Oecologia

, Volume 172, Issue 2, pp 551–562 | Cite as

Are cyanobacterial blooms trophic dead ends?

  • Marie-Elodie Perga
  • Isabelle Domaizon
  • Jean Guillard
  • Valérie Hamelet
  • Orlane Anneville
Ecosystem Ecology - Original Research

Abstract

Cyanobacterial blooms induce significant costs that are expected to increase in the near future. Cyanobacterial resistance to zooplankton grazing is one factor thought to promote bloom events. Yet, numerous studies on zooplankton ability to graze upon cyanobacteria have been producing contradictory results and such a puzzle might arise from the lack of direct observations in situ. Our objective was to track, using fatty acid (FA) and fatty acid stable isotope analyses (FA-SIA), the fate of cyanobacterial organic matter in the food web of a lake subjected to summer blooms of Planktothrix rubescens. A metalimnetic bloom of P. rubescens occurred in Lake Bourget (France) during the study period (May–November 2009). The bloom was especially rich in α-linolenic acid, 18:3(n-3), but none of the considered zooplankton taxa exhibited spiking content in this particular FA. FA-SIA revealed, however, that over a quarter of 18:3(n-3) in small zooplankton (<500 μm) was provided by P. rubescens while large cladocerans (>500 μm) did not benefit from it. P. rubescens 18:3(n-3) could be tracked up to perch (Perca fluviatilis) young of the year (YOY) to which it contributed to ~15 % of total 18:3(n-3). Although transferred with a much lower efficiency than micro-algal organic matter, the P. rubescens bloom supported a significant share of the pelagic secondary production and did not constitute, sensu stricto, a ‘trophic dead end’. The cyanobacterial bloom also provided perch YOY with components of high nutritional values at a season when these are critical for their recruitment. This cyanobacterial bloom might thus be regarded as a significant dietary bonus for juvenile fish.

Keywords

Lake Food web Fatty acid Fish Planktothrix rubescens 

Notes

Acknowledgments

Comments from two anonymous reviewers on a previous version of this manuscript were much appreciated. This work is part of a project funded by the Rhône-Alpes region (CIBLE project) and the French National Institute for Agronomical Research (Projet Innovant). J.F. Humbert provided useful comments on a previous version of the manuscript. We thank Jean-Christophe Hustache, Michel Colon, Leslie Lainé and Raphaël D’Elbee for their technical help during field sampling and laboratory analysis. We also would like to thank Sébastien Cachéra (CISALB) and Gérard Paolini (the technique cell of Bourget) for their logistical support during field sampling.

Supplementary material

442_2012_2519_MOESM1_ESM.doc (238 kb)
Supplementary material 1 (DOC 238 kb)
442_2012_2519_MOESM2_ESM.doc (377 kb)
Supplementary material 2 (DOC 377 kb)
442_2012_2519_MOESM3_ESM.doc (52 kb)
Supplementary material 3 (DOC 52 kb)

