Temporal occurrence of Ceratium furcoides (Dinophyceae: Ceratiaceae) during an extreme drought season in Pernambuco state, Northeast Brazil

Carlos Yure B. Oliveira Ayanne Jamyres Gomes da Silva Almeida Cicero Diogo Lins de Oliveira Alfredo Olivera Galvez Danielli Matias de Macedo Dantas About the authors

Abstract

Ceratium furcoides is an invasive species that has caused ecological imbalance in several reservoirs in Brazil. This study investigates the main factors that may favor the occurrence of Ceratium furcoides blooms in a tropical reservoir from the Northeast Brazil, during an extreme drought season. Samples containing phytoplankton were collected monthly from February to September 2017. Quantitative analysis of C. furcoides was performed and the cell volume was estimated using geometric formulas. Mean biovolume of C. furcoides showed significant differences, ranging from 0.78 mm3 L-1 to 11.29 mm3 L-1 reported in March and September, respectively. Environmental parameters presented low oscillation throughout the study, except the conductivity. Significant relationships among the C. furcoides biovolume, water temperature and soluble reactive phosphate were observed. The findings reported here suggest that adverse conditions caused by a drought season did not negatively affect this species.

Key words:
bioinvasion; dinoflagellate blooms; drought season; phytoplankton; reservoirs

Resumo

Ceratium furcoides é uma espécie invasora que tem causado desequilíbrio ecológico em vários reservatórios no Brasil. Este estudo investiga os principais fatores que podem favorecer a ocorrência de florações de C. furcoides em um reservatório tropical do Nordeste do Brasil, durante um período de seca extrema. Amostras contendo fitoplâncton foram coletadas mensalmente de fevereiro a setembro de 2017. Análises quantitativas de C. furcoides foram realizadas e o volume celular estimado por meio de fórmulas geométricas. O biovolume médio de C. furcoides apresentou diferenças significativas, variando de 0,78 mm3 L-1 a 11,29 mm3 L-1 relatado em março e setembro, respectivamente. Os parâmetros ambientais apresentaram baixa oscilação ao longo do estudo, exceto a condutividade. Relações significativas entre o biovolume de C. furcoides, temperatura da água e fosfato reativo solúvel foram observadas. Os resultados relatados aqui sugerem que as condições adversas causadas por uma estação de seca não afetam negativamente esta espécie.

Palavras-chave:
bioinvasão; florações de dinoflagelados; período de seca; fitoplâncton; reservatórios

Introduction

Invasive species represent serious problems to communities and endemic species, due to their ability of irreversibly changing ecological functioning of ecosystems (Simberloff 1996Simberloff D (1996) Impacts of introduced species in the United States. Consequences 2: 13-22.).

Increase in occurrence of biological invasions, associated to climate change, is becoming a prevailing situation worldwide, thus causing serious threats to biodiversity (Vitousek et al. 1997Vitousek PM, Mooney HA, Lubchenco J & Melillo JM (1997). Human domination of Earth’s ecosystems. Science 277: 494-499.; Traveset & Richardson 2014Traveset A & Richardson DM (2014) Mutualistic interactions and biological invasions. Annual Review of Ecology, Evolution, and Systematics 45: 89-113.). Success of dominance organisms depends on many factors, including their ability to survive under unfavorable conditions and their adaptability to new environments (García-Berthou et al. 2005García-Berthou E, Alcaraz C, Pou-Rovira Q, Zamora L, Coenders G & Feo C (2005) Introduction pathways and establishment rates of invasive aquatic species in Europe. Canadian Journal of Fisheries and Aquatic Sciences 62: 453-463.).

