Toxicity Overrides Morphology on Cylindrospermopsis raciborskii Grazing Resistance to the Calanoid Copepod Eudiaptomus gracilis

Microbial Ecology - Tập 71 Số 4 - Trang 835-844 - 2016
Luciana M. Rangel1, Kemal Ali Ger2, Lúcia Helena Sampaio da Silva1, Maria Carolina S. Soares3, Elisabeth J. Faassen4, Miquel Lürling4
1Departamento de Botânica - Museu Nacional, Universidade Federal do Rio de Janeiro, Rio de Janeiro, 20940-040, Brazil
2Departamento de Ecologia, Universidade Federal do Rio Grande do Norte, Natal, RN, Brazil
3Departamento de Engenharia Sanitária e Ambiental, Universidade Federal de Juiz de Fora, Juiz de Fora, MG, Brazil
4Department of Environmental Sciences, Aquatic Ecology and Water Quality Management Group, Wageningen University, Wageningen, The Netherlands

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O’Neil JM, Davis TW, Burford MA, Gobler CJ (2012) The rise of harmful cyanobacteria blooms: the potential roles of eutrophication and climate change. Harmful Algae 14:313–334. doi: 10.1016/j.hal.2011.10.027

Carey CC, Ibelings BW, Hoffmann EP et al (2012) Eco-physiological adaptations that favour freshwater cyanobacteria in a changing climate. Water Res 46:1394–1407. doi: 10.1016/j.watres.2011.12.016

Smayda TJ (2008) Complexity in the eutrophication–harmful algal bloom relationship, with comment on the importance of grazing. Harmful Algae 8:140–151. doi: 10.1016/j.hal.2008.08.018

Ger KA, Hansson L-A, Lürling M (2014) Understanding cyanobacteria-zooplankton interactions in a more eutrophic world. Freshw Biol 59:1783–1798. doi: 10.1111/fwb.12393

Panosso R, Carlsson P, Kozlowsky-Suzuki B et al (2003) Effect of grazing by a neotropical copepod, Notodiaptomus, on a natural cyanobacterial assemblage and on toxic and non-toxic cyanobacterial strains. J Plankton Res 25:1169–1175. doi: 10.1093/plankt/25.9.1169

Rohrlack T, Dittmann E, Henning M et al (1999) Role of microcystins in poisoning and food ingestion inhibition of Daphnia galeata caused by the cyanobacterium Microcystis aeruginosa. Appl Environ Microbiol 65:737–739

Lürling M (2003) Daphnia growth on microcystin-producing and microcystin-free Microcystis aeruginosa in different mixtures with the green alga Scenedesmus obliquus. Limnol Oceanogr 48:2214–2220

Lürling M (2003) Effects of microcystin-free and microcystin-containing strains of the cyanobacterium Microcystis aeruginosa on growth of the grazer Daphnia magna. Environ Toxicol 18:202–210. doi: 10.1002/tox.10115

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 51:1915–1924

Ghadouani A, Pinel-Alloul B, Prepas EE (2003) Effects of experimentally induced cyanobacterial blooms on crustacean zooplankton communities. Freshw Biol 48:363–381. doi: 10.1046/j.1365-2427.2003.01010.x

Reichwaldt ES, Song H, Ghadouani A (2013) Effects of the distribution of a toxic Microcystis bloom on the small scale patchiness of zooplankton. PLoS One 8:e66674. doi: 10.1371/journal.pone.0066674

Ger KA, Panosso R, Lürling M (2011) Consequences of acclimation to Microcystis on the selective feeding behavior of the calanoid copepod Eudiaptomus gracilis. Limnol Oceanogr 56:2103–2114

Bouvy M, Pagano M, Troussellier M (2001) Effects of a cyanobacterial bloom (Cylindrospermopsis raciborskii) on bacteria and zooplankton communities in Ingazeira reservoir (northeast Brazil). Aquat Microb Ecol 25:215–227

