Famine and feast in a common freshwater calanoid: Effects of diet and temperature on fatty acid dynamics of Eudiaptomus gracilis

Limnology and Oceanography

Volumn 59, Issue 3, 2014, Pages 947-958

  Koussoroplis, Apostolos Manuel ^a,d   Nussbaumer, Julia ^a   Arts, Michael T ^b,e   Guschina, Irina A ^c   Kainz, Martin J ^a  

^a Inter University Centre for Aquatic Ecosystem Research   (Austria)

^b ENVIRONMENT CANADA   (Canada)

^c CARDIFF UNIVERSITY   (United Kingdom)

^d UNIVERSITY OF POTSDAM   (Germany)

^e RYERSON UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BODY MASS; CRUSTACEAN; DIET; FATTY ACID; FOOD QUALITY; FRESHWATER ENVIRONMENT; GROWTH RATE; NUTRITION; PHOSPHOLIPID; PHYSIOLOGICAL RESPONSE; SURVIVAL; TEMPERATURE EFFECT;

EID: 84899642110     PISSN: 00243590     EISSN: None     Source Type: Journal    
DOI: 10.4319/lo.2014.59.3.0947     Document Type: Article

References (62)

1. Adams, M. 1998. Ecological role of lipids in the health and success of fish populations, p. 132-153. In M. T. Arts and B. C. Wainman [eds.], Lipids in freshwater ecosystems. Springer.
2. Ahlgren, G., I. B. Gustafsson, and M. Boberg. 1992. Fatty acid content and chemical composition of freshwater microalgae. J. Phycol. 28: 37-50, doi: 10. 1111/j. 0022-3646. 1992. 00037. x.
3. Arts, M. T. 1999. Lipids in freshwater zooplankton: Selected ecological and physiological aspects, p. 71-90. In M. T. Arts and B. C. Wainman [eds.], Lipids in freshwater ecosystems. Springer.
4. Arts, M. T., and M. S. Evans. 1991. Optical-digital measurement of energy reserves in calanoid copepods: Inter-segmental distribution and seasonal patterns. Limnol. Oceanogr. 36: 289-298, doi: 10. 4319/lo. 1991. 36. 2. 0289.
5. Arts, M. T., and C. C. Kohler. 2009. Health and condition in fish: The influence of lipids on membrane competency and immune response, p. 237-255. In M. Arts, M. Brett, and M. Kainz [eds.], Lipids in aquatic ecosystems. Springer.
6. Arts, M. T., R. D. Robarts, and M. S. Evans. 1993. Energy reserve lipids of zooplanktonic crustaceans from an oligotrophic saline lake in relation to food resources and temperature. Can. J. Fish. Aquat. Sci. 40: 2404-2420, doi: 10. 1139/f93-265.
7. Bourdier, G. G., and C. A. Amblard. 1989. Lipids in Acanthodiaptomus denticornis during starvation and fed on three different algae. J. Plankton Res. 11: 1201-1212, doi: 10. 1093/plankt/11. 6. 1201.
8. Brett, M. T., D. Müller-Navarra, and J. Persson. 2009. Crustacean zooplankton fatty acid composition, p. 115-146. In M. Arts, M. Brett, and M. Kainz [eds.], Lipids in aquatic ecosystems. Springer.
9. Bychek, E. A., G. A. Dobson, J. L. Harwood, and I. A. Guschina. 2005. Daphnia magna can tolerate short-term starvation without major changes in lipid metabolism. Lipids 40: 599-608, doi: 10. 1007/s11745-005-1421-1.
10. Dagg, M. 1977. Some effects of patchy food environments on copepods. Limnol. Oceanogr. 22: 99-107, doi: 10. 4319/lo. 1977. 22. 1. 0099.
11. DeMott, W. R., R. D. Gulati, and E. Van Donk. 2001. Daphnia food limitation in three hypereutrophic Dutch lakes: Evidence for exclusion of large-bodied species by interfering filaments of cyanobacteria. Limnol. Oceanogr. 46: 2054-2060, doi: 10. 4319/lo. 2001. 46. 8. 2054.
12. Desvilettes, C., G. Bourdier, and J.-C. Breton. 1994. Lipid class and fatty acid composition of planktivorous larval pike Esox lucius living in a natural pond. Aquat. Living Resour. 7: 67-77, doi: 10. 1051/alr: 1994009.
