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All issues Volume 57 (2021) Ann. Limnol. - Int. J. Lim., 57 (2021) 13 Full HTML
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Ann. Limnol. - Int. J. Lim.
Volume 57, 2021
Article Number 13
Number of page(s) 12
DOI https://doi.org/10.1051/limn/2021009
Published online 06 July 2021

© EDP Sciences, 2021

1 Introduction

One of the main objectives of ecological studies is to understand the causes and mechanisms that change the structure of communities in order to predict future patterns of species abundance, diversity and occurrence (Blaum et al., 2011). Functional diversity approaches have been an efficient tool in gaining a better understanding of how environmental conditions selected species in a given environment and how they share resources, linking ecological processes to biodiversity patterns (Mouchet et al., 2010). These approaches allows the investigation of ecosystem level processes at different scales (Xu et al., 2010), where different species with similar characteristics are categorized into ecological groups such as functional guilds or functional groups (Blaum et al., 2011; Luck et al., 2013). These categorizations are often more useful to ecologists than taxonomic classifications, as the former explore not just evolutionary history but also ecological functions (Mitra et al., 2016; Luck et al., 2013). Root (1967) introduced and defined the term “functional group” for ecology as “a group of species that exploit the same range of environmental resources in a similar way and thus overlap in their niche needs” where the use of resources is generally related to food or habitats suitable for species survival (Blaum et al., 2011).

In aquatic environments, protist ciliates occur in high abundances, have short generation times and show high dispersion capacity (Stoeck et al., 2018), forming communities with high taxonomic and functional diversity, in freshwater as well as marine environments (Parry, 2004; Kathol et al., 2011).

Ciliates have been recognized as morphologically and ecologically diversified organisms (Fauré-Fremiet, 1924), which manage to exploit a wide range of food resources, being important consumers of bacteria and phytoplankton (Weisse, 2002; Comte et al., 2006; Palijan, 2012). Some species are predators, consuming other protists (flagellates and ciliates) and even zooplanktonic organisms, such as rotifers (Simek et al., 1990; Weisse, 1990). However, most species have omnivorous “feeding modes”, feeding on a wide range of resources (Foissner et al., 1999). In this way, these protists play an important role in the flow of organic matter in pelagic and benthic environments (Azovsky and Mazei, 2018), constituting an important link between the microbial food chain and the metazoans of the classic food web (Mironova et al., 2012).

Thus, although the majority of ciliates are not highly specialized consumers, Functional Feeding Groups (FFGs) of species with similar food preferences can be identified (Dolan, 1991). Agasild et al. (2013) grouped the ciliate species according to the type of food resources used in four functional guilds: bacterivorous, algivorous, bacterivorous/algivorous and predators. The categorization of species according to the FFGs has already been investigated in other studies (Dolan, 1991; Zhang et al., 2012; Agasild et al., 2013), which showed that ciliate guilds are largely influenced by the abundance of food items.

One of the factors that influences the ciliates abundance and availability of food resources in aquatic ecosystems is the hydrodynamics of the environments and the temporal dynamics (Tundisi and Tundisi, 2008). In floodplains, changes in environmental conditions occur seasonally through changes in the hydrometric level caused by floods, which promote intense exchanges of nutrients, sediments and organisms between different habitats in the plains (Junk et al., 1989; Neiff, 1990). In these places, the change in the hydrometric level is strongly reflected in the abiotic and biotic factors (Junk et al., 1989), so that periodic floods are the main regulating factor of the physical and chemical characteristics of the environments (Thomaz et al., 2004) as well as in the organization of the different aquatic communities (Rodrigues et al., 2009; Lansac-Tôha et al., 2009).