Silva LHS, Huszar VLM, Marinho MM et al (2014) Drivers of phytoplankton, bacterioplankton, and zooplankton carbon biomass in tropical hydroelectric reservoirs. Limnol - Ecol Manag Inl Waters 48:1–10. doi: 10.1016/j.limno.2014.04.004

Heuschele J, Selander E (2014) The chemical ecology of copepods. J Plankton Res 36:895–913. doi: 10.1093/plankt/fbu025

DeMott WR (1986) The role of taste in food selection by freshwater zooplankton. Oecologia 69:334–340. doi: 10.1007/BF00377053

Kurmayer R, 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

Sinha R, Pearson LA, Davis TW et al (2012) Increased incidence of Cylindrospermopsis raciborskii in temperate zones-is climate change responsible? Water Res 46:1408–1419. doi: 10.1016/j.watres.2011.12.019

Briand J-F, Leboulanger C, Humbert J-F et al (2004) Cylindrospermopsis raciborskii (Cyanobacteria) invasion at mid-latitudes: selection, wide physiological tolerance, or global warming? J Phycol 40:231–238. doi: 10.1111/j.1529-8817.2004.03118.x

Bonilla S, Aubriot L, Soares MCS et al (2012) What drives the distribution of the bloom-forming cyanobacteria Planktothrix agardhii and Cylindrospermopsis raciborskii? FEMS Microbiol Ecol 79:594–607

Dittmann E, Fewer DP, Neilan BA (2013) Cyanobacterial toxins: biosynthetic routes and evolutionary roots. FEMS Microbiol Rev 37:23–43. doi: 10.1111/j.1574-6976.2012.12000.x

Neilan BA, Pearson LA, Muenchhoff J et al (2013) Environmental conditions that influence toxin biosynthesis in cyanobacteria. Environ Microbiol 15:1239–1253. doi: 10.1111/j.1462-2920.2012.02729.x

Boopathi T, Ki J-S (2014) Impact of environmental factors on the regulation of cyanotoxin production. Toxins (Basel) 6:1951–1978. doi: 10.3390/toxins6071951

Soares MCS, Lürling M, Huszar VLM (2013) Growth and temperature-related phenotypic plasticity in the cyanobacterium Cylindrospermopsis raciborskii. Phycol Res 61:61–67. doi: 10.1111/pre.12001

Hong Y, Burford MA, Ralph PJ et al (2013) The cyanobacterium Cylindrospermopsis raciborskii is facilitated by copepod selective grazing. Harmful Algae 29:14–21. doi: 10.1016/j.hal.2013.07.003

Sterner RW (1989) The role of grazers in phytoplankton succession. In: Sommer U (ed) Phytoplankt. Ecol. Succession Plankt. Communities. Springer, Berlin Heidelberg, Berlin, Heidelberg, pp 107–170

Panosso R, Lürling M (2010) Daphnia magna feeding on Cylindrospermopsis raciborskii: the role of food composition, filament length and body size. J Plankton Res 32:1393–1404. doi: 10.1093/plankt/fbq057

Marinho MM, Souza MBG, Lürling M (2013) Light and phosphate competition between Cylindrospermopsis raciborskii and Microcystis aeruginosa is strain dependent. Microb Ecol 66:479–488. doi: 10.1007/s00248-013-0232-1

Lürling M, Beekman W (1999) Grazer-induced defenses in Scenedesmus (Chlorococcales; Chlorophyceae): coenobium and spine formation. Phycologia 38:368–376. doi: 10.2216/i0031-8884-38-5-368.1

Lürling M, van Oosterhout F (2013) Controlling eutrophication by combined bloom precipitation and sediment phosphorus inactivation. Water Res 47:6527–6537. doi: 10.1016/j.watres.2013.08.019

Rocha O, Duncan A (1985) The relationship between cell carbon and cell volume in freshwater algal species used in zooplanktonic studies. J Plankton Res 7:279–294. doi: 10.1093/plankt/7.2.279