13. Evjemo, J., T. Danielsen, and Y. Olsen. 2001. Losses of lipid, protein and n23 fatty acids in enriched Artemia franciscana starved at different temperatures. Aquaculture 193: 65-80, doi: 10. 1016/S0044-8486(00)00470-1.
14. Farkas, T. 1979. Adaptation of fatty-acid compositions to temperature-study on planktonic crustaceans. Comp. Biochem. Physiol. B 64: 71-76.
15. Fuschino, J. R., I. A. Guschina, G. Dobson, N. D. Yan, J. L. Harwood, and M. T. Arts. 2011. Rising water temperatures alter lipid dynamics and reduce n-3 essential fatty acid concentrations in Scenedesmus obliquus (Chlorophyta). J. Phycol. 47: 763-774, doi: 10. 1111/j. 1529-8817. 2011. 01024. x.
16. Gillooly, J. F., J. H. Brown, G. B. West, V. M. Savage, and E. L. Charnov. 2001. Effects of size and temperature on metabolic rate. Science 293: 2248-2251, doi: 10. 1126/science. 1061967.
17. Gliwicz, Z. M., and E. Siedlar. 1980. Food size limitation and algae interfering with food collection in Daphnia. Arch. Hydrobiol. 88: 155-177.
18. Guillard, R. R., and C. J. Lorenzen. 1972. Yellow-green algae with chlorophyllide C. J. Phycol. 8: 10-14.
19. Hansen, J. Ø., and others. 2008. Apparent digestion and apparent retention of lipid and fatty acids in Atlantic cod (Gadus morhua) fed increasing dietary lipid levels. Aquaculture 284: 159-166, doi: 10. 1016/j. aquaculture. 2008. 07. 043.
20. Haubert, D., M. M. Häggblom, S. Scheu, and L. Ruess. 2008. Effects of temperature and life stage on the fatty acid composition of Collembola. Eur. J. Soil Biol., 44: 213-219, doi: 10. 1016/j. ejsobi. 2007. 09. 003.
21. Hazel, J. R., and B. D. Sidell. 2004. The substrate specificity of hormone-sensitive lipase from adipose tissue of the Antarctic fish Trematomus newnesi. J. Exp. Biol. 207: 897-903, doi: 10. 1242/jeb. 00823.
22. Heissenberger, M., J. Watzke, and M. J. Kainz. 2010. Effect of nutrition on fatty acid profiles of riverine, lacustrine, and aquaculture-raised salmonids of pre-alpine habitats. Hydrobiologia 650: 243-254, doi: 10. 1007/s10750-010-0266-z.
23. Hulbert, A. J., and P. L. Else. 2000. Mechanisms underlying the cost of living in animals. Annu. Rev. Physiol. 62: 207-235, doi: 10. 1146/annurev. physiol. 62. 1. 207.
24. IPCC. 2007. Climate change 2007: Synthesis report. In R. K. Pachauri and A. Reisinger [eds.]. Contribution of working groups I, II and III to the fourth assessment report of the intergovernmental panel on climate change. IPCC.
25. Jackson, D. A. 1993. Stopping rules in principal components analysis: a comparison of heuristical and statistical approaches. Ecology 74: 2204-2214, doi: 10. 2307/1939574.
26. Kainz, M., M. T. Arts, and A. Mazumder. 2004. Essential fatty acids in the planktonic food web and their ecological role for higher trophic levels. Limnol. Oceanogr. 49: 1784-1793, doi: 10. 4319/lo. 2004. 49. 5. 1784.
27. Kiefer, F. 1978. Freilebende Copepoda. Schweizerbartische Verlagsbuchhandlung. Schweizerbartische Editions. [Freeliving copepods.].
28. Kirk, K. L. 1997. Life-history responses to variable environments: Starvation and reproduction in planktonic rotifers. Ecology 78: 434-441, doi: 10. 1890/0012-9658(1997)078[0434: LHRTVE] 2. 0. CO; 2.
29. Koussoroplis, A.-M., M. J. Kainz, and M. Striebel. 2013. Fatty acid retention under temporally heterogeneous dietary intake in a cladoceran. Oikos 122: 1017-1026, doi: 10. 1111/j. 1600-0706. 2012. 20759. x.
30. Lampert, W., E. McCauley, and B. F. J. Manly. 2003. Tradeoffs in the vertical distribution of zooplankton: Ideal free distribution with costs? Proc. R. Soc. B 270: 765-773, doi: 10. 1098/rspb. 2002. 2291.