Dinoflagellates are a eukaryotic group of microalgae common in both marine and freshwater environments (Saldarriaga & Taylor 2017Saldarriaga JF & Taylor FJR (2017) Dinoflagellata. In: Archibald J, Simpson A & Slamovits C (eds.) Handbook of the Protists. Springer, Cham. Pp. 625-678.). Currently, there are about 250–300 freshwater dinoflagellates species known worldwide (Carty & Parrow 2015Carty S & Parrow MW (2015) Dinoflagellates. In: Wehr JD & Sheath RG (eds.) Freshwater algae of North America: ecology and classification. Academic Press, Boston. Pp. 773-807.). Ceratium genus is normally found in nutrient-rich waters, especially in phosphate and nitrate, and it was not a common component of freshwater phytoplankton in South America until the 2000s (Lund 1965Lund JWG (1965) The ecology of the freshwater phytoplankton. Biological Reviews 40: 231-290.; Cavalcante et al. 2016Cavalcante 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.). Recently, occurrence of this invasive dinoflagellate in South American freshwater ecosystems has caught the attention of the scientific community. Ceratium species have asymmetrical cells, and there are only seven species in inland waters (Popovský & Pfiester 1990Popovský J & Pfiester LA (1990) Dinophyceae (Dinoflagellida). In: Ettl H, Gerloff J, Heyning, H & Mollenhauer D (eds.) Das Süswasserflora von Mitteleuropa. Gustav Fischer Verlag, Stuttgart. 263p.). In fact, only Ceratium furcoides (Levander) Langhans and Ceratium hirundinella (O.F.Müller) Dujardin has been recorded in Brazil so far (Santos-Wisniewski et al. 2007Santos-Wisniewski M, Silva L, Leone I, 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. Brazilian Journal of Biology 67: 791-793.; Cavalcante et al. 2013Cavalcante KP, Zanotelli JC, Müller CC, Scherer KD, Frizzo JK, Ludwig TAV & Cardoso LDS (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: 862.; Oliveira et al. 2019Oliveira CY, Oliveira CD, Almeida AJ, Gálvez AO & Dantas DM (2019) Phytoplankton responses to an extreme drought season: a case study at two reservoirs from a semiarid region, northeastern Brazil. Journal of Limnology 78: 176-184.). Several authors reported the occurrence of this genus (Padisák 1985Padisák J (1985) Population dynamics of the freshwater dinoflagellate Ceratium hirundinella in the largest shallow lake of Central Europe, Lake Balaton, Hungary. Freshwater Biology 15: 43-52.; Wu & Chou 1998Wu JT & Chou JW (1998) Dinofagellate associations in Feitsui Reservoir, Taiwan. Botanical Bulletin of Academia Sinica 39: 137-145.; Whittington et al. 2000Whittington J, Sherman B, Green D & Oliver RL (2000) Growth of Ceratium hirundinella in a subtropical Australian reservoir: the role of vertical migration. Journal of Plankton Research 22: 1025-1045.; Oliveira et al. 2011Oliveira HSB, Moura ADN & Cordeiro-Araújo MK (2011) First record of Ceratium Schrank, 1973 (Dinophyceae: Ceratiaceae) in freshwater ecosystems in the semiarid region of Brazil. Check List 7: 626.; Gil et al. 2012Gil CB, 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 Limnologica Brasiliensia 24: 207-219.; Campanelli et al. 2017Campanelli LC, Tundisi JG, Abe DS, Sidagis-Galli C & Matsumura-Tundisi T (2017) Record of the occurrence of dinofagellate Ceratium furcoides in a fish farming lake located in the countryside of São Carlos (SP, Brazil). Brazilian Journal of Biology 77: 426-427.; Roriz et al. 2019Roriz PDRC, Batista BD & Fonseca BM (2019) Primeiro registro da espécie invasora Ceratium furcoides (Levander) Langhans 1925 (Dinophyceae) no Lago Paranoá, Distrito Federal. Oecologia Australis 23: 620-635.). Even in cases of not toxic algae as, Ceratium species biomass may be harmful to the fishes and crustaceans due to the high oxygen consumption by bacteria decomposers during bloom decay (Smayda 1997Smayda TJ (1997) What is a bloom? A commentary. Limnology & Oceanography 42: 1132-1136.).

Reservoirs are important aquatic bodies used to drinking water supply to regions that are affected by long drought seasons. The dynamics of the communities that inhabit these aquatic bodies, may be directly linked with drought events (Lacerda et al. 2018Lacerda LD, Santos JA, Marins RV & Silva FATF (2018) Limnology of the largest multi-use artifcial reservoir in NE Brazil: The Castanhão Reservoir, Ceará state. Anais da Academia Brasileira de Ciências 90: 2073-2096.; Crossetti et al. 2019Crossetti LO, Campos Bicudo D, Bini LM, Dala-Corte RB, Ferragut C & Mattos Bicudo CE (2019) Phytoplankton species interactions and invasion by Ceratium furcoides are infuenced by extreme drought and water-hyacinth removal in a shallow tropical reservoir. Hydrobiologia 831: 71-85.). The invasion and dominance by C. furcoides in a tropical semiarid reservoir (located at the state of Pernambuco, Northeastern Brazil) was reported by Oliveira et al. (2019)Oliveira CY, Oliveira CD, Almeida AJ, Gálvez AO & Dantas DM (2019) Phytoplankton responses to an extreme drought season: a case study at two reservoirs from a semiarid region, northeastern Brazil. Journal of Limnology 78: 176-184.. In addition, these authors showed the nine species occurrence, in addition to Ceratium, ecological indices and multivariate relationships with environmental parameters. However, it could be observed that the other species biomass present at the same reservoir was not significant when compared to Ceratium biomass. In this sense, the goal of the present study was to examine the same data set reported in Oliveira et al. (2019)Oliveira CY, Oliveira CD, Almeida AJ, Gálvez AO & Dantas DM (2019) Phytoplankton responses to an extreme drought season: a case study at two reservoirs from a semiarid region, northeastern Brazil. Journal of Limnology 78: 176-184. using univariate analyses focusing on how extreme drought season can affect the occurrence of this invasive species.

