Abstract
Ceratium furcoides is a dinoflagellate that exhibits invasive behavior in the aquatic ecosystems of South America and has been expanding its range in recent years. In this study, we monitored 151 municipalities in southern Brazil between 2012 and 2019 with the objective of detecting and recording the species’ occurrence and abundance in the state of Rio Grande do Sul, as well as to examine its expansion and persistence pattern. Ceratium furcoides was recorded in 84.1% of the monitored municipalities, in all three of the state’s hydrographic regions (HR). Spatially, the Guaiba HR showed the highest density for the species (10,912 cells mL−1); in temporal scales, 2014 and 2015 displayed density peaks, usually in the summer. The cumulative area invaded by C. furcoides gradually increased, reaching 266,625 km2 in 2018, corresponding to about 94% of the state; however, the highest expansion rate (3142 km year−1) and longest distance covered (40.4 km) occurred in 2012, during its introduction. The expansion varied over the studied years, initially heading toward HR Littoral and Guaiba (between 2012 and 2014), followed by a steady period (2015–2017), and subsequently a progression toward HR Uruguay (2018). The frequency analysis showed that persistence was short in most of the municipalities. The results indicate that local environmental characteristics, especially temperature and precipitation, could be key for the invasion and development of the species. Given its rapid expansion, statewide dispersibility, and extremely large bloom formation, Rio Grande do Sul looks to be C. furcoides’ second home.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The datasets generated and analyzed during the current study are available from the corresponding author on reasonable request.
Abbreviations
- CORSAN:
-
Companhia Riograndense de Saneamento
- ETAs:
-
Water treatment stations
- FEPAM:
-
Fundação Estadual de Proteção Ambiental
- FO:
-
Frequency of occurrence
- HB:
-
Hydrographic basins
- HR:
-
Hydrographic regions
- IBGE:
-
Instituto Brasileiro de Geografia e Estatística
- IDW:
-
Inverse distance weighted
- MCP:
-
Minimum convex polygon
- MS:
-
Meteorological stations
- RS:
-
Rio Grande do Sul
References
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
Almanza A, Bicudo CEM, 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
Almeida CR, Splandorello FB, Giroldo D, Yunes JS (2016) The effectiveness of conventional water treatment in removing Ceratium furcoides (Levander) Langhans, Microcystis spp. and microcystins. Water SA 42(4):606–610. https://doi.org/10.4314/wsa.v42i4.11
ANA – Agência Nacional de Águas (2015) Conjuntura dos recursos hídricos no Brasil: regiões hidrográficas brasileiras – Edição Especial. Brasília: ANA, 2015, p 163
Bellard C, Cassey P, Blackburn TM (2016) Alien species as a driver of recent extinctions. Biol Lett. https://doi.org/10.1098/rsbl.2015.0623
Boltovskoy A (1991) Colonization of freshwater bodies in Argentina and Chile by Ceratium hirundinella (Dinophyceae). Bol Soc Argent Bot 38:148
Boltovskoy A, Echenique RO, Guerrero JM (2003) Colonización de limnotopos de Argentina por Ceratium hirundinella (Dinophyceae). Bol Soc Argent Bot 38:148
Boltovskoy A, Echenique RO, Guerrero JM (2013) Sucesivas invasiones de especies de Ceratium (Dinophyceae) en Sudamérica: un proceso que lleva dos décadas. Bol Soc Argent Bot 48:27
BoQiang Q, Guang G, Guangwei Z, YunLin Z, YuZhi S, XiangMing T, Hai X, JianMing D (2013) Lake eutrophication and its ecosystem response. Chin Sci Bull 59(9):961–970. https://doi.org/10.1007/s11434-012-5560-x
Bordet F, Fontanarrosa MS, O’Farrell I (2017) Influence of light and mixing regime on bloom-forming phytoplankton in a subtropical reservoir. River Res Applic 33(8):1315–1326. https://doi.org/10.1002/rra.3189
