Acta Limnologica Brasiliensia
https://app.periodikos.com.br/journal/alb/article/doi/10.1590/S2179-975X10719
Acta Limnologica Brasiliensia
Original Article

Species-specific response of phytoplankton to zooplankton grazing in tropical eutrophic reservoirs

Resposta espécie-específica do fitoplâncton ao pastejo do zooplâncton em reservatórios eutróficos tropicais

Juliana dos Santos Severiano; Camila Bezerra Amaral; Anamaria Silva Diniz; Ariadne do Nascimento Moura

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Abstract

Abstract:: Aim: To test the hypothesis that zooplankton changes the structure of phytoplankton in tropical reservoirs by reducing the biomass of algal species susceptible to herbivory.

Methods: We experimentally evaluated the species-specific responses of phytoplankton to zooplankton within eutrophic reservoirs with different phytoplankton community structure in northeastern of Brazil. Water samples were collected from the subsurface in coastal regions of the Apipucos and Mundaú reservoirs in January/2012 and November/2014, respectively, and transported to the laboratory. The experiments were performed in Erlenmeyer flasks (1 liter) filled with water from the sample sites and were maintained for five days in the laboratory conditions. Two treatments were maintained (1) with phytoplankton and the presence of the native zooplankton and (2) without native zooplankton.

Results: Zooplankton proved to be an important factor, modifying the structure of the phytoplankton community, especially in the Apipucos reservoir. In this reservoir, we observed a significant reduction of biomass in diatom Cyclotella meneghiniana, and the chlorophyte Chlamydomonas sp., and an increase in the biomass of Raphidiopsis raciborskii. In the Mundaú reservoir, we observed a significant reduction of C. meneghiniana and R. raciborskii, while cyanobacteria Microcystis aeruginosa increased their biomasses in the presence of zooplankton.

Conclusions: These results show the importance of the microalgae community structure in phytoplankton-zooplankton interactions for food webs in tropical environments, as well as support the role of zooplankton in fostering cyanobacterial growth and maintain algal blooms.

Keywords

cyanobacterial blooms, Thermocyclops, top-down control, food webs

Resumo

Resumo:: Objetivo: Testar a hipótese de que o zooplâncton altera a estrutura do fitoplâncton em reservatórios tropicais, reduzindo a biomassa de espécies de algas susceptíveis a herbivoria.

Métodos: Avaliamos experimentalmente as respostas espécie-específicas do fitoplâncton ao zooplâncton em reservatórios eutróficos com diferentes estruturas da comunidade fitoplanctônica no nordeste do Brasil. Amostras de água foram coletadas da subsuperfície nas regiões costeiras dos reservatórios Apipucos e Mundaú em janeiro/2012 e novembro/2014, respectivamente, e transportadas para o laboratório. Os experimentos foram realizados em frascos Erlenmeyer (1 litro) cheios de água dos locais das amostras e mantidos por cinco dias nas condições laboratoriais. Dois tratamentos foram mantidos (1) com fitoplâncton e presença do zooplâncton nativo e (2) sem zooplâncton nativo.

Resultados: O zooplâncton provou ser um fator importante, modificando a estrutura da comunidade fitoplanctônica, principalmente no reservatório de Apipucos. Neste reservatório, observamos uma redução significativa na biomassa de Cyclotella meneghiniana e Chlamydomonas sp., e um incremento na biomassa de Raphidiopsis raciborskii. No reservatório Mundaú, observamos uma redução significativa de C. meneghiniana e R. raciborskii, enquanto a cianobactéria Microcystis aeruginosa aumentou sua biomassa na presença de zooplâncton.

Conclusões: Estes resultados mostram a importância da estrutura da comunidade de microalgas nas interações fitoplancton-zooplâncton para as cadeias alimentares em ambientes tropicais, bem como, apoiam o papel do zooplâncton na promoção do crescimento de cianobactérias e na manutenção da proliferação de algas.
 

