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Invasion of the dinoflagellate Ceratium furcoides (Levander) Langhans 1925 in South America: record of the pattern of expansion and persistence in tropical reservoirs in Northeastern Brazil

Abstract

Ceratium furcoides is a phytoplankton dinoflagellate that has received attention due to its invasive behavior in freshwater environments in South America. In this study, we monitored 87 tropical reservoirs in Northeastern Brazil between 2014 and 2020, with the objective of detecting and recording the occurrence of this species in these reservoirs, as well as to check its pattern of expansion and persistence. In total, between 2016 and 2020, there were 30 new records of C. furcoides in four of the six basins studied. The highest number of reservoirs with the occurrence of the species were located in the semiarid region, which suggests that it is an area of high susceptibility to invasion. The invaded area gradually increased over the sampled years, reaching 17,750 km2 in 2020 and the highest expansion rate occurred in 2017 (68.86 km year−1) with the longest distance covered in the first year of invasion (between 2016 and 2017, with 96.98 km). However, the species persistence in most environments was relatively low. Among the factors that facilitated the expansion of C. furcoides, we identified the action of an interbasin water transfer project as well as the resumption of rainfall patterns providing greater connectivity between the reservoirs. Further studies are required to understand the population dynamics of this dinoflagellate associated with climatic and limnological conditions. This information is essential for the development of management policies that guarantee ecosystem integrity and the provision of ecosystem services in aquatic systems.

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Fig. 1
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Source: AESA (2021)

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taken from the first record of C.furcoides in the reservoir

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References

  1. Accattatis V, Piccini C, Huber P, Metz S, Rueda E, Devercelli M (2020) Identifying invaders: the case of Ceratium furcoides (Gonyaulacales, Dinophyceae) in South America. J Phycol 56(5):1362–1366. https://doi.org/10.1111/jpy.13015

    Article  PubMed  Google Scholar 

  2. AESA. Agência Executiva de Gestão das Águas do Estado da Paraíba (2021) Volume dos açudes. Disponível em: http://www.aesa.pb.gov.br/aesa-website/monitoramento/. Acesso em: jan. de 2021

  3. Almanza V, Bicudo CEDM, Parra O, Urrutia R (2016) Características morfológicas y limnológicas de las floraciones de Ceratium furcoides (Dinophyta) en un lago somero de Chile Central. Limnetica 35(1):253–268. https://doi.org/10.23818/limn.35.21

  4. Alpert P, Bone E, Holzapfel C (2000) Invasiveness, invasibility and the role of environmental stress in the spread of non-native plants. Perspectives in Plant Ecology, Evolution and Systematics 3(1):52–66. https://doi.org/10.1078/1433-8319-00004

    Article  Google Scholar 

  5. Alvares CA, Stape JL, Sentelhas PC, De Moraes Gonçalves JL, Sparovek G (2013) Köppen’s climate classification map for Brazil. Meteorol Zeitschrift 22(6):711–728. https://doi.org/10.1127/0941-2948/2013/0507

    Article  Google Scholar 

  6. Anderson MJ (2017) Permutational multivariate analysis of variance (PERMANOVA). In: Balakrishnan N, Colton T, Everitt B, Piegorsch W, Ruggeri F, Teugels JL (eds) Wiley StatsRef: Statistics Reference Online. Wiley, Hoboken. https://doi.org/10.1002/9781118445112.stat07841

  7. Araújo JC, Döll P, Güntner A, Krol M, Abreu CBR, Hauschild M, Mendiondo EM (2004). Water Scarcity Under Scenarios for Global Climate Change and Regional Development in Semiarid Northeastern Brazil. Water International, 29(2):209–220. https://doi.org/10.1080/02508060408691770

  8. Asencio AD (2014) Diversity and distribution of microphytes and macrophytes in artificial irrigation ponds in a semi-arid mediterranean region (SE Spain). Int. J. Environ. Res 8(3):531–542. https://doi.org/10.22059/ijer.2014.747