BRASIL (2003) Ministério do Meio Ambiente, Secretaria Recursos Hídricos/Fundação Getúlio Vargas: Documento Base de Referência. Brasília, DF
BRASIL (2006) Ministério do Meio Ambiente, Secretaria de Recursos Hídricos: Caderno da Região Hidrográfica do Uruguai. https://www.gov.br/mma/pt-br. Accessed 12 Jan 2022
Bustamante-Gil C, Ramírez-Restrepo JJ, 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
Bustamante-Gil C, Amat E, Boltovskoy A, Ramírez-Restrepo JJ (2021) The first floristic study of freshwater dinoflagellates (Dinophyceae) in Colombia. J Limnol. https://doi.org/10.4081/jlimnol.2021.2023
Butterwick C, Heaney SI, Talling JF (2005) Diversity in the influence of temperature on the growth rates of freshwater algae, and its ecological relevance. Freshw Biol 50(2):291–300. https://doi.org/10.1111/j.1365-2427.2004.01317.x
Cai W, McPhaden MJ, Grimm AM, Rodrigues RR, Taschetto AS, Garreaud RD, Dewitte B, Poveda G, Ham YG, Santoso A, Ng B, Anderson W, Wang G, Geng T, Jo HS, Marengo JA, Alves LM, Osman M, Li S, Wu L, Karamperidou C, Takahashi K, Vera C (2020) Climate impacts of the El Niño–southern oscillation on South America. Nat Rev Earth Environ 1(4):215–231. https://doi.org/10.1038/s43017-020-0040-3
Canfield DE (2015) Baas Becking’s geobiology: or introduction to environmental science. Wiley. https://doi.org/10.1002/9781118295472
Carty S, Parrow MW (2015) Dinoflagellates. In: Wehr JD, Sheath RG, Kociolek JP (eds) Freshwater algae of North America, aquatic ecology, 2nd edn. Academic Press, Boston, pp 773–807
Cassie V (1978) Seasonal changes in phytoplankton densities in four north island lakes, 1973–74. NZ J Mar Freshwat Res 12:153–166. https://doi.org/10.1080/00288330.1978.9515736
Cavalcante KP, Zanotelli JC, Muller CC, Scherer KD, Frizzo JK, Ludwig TA, Cardoso LS (2013) First record of expansive Ceratium Schrank, 1793 species (Dinophyceae) in Southern Brazil, with notes on their dispersive patterns in Brazilian environments. Check List 9(4):862–866. https://doi.org/10.15560/9.4.862
Cavalcante KP, Cardoso LS, Sussella R, Becker V (2016) Towards a comprehension of Ceratium (Dinophyceae) invasion in Brazilian freshwaters: autecology of C. furcoides in subtropical reservoirs. Hydrobiologia 771:265–280. https://doi.org/10.1007/s10750-015-2638-x
CETESB - Companhia Ambiental do Estado de São Paulo (2005) Nota Técnica 06 L5.303. Fitoplâncton de água doce. Métodos qualitativo e quantitativo. São Paulo, SP
Chislock MF, Doster E, Zitomer RA, Wilson AE (2013) Eutrophication: causes, consequences, and controls in aquatic ecosystems. Nature Education Knowledge, 4(4): 10. https://www.nature.com/scitable/knowledge/library/eutrophication-causes-consequences-and-controls-in-aquatic-102364466/. Accessed 02 Dec 2023
Clarke AJ (2008) An introduction to the dynamics of El Nino and the Southern Oscillation. Elsevier Academic Press, Londres, p 324
Crossetti LO, Bicudo DC, Bini LM, Dala-Corte RB, Ferragut C, Bicudo CEM (2019) Phytoplankton species interactions and invasion by Ceratium furcoides are influenced by extreme drought and water-hyacinth removal in a shallow tropical reservoir. Hidrobiologia 831:71–85. https://doi.org/10.1007/s10750-018-3607-y
Daga IC, Belmonte MCF, Reyna SM (2020) Composicion algal y bioindicadores de calidad de agua. Caso de estudio: embalse San Roque, Córdoba. Argent, Cuad Curiham 26:1–11
Devlin M, Bricker S, Painting S (2011) Comparison of five methods for assessing impacts of nutrient enrichment using estuarine case studies. Biogeochemistry 106:177–205. https://doi.org/10.1007/s10533-011-9588-9
Didham RK, Tylianakis JM, Hutchison MA, Ewers RM, Gemmell NJ (2005) Are invasive species the drivers of ecological change? Trends Ecol Evol 20(9):470–474. https://doi.org/10.1016/j.tree.2005.07.006
