In the last two decades, Ceratium has proved to be an invader in South American waters, colonizing rapidly due to its adaptive strategies, such as mixotrophy, locomotion capacity, and encystment, which allow it to form large numbers of individuals during blooms (Cavalcante et al., 2013). Tropical and subtropical regions of South America are more susceptible to invasion by the dinoflagellate, because of the thermal stability of water column and relatively high temperatures, being determining factors in its distribution (Meichtry-de-Zaburlin et al., 2016). Our study showed the invasion of the dinoflagellate Ceratium furcoides in 59 municipalities, distributed in ten Hydrographic Basins, belonging to the Hydrographic Region of Uruguay (HR) in southern Brazil, from 2013 to 2019. The results represent the first report of the species expansion in this HR as a hole and deepen the knowledge to the South America region, which is susceptible to invasion by this dinoflagellate and is still in the process of expansion (Meichtry-de-Zaburlin et al., 2016; Accattatis et al., 2020).
Ceratium furcoides is a relatively large dinoflagellate, with cells measuring between 123–322 µm (Popovsky´ & Pfiester, 1990) and was never found in Brazilian environments until 2000s (Cavalcante et al., 2013). The first record for the species in the Rio Grande do Sul area was made by Cavalcante et al. (2013), in Uruguay River, the main water body of the HR Uruguay, in 2011. This study along with our results suggest that C. furcoides, since its introduction, has stablish itself and is well settled in the region, as the species was found permanently throughout the sample period. The authors also indicate that Ceratium has a radial dispersion in the area, from the southeastern region, where it was first detected, to northwards and southwards. Since its introduction in Rio Grande do Sul, C. furcoides has been recorded in some reservoirs and lakes (Cavalcante et al., 2016; Silva et al., 2019).
According to Meichtry-de-Zaburlin et al. (2016), the most suitable areas for the invasion of C. furcoides are mainly located in the subtropical regions of South America, which corroborates with the results presented for this Hydrographic Region. Other studies have shown the success of the invasion of C. furcoides in aquatic bodies in the subtropical region (Cavalcante et al., 2013, 2016; Silva et al., 2018; Silva et al., 2019). The results also suggest that the temperature range for the occurrence of the species is much wider than expected (between 18 and 22°C, according to Meichtry-de-Zaburlin et al., 2016), as we found the species in environments with temperatures as high as 34,5°C and as low as 3,6°C, provide that the spatial and temporal scales are expanded, as in this study. Pacheco et al. (2021) showed the species in temperatures ranging from 18 to 28,4°C in a Uruguayan lakes; however, in tropical area in Brazil, where the temperature variation is short, Severiano et al. (2022) evidenced C. furcoides in warm environments (around 26–28°C).
Furthermore, seems that high temperatures associated with high precipitation rates may spark the growth of Ceratium in these spring, as large densities occurred in years where these meteorological variables were high (2013 to 2015). Recently, Cavalcante et al. (2016) showed that occurrence and blooms of Ceratium in reservoirs in Caxias do Sul (RS) were related to ideal temperature conditions and nutrient availability. Moreover, the authors mention that high precipitation rates may be responsible for nutrient suspension in water bodies via the sediment flow from the soil. When associated with high temperatures, this can result in a metabolic increase for these organisms, eventually causing blooms. Other authors (Winder & Hunter, 2008; Strayer, 2010; Crossetti et al., 2019) mention that significant climate change tends to favor invasions, as with disturbances, niches become vacant, and organisms with invasive characteristics can be recruited.
Although high temperatures may benefit Ceratium, this is not a determining factor for its expansion, as the dinoflagellate maintains intermediate densities in later years (2016 onwards). This coincides with other studies, such as in Lake Blanca, Uruguay (Pacheco et al., 2021), where high temperatures were important during the initial stages of a bloom but not necessary to maintain it. C. furcoides has complex distribution and expansion patterns, usually colonizing freshwaters from basins that are geographically close (Moreira et al., 2015; Silva et al., 2018; Pacheco et al., 2021). Common phytoplankton dispersants such as wind, animals, and humans could play a part on the expansion of the dinoflagellate as they can be a very effective disperse route, as propagules are permanently living in water (Padisák et al., 2016), and can be further facilitated by the presence of reservoirs, that confer suitable environmental conditions for blooms of C. furcoides (Meichtry-de-Zaburlin et al., 2014; Silva et al., 2018).
The growth of these organisms is also controlled by physical and chemical variables, such as pH and organic matter, ions such as calcium and chloride, and various forms of nitrogen and phosphorus (Bustamante-Gil et al., 2012), as we also found in this study. Most of the time, Ceratium populations were directly related to alkalinity, pH, and organic matter. The first two variables were found to be highly correlated in the first three years of sampling (2013 to 2015). Bartram (1999) mentions that microalgae proliferation occurs at relatively high temperatures and neutral to basic pH (7 to 9), something that also occurred in this HR. This condition is already found in other reservoirs in Brazil (Matsumura-Tundisi et al., 2010; Silva et al., 2012) and elsewhere in South America (Bustamante-Gil et al., 2012). On the other hand, organic matter was correlated with Ceratium during the seven years of sampling. According to Olrik (1994), planktonic organisms contribute to the increase of organic matter, favoring nutritional alternatives for dinoflagellates through mixotrophy.
