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Effects of microcystin-producing and microcystin-free strains of Planktothrix agardhii on long-term population dynamics of Daphnia magna

Published online by Cambridge University Press:  18 September 2012

Florence D. Hulot ,
David Carmignac ,
Stéphane Legendre ,
Claude Yéprémian  and
Cécile Bernard
Florence D. Hulot*
Affiliation:
Écologie, Systématique et Évolution, UMR 8079, Univ. Paris-Sud, Orsay, France UFR Sciences de la Vie, UPMC Univ. Paris 06, Paris, France Bioemco, UMR 7618, École Normale Supérieure, Paris Cedex 05, France
David Carmignac
Affiliation:
Bioemco, UMR 7618, École Normale Supérieure, Paris Cedex 05, France
Stéphane Legendre
Affiliation:
Écologie et Évolution, UMR 7625, École Normale Supérieure, 46 rue d'Ulm, 75005 Paris, France
Claude Yéprémian
Affiliation:
UMR 7245 CNRS/MNHN MCAM, Cyanobactéries, Cyanotoxines et Environnement, Muséum National d'Histoire Naturelle, 57 rue Cuvier, CP 39, 75231 Paris Cedex 05, France
Cécile Bernard
Affiliation:
UMR 7245 CNRS/MNHN MCAM, Cyanobactéries, Cyanotoxines et Environnement, Muséum National d'Histoire Naturelle, 57 rue Cuvier, CP 39, 75231 Paris Cedex 05, France
*
*Corresponding author: [email protected]
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Abstract

The effects of cyanobacterial toxins on herbivorous zooplankton depend on cyanobacterial strains, zooplankton species and environmental conditions. To explore the relationship between zooplankton and cyanobacteria, we investigated the effects of Planktothrix agardhii extracts on Daphnia magna population dynamics. We designed an experiment where individuals were grown in the presence of extracts of two P. agardhii strains. We monitored daily life-history parameters of D. magna individuals subjected to microcystin-RR (MC-RR), intracellular and extracellular extracts of a microcystin-producing strain (MC-strain, PMC 75.02) and a microcystin-free strain (MC-free strain, PMC 87.02) of P. agardhii. Measured life-history parameters of D. magna were used to build population dynamics models and compute expected population growth rate, replacement rate, generation time and proportion of adult and juveniles at demographic equilibrium. Results show that MC-RR tends to slow the life history (reduced growth rate and larger proportion of adults). In contrast, intracellular extracts of the two strains tend to accelerate the life history (increased growth rate, decreased generation time and lower proportion of adults). Extracellular extracts produce the same trends as the intracellular extracts but to a lesser extent. However, the MC-strain has stronger effects than the MC-free strain. Interestingly, extracellular extracts of the MC-free strain may have effects comparable to pure MC-RR. Moreover, in the presence of MC-RR and both cyanobacterial extracts, the daily fecundities present a cyclic pattern. These results suggest that MC-RR and unknown metabolites of cyanobacterial extracts have negative effects on D. magna reproduction processes such as those observed with endocrine-disruptive molecules.

Keywords

Planktothrix agardhiiDaphnia magnatoxic cyanobacteriapopulation dynamicsmatrix population model
Type
Research Article
Information
Annales de Limnologie - International Journal of Limnology , Volume 48 , Issue 3 , 2012 , pp. 337 - 347
Copyright
© EDP Sciences, 2012

