormancy in three Calanus species (C. finmarchicus, C. glacialis and C. hyperboreus) from the North Atlantic. Arch. Hydrobiol. Special Iss. Adv. Limnol, 52, 359-369.
40. Hirche, H. J. and Kosobokova, K. (2011)Winter studies on zooplankton in Arctic seas: The Storfjord (Svalbard) and adjacent ice-Covered Barents Sea. Mar. Biol., 158, 2359-2376.
41. Hirche, H. J. and Mumm, N. (1992) Distribution of dominant copepods in the Nansen Basin, Arctic Ocean, in summer. Deep-Sea Res Part A, 39, S485-S505.
42. Hirst, A. G. and Kiorboe, T. (2002) Mortality of marine planktonic copepods: Global rates and patterns. Mar. Ecol. Prog. Ser., 230, 195-209.
43. Homma, T. and Yamaguchi, A. (2010) Vertical changes in abundance, biomass and community structure of copepods down to 3000 m in the southern Bering Sea. Deep-Sea Res Part I, 57, 965-977.
44. Huntley, M., Sykes, P., Rohan, S. et al. (1986) Chemically mediated rejection of dinoflagellate prey by copepods Calanus pacificus and Paraclanus parvus-Mechnism, occurrence and significance. Mar. Ecol. Prog. Ser., 28, 105-120.
45. Jonasdottir, S. H. (1999) Lipid content of Calanus finmarchicus during overwintering in the Faroe-Shetland Channel. Fish. Oceanogr., 8(Suppl. 1), 61-72.
46. Kaartvedt, S. (1996) Habitat preference during overwintering and timing of seasonal vertical migration of Calanus finmarchicus. Ophelia, 44, 145-156.
47. Kaartvedt, S. and Aksnes, D. L. (1992) Does freshwater discharge cause mortality of fjord-Living zooplankton Estuar. Coast Shelf Sci., 34, 305-313.
48. Kimmerer, W. J. and Mckinnon, A. D. (1990) High mortality in a copepod population caused by a parasitic dinoflagellate. Mar. Biol., 107, 449-452.
49. Koppelmann, R., Schafer, P. and Schiebel, R. (2000) Organic carbon losses measured by heterotrophic activity of mesozooplankton and CaCO3 flux in the bathypelagic zone of the Arabian Sea. Deep-Sea Res. Part II, 47, 169-187.
50. Kosobokova, K. N. (1999) The reproductive cycle and life history of the Arctic copepod Calanus glacialis in the White Sea. Polar Biol., 22, 254-263.
51. Kraft, A., Berge, J., Varpe, V. et al. (2013) Feeding in Arctic darkness: Mid-Winter diet of the pelagic amphipods Themisto abyssorum and T. libellula. Mar. Biol., 160, 241-248.
52. Landsberg, J. H. (2002) The effects of harmful algal blooms on aquatic organisms. Reviews in Fisheries Science, 10, 113-390.
53. Leu, E., Søreide, J. E., Hessen, D. O. et al. (2011) Consequences of changing sea-Ice cover for primary and secondary producers in the European Arctic shelf seas: Timing, quantity, and quality. Prog. Oceanogr., 90, 18-32.
54. Lopez, M. D. G. (1996) Effect of starvation on development and survivorship of naupliar Calanus pacificus (Brodsky). J. Exp. Mar. Biol. Ecol., 203, 133-146.
55. Madsen, S. D., Nielsen, T. G. and Hansen, B. W. (2001) Annual population development and production by Calanus finmarchicus, C. glacialis and C. hyperboreus in Disko Bay, western Greenland. Mar. Biol., 139, 75-93.
56. Marshall, S. M. and Orr, A. P. (1952) On the biology of Calanus finmarchicus. 7. Factors affecting egg production. J. Mar. Biol. Ass. UK, 30, 527-548.
57. Marshall, S. M. and Orr, A. P. (1955) The Biology of a Marine Copepod (Calanus finmarchicus Gunnerus). Oliver & Boyd, Springer.