It is during the low-water period, or limnophase, that the highest values of phytoplankton density (Rodrigues et al., 2009) and the lowest bacterial densities (Carvalho et al., 2003) are recorded. This occur due to a combination of factors in this period, such as the large amount of nutrients available, the daily mixing of the water column, and the fact that the lagoons are shallower (Thomaz et al., 1997). These factors mean that the primary production is high, and this is responsible for the largest source of organic carbon for the food webs (Anesio et al., 1997). Conversly, in the high-water period, or potamophase, the lowest densities of phytoplankton (Rodrigues et al., 2009) and highest densities of heterotrophic bacteria (Carvalho et al., 2003) are observed. These changes arise from the supply of allochthonous organic matter, which is the largest carbon source for aquatic organisms in this period (Anesio et al., 1997; Carvalho et al., 2003), and the resources prevenient of the decomposition processes exceed those of primary production, especially in ponds (Anesio et al., 1997).

Thus, this study aimed to verify the variations in the structure of the FFG of Protist Ciliates in environments with different hydrodynamics (lotic and lentic), in different hydrological periods (high and low water), in a neotropical floodplain. The following hypothesis was tested: from the perspective that communities are regulated by the availability of food resources in the environment, the ciliates FFGs will be structured differently in the different environments and periods, since the availability of the communities used as a food resource are strongly influenced by hydrodynamics and the flood pulse. Thus, it is expected that a possible greater abundance of phytoplankton in the period of low-waters and heterotrophic bacteria in high-waters will be the main responsible for the difference in the abundance and richness of the FFGs in the lentic and lotic environments. We still expect that the greatest abundance and richness of FFGs will be found in lentic environments, due to greater environmental stability when compared to lotic environments.

2 Materials and methods

2.1 Area of study

The present study was carried out in the lower stretch of the upper Paraná River floodplain (Fig. 1), which establishes the boundary between the states of Paraná and Mato Grosso do Sul and constitutes the last undammed stretch of the Paraná river in Brazilian territory (latitude 22° 30′ and 22° 00′ south; longitude 53° 00′ and 53° 30′ west). This stretch of the floodplain stands out for its great heterogeneity, due to the presence of numerous lentic (lakes and backwaters) and lotic (channels and rivers) environments (Agostinho et al., 2004), resulting in a large number of microhabitats. These environments support a high diversity of terrestrial and aquatic species, which is mainly regulated by the flood pulse regime (Junk et al., 1989; Neiff, 1990, Thomaz et al., 2007).

Water collections were carried out for the analysis of planktonic ciliate communities, and heterotrophic bacteria and phytoplankton (the last two were used as a proxy for food resources consumed by protists, with their abundance being related to the FFGs, in order to verify their influence on the abundance and richness of each FFGs) in the months of March and September of the years 2010 and 2011, at the subsurface (10–20 cm below the water-air interface) of 12 environments. Among them were rivers, two channels, four connected lakes and three unconnected lakes, belonging to three different subsystems of the upper Paraná River floodplain (Paraná, Bahia and Ivinheima) (Fig. 1).

thumbnail Fig. 1

Location of sampling stations. The gray dots represent the lotic environments while the white dots represent the lentic environments.

2.2 Sampling and laboratory analysis

For the analysis of protist ciliates, four litres of water were sampled and concentrated in 100 mL, through reverse filtration, with the aid of a 5 μm mesh. The counting and identification of the species were performed in vivo using a standard optical microscope. The species found were categorized according to their eating habits (Foissner and Berger, 1996; Foissner et al., 1999; Aescht et al., 2017) in FFG of bacterivorous, algivorous, bacterivorous/algivorous, predators and omnivorous. We consider omnivorous to be ciliates who consume food resources belonging to more than one trophic level (e.g., algae, bacteria and heterotrophic nanoflagellates or other ciliates) (Pimm and Lawton, 1978).

To calculate the density of heterotrophic bacteria, 50 mL of water was sampled, fixed in a solution of borate buffered formaldehyde, alkaline lugol and sodium thiosulfate (Sherr and Sherr, 1993). Subsequently, the bacterioplankton was analysed from 200 μL subsamples obtained by filtering with black Nuclepore/Watchman with 0.2 μm pore opening, stained with 1 mL of the fluorochrome 4,6′- diamidino-2-phenyl- indole (DAPI) at 0.1%, over 15 min, in the absence of light. Then, the filters were placed on slides and stored at a temperature of −8 °C, until counting. The bacteria were quantified in 1000× magnification in an epifluorescence microscope (OLYMPUS BX51) from field images, obtained through the Image Analysis Express Image System, with 10 fields per sample (Porter and Feig, 1980), and abundance was estimated according to Waterbury et al. (1986).