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References

Babica, P., Bláha, L. and Maršálek, B., 2006. Exploring the natural role of microcystins – A review of effects on photoautotrophic organisms. J. Phycol., 42, 9–20.CrossRefGoogle Scholar
Barbosa, I.R., Nogueira, A.J.A. and Soares, A., 2008. Acute and chronic effects of testosterone and 4-hydroxyandrostenedione to the crustacean Daphnia magna. Ecotoxicol. Environ. Safe., 71, 757–764.CrossRefGoogle ScholarPubMed
Brett, M.T. and Goldman, C.R., 1996. A meta-analysis of the freshwater trophic cascade. Proc. Natl. Acad. Sci. USA, 93, 7723–7726.CrossRefGoogle ScholarPubMed
Briand, J.F., Robillot, C., Quiblier-Lloberas, C. and Bernard, C., 2002. A perennial bloom of Planktothrix agardhii (Cyanobacteria) in a shallow eutrophic French lake: limnological and microcystin production studies. Arch. Hydrobiol., 153, 605–622.CrossRefGoogle Scholar
Burkhardt-Holm, P., 2010. Endocrine disruptors and water quality: a state-of-the-art review. Int. J. Water. Resour. D, 26, 477–493.CrossRefGoogle Scholar
Burns, C.W., 1968. The relationship between body size of filter-feeding Cladocera and the maximum size of particle ingested. Limnol. Oceanogr., 13, 675–678.CrossRefGoogle Scholar
Buryskova, B., Hilscherova, K., Babica, P., Vrskova, D., Marsalek, B. and Blaha, L., 2006. Toxicity of complex cyanobacterial samples and their fractions in Xenopus laevis embryos and the role of microcystins. Aquat. Toxicol., 80, 346–354.CrossRefGoogle ScholarPubMed
Carmichael, W.W., 1992. Cyanobacteria secondary metabolites – the cyanotoxins. J. Appl. Bacteriol., 72, 445–459.CrossRefGoogle ScholarPubMed
Caswell, H., 1989. Matrix Population Models, Sinauer Associates, Inc., Sunderland, Massachusetts, 328 p.Google Scholar
Catherine, A., Quiblier, C., Yepremian, C., Got, P., Groleau, A., Vincon-Leite, B., Bernard, C. and Troussellier, M., 2008. Collapse of a Planktothrix agardhii perennial bloom and microcystin dynamics in response to reduced phosphate concentrations in a temperate lake. FEMS Microbiol. Ecol., 65, 61–73.CrossRefGoogle Scholar
Codd, G.A., Lindsay, J., Young, F.M., Morrison, L.F. and Metcalf, J.S., 2005. Harmful cyanobacteria. From mass mortalities to management measures. In: Huisman, J., Matthijs, H.C.P. and Visser, P.M. (eds.), Harmful Cyanobacteria, Springer, 1–23.Google Scholar
DeMott, W., Zhang, Q. and Carmichael, W., 1991. Effects of toxic cyanobacteria and purified toxins on the survival and feeding of a copepod and three species of Daphnia. Limnol. Oceanogr., 36, 1346–1357.CrossRefGoogle Scholar
Ferrão-Filho, A., Azevedo, S. and DeMott, W., 2000. Effects of toxic and non-toxic cyanobacteria on the life history of tropical and temperate cladocerans. Freshwater Biol., 45, 1–19.CrossRefGoogle Scholar
Ferrière, R., Sarrazin, F., Legendre, S. and Baron, J.-P., 1996. Matrix population models applied to viability analysis and conservation: theory and practice using the ULM software. Acta Oecol., 17, 629–656.Google Scholar
Foy, R.H., 1980. The influence of surface to volume ratio on the growth-rates of planktonic blue-green-algae. Br. Phycol. J., 15, 279–289.CrossRefGoogle Scholar
Ghadouani, A., Pinel-Alloul, B. and Prepas, E.E., 2006. Could increased cyanobacterial biomass following forest harvesting cause a reduction in zooplankton body size structure? Can. J. Fish. Aquat. Sci., 63, 2308–2317.CrossRefGoogle Scholar
Gross, E.M., 2003. Allelopathy of aquatic autotrophs. Crit. Rev. Plant. Sci., 22, 313–339.CrossRefGoogle Scholar
Hamlaoui, S., Couté, A., Lacroix, G. and Lescher-Moutoué, F., 1998. Nutrient and fish effects on the morphology of the Dinoflagellate. C. R. Acad. Sci. Paris, Sciences de la Vie, 321, 39–45.Google Scholar
Hansson, L.A. and Carpenter, S., 1993. Relative importance of nutrient availability and food chain for size and community composition in phytoplankton. Oikos, 67, 257–263.CrossRefGoogle Scholar
