Feeding ecology of mesopelagic zooplankton of the subtropical and subarctic North Pacific Ocean determined with fatty acid biomarkers

Deep-Sea Research Part I: Oceanographic Research Papers

Volumn 57, Issue 10, 2010, Pages 1278-1294

  Wilson, S E ^a   Steinberg, D K ^b   Chu, F L E ^b   Bishop, J K B ^c,d  

^a MONTEREY BAY AQUARIUM RESEARCH INSTITUTE   (United States)

^b VIRGINIA INSTITUTE OF MARINE SCIENCE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

Biomarkers; Fatty acids; Feeding ecology; Mesopelagic zone; North Pacific Ocean; Zooplankton

Indexed keywords

BACTERIAL BIOMARKERS; BENTHIC FOOD WEBS; CARNIVORY; DEEP WATER; DEPTH PROFILE; EUPHOTIC ZONE; FEEDING ECOLOGY; FEEDING MODES; FOOD SOURCES; HERBIVORY; HIGHER PLANTS; LARGE PARTICLES; MESOPELAGIC; MESOPELAGIC ZONE; MESOTROPHIC; NORTH PACIFIC OCEAN; ORGANIC MATERIALS; ORGANIC MATTER; PACIFIC OCEAN; SINKING PARTICLES; VERTICAL MIGRATION; ZOOPLANKTON;

BACTERIOLOGY; BIOMARKERS; ECOLOGY; FATTY ACIDS; FEEDING; LOCATION; OCEANOGRAPHY; PHYTOPLANKTON;

OCEAN HABITATS;

BIOMARKER; DIATOM; DINOFLAGELLATE; ENVIRONMENTAL CONDITIONS; FATTY ACID; FEEDING ECOLOGY; FOOD CONSUMPTION; FOOD WEB; HERBIVORY; MESOPELAGIC ZONE; NUTRITIONAL REQUIREMENT; SUBARCTIC REGION; TIME SERIES; ZOOPLANKTON;

PACIFIC OCEAN; PACIFIC OCEAN (NORTH);

BACILLARIOPHYTA; BACTERIA (MICROORGANISMS); DINOPHYCEAE; EMBRYOPHYTA; EUCALANUS; NEOCALANUS; OSTRACODA;

EID: 77955957701     PISSN: 09670637     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dsr.2010.07.005     Document Type: Article

References (89)

