CC BY
112
Protistology 12 (4), 173-184 (2018)
Protistology
Free-living ciliates from a perturbed marsh in Central Mexico: some notes about taxonomy and ecology
Daniel Méndez-Sánchez1, Petra Sánchez-Nava1 and Rosaura Mayén-Estrada2
1 Facultad de Ciencias, Universidad Autónoma del Estado de México, campus El Cerrillo, Piedras Blancas, Desviación Tlachaloya, Carretera Toluca -Atlacomulco Kilo metro 15.5, C.P. 50200, Toluca, Edo. de México, Mexico
2 Laboratorio de Protozoología, Departamento de Biología Comparada, Facultad de Ciencias, Universidad Nacional Autónoma de México. Avenida Universidad 3000, Ciudad Universitaria, Circuito Exterior S/N, Coyoacán, CP. 04510, Ciudad de México, Mexico
| Submitted September 27, 2018 | Accepted October 5, 2018 |
Summary
Ciliates are a morphologically diverse group ofprotists inhabiting aquatic and terrestrial ecosystems. We studied the taxonomy and ecology of free-living ciliates from a freshwater marsh in Central Mexico during the period from 2012 to 2013 during both dry and rainy seasons. We found 30 ciliate species recorded for the first time from Atarasquillo marsh in Mexico, most of which are common species in freshwater ecosystems. The species richness was higher during the dry season than rainy season. Five trophic groups were observed: bacterivorous, bacteria-algae-heterotrophic flagellate consumers (BAF-consumers), omnivorous, predators, and mixotrophic species. The trophic group composition changed according to the season and the environmental conditions, e.g. vegetation and water level. Generally bacterivorous ciliates were more frequent during the rainy season, meanwhile the omnivorous during the dry season; thus, the feeding strategies in ciliates were different between both seasons. Due to the fact that Atarasquillo marsh is in a deterioration process, ciliate records could be used to assess water quality.
Key words: Ciliophora, marsh wetland, Mexico, seasonal variation, trophic role
Introduction
Free-living ciliates inhabit diverse aquatic and terrestrial environments (Foissner et al., 2008; Lynn, 2008), and have an important role in food webs (Finlay and Esteban, 1998; Weisse, 2002, 2017; Lynn, 2008). Heterotrophic ciliates feed on a
diversity of prey, including bacteria, sulphur bacteria, cyanobacteria, algae, diatoms, heterotrophic flagellates, protists including ciliates, and small metazoans (Foissner and Berger, 1996). In addition, mixotrophic ciliates are important contributors to primary production (Johnson, 2011). They and other protists are good indicators oftrophic status in
doi:10.21685/1680-0826-2018-12-4-2 © 2018 The Author(s)
Protistology © 2018 Protozoological Society Affiliated with RAS
101° 100° 99° 9903]' 99°30'
Fig. 1. Location of Lerma marshes (A) and Atarasquillo (Chignahuapan) wetland (B), showing the sampling sites in black circles. Sites 3 and 4 are outside of the protected area.
lakes (Beaver and Crisman, 1989) and bioindicators of water quality (Madoni, 2005; Jiang et al., 2011; Debastiani et al., 2016), mainly due to the fact that their species richness and biomass are affected by changes in the physicochemical conditions in the water (Mieczan, 2007a, 2007b; 2009).
Despite the importance of ciliates, knowledge about their diversity in wetlands is scarce. Henebry et al. (1981) studied the composition and structure of some protozoan communities, including ciliates, in seven different wetlands (bogs, fens, marshes, swamps) in the USA and found 2 to 12 ciliate species. Mieczan (2007a, 2007b) observed 7-37 species in peatbogs in Poland, and Lopes and Heckman (1996) found 55 ciliate species in the largest wetland of the world, Pantanal Mato Grosso in Brazil. The wetland where the highest ciliate diversity was recorded is a group of Sphagnum ponds in Simmelried, Germany, with 202 species identified (Kreutz and Foissner, 2006).
In Mexico, ciliate species diversity in wetlands is poorly understood, and only Glaucoma dragescui Corliss, 1971 has been reported from Lerma marshes in the Central region of the country (Madrazo-Garibay and Lopez-Ochoterena, 1985). However, Mexican wetlands have been mainly used for agricultural purposes causing perturbation and loss of biodiversity (Guerra and Ochoa, 2006; Zepeda-Gomez et al., 2012b). This is the case of Lerma marshes that comprise three wetlands: Chignahuapan, Chimaliapan and Chiconahuapan, that are considered as RAMSAR sites and are under
Mexican protection laws (SEMARNAT, 2002; Ceballos, 2003).
