Importance of sympagic production to Bering Sea zooplankton as revealed from fatty acid-carbon stable isotope analyses

Marine Ecology Progress Series

Volumn 518, Issue , 2015, Pages 31-50

  Wang, Shiway W ^a,b   Budge, Suzanne M ^c   Iken, Katrin ^a   Gradinger, Rolf R ^a   Springer, Alan M ^a   Wooller, Matthew J ^a,b  

^a UNIVERSITY OF ALASKA FAIRBANKS   (United States)

^b University of Alaska Fairbanks   (United States)

^c DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Climate change; Compound specific stable isotope analysis; Fatty acid biomarkers; Food web ecology; Phytoplankton; Sea ice algae

Indexed keywords

BIOMARKER; CRUSTACEAN; DIATOM; DIET; FATTY ACID; FOOD WEB; LIFE HISTORY; PELAGIC ECOSYSTEM; PHYTOPLANKTON; SEA ICE; STABLE ISOTOPE; ZOOPLANKTON;

BERING SEA; PACIFIC OCEAN;

ALGAE; BACILLARIOPHYTA; CALANUS; MASTIGOPHORA (FLAGELLATES); THEMISTO LIBELLULA; THYSANOESSA RASCHI;

EID: 84920659608     PISSN: 01718630     EISSN: None     Source Type: Journal    
DOI: 10.3354/meps11076     Document Type: Article

References (86)

1. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32-46
2. Arrigo KR, Mock T, Lizotte MP (2010) Primary producers and sea ice. In: Thomas DN, Dieckmann GS (eds) Sea ice. Wiley-Blackwell, Oxford, p 283-325
3. Auel H, Harjes M, da Rocha R, Stübing D, Hagen W (2002) Lipid biomarkers indicate different ecological niches and trophic relationships of the Arctic hyperiid amphipods Themisto abyssorum and T. libellula. Polar Biol 25:374-383
4. Baier CT, Napp JM (2003) Climate-induced variability in Calanus marshallae populations. J Plankton Res 25:771-782
5. Bec A, Martin-Creuzburg D, Von Elert E (2010) Fatty acid composition of the heterotrophic nanoflagellate Paraphysomonas sp.: influence of diet and de novo biosynthesis. Aquat Biol 9:107-112
6. Bec A, Perga ME, Koussoroplis A, Bardoux G, Desvilettes C, Bourdier G, Mariotti A (2011) Assessing the reliability of fatty acid-specific stable isotope analysis for trophic studies. Methods Ecol Evol 2:651-653
7. Bluhm BA, Gradinger R (2008) Regional variability in food availability for arctic marine mammals. Ecol Appl 18:S77-S96
8. Brett MT, Müller-Navarra DC, Persson J (2009) Custracean zooplankton fatty acid composition. In: Arts MT, Brett MT, Kainz MJ (eds) Lipids in aquatic ecosystems. Springer, New York, NY, p 115-146
9. Brown ZW, Arrigo KR (2012) Contrasting trends in sea ice and primary production in the Bering Sea and Arctic Ocean. ICES J Mar Sci 69:1180-1193
10. Budge SM, Parrish CC (1998) Lipid biogeochemistry of plankton, settling matter and sediments in Trinity Bay, Newfoundland. II. Fatty acids. Org Geochem 29:1547-1559
11. Budge SM, Iverson SJ, Koopman HN (2006) Studying trophic ecology in marine ecosystems using fatty acids: a primer on analysis and interpretation. Mar Mamm Sci 22:759-801
12. Budge SM, Wooller MJ, Springer AM, Iverson SJ, McRoy CP, Divoky GJ (2008) Tracing carbon flow in an arctic marine food web using fatty acid-stable isotope analysis. Oecologia 157:117-129
13. Budge SM, Wang SW, Hollmén TE, Wooller MJ (2011) Carbon isotopic fractionation in eider adipose tissue varies with fatty acid structure: implications for trophic studies. J Exp Biol 214:3790-3800
14. Claustre H, Marty JC, Cassiani L, Dagaut J (1988/1989) Fatty acid dynamics in phytoplankton and microzooplankton communities during a spring bloom in the coastal Ligurian Sea: ecological implications. Mar Microb Food Webs 3:51-66
15. Coyle KO, Eisner LB, Mueter FJ, Pinchuk AI and others (2011) Climate change in the southeastern Bering Sea: impacts on pollock stocks and implications for the oscillating control hypothesis. Fish Oceanogr 20:139-156
16. Cripps GC, Atkinson A (2000) Fatty acid composition as an indicator of carnivory in Antarctic krill, Euphausia superba. Can J Fish Aquat Sci 57:31-37
17. Dalpadado P, Yamaguchi A, Ellertsen B, Johannessen S (2008) Trophic interactions of macro-zooplankton (krill and amphipods) in the Marginal Ice Zone of the Barents Sea. Deep-Sea Res II 55:2266-2274
18. Dalsgaard J, St. John M, Kattner G, Müller-Navarra D, Hagen W (2003) Fatty acid trophic markers in the pelagic marine environment. Adv Mar Biol 46:225-340
19. Desvilettes C, Bec A (2009) Formation and transfer of fatty acids in aquatic microbial food webs: role of heterotrophic protists. In: Arts MT, Brett MT, Kainz MJ (eds) Lipids in aquatic ecosystems. Springer, New York, NY, p 25-42
20. Dunstan GA, Volkman JK, Barrett SM, Leroi JM (1993) Essential polyunsaturated fatty acids from 14 species of diatom (Bacillariophyceae). Phytochemistry 35:155-161
21. Durbin EG, Casas MC (2014) Early reproduction by Calanus glacialis in the Northern Bering Sea: the role of ice algae as revealed by molecular analysis. J Plankton Res 36:523-541
22. Falk-Petersen S, Sargent JR, Tande KS (1987) Lipid composition of zooplankton in relation to the sub-arctic food web. Polar Biol 8:115-120