1. Ackman R.G., Eaton C.A., Sipos J.C., Hooper S.N., Castell J.D. Lipids and fatty acids of two species of North Atlantic krill (Meganyctiphanes norvegia and Thysanoessa inermis) and their role in the aquatic food web. Journal of the Fisheries Research Board of Canada 1970, 27(3):513-533.
2. Ackman R.G., Tocher C.S., McLachlan J. Marine phytoplankter fatty acids. Journal of the Fisheries Research Board of Canada 1968, 25:1603-1620.
3. Alldredge A.L., Silver M.W. Characteristics, dynamics and significance of marine snow. Progress in Oceanography 1988, 20:41-82.
4. Angel M.V. Does mesopelagic biology affect the vertical flux?. Productivity of the Ocean: Present and Past 1989, 155-173. John Wiley and Sons, Ltd., New York. W.H. Berger, V. Smetacek, G. Wefer (Eds.).
5. Auel H., Harjes M., da Rocha R., Stubing D., Hagen W. Lipid biomarkers indicate different ecological niches and trophic relationships of the arctic hyperiid amphipods Themisto abyssorum and T. libellula. Polar Biology 2002, 25:374-383.
6. Azam F., Long R.A. Sea snow microcosms. Nature 2001, 414:495-498.
7. Bec A., Desvilettes C., Véra A., LeMarchand C., Fontvielle D., Bordier G. Nutritional quality of a freshwater heterotrophic flagellate: trophic upgrading of its microalgal diet for Daphnia hyaline. Aquatic Microbial Ecology 2003, 32:203-207.
8. Bec A., Martin-Creuzburg D., von Elert E. Trophic upgrading of autotrophic picoplankton by the heterotrophic nanoflagellate Paraphysomonas sp. Limnology and Oceanography 2006, 51:1699-1707.
9. Bishop J.K.B., Schupack D., Sherrell R.M., Conte M.H. A multiple unit large volume in situ filtration system (MULVFS) for sampling oceanic particulate matter in mesoscale environments. Mapping Strategies in Chemical Oceanography 1985, 155-175. American Chemical Society, Washington, DC. A. Zirino (Ed.).
10. Bishop J.K.B., Stepien J.C., Wiebe P.H. Particulate matter distributions, chemistry and flux in the Panama Basin: response to environmental forcing. Progress in Oceanography 1987, 17:1-59.
11. Bishop J.K.B., Wood T.J. Particulate matter chemistry and dynamics in the twilight zone at VERTIGO ALOHA and K2. Deep-Sea Research I 2008, 55:1684-1706.
12. Bligh E.G., Dyer W.J. A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology 1959, 37:911-917.
13. Böer M., Gannefors C., Kattner G., Graeve M., Hop H., Falk-Petersen S. The Arctic pteropod. Marine Biology 2005, 147:707-717.
14. Boyd P.W., Gall M.P., Silver M.W., Coale S.L., Bidigare R.R., Bishop J.K. Quantifying the surface-subsurface biogeochemical coupling during the VERTIGO ALOHA and K2 studies. Deep-Sea Research II 2008, 55(14-15):1578-1593.
15. Budge S.M., Parrish C.C. Lipid biogeochemistry of plankton, settling matter and sediments in Trinity Bay, Newfoundland. II. Fatty Acids. Organic Geochemistry 1998, 29(5-7):1547-1559.
16. Buesseler K.O., Bidigare R.R., Bishop J.K., Boyd P.W., Honda M.C., Karl D.M., Lam P.J., Lamborg C.H., Siegel D., Silver M.W., Steinberg D.K., Trull T.W. What we know from VERTIGO (VERtical Transport In the Global Ocean). Deep-Sea Research II 2008, 55(14-15):1522-1539.
17. Buesseler K.O., Lamborg C.H., Boyd P.W., Lam P.J., Trull T.W., Bidigare R.R., Bishop J.K.B., Casciotti K.L., DeHairs F., Karl D.M., Siegel D., Silver M.W., Steinberg D.K., Valdez J., Van Mooy B., Wilson S.E. Revisiting carbon flux through the ocean's twilight zone. Science 2007, 316:567-570.
18. Canuel E.A., Martens C.S. Reactivity of recently-deposited organic matter: degradation of lipid compounds near the sediment-water interface. Geochimica et Cosmochimica Acta 1996, 60:1793-1806.
19. Conte M.H., Dickey T.D., Weber J.C., Johnson R.J., Knap A.H. Transient physical forcing of pulsed export of bioreactive material to the deep Sargasso Sea. Deep-Sea Research I 2003, 50:1157-1187.
20. Conte M.H., Eglinton G., Madureira L.A.S., Rabouille C., Labeyrie L., Mudge S. Origin and fate of organic biomarker compounds in the water column and sediments of the eastern North Atlantic. Philosophical Transactions: Biological Sciences 1995, 348:169-178.
21. Conte M.H., Weber J.C., Ralph N. Episodic particle flux in the deep Sargasso Sea: an organic geochemical assessment. Deep-Sea Research I 1998, 45(11):1819-1841.
22. Cripps G.C., Atkinson A. Fatty acid composition as an indicator of carnivory in Antarctic krill, Euphausia superba. Canadian Journal of Fisheries and Aquatic Science 2000, 57(Suppl. 3):31-37.
