Marine Biology

, Volume 149, Issue 6, pp 1417–1429

Trophodynamics and seasonal cycle of the copepod Pseudocalanus acuspes in the Central Baltic Sea (Bornholm Basin): evidence from lipid composition

  • Janna Peters
  • Jasmin Renz
  • Justus van Beusekom
  • Maarten Boersma
  • Wilhelm Hagen
Research Article

Abstract

Seasonal lipid dynamics of the copepod Pseudocalanus acuspes were studied in the Bornholm Basin (Central Baltic Sea) on a monthly basis from March 2002 until March 2003 and were interpreted in light of life cycle strategies and diet selection. The individual total lipid content of females ranged from 0.9 to 1.8 μg, with relative wax ester content reaching a significant maximum in May (44% of total lipids) and minimum (17% of total lipids) in April and November. Significant changes in size, lipid content, lipid classes and fatty acid composition of structural as well as storage lipids suggested five characteristic seasonal phases that were induced by different feeding histories and environmental conditions. Storage lipids were characterized by 18:1(n−9) as major component, which ranged between 44% of total fatty acids in June and 23% in February. The strong coherence between 18:1(n−9) in the seston lipids and the occurrence of ciliates emphasized the importance of ciliates in the diet of P. acuspes. As indicated by changes in the amounts of fatty acid markers, other food sources varied over the year, suggesting an opportunistic feeding behavior. The spring period was characterized by an increase in typical diatom and dinoflagellate markers, whereas other sources, potentially cyanobacteria, became more important during summer. The life cycle strategy is discussed with respect to extant adaptations to high latitudinal habitats.