Hansson, L.A., Gustafsson, S., Rengefors, K. and Bomark, L., 2007. Cyanobacterial chemical warfare affects zooplankton community composition. Freshwater Biol., 52, 1290–1301.CrossRefGoogle Scholar
Jang, M.-H., Ha, K., Joo, G.-J. and Takamura, N., 2003. Toxin production of cyanobacteria is increased by exposure to zooplankton. Freshwater Biol., 48, 1540.CrossRefGoogle Scholar
Jang, M.H., Ha, K. and Takamura, N., 2008. Microcystin production by Microcystis aeruginosa exposed to different stages of herbivorous zooplankton. Toxicon, 51, 882–889.CrossRefGoogle ScholarPubMed
Jungmann, D., 1992. Toxic compounds isolated from microcystis Pcc7806 that are more active against daphnia than 2 microcystins. Limnol. Oceanogr., 37, 1777–1783.CrossRefGoogle Scholar
Keil, C., Forchert, A., Fastner, J., Szewzyk, U., Rotard, W., Chorus, I. and Kratke, R., 2002. Toxicity and microcystin content of extracts from a Planktothrix bloom and two laboratory strains. Water Res., 36, 2133–2139.CrossRefGoogle ScholarPubMed
Kilham, S.S., Kreeger, D.A., Lynn, S.G., Goulden, C.E. and Herrera, L., 1998. COMBO: a defined freshwater culture medium for algae and zooplankton. Hydrobiologia, 377, 147–159.CrossRefGoogle Scholar
Kim, Y., Jung, J., Oh, S. and Choi, K., 2008. Aquatic toxicity of cartap and cypermethrin to different life stages of Daphnia magna and Oryzias latipes. J. Environ. Sci. Health B, 43, 56–64.CrossRefGoogle ScholarPubMed
Kirk, K. and Gilbert, J.J., 1992. Variation in herbivore response to chemical defenses – zooplankton foraging on toxic cyanobacteria. Ecology, 73, 2208–2217.CrossRefGoogle Scholar
Kotai, J., 1972. Instructions for preparation of modified nutrient solution Z8 for algae, Publication B.11 69, Norwegian Institute for Water Research, Oslo, 1–5.
Kurmayer, R., 2001. Competitive ability of Daphnia under dominance of non-toxic filamentous cyanobacteria. Hydrobiologia, 442, 279–289.CrossRefGoogle Scholar
Kurmayer, R. and Jüttner, F., 1999. Strategies for the co-existence of zooplankton with the toxic cyanobacterium Planktothrix rubescens in Lake Zurich. J. Plankton. Res., 21, 659–683.CrossRefGoogle Scholar
Leflaive, J. and Ten-Hage, L., 2007. Algal and cyanobacterial secondary metabolites in freshwaters: a comparison of allelopathic compounds and toxins. Freshwater Biol., 52, 199–214.CrossRefGoogle Scholar
Legendre, S. and Clobert, J., 1995. ULM, a software for conservation and evolutionary biologists. J. Appl. Stat., 22, 817–834.CrossRefGoogle Scholar
Lürling, M., 2003a. Phenotypic plasticity in the green algae Desmodesmus and Scenedesmus with special reference to the induction of defensive morphology. Ann. Limnol. ‐ Int. J. Lim., 39, 85–101.CrossRefGoogle Scholar
Lürling, M., 2003b. Daphnia growth on microcystin-producing and microcystin-free Microcystis aeruginosa in different mixtures with the green alga Scenedesmus obliquus. Limnol. Oceanogr., 48, 2214–2220.CrossRefGoogle Scholar
Lürling, M. and Van Donk, E., 1997. Morphological changes in Scenedesmus induced by infochemicals released in situ from zooplankton grazers. Limnol. Oceanogr., 42, 783–788.CrossRefGoogle Scholar
Lyck, S., 2004. Simultaneous changes in cell quotas of microcystin, chlorophyll a, protein and carbohydrate during different growth phases of a batch culture experiment with Microcystis aeruginosa. J. Plankton Res., 26, 727–736.CrossRefGoogle Scholar
Oziol, L. and Bouaïcha, N., 2010. First evidence of estrogenic potential of the cyanobacterial heptotoxins the nodularin-R and the microcystin-LR in cultured mammalian cells. J. Hazard. Mater., 174, 610–615.CrossRefGoogle ScholarPubMed
Park, H.D., Iwami, C., Watanabe, M.F., Harada, K., Okino, T. and Hayashi, H., 1998. Temporal variabilities of the concentrations of intra- and extracellular microcystin and toxic microcystis species in a hypertrophic lake, Lake Suwa, Japan (1991–1994). Environ. Toxicol. Water Qual., 13, 61–72.3.0.CO;2-5>CrossRefGoogle Scholar