58. Miller, C. B., Frost, B. W., Batchelder, H. P. et al. (1984) Life Histories of large, grazing copepods in a subarctic ocean gyre-Neocalanus plumchrus, Neocalanus cristatus, and Eucalanus bungii in the Northeast Pacific. Prog. Oceanogr., 13, 201-243.
59. Ohman, M. D. (1984) Omnivory by Euphausia pacifica: The role of copepod prey. Mar. Ecol. Prog. Ser., 19, 125-131.
60. Ohman, M. D. (1986) Predator limited population growth of the copepod Pseudocalanus sp. J. Plankt. Res., 8, 673-713.
61. Ohman, M. D. (2012) Estimation of mortality for stage-Structured zooplankton populations: What is to be done J. Mar. Syst., 93, 4-10.
62. Ohman, M. D. and Wood, S. N. (1995) The inevitability of mortality. ICES J. Mar. Sci., 52, 517-522.
63. Piepenburg, D. (2005) Recent research on Arctic benthos: Common notions need to be revised. Polar Biol., 28, 733-755.
64. Rasband, W. S. (1997-2009) ImageJ. 1.41. U.S. National Institutes of Health, Bethesda, MD, USA, http://rsb.info.nih.gov/ij/.
65. Redden, A. M. and Daborn, G. R. (1991) Viability of subitaneous copepod eggs following fish predation on egg-Carrying calanoids. Mar. Ecol. Prog. Ser., 77, 307-310.
66. Renaud, P., Berge, J., Varpe, V. et al. (2012) Is the poleward expansion by Atlantic cod and haddock threatening native polar cod, Boreogadus saida Polar Biol., 35, 401-412.
67. Reuss, N. and Poulsen, L. K. (2002) Evaluation of fatty acids as biomarkers for a natural plankton community. A field study of a spring bloom and a post-Bloom period off West Greenland. Mar. Biol., 141, 423-434.
68. Roe, H. S. J. (1988) Midwater biomass profiles over the Madeira abyssal plain and the contribution of copepods. Hydrobiologia, 167, 169-181.
69. Rudels, B., Friedrich, H. J. and Quadfasel, D. (1999) The Arctic circumpolar boundary current. Deep-Sea Res. Part II, 46, 1023-1062.
70. Saloranta, T. M. and Haugan, P. M. (2001) Interannual variability in the hydrography of Atlantic water northwest of Svalbard. J. Geophys. Res.-Oceans, 106, 13931-13943.
71. Sameoto, D. D. (1986) Influence of the biological and physical environment on the vertical distribution of mesozooplankton and micronekton in the eastern tropical Pacific. Mar. Biol., 93, 263-279.
72. Sampei, M., Sasaki, H., Forest, A. et al. (2012) A substantial export flux of particulate organic carbon linked to sinking dead copepods during winter 2007-2008 in the Amundsen Gulf (southeastern Beaufort Sea, Arctic Ocean). Limnol. Oceanogr., 57, 90-96.
73. Sampei, M., Sasaki, H., Hattori, H. et al. (2009) Significant contribution of passively sinking copepods to the downward export flux in Arctic waters. Limnol. Oceanogr., 54, 1894-1900.
74. Scott, C. L., Kwasniewski, S., Falk-Petersen, S. et al. (2002) Lipids and fatty acids in the copepod Jaschnovia brevis (Jaschnov) and in particulates from Arctic waters. Polar Biol., 25, 65-71.
75. Sims, D. W. and Quayle, V. A. (1998) Selective foraging behaviour of basking sharks on zooplankton in a small-Scale front. Nature, 393, 460-464.
76. Skovgaard, A. and Saiz, E. (2006) Seasonal occurrence and role of protistan parasites in coastal marine zooplankton. Mar. Ecol. Prog. Ser., 327, 37-49.
77. Speirs, D. C., Gurney, W. S. C., Holmes, S. J. et al. (2004) Understanding demography in an advective environment: Modelling Calanus finmarchicus in the Norwegian Sea. J. Anim. Ecol., 73, 897-910.