References

  1. Båmstedt U, Håkanson JL, Brenner-Larsen J, Björnsen PK, Geertz-Hansen O, Tiselius P (1990) Copepod nutritional condition and pelagic production during autumn in Kosterfjorden, western Sweden. Mar Biol 104:197–208CrossRefGoogle Scholar
  2. Broglio E, Jónasdóttir SH, Calbet A, Jakobsen HH, Saiz E (2003) Effect of heterotrophic versus autotrophic food on feeding and reproduction of the calanoid copepod Acartia tonsa: relationship with prey fatty acid composition. Aquat Microb Ecol 31:267–278CrossRefGoogle Scholar
  3. Brown MR, Jeffrey SW, Volkman JK, Dunstan GA (1997) Nutritional properties of microalgae for mariculture. Aquaculture 151:315–331CrossRefGoogle Scholar
  4. Bucklin A, Frost BW, Bradford-Grieve J, Allen LD, Copley NJ (2003) Molecular systematic and phylogenetic assessment of 34 calanoid copepod species of the Calanidae and Clausocalanidae. Mar Biol 142:333–343Google Scholar
  5. Cairns AA (1967) The zooplankton of Tanquary Fjord, Ellesmere Island, with special reference to the calanoid copepods. J Fish Res Board Can 24:555–568Google Scholar
  6. Conover RJ, Siferd TD (1993) Dark-season survival strategies of coastal zone zooplankton in the Canadian Arctic. Arctic 46:303–311Google Scholar
  7. Corkett CJ, McLaren IA (1978) The biology of Pseudocalanus. Adv Mar Biol 15:1–231Google Scholar
  8. Cotonnec G, Brunet C, Sautour N, Thoumelin G (2001) Nutritive value and selection of food particles by copepods during a spring bloom of Phaeocystis sp. in the English Channel, as determined by pigment and fatty acid analyses. J Plankton Res 23:693–703CrossRefGoogle Scholar
  9. Daalsgard J, St. John M, Kattner G, Müller-Navarra D, Hagen W (2003) Fatty acid trophic markers in the pelagic marine environment. Adv Mar Biol 46:225–340CrossRefPubMedGoogle Scholar
  10. Davis CC (1976) Overwintering strategies of common planktic copepods in some north Norway fjords and sounds. Astarte 9:37–42Google Scholar
  11. Digby PSB (1950) The biology of the small planktonic copepods of Plymouth. J Mar Biol Assoc UK 29:393–438Google Scholar
  12. Dunstan GA, Volkman JK, Barrett SM, LeRoi J-M, Jeffrey SW (1994) Essential polyunsaturated fatty acids from 14 species of diatoms (Bacillariophyceae). Phytochemistry 35:155–161CrossRefGoogle Scholar
  13. Ederington MC, McManus GB, Harvey HR (1995) Trophic transfer of fatty acids, sterols, and triterpenoid alcohol between bacteria, a ciliate, and the copepod Acartia tonsa. Limnol Oceanogr 40:860–867CrossRefGoogle Scholar
  14. Edler L (1979) Recommendations on methods for marine biological studies in the Baltic Sea. Phytoplankton and chlorophyll. Baltic Mar Biol Publ 5:1–38Google Scholar
  15. 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. Proceedings of the 24th European marine biological symposium. Aberdeen University Press, Aberdeen, pp 315–333Google Scholar
  16. Folch J, Lees M, Sloane-Stanley GH (1957) A simple method for isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509PubMedGoogle Scholar
  17. Fraser AJ, Sargent JR, Gamble JC (1989) Lipid class and fatty acid composition of Calanus finmarchicus (Gunnerus), Pseudocalanus sp. and Temora longicornis Muller from nutrient-enriched seawater enclosure. J Exp Mar Biol Ecol 130:81–92CrossRefGoogle Scholar
  18. Frost BW (1989) A taxonomy of the marine calanoid copepod genus Pseudocalanus. Can J Zool 67:525–551Google Scholar
  19. Geen GH, Hargrave BT (1966) Primary and secondary production in Bras d´Or Lake, Nova Scotia, Canada. Verh Int Ver Theor 16:333–340Google Scholar
  20. 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 182:97–110CrossRefGoogle Scholar
  21. Graeve M, Dauby P, Scailteur Y (2001) Combined lipid, fatty acid and digestive tract content analyses: a penetrating approach to estimate feeding modes in Antarctic amphipods. Polar Biol 24:853–862CrossRefGoogle Scholar
  22. Gugger M, Lyra C, Suominen I, Tsitko I, Humbert J-F, Salkinoja-Salonen MS, Sivonen K (2002) Cellular fatty acids as chemotaxonomic markers of the genera Anabaena, Aphanizomenon, Microcystis, Nostoc and Planktothrix (cyanobacteria). Int J Syst Evol Microbiol 52:1007–1015CrossRefPubMedGoogle Scholar
  23. Harvey HR, Ederington MC, McManus GB (1997) Lipid composition of the marine ciliates Pleuronema sp. and Fabrea salina: shifts in response to changes in diet. J Euk Microbiol 44:189–193CrossRefGoogle Scholar
  24. Hay SJ, Evans GT, Gamble JC (1988) Birth, growth and death rates for enclosed populations of calanoid copepods. J Plankton Res 10:431–454CrossRefGoogle Scholar
  25. Henroth L (1985) Recommendations on methods for marine biological studies in the Baltic Sea: Mesozooplankton biomass assessment. Baltic Mar Biol Publ 10:1–32Google Scholar
  26. Henroth L, Ackefors H (1979) The zooplankton of the Baltic proper: a long-term investigation of the fauna, its biology and ecology. Rep Fish Bd Sweden Inst Mar Res 2:1–160Google Scholar