  9. Barbosa JEL, Medeiros ESF, Brasil J, Cordeiro RDS, Crispim MCB, Silva GHGD (2012) Aquatic systems in semi-arid Brazil: limnology and management. Acta Limnol Bras 24(1):103–118. https://doi.org/10.1590/S2179-975X2012005000030

    Article  Google Scholar 

  10. Barbosa JEL, Severiano JS, Cavalcante H, Lucena-Silva D, Mendes CF, Barbosa VV, Silva RDS, Oliveira DA, Molozzi J (2021) Impacts of inter-basin water transfer on the water quality of receiving reservoirs in a tropical semi-arid region. Hydrobiologia 848:651–673. https://doi.org/10.1007/s10750-020-04471-z

    Article  Google Scholar 

  11. Bicudo CEM, Menezes M (2006) Gêneros de algas de águas continentais do Brasil. São Carlos, Brasil.

  12. Bordet F, Fontanarrosa MS, O’Farrell I (2017) Influence of light and mixing regime on bloom-forming phytoplankton in a subtropical reservoir. River Res Appl 33(8):1315–1326. https://doi.org/10.1002/rra.3189

    Article  Google Scholar 

  13. Brasil J, Santos JB, Sousa W, Menezes RF, Huszar VL, Attayde JL (2020) Rainfall leads to habitat homogenization and facilitates plankton dispersal in tropical semiarid lakes. Aquat Ecol 54(1):225–241. https://doi.org/10.1007/s10452-019-09738-9

    CAS  Article  Google Scholar 

  14. Bustamante GC, Ramírez RJJ, Boltovskoy A, Vallejo A (2012) Spatial and temporal change characterization of Ceratium furcoides (Dinophyta) in the equatorial reservoir Riogrande II. Colombia Acta Limnol Bras 24(2):207–219. https://doi.org/10.1590/S2179-975X2012005000039

    Article  Google Scholar 

  15. Cassol APV, Pereira-Filho W, Oliveira MA, Domingues AL, Correa FS, Buriol GA (2014) First record of a bloom of the invasive species Ceratium furcoides (Levander) Langhans 1925 in Rio Grande do Sul state. Brazil Braz J Biol 74(2):515–517. https://doi.org/10.1590/1519-6984.05413

    CAS  Article  PubMed  Google Scholar 

  16. Datry T, Bonada N, Heino J (2016) Towards understanding the organisation of metacommunities in highly dynamic ecological systems. Oikos 125(2):149–159. https://doi.org/10.1111/oik.02922

    Article  Google Scholar 

  17. Datry T, Larned ST, Tockner K (2014) Intermittent rivers: a challenge for freshwater ecology. Bioscience 64(3):229–235. https://doi.org/10.1093/biosci/bit027

    Article  Google Scholar 

  18. Davies BR, Thoms M, Meador M (1992) An assessment of the ecological impacts of inter-basin water transfers, and their threats to river basin integrity and conservation. Aquat Conserv 2(4):325–349. https://doi.org/10.1002/aqc.3270020404

    Article  Google Scholar 

  19. Epanchin-Niell RS, Wilen JE (2012) Optimal spatial control of biological invasions. J Environ Econ Manag 63(2):260–270. https://doi.org/10.1016/j.jeem.2011.10.003

    Article  Google Scholar 

  20. Esnal JPP, Frizzera CI, Goyenola G, de-Mello FT, Fosalba C, Baattrup-Pedersen A, Meerhoff M, Jeppesen, E (2021) Invasion of Ceratium furcoides in subtropical lakes in Uruguay: environmental drivers and first fish kill record during its bloom. Biol Invasions. https://doi.org/10.1007/s10530-021-02600-w

  21. Ewerts HE, Swanepoel A, du Preez HH (2013) Efficacy of conventional drinking water treatment processes in removing problem-causing phytoplankton and associated organic compounds. Water Sa 39(5):739–750. https://doi.org/10.4314/wsa.v39i5.19