Palavras-chave

florações de cianobactérias, Thermocyclops, controle top-down, teia alimentar

References

ALMEIDA, V.L.S., DANTAS, Ê.W., MELO-JÚNIOR, M., BITTENCOURT-OLIVEIRA, M.C. and MOURA, A.N. Zooplanktonic community of six reservoirs in northeast Brazil. Brazilian Journal of Biology = Revista Brasileira de Biologia, 2009, 69(1), 57-65. http://dx.doi.org/10.1590/S1519-69842009000100007. PMid:19347146.

ALMEIDA, V.L.S., MELÃO, M.G.G. and MOURA, A.N. Plankton diversity and limnological characterization in two shallow tropical urban reservoirs of Pernambuco State, Brazil. Anais da Academia Brasileira de Ciências, 2012, 84(2), 537-550. http://dx.doi.org/10.1590/S0001-37652012005000027. PMid:22534751.

ANDRADE, A. and LÓPEZ, C. Predatory interactions between Thermocyclops decipiens Kiefer (Cyclopoida: Copepoda) and two small cladocerans: behavior and prey post-encounter vulnerability. Annales de Limnologie - International Journal of Limnology, 2005, 41(3), 153-159. http://dx.doi.org/10.1051/limn:20054130153.

BITTENCOURT-OLIVEIRA, M.C., MOURA, A.N., HEREMAN, T.C. and DANTAS, Ê.W. Increase in straight and coiled Cylindrospermopsis raciborskii (Cyanobacteria) Populations under Conditions of Thermal De-Stratification in a Shallow Tropical Reservoir. Journal of Water Resource and Protection, 2011, 3(4), 245-252. http://dx.doi.org/10.4236/jwarp.2011.34031.

BORGES, P.A.F., TRAIN, S., DIAS, J.D. and BONECKER, C.C. Effects of fish farming on plankton structure in a Brazilian tropical reservoir. Hydrobiologia, 2010, 649(1), 279-291. http://dx.doi.org/10.1007/s10750-010-0271-2.

CARVALHO, M.A.J. On feeding behavior of Thermocyclops crassus. Crustaceana, 1984, 7, 122-125.

CHALAR, G. The use of phytoplankton patterns of diversity for algal bloom management. Limnologica, 2009, 39(3), 200-208. http://dx.doi.org/10.1016/j.limno.2008.04.001.

COLINA, M., CALLIARI, D., CARBALLO, C. and KRUK, C. A trait-based approach to summarize zooplankton–phytoplankton interactions in fresh waters. Hydrobiologia, 2016, 767(1), 221-233. http://dx.doi.org/10.1007/s10750-015-2503-y.

DANIELSDOTTIR, M.G., BRETT, M.T. and ARHONDITSIS, G.B. Phytoplankton food quality control of planktonic food web processes. Hydrobiologia, 2007, 589(1), 29-41. http://dx.doi.org/10.1007/s10750-007-0714-6.

DANTAS, Ê.W., MOURA, A.N., BITTENCOURT-OLIVEIRA, M.C., ARRUDA NETO, J.D.T. and CAVALCANTI, A.D.C. Temporal variation of the phytoplankton community at short sampling intervals in the Mundaú reservoir, Northeastern Brazil. Acta Botanica Brasílica, 2008, 22(4), 970-982. http://dx.doi.org/10.1590/S0102-33062008000400008.

DINIZ, A.S., SEVERIANO, J.S., MELO JÚNIOR, M., DANTAS, Ê.W. and MOURA, A.N. Phytoplankton–zooplankton relationships based on phytoplankton functional groups in two tropical reservoirs. Marine and Freshwater Research, 2019, 70(5), 721-733. http://dx.doi.org/10.1071/MF18049.

GEBREHIWOT, M., KIFLE, D. and TRIEST, L. Grazing and growth rate of a cyclopoid copepod fed with a phytoplankton diet constituted by a filamentous cyanobacterium. Hydrobiologia, 2019, 828(1), 213-227. http://dx.doi.org/10.1007/s10750-018-3813-7.