References

  1. Ahlgren G, Gustafsson IB, Boberg M (1992) Fatty-acid content and chemical composition of freshwater microalgae. J Phycol 28:37–50CrossRefGoogle Scholar
  2. Anderson DM, Glibert PM, Burkholder JM (2002) Harmful algal blooms and eutrophication: nutrient sources, composition and consequences. Estuaries 25:704–726CrossRefGoogle Scholar
  3. Angeli N, Pinel-Alloul B, Balvay G, Menard I (1995) Diel patterns of feeding and vertical migration in Daphnids and Diaptomids during the clear water phase in Lake Geneva (France). Hydrobiologia 301:163–184CrossRefGoogle Scholar
  4. Ballantyne AP, Brett MT, Schindler DE (2003) The importance of dietary phosphorus and highly unsaturated fatty acids for sockeye (Oncorhynchus nerka) growth in Lake Washington—a bioenergetics approach. Can J Fish Aquat Sci 60:12–22CrossRefGoogle Scholar
  5. Bastviken D, Ejlertsson J, Sundh I, Tranvik L (2003) Methane as a source of carbon and energy for lake pelagic food webs. Ecology 84:969–981CrossRefGoogle Scholar
  6. Bec A et al (2011) Experimental test of the reliability of fatty-acid-specific stable isotope analyses as trophic biomarkers. Methods Ecol Evol 2:651–659CrossRefGoogle Scholar
  7. Bell MV, Sargent JR (1996) Lipid nutrition and fish recruitment. Mar Ecol Prog Ser 134:315–316CrossRefGoogle Scholar
  8. Berthon JL, Brousse S (1995) Modification of migratory behavior of planktonic crustacea in the presence of a bloom of Microcystis aeruginosa (Cyanobacteria). Hydrobiologia 300:185–193CrossRefGoogle Scholar
  9. Brett MT, Muller-Navarra DC (1997) The role of highly unsaturated fatty acids in aquatic food web processes. Freshw Biol 38:483–499CrossRefGoogle Scholar
  10. 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 157:117–129PubMedCrossRefGoogle Scholar
  11. Burns CW, Brett MT, Schallenberg M (2011) A comparison of the trophic transfer of fatty acids in freshwater plankton by cladocerans and calanoid copepods. Freshw Biol 56:889–903CrossRefGoogle Scholar
  12. Christoffersen K, Riemann B, Hansen LR, Klysner A, Sorensen HB (1990) Qualitative importance of the microbial loop and plankton community structure in a eutrophic lake during a bloom of cyanobacteria. Microb Ecol 20:253–272CrossRefGoogle Scholar
  13. Dalsgaard J, St John M (2004) Fatty acids biomarkers: validation of food web and trophic markers using 13C-labelled fatty acids in juvenile sandeel (Ammodytes tobianus). Can J Fish Aquat Sci 61:1671–1680CrossRefGoogle Scholar
  14. Dalsgaard J, St John M, Kattner G, Müller-Navarra DC, Hagen W (2003) Fatty acid trophic markers in the pelagic marine environment. In: Southward AJ, Tyler PA, Young CM, Fuiman LA (eds) Advances in marine biology, vol 46. Academic, Amsterdam, pp 225–340Google Scholar
  15. David J (1967) Pêche, pêcheurs professionnels, pollution dans le lac du Bourget. Bull Fr Pêche Piscic 224:81–94CrossRefGoogle Scholar
  16. De Bernardi R, Giussani G (1978) The effect of mass fish mortality on zooplankton structure and dynamics in a small Italian lake (Lago di Annone). Verh Int Verein Limnol 21:285–295Google Scholar
  17. De Bernardi R, Giussani G (1990) Are blue-green algae a suitable food for zooplankton? An overview. Hydrobiologia 200(201):29–41CrossRefGoogle Scholar
  18. De Mott WR (1986) The role of taste in food selection by freshwater zooplankton. Oecologia 69:334–340CrossRefGoogle Scholar
  19. De Mott WR (1998) Utilization of a cyanobacterium and a phosphorus-deficient green alga as complementary resources by Daphnids. Ecology 79:2463–2481CrossRefGoogle Scholar
  20. De Mott WR, Zhang QX, Carmichael WW (1991) Effects of toxic cyanobacteria and purified toxins on the survival and feeding of a copepod and three species of Daphnia. Limnol Oceanogr 36:1346–1357CrossRefGoogle Scholar
