Seasonal variation of Microcystis aeruginosa and factors related to blooms in a deep warm monomictic lake in Mexico

https://doi.org/10.4081/jlimnol.2021.2013

Authors

Abstract

The occurrence of cyanobacterial blooms has increased globally over the last decades, with the combined effect of climate change and eutrophication as its main drivers. The seasonal dynamic of cyanobacterial blooms is a well-known phenomenon in lakes and reservoirs in temperate zones. Nevertheless, in the tropics, most studies have been performed in shallow and artificial lakes; therefore, the seasonal dynamic of cyanobacterial blooms in deep and eutrophic tropical lakes is still under research. We studied the seasonal variation of the phytoplankton community and the factors associated with Microcystis aeruginosa blooms along the water column of Lake Alberca de Tacámbaro, a warm monomictic crater lake located in Mexico, during 2018 and 2019. According to previous studies performed in 2006 and 2010, this lake was mesotrophic-eutrophic, with Chlorophyta and Bacillariophyta as the dominant groups of the phytoplankton community. During 2018 and 2019, the lake was eutrophic and occasionally, hypertrophic, a phenomenon likely associated with the increase of farmland area around the lake. The dominant species was M. aeruginosa, forming blooms from the surface to 10 m depth in winter, in the hypolimnion in spring and summer, and along the full water column in autumn. These findings suggest that M. aeruginosa in Lake Alberca de Tacámbaro displays seasonal and spatial population dynamics. Total phosphorus, dissolved inorganic nitrogen, water temperature and photosynthetically active radiation were the environmental factors related to M. aeruginosa blooms. Our results suggest that the changes in the structure of the phytoplankton community through time, and M. aeruginosa blooms in Lake Alberca de Tacámbaro, are mainly related to changes in land use from forest to farmland in areas adjacent to the lake, which promoted its eutrophication in the last years through runoffs. Comparative studies with other deep and eutrophic lakes will allow us to gain a deeper understanding of the dynamic of cyanobacterial blooms in natural and artificial water reservoirs strongly stressed by human activities.

Dimensions

Altmetric

PlumX Metrics

Downloads

Download data is not yet available.

References

Alcántara I, Piccini C, Segura AM, Deus S, González C, Martínez de la Escalera G, Kruk C, 2018. Improved biovolume estimation of Microcystis aeruginosa colonies: A statistical approach. J. Microbiol. Methods 151:20–27. DOI: https://doi.org/10.1016/j.mimet.2018.05.021

Alcocer J, Kato E, Robles E, Vilaclara G, 1998. Estudio preliminar del efecto del dragado sobre el estado trófico del lago viejo de Chapultepec. Rev. Int. Contam. Ambient. 4:43-56.

Almanza V, Pedreros P, Dail Laughinghouse H, Félez J, Parra O, Azócar M, Urrutia R, 2019. Association between trophic state, watershed use, and blooms of cyanobacteria in south-central Chile. Limnologica 75:30–41.

Arzate-Cárdenas MA, Olvera-Ramírez R, Martínez-Jerónimo F, 2010. Microcystis toxigenic strains in urban lakes: a case of study in Mexico City. Ecotoxicology 19:1157–1165.

APHA, 1998. Standard Methods for the Examination of Water and Wastewater. 20th Edition. American Public Health Association, Washington, D.C.

Beversdorf LJ, Miller TR, McMahon KD, 2013. The role of nitrogen fixation in cyanobacterial bloom toxicity in a temperate, eutrophic lake. PLoS One 8:e56103.

Boström B, Pettersson AK, Ahlgren I, 1989. Seasonal dynamics of a cyanobacteria-dominated microbial community in surface sediments of a shallow, eutrophic lake. Aquat. Sci. 51:153–178.

Bourrelly P, 1968. Les Algues d’eau douce : initiation à la systématique. Tome II, p Les Algues jaunes et brunes. Chrysophycées, Phéophycées, Xanthophycées et Diatomées. Editions N. Boubée & Cie, Paris.

Brunberg A-K, Blomqvist P, 2003. Recruitment of Microcystis (Cyanophyceae) from lake sediments: the importance of littoral inocula. J. Phycol. 39:58–63.