Materials and Methods

Study area

The present study was carried out at the Cachoeira II reservoir (07°58’12”S, 38°19’52”W) (Fig. 1) located in the state of Pernambuco, Northeast Brazil. This reservoir has a 21,031,000 m3 of water capacity, but due to a long period of drought before and during this study, the reservoirs were at low levels. According to the Departamento Nacional de Obras Contra as Secas (DNOCS, Brazilian Department of Constructions Against Droughts), since January 2017 this reservoir is at less than 1% of its maximum capacity.

Figure 1
Map of study area, showing the municipalities in Pernambuco state, Brazil, and the Cachoeira II reservoir located in Serra Talhada city (highlight point). The reservoir area during the study is represented by the gray color.

Sampling procedures

Samples containing phytoplankton were collected, between February and September 2017, in three different points, monthly during daytime (approx. at 10 a.m.). In October 2017, this reservoir was completely dry, making it impossible to continue sampling for this study. Vertical sampling (with bottles) were carried out at an average depth of 0.5m.

Environmental variables

Water temperature, pH and conductivity parameters were measured in situ, at the same point of the plankton sampling, with a multiparameter probe (HI 9829 model, Hanna Instruments Lda., Portugal). Water samples were collected from the lake surface for chemical analysis. Nitrate (NO3), nitrite (NO2) and ammonia (NH4) levels were evaluated by spectrometry with wavelengths ranging from 420 to 630nm, using Alpha’s colorimetric test kits. Soluble reactive phosphate (SRP) analyses were performed, following the ascorbic acid method (APHA 2012APHA (2012) Standard methods for the examination of water and wastewater. 22nd edition. American Public Health Association, Washington D.C. 1360p.). Rainfall data were obtained from Serra Talhada-A350 meteorological station (OMM: 81912 at ca. 7 km from reservoir), available from the National Institute of Meteorology website (INMET 2018INMET - Instituto Nacional de Meteorologia (2018) BDMEP - Banco de dados meteorológicos para ensino e pesquisa. Available at http://www.inmet.gov.br. Access on 13 July 2018.
http://www.inmet.gov.br...
).

Rainfall data showed that 2017 was an atypical year for Serra Talhada city (Fig. 2). Highest recorded rainfall was 125.0 mm on July 2017. In August and September 2017, the same volumes (2.4 mm) were recorded, the lowest values recorded in this study. These data are opposite to the historical average (last 30 years) for this region, when rainfall highest occurred between January and March.

Figure 2
Monthly and historical (last 30 years) rainfall (mm) at the Serra Talhada-A350 meteorological station (OMM: 81912) at ca. 7 km from Cachoeira II reservoir.

Data analysis

Samples for quantitative phytoplankton analysis were taken and were immediately fixed with formaldehyde (4%). The species was identified according to Popovský & Pfiester (1990)Popovský J & Pfiester LA (1990) Dinophyceae (Dinoflagellida). In: Ettl H, Gerloff J, Heyning, H & Mollenhauer D (eds.) Das Süswasserflora von Mitteleuropa. Gustav Fischer Verlag, Stuttgart. 263p.. Quantitative analyses were conducted on three water samples from different collection points, with an optical microscope binocular (model BA300, Motic®, China), and a Sedgwick-Rafter (ind mL-1), the species were counted at 400x of magnification. After the sample was added to the chamber, it was left resting for 15 min for a complete sedimentation of the specimens.