The phytoplankton community was sampled by obtaining aliquots of 50mL of water, fixed in situ with Lugol solution. Phytoplankton density was estimated using an inverted microscope, according to the Utermöhl method (Utermöhl, 1958). The volume from the sedimentation was defined according to the concentration of algae and/or debris present in the sample and the sedimentation time was determined according to the height of the sedimentation chamber, assigning at least three hours for each centimetre height of the chamber (Margalef, 1983). Counting was performed randomly, by field, until 100 individuals of the most frequent species were obtained, with an error of less than 20%, with a 95% confidence coefficient (Lund et al., 1958).

Concomitantly, we measured the following environmental aspects, such as water temperature, dissolved oxygen concentration (YSI 550A meter), pH, water electrical conductivity (YSI 63 meters), water transparency (Secchi disk). Water samples were also collected for the analysis of inorganic nutrients in the laboratory. Orthophosphate was obtained from spectrometry (Hansen and Koroleff, 1999) and nitrate and ammonium were determined by oxidation in an acid medium (Mackereth et al., 1978; Giné et al., 1980).

2.3 Data analysis

To test for significant spatial changes in the composition of ciliate functional feeding groups (FFG) for both presence-absence and abundance data, we performed a permutational multivariate analysis of variance (PERMANOVA, 9 999 permutations; Anderson, 2005) using the hydrological period (i.e., dry and flood seasons), the type of environment (i.e., lentic and lotic), the year of sampling (i.e., 2010 and 2011), as well as their interactions, as factors. PERMANOVAs were performed on Sørensen (presence-absence) and Bray-Curtis (abundance) dissimilarities, using function “adonis2” from R package vegan (Oksanen et al., 2019).

In order to search for patterns in the differences in FFG between the two hydrological periods, between environments of different hydrodynamics and years of sampling, a redundancy analysis (RDA; Legendre and Legendre, 2012) was performed using the function “rda” from R package vegan (Oksanen et al., 2019). Environmental matrix was composed of the standardized environmental variables described above. We checked the multicollinearity among environmental variables using variance inflation factors (VIF) and removed variables that were strongly correlated with other variables (VIF > 5) before statistical analyses (Oksanen et al., 2019). We applied a forward selection with two stopping rules to identify the final sets of environmental variables separately for presence-absence and abundance data (function “ordiR2step” from R package vegan). Statistical significance was tested through 9,999 permutations.

All statistical analyses were performed in the R environment. The figures were drawn using the R package ggplot2.

3 Results

The years 2010 and 2011 showed characteristic seasonality with well-defined periods of high and low-water levels. The values for the hydrometric level of the Paraná River varied between 200 and 669.5 cm, and the months with values for hydrometric level greater than 350 cm were considered periods of high water (Thomaz et al., 2007) (Fig. 2).

Altogether 108 species of ciliates were identified, in all studied environments (Tab. 1). Most species of ciliates had an omnivorous feeding habit (41), followed by bacterivorous/algivorous (28 species), bacterivorous (16 species), algivorous (12 species) and predators (11 species) (Tab. 1).

In lentic environments, FFGs were represented in greater proportion by bacterial grazers, reaching 40% in the low-water period (Fig. 3A) and 28% in the high-water period (Fig. 3B). In the low-water period, the second most abundant FFG group was algivorous (25%), followed by bacterivorous-algivorous and omnivorous (17%). Lastly, the predators were the least representative, with only 1% (Fig. 3A). For the high-water period, the FFG with the highest representation was bacterivorous-algivorous (23%), followed by omnivorous (22%) algivorous (21%) and predators (7%) (Fig. 3B).