Caballero M, Vázquez G, 2020. Mixing patterns and deep chlorophyll a maxima in an eutrophic tropical lake in western Mexico. Hydrobiologia 847:4161–4176.

Caballero M, Vázquez G, Ortega B, Favila ME, Lozano-García S, 2016. Responses to a warming trend and “El Niño” events in a tropical lake in western Mexico. Aquat. Sci. 78:591–604.

Carey CC, Ibelings BW, Hoffmann EP, Hamilton DP, Brookes JD, 2012. Eco-physiological adaptations that favour freshwater cyanobacteria in a changing climate. Water Res. 46:1394–1407.

Carlson RE, 1977. A trophic state index for lakes. Limnol. Oceanogr. 22:361–369.

Carlson RE, 2007. Estimating trophic state. LakeLine 27:25–28.

Chalar G, 2009. The use of phytoplankton patterns of diversity for algal bloom management. Limnologica 39:200–208. DOI: https://doi.org/10.1016/j.limno.2008.04.001

Chao A, Chiu C-H, Jost L, 2014. Unifying species diversity, phylogenetic diversity, functional diversity, and related similarity and differentiation measures through Hill numbers. Annu. Rev. Ecol. Evol. Syst. 45:297–324. DOI: https://doi.org/10.1146/annurev-ecolsys-120213-091540

Chen X, Huang Y, Chen G, Li P, Shen Y, Davis TW, 2018. The secretion of organics by living Microcystis under the dark/anoxic conditions and its enhancing effect on nitrate removal. Chemosphere 196:280–287. DOI: https://doi.org/10.1016/j.chemosphere.2017.12.197

Chien YC, Wu SC, Chen WC, Chou CC, 2013. Model simulation of diurnal vertical migration patterns of different-sized colonies of Microcystis employing a particle trajectory approach. Environ. Eng. Sci. 30:179–186. DOI: https://doi.org/10.1089/ees.2012.0318

Chorus I, Bartram J, 1999. Toxic Cyanobacteria in Water: A Guide to Their Public Health Consequences, Monitoring and Management. St Edmundsbury Press, Bury St Edmunds: 203 pp. DOI: https://doi.org/10.1201/9781482295061

Davis T, Harke M, Marcoval M, Goleski J, Orano-Dawson C, Berry D, Gobler CJ, 2010. Effects of nitrogenous compounds and phosphorus on the growth of toxic and non-toxic strains of Microcystis during cyanobacterial blooms. Aquat. Microb. Ecol. 61:149–162. DOI: https://doi.org/10.3354/ame01445

Davis TW, Berry DL, Boyer GL, Gobler CJ, 2009. The effects of temperature and nutrients on the growth and dynamics of toxic and non-toxic strains of Microcystis during cyanobacteria blooms. Harmful Algae 8:715–725. DOI: https://doi.org/10.1016/j.hal.2009.02.004

Deng J, Qin B, Paerl HW, Zhang Y, Ma J, Chen Y, 2014. Earlier and warmer springs increase cyanobacterial (Microcystis spp.) blooms in subtropical Lake Taihu, China. Freshw. Biol. 59:1076–1085. DOI: https://doi.org/10.1111/fwb.12330

Dı́az-Pardo E, Vazquez G, López-López E, 1998. The phytoplankton community as a bioindicator of health conditions of Atezca Lake, Mexico. Aquat. Ecosyst. Heal. Manag. 1:257–266. DOI: https://doi.org/10.1080/14634989808656922

Dokulil MT, Teubner K, 2000. Cyanobacterial dominance in lakes. Hydrobiologia 438:1–12. DOI: https://doi.org/10.1023/A:1004155810302

Dunn PK, Smyth GK, 2018. Chapter 11: Positive continuous data: gamma and inverse gaussian GLMs, p. 425-456. In: P.K. Dunn and G.K. Smyth (eds.), Generalized linear models with examples in R. Springer New York. DOI: https://doi.org/10.1007/978-1-4419-0118-7_11

Edwin W, Kardinaal A, Visser PM, 2005. Dynamics of Cyanobacterial Toxins, p. 41-63. In: Huisman J, HCP Matthijs, and PM Visser (eds.), Harmful cyanobacteria. Springer Netherlands. DOI: https://doi.org/10.1007/1-4020-3022-3_3

Feinsinger P, 2001. Designing Field Studies for Biodiversity Conservation. Island Press, Washington, D.C: 138 pp.