    CAS  Article  Google Scholar 

  22. Francisco PRM, Medeiros RD, Santos D, Matos RD (2015) Classificação climática de Köppen e Thornthwaite para o estado da Paraíba. Revista Brasileira De Geografia Física 8(4):1006–1016. https://doi.org/10.5935/1984-2295.20150049

    Article  Google Scholar 

  23. Gallardo B, Aldridge DC (2018) Inter-basin water transfers and the expansion of aquatic invasive species. Water Res 143:282–291. https://doi.org/10.1016/j.watres.2018.06.056

    CAS  Article  PubMed  Google Scholar 

  24. Gil CB, Restrepo JJR, Boltovskoy A, Vallejo A (2012) Spatial and temporal change characterization of Ceratium furcoides (Dinophyta) in the equatorial reservoir Riogrande II. Colombia Acta Limnol Bras 24(2):207–219. https://doi.org/10.1590/S2179-975X2012005000039

    Article  Google Scholar 

  25. Good IJ (1953) The population frequencies of species and the estimation of population parameters. Biometrika 40(3–4):237–264. https://doi.org/10.2307/2333344

    Article  Google Scholar 

  26. Hart RC, Wragg PD (2009) Recent blooms of the dinoflagellate Ceratium in Albert Falls Dam (KZN): History, causes, spatial features and impacts on a reservoir ecosystem and its zooplankton. Water as 35(4):455–468. https://doi.org/10.4314/wsa.v35i4.76807

    CAS  Article  Google Scholar 

  27. Heaney SI, Chapman DV, Morison HR (1983) The role of the cyst stage in the seasonal growth of the dinoflagellate Ceratium hirundinella within a small productive lake. Brit Phycol J 18(1):47–59. https://doi.org/10.1080/00071618300650061

    Article  Google Scholar 

  28. Hickel B (1988) Sexual reproduction and life cycle of Ceratium furcoides (Dinophyceae) in situ in the lake Plußsee (FR). In: Jones R, Ilmavirta V (eds) Flagellates in Freshwater Ecosystems. Springer, Dordrecht, pp 41–48

    Chapter  Google Scholar 

  29. Hill MO (2012) Local frequency as a key to interpreting species occurrence data when recording effort is not known. Methods Ecol Evol 3(1):195–205. https://doi.org/10.1111/j.2041-210X.2011.00146.x

    Article  Google Scholar 

  30. Incagnone G, Marrone F, Barone R, Robba L, Naselli-flores L (2015) How do freshwater organisms cross the “dry ocean”? A review on passive dispersal and colonization processes with a special focus on temporary ponds. Hydrobiologia 750(1):103–123. https://doi.org/10.1007/s10750-014-2110-3

    Article  Google Scholar 

  31. ISSG. Global Invasive Species Database. Ref Type: Internet Communication, 2008.

  32. Johnson PT, Olden JD, Vander Zanden MJ (2008) Dam invaders: impoundments facilitate biological invasions into freshwaters. Front Ecol Environ 6(7):357–363. https://doi.org/10.1890/070156

    Article  Google Scholar 

  33. Kernan M (2015) Climate change and the impact of invasive species on aquatic ecosystems. Aquat Ecosyst Health Manage 18(3):321–333. https://doi.org/10.1080/14634988.2015.1027636

    Article  Google Scholar 

  34. Knappe DRU, Briley D, Belk R (2004) Algae detection and removal strategies for drinking water treatment plants. American Water Works Association.

  35. Latini AO, Resende DC, Pombo VB, Coradin L (2016) Espécies exóticas invasoras de águas continentais no Brasil. Brasília: MMA, pp. 791, (Série Biodiversidade, 39).

