Trophic upgrading of picocyanobacterial carbon by ciliates for nutrition of Daphnia magna

Aquatic Microbial Ecology

Volumn 41, Issue 3, 2005, Pages 271-280

  Martin Creuzburg, Dominik ^a,b   Bec, Alexandre ^a,c   Von Elert, Eric ^a  

^a UNIVERSITY OF KONSTANZ   (Germany)

^b UNIVERSITY OF BAYREUTH   (Germany)

^c UNIVERSITÉ BLAISE PASCAL   (France)

Author keywords

Colpidium campylum; Cyclidium spp.; Hopanoids; Sterols; Synechococcus spp.; Tetrahymanol

Indexed keywords

CILIOPHORA; COLPIDIUM CAMPYLUM; CYCLIDIUM; DAPHNIA; DAPHNIA MAGNA; DAPHNIIDAE; SYNECHOCOCCUS;

EID: 31544480624     PISSN: 09483055     EISSN: None     Source Type: Journal    
DOI: 10.3354/ame041271     Document Type: Article

References (76)

1. Beaver JR, Crisman TL (1982) The trophic response of ciliated protozoans in freshwater lakes. Limnol Oceanogr 27:246-253
2. Bec A, Desvilettes C, Véra A, Fontvieille D, Bourdier G (2003a) Nutritional value of different food sources for the benthic Daphnidae Simocephalus vetulus: role of fatty acids. Arch Hydrobiol 156:145-163
3. Bee A, Desvilettes C, Véra A, Lemarchand C, Fontvieille D, Bourdier G (2003b) Nutritional quality of a freshwater heterotrophic flagellate: trophic upgrading of its microalgal diet for Daphnia hyalina. Aquat Microb Ecol 32:203-207
4. Becker C, Boersma M (2003) Resource quality effects on life histories of Daphnia. Limnol Oceanogr 48:700-706
5. Bratbak G (1985) Bacterial biovolume and biomass estimations. Appl Environ Microbiol 49:1488-1493
6. Callieri C, Stockner JG (2002) Freshwater autotrophic picoplankton: a review. J Limnol 61:1-14
7. Carrick HJ, Fahnenstiel GLF, Stoermer EF, Wetzel RG (1991) The importance of zooplankton-protozoan trophic couplings in Lake Michigan. Limnol Oceanogr 36:1335-1345
8. Conner RL, Landrey JR, Burns CH, Mallory FB (1968) Cholesterol inhibition of pentacyclic triterpenoid biosynthesis in Tetrahymena pyriformis. J Protozool 15:600-605
9. Cook HW (1996) Fatty acid desaturation and chain elongation in eukaryotes. In: Vance DE, Vance JE (eds) Biochemistry of lipids, lipoproteins and membranes. Elsevier Science, Amsterdam, p 129-152
10. DeBiase AE, Sanders RW, Porter KG (1990) Relative nutritional value of ciliate protozoa and algae as food for Daphnia. Microb Ecol 19:199-210
11. DeMott WR (1998) Utilization of a cyanobacterium and a phosphorus-deficient green alga as complementary resources by daphnids. Ecology 79:2463-2481
12. DeMott WR, Müller-Navarra DC (1997) The importance of highly unsaturated fatty acids in zooplankton nutrition: evidence from experiments with Daphnia, a cyanobacterium and lipids emulsions. Freshw Biol 38:649-664
13. Desvilettes C, Bourdier G, Amblard C, Barth B (1997) Use of fatty acids for the assessment of zooplankton grazing on bacteria, protozoans and microalgae. Freshw Biol 38:629-637
14. Ederington M, McManus GB, Harvey HR (1995) Trophic transfer of fatty acids, sterols, and a triterpenoid alcohol between bacteria, a ciliate, and the copepod Acartia tonsa. Limnol Oceanogr 40:860-867
15. Ernst A, Sandmann G, Postius C, Brass S, Kenter U, Böger P (1991) Cyanobacterial picoplankton from Lake Constance. II. Classification of isolates by cell morphology and pigment composition. Bot Acta 105:161-167
16. Fahnenstiel GL, Carrick HJ, Iturriaga R (1991) Physiological characteristics and food-web dynamics of Synechococcus in Lakes Huron and Michigan. Limnol Oceanogr 36:219-234
17. Gifford DJ (1991) The protozoan-metazoan trophic link in pelagic ecosystems. J Protozool 38:81-86
18. Gladu PK, Patterson GW, Wikfors GH, Chitwood DJ, Lusby WR (1990) The occurrence of brassicasterol and epibrassicasterol in the chromophycota. Comp Biochem Physiol B 97:491-494
19. Goad LJ (1981) Sterol biosynthesis and metabolism in marine invertebrates. Pure Appl Chem 51:837-852
20. Goad LJ, Holz GG Jr, Beach DH (1983) Identification of (24S)-24-methylcholesta-5,22-dien-3β-ol as the major sterol of a marine cryptophyte and a marine prymnesiophyte. Phytochemistry 22:475-476
21. Greenberg AE, Trussell RR, Clesceri LS (1985) Standard methods for the examination of water and wastewater. American Public Health Association, Washington, DC
22. Guillard RR (1975) Cultures of phytoplankton for feeding of marine invertebrates. In: Smith WL, Chanley MH (eds) Culture of marine invertebrate animals. Plenum Press, New York, p 26-60
