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Ceratium furcoides (Levander) Langhans: first record in Nova Avanhandava reservoir, Southeast Brazil1 1 Part of the Doctoral Thesis of the first Author

Ceratium furcoides (Levander) Langhans: primeiro registro no reservatório Nova Avanhandava, Sudeste do Brasil

ABSTRACT

This is the first record of Ceratium furcoides in the Nova Avanhandava reservoir, São Paulo, whose samples were collected in three stations (S1, S2, S3) in March and October of the years 2015 and 2016. Physico-chemical analyzes of the water were performed. The reservoir was classified, according to the TSI, as mesotrophic. The first record of the species occurred in October 2015 at S3 and, the following year, the dispersion for the other stations was verified. The highest density of the species (28 org mL-1) was recorded in October 2016. Similar values were documented in Furnas (MG) and Ilha Solteira (SP). The low density values of C. furcoides and the presence of phytoplankton groups with higher densities (Cyanobacteria and Cryptophyceae) suggest that the colonization of the species is at an early stage. Thus, studies about dispersion, dynamics, and interaction of C. furcoides with phytoplankton and the potential impacts on aquatic communities are essential to understand the responses of this species to environmental conditions.

Keywords:
adaptative strategies; bioinvasion; mesotrophic; net cages

RESUMO

Trata-se do primeiro registro de Ceratium furcoides no reservatório Nova Avanhandava, São Paulo, cuja as amostras foram coletadas em três estações (E1, E2, E3) em março e outubro dos anos de 2015 e 2016. Análises físico-químicas da água foram realizadas. O reservatório foi classificado, de acordo com o cálculo do IET como mesotrófico. O primeiro registro da espécie ocorreu em outubro de 2015 na E3 e, no ano seguinte, verificou-se a dispersão para as outras estações. A maior densidade da espécie (28 org mL-1) foi registrada em outubro de 2016. Valores semelhantes foram documentados em Furnas (MG) e Ilha Solteira (SP). Os baixos valores de densidade de C. furcoides e a presença de grupos fitoplanctônicos com densidades superiores (Cyanobacteria e Cryptophyceae), sugerem que a colonização da espécie está no início. Assim, estudos sobre a dispersão, dinâmica e interação de C. furcoides com o fitoplâncton e os potenciais impactos sobre as comunidades aquáticas são essenciais para entender as respostas desta espécie às condições ambientais.

Palavras-chave:
bioinvasão; estratégias adaptativas; mesotrófico; tanques-rede

Introduction

Reservoirs are habitats prone to bioinvasion, especially for ease of dispersion through the flow of water. The invasion of microscopic alien species in these environments is still poorly understood, and it is not possible to accurately estimate what impacts such species would promote to communities, including phytoplankton (Kastovsky et al. 2010Kastovsky, J., Hauer, T., Mares, J., Krautova, M., Besta, T., Komarek, J., Desortova, B., Hetesa, J., Hindakova, A., Houk, V., Janecek, E., Kopp, R., Marvan, P., Pumann, P., Skacelova, O. & Zapomelova, E. 2010. A review of the alien and expansive species of freshwater cyanobacteria and algae, a case study from the Czech Republic. Biological Invasions 12(10): 3599-3625., Silva et al. 2012Silva, L. C. D., Leone, I. C., Santos-Wisniewski, M. J. D., Peret, A. C., & Rocha, O. 2012. Invasion of the dinoflagellate Ceratium furcoides (Levander) Langhans 1925 at tropical reservoir and its relation to environmental variables. Biota Neotropica 12(2): 93-100.). However, based on studies of invasion of alien species in other environments, it is possible to predict that the establishment of an invasive species may result in changes in species composition, diversity, and dominance, and in primary production (Elbrächter 1999Elbrächter, M. 1999: Exotic flagellates of coastal North Sea waters. Helgol. Meeresunt 52: 235-242., Ricciardi & Kipp 2008Ricciardi, A., & Kipp, R. 2008. Predicting the number of ecologically harmful exotic species in an aquatic system. Diversity and Distributions 14(2): 374-380., Souza et al. 2009Souza, R. C. C. L. D., Calazans, S. H., & Silva, E. P. 2009. Impacto das espécies invasoras no ambiente aquático. Ciência e Cultura 61(1): 35-41., Vitule & Prodocimo 2012Vitule, J. R. S., & Prodocimo, V. 2012. Introdução de espécies não nativas e invasões biológicas. Estudos de Biologia 34(83).).