  36. Lindström K (1992) Ceratium in Lake Erken: vertical distribution, migration and form variation. Nord J Bot 12(5):541–556. https://doi.org/10.1111/j.1756-1051.1992.tb01833.x

    Article  Google Scholar 

  37. Macêdo RL, Franco ACS, Corrêa RF, Costa KN, Pereira LG, Oliveira FDM, Klippel G, Cordeiro BD, Thiago MGR, Rocha MIA, Huszar VLM, Santos LN, Branco CWC (2021a) Spreading of the invasive dinoflagellate Ceratium furcoides (Levander) Langhans throughout the Paraiba do Sul ecoregion, South America. Brazil Limnetica 40(2). https://doi.org/10.23818/limn.40.16

  38. Macêdo RL, Russo P, Correa RF, Rocha O, dos Santos LN, Branco CW (2021b) The drifting dinoflagellate Ceratium furcoides (Levander) Langhans 1925: fundamental niche shift during global invasion. Hydrobiologia 848(9):2105–2117. https://doi.org/10.1007/s10750-020-04495-5

    Article  Google Scholar 

  39. Marengo JÁ, Cunha AP, Alves LM (2016) A seca de 2012–15 no semiárido do Nordeste do Brasil no contexto histórico. Climanálise 3(1):1–6

    Google Scholar 

  40. Matteucci SD, Colma A (1982) Metodología para el estudio de la vegetación. Secretaria General de la Organización de los Estados Americanos, Washington, DC

    Google Scholar 

  41. Matsumura-Tundisi T, Tundisi JG, Luzia AP, Degani RM (2010) Occurrence of Ceratium furcoides (Levander) Langhans 1925 bloom at the Billings Reservoir, São Paulo State. Brazil Brazilian Journal of Biology 70(3):825–829. https://doi.org/10.1590/S1519-69842010000400013

    CAS  Article  Google Scholar 

  42. Meichtry de Zaburlín N, Vogler RE, Molina MJ, Llano VM (2016) Potential distribution of the invasive freshwater dinoflagellate Ceratium furcoides (Levander) Langhans (Dinophyta) in South America. J Phycol 52(2):200–208. https://doi.org/10.1111/jpy.12382

    Article  PubMed  Google Scholar 

  43. Meichtry de Zaburlín N, Boltovskoy A, Rojas CC, Rodriguez RM (2014) Primer registro del dinoflagelado invasor Ceratium furcoides (Levander) Langhans 1925 en la Argentina y su distribución en el área de influencia del Embalse Yacyretá (río Paraná, Argentina-Paraguay). Limnetica 33(1):153–160. https://doi.org/10.23818/limn.33.12

  44. Moestrup Ø, Calado AJ (2018) Süßwasserflora von Mitteleuropa, Bd. 6-Freshwater Flora of Central Europe, Dinophyceae. Springer-Verlag 6

  45. Mooney HA (2005) Invasive alien species: the nature of the problem. In: Mooney HA et al. (ed) Invasive alien species: a new synthesis. IslandPress, Washington.

  46. Morais-Junior CS, Melo-Júnior M, Gonçalves-Souza T, Lyra-Neves RM (2019) Zoochory of zooplankton: seasonality and bird morphological diversity can influence metacommunity dynamics of temporary ponds. J Plankton Res 41(4):465–477. https://doi.org/10.1093/plankt/fbz028

    Article  Google Scholar 

  47. Morales EA (2016) Floración de Ceratium furcoides (Levander) Langhans (Dinoflagellata, Dinophyceae) en la represa de La Angostura, Cochabamba. Bolivia Acta Nova 7(4):389–398

    Google Scholar 

  48. Moreira RA, Rocha O, Santos RM, Laudares-Silva R, Dias ES, Eskinazi-Sant’Anna EM, (2015) First record of Ceratium furcoides (Dinophyta), an invasive species, in a temporary high-altitude lake in the Iron Quadrangle (MG, Southeast Brazil). Braz J Biol 75(1):98–103. https://doi.org/10.1590/1519-6984.08013

    CAS  Article  PubMed  Google Scholar 

  49. Naselli-Flores L, Termine R, Barone R (2016) Phytoplankton colonization patterns. Is species richness depending on distance among freshwaters and on their connectivity? Hydrobiologia 764(1):103–113. https://doi.org/10.1007/s10750-015-2283-4

  50. Naselli-flores L, Padisák J (2016) Blowing in the wind: how many roads can a phytoplanktont walk down? A synthesis on phytoplankton biogeography and spatial processes. Hydrobiologia 764(1):303–313. https://doi.org/10.1007/s10750-015-2519-3

    Article  Google Scholar 

  51. Nishimura PY, Pompêo M, Moschini-Carlos V (2015) Invasive dinoflagellate Ceratium furcoides (Levander) Langhans in two linked tropical reservoirs. In: Pompêo M, Moschini-Carlos V, Nishimura PY, Silva SC, Doval JCL (Eds.) Ecologia de reservatórios e interfaces, Instituto de Biociências, São Paulo, pp 132–142.