  27. Hinrichsen H-H, Möllmann C, Voss R, Köster FW, Kornilovs G (2002) Biophysical modeling of larval Baltic cod (Gadus morhua) growth and survival. Can J Fish Aquat Sci 12:1858–1873CrossRefGoogle Scholar
  28. Hinrichsen H-H, Lehmann A, Möllmann C, Schmidt J (2003) Dependency of larval fish survival on retention/dispersion in food limited environments: the Baltic as a case study. Fish Oceanogr 12:425–433CrossRefGoogle Scholar
  29. Hoppe HG (1981) Blue-green algae agglomeration in surface water: a microbiotop of high bacterial activity. Kieler Meeresforschung Sonderhefte 5:291–303Google Scholar
  30. Kattner G, Fricke HSG (1986) Simple gas–liquid chromatography method for simultaneous determination of fatty acids and alcohols in wax esters of marine organisms. J Chromatogr 361:263–268CrossRefGoogle Scholar
  31. Kattner G, Hagen W (1998) Lipid metabolism of the Antarctic euphausiid Euphausia crystallorophias and its ecological implications. Mar Ecol Prog Ser 170:203–212CrossRefGoogle Scholar
  32. Kattner G, Krause M (1989) Seasonal variations of lipids (wax esters, fatty acids and alcohols) in calanoid copepods from the North Sea. Mar Chem 26:261–275CrossRefGoogle Scholar
  33. Kattner G, Krause M, Trahms J (1981) Lipid composition of some typical North Sea copepods. Mar Ecol Prog Ser 4:69–74CrossRefGoogle Scholar
  34. Kattner G, Graeve M, Hagen W (1994) Ontogenetic and seasonal changes in lipid and fatty acid/alcohol compositions of the dominant Antarctic copepod Calanus propinquus, Calanoides acutus and Rhincalanus gigas. Mar Biol 118:637–644CrossRefGoogle Scholar
  35. Klein Breteler WCM, Gonzalez SR (1988) Influence of temperature and food concentration on body size, weight and lipid content of two Calanoid copepod species. In: Boxshall GA, Schminke HK (eds) Biology of copepods. Kluwer, Dordrecht, pp 201–210Google Scholar
  36. Klein Breteler WCM, Schogt N, Gonzalez SR (1990) On the role of food quality in grazing and development of life stages, and genetic change of body size during cultivation of pelagic copepods. J Exp Mar Biol Ecol 135:177–189CrossRefGoogle Scholar
  37. Klein Breteler WCM, Koski M, Rampen S (2004) Role of essential lipids in copepod nutrition: no evidence for trophic upgrading of food quality by a marine ciliate. Mar Ecol Prog Ser 274:199–208CrossRefGoogle Scholar
  38. Koski M, Klein Breteler WCM (2003) Influence of diet on copepod survival in the laboratory. Mar Ecol Prog Ser 264:73–82CrossRefGoogle Scholar
  39. Koski M, Klein Breteler W, Schogt N (1998) Effect of food quality on the rate of growth development of the pelagic copepod Pseudocalanus elongatus (Copepoda: Calanoida). Mar Ecol Prog Ser 170:169–187CrossRefGoogle Scholar
  40. Lee RF, Nevenzel JC, Paffenhöfer G-A (1971) Importance of wax esters and other lipids in the marine food chain: phytoplankton and copepods. Mar Biol 9:99–108CrossRefGoogle Scholar
  41. Lischka S, Hagen W (2005) Life histories of the copepods Pseudocalanus minutus, P. acuspes (Calanoida) and Oithona similis (Cyclopoida) in the Arctic Kongsfjorden (Svalbard). Polar Biol 28:910–921CrossRefGoogle Scholar
  42. Marshall SM (1949) On the biology of the small copepods in Loch Striven. J Mar Biol Assoc UK 28:45–122CrossRefGoogle Scholar
  43. McLaren IA, Laberge E, Corkett CJ, Sévigny J-M (1989) Life cycles of four species of Pseudocalanus in Nova Scotia. Can J Zool 67:552–558CrossRefGoogle Scholar
  44. Meyer-Harms B, Reckermann M, Voß M, Siegmund H, Bodungen Bv (1999) Food selection by calanoid copepods in the eutrophic layer of the Gotland Sea (Baltic Proper) during mass occurrence of N2-fixing cyanobacteria. Mar Ecol Prog Ser 191:243–250CrossRefGoogle Scholar
  45. Möllmann C, Köster FW (1999) Food consumption by clupeids in the Central Baltic: evidence for top-down control? ICES J Mar Sci 56:100–113CrossRefGoogle Scholar
  46. Möllmann C, Köster FW (2002) Population dynamics of calanoid copepods and the implications of their predation by clupeid fish in the Central Baltic Sea. J Plankton Res 24:959–978CrossRefGoogle Scholar
  47. Möllmann C, Kornilovs G, Fetter M, Köster FW, Hinrichsen H-H (2003) The marine copepod Pseudocalanus elongatus as a mediator between climate variability and fisheries in the Central Baltic Sea. Fish Oceanogr 12:360–368CrossRefGoogle Scholar
  48. Murata N, Nishida I (1987) Lipids of blue-green algae (cyanobacteria). In: Stumpf PK (ed) The biochemistry of plants. Academic, New York, pp 315–347Google Scholar
  49. Nichols DS, Nichols PD, Sullivan CW (1993) Fatty acid, sterol and hydrocarbon composition of Antarctic sea ice diatom communities during the spring bloom in McMurdo Sound. Antarct Sci 5:271–278Google Scholar
  50. Norrbin MF (1991) Gonad maturation as an indication of seasonal cycles for several species of small copepods in the Barents Sea. In: Sakshaug E, Hopkins CCE, Øritsland NA (eds) Proceedings of the pro mare symposium on polar marine ecology, pp 421–432Google Scholar