23. Dagg M.J. Sinking particles as a possible source of nutrition for the large calanoid copepod Neocalanus cristatus in the subarctic Pacific Ocean. Deep-Sea Research I 1993, 40(7):1431-1445.
24. Dalsgaard J., John M.A., Kattner G., Müller-Navarra D.C., Hagen W. Fatty acid trophic markers in the pelagic marine environment. Advances in Marine Biology 2003, 46:225-340.
25. DeMott W.R., Müller-Navarra D.C. The importance of highly unsaturated fatty acids in zooplankton nutrition: evidence from experiments with Daphnia, a cyanobacterium and lipid emulsions. Freshwater Biology 1997, 38:649-664.
26. Desvilettes C., Bourdier G., Amblard C., Barth B. Use of fatty acids for the assessment of zooplankton grazing on bacteria, protozoans and microalgae. Freshwater Biology 1997, 28:629-637.
27. Dilling L., Wilson J., Steinberg D.K., Alldredge A.L. Feeding by the euphausiid Euphausia pacifica and the copepod Calanus pacificus on marine snow. Marine Ecology Progress Series 1998, 170:189-201.
28. Elskens M., Brion N., Buesseler K.O., Van Mooy B.A.S., Boyd P.W., Dehairs F., Savoye N., Baeyens W. Primary, new and export production in the NW Pacific subarctic gyre during the VERTIGO K2 experiments. Deep-Sea Research II 2008, 55(14-15):1594-1604.
29. Falk-Peterson S., Sargent J.R., Lønne O.J., Timofeev S. Functional biodiversity of lipids in Antarctic zooplankton: Calanoides acutus, Calanus propinquus, Thysanoessa macrura, and Euphausia crystallorophias. Polar Biology 1999, 21:37-47.
30. Folch J., Lees M., Sloane-Stanley G.H. A simple method for the isolation and purification of total lipids from animal tissues. Journal of Biological Chemistry 1957, 226:497-509.
31. Fowler S.W., Knauer G.A. Role of large particles in the transport of elements and organic compounds through the oceanic water column. Progress in Oceanography 1986, 16:147-194.
32. Gowing M.M., Wishner K.F. Trophic relationships of deep-sea calanoid copepods from the benthic boundary layer of the Santa Catalina Basin, California. Deep-Sea Research 1986, 33(7):939-961.
33. Gowing M.M., Wishner K.F. Feeding ecology of benthopelagic zooplankton on an eastern tropical Pacific seamount. Marine Biology 1992, 112:451-467.
34. Graeve M., Kattner G., Hagen W. Diet-induced changes in the fatty acid composition of Arctic herbivorous copepods: experimental evidence of trophic markers. Journal of Experimental Marine Biology and Ecology 1994, 182:97-110.
35. Graeve M., Kattner G., Piepenburg D. Lipids in Arctic benthos: does the fatty acid and alcohol composition reflect feeding and trophic interactions?. Polar Biology 1997, 18:53-61.
36. Graeve M., Lundberg M., Böer M., Kattner G., Hop H., Falk-Petersen S. The fate of dietary lipids in the Arctic ctenophore Mertensia ovum (Fabricius 1780). Marine Biology 2008, 153:643-651.
37. Hakanson J.L. The long and short term feeding condition in field-caught Calanus pacificus, as determined from the lipid content. Limnology and Oceanography 1984, 29(4):794-804.
38. Hedges J.I., Stern J.H. Carbon and nitrogen determinations of carbonate-containing solids. Limnology and Oceanography 1984, 29(3):657-663.
39. Kaneda T. Iso- and Anteiso-fatty acids in bacteria: biosynthesis, function, and taxonomic significance. Microbiological Reviews 1991, 55(2):288-302.
40. Kattner G., Albers C., Graeve M., Schnack-Schiel S.B. Fatty acid and alcohol composition of the small polar copepods, Oithona and Oncaea: indication on feeding modes. Polar Biology 2003, 26:666-671.
41. Kobari T., Ikeda T. Vertical distribution, population structure and life cycle of Neocalanus cristatus (Crustacea: Copepoda) in the Oyashio region, with notes on its regional variations. Marine Biology 1999, 134:683-696.
42. Kobari T., Ikeda T. Ontogenetic vertical migration and life cycle of Neocalanus plumchrus (Crustacea: Copepoda) in the Oyashio region, with notes on regional variations in body sizes. Journal of Plankton Research 2001, 23(3):287-302.
43. Kobari T., Moku M., Takahashi K. Seasonal appearance of expatriated boreal copepods in the Oyashio-Kuroshio mixed region. ICES Journal of Marine Science 2008, 65:469-476.
44. Kobari T., Shinada A., Tsuda A. Functional roles of interzonal migrating mesozooplankton in the western subarctic Pacific. Progress in Oceanography 2003, 57:279-298.
45. Kobari T., Steinberg D.K., Ueda A., Tsuda A., Silver M.W., Kitamurae M. Impacts of ontogenetically migrating copepods on downward carbon flux in the western subarctic Pacific Ocean. Deep-Sea Research II 2008, 55(14-15):1648-1660.