Species of the genus Ceratium are considered invasive in continental aquatic environments of South America (Silva et al. 2012Silva, L. C. D., Leone, I. C., Santos-Wisniewski, M. J. D., Peret, A. C., & Rocha, O. 2012. Invasion of the dinoflagellate Ceratium furcoides (Levander) Langhans 1925 at tropical reservoir and its relation to environmental variables. Biota Neotropica 12(2): 93-100., Pereira et al. 2013Pereira, H.M., Ferrier, S., Walters, M., Geller, G.N., Jongman, R.H.G., Scholes, R.J., Bruford,M.W., Brummitt, N., Butchart, S.H.M., Cardoso, A.C., Coops, N.C., Dulloo, E., Faith,D.P., Freyhof, J., Gregory, R.D., Heip, C., Höft, R., Hurtt, G., Jetz, W., Karp, D.S.,McGeoch, M.A., Obura, D., Onoda, Y., Pettorelli, N., Reyers, B., Sayre, R.,Scharlemann, J.P.W., Stuart, S.N., Turak, E., Walpole, M., Wegmann, M. 2013. Essential Biodiversity Variables. Science 339: 277-278., Cavalcante et al. 2016Cavalcante, K. P., de Souza Cardoso, L., Sussella, R., & Becker, V. 2016. Towards a comprehension of Ceratium (Dinophyceae) invasion in Brazilian freshwaters: autecology of C. furcoides in subtropical reservoirs. Hydrobiologia 771(1): 265-280., Crossetti et al. 2019Crossetti, L. O., de Campos Bicudo, D., Bini, L. M., Dala-Corte, R. B., Ferragut, C., & de Mattos Bicudo, C. E. 2019. Phytoplankton species interactions and invasion by Ceratium furcoides are influenced by extreme drought and water-hyacinth removal in a shallow tropical reservoir. Hydrobiologia 831(1): 71-85.). The species Ceratium furcoides (Levander) Langhans demonstrates easy adaptation to different temperatures, trophies and physical and chemical conditions of the water thus presenting rapid dispersal and establishment in tropical reservoirs, including Brazilian ones, whose records of the species have been frequent (Santos-Wisniewski et al. 2007Santos-Wisniewski,M. J., L. C. Silva, I. C. Leone, R. Laudares-Silva & O. Rocha. 2007. First record of the occurrence of Ceratium furcoides (Levander) Langhans 1925, an invasive species in the hydroelectricity power plant Furnas Reservoir, MG, Brazil. Brazilian Journal of Biology 67(4): 791-793., Matsumura-Tundisi et al. 2010Matsumura-Tundisi, T., Tundisi, J. G., Luzia, A. P., & Degani, R. M. 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., Oliveira et al. 2011Oliveira, H. S., 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., Cavalcante et al. 2013, Jati et al. 2014Jati, S., Rodrigues, L. C., Bortolini, J. C., Paula, A. C. M., Moresco, G. A., Reis, L. M., ... & Train, S. 2014. First record of the occurrence of Ceratium furcoides (Levander) Langhans (Dinophyceae) in the Upper Paraná River Floodplain (PR/MS), Brazil. Brazilian Journal of Biology 74(3): 235-236., Nishimura et al. 2015Nishimura, P. Y., Pompêo, M., & Moschini-Carlos, V. 2015. Invasive dinoflagellate Ceratium furcoides (Levander) Langhans in two linked tropical reservoirs. In: Pompêo, M., Moschini-Carlos, V., Nishimura, P. Y., Silva, S.C. & López Doval, J.C.[Eds.]. Ecologia de reservatórios e interfaces. Instituto de Biociências, USP, SP, pp. 132-142., Oliveira et al. 2016Oliveira, F.H.P.C., Macêdo, I.M.E., Moreira, C.H.P., Shinohara, N.K.S., Lira, O.O. and Ramalho, W.P. 2016. Occurrence of Ceratium furcoides (Levander) Langhans 1925 (Dinophyceae : Ceratiaceae) in two reservoirs of the Capibaribe watershed located in Semiarid region. Revista GEAMA 6(1): 25-33., Rosini et al. 2016Rosini, E. F., Tucci, A., do Carmo, C. F., Rojas, N. E. T., de Barros, H. P., & Mallasen, M. 2016. Changes in phytoplankton spatial and temporal dynamics in a Brazilian tropical oligotrophic reservoir after net cage installation. Brazilian Journal of Botany 39(2): 569-581., Campanelli et al. 2017Campanelli, L. C., Tundisi, J. G., Abe, D. S., Sidagis-Galli, C., & Matsumura-Tundisi, T. 2017. Record of the occurrence of dinoflagellate Ceratium furcoides in a fish farming lake located in the countryside of São Carlos (SP, Brazil). Brazilian Journal of Biology 77(2): 426-427., Silva et al. 2018, Roriz et al. 2019Roriz, P. D. R. C., Batista, B. D., & Fonseca, B. M. 2019. Primeiro registro da espécie invasora Ceratium furcoides (Levander) Langhans 1925 (Dinophyceae) no lago Paranoá, Distrito Federal. Oecologia Australis.).