  51. Norrbin F (1992) Overwintering strategies of small copepods in high latitude marine environments. Dissertation, Faculty of Natural Sciences, GöteborgGoogle Scholar
  52. Norrbin MF (1996) Timing of diapause in relation to the onset of winter in the high-latitude copepods Pseudocalanus acuspes and Acartia longiremis. Mar Ecol Prog Ser 142:99–109CrossRefGoogle Scholar
  53. Norrbin MF, Olsen R-E, Tande KS (1990) Seasonal variation in lipid class and fatty acid composition of two small copepods in Balsfjorden, northern Norway. Mar Biol 105:205–211CrossRefGoogle Scholar
  54. Pascal JC, Ackman RG (1976) Long chain monoethylenic alcohol and acid isomers in lipids of copepods and capelin. Chem Phys Lipids 16:219–223CrossRefGoogle Scholar
  55. Pavlovskaya TV, Pechen´-Finenko GA (1975) Comparison of the relative role of living and non-living organic matter in the nutrition of Pseudocalanus elongatus (Boeck) (in Russian). Biol Morya Kiev 34:65–70Google Scholar
  56. Pertsova NM (1981) Number of generations and their span in Pseudocalanus elongatus (Copepoda, Calanoida) in the White Sea (in Russian). J Zool 60:673–684Google Scholar
  57. Peters J, Tuschling K, Brandt A (2004) Zooplankton in the arctic Laptev Sea - feeding ecology as indicated by fatty acid composition. J Plankton Res 26:227–234CrossRefGoogle Scholar
  58. Poulet SA (1974) Seasonal grazing of Pseudocalanus minutus on particles. Mar Biol 25:109–123CrossRefGoogle Scholar
  59. Poulet SA (1976) Feeding of Pseudocalanus minutus on living and non-living particles. Mar Biol 34:117–125CrossRefGoogle Scholar
  60. Putt D, Stoecker DK (1989) An experimentally determined carbon:volume ratio for marine “oligotrichous” ciliates from estuarine and coastal waters. Limnol Oceanogr 34:1097–1103CrossRefGoogle Scholar
  61. Renz J, Hirche H-J (2006) Life cycle of Pseudocalanus acuspes Giesbrecht (Copepoda, Calanoida) in the Central Baltic Sea: I. Seasonal and spatial distribution. Mar Biol 148:567–580CrossRefGoogle Scholar
  62. Runge JA, Ingram RG (1991) Under-ice feeding and diel migration by the planktonic copepods Calanus glacialis and Pseudocalanus minutus in relation to the ice algal production cycle in southeastern Hudson Bay, Canada. Mar Biol 108:217–225CrossRefGoogle Scholar
  63. 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 62:131–137CrossRefGoogle Scholar
  64. Sargent JR, Henderson RJ (1986) Lipids. In: Corner EDS, O´Hara SCM (eds) The biological chemistry of marine copepods. Clarendon Press, Oxford, pp 59–108Google Scholar
  65. Sargent JR, Whittle KJ (1981) Lipids and hydrocarbons in the marine food web. In: Longhurst AR (ed) Analysis of marine ecosystems. Academic, San Diego, pp 491–533Google Scholar
  66. Sargent JR, Parkes RJ, Mueller-Harvey I, Henderson RJ (1987) Lipid biomarkers in marine ecology. In: Sleigh MA (ed) Microbes in the sea. Ellis Horwood, Chichester, pp 119–138Google Scholar
  67. Schlitzer R (2005) Ocean data view. http://www.awi-bremerhaven.de/GEO/ODV
  68. Schnack S (1975) Studies on the feeding biology of copepods (Crustacea) in the Kiel Bight (in German). Doctoral Thesis, Kiel UniversityGoogle Scholar
  69. Siferd TD, Conover RJ (1992) Natural history of ctenophores in the Resolute Passage area of the Canadian High Arctic with special reference to Mertensia ovum. Mar Ecol Prog Ser 86:133–144CrossRefGoogle Scholar
  70. Skerratt JH, Nichols PD, McMeekin TA, Burton HR (1997) Identification of dominant taxa in coastal Antarctic water and ice core samples using lipid signatures. In: Battaglia B, Valencia J, Walton DWH (eds) Antarctic communities. Species, structure and survival. Cambridge University Press, Cambridge, pp 79–85Google Scholar
  71. Vargas MA, Rodríguez H, Moreno J, Olivares H, Del Campo JA, Rivas J, Guerrero MG (1998) Biochemical composition and fatty acid content of filamentous nitrogen-fixing cyanobacteria. J Phycol 34:812–817CrossRefGoogle Scholar
  72. Vidal J (1980) Physioecology of zooplankton. I. Effects of phytoplankton concentration, temperature, and body size on the growth rate of Calanus pacificus and Pseudocalanus sp. Mar Biol 56:111–134CrossRefGoogle Scholar
  73. Wasmund N, Pollehne F, Postel L, Siegel H, Zettler ML (2003) Assessment of the biological state of the Baltic Sea in 2002 (in German). Meereswiss Ber 56:1–78Google Scholar
  74. Zagorodnyaya YA (1974) Nutrition and migration of Black Sea Pseudocalanus elongatus (Boeck) in the winter period (in Russian). Gidrobiol Zhurnal 10:49–56Google Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Janna Peters
    • 1
  • Jasmin Renz
    • 2
  • Justus van Beusekom
    • 2
  • Maarten Boersma
    • 2
  • Wilhelm Hagen
    • 1
  1. 1.Marine ZoologyUniversity of BremenBremenGermany
  2. 2.Alfred Wegener Institute for Polar and Marine ResearchBremerhavenGermany

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