23. Falk-Petersen S, Hopkins CCE, Sargent JR (1990) Trophic relationships in the pelagic, Arctic food web. In: Barnes M, Gibson RN (eds) Trophic relationships in the marine environment. Proc 24th Eur Mar Biol Symp, Oban, 4-10 Oct 1989. Aberdeen University Press, Aberdeen, p 315-333
24. Falk-Petersen S, Hagen W, Kattner G, Clarke A, Sargent J (2000) Lipids, trophic relationships, and biodiversity in Arctic and Antarctic krill. Can J Fish Aquat Sci 57:178-191
25. Falk-Petersen S, Dahl TM, Scott CL, Sargent JR and others (2002) Lipid biomarkers and trophic linkages between ctenophores and copepods in Svalbard waters. Mar Ecol Prog Ser 227:187-194
26. Falk-Petersen S, Mayzaud P, Kattner G, Sargent JR (2009) Lipids and life strategy of Arctic Calanus. Mar Biol Res 5:18-39
27. Folch J, Lees M, Sloane-Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497-509
28. Frost KJ, Lowry LF (1981) Foods and trophic relationships of cetaceans in the Bering Sea. In: Hood DW, Calder JA (eds) The Bering Sea shelf: oceanography and resources, Vol 1. Office of Marine Pollution Assessment, NOAA. University of Washington Press, Seattle, WA, p 825-836
29. Gladyshev MI, Sushchik NN, Makhutova ON, Kalachova GS (2014) Trophic fractionation of isotope composition of polyunsaturated fatty acids in the trophic chain of a river ecosystem. Dokl Biochem Biophys 454:4-5
30. Gradinger RR (2002) Sea ice microorganisms. In: Bitten G (ed) Encyclopedia of environmental microbiology. Wiley & Sons, Hoboken, NJ, p 2833-2844
31. Graeve M, Kattner G, Hagen W (1994) Diet-induced changes in the fatty acid composition of Arctic herbivorous copepods: experimental evidence of trophic markers. J Exp Mar Biol Ecol 182:97-110
32. Graeve M, Kattner G, Piepenburg D (1997) Lipids in Arctic benthos: Does the fatty acid and alcohol composition reflect feeding and trophic interactions? Polar Biol 18:53-61
33. 13C labelled diatom. J Exp Mar Biol Ecol 317:109-125
34. Graham C, Oxtoby L, Wang SW, Budge SM, Wooller MJ (2014) Sourcing fatty acids to juvenile polar cod (Boreogadus saida) in the Beaufort Sea using compound-specific stable carbon isotope analyses. Polar Biol 37:697-705
35. Hagen W, Auel H (2001) Seasonal adaptations and the role of lipids in oceanic zooplankton. Zoology 104:313-326
36. Harvey HR, Pleuthner RL, Lessard EJ, Bernhardt MJ, Shaw CT (2012) Physical and biochemical properties of the euphausiids Thysanoessa inermis, Thysanoessa raschii, and Thysanoessa longipes in the eastern Bering Sea. Deep-Sea Res II 65-70:173-183
37. 15N) model for the North Water food web: implications for evaluating trophodynamics and the flow of energy and contaminants. Deep-Sea Res II 49:5131-5150
38. Hop H, Falk-Petersen S, Svendsen H, Kwasniewski S, Pavlov V, Pavlova O, Søreide JE (2006) Physical and biological characteristics of the pelagic system across Fram Strait to Kongsfjorden. Prog Oceanogr 71:182-231
39. Horner RA (1985) Taxonomy of sea ice microalgae. In: Horner RA (ed) Sea ice biota. CRC Press, Boca Raton, FL, p 147-158
40. Kaufman MR, Gradinger RR, Bluhm BA, O'Brien DM (2008) Using stable isotopes to assess carbon and nitrogen turnover in the Arctic sympagic amphipod Onisimus litoralis. Oecologia 158:11-22
41. Lee RF, Hagen W, Kattner G (2006) Lipid storage in marine zooplankton. Mar Ecol Prog Ser 307:273-306
42. Lomas MW, Moran SB, Casey JR, Bell DW and others (2012) Spatial and seasonal variability of primary production on the Eastern Bering Sea shelf. Deep-Sea Res II 65-70:126-140
43. Marion A, Harvey M, Chabot D, Brethes J (2008) Feeding ecology and predation impact of the recently established amphipod, Themisto libellula, in the St. Lawrence marine system, Canada. Mar Ecol Prog Ser 373:53-70
44. Mauchline J, Fischer LR (1969) The biology of euphausiids, Vol 7. Academic Press, London
45. Moran SB, Lomas MW, Kelly RP, Gradinger R, Iken K, Mathis JT (2012) Seasonal succession of net primary productivity, particulate organic carbon export, and autotrophic community composition in the eastern Bering Sea. Deep-Sea Res II 65-70:84-97