The increase in the density of C. furcoides and the formation of blooms in tropical reservoirs is mainly associated with the availability of nutrients (Matsumura-Tundisi et al. 2010Matsumura-Tundisi, T., Tundisi, J. G., Luzia, A. P., & Degani, R. M. 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., Silva et al. 2012Silva, L. C. D., Leone, I. C., Santos-Wisniewski, M. J. D., Peret, A. C., & Rocha, O. 2012. Invasion of the dinoflagellate Ceratium furcoides (Levander) Langhans 1925 at tropical reservoir and its relation to environmental variables. Biota Neotropica 12(2): 93-100.). In this way, reservoirs that receive external loads of nutrients or where intensive activities are carried out, such as the creation of fish in net cages, become environments conducive to the mass development of the species in question. In this context, the aim of this work was to document the first occurrence of Ceratium furcoides in the Nova Avanhandava reservoir, one of the three main centers of the fish farm in State of São Paulo.

Materials and Methods

Ceratium furcoides (Levander) Langhans was identified from phytoplankton sampling carried out during the development of a doctorate degree project in which three reservoirs from the State of São Paulo with fish farms were sampled: Chavantes, Nova Avanhandava, and Ilha Solteira. In this study, we documented the first record of the species in Nova Avanhandava Reservoir.

Study area - The reservoir of the Nova Avanhandava Hydroelectric Plant (21°07’01” S and 50°12’06” W) is located in Buritama city and is in Baixo Tietê Basin (figure 1). It presents an area of 210 km2, a maximum depth of 30 m and residence time of 46 days. Nova Avanhandava is the penultimate reservoir of a system of consecutive lakes, with the reservoirs of Promissão upstream of it and Três Irmãos downstream.

Figure 1
Location of São Paulo State, Brazil and Nova Avanhandava reservoir (N.A.). In detail, the map of Nova Avanhandava reservoir showing the location of the three samplings stations (S1, S2, and S3).

Samplings were carried out in the subsurface of the water column in March and October of 2015 and of 2016 in three sampling stations (S1, S2 and S3) corresponding to the three different fish farms (f) of creation and their respective upstream areas (u) and downstream (d) (n = 28). S2 is located upstream of S3 and, consequently, only upstream and downstream were sampled for the two stations.

In situ measurements of dissolved oxygen (mg L-1), pH, water temperature (oC) and electrical conductivity (µS cm-1) were carried out by the EXO YSI multi-parameter probe. The water transparency (m) was estimated by the disappearance of the Secchi disk. (Esteves 2011Esteves, F.A. 2011. Fundamentos de Limnologia. 3. ed. Rio de Janeiro: Interciência. Rio de Janeiro.). The concentrations of total phosphorus (µg L-1) and total nitrogen (µg L-1) (Valderrama 1981Valderrama, J. C. 1981. The simultaneous analysis of total nitrogen and total phosphorus in natural waters. Marine Chemistry 10(2): 109-122.), orthophosphate (µg L-1) (Strickland & Parsons 1960Strickland, J. D. H., & Parsons, T. R. 1960. A Manual of Sea Water Analysis: With Special Reference to the More Common Micronutrients and to Particulate Organic Material (No. 125). Fisheries Research Board of Canada.), ammonium ion (µg L-1) (Apha et al. 2005APHA, Awwa. WEF. 2005. Standard methods for the examination of water and wastewater. 21st ed. Washington, D.C: APHA - American Public Health Association, AWWA - American Water Works Association, and WPCF - Water Pollution Control Federation, Estados Unidos.), nitrite (µg L-1) e nitrate (µg L-1) (Giné et al. 1980Giné, M. F., Zagatto, E. A. G., & Reis, B. F. 1980. Simultaneous determination of nitrate and nitrite by flow injection analysis. Analytica Chimica Acta 114: 191-197.) were determined. The Trophic State Index (TSI) was calculated according to Lamparelli (2004)Lamparelli, M. C. 2004. Graus de trofia em corpos d\’água do estado de São Paulo: avaliação dos métodos de monitoramento (Doctoral dissertation, Universidade de São Paulo)..

For the phytoplankton taxonomic study, the samples were obtained with 20 µm mesh plankton net and fixed in situ with formaldehyde in the final concentration of 4 to 5%. The phytoplankton community was identified using an optical microscope with a capture camera, specialized bibliography and measurements were obtained with the aid of the Axio Vision 4.8 program. The identification of the Ceratium furcoides species (n= 25) was performed according to Santos-Wieniewski et al. (2007) and Cavalcante et al. (2013)Cavalcante, K. P., Zanotelli, J. C., Müller, C. C., Scherer, K. D., Frizzo, J. K., Ludwig, T. A. V., & de Souza Cardoso, L. 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..