Diez JM, D’Antonio CM, Dukes JS, Grosholz ED, Olden JD, Sorte CJ, Blumenthal DM, Bradley B, Early R, Ibáñez I, Jones SJ, Lawler JJ, Miller LP (2012) Will extreme climatic events facilitate biological invasions? Front Ecol Environ 10(5):249–257. https://doi.org/10.1890/110137
Dodds WK, Bouska WW, Eitzmann JL, Pilger TJ, Pitts KL, Riley AJ, Schloesser JT, Thornbrugh DJ (2009) Eutrophication of US freshwaters: analysis of potential economic damages. Environ Sci Technol 43(1):12–19. https://doi.org/10.1021/es801217q
Dukes JS, Mooney HA (1999) Does global change increase the success of biological invaders? Trends Ecol Evol 14(4):135–139. https://doi.org/10.1016/s0169-5347(98)01554-7
Easterling DR, Meehl GA, Parmesan C, Changnon SA, Karl TR, Mearns LO (2000) Climate extremes: observations, modeling, and impacts. Science 289(5487):2068–2074. https://doi.org/10.1126/science.289.5487.2068
El-Otify AM, Shafik HM, Szőke E (2003) Analyses of physico-chemical characteristics and phytoplankton communities of Lake Nasser during the last two decades. Acta Bot Hungar 45(1–2):75–100. https://doi.org/10.1556/abot.45.2003.1-2.8
Engel K, Tollrian R, Jeschke JM (2011) Integrating biological invasions, climate change and phenotypic plasticity. Commun Integr Biol 4(3):247–250. https://doi.org/10.4161/cib.4.3.14885
Fenchel TOM, Finlay BJ (2004) The ubiquity of small species: patterns of local and global diversity. Bioscience 54(8):777–784. https://doi.org/10.1641/0006-3568(2004)054[0777:TUOSSP]2.0.CO;2
FEPAM – Fundação Estadual de Proteção Ambiental Henrique Luis Roessler (2018) Base Cartográfica do Estado do Rio Grande do Sul, escala 1:25.000 – BCRS25. http://ww2.fepam.rs.gov.br/bcrs25/. Accessed 22 Aug 2023
FEPAM – Fundação Estadual de Proteção Ambiental Henrique Luis Roessler (2022) Regiões Hidrográficas do estado do RS. http://www.fepam.rs.gov.br/qualidade/regioes_hidro.asp. Accessed 4 July 2022
Fuhrman JA (2009) Microbial community structure and its functional implications. Nature 459:193–199. https://doi.org/10.1038/nature08058
Guerrero J, Echenique R (1997) Ceratium hirundinella blooms in Argentine reservoirs. Harmful Algae News 16:3
Haase J, Stringuini MH, Silva MLBC, Rodrigues MLK, Koch SMV (2003) VI 049 - Qualidade das Águas Superficiais do Litoral Norte e Médio do Rio Grande Do Sul, 22º Congresso Brasileiro de Engenharia Sanitária e Ambiental, ABES - Associação Brasileira de Engenharia Sanitária e Ambiental
Haochen T, Yuanyuan W, Shuyin L, Qi Z, Guoxiang L, Benwen L (2020) A newly recorded species of freshwater blooming dinoflagellates from China and its ecological risks. J Lake Sci 32:784–792. https://doi.org/10.18307/2020.0318
Hellmann JJ, Byers JE, Bierwagen BG, Dukes JS (2008) Five potential consequences of climate change for invasive species. Conserv Biol 22(3):534–543. https://doi.org/10.1111/j.1523-1739.2008.00951.x
Huntington TG (2010) Climate warming-induced intensification of the hydrologic cycle: an assessment of the published record and potential impacts on agriculture. Advances in agronomy, vol 109. Elsevier, pp 1–53
IBGE - Instituto Brasileiro de Geografia e Estatística (2022) Malha Municipal Digital e Áreas Territoriais. Nota metodológica n. 01 Informações Técnicas e Legais para a Utilização dos Dados Publicados. https://biblioteca.ibge.gov.br/visualizacao/livros/liv101998.pdf. Accessed 22 Aug 2023
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 750:103–123. https://doi.org/10.1007/s10750-014-2110-3
INMET – Instituto Nacional de Meteorologia (2023) Tabela de Dados das Estações. https://tempo.inmet.gov.br/TabelaEstacoes. Accessed 22 August 2023
Komárek J, Komárková-Legnerová J, Santanna CL, Azevedo MTP, Senna PA (2002) Two common Microcystis species from tropical América. Criptogam/algologie 23:159–177