23. Hadas O, Berman T (1998) Seasonal abundance and vertical distribution of protozoa (flagellates, ciliates) and bacteria in Lake Kinneret, Israel. Aquat Microb Ecol 14:161-170
24. Harvey HR, McManus GB (1991) Marine ciliates as a widespread source of tetrahymanol and hopan-3β-ol in sediments. Geochim Cosmochim Acta 55:3387-3390
25. Harvey HR, Ederington MC, McManus GB (1997) Lipid composition of the marine ciliates Pleuronema sp. and Fabrea salina: shifts in response to changes in diets. J Eukaryot Microbiol 44:189-193
26. Hillebrand H, Dürselen CD, Kirschtel D, Pollingher U, Zohary T (1999) Biovolume calculation for pelagic and benthic microalgae. J Phycol 35:403-424
27. Jack JD, Gilbert JJ (1993) Susceptibilities of different-sized ciliates to direct suppression by small and large cladocerans. Freshw Biol 29:19-29
28. Jürgens K (1994) Impact of Daphnia on planktonic microbial food webs - a review. Mar Microb Food Webs 8:295-324
29. Jürgens K, Skibbe O, Jappesen E (1999) Impact of metazooplankton on the composition and population dynamics of planktonic ciliates in a shallow, hypertrophic lake. Aquat Microb Ecol 17:61-75
30. Jüttner F, Leonhardt J, Möhren S (1983) Environmental factors affecting the formation of mesityloxid, dimethylallylic alcohol and other volatile compounds excreted by Anabaena cylindrica. J Gen Microbiol 129:407-412
31. Kaneshiro ES, Beischel LS, Merkel SJ, Rhoads DE (1979) The fatty acid composition of Paramecium aurelia cells and cilia: changes with culture age. J Protozool 26:147-158
32. Klein Breteler WCM, Schogt N, Baas M, Schouten S, Kraay GW (1999) Trophic upgrading of food quality by protozoans enhancing copepod growth: role of essential lipids. Mar Biol 135:191-198
33. 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 274:199-208
34. 14C for the measurement of carbon assimilation. Arch Hydrobiol Suppl 48:287-309
35. Lampert W (1977b) Studies on the carbon balance of Daphnia pulex as related to environmental conditions. II. The dependence of carbon assimilation on animal size, temperature, food concentration and diet species. Arch Hydrobiol Suppl 48:310-335
36. Lampert W (1981) Inhibitory and toxic effects of blue-green algae on Daphnia. Int Rev Ges Hydrobiol 66:285-298
37. Lampert W (1991) The dynamics of Daphnia in a shallow lake. Verh Int Ver Limnol 24:795-798
38. Mallory FB, Gordon JT, Connor RL (1963) The isolation of a pentacyclic triterpenoid alcohol from a protozoan. J Am Chem Soc 85:1362-1363
39. Marchessault P, Mazumder A (1997) Grazer and nutrient impacts on epilimnetic ciliate communities. Limnol Oceanogr 42:893-900
40. Martin-Creuzburg D, Von Elert E (2004) Impact of 10 dietary sterols on growth and reproduction of Daphnia galeata. J Chem Ecol 30:483-500
41. Martin-Creuzburg D, Wacker A, Von Elert E (2005) Life history consequences of sterol availability in the aquatic keystone species Daphnia. Oecologia 144:362-372
42. Müller H (1989) The relative importance of different ciliate taxa in the pelagic food web of Lake Constance. Microb Ecol 18:261-273
43. Müller-Navarra DC (1995) Evidence that a highly unsaturated fatty acid limits Daphnia growth in nature. Arch Hydrobiol 132:297-307
44. Müller-Navarra DC, Brett M, Liston AM, Goldman CR (2000) A highly unsaturated fatty acid predicts carbon transfer between primary producers and consumers. Nature 403:74-77
45. Pace ML (1982) Planktonic cillates: their distribution, abundance, and relationship to microbial resources in a monomictic lake. Can J Fish Aquat Sci 39:1106-1116
46. Pace ML, Funke E (1991) Regulation of planktonic microbial communities by nutrients and herbivores. Ecology 72:904-914
47. Pace ML, Orcutt JD (1981) The relative importance of protozoans, rotifers, and crustaceans in a planktonic community. Limnol Oceanogr 26:822-830
48. Pernthaler J, Šimek K, Sattler B, Schwarzenbacher A, Bobkova J, Psenner R (1996) Short-term changes of protozoan control on autotrophic picoplankton in an oligomesotrophic lake. J Plankton Res 18:443-462
49. Pomeroy LR, Wiebe WJ (1988) Energetics of microbial food webs. Hydrobiologia 159:7-18
50. Porter KG, Pace ML, Battey JF (1979) Ciliate protozoans as links in freshwater planktonic food chains. Nature 277:563-565
51. Porter KG, Sherr EB, Sherr BF, Pace ML, Sanders RW (1985) Protozoa in planktonic food webs. J Protozool 32:409-415