GER, K.A., HANSSON, L.A. and LÜRLING, M. Understanding cyanobacteria-zooplankton interactions in a more eutrophic world. Freshwater Biology, 2014, 59(9), 1783-1798. http://dx.doi.org/10.1111/fwb.12393.

GER, K.A., URRUTIA-CORDERO, P., FROST, P.C., HANSSON, L.A., SARNELLE, O., WILSON, A.E. and LÜRLING, M. The interaction between cyanobacteria and zooplankton in a more eutrophic world. Harmful Algae, 2016, 54, 128-144. http://dx.doi.org/10.1016/j.hal.2015.12.005. PMid:28073472.

GILBERT, J.J. and STARKWEATHER, P.L. Feeding in the rotifer Brachionus calyciflorus. Oecologia, 1977, 28(2), 125-131. http://dx.doi.org/10.1007/BF00345247. PMid:28309010.

GLIWICZ, Z.M. and LAMPERT, W. Food thresholds in Daphnia species in the absence and presence of blue-green filaments. Ecology, 1990, 71(2), 691-702. http://dx.doi.org/10.2307/1940323.

GLIWICZ, Z.M. Zooplankton. In: P.E. O’SULLIVAN and C.S. REYNOLDS, eds. The Lakes Handbook: Limnology and limnetic ecology. Oxford: Blackwell Science, 2004, pp. 461–516.

HANEY, J. Field studies on zooplankton-cyanobacteria interactions. New Zealand Journal of Marine and Freshwater Research, 1987, 21(3), 467-475. http://dx.doi.org/10.1080/00288330.1987.9516242.

HANSSON, L.A., GUSTAFSSON, S., RENGEFORS, K. and BOMARK, L. Cyanobacterial chemical warfare affects zooplankton community composition. Freshwater Biology, 2007, 52(7), 1290-1301. http://dx.doi.org/10.1111/j.1365-2427.2007.01765.x.

HEATHCOTE, A.J., FILSTRUP, C.T., KENDALL, D. and DOWNING, J.A. Biomass pyramids in lake plankton: influence of Cyanobacteria size and abundance. Inland Waters, 2016, 6(2), 250-257. http://dx.doi.org/10.5268/IW-6.2.941.

HILL, M., CHADD, R.P., MORRIS, N., SWAINE, J.D. and WOOD, P.J. Aquatic macroinvertebrate biodiversity associated with artificial agricultural drainage ditches. Hydrobiologia, 2016, 776(1), 249-260. http://dx.doi.org/10.1007/s10750-016-2757-z.

HILLEBRAND, H., DÜRSELEN, C., KIRSCHTEL, D., POLLINGHER, U. and ZOHARY, T. Biovolume calculation for pelagic and benthic microalgae. Journal of Phycology, 1999, 35(2), 403-424. http://dx.doi.org/10.1046/j.1529-8817.1999.3520403.x.

HONG, Y., BURFORD, M.A., RALPH, P.J., UDY, J.W. and DOBLIN, M.A. The cyanobacterium Cylindrospermopsis raciborskii is facilitated by copepod selective grazing. Harmful Algae, 2013, 29, 14-21. http://dx.doi.org/10.1016/j.hal.2013.07.003.

HOPP, U., MAIER, G. and BLEHER, R. Reproduction and adult longevity of five species of planktonic cyclopoid copepods reared on different diets: a comparative study. Freshwater Biology, 1997, 38(2), 289-300. http://dx.doi.org/10.1046/j.1365-2427.1997.00214.x.

IGLESIAS, C., MAZZEO, N., GOYENOLA, G., FOSALBA, C., DE MELLO, F., GARCIA, S. and JEPPESEN, E. Field and experimental evidence of the effect of Jenynsia multidentata, a small omnivorous-planktivorous fish, on the size distribution of zooplankton in subtropical lakes. Freshwater Biology, 2008, 53(9), 1797-1807. http://dx.doi.org/10.1111/j.1365-2427.2008.02007.x.