  21. Del Giorgio PA, France RL (1996) Ecosystem-specific patterns in the relationship between zooplankton and POM or microplankton δ13C. Limnol Oceanogr 41:359–365CrossRefGoogle Scholar
  22. Ederington MC, 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 40:860–867CrossRefGoogle Scholar
  23. Elser JJ (1999) The pathway to noxious cyanobacteria blooms in lakes: the food web as the final turn. Freshw Biol 42:537–543CrossRefGoogle Scholar
  24. Fahnenstiel GL, Scavia D (1987) Dynamics of Lake Michigan phytoplankton: recent changes in surface and deep communities. Can J Fish Aquat Sci 44:509–514CrossRefGoogle Scholar
  25. Feuillade J (1994) The cyanobacterium (blue-green alga) Oscillatoria rubescens D.C. Adv Limnol 41:77–93Google Scholar
  26. France RL, del Giorgio PA, Westcott KA (1997) Productivity and heterotrophy influences on zooplankton δ13C in Northern Temperate lakes. Aquat Microb Ecol 12:85–93CrossRefGoogle Scholar
  27. Fulton RS (1988) Grazing on filamentous algae by herbivorous zooplankton. Freshw Biol 20:263–271CrossRefGoogle Scholar
  28. Fulton RS, Paerl HW (1988) Effects of the blue-green alga Microcystis aeruginosa on zooplankton competitive relations.Oecologia 76:383–389Google Scholar
  29. Gliwicz Z (1977) Food size selection and seasonal succession of filter-feeding zooplankton in an eutrophic lake. Ekol Polska 25:179–225Google Scholar
  30. Gliwicz Z (1990) Why do cladocerans fail to control algal blooms? Hydrobiologia 200–201:83–97Google Scholar
  31. Guillard J, Perga ME, Colon M, Angeli N (2006) Hydroacoustic assessment of young-of-year perch, Perca fluviatilis, population dynamics in an oligotrophic lake (Lake Annecy, France). Fish Manag Ecol 13:319–327CrossRefGoogle Scholar
  32. Guo N, Xie P (2006) Development of tolerance against toxic Microcystis aeruginosa in three cladocerans and the ecological implications. Environ Pollut 143:513–518PubMedCrossRefGoogle Scholar
  33. Hansson LA, Gustafsson S, Rengefors K, Bomark L (2007) Cyanobacterial chemical warfare affects zooplankton community composition. Freshw Biol 52:1290–1301CrossRefGoogle Scholar
  34. Havens KE (2008) Cyanobacterial blooms: effects on aquatic ecosystems. In: Hudnell HK (ed) Cyanobacterial harmful algal blooms: state of the science and research needs. Springer, New York, pp 733–746CrossRefGoogle Scholar
  35. Henderson RJ, Tocher DR (1981) The lipid composition and biochemistry of freshwater fish. Prog Lipid Res 26:281–347CrossRefGoogle Scholar
  36. Huber V, Wagner C, Gerten D, Adrian R (2012) To bloom or not to bloom: contrasting responses of cyanobacteria to recent heat waves explained by critical thresholds of abiotic drivers. Oecologia 169:245–256PubMedCrossRefGoogle Scholar
  37. Hyenstrand P, Blomqvist P, Petterson A (1998) Factors determining cyanobacterial success in aquatic systems—a literature review. Arch Hydrobiol Spec Issue Adv Limnol 15:41–62Google Scholar
  38. Ishizaki Y, Masuda R, Uematsu K, Shimizu K, Arimoto M, Takeuchi T (2001) The effect of dietary docosahexaenoic acid on schooling behavior and brain development in larval yellowtail. J Fish Biol 58:1691–1703CrossRefGoogle Scholar
  39. Jacquet S et al (2005) The proliferation of the toxic cyanobacterium Planktothrix rubescens following restoration of the largest natural French lake (Lac du Bourget). Harmful Algae 4:651–672CrossRefGoogle Scholar
  40. Ka S, Mendoza-Vera JM, Bouvy M, Champalbert G, N’Gom-Ka R, Pagano M (2012) Can tropical freshwater zooplankton graze efficiently on cyanobacteria? Hydrobiologia 679:119–138CrossRefGoogle Scholar
  41. Kagami M, Von Elert E, Ibelings BW, de Bruin A, Van Donk E (2007) The parasitic chytrid, Zygorhizidium facilitates the growth of the cladoceran zooplankter, Daphnia in cultures of the inedible alga, Asterionella. Proc R Soc Lond B 274:1561–1566CrossRefGoogle Scholar
  42. Kappes H, Mechenich C, Sinsch U (2000) Long-term dynamics of Asplanchna priodonta in Lake Windsborn with comments on the diet. Hydrobiologia 432:91–100CrossRefGoogle Scholar