52. Raederstorff D, Rohmer M (1988) Polyterpenoids as cholesterol and tetrahymanol surrogates in the ciliate Tetrahymena pyriformis. Biochim Biophys Acta 960:190-199
53. Ravet JL, Brett MT, Müller-Navarra DC (2003) A test of the role of polyunsaturated fatty acids in phytoplankton food quality for Daphnia using liposome supplementation. Limnol Oceanogr 48:1938-1947
54. Sanders RW, Porter KG, Bennett SJ, DeBiase AE (1989) Seasonal patterns of bacterivory by flagellates, ciliates, rotifers, and cladocerans in a freshwater planktonic community. Limnol Oceanogr 34:673-687
55. Sanders RW, Williamson CE, Stutzman PL, Moeller RE, Goulden CE, Aoki-Goldsmith R (1996) Reproductive success of 'herbivorous' zooplankton fed algal and nonalgal food resources. Limnol Oceanogr 41:1295-1305
56. Sherr EB, Sherr BF, Berman T, Hadas O (1991) High abundance of picoplankton-ingesting ciliates during late fall in Lake Kinneret 1991. J Plankton Res 13:789-799
57. Šimek K, Bobkova J, Macek M, Nedoma J, Psenner R (1995) Ciliate grazing on picoplankton in a eutrophic reservoir during the summer phytoplankton maximum: a study at the species and community level. Limnol Oceanogr 40:1077-1090
58. Šimek K, Macek M, Pernthaler J, Straškrabová V, Psenner R (1996) Can freshwater ciliates survive on a diet of picoplankton? J Plankton Res 18:597-613
59. Sterner RW, Schulz KL (1998) Zooplankton nutrition: recent progress and a reality check. Aquat Ecol 32:261-279
60. Stoecker DK, Capuzzo JM (1990) Predation on Protozoa: its importance to zooplankton. J Plankton Res 12:891-908
61. Sul D, Erwin JA (1997) The membrane lipids of the marine ciliated protozoan Parauronema acutum. Biochim Biophys Acta 1345:162-171
62. Sul D, Kaneshiro ES, Jayasimhulu K, Erwin JA (2000) Neutral lipids, their fatty acids, and the sterols of the marine ciliated protozoon, Parauronema acutum. J Eukaryot Microbiol 47:373-378
63. Tang KW, Taal M (2005) Trophic modification of food quality by heterotrophic protists: species-specific effects on copepod egg production and egg hatching. J Exp Mar Biol Ecol 318:85-98
64. Ten Haven HL, Rohmer M, Rullkötter J, Bisseret P (1989) Tetrahymanol, the most likely precursor of gammacerane, occurs ubiquitously in marine sediments. Geochim Cosmochim Acta 53:3073-3079
65. Tezuka Y (1974) An experimental study on the food chain among bacteria, Paramecium and Daphnia. Int Rev Ges Hydrobiol 59:31-37
66. Venkatesan MI (1989) Tetrahymanol: its widespread occurrence and geochemical significance. Geochim Cosmochim Acta 53:3095-3101
67. Von Elert E (2002) Determination of limiting polyunsaturated fatty acids in Daphnia galeata using a new method to enrich food algae with single fatty acids. Limnol Oceanogr 47:1764-1773
68. Von Elert E, Stampfl P (2000) Food quality for Eudiaptomus gracilis: the importance of particular highly unsaturated fatty acids. Freshw Biol 45:189-200
69. Von Elert E, Wolffrom T (2001) Supplementation of cyanobacterial food with polyunsaturated fatty acids does not improve growth of Daphnia. Limnol Oceanogr 46:1552-1558
70. Von Elert E, Martin-Creuzburg D, Le Coz JR (2003) Absence of sterols constrains carbon transfer between cyanobacteria and a freshwater herbivore (Daphnia galeata). Proc R Soc Lond B 270:1209-1214
71. Wacker A, Von Elert E (2001) Polyunsaturated fatty acids: evidence for non-substitutable biochemical resources in Daphnia galeata. Ecology 82:2507-2520
72. Weers PMM, Siewertsen K, Gulati RD (1997) Is the fatty acid composition of Daphnia galeata determined by the fatty acid composition of the ingested diet? Freshw Biol 38:731-738
73. Weisse T (1993) Dynamics of autotrophic picoplankton in marine and freshwater ecosystems. In: Jones JG (ed) Advances in microbial ecology, Vol 13. Plenum Press, New York, p 327-370
74. Weisse T, Müller H, Pinto-Coelho RM, Schweizer A, Springmann D, Baldringer G (1990) Response of the microbial loop to the phytoplankton spring bloom in a large prealpine lake. Limnol Oceanogr 35:781-794
75. Wickham SA, Gilbert JJ, Berninger UG (1993) Effects of rotifers and ciliates on the growth and survival of Daphnia. J Plankton Res 15:317-334
76. Zöllner E, Santer B, Boersma M, Hoppe HG, Jürgens K (2003) Cascading predation effects of Daphnia and copepods on microbial food web components. Freshw Biol 48:2174-2193