Fernández C, Parodi ER, Cáceres EJ, 2012. Phytoplankton structure and diversity in the eutrophic-hypereutrophic reservoir Paso de las Piedras, Argentina. Limnology 13:13–25. DOI: https://doi.org/10.1007/s10201-011-0347-3

Figueiredo DR de, Reboleira ASSP, Antunes SC, Abrantes N, Azeiteiro U, Gonçalves F, Pereira MJ, 2006. The effect of environmental parameters and cyanobacterial blooms on phytoplankton dynamics of a Portuguese temperate Lake. Hydrobiologia 568:145–157. DOI: https://doi.org/10.1007/s10750-006-0196-y

Filstrup CT, Hillebrand H, Heathcote AJ, Harpole WS, Downing JA, 2014. Cyanobacteria dominance influences resource use efficiency and community turnover in phytoplankton and zooplankton communities. Ecol. Lett. 17:464–474. DOI: https://doi.org/10.1111/ele.12246

Frias HV, Mendes MA, Cardozo KHM, Carvalho VM, Tomazela D, Colepicolo P, Pinto E, 2006. Use of electrospray tandem mass spectrometry for identification of microcystins during a cyanobacterial bloom event. Biochem. Biophys. Res. Commun. 344:741–746. DOI: https://doi.org/10.1016/j.bbrc.2006.03.199

Gkelis S, Papadimitriou T, Zaoutsos N, Leonardos I, 2014. Anthropogenic and climate-induced change favors toxic cyanobacteria blooms: Evidence from monitoring a highly eutrophic, urban Mediterranean lake. Harmful Algae 39:322–333. DOI: https://doi.org/10.1016/j.hal.2014.09.002

Global Water Research Coalition, Water Quality Research Australia, 2009. International Guidance Manual for the Management of Toxic Cyanobacteria. Available from https://www.waterra.com.au/cyanobacteria-manual/PDF/GWRCGuidanceManualLevel1.pdf

Gobler CJ, Burkholder JM, Davis TW, Harke MJ, Johengen T, Stow CA, Waal DB Van de, 2016. The dual role of nitrogen supply in controlling the growth and toxicity of cyanobacterial blooms. Harmful Algae 54:87–97. DOI: https://doi.org/10.1016/j.hal.2016.01.010

Haande S, Ballot A, Rohrlack T, Fastner J, Wiedner C, Edvardsen B, 2007. Diversity of Microcystis aeruginosa isolates (Chroococcales, Cyanobacteria) from East-African water bodies. Arch. Microbiol. 188:15–25. DOI: https://doi.org/10.1007/s00203-007-0219-8

Hernández-Morales R, Ortega MR, Sánchez JD, Alvarado R, Aguilera MS, 2011. Distribución estacional del fitoplancton en un lago cálido monomíctico en Michoacán, México. Biológicas 13:21–28.

Hillebrand H, Dürselen C-D, Kirschtel D, Pollingher U, Zohary T, 1999. Biovolume calculation for pelagic and benthic microalgae. J. Phycol. 35:403–424. DOI: https://doi.org/10.1046/j.1529-8817.1999.3520403.x

Hsieh TC, Ma KH, Chao A, 2016. iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods Ecol. Evol. 7:1451–1456. DOI: https://doi.org/10.1111/2041-210X.12613

Huisman J, Sharples J, Stroom JM, Visser PM, Kardinaal WEA, Verspagen JMH, Sommeijer B, 2004. Changes in turbulent mixing shift competition for light between phytoplankton species. Ecology 85:2960–2970. DOI: https://doi.org/10.1890/03-0763

Huisman J, Codd GA, Paerl HW, Ibelings BW, Verspagen JMH, Visser PM, 2018. Cyanobacterial blooms. Nat. Rev. Microbiol. 16:471–483.