Kottek M, Grieser J, Beck C, Rudolf B, Rubel F (2006) World map of the Köppen–Geiger climate classification updated. Meteorol Z 15(3):259–263. https://doi.org/10.1127/0941-2948/2006/0130
Kruk C, Piccini C, Devercelli M, Nogueira L, Accattatis V, Sampognaro L, Marley A (2021) A trait-based approach predicting community assembly and dominance of microbial invasive species. Oikos 130(4):571–586. https://doi.org/10.1111/oik.07694
Kumschick S, Gaertner M, Vilà M, Essl F, Jeschke JM, Pyšek P, Ricciardi A, Bacher S, Blackburn TM, Dick JTA, Evans T, Hulme PE, Kühn I, Mrugała A, Pergl J, Rabitsch W, Richardson DM, Sendek A, Winter M (2015) Ecological impacts of alien species: quantification, scope, caveats, and recommendations. Bioscience 65(1):55–63. https://doi.org/10.1093/biosci/biu193
Laurance WF, Sayer J, Cassman KG (2014) Agricultural expansion and its impacts on tropical nature. Trends Ecol Evol 29(2):107–116. https://doi.org/10.1016/j.tree.2013.12.001
Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391. https://doi.org/10.1016/S0169-5347(02)02554-5
Lesschen JP, Schoorl JM, Cammeraat LH (2009) Modelling runoff and erosion for a semi-arid catchment using a multi-scale approach based on hydrological connectivity. Geomorphology 109(3–4):174–183. https://doi.org/10.1016/j.geomorph.2009.02.030
Lu GY, Wong DW (2008) An adaptive inverse-distance weighting spatial interpolation technique. Comput Geosci 34(9):1044–1055. https://doi.org/10.1016/j.cageo.2007.07.010
Mac Donagh ME, Casco MA, Claps MC (2005) Colonization of a neotropical Reservoir (Cordoba, Argentina) by Ceratium hirundinella (OF Muller) Bergh. Int J Limnol 41(4):291–299. https://doi.org/10.1051/limn/2005020
Macêdo R, Russo P, Corrêa R, Rocha O, Neves-Dos-Santos L, Branco C (2021) The drifting dinoflagellate Ceratium furcoides (Levander) Langhans 1925: fundamental niche shift during global invasion. Hydrobiologia 4:2105–2117. https://doi.org/10.1007/s10750-020-04495-5
Masotti I, Moulin C, Alvain S, Bopp L, Tagliabue A, Antoine D (2011) Large-scale shifts in phytoplankton groups in the Equatorial Pacific during ENSO cycles. Biogeosciences 8(3):539–550. https://doi.org/10.5194/bg-8-539-2011
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. Braz J Biol 70(3):825–829. https://doi.org/10.1590/S1519-69842010000400013
Matteucci SD, Colma A (1982) Metodología para el estudio de la vegetacion. Secretaria General de la Organizacion de los Estados Americanos, Washington, DC
Meichtry-de-Zaburlin 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
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
Mendoza-Carbajal L, Contreras D, Baylon M, Dominguez A, Valdivia E, Samanez Z, Johnson F, Salazar-Torres A (2022) Especies invasoras de Ceratium Schrank, 1973 (Dinophyceae: Ceratiaceae) en cuerpos de agua continentales de Perú. Rev Peru Biol 29(4):e23765. https://doi.org/10.15381/rpb.v29i4.23765
Mooney HA, Cleland EE (2001) The evolutionary impact of invasive species. Proc Natl Acad Sci USA 98:5446–5451. https://doi.org/10.1073/pnas.091093398
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
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
Naselli-Flores L (2003) Man-made lakes in Mediterranean semi-arid climate: the strange case of Dr Deep Lake and Mr Shallow Lake. Hydrobiologia 506:13–21. https://doi.org/10.1023/B:HYDR.0000008550.34409.06
NOAA - National Oceanic and Atmospheric Administration (2023) El Niño and La Niña. https://www.noaa.gov/education/resource-collections/weather-atmosphere/el-nino. Accessed 22 Aug 2023
Nishimura PY, Pompêo M, Moschini-Carlos V (2015) Invasive dinoflagellate Ceratium furcoides (Levander) Langhans in two linked tropical reservoirs. Ecologia de reservatórios e interfaces, 460. http://ecologia.ib.usp.br/reservatorios/PDF/Cap._10_Ceratium.pdf Accessed 1 Sept 2023