31. Lampert, W., and P. Muck. 1985. Multiple aspects of food limitation in zooplankton communities: The Daphnia-Eudiaptomus example. Arch. Hydrobiol. Beih. Ergeb. Limnol. 21: 311-322.
32. Lee, R. F., W. Hagen, and G. Kattner. 2006. Lipid storage in marine zooplankton. Mar. Ecol. Prog. Ser. 307: 273-306, doi: 10. 3354/meps307273.
33. Martin-Creuzburg, D., E. Sperfeld, and A. Wacker. 2009. Colimitation of a freshwater herbivore by sterols and polyunsaturated fatty acids. Proc. R. Soc. B 276: 1805-1814, doi: 10. 1098/rspb. 2008. 1540.
34. Martin-Creuzburg, D., and E. Von Elert. 2009. Ecological significance of sterols in aquatic food webs, p. 43-64. In M. Arts, M. Brett, and M. Kainz [eds.], Lipids in aquatic ecosystems. Springer.
35. Martin-Creuzburg, D., A. Wacker, C. Ziese, and M. J. Kainz. 2011. Dietary lipid quality affects temperature-mediated reaction norms of a freshwater key herbivore. Oecologia 168: 901-912, doi: 10. 1007/s00442-011-2155-1.
36. Masclaux, H., A. Bec, M. J. Kainz, C. Desvilettes, L. Jouve, and G. Bourdier. 2009. Combined effects of food quality and temperature on somatic growth and reproduction of two freshwater cladocerans. Limnol. Oceanogr. 54: 1323-1332, doi: 10. 4319/lo. 2009. 54. 4. 1323.
37. Mayor, D. J., K. Cook, B. Thornton, P. Walsham, U. F. M. Witte, A. F. Zuur, and T. R. Anderson. 2011. Absorption efficiencies and basal turnover of C, N and fatty acids in a marine Calanoid copepod. Funct. Ecol. 25: 509-518, doi: 10. 1111/j. 1365-2435. 2010. 01791. x.
38. Mezek, T., T. Simcic, M. T. Arts, and A. Brancelj. 2010. Effect of fasting on hypogean (Niphargus stygius) and epigean (Gammarus fossarum) amphipods: A laboratory study. Aquat. Ecol. 44: 397-408, doi: 10. 1007/s10452-009-9299-7.
39. Müller-Navarra, D. C., M. T. Brett, S. Park, S. Chandra, A. P. Ballantyne, E. Zorita, and C. Goldman. 2004. Unsaturated fatty acid content in seston and tropho-dynamic coupling in lakes. Nature 427: 69-71, doi: 10. 1038/nature02210.
40. Ortega-Mayagoitia, E., J. Ciros-Perez, and M. SanchezMartinez. 2011. A story of famine in the pelagic realm: Temporal and spatial patterns of food limitation in rotifers from an oligotrophic tropical lake. J. Plankton Res. 33: 1574-1585, doi: 10. 1093/plankt/fbr045.
41. Pasquevich, M. Y., M. S. Dreon, S. Lavarías, and H. Heras. 2011. Triacylglycerol catabolism in the prawn Macrobrachium borellii (Crustacea: Palaemoniade). Comp. Biochem. Physiol. B 160: 201-207, doi: 10. 1016/j. cbpb. 2011. 08. 006.
42. Persson, J., and T. Vrede. 2006. Polyunsaturated fatty acids in zooplankton: Variation due to taxonomy and trophic position. Freshw. Biol. 51: 887-900, doi: 10. 1111/j. 1365-2427. 2006. 01540. x.
43. Pond, D. W. 2012. The physical properties of lipids and their role in controlling the distribution of zooplankton in the oceans. J. Plankton Res. 34: 443-453, doi: 10. 1093/plankt/fbs027.
44. R Development Core Team. 2008. R: A language and environment for statistical computing [Internet]. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. Available from http://www. R-project. org.
45. Raclot, T. 2003. Selective mobilization of fatty acids from adipose tissue triacylglycerols. Prog. Lipid Res. 42: 257-288, doi: 10. 1016/S0163-7827(02)00066-8.
46. Rauch, A., C. Fesl, and M. Schagerl. 2006. Influence of environmental variables on algal associations from a floating vegetation mat (Schwingmoor Lake Lunzer Obersee, Austria). Aquat. Bot. 84: 129-136, doi: 10. 1016/j. aquabot. 2005. 08. 004.