Hunter PD, Tyler AN, Willby NJ, Gilvear DJ, 2008. The spatial dynamics of vertical migration by Microcystis aeruginosa in a eutrophic shallow lake: a case study using high spatial resolution time-series airborne remote sensing. Limnol. Oceanogr. 53:2391–2406.

Ibelings BW, Vonk M, Los HFJ, Molen DT van der, Mooij WM, 2003. Fuzzy modeling of cyanobacterial surface waterblooms: validation with NOAA-AVHRR satellite images. Ecol. Appl. 13:1456–1472.

Instituto Nacional de Estadística y Geografía, 2016. Conjunto de datos vectoriales de uso del suelo y vegetación. Available from: https://www.inegi.org.mx/app/biblioteca/ficha.html?upc=889463173359

Jacoby JM, Collier DC, Welch EB, Hardy FJ, Crayton M, 2000. Environmental factors associated with a toxic bloom of Microcystis aeruginosa. Can. J. Fish. Aquat. Sci. 57:231–240.

Jöhnk KD, Huisman JEF, Sharples J, Sommeijer BEN, Visser PM, Stroom JM, 2008. Summer heatwaves promote blooms of harmful cyanobacteria. Glob. Chang. Biol. 14:495–512.

Jost L, 2007. Partitioning diversity into independent alpha and beta components. Ecology 88:2427–2439.

Jost L, DeVries P, Walla T, Greeney H, Chao A, Ricotta C, 2010. Partitioning diversity for conservation analyses. Divers. Distrib. 16:65–76. DOI: https://doi.org/10.1111/j.1472-4642.2009.00626.x

Kalff J, 2002. Limnology: Inland Water Ecosystems. Prentice Hall, New Jersey: 148 pp.

Komárek J, 2008. Cyanoprokaryota. Teil 1 / Part 1: Chroococcales. Springer Spektrum.

Komárek J, Anagnostidis K, 2007. Süßwasserflora von Mitteleuropa, Bd. 19/2: Cyanoprokaryota. Bd. 2 / Part 2: Oscillatoriales. Springer Spektrum.

Kosten S, Huszar VLM, Bécares E, Costa LS, Donk E van, Hansson L-A, Jeppesen E, Kruk C, Lacerot G, Mazzeo N, Meester L De, Moss B, et al., 2012. Warmer climates boost cyanobacterial dominance in shallow lakes. Glob. Chang. Biol. 18:118–126.

Krammer K, Lange-Bertalot H, 1997. Süßwasserflora von Mitteleuropa, Bd. 02/2: Bacillariophyceae. Teil 2: Bacillariaceae, Epithemiaceae, Surirellaceae. Springer Spektrum.

Krammer K, Lange-Bertalot H, 1999. Süßwasserflora von Mitteleuropa, Bd. 02/1: Bacillariophyceae, 1. Teil: Naviculaceae, A: Text; B: Tafeln. Springer Spektrum.

Krammer K, Lange-Bertalot H, 2000. Bacillariophyceae. Teil 3: Centrales, Fragilariaceae, Eunotiaceae. Springer Spektrum.

Latour D, Sabido O, Salencon MJ, Giraudet H, 2004. Dynamics and metabolic activity of the benthic cyanobacterium Microcystis aeruginosa in the Grangent reservoir (France). J. Plankton Res. 27:716–726.

Lee RE, 2008. Cyanobacteria, p. 33-80. In: R.E. Lee (ed.), Phycology. Cambridge University Press.

Li J, Wang Z, Cao X, Wang Z, Zheng Z, 2015. Effect of orthophosphate and bioavailability of dissolved organic phosphorous compounds to typically harmful cyanobacterium Microcystis aeruginosa. Mar. Pollut. Bull. 92:52–58.

López-Archilla AI, Moreira D, López-García P, Guerrero C, 2004. Phytoplankton diversity and cyanobacterial dominance in a hypereutrophic shallow lake with biologically produced alkaline pH. Extremophiles 8:109–115.

Lund JWG, Kipling C, Cren ED Le, 1958. The inverted microscope method of estimating algal numbers and the statistical basis of estimations by counting. Hydrobiologia 11:143–170.