JAMES, M.R. and FORSYTH, D.J. Zooplankton-phytoplankton interactions in a eutrophic lake. Journal of Plankton Research, 1990, 12(3), 455-472. http://dx.doi.org/10.1093/plankt/12.3.455.

JEPPESEN, E., NÕGES, P., DAVIDSON, T.A., HABERMAN, J., NÕGES, T., BLANK, K., LAURIDSEN, T.L., SØNDERGAARD, M., SAYER, C., LAUGASTE, R., JOHANSSON, L.S., BJERRING, R. and AMSINCK, S.L. Zooplankton as indicators in lakes: a scientific-based plea for including zooplankton in the ecological quality assessment of lakes according to the European Water Framework Directive (WFD). Hydrobiologia, 2011, 676(1), 279-297. http://dx.doi.org/10.1007/s10750-011-0831-0.

JEPPESEN, E., PEDER JENSEN, J., SØNDERGAARD, M., LAURIDSEN, T. and LANDKILDEHUS, F. Trophic structure, species richness and biodiversity in Danish lakes: Changes along a phosphorus gradient. Freshwater Biology, 2000, 45(2), 201-218. http://dx.doi.org/10.1046/j.1365-2427.2000.00675.x.

KÂ, S., MENDOZA-VERA, J.M., BOUVY, M., CHAMPALBERT, G., N’GOM-KÂ, R. and PAGANO, M. Can tropical freshwater zooplankton graze efficiently on cyanobacteria? Hydrobiologia, 2012, 679(1), 119-138. http://dx.doi.org/10.1007/s10750-011-0860-8.

KANDATHIL RADHAKRISHNAN, D., AKBARALI, I., THUNDIPARAMBIL SATHRAJITH, A., SCHMIDT, B.V., SIVANPILLAI, S. and THAZHAKOT VASUNAMBESAN, S. Grazing rates of freshwater copepod Thermocyclops decipiens (Kiefer, 1929) on Chlorella vulgaris under different light intensities. Aquaculture (Amsterdam, Netherlands), 2020, 525, 735321. http://dx.doi.org/10.1016/j.aquaculture.2020.735321.

LAMPERT, W. Laboratory studies on zooplankton‐cyanobacteria interactions. New Zealand Journal of Marine and Freshwater Research, 1987, 21(3), 483-490. http://dx.doi.org/10.1080/00288330.1987.9516244.

LEITÃO, E., GER, K.A. and PANOSSO, R. Selective grazing by a tropical copepod (Notodiaptomus iheringi) facilitates Microcystis dominance. Frontiers in Microbiology, 2018, 9, 301. http://dx.doi.org/10.3389/fmicb.2018.00301. PMid:29527199.

LEITÃO, E., PANOSSO, R., MOLICA, R. and GER, K.A. Top‐down regulation of filamentous cyanobacteria varies among a raptorial versus current feeding copepod across multiple prey generations. Freshwater Biology, 2020, 66(1), 142-156. http://dx.doi.org/10.1111/fwb.13625.

LI, Y., MENG, J., ZHANG, C., JI, S., KONG, Q., WANG, R. and LIU, J. Bottom-up and top-down effects on phytoplankton communities in two freshwater lakes. PLoS One, 2020, 15(4), e0231357. http://dx.doi.org/10.1371/journal.pone.0231357. PMid:32271852.

LIRA, G.A.S.T., MOURA, A.N., VILAR, M.C.P., CORDEIRO-ARAÚJO, M.K. and BITTENCOURT-OLIVEIRA, M.C. Vertical and temporal variation in phytoplankton assemblages correlated with environmental conditions in the Mundaú reservoir, semi-arid northeastern Brazil. Brazilian Journal of Biology = Revista Brasileira de Biologia, 2014, 74(3, Suppl 1), S093-S102. http://dx.doi.org/10.1590/1519-6984.27612. PMid:25627370.