The goal of this study is to record free-living ciliate species communities and provide data on their trophic role in a perturbed marsh from Central Mexico.
Material and methods
Study Area
Atarasquillo wetland, also known as Chigna-huapan Lake (Fig. 1), is a freshwater marsh near Lerma town in Mexico State, Central Mexico at 2,600 meters above sea level, with 346 ha. The weather is temperate with an annual average temperature of 19 °C (maximum 30 °C and minimum 7 °C). The annual rainfall (1,700 mm total, on average) occurs in summer (June-September) while the dry season occurs in the rest of the year (Ceballos, 2003).
Sampling
We sampled at five sites (sites 1-5, Figs 2 a-j), where sites 3 and 4 were located outside the protected area (Fig. 1; SEMARNAT, 2002). A total of 39 water samples were manually collected by using plastic jars of 250 ml, and extracting a volume of 200 ml. Twenty samples were taken during the dry season and 19 during the rainy season. The pH, water temperature and depth were registered in situ.
Fig. 2. Photographs of sampling sites during rainy (left picture) and dry season (right picture). Site 1 (A, B), site 2 (C, D), site 3 (E, F), site 4 (G, H), site 5 (I, J).
Ciliates identification
Water samples were immediately transported to the Laboratorio de Ictiología y Acuicultura, Universidad Autónoma del Estado de México (UAEMex). Ciliates were observed with bright field (Motic BA200) and phase contrast (Carl Zeiss) microscopy. Microphotographs and morphometric data were obtained with Motic Image Plus 2.0 software. Harris hematoxylin and nigrosine staining, and also dry silver nitrate impregnation techniques were used to reveal cytological structures (Klein,
1958; Borror, 1969; Lee et al., 1985; Foissner, 2014). For species identification, Foissner et al. (1991, 1992, 1994, 1995), Borror and Hill (1995), and Berger (1999) were consulted. Taxonomy was based on Lynn (2008).
For each species, their main food, as proposed by Foissner and Berger (1996), was considered, and then categorized into five trophic groups: bacterivorous, omnivorous, mixotrophic, bacteria-algae-heterotrophic flagellate consumers (BAF-consumers), and predators.
Statistical analysis
The species richness (number of species) registered in each sampling site (Magurran, 2004) was estimated and compared using U-Man Whitney test to determine the temporal variation between rainy and dry seasons.
We used presence-absence data of ciliate species, regarding the trophic groups, in each site during rainy and dry seasons to calculate frequency, and to identify changes in trophic structure of ciliate communities. Water temperature, pH and water depth of each sampling site were compared between rainy and dry seasons by using U-Man Whitney test to probe any factor that could be involved in the ciliate composition. All analyses were carried out in StatGraphics XVII software by using a confidence interval of 95%.
Results
Abiotic factors
Temperature, pH and water depth data are shown in Table 1. Water temperature and pH were not significantly different between seasons (p>0.05) in each sampling site, but water depth was greater in the rainy season than in the dry season (p<0.05).
Species richness and species composition
Thirty ciliate species were identified (Table 2, Figs 3 and 4) belonging to two subphyla, nine classes, 14 orders and 22 families.
Species richness was significantly different between dry (mean 13, total 29) and rainy (mean 6, total 24) seasons (U= 45.5, p<0.05), with dry season having higher species richness in all sampling sites (Fig. 5).
Site 1 showed the highest number of species (26
Table 1. Abiotic data of Atarasquillo wetland from Mexico (2012-2013).
Site Location Season pH Water temperature (°C) Depth water (cm)
1* 19°21'32.5" N, 99°31'6.3" W R 5.5±1 19±2.4 40
D 6.5±1 19.7±5.7 10
2* 19°21'23.1" N, 99°31'0" W R 5.5±0.5 20.5±1.9 60
D 6±0.8 18.2±3.5 40
3 19°20'36.7" N, 99°30'9.1" W R 5.5±0.5 18±2.1 150
D 5 17±7.1 50
4 19°20'36.7" N, 99°30'8.7" W R 5.5±0.5 15.7±1.5 120
D 5 15.2±6.8 50
5* 19°21'43.4" N, 99°30'32.8" W R 6.3±0.5 24.3±4.5 20
D 6.5±0.5 23±6.6 10
Notes. R - rainy season, D - dry season, * protected area sampling sites.
species), and the lowest number (17 species) was registered in site 5 (Table 2).