Olrik K (1994) Phytoplankton ecology. Determining factors for the distribution of phytoplankton in freshwaters and the sea. Denmark: Danish Environmental Protection Agency. Miljǿproject
Pacheco JP, Frizzera CI, Goyenola G, Teixeira-de-Mello F, Fosalba C, Baattrup-Pedersen A, Meerhoff M, Jeppesen E (2021) Invasion of Ceratium furcoides in subtropical lakes in Uruguay: Environmental drivers and fish kill record during its bloom. Biol Invasions 23:3597–3612. https://doi.org/10.1007/s10530-021-02600-w
Padisák J, Vasas G, Borics G (2016) Phycogeography of freshwater phytoplankton: traditional knowledge and new molecular tools. Hydrobiologia 764:3–27. https://doi.org/10.1007/s10750-015-2259-4
Pitcher GC, Krock B, Cembella AD (2011) Accumulation of diarrhetic shellfish poisoning toxins in the oyster Crassostrea gigas and the mussel Choromytilus meridionalis in 41 the southern Benguela ecosystem. Afr J Mar Sci 33(2):273–281. https://doi.org/10.2989/1814232X.2011.600372
Pollingher U, Zemel E (1981) In situ and experimental evidence of the influence of turbulence on cell division processes of Peridinium cinctum forma westii (Lemm) Lefevre. Br Phycol J 16(3):281–287. https://doi.org/10.1080/00071618100650301
Preuss S, Low M, Cassel-Lundhagen A, Berggren A (2014) Evaluating range-expansion models for calculating non-native species expansion rate. Ecol Evol 4(14):2812–2822. https://doi.org/10.1002/ece3.1106
Pringle CM (2001) Hydrologic connectivity and the management of biological reserves: a global perspective. Ecol Appl 11(4):981–998. https://doi.org/10.1890/1051-0761(2001)011[0981:HCATMO]2.0.CO;2
QGIS Geographic Information System (2023) Open-Source Geospatial Foundation Project. http://qgis.osgeo.org
R Development Core Team (2023) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.Rproject.org
Rehage JS, Blanchard JR (2016) What can we expect from climate change for species invasions? Fisheries 41(7):405–407. https://doi.org/10.1080/03632415.2016.1180287
Reynolds CS (2006) The ecology of phytoplankton (Ecology, Biodiversity and Conservation). Cambridge University Press, Cambridge
Reynolds CS, Huszar V, Kruk C, Naselli-Flores L, Melo S (2002) Towards a functional classification of the freshwater phytoplankton. J Plankton Res 24(5):417–428. https://doi.org/10.1093/plankt/24.5.417
Richardson DM, Bond WJ, Dean WRJ, Higgins SI, Midgley GF, Milton SJ, Powrie LW, Rutherford MC, Samways MJ, Schulze RE (2000) Invasive alien organisms and global change. Invasive species in a changing world. Island Press, Washington, DC, pp 303–349
Rio Grande do Sul (2023) Geografia. https://estado.rs.gov.br/geografia. Accessed 22 August 2023
Rodríguez MI, Busso F, Bustamante MA, Ruibal Conti AL, Ruiz M, Angelaccio CM (2005) Floraciones de algas en el Embalse San Roque (Córdoba). In: XX Congreso Nacional del Agua y III Simposio de Recursos Hídricos del Cono Sur, Mendoza, Argentina
Rojas-Castillo AO, Pereira L, Buffon P, Cardoso LS (2023) Drivers and ecology of Ceratium furcoides invasion of a Brazilian subtropical reservoir and its interaction with the phytoplankton community. Limnologica. https://doi.org/10.1016/j.limno.2023.126080
Rousseaux CS, Gregg WW (2012) Climate variability and phytoplankton composition in the Pacific Ocean. J Geophys Res: Oceans. https://doi.org/10.1029/2012JC008083
Salusso MM, Moraña LB (2014) Fitoplancton de embalses subtropicales del noroeste argentino. Gest Ambient 17(1):209–222
Santos-Wisniewski MJ, Silva LC, Leone IC, Laudares-Silva R, Rocha O (2007) First record of the occurrence of Ceratium furcoides (Levander) Langhans 1925, an invasive species in the hydroelectricity power plant Furnas Reservoir, MG, Brazil. Braz J Biol 67(4):791–793