In the lotic environments, the dominant FFG in the low-water period was algivorous (37% of the ciliates) and in the high-water period it was the bacterivorous/algivorous (37% of the ciliate) (Fig. 3C,D). In these environments, in the low-water period, bacterivorous accounted also for a high proportion (28%) and predators ciliate species were not found (Fig. 3C). In high waters, omnivorous were the second most representative FFG (26%) and predators had only 1% representativeness (Fig. 3D).

In the descriptive graphs, the lentic environments in the low-water periods in the year 2010 presented the highest values of richness (except for predators and omnivorous FFG) (Fig. 4) and abundance (except for predators) (Fig. 5). Therefore, regardless of the period and the year, the wealth and abundance of almost all FFGs were greater in the lentic environments when compared to the lotics. In relation to FFGs, the temporal variation (period and year) is an important factor for the grouping of FFGs, especially for lentic environments, where the change in the flow of matter is drastic in relation to the period.

The results of the Redundancy Analysis (RDA) to richness (Fig. 6A) was significant for the axis 1 (p = 0.001); with explain 25.62% of the variation in the data, showed a spatial and temporal (period and year) segregation of the sampling units in relation to the FFG. For abundance (Fig. 6B), the results of the RDA were significant for the two axes, axis 1 (p = 0.001) and axis 2 (p = 0.008); these axes explained 29.38% of the variation in the data, showed a spatial and temporal (period and year) segregation of the sampling units. For both abundance and richness, the FFGs experienced strong temporal segregation over the years, and the highest values of FFGs were found in 2010 (Fig. 6). For richness, predators and omnivorous were associated with periods of high-water and pH, while in the period of low-water, bacterivorous, bacterivorous/algivorous and algivorous FFGs were associated with high values of chlorophyll and heterotrophic bacteria (Fig. 6A). 2011 was mainly characterized by higher values of water transparency (Secchi), PO4, NO3 and dissolved oxygen (Fig. 6A). The abundance followed a pattern similar to that found for the richness, where the highest values of FFGs were found in the year 2010, in lentic environments and during the dry period (Fig. 6B). The flood period in this year was related to higher values of temperature and pH, while in 2011 was mainly correlated with a high concentration of dissolved oxygen and NO3 (Fig. 6B).

The RDA ordination suggested a clear distinction between the categorical factors analysed, although differences between periods showed to be more pronounced for abundance data (Fig. 6). This pattern was evidenced by the PERMANOVAs, which revealed significant differences between type of environment (p = 0.002; p = 0.001) and sampling year (p = 0.001; p = 0.001) for both presence-absence and abundance data, respectively. In contrast, for hydrological period, PERMANOVA were significant for abundance (p = 0.001), while no difference was found for richness (p = 0.426).

thumbnail Fig. 2

Variation of the hydrometric level of the Paraná River in the years 2010 and 2011 of the Paraná River. The reference level represents the division of the low-water or limnophase period (below the line) and the high-water or potamophase period (above the line).
Table 1

Species of ciliate protists categorized into FFGs according to feeding habits. The presence of FFGs in the different periods and types of environments are indicated by “X”.

thumbnail Fig. 3

Functional Feeding Groups (FFG) represented in proportion. A) Low water lentic; B) High water lentic; C) Low water lotic; D) High water lotic. ALG = algivorous; BACT = bacterivorous; BAC/ALG = bacterivorous/algivorous; OMN = omnivorous and PRE = predators.
thumbnail Fig. 4

Species richness by Functional Feeding Group (FFG) for two-year hydrological periods in lentic and lotic environments. The red color represents the dry period and the blue color represents the flood period.
thumbnail Fig. 5

Abundance of species by Functional Feeding Group (FFG) for two-year hydrological periods in lentic and lotic environments. The red color represents the dry period and the blue color represents the flood period.
thumbnail Fig. 6

RDA between samples, environmental variables, and Functional Group (FFG) for hydrological periods in lentic and lotic environments. BACT = Bacterivorous, OMN = Omnivorous, PRED = Predators, BAC. ALG = Bacterivorous/Algivorous, ALG = Algivorous, Chloro = chlorophyll, Bact = Heterotrophic Bacteria, Temp = Temperature, PO4 = Phosphate, DO = Dissolved oxygen, NO3 = Nitrate. A) Richness of species by Functional Feeding Group (FFG). B) Abundance of species by Functional Feeding Group (FFG).