The community composition of ciliates in each sampling site was different during rainy and dry seasons (Table 2).
Seasonal composition of trophic groups
We observed eight bacterivorous species, eight BAF-consumers, seven omnivorous species, five predators and two mixotrophic species (Table 2).
The frequency of trophic groups in all sampling sites was different between rainy and dry seasons (Table 3; Fig. 6); however, bacterivorous and omnivorous species were more frequent than predator species during both seasons. Mixotrophic species were only found in two sites: 4 and 1.
In sites 1 and 5, during the rainy season, bacterivorous ciliates were more frequent (42.9 % in site 1, 51.6 % in site 5), as compared with dry season (18.4 % in site 1, 28.5 % in site 5), and omnivorous ciliates were more frequent during dry season (44 % site 1, 45.3 % site 5). In site 5, during rainy season about 22.6 % ofspecies were predator ciliates, but in dry season those were less frequent, as compared to the other sampling sites, both in rainy and dry season (except for the mixotrophic ciliate, Paramecium cf. bursaria from site 1). In site 3, omnivorous ciliates were more frequent (36 %) during rainy season than in dry season (25.5 %), and bacterivorous species were more frequent during dry season (36.6 %).
In site 4, omnivorous ciliates were more frequent in both seasons than other ciliates (35.4 % at rainy and 42. 1 % at dry season); mixotrophic ciliates were present in both seasons, but were more frequent during the dry season (14.8 %) than in rainy season (10.8 %).
BAF-consumers ciliates in sites 1, 2, 4 and 5 were more frequent during dry season than rainy season, while in site 3 they were more frequent during rainy season (Table 3).
Discussion
Diversity of ciliates in Atarasquillo marsh
Atarasquillo marsh provided the conditions for colonization of 30 free-living ciliate species during the 2012-2013.
The ciliate species richness in Atarasquillo marsh was greater than in two marshes in Florida, USA where only 3-5 ciliate species were recorded (Henebry et al., 1981), was similar to some peatbogs from poland (Mieczan, 2007a, 2009), and was lower than in Pantanal Mato Grosso in Brazil (55 species) (Lopes and Heckman 1996), suggesting the appropriate environmental conditions were present for ciliates.
All species have been previously recorded in other aquatic ecosystems, including wetlands (Lopes and Heckman, 1996; Kreutz and Foissner, 2006; Mieczan, 2008, 2009; Tirjakova and Vd'acny, 2013). With the exception of Glaucoma dragescui Corliss, 1971, recorded by Madrazo-Garibay and Lopez-ochoterena (1985) in Lerma marshes, all species are recorded for the first time in Mexican wetlands.
Species richness and composition
The composition of trophic groups and species richness during dry and rainy seasons was different in each sampling site (Figs 5 and 6). These results agree with studies of ciliate assemblages in some
Table 2. Ciliate species composition, seasonal and spatial distribution, and their trophic role
in Atarasquillo wetland from Mexico.