Samples referring to the first records of C. furcoides in the Nova Avanhandava reservoir are deposited in the collection of Herbário Maria Eneyda P. Kauffmann Fidalgo of the Institute de Botânica of São Paulo State.

Samples for quantitative analysis were collected with a Van Dorn bottle and fixed in situ with 1% Lugol solution. The count of the phytoplanktonic community and consequently of the populations of Ceratium furcoides was carried out by the method of Utermölh (1958)Utermölh. 1958. Zur vervollkommnung der quantative phyto-plankton-methodik. Mitteilungen aus Institut Verhein Lim-nologie 9:1-38. [For perfection of the quantitative phyto-plankton methodology].. The results of the densities were expressed in org mL-1 and the biomass was estimated by calculating the biovolume based on the work of Hillebrand et al. (1999)Hillebrand, H., Dürselen, C. D., Kirschtel, D., Pollingher, U., & Zohary, T. 1999. Biovolume calculation for pelagic and benthic microalgae. Journal of Phycology 35(2): 403-424. and Fonseca et al. (2014)Fonseca, B. M., Ferragut, C., Tucci, A., Crossetti, L. O., Ferrari, F., Bicudo, D. D. C., ... & Bicudo, C. E. D. M. 2014. Biovolume de cianobactérias e algas de reservatórios tropicais do Brasil com diferentes estados tróficos. Hoehnea 41(1): 9-30..

Descriptive statistics were performed: mean and standard deviation of limnological variables and nutrients.

Results

Nova Avanhandava presented at the sampling stations, high conductivity, neutral pH and temperature ranging between 23°C and 29 °C. As for the trophic level, the seasons were classified as mesotrophic in all samples (mean TSI: 59). The mean values of the physical, chemical and nutrient variables recorded at the sampling stations are presented in Table 1 and 2.

Table 1
Mean, minimum and maximum values of the physical. WT: Water Temperature; DO: Dissolved Oxygen; Cond.: Conductivity; Transp.: Transparency; Turb.: Turbidity and chemical variables; Chl α: Chlorophyll-α measured at the three samplings stations.
Table 2
Mean values and standard deviation of nutrients concentrations for the samplings stations in Nova Avanhandava reservoir, São Paulo State, Brazil, recorded in March and October 2015, and March and October 2016.

During the study period, we identified 156 taxa distributed in 12 taxonomic goups: Cyanobacteria (33 taxa), Chlorophyceae (33 taxa), Cryptophyceae (nine taxa), Bacillariophyceae (six taxa), Euglenophyceae (6 taxa), Trebouxiophyceae (6 taxa), Coscinodiscophyceae (4 taxa), Chrysophyceae (four taxa), Zygnemophyceae (four taxa), Dinophyceae (two taxa), Choanoflagellata (one taxa), Klebsormidiophyceae (one taxa).

Ceratium furcoides (Levander) Langhans (1925)Langhans, V.H. 1925. Gemischte Populationen von Ceratium hirundella (O.F.M) schrank und ihre Deutung. Archiv für Protistenkunde 52: 585-602.. Published in: Langhans, V.H. (1925). Gemischte Populationen von Ceratium hirundinella (O.F.M) schrank und ihre Deutung. Archiv für Protistenkunde 52: 585-602.

Basionym - C. hirundinella var. furcoides Levander

Figure 2

Figure 2
Specimens of Ceratium furcoides (Levander) Langhans found in Nova Avanhandava reservoir, São Paulo State, Brazil, in station S2 (SP470024 and SP470025). a. ventral view; b. dorsal view; c-d. lateral views.

Cells slightly fusiform, flattened dorsiventrally, 46-58 µm wide, 185-274 µm in length, reticulated plates. The epitheca is conical with a long horn formed above the cingulum, with four apical plates (1’,2’,3’ and 4’). The hypovalve is large and small, with two or three posterior horns of varied sizes formed by antapical plates (1’” and 2’”). Chloroplasts are oval-shaped and numerous. Planktonic habit.

Comments - Some specimens presented morphological variation characterized by the third horn, which makes them similar to C. hirundinella, however, Bourrelly (1970)Bourrelly, P. 1970. Les Algues D’eau Douce. Initiation à la Systématique. Tome III: Les Algues bleues et rouges, Les Eugléniens, Peridiniens et Cryptomonadines. Paris VI: Boubée & Cie. France. points out that variations in the number and size of horns are linked to environmental changes such as temperature. Thus, the confirmation of the C. furcoides populations was carried out observing that the fourth apical plate (4’) does not reach the apex of the epitheca.

Material examined - BRAZIL. São Paulo: Zacarias, Nova Avanhandava reservoir, 11-III-2016, A.Dias s.n. (SP470024); idem, 03-X-2015, A.Dias s.n. (SP470025); idem, 03-X-2015, A.Dias s.n. (SP470026); idem, 05-X-2016, A.Dias & A.Tucci s.n. (SP470027); idem, 05-X-2016, A.Dias & A.Tucci s.n. (SP470028).