SEMA – Secretaria do Meio Ambiente e Infraestrutura (2018) Decreto nº 53.885, de 16 de janeiro de 2018. Institui subdivisão das Regiões Hidrográficas do Estado do Rio Grande do Sul em Bacias Hidrográficas. https://sema.rs.gov.br/upload/arquivos/201803/08095109-decreto-53885-2017.pdf. Accessed 22 Aug 2023
SEMA – Secretaria do Meio Ambiente e Infraestrutura (2020) Nota Técnica nº 002/2020/DIPLA/DRHS: Inserção de municípios e bacias hidrográficas no Estado do Rio Grande do Sul. https://sema.rs.gov.br/upload/arquivos/202108/23155725-nt-dipla-2020-002-municipios-e-bacias.pdf Accessed 1 Sept 2023
SenckenbergDZMB (2018) Tillmann Fragilidium subglobosum engulfment feeding | dinoflagellates. July 17, 2018. [Video]. Youtube. https://www.youtube.com/watch?v=KFFsnHVlHyo. Accessed 19 Nov 2023
Sendra MD, Moschini-Carlos V, Pompêo ML, Sòria Perpiñà X, Soria García JM, Vicente Pedrós E (2022) Ceratium furcoides (Levander) Langhans in reservoirs at the Ebro watershed, Spain and Sao Paulo state, Brazil. Limnetica 41(2):219–234. https://doi.org/10.23818/limn.41.26
Severiano JS, Oliveira ES, Lucena-Silva D, Moura GC, Silva EA, Barbosa JEL (2021) 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 24:217–233. https://doi.org/10.1007/s10530-021-02641-1
Silva LC, Leone IC, Santos-Wisniewski MJ, 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
Silva WJ, Nogueira IS, Melo-Magalhães EM, 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. https://doi.org/10.1590/S2179-975X5917
Silva LN, Medeiros CM, Cavalcante KP, Cardoso LS (2019) Invasion and establishment of Ceratium furcoides (Dinophyceae) in an urban lake in Porto Alegre, RS, Brazil. Acta Bot Bras 33(4):654–663. https://doi.org/10.1590/0102-33062018abb0429
Silva KA, de Souza RG, de Oliveira Aparecido LE (2022) Forecasting El Niño and La Niña events using decision tree classifier. Theor Appl Climatol 148:1279–1288. https://doi.org/10.1007/s00704-022-03999-5
Silverio MJ, Montañez G, Fra E, Saracho M, Arjona M, Amaya S, Traccanna B (2009) Variación poblacional de Ceratium hirundinella (Dinophyceae) en Embalses Eutróficos de Catamarca (Argentina) y su relación con parámetros ambientales. Huayllu-Bios 3:13–31
Soto D, Lembeye G (1999) Factores que determinan la presencia y florecimiento de Ceratium hirundinella en lagos del sur de Chile: condiciones que impiden y facilitan la introducción de esta especie. In: Resúmenes del V Congreso Latinoamericano de Ficología, 23
Stefaniak K, Goldyn R, Kowalczewska-Madura K (2007) Changes of summer phytoplankton communities in Lake Swarzedzkie in the 2000–2003 period. Oceanol Hydrobiol Stud 36:77–85
Strayer DL (2010) Alien species in fresh waters: ecological effects, interactions with other stressors, and prospects for the future. Freshw Biol 55(1):152–174. https://doi.org/10.1111/j.1365-2427.2009.02380.x
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
Taylor F, Fukuyo Y, Larson J (1995) Taxonomy of harmful dinoflagellates. Man Harmful Mar Microalgae, UNESCO-IOC Man Guides 33:283–317
Thuiller W, Richardson DM, Midgley GF (2007) Will climate change promote alien plant invasions? In: Nentwig W (ed) Ecological studies, vol 193. Springer, Berlin, Heidelberg, pp 197–211. https://doi.org/10.1007/978-3-540-36920-2_12
Trenberth KE, Jones PD, Ambenje P, Bojariu R, Easterling D, Tank KA, Parker D, Rahimzadeh F, Renwick JA, Rusticucci M, Soden B, Zhai P (2007) Observations: Surface and Atmospheric Climate Change. In: Solomon SD, Qin M, Manning Z, Chen M, Marquis KB, Averyt M, Tignor, Miller HL (eds) Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA
Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11(12):1351–1363. https://doi.org/10.1111/j.1461-0248.2008.01250.x
Van Ginkel CE, Hohls BC, Vermaak EA (2001) Ceratium hirundinella (O.F. Muller) bloom in the Hartbeespoort Dam. South Africa. Water SA 27(2):269–276. https://doi.org/10.4314/wsa.v27i2.5000