Lürling M, Verschoor AM (2003) F O -spectra of chlorophyll fluorescence for the determination of zooplankton grazing. Hydrobiologia 491:145–157. doi: 10.1023/A:1024436508387

Yamamoto Y, Shiah F-K (2014) Growth, trichome size and akinete production of Cylindrospermopsis raciborskii (cyanobacteria) under different temperatures: comparison of two strains isolated from the same pond. Phycol Res 62:147–152. doi: 10.1111/pre.12040

Alster A, Kaplan-Levy RN, Sukenik A, Zohary T (2009) Morphology and phylogeny of a non-toxic invasive Cylindrospermopsis raciborskii from a Mediterranean Lake. Hydrobiologia 639:115–128. doi: 10.1007/s10750-009-0044-y

Castro D, Vera D, Lagos N et al (2004) The effect of temperature on growth and production of paralytic shellfish poisoning toxins by the cyanobacterium Cylindrospermopsis raciborskii C10. Toxicon 44:483–489. doi: 10.1016/j.toxicon.2004.06.005

Saker ML, Griffiths DJ (2000) The effect of temperature on growth and cylindrospermopsin content of seven isolates of Cylindrospermopsis raciborskii (Nostocales, Cyanophyceae) from water bodies in northern Australia. Phycologia 39:349–354

Engstrom J, Koski M, Viitasalo M et al (2000) Feeding interactions of the copepods Eurytemora affinis and Acartia bifilosa with the cyanobacteria Nodularia sp. J Plankton Res 22:1403–1409

Munday R, Reeve J (2013) Risk assessment of shellfish toxins. Toxins (Basel) 5:2109–2137. doi: 10.3390/toxins5112109

DeMott WR, Moxter F (1991) Foraging cyanobacteria by copepods: responses to chemical defense and resource abundance. Ecology 72:1820–1834

Ger KA, Panosso R (2014) The effects of a microcystin-producing and lacking strain of Microcystis on the survival of a widespread tropical copepod (Notodiaptomus iheringi). Hydrobiologia 738:61–73. doi: 10.1007/s10750-014-1915-4

Litchman E, de Tezanos PP, Klausmeier CA et al (2010) Linking traits to species diversity and community structure in phytoplankton. Hydrobiologia 653:15–28. doi: 10.1007/s10750-010-0341-5

Litchman E, Klausmeier CA (2008) Trait-based community ecology of phytoplankton. Annu Rev Ecol Evol Syst 39:615–639. doi: 10.1146/annurev.ecolsys.39.110707.173549

Fulton RS, Paerl HW (1987) Toxic and inhibitory effects of the blue-green alga Microcystis aeruginosa on herbivorous zooplankton. J Plankton Res 9:837–855. doi: 10.1093/plankt/9.5.837

Bednarska A, Pietrzak B, Pijanowska J (2014) Effect of poor manageability and low nutritional value of cyanobacteria on Daphnia magna life history performance. J Plankton Res 36:838–847. doi: 10.1093/plankt/fbu009

Kâ S, Mendoza-Vera JM, Bouvy M et al (2011) Can tropical freshwater zooplankton graze efficiently on cyanobacteria? Hydrobiologia 679:119–138. doi: 10.1007/s10750-011-0860-8

Berggreen U, Hansen B, Kiørboe T (1988) Food size spectra, ingestion and growth of the copepod Acartia tonsa during development: implications for determination of copepod production. Mar Biol 99:341–352. doi: 10.1007/BF02112126

Galloway AWE, Winder M (2015) Partitioning the relative importance of phylogeny and environmental conditions on phytoplankton fatty acids. PLoS One 10:e0130053. doi: 10.1371/journal.pone.0130053

Cowles TJ, Olson RJ, Chisholm SW (1988) Food selection by copepods: discrimination on the basis of food quality. Mar Biol 100:41–49. doi: 10.1007/BF00392953