4 Discussion

In this study, in general, we found higher values of richness and abundance of FFG in lentic environments to the detriment of lotics. The hydrodynamic stability of lentic environments provides ideal conditions for the development of planktonic organisms, allowing the establishment of high abundance and species richness when compared to lotic environments. Lotic environments are more turbulent with a continuous alteration in of the flow of water impairing the establishment and development of large populations of planktonic organisms (Negreiros et al., 2017). The high speed of the current favors the transport of organisms downstream, besides leading to other negative effects determined by the mechanical forces caused by the current (Horvath and Lamberti, 1999).

The study showed a contrast regarding the difference in years and seasonal differences. Seasonal patterns indicate the main inter-annual differences in the abundance of ciliates (Strom et al., 2019), while seasonal dynamics may promote inter-annual changes. The environmental variables varied temporally and spatially, characterizing the studied environments. However, FFGs seem to have been structured mainly with food resources, with little influence from physical and chemical variables. In the case of the year 2010, which grouped the chlorophyll variables and bacteria, this was responsible for the association of FFGs that use these food resources. The high abundance of bacterivorous FFGs in lentic environments can be explained by the high concentration of organic matter to be decomposed. The fact that bacterivorous are a prominent group in aquatic environments indicates that the main sources of carbon come from bacteria and debris (Wetzel, 1983). Shallow lagoons are part of the earth's landscape and the watershed can contribute allochthonous carbon to the lake (Furey et al., 2018).

The alternation in resource availability in different hydrological periods can cause changes in the density of algae and bacteria, resulting in successions of ciliate species. Our results showed that the greater abundance and richness of the bacterivorous/algivorous, bacterivorous and algivorous FFGs were related to the higher concentrations of heterotrophic bacteria and chlorophyll, suggesting that the abundance of food resources is responsible for the structuring of these FFGs in this study. The trend towards higher densities and number of species in the high-water period may suggest that bacteria played a more important role as a food resource for bacterivorous FFGs. Sonntag et al. (2006) found similar results, in which the most predictive food for the bacterivorous/algivorous FFG was heterotrophic bacteria due to their availability in environments, while only a small fraction of the smaller phytoplankton was consumed by these organisms.

As a FFG, algivores are specialists, feeding strictly on phytoplankton, and they are directly influenced by fluctuations, responding rapidly to temporal changes in primary production (Posch et al., 2015). Studies in the upper Paraná River plain indicate that phytoplankton is influenced by lower turbidity and greater stability of environments, reaching the highest biomass peaks in the low-water period (Rodrigues et al., 2009). The entry of organic material in high-water periods determines changes in the proportion of algivorous and bacterivorous/algivorous FFGs, assuming a higher proportion for both lentic and lotic environments.

Among the FFGs studied, the omnivorous ciliates presented the largest number of species. Other studies with a FFG approach to ciliates also pinpointed out omnivores as the most representative (Arndt et al., 1990; Balazi and Matis, 2002). The predominance of omnivorous organisms in aquatic environments is widely documented for the most varied taxonomic groups, in different geographic and climatic regions (Walker, 2009). This is because these organisms generally have a wide variety of niches and can feed at a more trophic level (Pimm and Lawton, 1978) and, therefore, use a broad range of resources (Pfister and Arndt, 1998). For these reasons, omnivores contribute to the stabilization of communities, since they can resort to alternative food resources, which could reduce the exclusion of species by competition. In addition, our results show a high abundance of omnivores, along with high concentrations of chlorophyll and heterotrophic bacteria, suggesting that these may be the main dietary resources that were consumed by this FFG in this study.