Species Trophic Rainy season Dry season
group Site 1 Site 2 Site 3 Site 4 Site 5 Site 1 Site 2 Site 3 Site 4 Site 5
Loxodes sp.* O - - - + - + + + + +
Blepharisma lateritium BAF +
(Ehrenberg)
Spirostomum minus Roux* B - + + - - - - + + -
Spirostomum teres Claparède & Lachmann* BAF - + + + - + + + + +
Spirostomum sp.* BAF - - - - - + + - - -
Stentor coeruleus (Pallas)* O + - + - - + + - + -
Stentor roeselii Ehrenberg* O + + + + - + + + + +
Aspidisca sp. * B + + + + + + + + + +
Euplotes moebiusi Kahl BAF + + + - + + + + - +
Euplotoides sp. M - - - + - - - - + -
Euplotoides eurystomus O + + +
(Wrzesniowski)
Halteria sp.* BAF + + - + + + + + + +
Stylonychia sp.* O + + + - - + + + + +
Caenomorpha sp. B - - - - - - - - + -
Brachonella sp. B - - - + - - - - + -
Didinium sp.* P - - - - - + - - - -
Lacrymaria sp.* P - - - - - + + - - -
Litonotus lamella (Müller)* P + + + + + + + + + +
Litonotus sp.* P + - - - + + - + - +
Chilodonella uncinata (Ehrenberg)* B + - - + + + + + + +
Coleps hirtus (Müller)* O + + + + + + + + + +
Prorodon sp.* P - - - - - + + - + -
Plagiopyla nasuta Stein BAF + + - + - - - - - -
Frontonia sp.* O + - - + - + + - + +
Paramecium aurelia complex B + + + - + + + + + +
Paramecium cf. bursaria* M - - - - - + - - + -
Paramecium caudatum Ehrenberg* BAF + + + + - + + + + +
Urocentrum turbo (Müller)* BAF + - + - - + - + + -
Cyclidium glaucoma Müller* B + + + + + + + + + +
Tetrahymena pyriformis B + + + + + + + + + +
complex
Species richness 17 14 15 16 10 25 20 18 23 17
Notes. * Previously recorded in wetlands (Henebry et al. 1981; Lopes and Heckman 1996; Mieczan 2007a, 2009); B - bacterivorous, BAF - consumers of bacteria, algae and small heterotrophic flagellates, M - mixotrophic, O -omnivorous, P - predators, + present, - absent.
Fig. 3. Ciliates from Atarasquillo wetland. A — Loxodes sp.; B — Blepharisma lateritium; C, D — Spirostomum minus; E, F — Spirostomum teres; G, H — Stentor coeruleus; I, J — Stentor roeselii; K, L — Euplotoides eurystomus; M — Aspidisca sp.; N, O — Euplotes moebiusi; P — Euplotoides sp. Abbreviations: AZM — adoral zone of membranelles, CV — contractile vacuole, SK — somatic kineties, Ma — macronucleus, PK — perioral kineties, FVC — frontoventral cirri, TC — transversal cirri, en — endosymbiotic algae. Scale bars: 50 ^m.
Fig. 4. Ciliates from Atarasquillo wetlands. A — Halteria sp.; B — Stylonychia sp.; C — Brachonella sp.; D — Caenomorpha sp.; E — Didinium sp.; F — Lacrymaria sp.; G — Litonotus lamella.; H — Chilodonella uncinata; I — Coleps hirtus; J — Prorodon sp.; K — Plagiopyla nasuta; L — Paramecium cf. bursaria; M — Paramecium caudatum; N — Parameciun aurelia; O — Urocentrum turbo; P — Tetrahymena pyriformis. Abbreviations: Br -bristles, CC - caudal cirri, Sp - spine, OC - oral cone, N - neck, Cyr - cyrtos, Cy - cytostome, OR - oral region, for explanation of other symbols see Fig. 3. Scale bars: 50 цт.
Table 3. Frequency (%) of ciliates trophic groups in every site during rainy and dry seasons.
Site 1* 2* 3 4 S*
Season R D R D R D R D R D
Bacterivorous 42.9 18.4 39.3 19.б 22.7 3б.2 23.1 14.8 S1.6 28.S
BAF-consumers 18.2 23.1 32.8 3б.9 32.0 28.2 23.1 2б.3 9.7 1б.8
Omnivorous 28.б 44.0 21.3 31.3 3б.0 2S.S 3S.4 42.1 1б.1 4S.3
Predators 10.4 13.2 б.б 12.1 9.3 10.1 7.7 1.9 22.б 9.S
Mixotrophic 0.0 1.3 0.0 0.0 0.0 0.0 10.8 14.8 0.0 0.0
Notes. R - rainy season, D - dry season, * protected area sampling sites.
peatbogs from Poland, which changed when reeds were removed, suggesting the involvement of physicochemical processes in determining community assemblages (Mieczan et al., 2018). In Atarasquillo wetland marsh some macrophytes, e.g. Hydrocotyle sp., Typha sp., are removed during the dry season by human activities, which may contribute to changes in ciliate richness and assemblage composition. In addition, heavy metals have been reported from Hydrocotyle sp. in surrounding areas ofAtarasquillo wetland (Ceballos, 2003; Zarazua et al., 2013), and it has been reported that heavy metals can be toxic to ciliates (Madoni and Giuseppa, 2006).