Viana DS, Santamaría L, Figuerola J (2016) Migratory birds as global dispersal vectors. Trends in Ecol Evol 31(10):763–775. https://doi.org/10.1016/j.tree.2016.07.005
Vidal L, Kruk C (2008) Cylindrospermopsis raciborskii (Cyanobacteria) extends its distribution to Latitude 34 53’S: taxonomical and ecological features in Uruguayan eutrophic lakes. Pan-Am J Aquat Sci 3(2):142–151
Vilà M, Corbin JD, Dukes JS, Pino J, Smith SD (2007) Linking plant invasions to global environmental change. Terrestrial ecosystems in a changing world. Springer, Berlin Heidelberg, pp 93–102. https://doi.org/10.1007/978-3-540-32730-1_8
Walther GR, Roques A, Hulme PE, Sykes MT, Pyšek P, Kühn I, Zobel M, Bacher S, Botta-Dukát Z, Bugmann H, Czúcz B, Dauber J, Hickler T, Jarosík V, Kenis M, Klotz S, Minchin D, Moora M, Nentwig W, Ott J, Panov V, Reineking B, Robinet C, Semenchenko V, Solarz W, Thuiller W, Vilà M, Vohland K, Settele J (2009) Alien species in a warmer world: risks and opportunities. Trends Ecol Evol 24(12):686–693. https://doi.org/10.1016/j.tree.2009.06.008
WHSRN - Western Hemisphere Shorebird Reserve Network (2023) Lagoa do Peixe. www.whsrn.org/siteprofile/lagoa-do-peixe. Accessed 22 Aug 2023
Wieliczko AR, Crossetti LO, Cavalcanti JR, Hessel MS, da Motta-Marques D, Rodrigues LR (2021) Meteorological drivers and ENSO influence on phytoplankton biomass dynamics in a shallow subtropical lake. Environ Monit Assess 193:1–13. https://doi.org/10.1007/s10661-021-09288-4
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
Wit RD, Bouvier T (2006) Everything is everywhere, but, the environment selects’; what did Baas Becking and Beijerinck really say? Environ Microbiol 8(4):755–758. https://doi.org/10.1111/j.1462-2920.2006.01017.x
Wu JT, Chou JW (1998) Dinoflagellate associations in Feitsui Reservoir, Taiwan. Bot Bull Acad Sin 39:137–145
Acknowledgements
We would like to thank FAPERGS (Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul) and UFRGS (Universidade Federal do Rio Grande do Sul) for the undergraduate fellowship granted to the first author; Coordenação de Aperfeiçoamento de Pessoal de Nível Superior–Brasil (CAPES) for the postgraduate fellowship to the first author; and CORSAN (Companhia Riograndense de Saneamento), through Carla Cristine Müller, Karen Dornelles Scherer and Juliana Karl Frizzo, for providing the data to carry out this study. The English language review was done by Cary Collett. This study was financed, in part, by CAPES–Finance Code 001.
Funding
This work was supported by CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior–Brasil)–Finance Code 001 and funded by PROBIC (Programa Institucional de Bolsas de Iniciação Científica), FAPERGS (Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul), BIC (Bolsas de Iniciação Científica), and UFRGS (Universidade Federal do Rio Grande do Sul).
Author information
Authors and Affiliations
Contributions
RDS: Conceptualization, Methodology, Validation, Formal analysis, Investigation, Data curation, Writing—Original draft, Writing—Review & editing, Visualization; LMR: Methodology, Resources, Data curation; LSC: Conceptualization, Methodology, Validation, Formal analysis, Investigation, Resources, Writing—Review & editing, Funding acquisition, Project administration, Supervision.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no relevant financial or non-financial interests to disclose.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
da Silva, R.D., da Rosa, L.M. & de Souza Cardoso, L. Spread and persistence of the invasive dinoflagellate Ceratium furcoides (Levander) Langhans through South America: watersheds in Rio Grande do Sul, Brazil. Aquat Sci 86, 28 (2024). https://doi.org/10.1007/s00027-024-01042-5
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00027-024-01042-5