  52. Oksanen J, Guillaume FB, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2019) vegan: Community Ecology Package. R package version 2.5–6. https://CRAN.R-project.org/package=vegan

  53. Oliveira FHPC, Macêdo IME, Moreira CHPM, Shinohara NKS, Lira OO, Ramalho WP (2016) Occurrence of Ceratium furcoides (Levander) Langhans 1925 (Dinophyceae: Ceratiaceae) in Two Reservoirs of the Capibaribe Watershed Located in Semiarid Region. Revista Geama 2(3):300–308

    Google Scholar 

  54. Oliveira CYB, Oliveira CDL (2018) Geographical distribution of exotic dinoflagellate of freshwater Ceratium furcoides (Levander) Langhans 1925 in Brazil. Journal of Neotropical Biology 15(2):109–113

    Google Scholar 

  55. Oliveira CYB (2018) Microalgas do Semiárido: Florações nocivas, variabilidade sazonal e suas possíveis aplicações biotecnológias. Universidade Federal Rural de Pernambuco, Trabalho de Conclusão de Curso

    Google Scholar 

  56. Oliveira HS, Moura A, Cordeiro-Araújo M (2011) First record of Ceratium Schrank, 1973 (Dinophyceae: Ceratiaceae) in freshwater ecosystems in the semiarid region of Brazil. Check List 7(5):626–628. https://doi.org/10.15560/7.5.626

  57. Olrik K (1994) Phytoplankton-Ecology: Determining factors for the distribution of phytoplankton in freshwater and the sea. Ministry of the Environment, Danish Environmental Protection Agency.

  58. Padisák J, Vasas G, Borics G (2016) Phycogeography of freshwater phytoplankton: traditional knowledge and new molecular tools. Hydrobiologia 764(1):3–27. https://doi.org/10.1007/s10750-015-2259-4

    CAS  Article  Google Scholar 

  59. Park YS, Chang J, Lek S, Cao W, Brosse S (2003) Conservation strategies for endemic fish species threatened by Three Gorges Dam. Conserv Biol 17(6):1748–1758

    Article  Google Scholar 

  60. Pejchar L, Mooney HÁ (2009) Invasive species, ecosystem services and human well-being. Trends Ecol Evol 24(9):497–504. https://doi.org/10.1016/j.tree.2009.03.016

    Article  PubMed  Google Scholar 

  61. Pollingher U (1987) Freshwater Ecosystems. In: Taylor FJR, Pollingher U (eds) Ecology of dinoflagellates. Botanical Monographs, Blackwell Scientific Publications, The biology of dinoflagellates, pp 502–529

    Google Scholar 

  62. Pollingher U (1988) Freshwater armored dinoflagellates: growth, reproduction strategies, and population dynamics. In: Sandgren CD (ed) Growth and Reproductive Strategies of Freshwater Phytoplankton. Cambridge University Press, New York, pp 134–174

    Google Scholar 

  63. Popovsky J, Pfiester LA, (1990) Dinophyceae (Dinoflagellida). In: Ettl H, Gerloff J, Heyning H, Mollenhauer D (eds) Das Süsswasserflora von Mitteleuropa. G. Fischer Verlag, Stuttgart, p 263

    Google Scholar 

  64. Preuss S, Low M, Cassel‐Lundhagen A, Berggren A (2014) Evaluating range‐expansion models for calculating nonnative species' expansion rate. Ecol Evol 4(14):2812–2822. https://doi.org/10.1002/ece3.1106