In both lotic and lentic environments, and regardless of the period, the abundance predatory FFGs was very low. This result corroborates what was found by Zingel (1999), in a study showing that predatory ciliates were not abundant in the ecosystems. The transfer of energy within food webs depends on a high abundance of producers to sustain a lower abundance of primary consumers (e.g. herbivores) (Lindeman, 1942; Odum and Barrett, 2007). These, in turn, sustain an even lower abundance of secondary consumers, such as predatory ciliates because, with each transfer of energy to the upper trophic level, a significant part of it is lost. Low predator abundance over time, may also be associated with intraguild predation, in which the competition between predators promotes a more negative relationship, than the prey limitation itself (Diehl and Feissel, 2001). This means that there is no relationship between an increase in prey and an increase in predators, but rather a contrary relationship, in which predators compete with each other, and prey benefits them. Thus, where intraguild predation is intense, it can reduce the effect of predators on prey, keeping them at high abundance (Price and Morin, 2004), which corroborates with the results, where even with prey availability the predators remained at low abundance. Another point is that temporal variability is notably lower over many generations of predators and prey, which is observed in some diverse plankton communities, e.g. ciliates and algae (Tirok and Gaedke, 2010), highlighting that both biotic (competition, predation, intraspecific relationships) and abiotic factors related to time and space, can shape FFG predators. Thus, time-varying species interactions are key components of communities when considering the need for a better understanding of their dynamics and stability (Karakoç et al., 2020). This is especially true when dealing with floodplains, in order to understand how ecosystem functioning based on river dynamics can influence the taxonomic and functional composition of species, as well as their interaction.

It is known that protists can exploit a wide range of food resources, which leads them to be classified as bacterivores, algivores, carnivores, parasites, osmotrophs, detritivores, histophages, mixotrophs and omnivores, among others (Fenchel 1987; Foissner et al., 1999; Weisse et al., 2016). These microorganisms can obtain their resources using different and extremely versatile feeding methods, such as feeding by filtration of particles, interception and direct diffusion, and also including prey capture strategies, such as passive or active ambush (Fenchel 1987; Kiørboe 2011; Weisse et al., 2016). In this study we opted to classify the FFGs as bacterivorous, algivorous, bacterivorous/algivorous, predators and omnivorous, and we identified patterns in the structure of each FFG in different hydrodynamics and hydrological periods. However, it should be emphasized that this classification is not fixed or immutable, and a number of studies point to feeding flexibility among many protists, which depends on several factors (Weisse et al., 2016; Simek et al., 2019). Different natural ecosystems can produce very varied results regarding the feeding habits of these protists. In distinct environments, various factors can alter the feeding of ciliates, such as the quantity and quality of the food, characteristics of the prey itself (size, shape, type of swimming habit, swimming speed, etc.) (Buskey et al., 1993; Matz et al., 2002), limnological factors such as temperature, light and turbulence (Weisse et al., 2016), and trophic degree (Simek et al., 2019), among others.

Furthermore, there is methodological bias in relation to studies that classify the feeding habits of protists. Most studies are carried out with experiments that use monospecific cultures, which can generate results that do not truly reflect the conditions experienced in natural environments. For example, this process selects some species that are more likely to survive in laboratory conditions, thus excluding a large number of the other species present in nature (Weisse et al., 2016). In addition, the use of clones or a single strain of each species ignores the interspecific interactions that can alter the behaviour of organisms, for example in relation to niche partitioning (Calbet et al., 2013; Weisse et al., 2016). Standardization of variables in experimental approaches thus results in important responses, but research involving the analysis of the content of vacuoles in specimens found in natural environments is also extremely important (Weisse et al., 2016). In our results, as expected, we found correlations between the food resources and the FFGs analysed, supporting the classification adopted here as a reflection of real patterns found in these environments and confirming that the consumption of these food items contributes to structuring these FFGs in the ecosystems studied.