  43. Kerfoot WC, Kirk KL (1991) Degree of taste discrimination among suspension-feeding cladocerans and copepods—implications for detritivory and herbivory. Limnol Oceanogr 36:1107–1123CrossRefGoogle Scholar
  44. Kosten S et al (2012) Warmer climates boost cyanobacterial dominance in shallow lakes. Glob Change Biol 18:118–126CrossRefGoogle Scholar
  45. Koussoroplis AM, Bec A, Perga ME, Koutrakis E, Desvilettes C, Bourdier G (2010) Nutritional importance of minor dietary sources for leaping grey mullet Liza saliens (Mugilidae) during settlement: insights from fatty acid δ13C analysis. Mar Ecol Prog Ser 404:207–217CrossRefGoogle Scholar
  46. Leboulanger C, Dorigo U, Jacquet S, Le Berre B, Paolini G, Humbert JF (2002) Application of a submersible spectrofluorometer for rapid monitoring of freshwater cyanobacterial blooms: a case study. Aquat Microb Ecol 30:83–89CrossRefGoogle Scholar
  47. Lynch M, Shapiro J (1981) Predation, enrichment, and phytoplankton community structure. Limnol Oceanogr 26:86–102Google Scholar
  48. Martin-Creuzburg D, Wacker A, von Elert E (2005) Life history consequences of sterol availability in the aquatic keystone species Daphnia. Oecologia 144:362–372PubMedCrossRefGoogle Scholar
  49. Martin-Creuzburg D, von Elert E, Hoffmann KH (2008) Nutritional constraints at the cyanobacteria–Daphnia magna interface: the role of sterols. Limnol Oceanogr 53:456–468CrossRefGoogle Scholar
  50. Masson S, Angeli N, Guillard J, Pinel-Alloul B (2001) Diel vertical and horizontal distribution of crustacean zooplankton and young of the year fish in a sub-alpine lake: an approach based on high frequency sampling. J Plankton Res 23:1041–1060CrossRefGoogle Scholar
  51. Muller-Navarra DC, Brett MT, Liston AM, Goldman CR (2000) A highly unsaturated fatty acid predicts carbon transfer between primary producers and consumers. Nature 403:74–77PubMedCrossRefGoogle Scholar
  52. O’Leary MH (1988) Carbon isotopes in photosynthesis. Bioscience 38:328–336CrossRefGoogle Scholar
  53. Oberhaus L, Gélinas M, Pinel-Alloul B, Ghadouani A, Humbert J-F (2007) Grazing of two toxic Planktothrix species by Daphnia pulicaria: potential for bloom control and transfer of microcystins. J Plankton Res 29:827–838CrossRefGoogle Scholar
  54. Oberholster PJ, Botha AM, Cloete TE (2006) Use of molecular markers as indicators for winter zooplankton grazing on toxic benthic cyanobacteria colonies in an urban Colorado lake. Harmful Algae 5:705–716CrossRefGoogle Scholar
  55. Paerl HW (1996) Microscale physiological and ecological studies of aquatic cyanobacteria: macroscale implications. Microsc Res Tech 33:47–72PubMedCrossRefGoogle Scholar
  56. Paerl H, Huisman J (2008) Blooms like it hot. Science 320:57–58PubMedCrossRefGoogle Scholar
  57. Parnell A, Inger R, Bearhop S, Jackson AL (2008) SIAR: stable isotope analysis in R. http://cran.r-project.org/web/packages/siar/index.html
  58. 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, Berlin, pp 4–20CrossRefGoogle Scholar
  59. Pelletier JP, Orand A (1978) Appareil de prélèvement d'un échantillon dans un fluide. in. Patent number: 76.08579, FranceGoogle Scholar
  60. Piola RF, Suthers IM, Rissik D (2008) Carbon and nitrogen stable isotope analysis indicates freshwater shrimp Paratya australiensis Kemp, 1917 (Atyidae) assimilate cyanobacterial accumulations. Hydrobiologia 608:121–132CrossRefGoogle Scholar
  61. Porter KG, Orcutt GD (1980) Nutritional adequacy, manageability, and toxicity as factors that determine food quality of green and blue-green algae for Daphnia. Am Soc Limnol Oceanogr Spec Symp 3:268–281Google Scholar
  62. Ravet JL, Brett MT, Muller-Navarra DC (2003) A test of the role of polyunsaturated fatty acids in phytoplankton food quality for Daphnia using liposome supplementation. Limnol Oceanogr 48:1938–1947CrossRefGoogle Scholar