  65. QGIS Geographic Information System (2020) Open Source Geospatial Foundation Project. http://qgis.osgeo.org

  66. R Core Team (2019) R: a language and environment for sta- tistical computing. R Foundation for Statistical Comput- ing, Vienna, Austria. http://www.rproject.org/

  67. Rengefors K, Anderson DM (1998) Environmental and endogenous regulation of cyst germination in two freshwater dinoflagellates. J Phycol 34(4):568–577. https://doi.org/10.1046/j.1529-8817.1998.340568.x

    Article  Google Scholar 

  68. Rengefors K, Karlsson I, Hansson LA (1998) Algal cyst dormancy: a temporal escape from herbivory. Proc R Soc Lond Biol 265(1403):1353–1358. https://doi.org/10.1098/rspb.1998.0441

  69. Reynolds CS (1984) The ecology of freshwater phytoplankton. Cambridge university press, pp 396.

  70. Ruhi A, Catford JA, Cross WF, Escoriza D, Olden JD (2019) Understanding the nexus between hydrological alteration and biological invasions. In: Sabater S, Elosegi A, Ludwig R (ed) Multiple Stressors in River Ecosystems, Elsevier pp 45–64. https://doi.org/10.1016/B978-0-12-811713-2.00003-0

  71. Silva LCD, Leone IC, Santos-Wisniewski MJD, Peret AC, Rocha O (2012) Invasion of the dinoflagellate Ceratium furcoides (Levander) Langhans 1925 at tropical reservoir and its relation to environmental variables. Biota Neotrop 12(2):93–100. https://doi.org/10.1590/S1676-06032012000200010

    CAS  Article  Google Scholar 

  72. Silva LND, Medeiros CMD, Cavalcante KP, Cardoso LDS (2019) Invasion and establishment of Ceratium furcoides (Dinophyceae) in an urban lake in Porto Alegre, RS. Brazil Acta Botanica Brasilica 33(4):654–663. https://doi.org/10.1590/0102-33062018abb0429

    Article  Google Scholar 

  73. Silva TJM, Callado NH, Souza VCB, Vasconcelos MRS (2020) Respostas da qualidade da água e fitoplânctons à redução de vazão e recepção de cargas de sedimentos no reservatório de Xingó/AL. Revista de Gestão de Água da América Latina 17, e15.

  74. Silva WJD, Nogueira IDS, Melo-magalhães EMD, Benício SHM, Pessoa SM, Menezes M (2018) Expansion of invasive Ceratium furcoides (Dinophyta) toward north-central Brazil: new records in tropical environments. Acta Limnol Bras 30:e210. https://doi.org/10.1590/s2179-975x5917

    CAS  Article  Google Scholar 

  75. Smalley GW, Coats DW, Stoecker DK (2003) Feeding in the mixotrophic dinoflagellate Ceratium furca is in fluenced by intracellular nutrient concentrations. Mar Ecol Prog Ser 262:137–151

    Article  Google Scholar 

  76. Smalley GW, Coats DW (2002) Ecology of the red-tide dinoflagellate Ceratium furca: distribution, mixotrophy, and grazing impact on ciliate populations of Chesapeake Bay. J Eukaryot Microbiol 49(1):63–73. https://doi.org/10.1111/j.1550-7408.2002.tb00343.x

    Article  PubMed  Google Scholar 

  77. Somenzari M, Amaral PP, Cueto VR, Guaraldo AC, Jahn AE, Lima DM, Lima PC, Lugarini C, Machado CG, Martinez J, Nascimento JLX, Pacheco JF, Paludo D, Prestes NP, Serafini PP, Silveira LF, Sousa AEBA, Sousa NA, Souza MA, Telino-Júnior WR, Whitney BM (2018) An overview of migratory birds in Brazil. Papéis Avulsos De Zoologia 58, e20185803. https://doi.org/10.11606/1807-0205/2018.58.03

  78. Souza RCCL, Calazans SH, Silva EP (2009) Impacto das espécies invasoras no ambiente aquático. Ciência e Cultura 61(1):35–41