Although the possible nutritional increase is associated with blooms, the HR did not have clear nutrient patterns. Ceratium peaks were directly correlated to total phosphorus and NO3, but only in punctual municipalities. High dinoflagellate densities have been related to high phosphorus concentration in a tropical reservoir (Matsumura-Tundisi et al., 2010). According to Oliver & Ganf (2000), blooms are a response to an environmental imbalance, generally linked to nutritional contribution, especially phosphorus for algal organisms. Bustamante-Gil et al. (2012) pointed out that Ceratium has a large storage capacity for phosphorus, tolerating ample nutritional stress. According to Esteves & Amado (2013) and Lira et al. (2015), nitrogenous forms, especially NO3, are the most commonly used by phytoplankton. In Brazilian reservoirs, the genus showed better development in environments with high concentrations of this nutrient, such as in São Paulo in the Billings Reservoir (Nishimura et al., 2015) and in Garças Lake (Crossetti et al., 2019), in addition to Minas Gerais in Furnas Reservoir (Silva et al., 2012). These results suggest that local environmental characteristics (abiotic conditions and biotic interactions) are key for the development of C. furcoides in this Hydrographic Region, as these features can act as ecological filters, determining if the species can survive, reproduce, and persist in the habitat (Incagnone et al., 2015). Studies in other aquatic ecosystems in South America reveal that the presence of species differs in relation to the local conditions, ranging from a single record (Silva et al., 2018; Macêdo et al., 2021) to permanent frequency (Silva et al., 2012; Silva et al., 2019).
Competitive pressures from introduced species under native populations can alter the composition and response of local communities, with short and long-term effects (Delariva & Agostinho, 1999). During the beginning of the study (2013 to 2015), Ceratium dominated in HR Uruguay (59 monitored municipalities), with a rapid expansion associated with high densities (1,398 to 3,046 cel.mL− 1). This aggressive behavior, also reported by Cavalcante et al. (2016), caused an imbalance in the phytoplankton community, especially for the dominance of Microcystis, since the increase in dinoflagellate densities, in most cases, coincided with the decrease in populations of these cyanobacteria. Due to its ecological relevance (formation of blooms) and public health concerns (production of toxins), Microcystis is considered one of the most important genera of cyanobacteria, being able to attribute color and odor to water, form biofilm and cause corrosion, in addition to persisting in water distribution systems (Komárek et al., 2002). The coexistence and competition between Ceratium and Microcystis have been reported by several authors (Van Ginkel et al., 2001; Reynolds et al., 2002; Padisák et al., 2009; Matsumura-Tundisi et al., 2010; Grigorszky et al., 2019). The Ceratium and Microcystis species are effective at limiting and competing for nutrients, using vertical migration over long distances to microenvironments with greater availability of light and nutrients (Reynolds et al., 2002; 2006). In this scenario, even with similar strategies, Ceratium prevails, as it can use mixotrophy when necessary (Reynolds et al., 2002; 2006) and is resistant to herbivores due to its horns and spines (Van Ginkel et al., 2001), in addition to having a large storage capacity for nutrients, especially phosphorus (Bustamante-Gil et al., 2012). After this initial period, the community stabilized, establishing a coexistence between both genders. According to Kruk et al. (2021), this is due to a difference between ecological niches, since the mechanism that influences these associations is vertical migration, where Microcystis occupies the water surface, while Ceratium is distributed below the surface. In a shallow and urban lake, the invasion of Ceratium proved to be beneficial in controlling Microcystis blooms and enabling the more diverse phytoplankton community to re-establish itself (Silva et al., 2019). It is necessary more efforts in this sense if the establishment of Ceratium in subtropical environments could become an aggregating factor to reestablish existing communities before the problem of eutrophication, with harmful blooms.
The development and success of phytoplankton communities during blooms is mainly due to the temporal organization of nutrients and energy (Reynolds, 1997). Thus, seasonality and trophic conditions in the environment are important factors in ecological studies, as they influence the structure of the phytoplankton community and the dominance relationships between algal groups (Falco, 2000). The stocks monitored by CORSAN showed seasonal patterns, with peaks of Ceratium and Microcystis occurring in summer and fall. This preference for relatively high temperatures also corroborates dispersion models, which relate invasive phytoplankton species to climatic variables, especially temperature (Meichtry-de-Zaburlin et al., 2016; Macêdo et al., 2021). This pattern regarding higher temperatures also held for Ceratium in other subtropical reservoirs (Cavalcante et al., 2016; Rocha, 2016).
Although not toxic, Ceratium blooms can cause impacts in water treatment company, resulting in changes in taste, color, and odor, as well impact in the ecosystem functioning through oxygen depletion, which can result in death of animal, such as fish and zooplankton (Hart & Wragg, 2009; Meichtry-de-Zaburlin et al., 2016). Other problem associated with its presence in reservoir is the hindrance in the process of coagulation and flocculation, in addition to filter clogging and an increase in chlorine demand (Knappe et al., 2004; Ewerts et al., 2013; 2014). In freshwater environments, the construction of reservoirs has increased the chance of establishment of invasive species (Davies et al., 1992; Vieira et al., 2020), and for this reason, methods to avoid this are necessary. Studies have shown that the treatment conditions and the phytoplankton species present in the water influence the removal of its cells (De Julio et al., 2010; Zamyadi et al, 2012). Almeida et al. (2016) showed that the physical process of removing Ceratium is viable, as 89% of the cells were removed with this technique in Caxias do Sul (RS), Brazil. Other alternative is the addition of chlorine before conventional treatment for its removal, as it is a compound that can inactivate cells (Van der Walt, 2011; Almeida et al., 2016). However, this method should be used with wariness, as it can increases cell lysis and consequently, the load of undesirable odor and taste compounds dissolved in water (Ho et al., 2013). Calcium hydroxide could also be another choice to immobilizes and inactivate Ceratium cells (Ewerts et al., 2014). Keeping the cell levels within the standard ranges is essential to ensuring drinking water quality, as CORSAN provide domestic water supply to almost six million people. For the company and public health, it is much easier and low cost to do water treatment with not harmful Ceratium than with Microcystis and its possible toxicity.