Distribution - They occur from oligotrophic lakes and reservoirs to eutrophic ones. There are records of the species on all continents. (Guiry 2019Guiry, M.D. & Guiry, G.M. 2019. AlgaeBase. World-wide electronic publication, National University of Ireland. Galway. Available in http://www.algaebase.org. (access in 14-V-2019).
http://www.algaebase.org....
). In Brazil, there are records in almost all regions, except for the Northern Region (Flora do Brasil 2020Flora do Brasil 2020 (em construção). Dinophyceae. Jardim Botânico do Rio de Janeiro. Available in http://floradobrasil.jbrj.gov.br/reflora/floradobrasil/FB124330 (access in 14-V-2019).
http://floradobrasil.jbrj.gov.br/reflora...
- under construction, Silva et al. 2018Silva, W. J., Nogueira, I. S., Melo-Magalhães, E. M. M., Benício, S. H. M., Pessoa, S. M., & Menezes, M. 2018. Expansion of invasive Ceratium furcoides (Dinophyta) toward north-central Brazil: new records in tropical environments. Acta Limnologica Brasiliensia 30.).

The first occurrence of populations of C. furcoides in the Nova Avanhandava reservoir occurred in October 2015 (S2u) and remained in the other samples: March 2016 (S1u) e October 2016 (S1u, S2f1, S3f2). The density and biovolume of C. furcoides were low in comparison to the other organisms of the phytoplankton community recorded together, being the highest values (density: 28 org mL-1; biovolume: 0,442 mm³ L-1) for the species registered upstream of S1 (u), in October 2016 (figure 3 a-b).

Figure 3
Total density (org mL-1) (a.) and biovolume (mm3 L-1) (b.) of the Ceratium furcoides (Levander) Langhans in compared to phytoplanktonic classes at the six samplings stations (upstream: U, fish farm: F and downstream: D during the period of 2015 and 2016. On the left, scale of the phytoplankton community (bars graph). On the right, scale of the species Ceratium furcoides (area graph).