46. Nayar S, Chou LM (2003) Relative efficiencies of different filters in retaining phytoplankton for pigment and productivity studies. Estuar Coast Shelf Sci 58:241-258
47. Nelson RJ, Carmack EC, McLaughlin FA, Cooper GA (2009) Penetration of Pacific zooplankton into the western Arctic Ocean tracked with molecular population genetics. Mar Ecol Prog Ser 381:129-138
48. NOAA (2013) Bering climate: a current view of the Bering Sea ecosystem and climate. www.beringclimate.noaa.gov (accessed 10 Dec 2013)
49. Noyon M, Gasparini S, Mayzaud P (2009) Feeding of Themisto libellula (Amphipoda Crustacea) on natural copepods assemblages in an Arctic fjord (Kongsfjorden, Svalbard). Polar Biol 32:1559-1570
50. Noyon M, Narcy F, Gasparini S, Mayzaud P (2012) Ontogenic variations in fatty acid and alcohol composition of the pelagic amphipod Themisto libellula in Kongsfjorden (Svalbard). Mar Biol 159:805-816
51. NSIDC (2009) Arctic sea ice younger, thinner as melt season begins. Arctic sea ice news & analysis, National Snow and Ice Data Center, Boulder, CO, http://nsidc.org/arcticseaicenews/2009/04/arctic-sea-ice-younger-thinner-as-melt-season-begins
52. Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source partitioning using stable isotopes: coping with too much variation. PLoS ONE 5:e9672
53. Parrish CC (1999) Determination of total lipid, lipid classes and fatty acids in aquatic samples. In: Arts MT, Wainman BC (eds) Lipids in freshwater ecosystems. Springer-Verlag, New York, NY, p 4-12
54. Parrish CC, French VM, Whiticar MJ (2012) Lipid class and fatty acid composition of copepods (Calanus finmarchicus, C. glacialis, Pseudocalanus sp., Tisbe furcata and Nitokra lacustris) fed various combinations of autotrophic and heterotrophic protists. J Plankton Res 34:356-375
55. Phillips DL, Koch PL (2002) Incorporating concentration dependence in stable isotope mixing models. Oecologia 130:114-125
56. Pinchuk AI, Coyle KO (2012) Variability in Calanus spp. populations on the eastern Bering Sea shelf during the recent cold phase. Ocean sciences meeting, 20-24 Feb 2012, Salt Lake City, UT (Abstract)
57. Pinchuk AI, Coyle KO, Farley EV, Renner HM (2013) Emergence of the Arctic Themisto libellula (Amphipoda: Hyperiidae) on the southeastern Bering Sea shelf as a result of the recent cooling, and its potential impact on the pelagic food web. ICES J Mar Sci 70:1244-1254
58. th edn. Blackwell Science, Oxford, p 151-179
59. Reuss N, Poulsen LK (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
60. Richter-Menge J, Overland J (2010) Arctic report card 2010. www.arctic.noaa.gov/reportcard
61. Sambrotto RN, Mordy C, Zeeman SI, Stabeno PJ, Macklin SA (2008) Physical forcing and nutrient conditions associated with patterns of chl a and phytoplankton productivity in the southeastern Bering Sea during summer. Deep-Sea Res II 55:1745-1760
62. Sargent JR, Falk-Petersen S (1981) Ecological investigations on the zooplankton community in Balsfjorden, northern Norway: lipids and fatty acids in Meganyctiphanes norvegica, Thysanoessa raschi and T. inermis during mid-winter. Mar Biol 62:131-137
63. Sargent JR, Henderson RJ (1986) Lipids. In: Corner EDS, O'Hara SCM (eds) The biological chemistry of marine copepods. Clarendon Press, Oxford, p 59-108
64. Sargent JR, Parkes RJ, Mueller-Harvey I, Henderson RJ (1987) Lipid biomarkers in marine ecology. In: Sleigh MA (ed) Microbes in the sea. Wiley & Sons, New York, NY, p 119-138
65. Scott CL, Falk-Petersen S, Sargent JR, Hop H, Lønne OJ, Poltermann M (1999) Lipids and trophic interactions of ice fauna and pelagic zooplankton in the marginal ice zone of the Barents Sea. Polar Biol 21:65-70
66. Scott CL, Falk-Petersen S, Gulliksen B, Lonne OJ, Sargent JR (2001) Lipid indicators of the diet of the sympagic amphipod Gammarus wilkitzkii in the Marginal Ice Zone and in open waters of Svalbard (Arctic). Polar Biol 24:572-576