Marinho MM, Oliveira e Azevedo SMF de, 2007. Influence of N/P ratio on competitive abilities for nitrogen and phosphorus by Microcystis aeruginosa and Aulacoseira distans. Aquat. Ecol. 41:525–533.

McCune B, Grace JB, 2002. Analysis of ecological communities. Gleneden Beach (OR): MjM Software Design.

Meeks JC, 1974. Chlorophylls, p. 161 - 175. In: W.D.P. Stewart (ed.), Algal physiology and biochemistry. Blackwell Scientific Publications.

Moestrup Ø, Calado A, 2018. Süßwasserflora von Mitteleuropa, Bd. 6 - Freshwater Flora of Central Europe, Vol. 6: Dinophyceae. Springer Spektrum.

Mowe MAD, Mitrovic SM, Lim RP, Furey A, Yeo DCJ, 2014. Tropical cyanobacterial blooms: a review of prevalence, problem taxa, toxins and influencing environmental factors. J. Limnol. 74:205-224.

Newcombe G, House J, Ho L, Baker P, Burch M, 2010. Management strategies for cyanobacteria (blue-green algae): a guide for water utilities. Research report 74. Water Quality Research Australia (WQRA). Available from https://www.waterra.com.au/publications/document-search/?download=106

Ninio S, Lupu A, Viner-Mozzini Y, Zohary T, Sukenik A, 2020. Multiannual variations in Microcystis bloom episodes – Temperature drives shift in species composition. Harmful Algae 92:101710.

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: https://doi.org/10.1016/j.hal.2011.10.027

Oliver RL, Ganf GG, 2002. Freshwater Blooms, p. 149-194. In: B.A. Whitton and M. Potts (eds.), The ecology of cyanobacteria: their diversity in space and time. Springer Netherlands. DOI: https://doi.org/10.1007/0-306-46855-7_6

Padedda BM, Sechi N, Lai GG, Mariani MA, Pulina S, Sarria M, Satta CT, Virdis T, Buscarinu P, Lugliè A, 2017. Consequences of eutrophication in the management of water resources in Mediterranean reservoirs: A case study of Lake Cedrino (Sardinia, Italy). Glob. Ecol. Conserv. 12:21–35. DOI: https://doi.org/10.1016/j.gecco.2017.08.004

Paerl H, 2008. Nutrient and other environmental controls of harmful cyanobacterial blooms along the freshwater–marine continuum, p. 217-237. In: H.K. Hudnell (ed.), Cyanobacterial harmful algal blooms: state of the science and research needs. Springer New York. DOI: https://doi.org/10.1007/978-0-387-75865-7_10

Paerl HW, Fulton RS, Moisander PH, Dyble J, 2001. Harmful freshwater algal blooms, with an emphasis on cyanobacteria. Sci. World J. 1:139109. DOI: https://doi.org/10.1100/tsw.2001.16

Paerl HW, Paul VJ, 2012. Climate change: Links to global expansion of harmful cyanobacteria. Water Res. 46:1349–1363. DOI: https://doi.org/10.1016/j.watres.2011.08.002

Pineda-Mendoza RM, Olvera-Ramírez R, Martínez-Jerónimo F, 2012. Microcystins produced by filamentous cianobacteria in urban lakes. A case study in Mexico City. Hidrobiológica 22:290-298.

Planas D, Paquet S, 2016. Importance of climate change-physical forcing on the increase of cyanobacterial blooms in a small, stratified lake. J. Limnol. 75:201-2014. DOI: https://doi.org/10.4081/jlimnol.2016.1371

Preston T, Stewart W, Reynolds C, 1980. Bloom-forming cyanobaterium Microcystis aeruginosa overwinters on sediment surface. Nature 288:365–367. DOI: https://doi.org/10.1038/288365a0

Puddick J, Prinsep MR, Wood SA, Cary SC, Hamilton DP, Holland PT, 2015. Further characterization of glycine-containing microcystins from the McMurdo dry Valleys of Antarctica. Toxins 7:493-515. DOI: https://doi.org/10.3390/toxins7020493