Most ofthe identified species: i.e., Spirostomum minus, Stentor coeruleus, S. roeselii, Chilodonella uncinata, Coleps hirtus, Paramecium caudatum (bacterivorous, BAF-consumers and omnivorous), were found in more than three sampling sites, including both or one season, and have been considered as freshwater common species due to their capacity to tolerate changes in their habitats (Foissner et al., 1991, 1992, 1994, 1995; Foissner and Berger, 1996; Pfister et al., 2002). Regarding their wide distribution, Spirostomum minus, S. teres, Paramecium aurelia, P. caudatum, Coleps hirtus, have been recorded in the five continents (Fokin, 2010; Bos-caro et al., 2014), and Stentor coeruleus, S. roeselii, S. minus, Euplotoides eurystomus in four continents (Foissner et al., 1991, 1992).
In site 5, where the vegetation coverage was lesser or absent relative to the other sites, the ciliate species richness was lower as well. Madoni (1991), Lugo et al. (1998), Song (2000) and Babko et al. (2010) concluded that habitats with macrophyte presence are appropriate for ciliate assemblages, with high content of organic matter favoring bacteria growing. Thus, we agree that macrophyte presence is an important factor for the assemblages of ciliates in wetlands, setting a microbial food web with bacterivorous ciliates and BAF-consumers, that are the
food resources for omnivorous and predator ciliates.
Seasonal variation of trophic groups
Seasonally we observed changes between bacterivorous and omnivorous ciliates (Fig. 6). In general, in sites 1, 2 and 5, during rainy season, most bacterivorous ciliates were found, in comparison to the dry season where the water level dropped off (Table 1), causing some changes in the composition of vegetation (Zepeda-Gomez et al., 2012a). Moreover, Ceballos (2003) reported in Lerma marshes that the total density of coliforms was lower during dry season than in rainy season. Indirectly we could assume that total coliforms are changing between seasons because our data showed the bacterivorous ciliates decreased in the dry season. Also, Debastiani et al. (2016) found a positive correlation between the presence ofbacterivorous ciliates and total coliforms. During the dry season, omnivorous ciliates were more frequent than the remaining groups, likely due to the advantages for a wider diet feeding on algae, protists and small metazoan (Foissner and Berger, 1996; Dias and D'Agosto, 2006).
Regarding ciliate composition in site 4, we observed that omnivorous ciliates were more frequent than other groups, and in addition, two mixotrophic ciliates were also observed, Paramecium cf. bursaria and Euplotoides sp. Mieczan (2009) observed a major percentage of mixotrophic and a relatively high percentage of omnivorous ciliates in Sphagnum-peatlands, similarly to our results. Furthermore, we found some anaerobic ciliates, i.e. Brachonella sp., Caenomorpha sp. and Plagiopyla nasuta (Foissner et al., 1994, 1995; Foissner and Berger, 1996; Guhl et al., 1996), and microaerophilic ciliates, i.e. Spirostomum teres (Madoni, 1991), probably due to low oxygen concentrations. This finding agrees with Headley and Tanner (2012) who showed that low dissolved oxygen concentrations are common in wetlands dominated by free-floating macrophytes,
Site 1 Site 2 Site 3 Site 4 Site 5
ISRainy IIBDry ifiSAnnual
Fig. 5. Ciliate species richness during rainy and dry seasons and for an annual period, for each sampling site.
as in site 4, which was covered in whole sampling period with free-floating macrophytes i.e. Marsilea mollis and Lemna sp., providing a barrier against aeration from the atmosphere. Sipauba-Tavares and Dias (2014) mentioned that shallow waters with macrophytes promote good conditions to maintain a highly diverse planktonic community and macrofauna associated with plants.
Only four species were categorized as predator ciliates and they were less frequent, as has been observed in other aquatic ecosystems (Mieczan, 2009; Babko et al., 2010).
Abiotic factors
Pfister et al. (2002) argued that the ecological preferences of some common ciliates seem to be wider, and that temperature, pH and oxygen seem to have only weak influence on the distribution of some ciliate species. All species from Atarasquillo wetland have been previously recorded in a wide range of temperature (Foissner et al., 1991, 1992, 1994, 1995; Pfister et al., 2002), and because our physicochemical results were not significantly different between seasons at each sampling site (p>0.05), we conclude that there was no influence of these factors on the ciliate species distribution (Figs 5 and 6, Table 1).