Discussion

Since its first occurrence of Ceratium furcoides in 2007 on Furnas reservoir in Minas Gerais, 13 new studies have been published, whose results document the dispersion of the species to all regions of Brazil, except the Northern Region (Santos-Wisniewski 2007Santos-Wisniewski,M. J., L. C. Silva, I. C. Leone, R. Laudares-Silva & O. Rocha. 2007. First record of the occurrence of Ceratium furcoides (Levander) Langhans 1925, an invasive species in the hydroelectricity power plant Furnas Reservoir, MG, Brazil. Brazilian Journal of Biology 67(4): 791-793., Matsumura-Tundisi et al. 2010Matsumura-Tundisi, T., Tundisi, J. G., Luzia, A. P., & Degani, R. M. 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., Oliveira et al. 2011Oliveira, H. S., 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., Pires et al. 2012Pires, D.A., Carvalho, M. C., Morandini, M. & Lamparelli, M. C. 2012. Ocorrência de Ceratium furcoides (Levander) Langhans 1925 em Reservatórios do Estado de São Paulo, SP-Brasil. Available in Anais do XIV Congresso Brasileiro de Ficologia <http://www.sbfic.org.br/cbfic2012/ocs-2.3.4/index.php/xivcbfic/congresso/paper/view/29> (access in 15-VII-2015).
http://www.sbfic.org.br/cbfic2012/ocs-2....
, Cavalcante et al. 2013Cavalcante, K. P., Zanotelli, J. C., Müller, C. C., Scherer, K. D., Frizzo, J. K., Ludwig, T. A. V., & de Souza Cardoso, L. 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., Cassol et al. 2014Cassol, A. P. V., Pereira Filho, W., Oliveira, M. A., Domingues, A. L., Correa, F. S. & Buriol, G. A. 2014. First record of a bloom of the invasive species Ceratium furcoides (Levander) Langhans 1925 in Rio Grande do Sul state, Brazil. Brazilian Journal of Biology 74: 515-517., Jati et al. 2014Jati, S., Rodrigues, L. C., Bortolini, J. C., Paula, A. C. M., Moresco, G. A., Reis, L. M., ... & Train, S. 2014. First record of the occurrence of Ceratium furcoides (Levander) Langhans (Dinophyceae) in the Upper Paraná River Floodplain (PR/MS), Brazil. Brazilian Journal of Biology 74(3): 235-236., Moreira et al. 2015Moreira, R.A., Rocha, O., Santos, R.M., Laudares-Silva, R., Dias, E.S. & 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). Brazilian Journal of Biology 75(1): 98-103., Nishimura et al. 2015Nishimura, P. Y., Pompêo, M., & Moschini-Carlos, V. 2015. Invasive dinoflagellate Ceratium furcoides (Levander) Langhans in two linked tropical reservoirs. In: Pompêo, M., Moschini-Carlos, V., Nishimura, P. Y., Silva, S.C. & López Doval, J.C.[Eds.]. Ecologia de reservatórios e interfaces. Instituto de Biociências, USP, SP, pp. 132-142., Cavalcante et al. 2016, Silva et al. 2018Silva, W. J., Nogueira, I. S., Melo-Magalhães, E. M. M., Benício, S. H. M., Pessoa, S. M., & Menezes, M. 2018. Expansion of invasive Ceratium furcoides (Dinophyta) toward north-central Brazil: new records in tropical environments. Acta Limnologica Brasiliensia 30., Crossetti et al., 2019Crossetti, L. O., de Campos Bicudo, D., Bini, L. M., Dala-Corte, R. B., Ferragut, C., & de Mattos Bicudo, C. E. 2019. Phytoplankton species interactions and invasion by Ceratium furcoides are influenced by extreme drought and water-hyacinth removal in a shallow tropical reservoir. Hydrobiologia 831(1): 71-85., Roriz et al. 2019Roriz, P. D. R. C., Batista, B. D., & Fonseca, B. M. 2019. Primeiro registro da espécie invasora Ceratium furcoides (Levander) Langhans 1925 (Dinophyceae) no lago Paranoá, Distrito Federal. Oecologia Australis.). In the State of São Paulo, the specie has been registered on the reservoirs: Billings (Matsumura-Tundisi et al. 2010), Barra Bonita, Itupararanga and Mirinheirinho (Pires et al. 2012), Billings and Guarapiranga (Nishimura et al., 2015), Jaguari e Jacareí (Hackbart et al., 2015Hackbart, V. C. S., Marques, A. R. P., Kida, B. M. S., Tolussi, C. E., Negri, D. D. B., Martins, I. A., ... & Silva, S. C. D. 2015. Avaliação expedita da heterogeneidade espacial horizontal intra e inter reservatórios do sistema Cantareira (represas Jaguari e Jacarei, São Paulo). Ecologia de reservatórios e interfaces. São Paulo: Instituto de Biociências da Universidade de São Paulo. 96-108.), Ilha Solteira (Rosini et al., 2016Rosini, E. F., Tucci, A., do Carmo, C. F., Rojas, N. E. T., de Barros, H. P., & Mallasen, M. 2016. Changes in phytoplankton spatial and temporal dynamics in a Brazilian tropical oligotrophic reservoir after net cage installation. Brazilian Journal of Botany 39(2): 569-581.), Lago das Garças (Crossetti et al., 2019). This work is the first record of the occurrence of the species for the Nova Avanhandava reservoir in the State of São Paulo, Southeastern Region.

The records of C. furcoides in such distinct aquatic environments demonstrate the great ecophysiological plasticity of the species. In addition, Ceratium presents important adaptive strategies for the development and establishment in tropical reservoirs such as encystment (resistance to sedimentation, dispersion capacity, population survival), mobility and low predation by zooplankton (Hickel 1988Hickel, B. 1988. Sexual reproduction and life cycle of Ceratium furcoides (Dinophyceae) in situ in the lake Plubsee (F.R.). Hydrobiologia 161: 41-48., Pollingher 1988Pollingher, U. 1988. Freshwater armored dinoflagellates: growth, reproduction strategies, and population dynamics. Growth and reproductive strategies of freshwater phytoplankton. 134-174., Xie et al. 1998Xie, P., T. Iwakuma & K. Fujii. 1998. Changes in the structure of a zooplankton community during a Ceratium (Dinoflagellate) bloom in a eutrophic fishless pond. Journal of Plankton Research 20: 1663-1678., Cavalcante et al. 2016Cavalcante, K. P., de Souza Cardoso, L., Sussella, R., & Becker, V. 2016. Towards a comprehension of Ceratium (Dinophyceae) invasion in Brazilian freshwaters: autecology of C. furcoides in subtropical reservoirs. Hydrobiologia 771(1): 265-280.).