Qin B, Yang G, Ma J, Wu T, Li W, Liu L, Deng J, Zhou J, 2018. Spatiotemporal changes of cyanobacterial bloom in large shallow eutrophic Lake Taihu, China. Front. Microbiol. 9:451. DOI: https://doi.org/10.3389/fmicb.2018.00451

R Core Team, 2019. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from: http://www.R-project.org

Ramírez García P, Nandini S, Sarma SSS, Robles Valderrama E, Cuesta I, Hurtado MD, 2002. Seasonal variations of zooplankton abundance in the freshwater reservoir Valle de Bravo (Mexico). Hydrobiologia 467:99–108. DOI: https://doi.org/10.1007/978-94-010-0415-2_8

Reynolds CS, 1971. The ecology of the planktonic blue-green algae in the North Shropshire meres. Fld. Stud. 3:409–432.

Reynolds CS, Walsby AE, 1975. Water blooms. Biol. Rev. 50:437–481. DOI: https://doi.org/10.1111/j.1469-185X.1975.tb01060.x

Reynolds CS, 1987. Cyanobacterial Water-Blooms. Adv. Bot. Res. 13:67-143.

Reynolds CS, 1999. Non-determinism to Probability, or N : P in the community ecology of phytoplankton. Arch. für Hydrobiol. 146:23–35.

Reynolds CS, Jaworski GHM, Cmiech HA, Leedale GF, Lund JWG, 1981. On the annual cycle of the blue-green alga Microcystis Aeruginosa Kütz. Emend. Elenkin. Philos. Trans. R. Soc. London. B, Biol. Sci. 293:419–477.

Richardson J, Feuchtmayr H, Miller C, Hunter PD, Maberly SC, Carvalho L, 2019. Response of cyanobacteria and phytoplankton abundance to warming, extreme rainfall events and nutrient enrichment. Glob. Chang. Biol. 25:3365–3380.

Šejnohová L, Maršálek B, 2012. Microcystis, p. 195-228. In: B.A. Whitton (ed.), Ecology of cyanobacteria II: their diversity in space and time. Springer Netherlands.

Servicio Nacional Mateorológico (SNM), 2020. Información estadística climatológica. Available from: https://smn.conagua.gob.mx/es/climatologia/informacion-climatologica/informacion-estadistica-climatologica

Shi XL, Kong FX, Yu Y, Yang Z, 2007. Survival of Microcystis aeruginosa and Scenedesmus obliquus under dark anaerobic conditions. Mar. Freshwater Res. 58:634–639.

Smayda TJ, 1997. What is a bloom? A commentary. Limnol. Oceanogr. 42:1132–1136.

Smith VH, 1983. Low nitrogen to phosphorus ratios favor dominance by blue-green algae in lake phytoplankton. Science 221:669–671.

Smith VH, 2003. Eutrophication of freshwater and coastal marine ecosystems a global problem. Environ. Sci. Pollut. Res. 10:126–139.

Soares M, de A Rocha MI, Marinho MM, Azevedo SMFO, Branco CWC, Huszar MVL, 2009. Changes in species composition during annual cyanobacterial dominance in a tropical reservoir: physical factors, nutrients and grazing effects. Aquat. Microb. Ecol. 57:137–149.

Sun J, Liu D, 2003. Geometric models for calculating cell biovolume and surface area for phytoplankton. J. Plankton Res. 25:1331–1346.

Vasconcelos V, Martins A, Vale M, Antunes A, Azevedo J, Welker M, Lopez O, Montejano G, 2010. First report on the occurrence of microcystins in planktonic cyanobacteria from Central Mexico. Toxicon 56:425–431. DOI: https://doi.org/10.1016/j.toxicon.2010.04.011

Vázquez G, Jiménez S, Favila ME, Martínez A, 2005. Seasonal dynamics of the phytoplankton community and cyanobacterial dominance in a eutrophic crater lake in Los Tuxtlas, Mexico. Écoscience 12:485–493. DOI: https://doi.org/10.2980/i1195-6860-12-4-485.1