Further considerations
Most species that we found have been categorized as key species of a-mesosaprobic and P-meso-saprobic waters (Foissner and Berger, 1996);
however, we also found, mainly in site 4, species known as indicators of polysaprobic, metasaprobic and isosaprobic waters, i.e. Loxodes sp., Paramecium caudatum, Brachonella sp., Caenomorpha sp., Plagiopyla nasuta (Foissner and Berger, 1996; Luna-Pabello, 2006). Moreover, Brachonella sp., Caenomorpha sp. and Plagiopyla nasuta produce gas methane, thus, those ciliates could be used to determinate water quality in Lerma marshes, as in other aquatic ecosystems (Beaver and Crisman, 1989; Foissner and Berger, 1996; Jiang et al., 2011; Tirjakova and Vdacny, 2013; Debastiani et al., 2016).
Furthermore, our results showed that seasona-lity could be an important factor for the assemblages of ciliated trophic groups through changes in water level and vegetation composition.
Atarasquillo marsh is the most diverse and the most heterogeneous in composition of macrophyte communities than the other two Lerma marshes (Zepeda-Gomez et al., 2012a), and despite this wetland is under legal protection, it has been altered by anthropogenic activities resulting in lower water quality where some heavy metals have been found threatening the biota (Ceballos, 2003). Wetlands are important ecosystems playing a role as soil and minerals recyclers, climate stabilizers, and providing habitat for the biota (Mitsch and Gosselink, 2015), where ciliates are mineral recyclers in water as part of microbial food webs and could be used in further studies in monitoring the restoration of wetlands (Mieczan et al., 2018) like Lerma marshes, which are threatened of area reduction (Zepeda-Gomez et al., 2012b).
Fig. 6. Frequency of ciliate trophic groups during rainy and dry seasons in each sampling site (numbers 1-5).
Acknowledgements
The authors acknowledge Universidad Autónoma del Estado de México Project 3429/2013CHT for financial support of field research and Biól. M. Reyes-Santos, Lab. de Protozoología, Universidad Nacional Autónoma de México, for her assistance in staining and impregnations techniques. We thank to Dr. Rebecca Zufall, Department of Biology and Biochemistry, University of Houston, USA, for assisting with the English.
References
Babko R., Fyda J., Kuzmina T. and Hutorowicz A. 2010. Ciliates on the macrophytes in industrially heated lakes (Kujawy Lakeland, Poland). Vestn. Zool. 46 (6), 1-11.
Beaver J.R. and Crisman T.L. 1989. Analysis of the community structure of planktonic ciliated protozoa relative to trophic state in Florida lakes. Hydrobiologia. 174, 177-184.
Berger H. 1999. Monograph ofthe Oxytrichidae (Ciliophora, Hypotrichia). Kluwer Academy Pub., London.
Borror A.C. 1969. Application for stain-fixative nigrosin-HCl2-formalin to fragile or contractile ciliates. Trans. Am. Microsc. Soc. 88, 454-458.
Borror A.C. and Hill B.F. 1995. The order Euplotida (Ciliophora): taxonomy, with division of Euplotes into several genera. J. Eukaryot. Microbiol. 42, 457-466.
Boscaro V., Carducci D., Barbieri G., Senra M.V.X., Andreoli I., Erra F., Petroni G., Verni F. and Fokin S.I. 2014. Focusing on genera to improve species identification: Revised systematics of the ciliate Spirostomum. Protist. 165, 527—541.
Ceballos G. 2003. Ficha informativa de los humedales Ramsar (FIR): Ciénegas de Lerma. In: Ramsar sites information service. Available via pdf https://rsis.ramsar.org/ris/1335 accessed 28 November 2016.
Debastiani C., Meira B.R., Lansac-Töha M.N., Velho L.F.M. and Lansac-Töha F.A. 2016. Protozoa ciliates community structure in urban streams and their environmental use as indicators. Braz. J. Biol. 76, 1043-1053.
Dias R.J.P. and D'Agosto M. 2006. Feeding behavior of Frontonia leucas (Ehrenberg) (Protozoa, Ciliophora, Hymenostomatida) under different environmental conditions in a lotic system. Rev. Bras. Zool. 23, 758-763.