LOBO, E. and LEIGHTON, G. Estructuras comunitarias de las fitocenosis planctónicas de los sistemas de desembocaduras de rios y esteros de la zona central. Revista de Biología Marina y Oceanografía, 1986, 22(1), 1-29.

LÜRLING, M. and VAN DONK, E. Grazer-induced colony formation in Scenedesmus: are there costs to being colonial? Oikos, 2000, 88(1), 111-118. http://dx.doi.org/10.1034/j.1600-0706.2000.880113.x.

LÜRLING, M. Phenotypic plasticity in the green algae Desmodesmus and Scenedesmus with special reference to the induction of defensive morphology. Annales de Limnologie-International Journal of Limnology, 2003, 39(2), 85-101. http://dx.doi.org/10.1051/limn/2003014.

MELO JÚNIOR, M.D., ALMEIDA, V.L.S., PARANAGUÁ, M.N. and MOURA, A.N. Crustáceos planctônicos de um reservatório oligotrófico do Nordeste do Brasil. Revista Brasileira de Zoociências, 2007, 9(1), 19-30.

MITRA, F. and FLYNN, K.J. Promotion of harmful algal blooms by zooplankton predatory activity. Biology Letters, 2006, 2(2), 194-197. http://dx.doi.org/10.1098/rsbl.2006.0447. PMid:17148360.

MOURA, A.N., BITTENCOURT-OLIVEIRA, M.C., DANTAS, Ê.W. and ARRUDA NETO, J.D.D.T. Phytoplanktonic associations: a tool to understanding dominance events in a tropical Brazilian reservoir. Acta Botanica Brasílica, 2007, 21(3), 641-648. http://dx.doi.org/10.1590/S0102-33062007000300011.

MÜLLER-NAVARRA, D.C., BRETT, M.T., LISTON, A.M. and GOLDMAN, C.R. A highly unsaturated fatty acid predicts carbon transfer between primary producers and consumers. Nature, 2000, 403(6765), 74-77. http://dx.doi.org/10.1038/47469. PMid:10638754.

NEUMANN-LEITÃO, S., NOGUEIRA-PARANHOS, J.D. and SOUZA, F.B.V.A. Zooplâncton do açude de Apipucos, Recife - PE (Brasil). Arquivos de Biologia e Tecnologia, 1989, 32(4), 803-821.

OLIVEIRA, F.H., ARA, A.L., MOREIRA, C.H., LIRA, O.O., PADILHA, M.R. and SHINOHARA, N.K. Seasonal changes of water quality in a tropical shallow and eutrophic reservoir in the metropolitan region of Recife (Pernambuco-Brazil). Anais da Academia Brasileira de Ciências, 2014, 86(4), 1863-1872. http://dx.doi.org/10.1590/0001-3765201420140128. PMid:25590722.

PAERL, H.W., FULTON, R.S. 3rd., MOISANDER, P.H. and DYBLE, J. Harmful Freshwater Algal Blooms, with an emphasis on Cyanobacteria. TheScientificWorldJournal, 2001, 1, 76-113. http://dx.doi.org/10.1100/tsw.2001.16. PMid:12805693.

PAGANO, M. Feeding of tropical cladocerans (Moina micrura, Diaphanosoma excisum) and rotifer (Brachionus calyciflorus) on natural phytoplankton: effect of phytoplankton size–structure. Journal of Plankton Research, 2008, 30(4), 401-414. http://dx.doi.org/10.1093/plankt/fbn014.

PEREIRA, S.M.B. and NASCIMENTO, P.R.F. Macrófitas Aquáticas. In: K. BURGOS and E. ARANTES, eds. Açude de Apipucos: história e ecologia. Recife: Companhia Editora de Pernambuco, 2009, pp.1-176.

PIELOU, E.C. The measurement of diversity in different types of biological collections. Journal of Theoretical Biology, 1966, 13, 131-144. http://dx.doi.org/10.1016/0022-5193(66)90013-0.