Pawlik-Skowronska, B., Pirszel, J. and Kornijow, R., 2008. Spatial and temporal variation in microcystin concentrations during perennial bloom of Planktothrix agardhii in a hypertrophic lake. Ann. Limnol. ‐ Int. J. Lim., 44, 145–150.CrossRefGoogle Scholar
Rohrlack, T. and Hyenstrand, P., 2007. Fate of intracellular microcystins in the cyanobacterium Microcystis aeruginosa (Chroococcales, Cyanophyceae). Phycologia, 46, 277–283.CrossRefGoogle Scholar
Rohrlack, T., Dittmann, E., Henning, M., Borner, T. and Kohl, J.G., 1999a. Role of microcystins in poisoning and food ingestion inhibition of Daphnia galeata caused by the cyanobacterium Microcystis aeruginosa. Appl. Environ. Microbiol., 65, 737–739.Google Scholar
Rohrlack, T., Henning, M. and Kohl, J.G., 1999b. Mechanisms of the inhibitory effect of the cyanobacterium Microcystis aeruginosa on Daphnia galeata's ingestion rate. J. Plankton Res., 21, 1489–1500.CrossRefGoogle Scholar
Rohrlack, T., Christoffersen, K., Kaebernick, M. and Neilan, B.A., 2004. Cyanobacterial protease inhibitor microviridin J causes a lethal molting disruption in Daphnia pulicaria. Appl. Environ. Microbiol., 70, 5047–5050.CrossRefGoogle ScholarPubMed
Schatz, D., Keren, Y., Vardi, A., Sukenik, A., Carmeli, S., Boerner, T., Dittmann, E. and Kaplan, A., 2007. Towards clarification of the biological role of microcystins, a family of cyanobacterial toxins. Environ. Microbiol., 9, 965–970.CrossRefGoogle ScholarPubMed
Sivonen, K. and Jones, G., 1999. Cyanobacterial toxins. In: Chorus, I. and Bartram, (eds.), Toxic Cyanobacteria in Water: A Guide to Public Health. Significance, Monitoring and Management, Published on Behalf of the World Health Organization by Spon/Chapman & Hall, London, 41–111.Google Scholar
Tillmann, U. and John, U., 2002. Toxic effects of Alexandrium spp. on heterotrophic dinoflagellates: an allelochemical defence mechanism independent of PSP-toxin content. Mar. Ecol. Prog. Ser., 230, 47–58.CrossRefGoogle Scholar
Tillmanns, A.R., Wilson, A.E., Pick, F.R. and Sarnelle, O., 2008. Meta-analysis of cyanobacterial effects on zooplankton population growth rate: species-specific responses. Fundam. Appl. Limnol., 171, 285–295.CrossRefGoogle Scholar
Turner, J.T. and Tester, P.A., 1997. Toxic marine phytoplankton, zooplankton grazers, and pelagic food webs. Limnol. Oceanogr., 42, 1203–1214.CrossRefGoogle Scholar
Vanni, M.J., 1987. Effects of nutrients and zooplankton size on the structure of a phytoplankton community. Ecology, 68, 624–635.CrossRefGoogle Scholar
Vanni, M.J. and Findlay, D.L., 1990. Trophic cascades and phytoplankton community structure. Ecology, 71, 921–937.CrossRefGoogle Scholar
Vasconcelos, V.M. and Pereira, E., 2001. Cyanobacteria diversity and toxicity in a wastewater treatment plant (Portugal). Water Res., 35, 1354–1357.CrossRefGoogle Scholar
Webster, K.E. and Peters, R.H., 1978. Some size-dependent inhibitions of larger cladoceran filterers in filamentous suspensions. Limnol. Oceanogr., 23, 1238–1245.CrossRefGoogle Scholar
Wiegand, C. and Pflugmacher, S., 2005. Ecotoxicological effects of selected cyanobacterial secondary metabolites a short review. Toxicol. Appl. Pharm., 203, 201–218.CrossRefGoogle ScholarPubMed
Wilson, A.E. and Hay, M.E., 2007. A direct test of cyanobacterial chemical defense: variable effects of microcystin-treated food on two Daphnia pulicaria clones. Limnol. Oceanogr., 52, 1467–1479.CrossRefGoogle Scholar
Wilson, A.E., Sarnelle, O. and Tillmanns, A.R., 2006. Effects of cyanobacterial toxicity and morphology on the population growth of freshwater zooplankton: meta-analyses of laboratory experiments. Limnol. Oceanogr., 51, 1915–1924.CrossRefGoogle Scholar
Yéprémian, C., Gugger, M.F., Briand, E., Catherine, A., Berger, C., Quiblier, C. and Bernard, C., 2007. Microcystin ecotypes in a perennial Planktothrix agardhii bloom. Water Res., 41, 4446–4456.CrossRefGoogle Scholar