46. Kosobokova K.N., Hirche H.-J., Scherzinger T. Feeding ecology of Spinocalanus antarcticus, a mesopelagic copepod with a looped gut. Marine Biology 2002, 141:503-511.
47. Lamborg C.H., Buesseler K.O., Valdez J., Bertrand C.H., Bidigare R.R., Manganini S.J., Pike S., Steinberg D.K., Trull T.W., Wilson S.E. The flux of bio- and lithogenic material associated with sinking particles in the mesopelagic "twilight zone" of the northwest and North Central Pacific Ocean. Deep-Sea Research II 2008, 55(14-15):1540-1563.
48. Lampitt R.S. The contribution of deep-sea macroplankton to organic remineralization: results from sediment trap and zooplankton studies over the Madeira Abyssal Plain. Deep-Sea Research 1992, 39(2):221-233.
49. Lampitt R.S., Hillier W.R., Challenor P.G. Seasonal and diel variation in the open ocean concentration of marine snow aggregates. Nature 1993, 362:737-739.
50. Lampitt R.S., Wishner K.F., Turley C.M., Angel M.V. Marine snow studies in the Northeast Atlantic Ocean: distribution, composition and role as a food source for migrating plankton. Marine Biology 1993, 116:689-702.
51. Lee R.F., Hirota J. Wax esters in tropical zooplankton and nekton and the geographical distribution of wax esters in marine copepods. Limnology and Oceanography 1973, 18(2):227-239.
52. Lee R.F., Hirota J., Barnett A.M. Distribution and importance of wax esters in marine copepods and other zooplankton. Deep-Sea Research 1971, 18:1147-1165.
53. Lee R.F., Nevenzel J.C., Paffenhofer G.-A. Importance of wax esters and other lipids in the marine food chain: phytoplankton and copepods. Marine Biology 1971, 9:99-108.
54. Marty Y., Delaunay F., Moal J., Samain J.-F. Changes in the fatty acid composition of Pecten maximus (L.) during larval development. Journal of Experimental Marine Biology and Ecology 1992, 163:221-234.
55. Mayzaud P., Laureillard J., Merien D., Brinis A., Godard C., Razouls S., Labat J.-P. Zooplankton nutrition, storage and fecal lipid composition in different water masses associated with the Agulhas and subtropical fronts. Marine Chemistry 2007, 107:202-213.
56. Mayzaud P., Virtue P., Albessard E. Seasonal variations in the lipid and fatty acid composition of the euphausiid Meganyctiphanes norvegica from the Ligurian Sea. Marine Ecology Progress Series 1999, 186:199-210.
57. Metcalfe L.D., Schmitz A.A. The rapid preparation of fatty acid esters for gas chromatographic analysis. Analytical Chemistry 1961, 33:363-364.
58. Meziane T., Tsuchiya M. Fatty acids as tracers of organic matter in the sediment and food web of a mangrove/intertidal flat ecosysterm, Okinawa, Japan. Marine Ecology Progress Series 2000, 200:49-57.
59. Müller-Navarra D.C., Brett M.T., Liston A.M., Goldman C.R. A highly unsaturated fatty acid predicts carbon transfer between primary producers and consumers. Nature 2000, 403:74-77.
60. Müller-Navarra D.C., Brett M.T., Park S., Chandra S., Ballantyne A.P., Zorita E., Goldman C.R. Unsaturated fatty acid content in seston and tropho-dynamic coupling in lakes. Nature 2004, 427:69-72.
61. Nelson M.M., Mooney B.D., Nichols P.D., Phleger C.F. Lipids of Antarctic Ocean amphipods: food chain interactions and the occurence of novel biomarkers. Marine Chemistry 2001, 73:53-64.
62. Noji, T.T., 1991. Macrozooplankton influence on the fate of particles in the ocean. In: Wassmann, P., Heiskanen, A.S., Lindahl, O. (Eds.), Sediment Trap Studies in the Nordic Countries, Symposium Proceedings.
63. Phleger C.F., Nichols P.D., Virtue P. Lipids and trophodynamics of Antarctic zooplankton. Comparative Biochemistry and Physiology. Part B 1998, 120:311-323.
64. Pranal V., Fiala-Médioni A., Guezennec J. Fatty acid characteristics in two symbiotic gastropods from a deep hydrothermal vent of the West Pacific. Marine Ecology Progress Series 1996, 142:175-184.
65. Reuss N., Poulsen L.K. Evaluation of fatty acids as biomarkers for a natural plankton community. A field study of a spring bloom and post-bloom period off West Greenland. Marine Biology 2002, 141:423-434.
66. Sargent J.R., Falk-Petersen S. Ecological investigation of the zooplankton community in Balsfjorden northern Norway: lipids and fatty acids in Meganyctiphanes norvegica, Thysanoessa raschi, and T. inermis during mid-winter. Marine Biology 1981, 62:131-137.