PINTO-COELHO, R.M. Métodos de coleta, preservação, contagem e determinação de biomassa em zooplâncton de águas epicontinentais. In: C.E.M. BICUDO and D.C. BICUDO, eds. Amostragem em limnologia. São Carlos: RiMa, 2004, pp. 149-166.

PINTO-COELHO, R.M., BEZERRA-NETO, J.F. and MORAIS-JR, C.A. Effects of eutrophication on size and biomass of crustacean zooplankton in a tropical reservoir. Brazilian Journal of Biology = Revista Brasileira de Biologia, 2005, 65(2), 325-338. http://dx.doi.org/10.1590/S1519-69842005000200017. PMid:16097736.

R CORE TEAM. R: A Language and Environment for Statistical Computing [online]. Vienna, Austria: R Foundation for Statistical Computing, 2016. [viewed 27 Nov. 2019]. Available from: http://www.R-project.org/

REYNOLDS, C.S. Ecology of phytoplankton. Cambridge: Cambridge University Press, 2006. http://dx.doi.org/10.1017/CBO9780511542145.

RUTTNER-KOLISKO, A. Suggestions for biomass calculation of planktonic rotifers. Archiv für Hydrobiologie, 1977, 8, 71-77.

SANTER, B. and VAN DEN BOSCH, F. Herbivorous nutrition of Cyclops vicinus: the effect of a pure algal diet on feeding, development, reproduction and life cycle. Journal of Plankton Research, 1994, 16(2), 171-195. http://dx.doi.org/10.1093/plankt/16.2.171.

SCASSO, F., MAZZEO, N., GORGA, J., KRUK, C., LACEROT, G., CLEMENTE, J., FABIÁN, D. and BONILLA, S. Limnological changes in a sub-tropical shallow hypertrophic lake during its restoration two years of a whole-lake experiment. Aquatic Conservation, 2001, 11(1), 31-44. http://dx.doi.org/10.1002/aqc.420.

SECRETARIA DOS RECURSOS HÍDRICOS – SRH. Plano Estadual de Recursos Hídricos do Estado de Pernambuco - Documento Síntese [online]. Recife: SRH, 2000. [viewed 27 Nov. 2019]. Available from: https://www.srh.ce.gov.br/

SHANNON, C.E. A mathematical theory of communication. The Bell System Technical Journal, 1948, 27(3), 379-423. http://dx.doi.org/10.1002/j.1538-7305.1948.tb01338.x.

SILVA, V.L., FIGUEIREDO, A.C. and CORRÊA, M.M. Qualidade da água do Açude de Apipucos. In: K. BURGOS and E. ARANTES, eds. Açude de Apipucos: história e ecologia. Recife: CEPE, 2009, pp. 77-84.

SILVEIRA, R.M.L., PAIVA, L.L.A.R. and CAMARGO, J.C. Top-down control in a tropical shallow lake of Northern Pantanal, Brazil. Acta Limnologica Brasiliensia, 2010, 22(4), 455-465. http://dx.doi.org/10.4322/actalb.2011.009.

SIPAÚBA-TAVARES, L.H., BACHION, M.A. and ROCHA, O. Estudo do crescimento populacional de três espécies zooplanctônicas em laboratório e o uso de plâncton na alimentação de alevinos de Oreochromis niloticus (tilápia) e Astyanax scabripinus paranae (lambari). Revista Unimar, 1994, 16(3), 189-201.

SOARES, M.C.S., LÜRLING, M. and HUSZAR, V.L.M. Responses of the rotifer Brachionus calyciflorus to two tropical toxic cyanobacteria (Cylindrospermopsis raciborskii and Microcystis aeruginosa) in pure and mixed diets with green algae. Journal of Plankton Research, 2010, 32(7), 999-1008. http://dx.doi.org/10.1093/plankt/fbq042.

SOTO, D. and HURLBERT, S.H. Long-term experiments on calanoid–cyclopoid interactions. Ecological Monographs, 1991, 61(3), 245-265. http://dx.doi.org/10.2307/2937108.