For cell volume (µm3) calculation, twenty specimens of C. furcoides, randomly selected, were measured. The cell volume was estimated using geometric formulas adapted from Cavalcante et al. (2018)Cavalcante KP, Becker V & Cardoso LS (2018) A proxy for estimating the cell volume of Ceratium furcoides (Dinophyceae): basis for monitoring Brazilian reservoirs. Lakes & Reservoirs: Research & Management 23: 168-171., where the cell has the shape: ellipsoid + 2 cones + cylinder (Fig. 3) and its volume is determined by formula: V=π4.a2.b22+π12.a3.b32+π12a4.b42+π6.a1.b1.b2

Figure 3
Dimensions evaluated for each Ceratium furcoides cell. a = length, b = width. Scale bar: 40 µm

Monthly biovolume of C. furcoides was estimated by multiplying cell density (obtained in the Sedgwick-Rafter chamber) by the mean cell volume.

In the present study, we arbitrarily assumed bloom cells densities above 100 cells mL-1, because from this threshold had a distinct ecological importance at the Cachoeira II reservoir on the same studied period (Oliveira et al. 2019Oliveira CY, Oliveira CD, Almeida AJ, Gálvez AO & Dantas DM (2019) Phytoplankton responses to an extreme drought season: a case study at two reservoirs from a semiarid region, northeastern Brazil. Journal of Limnology 78: 176-184.).

Statistical analysis

One-way analysis of variance (ANOVA) was carried out to test monthly differences of biovolume with a post hoc Tukey’s test to compare means (Zar 2013Zar JH (2013) Biostatistical analysis: pearson new international edition. 5th ed. Pearson Education Limited, Harlow. 760p.). Linear regressions (data log transformed) was performed to identify the influence of the environmental variables on biovolume of C. furcoides. Statistical analyses were performed at 5% significance level on Statistics version 6.0 (Statsoft Inc., USA).

Results

Environmental variables are showed in Table 1. The highest and lowest water temperature values were measured in April and July 2017 (26.78 and 22.03 ºC, respectively). The gradual reduction in the water temperature observed between March and July 2017 is related to the increase in the reservoir volume caused by the rains. Even though there was a variation of more than 4 ºC, no significant differences were observed (p = 0.496). The pH recorded was 8.08 ± 0.38 with no significant differences throughout the study (p = 0.489). Variations in NH4 (p = 0.417), NO2 (p = 0.58), NO3 (p = 0. 154), and SRP (p = 0.327) did not significant differences during the study months. Only conductivity data presented statistical differences (p < 0.001) in this study.

Table 1
Range, mean and standard deviation (n = 24) of environmental variables of Cachoeira II reservoirs, during Ceratium furcoides occurrence in 2017.

Ceratium furcoides was recorded in all months of this study; in February at an average density of 150 ± 32 cells mL-1 fallowed by an 80% bloom-decay in March (Fig. 4). The highest densities were reported in September (435 ± 31 cells mL-1), August (400 ± 28 cells mL-1) and June (370 ± 32 cells mL-1). As the biovolumes for the 20 cells counted each month did not present significant differences (p = 0.674) among the months of the study, the monthly biovolume showed similarity with cell density. As with cell density, higher biovolumes was reported in September (11.29 mm3 L-1) and August (10.38 ± 0.70 mm3 L-1), followed by 9.60 ± 1.09 mm3 L-1 reported in June.

Figure 4
Biovolume (mm3 L-1) and cell density (cells mL-1) of Ceratium furcoides during February-September 2017 in Cachoeira II reservoir, Brazil. Data presented in mean ± standard deviation. Equivalent letters indicate statistical equality (p < 0.05) using one-way ANOVA (Kruskal-Wallis test) followed by the Tukey’s test.

Direct and inverse relations among abiotic and biovolume suggested some preferences during this drought season. The determination coefficient in linear regression between C. furcoides and water temperature (R2 = -0.738; p = 0.008) was the most significant in this study. In addition, correlations with SRP (R2 = 0.707; p = 0.009) was also significant. However, while the correlation with SRP was positive, with water temperature it was negative (Fig. 5).

Figure 5
Linear regression between Ceratium furcoides biovolume and the environmental variables. Data normalized by Log + 1. Temp = temperature; Cond = conductivity; Rain = rainfall; Biov = biovolume.

Discussion

Several factors are associated with the dispersion of phytoplankton species and may positively contribute to invasion success. These are: independent wind mediated dispersion, which enables spore transportation and high contamination of water bodies through anthropogenic actions. In general, any de-structuring of the physical and chemical environment of inland water bodies can lead to changes in the natural dynamics of their biological communities (Nogueira et al. 2010Nogueira M, Ferrareze M, Moreira M & Gouvêa R (2010) Phytoplankton assemblages in a reservoir cascade of a large tropical - subtropical river (SE, Brazil). Brazilian Journal of Biology 70: 781-793.). Here, rainfall data may explain the variations of the environmental variables.