67. Sargent J.R., Henderson R.J. The structure, metabolism and function of lipids in marine organisms. Biochemical and Biophysical Perspectives in Marine Biology 1976, 149-212. Academic Press, London. D.C. Malins, J.R. Sargent (Eds.).
68. Sasaki H., Hattori H., Nishizawa S. Downward flux of particulate organic matter and vertical distribution of calanoid copepods in the Oyashio Water in summer. Deep-Sea Research 1988, 35(4):505-515.
69. Schnetzer A., Steinberg D.K. Natural diets of vertically migrating zooplankton in the Sargasso Sea. Marine Biology 2002, 141:89-99.
70. Sheridan C.C., Lee C., Wakeham S.G., Bishop J.K.B. Suspended particle organic composition and cycling in surface and midwaters of the equatorial Pacific Ocean. Deep-Sea Research I 2002, 49:1983-2008.
71. Shoden S., Ikeda T., Yamaguchi A. Vertical distribution, population structure and life cycle of Eucalanus bungii (Copepoda: Calanoida) in the Oyashio region, with notes on regional variations. Marine Biology 2005, 146:497-511.
72. Silver M.W., Alldredge A.L. Bathypelagic marine snow: deep-sea algal and detrital community. Journal of Marine Research 1981, 39:501-530.
73. Silver M.W., Bruland K.W. Differential feeding and fecal pellet composition of salps and pteropods, and the possible origin of the deep-water flora and olive-green "cells". Marine Biology 1981, 62:263-273.
74. Steinberg D.K. Diet of copepods (Scopalatum vorax) associated with mesopelagic detritus (giant larvacean houses) in Monterey Bay, California. Marine Biology 1995, 122:571-584.
75. Steinberg D.K., Cope J.S., Wilson S.E., Kobari T. A comparison of mesopelagic mesozooplankton community structure in the subtropical and subarctic North Pacifc Ocean. Deep-Sea Research II 2008, 55(14-15):1615-1635.
76. Steinberg D.K., Van Mooy B., Buesseler K.O., Boyd P.W., Kobari T., Karl D.M. Bacterial vs. zooplankton control of sinking particle flux in the ocean's twilight zone. Limnology and Oceanography 2008, 53(4):1327-1338.
77. Stevens C.J., Deibel D., Parrish C.C. Copepod omnivory in the North Water Polynya (Baffin Bay) during autumn: spatial patterns in lipid composition. Deep-Sea Research I 2004, 51:1637-1658.
78. Stevens C.J., Deibel D., Parrish C.C. Incorporation of bacterial fatty acids and changes in a wax ester-based omnivory index during a long-term incubation experiment with Calanus glacialis Jaschnov. Journal of Experimental Marine Biology and Ecology 2004, 303:135-156.
79. Stevens C.J., Deibel D., Parrish C.C. Species-specific differences in lipid composition and omnivory indices in Arctic copepods collected in deep water during autumn (North Water Polynya). Marine Biology 2004, 144:905-915.
80. Tsuda A., Saito H., Kasai H. Life histories of Neocalanus flemingeri and Neocalanus plumchrus (Calanoida: Copepoda) in the western subarctic Pacific. Marine Biology 1999, 135:533-544.
81. Tsuda A., Saito H., Kasai H. Life history strategies of subarctic copepods Neocalanus flemingeri and N. plumchrus, especially concerning lipid accumulation patterns. Plankton Biology and Ecology 2001, 48:52-58.
82. Uttal L., Buck K.R. Dietary study of the midwater polychaete Poebius meseres in Monterey Bay. Calinfornia. Marine Biology 1996, 125:333-343.
83. Viso A.-C., Marty J.-C. Fatty acids from 28 marine microalgae. Phytochemistry 1993, 34(6):1521-1533.
84. Wakeham S.G. Lipid biomarkers for heterotrophic alteration of suspended particulate organic matter in oxygenated and anoxic water columns of the ocean. Deep-Sea Research I 1995, 42(10):1749-1771.
85. Wakeham S.G., Canuel E.A. Organic geochemistry of particulate matter in the eastern tropical North Pacific Ocean: implications for particle dynamics. Journal of Marine Research 1988, 46:183-213.
86. Wiebe P.H., Morton A.W., Bradley A.M., Backus R.H., Craddock J.E., Barber V., Cowles T.J., Flierl G.R. New developments in the MOCNESS, an apparatus for sampling zooplankton and micronekton. Marine Biology 1985, 87:313-323.
87. Wilson S.E., Steinberg D.K., Buesseler K.O. 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 Research II 2008, 55(14-15):1636-1647.
88. Wilson S.E., Steinberg D.K. Autotrophic picoplankton in mesozooplankton guts: evidence of aggregate feeding in the mesopelagic zone and export of small phytoplankton. Marine Ecology Progress Series 2010, doi:10.3354/meps08648.
89. Zhang Y., Jiao N.Z., Hong N. Comparative study of picoplankton biomass and community structure in different provinces from subarctic to subtropical oceans. Deep-Sea Research II 2008, 55(14-15):1605-1614.