  63. Ravet JL, Brett MT, Arhonditsis GB (2010) The effects of seston lipids on zooplankton fatty acid composition in Lake Washington, Washington, USA. Ecology 91:180–190PubMedCrossRefGoogle Scholar
  64. Rezanka T, Dor I, Prell A, Dembitsky VM (2003) Fatty acid composition of six freshwater wild cyanobacterial species. Folia Microbiol 48:71–75CrossRefGoogle Scholar
  65. Shapiro J (1973) Blue-green algae: why they become dominant. Science 179:382–384PubMedCrossRefGoogle Scholar
  66. Sigee DC et al (1999) Biological control of cyanobacteria: principles and possibilities. Hydrobiologia 395:161–172CrossRefGoogle Scholar
  67. Sondergaard M, Liboriussen L, Pedersen AR, Jeppesen E (2008) Lake restoration by fish removal: short- and long-term effects in 36 Danish lakes. Ecosystems 11:1291–1305CrossRefGoogle Scholar
  68. Sonstebo JH, Rohrlack T (2011) Possible implications of chytrid parasitism for population subdivision in freshwater cyanobacteria of the genus Planktothrix. Appl Environ Microbiol 77:1344–1351PubMedCrossRefGoogle Scholar
  69. Sotton B, Anneville O, Cadel-Six S, Domaizon I, Krys S, Guillard J (2011) Spatial match between Planktothrix rubescens and whitefish in a mesotrophic peri-alpine lake: evidence of toxins accumulation. Harmful Algae 10:749–758CrossRefGoogle Scholar
  70. Straskraba M (1964) Preliminary results of a new method for the quantitative sorting of freshwater net plankton into main groups. Limnol Oceanogr 9:268–269Google Scholar
  71. Taipale SJ, Kainz MJ, Brett MT (2011) Diet-switching experiments show rapid accumulation and preferential retention of highly unsaturated fatty acids in Daphnia. Oikos 120:1674–1682CrossRefGoogle Scholar
  72. Tillmanns AR, Wilson AE, Pick FR, Sarnelle O (2008) Meta-analysis of cyanobacterial effects on zooplankton population growth rate: species-specific responses. Arch Hydrobiol 171:285–295CrossRefGoogle Scholar
  73. Tittel J et al (2003) Mixotrophs combine resource use to outcompete specialists: implications for aquatic food webs. Proc Natl Acad Sci USA 100:12776–12781PubMedCrossRefGoogle Scholar
  74. Utermohl H (1958) Zur Vervollkommung der quantitativen Phytoplankton-methodik. Mitt Int Verein Theor Angew Limnol 9:1–38Google Scholar
  75. 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 47:1764–1773CrossRefGoogle Scholar
  76. Von Elert E, Wolffrom T (2001) Supplementation of cyanobacterial food with polyunsaturated fatty acids does not improve growth of Daphnia. Limnol Oceanogr 46:1552–1558CrossRefGoogle Scholar
  77. Walsby AE, Dunn GNC, Davies PA (2004) Comparison of the depth where Planktothrix rubescens stratifies and the depth where the daily insolation supports its neutral buoyancy. New Phytol 162:109–122CrossRefGoogle Scholar
  78. Wetzel RG, Likens GE (2000) Limnological analyses, 3rd edn. Springer, New YorkGoogle Scholar
  79. White JD, Kaul RB, Knoll LB, Wilson AE, Sarnelle O (2011) Large variation in vulnerability to grazing within a population of the colonial phytoplankter, Microcystis aeruginosa. Limnol Oceanogr 56:1714–1724Google Scholar
  80. Wilson AE, Sarnelle O, Tillmanns AR (2006) Effects of cyanobacterial toxicity and morphology on the population growth of freshwater zooplankton: meta-analyses of laboratory experiments. Limnol Oceanogr 51:1915–1924CrossRefGoogle Scholar
  81. Wu FC, Chen HY (2012) Effects of dietary linolenic acid to linoleic acid ratio on growth, tissue fatty acid profile and immune response of the juvenile grouper Epinephelus malabaricus. Aquaculture 324:111–117CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Marie-Elodie Perga
    • 1
  • Isabelle Domaizon
    • 1
  • Jean Guillard
    • 1
  • Valérie Hamelet
    • 1
  • Orlane Anneville
    • 1
  1. 1.INRA, UMR 0042 CARRTELThononFrance

Personalised recommendations