In our previous study, Ceratium furcoides even at a low density (about 100 cells mL-1) was caused an apparent ecological imbalance in the Cachoeira II reservoir. In February at an average density of 150 ± 32 cells mL-1 was able to result Shannon and Simpson indices equal to zero. In March, when the C. furcoides population was reduced on 80%, these same indices increased until June (one of the highest reported densities, 370 ± 32 cells mL-1). In the months following the bloom reported in June, diversity and richness indices fell gradually to zero (in August) once again, expressing a new dominance (Oliveira et al. 2019Oliveira CY, Oliveira CD, Almeida AJ, Gálvez AO & Dantas DM (2019) Phytoplankton responses to an extreme drought season: a case study at two reservoirs from a semiarid region, northeastern Brazil. Journal of Limnology 78: 176-184.).

Ceratium furcoides had its first report in 2007 in Minas Gerais, Brazil (Santos-Wisniewski et al. 2007Santos-Wisniewski M, Silva L, Leone I, 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. Brazilian Journal of Biology 67: 791-793.), and was later recorded for the first time in a Brazilian semiarid region, in 2011 (Oliveira et al. 2011Oliveira HSB, Moura ADN & Cordeiro-Araújo MK (2011) First record of Ceratium Schrank, 1973 (Dinophyceae: Ceratiaceae) in freshwater ecosystems in the semiarid region of Brazil. Check List 7: 626.). Despite the scarce records, the species is in continuous expansion in Brazil, to the north and south of this country (Oliveira & Oliveira 2018Oliveira CYB & Oliveira CDL (2018) Geographical distribution of exotic dinoflagellate of freshwater Ceratium furcoides (Levander) Langhans 1925 in Brazil. Revista de Biologia Neotropical/Journal of Neotropical Biology 15: 109-113.). According to Meichtry de Zaburlín et al. (2016)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. Journal of Phycology 52: 200-208. and Cassol et al. (2014)Cassol A, Pereira Filho W, Oliveira M, Domingues A, Correa F, Buriol G (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., the Ceratium invasion and appropriation in new areas can be linked to climate change and reservoir constructions, since it eventually develops better in lentic environments.

Ceratium furcoides was commonly found in cold waters; Cavalcante et al. (2016)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. found that temperatures of 15 to 27 ºC are considered optimal for the development of C. furcoides in reservoirs in Southern Brazil. Also, in Brazil at relatively low temperatures (19 ± 3 ºC) the C. furcoides occurrences at the Garças reservoir, São Paulo state was reported (Crossetti et al. 2019Crossetti LO, Campos Bicudo D, Bini LM, Dala-Corte RB, Ferragut C & Mattos Bicudo CE (2019) Phytoplankton species interactions and invasion by Ceratium furcoides are infuenced by extreme drought and water-hyacinth removal in a shallow tropical reservoir. Hydrobiologia 831: 71-85.). However, some reports showed its adaptation to tropical environments: e.g. on the São Francisco River, occurrences C. furcoides occurrences were reported at an average temperature of 29.9 °C (Silva et al. 2018Silva 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 Limnologica Brasiliensia 30: e210.). Here, with higher temperatures (from 21 to 29 °C), the establishment this specie at the Cachoeira II reservoir was verified. Although the temperature was not limiting factor, in the linear regression, the preference for lower temperatures was proven, corroborating with previous studies (Silva et al. 2012Silva 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 Neotropica 12: 93-100.; Jati et al. 2013Jati S, Rodrigues L, Bortolini J, Paula ACM, Moresco GA, Reis LM, Zanco BF & Train S (2013) 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: s235-s236.). High Ceratium biovolumes were recorded as ordinary events in annual phytoplankton fluctuations of many temperate waterbodies. In subtropical environments, Ceratium spp. were reported at higher densities, as C. hirundinella in Argentina (Silveiro et al. 2009Silveiro MJ, Montañez G, Fra E, Saracho M, Arjona M, Amaya S & Traccanna B (2009) Variación poblacional de Ceratium hirundinella (Dinophyceae) en Embalses Eutrófcos de Catamarca (Argentina) y su relación con parámetros ambientales. Huayllu-Bios 3: 13-31.) with 5,634 cells mL-1 and C. furcoides in Southern Brazil with 2,819 cells mL-1 (Cavalcante et al. 2016Cavalcante 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.). The differences in temperature could justify the low density in the present study, when compared to those previously mentioned. However, up to the temperature range reported in this study, it cannot consider temperature as a limiting environmental variable.