Visser PM, Ibelings BW, Mur LR, Walsby AE, 2005. The Ecophysiology of the Harmful Cyanobacterium Microcystis, p. 109-142. In: J. Huisman, H.C.P. Matthijs, and P.M. Visser (eds.), Harmful cyanobacteria. Springer Netherlands. DOI: https://doi.org/10.1007/1-4020-3022-3_6

Visser PM, Passarge J, Mur LR, 1997. Modelling vertical migration of the cyanobacterium Microcystis. Hydrobiologia 349:99–109. DOI: https://doi.org/10.1023/A:1003001713560

Walsby AE, 1981. Cyanobacteria: Planktonic Gas-Vacuolate Forms, p.224-235. In: M.P. Starr, H. Stolp, H.G. Trüper, A. Balows, and H.G. Schlegel (eds.), The prokaryotes: a handbook on habitats, isolation, and identification of bacteria. Springer Berlin. DOI: https://doi.org/10.1007/978-3-662-13187-9_10

Wan L, Chen X, Deng Q, Yang L, Li X, Zhang J, Song C, Zhou Y, Cao X, 2019. Phosphorus strategy in bloom-forming cyanobacteria (Dolichospermum and Microcystis) and its role in their succession. Harmful Algae 84:46–55. DOI: https://doi.org/10.1016/j.hal.2019.02.007

Wells ML, Trainer VL, Smayda TJ, Karlson BSO, Trick CG, Kudela RM, Ishikawa A, Bernard S, Wulff A, Anderson DM, Cochlan WP, 2015. Harmful algal blooms and climate change: Learning from the past and present to forecast the future. Harmful Algae 49:68–93. DOI: https://doi.org/10.1016/j.hal.2015.07.009

Wetzel RG, 2001. Limnology. Lake and River Ecosystems. Academic Press, San Diego: 81 pp.

Wilkinson AA, Hondzo M, Guala M, 2020. Vertical heterogeneities of cyanobacteria and microcystin concentrations in lakes using a seasonal In situ monitoring station. Glob. Ecol. Conserv. 21:e00838. DOI: https://doi.org/10.1016/j.gecco.2019.e00838

Winder M, Hunter DA, 2008. Temporal organization of phytoplankton communities linked to physical forcing. Oecologia 156:179–192. DOI: https://doi.org/10.1007/s00442-008-0964-7

Wurtsbaugh WA, Paerl HW, Dodds WK, 2019. Nutrients, eutrophication and harmful algal blooms along the freshwater to marine continuum. WIREs Water 6:e1373. DOI: https://doi.org/10.1002/wat2.1373

Xie L, Xie P, Li S, Tang H, Liu H, 2003. The low TN:TP ratio, a cause or a result of Microcystis blooms? Water Res. 37:2073–2080. DOI: https://doi.org/10.1016/S0043-1354(02)00532-8

Yao B, Liu Q, Gao Y, Cao Z, 2017. Characterizing vertical migration of Microcystis aeruginosa and conditions for algal bloom development based on a light-driven migration model. Ecol. Res. 32:961–969. DOI: https://doi.org/10.1007/s11284-017-1505-9

Zhao CS, Shao NF, Yang ST, Ren H, Ge YR, Feng P, Dong BE, Zhao Y, 2019. Predicting cyanobacteria bloom occurrence in lakes and reservoirs before blooms occur. Sci. Total Environ. 670:837–848. DOI: https://doi.org/10.1016/j.scitotenv.2019.03.161

Published
2021-06-21
Info
Issue
Section
Original Articles
Edited by
Diego Fontaneto, CNR-IRSA Water Research Institute, Verbania, Italy
Keywords:
Cyanobacterial bloom, cyanobacterial dominance , phytoplankton community, eutrophication, tropical lake
Statistics
  • Abstract views: 177

  • PDF: 86
  • Supplementary: 14
How to Cite
1.
Montero E, Vázquez G, Caballero M, Favila ME, Martínez-Jerónimo F. Seasonal variation of <em>Microcystis aeruginosa</em> and factors related to blooms in a deep warm monomictic lake in Mexico. J Limnol [Internet]. 2021 Jun. 21 [cited 2021 Sep. 24];80(2). Available from: https://jlimnol.it/index.php/jlimnol/article/view/2013

Most read articles by the same author(s)