    Google Scholar 

  79. Stefaniak K, Goldyn R, Kowalczewska-madura K (2007) Changes of summer phytoplankton communities in Lake Swarzedzkie in the 2000–2003 period. Oceanol Hydrobiol Stud 36(1):77–85

    Google Scholar 

  80. Stolf R, Piedade SMDS, Silva JRD, da Silva LC, Maniero MÂ (2012) Water transfer from São Francisco river to semiarid northeast of Brazil: technical data, environmental impacts, survey of opinion about the amount to be transferred. Engenharia Agrícola 32(6):998–1010

    Article  Google Scholar 

  81. Strayer DL (2010) Alien species in fresh waters: ecological effects, interactions with other stressors, and prospects for the future. Freshw Biol 55:152–174. https://doi.org/10.1111/j.1365-2427.2009.02380.x

    Article  Google Scholar 

  82. Sukenik A, Hadas O, Kaplan A, Quesada A (2012) Invasion of Nostocales (cyanobacteria) to subtropical and temperate freshwater lakes–physiological, regional, and global driving forces. Front Microbiol 3:86. https://doi.org/10.3389/fmicb.2012.00086

    Article  PubMed  PubMed Central  Google Scholar 

  83. Suweis S, Bertuzzo E, Mari L, Rodriguez-Iturbe I, Maritan A, Rinaldo A (2012) On species persistence-time distributions. J Theor Biol 303:15–24. https://doi.org/10.1016/j.jtbi.2012.02.022

    CAS  Article  PubMed  Google Scholar 

  84. Vieira PR, Pruski FF, Souza JRC (2020) Dimensioning of reservoirs for semiarid regions using synthetic series. Revista Brasileira De Engenharia Agrícola e Ambiental 24(9):581–589. https://doi.org/10.1590/1807-1929/agriambi.v24n9p581-589

    Article  Google Scholar 

  85. Wilson JR, Dormontt EE, Prentis PJ, Lowe AJ, Richardson DM (2009) Something in the way you move: dispersal pathways affect invasion success. Trends Ecol Evol 24(3):136–144. https://doi.org/10.1016/j.tree.2008.10.007

    Article  PubMed  Google Scholar 

  86. Zhao ZY, Zuo J, Zillante G (2017) Transformation of water resource management: a case study of the South-to-North Water Diversion project. J Clean Prod 163:136–145. https://doi.org/10.1016/j.jclepro.2015.08.066

    Article  Google Scholar 

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Acknowledgements

We would like to thank Ministry of Science, Technology and Innovation/Financier of Studies and Projects (MCTI/FINEP—CTHIDRO 01/2013), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brazil (CAPES—Finance Code 001) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).

Funding

This study was funded by Ministry of Science, Technology and Innovation/Financier of Studies and Projects (MCTI/FINEP—CTHIDRO 01/2013) and the Coordination for the Improvement of Higher Education Personnel—Brazil (CAPES)—Finance Code 001.

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Conceptualization:JSS, ESO, JELB; Data curation: JSS, DLS; Formal analysis: JSS, GCM, EAS; Investigation: JSS, ESO, DLS; Methodology: JSS, EAS; Funding acquisition: JELB; Project administration: JSS, JELB; Resources: JELB; Supervision: JSS, JELB; Validation: JSS, DLS, GCM, EAS, JELB; Visualization: JSS, ESO, DSL, GCM, JELB; Writing – original draft: JSS, ESO; Writing – review & editing: JSS, ESO, DSL, GCM, EAS, JELB.

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Correspondence to Juliana dos Santos Severiano.

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Severiano, J.S., Oliveira, E.S., Lucena-Silva, D.d. et al. Invasion of the dinoflagellate Ceratium furcoides (Levander) Langhans 1925 in South America: record of the pattern of expansion and persistence in tropical reservoirs in Northeastern Brazil. Biol Invasions (2021). https://doi.org/10.1007/s10530-021-02641-1

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Keywords

  • Dispersion
  • Phytoplankton
  • Biological invasion
  • Semiarid
  • Water transfer
  • Prolonged drought