The affinity of Ceratium for high phosphate concentrations in the Faxinal reservoir was also showed by Cavalcante et al. (2016)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.. According to these authors, Ceratium blooms occurred when the concentrations were higher than 0.05 mg L-1. In fact, the phosphate concentrations presented by them were significantly lower than those reported at the Cachoeira II reservoir. The results of the present study, besides corroborating with the direct relationship between Ceratium and SRP, show that this species was able to withstand high concentrations (higher than 0.80 mg L-1). The phosphorus is an important macronutrient for phytoplankton growth and its assimilation is to produce phospholipids, ATP and nucleic acids (Ji et al. 2013Ji M-K, Abou-Shanab RAI, Kim S-H, Salama E, Lee S-H, Kabra AN, Lee Y-S, Hong S & Jeon B-H (2013) Cultivation of microalgae species in tertiary municipal wastewater supplemented with CO2 for nutrient removal and biomass production. Ecological Engineering 58: 142-148.). However, high concentrations can cause cell damage and even inhibit growth (Li et al. 2018Li Q, Fu L, Wang Y, Zhou D & Rittmann BE (2018) Excessive phosphorus caused inhibition and cell damage during heterotrophic growth of Chlorella regularis. Bioresource Technology 268: 266-270.); here, Ceratium cells proved to be resistant to this nutrient. Other studies suggest positive correlations between Ceratium and nitrogen compounds (NH4, NO2 and/or NO3; Gil et al. 2012Gil CB, 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 Limnologica Brasiliensia 24: 207-219.; Nishimura et al. 2015Nishimura PY, Pômpeo M & Moschini-Carlos V (2015) Invasive dinofagellate Ceratium furcoides (Levander) Langhans in two linked tropical reservoirs. In: Pômpeo M, Moschini-Carlos V, Nishimura PY, Silva SC & Doval JCL (eds.) Ecologia de reservatórios e interfaces. Instituto de Biociências da Universidade de São Paulo, São Paulo. Pp. 132-142.), however, this was not a behavior found in the present study.

High Ceratium biovolumes are recorded as ordinary events in annual phytoplankton fluctuations of many temperate waterbodies. In subtropical environments, Ceratium spp. were reported at higher densities, as C. furcoides in São Francisco River with 5,600 cells mL-1 (Silva et al. 2018Silva 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 Limnologica Brasiliensia 30: e210.) and C. furcoides in southern Brazil with 2,819 cells mL-1 (Cavalcante et al. 2016Cavalcante 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.). The differences in temperature could justify the low density in the present study, when compared to those previously mentioned. However, we cannot consider temperature as a limiting environmental variable.

The results of the present study showed that C. furcoides was adapted to the environmental conditions in the Cachoeira II reservoir. In fact, corroborating Cavalcante et al. (2016)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., the highest biovolumes of C. furcoides were recorded in spring-summer. Biovolume recorded in the present study, although relatively lower than the densities recorded in Southern Brazil, can pose a great risk to local biodiversity.

Our results showed that the adverse environmental conditions, caused by extreme drought, did not affect the Ceratium population in Cachoeira II reservoir. Individuals of Ceratium furcoides were recorded during all months of the study - February to September 2017. Higher biovolume were positively related to SRP and temperature, showed by the direct and inverse relationship in the linear regression. An apparent adaptation of C. furcoides to Cachoeira II reservoir was evident, corroborating with reports in the worldwide. Further studies may be performed to evaluate strategies to reduce the population of this invasive dinoflagellate.

Acknowledgements

We acknowledge to the Programa de Educação Tutorial (FNDE), for the grant offered to Carlos Yure Oliveira during this study; and to Brazilian National Counsil for Scientific and Technological Development (CNPq), for the aid granted to the Professor Alfredo Olivera Gálvez (PQ 311058/2015-9). This study was financed in part by the Coordenação de Aperfeiçoamento Pessoal de Nível Superior - Brasil (CAPES) -Finance Code 001.

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Publication Dates

  • Publication in this collection
    11 June 2021
  • Date of issue
    2021

History

  • Received
    21 Jan 2019
  • Accepted
    01 May 2020
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