5 Conclusion

Ciliate FFGs can exhibit spatial preferences, in accordance with the prevailing environmental conditions (Jiang et al., 2013). Floodplain environments are dynamic, and the hydric regime can alter the distribution of these groups, as demonstrated in this study. In the last five years, there have been no studies relating to ciliate FFGs in Neotropical floodplains, and so these results may mark a return to discussions related to FFGs and prospects for future work in the area. This could mainly concern functional groups as environmental indicators, for example in issues related to climate change (e.g., precipitation), which may help to predict how functional groups will be affected by these alterations, bearing in mind that many ciliates within a single functional group can have different functions in structuring communities (Jiang et al., 2013).

The results obtained in this work corroborate the idea that the different ciliate FFGs are structured according to the availability of types of food resources. These resources vary according to seasonality and with the types of environments of different hydrodynamics, which in turn lead to clear changes in the functional structure of protist ciliate communities. In this context, ciliates act on different trophic levels of the food web and occupy a large number of ecological niches.

In summary, the results of the categorization of ciliate species into functional feeding groups responded satisfactorily to temporal and spatial variations, which reinforces the idea that the grouping of species by functional characteristics can be a good indicator of an organism's responses to environmental changes. This confirmation will allow ecologists to carry out more detailed studies on the ecological role of protists in ecosystems.

Acknowledgments

The authors thank the Graduate Program in Ecology of Inland Water Ecosystems (PEA) and Research Center in Limnology, Ichthyology and Aquaculture of the State (NUPELIA) of the University of Maringá (UEM) to support for development and promotion this research. The authors also thank the CAPES (Brazilian Federal Agency for Coordination for the Improvement of Higher Education Personnel) and Brazilian Research Council (CNPq) for financial support.

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Cite this article as: Meira BR, Progênio M, Corrêa Leite E, Lansac-Tôha FM, Guimarães Durán CL, Jati S, Rodrigues LC, Lansac-Tôha FA, Velho LFM. 2021. Functional feeding groups of Protist Ciliates (Protist: Ciliophora) on a neotropical flood plain. Ann. Limnol. - Int. J. Lim. 57: 13

All Tables

Table 1

Species of ciliate protists categorized into FFGs according to feeding habits. The presence of FFGs in the different periods and types of environments are indicated by “X”.

In the text

All Figures

thumbnail Fig. 1

Location of sampling stations. The gray dots represent the lotic environments while the white dots represent the lentic environments.
In the text
thumbnail Fig. 2

Variation of the hydrometric level of the Paraná River in the years 2010 and 2011 of the Paraná River. The reference level represents the division of the low-water or limnophase period (below the line) and the high-water or potamophase period (above the line).
In the text
thumbnail Fig. 3

Functional Feeding Groups (FFG) represented in proportion. A) Low water lentic; B) High water lentic; C) Low water lotic; D) High water lotic. ALG = algivorous; BACT = bacterivorous; BAC/ALG = bacterivorous/algivorous; OMN = omnivorous and PRE = predators.
In the text
thumbnail Fig. 4

Species richness by Functional Feeding Group (FFG) for two-year hydrological periods in lentic and lotic environments. The red color represents the dry period and the blue color represents the flood period.
In the text
thumbnail Fig. 5

Abundance of species by Functional Feeding Group (FFG) for two-year hydrological periods in lentic and lotic environments. The red color represents the dry period and the blue color represents the flood period.
In the text
thumbnail Fig. 6

RDA between samples, environmental variables, and Functional Group (FFG) for hydrological periods in lentic and lotic environments. BACT = Bacterivorous, OMN = Omnivorous, PRED = Predators, BAC. ALG = Bacterivorous/Algivorous, ALG = Algivorous, Chloro = chlorophyll, Bact = Heterotrophic Bacteria, Temp = Temperature, PO4 = Phosphate, DO = Dissolved oxygen, NO3 = Nitrate. A) Richness of species by Functional Feeding Group (FFG). B) Abundance of species by Functional Feeding Group (FFG).
In the text

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