78. Stearns, S. C. (1992) The Evolution of Life Histories. Oxford University Press, Oxford.
79. Tamelander, T., Renaud, P. E., Hop, H. et al. (2006) Trophic relationships and pelagic-Benthic coupling during summer in the Barents Sea Marginal Ice Zone, revealed by stable carbon and nitrogen isotope measurements. Mar. Ecol. Prog. Ser., 310, 33-46.
80. Tang, K. W., Freund, C. S. and Schweitzer, C. L. (2006) Occurrence of copepod carcasses in the lower Chesapeake Bay and their decomposition by ambient microbes. Estuar. Coast Shelf Sci., 68, 499-508.
81. Tarling, G. A., Shreeve, R. S., Ward, P. et al. (2004) Life-Cycle phenotypic composition and mortality of Calanoides acutus (Copepoda : Calanoida) in the Scotia Sea: A modelling approach. Mar. Ecol. Prog. Ser., 272, 165-181.
82. Terazaki, M. andWada, M. (1988) Occurrence of large numbers of carcasses of the large, grazing coepod Calanus cristatus from the Japan Sea. Mar. Biol., 97, 177-183.
83. Tsuda, A. (1994) Starvation tolerance of a planktonic marine copepods Pseudocalanus newmani Frost J. Exp. Mar. Biol. Ecol., 181, 81-89.
84. Varpe, V. (2012) Fitness and phenology: Annual routines and zooplankton adaptations to seasonal cycles. J. Plankt. Res., 34, 267-276.
85. Varpe, V., Fiksen, V. and Slotte, A. (2005) Meta-Ecosystems and biological energy transport from ocean to coast: The ecological importance of herring migration. Oecologia, 146, 443-451.
86. Varpe, V., Jørgensen, C., Tarling, G. A. et al. (2007) Early is better: Seasonal egg fitness and timing of reproduction in a zooplankton lifehistory model. Oikos, 116, 1331-1342.
87. Varpe, V., Jørgensen, C., Tarling, G. A. et al. (2009) The adaptive value of energy storage and capital breeding in seasonal environments. Oikos, 118, 363-370.
88. Vogedes, D., Varpe, V., Søreide, J. E. et al. (2010) Lipid sac area as a proxy for individual lipid content of arctic calanoid copepods. J. Plankt. Res., 32, 1471-1477.
89. Weikert, H. (1977) Copepod carcasses in upwelling regions south of Cap Blanc, NWAfrica. Mar. Biol., 42, 351-355.
90. Weikert, H. (1982) The vertical distribution of zooplankton in relation to habitat zones in the area of the Atlantis II Deep, central Red Sea. Mar. Ecol. Prog. Ser., 8, 129-143.
91. Weslawski, J. M. and Legezynska, J. (1998) Glaciers caused zooplankton mortality J. Plankt. Res., 20, 1233-1240.
92. Wheeler, E. H. (1967) Copepod detritus in deep sea. Limnol. Oceanogr., 12, 697-702.
93. Wishner, K. F. (1980) Aspects of the community ecology of deep sea, benthopelagic plankton, with special attention to gymnopleid copepods. Mar. Biol., 60, 179-187.
94. Yamaguchi, A. and Ikeda, T. (2001) Abundance and population structure of three mesopelagic Paraeuchaeta species (Copepoda: Calanoida) in the Oyashio region, western subarctic Pacific Ocean with notes on their carcasses and epizoic ciliates. Plankton Biol. Ecol., 48, 104-113.
95. Yamaguchi, A., Watanabe, Y., Ishida, H. et al. (2002) Community and trophic structures of pelagic copepods down to greater depths in the western subarctic Pacific (WEST-COSMIC). Deep-Sea Res. Part I, 49, 1007-1025.
96. Yanez, S., Hidalgo, P. and Escribano, R. (2012) Natural mortality of Paracalanus indicus (Copepoda: Calanoida) in coastal upwelling areas associated with oxygen minimum zone in the Humboldt Current system: Implications for the passive carbon flux. Rev. Biol. Mar. Oceanogr., 47, 295-310.