We do not have results that indicate concretely how the species was introduced into the reservoir in question, but we considered a passive dispersion of cysts or specimens from Barra Bonita reservoir, whose species had previously been recorded by Pires et al. (2012)Pires, D.A., Carvalho, M. C., Morandini, M. & Lamparelli, M. C. 2012. Ocorrência de Ceratium furcoides (Levander) Langhans 1925 em Reservatórios do Estado de São Paulo, SP-Brasil. Available in Anais do XIV Congresso Brasileiro de Ficologia <http://www.sbfic.org.br/cbfic2012/ocs-2.3.4/index.php/xivcbfic/congresso/paper/view/29> (access in 15-VII-2015).
http://www.sbfic.org.br/cbfic2012/ocs-2....
, carried by the water flow of the central body of the reservoir where the endorheic river Tietê flows. However, other forms of dispersal should also be considered: transport of specimens or their form of resistance attached to birds and aquatic insects moving between reservoirs or by anthropic intervention, as mentioned by Kristiansen (1996)Kristiansen, J. 1996. Dispersal of freshwater algae - a review. Hydrobiologia 336: 151 - 157. and Meichtry et al. (2014)Meichtry, N. Z., Boltovskoy, A., Rojas, C. C. & Rodriguez, R. M. 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. or consider Ceratium propagules already existing in the sediment, but which only now did they become available for invasion (Reynolds 1996, Rengefors et al. 2004, Padisàk 2010).

The literature indicates that some limnological variables are essential in the establishment of populations of C. furcoides. Thus, it has been observed the dominance of dinoflagellates, including the Ceratium genus in mesotrophic conditions (Periotto et al. 2007Periotto, M., Prósperi, C., Daga, C. & Rincón, A. 2007. Estudio de Ceratium hirundinella en El Embalse La Quebrada, Córdoba, Argentina. In: International Congress on Development Environment and Natural Resources: Multi-level and Multi-scale Sustainability. Cochabamba, Bolívia., Santos-Wisniewskis et al. 2007Santos-Wisniewski,M. J., L. C. Silva, I. C. Leone, R. Laudares-Silva & O. Rocha. 2007. First record of the occurrence of Ceratium furcoides (Levander) Langhans 1925, an invasive species in the hydroelectricity power plant Furnas Reservoir, MG, Brazil. Brazilian Journal of Biology 67(4): 791-793., Silva et al. 2018Silva, W. J., Nogueira, I. S., Melo-Magalhães, E. M. M., Benício, S. H. M., Pessoa, S. M., & Menezes, M. 2018. Expansion of invasive Ceratium furcoides (Dinophyta) toward north-central Brazil: new records in tropical environments. Acta Limnologica Brasiliensia 30.) and development of C. furcoides between 10° e 25°C (Cassol et al. 2014Cassol, A. P. V., Pereira Filho, W., Oliveira, M. A., Domingues, A. L., Correa, F. S. & Buriol, G. A. 2014. First record of a bloom of the invasive species Ceratium furcoides (Levander) Langhans 1925 in Rio Grande do Sul state, Brazil. Brazilian Journal of Biology 74: 515-517., Cavalcante et al. 2016Cavalcante, K. P., de Souza Cardoso, L., Sussella, R., & Becker, V. 2016. Towards a comprehension of Ceratium (Dinophyceae) invasion in Brazilian freshwaters: autecology of C. furcoides in subtropical reservoirs. Hydrobiologia 771(1): 265-280.) and recurrence of the species in environments with high transparency associated with lower stability of the water column and also at high concentrations of ammonia and nitrite.

New Avanhandava is one of the three largest fish farming centers of São Paulo and as well as all economic activity fish farming is likely to cause pollution in the environment. In this case, the continuous and pronounced nutrient discharge from fish feeds and metabolism effectively alter the phytoplankton community, favoring the development of certain groups over the decrease of others, as well as favoring the establishment of invasive species (Mack et al. 2000Mack, R. N. 2000. Cultivation fosters plant naturalization by reducing environmental stochasticity. Biological Invasions , 2(2): 111-122., Degefu et al. 2011Degefu, F., Mengistu, S., & Schagerl, M. 2011. Influence of fish cage farming on water quality and plankton in fish ponds: A case study in the Rift Valley and North Shoa reservoirs, Ethiopia. Aquaculture. 316(1-4): 129-135.).