67. Sherr EB, Sherr BF, Ross C (2013) Microzooplankton grazing impact in the Bering Sea during spring sea ice conditions. Deep-Sea Res II 94:57-67
68. Smith SL (1990) Egg production and feeding by copepods prior to the spring bloom of phytoplankton in Fram Strait, Greenland Sea. Mar Biol 106:59-69
69. Smith SL (1991) Growth, development and distribution of the euphausiids Thysanoessa raschii (M. Sars) and Thysanoessa inermis (Krøyer) in the southeastern Bering Sea. Polar Res 10:461-478
70. Søreide JE, Hop H, Carroll ML, Falk-Petersen S, Hegseth EN (2006) Seasonal food web structures and sympagicpelagic coupling in the European Arctic revealed by stable isotopes and a two-source food web model. Prog Oceanogr 71:59-87
71. Søreide JE, Falk-Petersen S, Hegseth EN, Hop H, Carroll ML, Hobson KA, Blachowiak-Samolyk K (2008) Seasonal feeding strategies of Calanus in the high-Arctic Svalbard region. Deep-Sea Res II 55:2225-2244
72. Søreide JE, Carroll ML, Hop H, Ambrose WG, Hegseth EN, Falk-Petersen S (2013) Sympagic-pelagic-benthic coupling in Arctic and Atlantic waters around Svalbard revealed by stable isotopic and fatty acid tracers. Mar Biol Res 9:831-850
73. Springer AM, Roseneau DG (1985) Copepod-based food webs: auklets and oceanography in the Bering Sea. Mar Ecol Prog Ser 21:229-237
74. Stabeno P, Napp J, Mordy C, Whitledge T (2010) Factors influencing physical structure and lower trophic levels of the eastern Bering Sea shelf in 2005: sea ice, tides and winds. Prog Oceanogr 85:180-196
75. Stabeno PJ, Kachel NB, Moore SE, Napp JM, Sigler M, Yamaguchi A, Zerbini AN (2012) Comparison of warm and cold years on the southeastern Bering Sea shelf and some implications for the ecosystem. Deep-Sea Res II 65-70:31-45
76. Stevens CJ, Deibel D, Parrish CC (2004a) Copepod omnivory in the North Water Polynya (Baffin Bay) during autumn: spatial patterns in lipid composition. Deep-Sea Res I 51:1637-1658
77. Stevens CJ, Deibel D, Parrish CC (2004b) Species-specific differences in lipid composition and omnivory indices in Arctic copepods collected in deep water during autumn (North Water Polynya). Mar Biol 144:905-915
78. Stevens CJ, Deibel D, Parrish CC (2004c) Incorporation of bacterial fatty acids and changes in a wax ester-based omnivory index during a long-term incubation experiment with Calanus glacialis Jaschnov. J Exp Mar Biol Ecol 303:135-156
79. Sukhanova I, Semina H, Venttsel M (1999) Dynamics of the Bering Sea. In: Loughlin T, Ohtani K (eds) Dynamics of the Bering Sea. University of Alaska Sea Grant, Fairbanks, AK, p 453-484
80. Tamelander T, Renaud PE, Hop H, Carroll ML, Ambrose WG Jr, Hobson KA (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
81. Tamelander T, Reigstad M, Hop H, Carroll M, Wassmann P (2008) Pelagic and sympagic contribution of organic matter to zooplankton and vertical export in the Barents Sea marginal ice zone. Deep-Sea Res II 55:2330-2339
82. Tamelander T, Kivimäe C, Bellerby R, Renaud P, Kristiansen S (2009) Base-line variations in stable isotope values in an Arctic marine ecosystem: effects of carbon and nitrogen uptake by phytoplankton. Hydrobiologia 630:63-73
83. Tourangeau S, Runge JA (1991) Reproduction of Calanus glacialis under ice in spring in southeastern Hudson Bay, Canada. Mar Biol 108:227-233
84. Viso AC, Marty JC (1993) Fatty acids from 28 marine microalgae. Phytochemistry 34:1521-1533
85. Volkman JK, Jeffrey SW, Nichols PD, Rogers GI, Garland CD (1989) Fatty acid and lipid composition of 10 species of microalgae used in mariculture. J Exp Mar Biol Ecol 128:219-240
86. Wang SW, Budge SM, Gradinger RR, Iken K, Wooller MJ (2014) Fatty acid and stable isotope characteristics of sea ice and pelagic particulate organic matter in the Bering Sea: tools for estimating sea ice algal contribution to Arctic food web production. Oecologia 174:699-712