47. Riccardi, N., and G. Giussani. 2007. The relevance of life-history traits in the establishment of the invader Eudiaptomus gracilis and the extinction of Eudiaptomus padanus in Lake Candia (Northern Italy): Evidence for competitive exclusion? Aquat. Ecol. 41: 243-254, doi: 10. 1007/s10452-006-9061-3.
48. Rinke, K., and J. Vijverberg. 2005. A model approach to evaluate the effects of temperature and food concentration on individual life history and population dynamics of Daphnia. Ecol. Model. 186: 326-344, doi: 10. 1016/j. ecolmodel. 2005. 01. 031.
49. Sanchez-Paz, A., F. Garcia-Carreno, A. Muhlia-Almazan, A. B. Peregrino-Uriante, J. Hernandez-Lopez, and G. Yepiz-Plascencia. 2006. Usage of energy reserves in crustaceans during starvation: Status and future directions. Insect Biochem. Mol. Biol. 36: 241-249.
50. Santer, B. 1994. Influences of food type and concentration on the development of Eudiaptomus gracilis and implications for interactions between calanoid and cyclopoid copepods. Arch. Hydrobiol. 131: 141-159.
51. Santer, B., E. Blohm-Sievers, C. E. Caceres, and N. G. Hairston. 2000. Life-history variation in the coexisting freshwater copepods Eudiaptomus gracilis and Eudiaptomus graciloides. Arch. Hydrobiol. 149: 441-458.
52. Sardesai, V. M. 1992. Biochemical and nutritional aspects of eicosanoids. J. Nutr. Biochem. 3: 562-579, doi: 10. 1016/0955-2863(92)90050-S.
53. Schlechtriem, C., M. T. Arts, and I. D. Zellmer. 2006. Effect of temperature on the fatty acid composition and temporal trajectories of fatty acids in fasting Daphnia pulex (Crustacea, Cladocera). Lipids 41: 397-400, doi: 10. 1007/s11745-006-5111-9.
54. Sterner, R. W., and J. J. Elser. 2002. Ecological stoichiometry: The biology of elements from molecules to the Biosphere. Princeton Univ. Press.
55. Straile, D., and W. Geller. 1998. Crustacean zooplankton in Lake Constance from 1920 to 1995: Response to eutrophication issues. Adv. Limnol. 53: 255-274.
56. Stuart, J. A., T. E. Gillis, and J. S. Ballantyne. 1998. Compositional correlates of metabolic depression in the mitochondrial membranes of aestivating snails. Am. J. Physiol. Regul. Integr. Comp. Physiol. 275: 1977-1982.
57. Tessier, A. J., L. Henry, and C. E. Goulden. 1983. Starvation in Daphnia: Energy reserves and reproductive allocation. Limnol. Oceanogr. 28: 667-676, doi: 10. 4319/lo. 1983. 28. 4. 0667.
58. Threlkeld, S. T. 1976. Starvation and the size structure of zooplankton communities. Freshw. Biol. 6: 489-496, doi: 10. 1111/j. 1365-2427. 1976. tb01640. x.
59. Van Dooremalen, C., and J. Ellers. 2010. A moderate change in temperature induces changes in fatty acid composition of storage and membrane lipids in a soil arthropod. J. Insect Physiol. 56: 178-184, doi: 10. 1016/j. jinsphys. 2009. 10. 002.
60. Vanderploeg, H. A., W. S. Gardner, C. C. Parish, J. R. Liebig, and J. F. Cavaletto. 1992. Lipids and life-cycle strategy of a hypolimnetic copepods in Lake Michigan. Limnol. Oceanogr. 37: 413-424, doi: 10. 4319/lo. 1992. 37. 2. 0413.
61. Von Elert, E., and P. Stampfl. 2000. Food quality for Eudiaptomus gracilis: The importance of particular highly unsaturated fatty acids. Freshw. Biol. 45: 189-200, doi: 10. 1046/j. 1365-2427. 2000. 00671. x.
62. Wacker, A., and D. Martin-Creuzburg. 2012. Biochemical nutrient requirements of the rotifer Brachionus calyciflorus: Co-limitation by sterols and amino acids. Funct. Ecol. 26: 1135-1143, doi: 10. 1111/j. 1365-2435. 2012. 02047. x.