STARKWEATHER, P.L. and KELLAR, P.E. Utilization of cyanobacteria by Brachionus calyciflorus: Anabaena flos-aquae (NRC-44-1) as a sole or complementary food source. Hydrobiologia, 1983, 104(1), 373-377. http://dx.doi.org/10.1007/BF00045994.

STOECKER, D. and PIERSON, J. Predation on protozoa: its importance to zooplankton revisited. Journal of Plankton Research, 2019, 41(4), 367-373. http://dx.doi.org/10.1093/plankt/fbz027.

TÕNNO, I., AGASILD, H., KÕIV, T., FREIBERG, R., NÕGES, P. and NÕGES, T. Algal diet of small-bodied crustacean zooplankton in a cyanobacteria-dominated eutrophic lake. PLoS One, 2016, 11(4), e0154526. http://dx.doi.org/10.1371/journal.pone.0154526. PMid:27124652.

URRUTIA‐CORDERO, P., EKVALL, M.K. and HANSSON, L. Responses of cyanobacteria to herbivorous zooplankton across predator regimes: who mows the bloom? Freshwater Biology, 2015, 60(5), 960-972. http://dx.doi.org/10.1111/fwb.12555.

UTERMÖHL, H. Zur vervollkommnung der quantitativen phytoplankton-methodik: Mit 1 Tabelle und 15 abbildungen im Text und auf 1 Tafel. Internationale Vereinigung für theoretische und angewandte Limnologie Mitteilungen, 1958, 9(1), 1-38.

VON RÜCKERT, G. and GIANI, A. Biological interactions in the plankton community of a tropical eutrophic reservoir: is the phytoplankton controlled by zooplankton? Journal of Plankton Research, 2008, 30(10), 1157-1168. http://dx.doi.org/10.1093/plankt/fbn065.

WANG, C., HUANG, Y., HE, S., LIN, Y., WANG, X. and KONG, H. Variation of phytoplankton community before an induced cyanobacterial (Arthrospira platensis) bloom. Journal of Environmental Sciences (China), 2009, 21(12), 1632-1638. http://dx.doi.org/10.1016/S1001-0742(08)62466-3. PMid:20131591.

WANG, X.D., QIN, B.Q., GAO, G. and PAERL, H.W. Nutrient enrichment and selective predation by zooplankton promote Microcystis (Cyanobacteria) bloom formation. Journal of Plankton Research, 2010, 32(4), 457-470. http://dx.doi.org/10.1093/plankt/fbp143.

WILSON, A.E., SARNELLE, O. and TILLMANNS, A.R. Effects of cyanobacterial toxicity and morphology on the population growth of freshwater zooplankton: Meta-analyses of laboratory experiments. Limnology and Oceanography, 2006, 51(4), 1915-1924. http://dx.doi.org/10.4319/lo.2006.51.4.1915.

YANG, Z., KONG, F., SHI, X. and CAO, H. Morphological response of Microcystis aeruginosa to grazing by different sorts of zooplankton. Hydrobiologia, 2006, 563(1), 225-230. http://dx.doi.org/10.1007/s10750-005-0008-9.

ZHANG, J., XIE, P., TAO, M., GUO, L., CHEN, J., LI, L., ZHANG, X.Z. and ZHANG, L. The impact of fish predation and cyanobacteria on zooplankton size structure in 96 subtropical lakes. PLoS One, 2013, 8(10), e76378. http://dx.doi.org/10.1371/journal.pone.0076378. PMid:24124552.

ZHANG, L., WANG, Z., WANG, N., GU, L., SUN, Y., HUANG, Y., CHEN, Y. and YANG, Z. Mixotrophic Ochromonas addition improves the harmful Microcystis-dominated phytoplankton community in in situ microcosms. Environmental Science & Technology, 2020, 54(7), 4609-4620. http://dx.doi.org/10.1021/acs.est.9b06438. PMid:32126758.
 


Submitted date:
11/27/2019

Accepted date:
05/27/2021

Publication date:
06/23/2021

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