In this study, the maximum value of density and biovolume of C. furcoides was, respectively, 28 org mL-1 and 0,442 mm3 L-1 recorded in S1(Oct/16). Density values are extremely low compared to densities in other São Paulo reservoirs recorded by Matsumura-Tundisi et al. (2010)Matsumura-Tundisi, T., Tundisi, J. G., Luzia, A. P., & Degani, R. M. 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. (535 ind.mL-1) on the Taquacetuba arm at the Billings dam or by Hackbart et al. (2015)Hackbart, V. C. S., Marques, A. R. P., Kida, B. M. S., Tolussi, C. E., Negri, D. D. B., Martins, I. A., ... & Silva, S. C. D. 2015. Avaliação expedita da heterogeneidade espacial horizontal intra e inter reservatórios do sistema Cantareira (represas Jaguari e Jacarei, São Paulo). Ecologia de reservatórios e interfaces. São Paulo: Instituto de Biociências da Universidade de São Paulo. 96-108. on Jaguari dam (131.954,0 ind.mL-1) and low biomass compared to the records of Nishimura et al. (2015)Nishimura, P. Y., Pompêo, M., & Moschini-Carlos, V. 2015. Invasive dinoflagellate Ceratium furcoides (Levander) Langhans in two linked tropical reservoirs. In: Pompêo, M., Moschini-Carlos, V., Nishimura, P. Y., Silva, S.C. & López Doval, J.C.[Eds.]. Ecologia de reservatórios e interfaces. Instituto de Biociências, USP, SP, pp. 132-142. on Billings dam (5,7 mm3 L-1) and on Guarapiranga (2,6 mm3 L-1), of Rosini et al. (2016)Rosini, E. F., Tucci, A., do Carmo, C. F., Rojas, N. E. T., de Barros, H. P., & Mallasen, M. 2016. Changes in phytoplankton spatial and temporal dynamics in a Brazilian tropical oligotrophic reservoir after net cage installation. Brazilian Journal of Botany 39(2): 569-581. on Ilha Solteira (15,698 mm3 L-1) and of Crossetti et al. (2019)Crossetti, L. O., de Campos Bicudo, D., Bini, L. M., Dala-Corte, R. B., Ferragut, C., & de Mattos Bicudo, C. E. 2019. Phytoplankton species interactions and invasion by Ceratium furcoides are influenced by extreme drought and water-hyacinth removal in a shallow tropical reservoir. Hydrobiologia 831(1): 71-85. on Lago das Garças (12,3 µg L-1).

Based on the limnological and phytoplankton community results obtained and based on reports in the literature of limnological conditions of the others Brazilian environments in which C. furcoides has been registered, it can be said that Nova Avanhandava has environmental conditions favorable to the adaptive success of the species since both the maximum density and the peaks above 15 org mL-1 of C. furcoides recorded in Oct/15 (u and f1 of S1) and Oct/16 (u S1 and f2 S3) were associated with high values of electrical conductivity and at temperatures of 24° C and high dissolved inorganic nitrogen values, principally in the fish farm areas. However, the low density and biovolume values, as well as the absence of C. furcoides in other sampled compartments, suggest that the colonization of the species is at an early stage.

At first, were not observed changes of phytoplankton due to the presence of C. furcoides on this aquatic environment, it was found that other phytoplankton groups (Cyanobacteria and Cryptophyceae) showed high densities / biovolumes compared to C. furcoides, which corroborates the hypothesis that the species is in the process of colonization of the reservoir, establishing competition with the other species for nutrients due to its migration capacity vertical in the water column (Stephaniak et al. 2007Stephaniak, K., Goldyn, R. & Kowalczewska-Madura, K. 2007. Changes of summer phytoplankton communities in Lake Swarzedzkiein the 2000-2003 period. International Journal of Oceanography and Hydrobiology 36(1): 77-85., Cassol et al. 2014Cassol, A. P. V., Pereira Filho, W., Oliveira, M. A., Domingues, A. L., Correa, F. S. & Buriol, G. A. 2014. First record of a bloom of the invasive species Ceratium furcoides (Levander) Langhans 1925 in Rio Grande do Sul state, Brazil. Brazilian Journal of Biology 74: 515-517., Moreira et al. 2015Moreira, R.A., Rocha, O., Santos, R.M., Laudares-Silva, R., Dias, E.S. & 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). Brazilian Journal of Biology 75(1): 98-103., Almanza et al. 2016Almanza, V., Bicudo, C. E. M., 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.).

Punctual records in different environments and some possible equivocal identifications of Ceratium species may be underestismating the invasion of the species in the Brazilian territory since the species demonstrate a great capacity of dispersion and adaptation to different conditions. Thus, a greater number of studies in aquatic environments with similar limnological conditions and consequently their sediments (to verify the presence of cysts) could indicate if C. furcoides is already dispersed but not yet registered. From our results, we can suggest more specific studies in the Nova Avanhandava reservoir that establish the dispersion forms of Ceratium furcoides as well as studies that identify the closest aquatic environments that are favorable to the bioinvasion of the species and later studies to understand the relationships with the other groups of phytoplanktonic algae in addition to evaluating the consequences of establishing the species for the ecosystem.

  • 1
    Part of the Doctoral Thesis of the first Author

Acknowledgments

The authors would like to thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - CAPES, for funding the Doctorate degree of the first Author; to thank the Fundação de Amparo à Pesquisa do Estado de São Paulo - FAPESP (Grant 2013/50504-5), for funding the IMPCON Thematic Project of which the Doctoral Project was part; and all integrants of IMPCON Group, especially the coordinator Reinaldo José da Silva.

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Publication Dates

  • Publication in this collection
    09 Oct 2020
  • Date of issue
    2020

History

  • Received
    01 July 2019
  • Accepted
    07 May 2020
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