Finlay J.B. and Esteban G.F. 1998. Freshwater protozoa: biodiversity and ecological function. Biodivers. Conserv. 7, 1173-1186.
Foissner W. 2014. An update of 'basic light and scanning electron microscopic methods for taxonomic studies of ciliated protozoa'. Int. J. Syst. Evol. Microbiol. 64, 271-292.
Foissner W. and Berger H. 1996. An user friendly guide to the ciliates (Protozoa, Ciliophora) commonly used by hydrobiologists as bioindicators in rivers, lakes, and waste waters, with notes on their ecology. Freshwater Biol. 35, 375-482.
Foissner W., Berger H. and Kohmann F. 1994. Taxonomische und Ökologische Revision der Ciliaten des Saprobiensystems. Band III: Hyme-nostomata, Prostomatida, Nassulida. Informationsberichte des Bayer. Landesamts für wasserwirschaft. 1/94, 1-548.
Foissner W., Blatterer H., Berger H. and Kohmann F. 1991 Taxonomische und Ökologische Revision der Ciliaten des Saprobiensystems. Band I: Cyrtophorida, Oligotrichida, Hypotrichia, Colpo-dea. Informationsberichte des Bayer. Landesamts für wasserwirschaft. 1/91, 1-478.
Foissner W., Blatterer H., Berger H. and Kohmann F. 1992. Taxonomische und Ökologische Revision der Ciliaten des Saprobiensystems. Band II: Peritrichia, Heterotrichida, Odontostomatida. Informationsberichte des Bayer. Landesamts für wasserwirschaft. 5/92, 1-502.
Foissner W., Blatterer H., Berger H. and Kohmann F. 1995. Taxonomische und Ökologische Revision der Ciliaten des Saprobiensystems. Band IV: Gymnostomatea, Loxodes, Suctoria. Informationsberichte des Bayer. Landesamts für wasserwirschaft. 1/95, 1-540.
Foissner W., Chao A. and Katz L.A. 2008. Diversity and geographic distribution of ciliates (Protista: Ciliophora). Biodivers. Conserv. 17, 345-363.
Fokin S.I. 2010. Paramecium genus: biodiversity, some morphological features and the key to the main morphospecies discrimination. Protistology. 6 (4), 227-235.
Guerra V.M. and Ochoa G.S. 2006. Evaluación espacio-temporal de la vegetación y uso del suelo en la Reserva de la Biósfera Pantanos de Centla, Tabasco (1990-2000). Invest. Geog. 59, 7-25.
Guhl B.E., Finlay B.J. and Schink B. 1996. Comparison of ciliate communities in the anoxic hypolimnion of three lakes: general influence features and the influence of lake characteristics. J. Plankton Res. 18, 335-353.
Headley T.R. and Tanner C.C. 2012. Constructed wetlands with floating emergent macrophytes: an innovative stormwater treatment technology. Crit. Rev. Env. Sci. Tec. 42, 2261-2310.
Henebry M.S., Cairns J.J., Schwintzer C.R. and Yongue W.H.J. 1981. A comparison ofvascular vegetation and protozoa communities in some freshwater wetlands of Northern Lower Michigan. Hydrobiologia. 83, 353-375.
Jiang Y., Xu H., Hu X., Zhu M., Al-Rasheid K.A.S. and Warren A. 2011. An approach to analy-
zing spatial patterns of planktonic ciliates communities for monitoring water quality in Jiaozhou Bay, northern China. Mar. Pollut. Bull. 62, 227235.
Johnson M.D. 2011. Acquired phototrophy in ciliates: a review of cellular interactions and structural adaptations. J. Eukaryot. Microbiol. 58, 185-195.
Klein B.M. 1958. The "dry" silver method and its proper use. J. Protozool. 5, 99-103.
Kreutz M. and Foissner W. 2006. The sphagnum ponds of Simmelried in Germany: a biodiversity Hot-Spot for microscopic organisms. Protozo-ological Monographs. 3, 1-267.
Lee J.J., Small E.B., Lynn D.H. and Bovee E.C. 1985. Some techniques for collecting, cultivating and observing protozoa. In: An illustrated guide to the protozoa (Eds: Lee J.J., Hutner S.H. and Bovee E.C.). Society of Protistologists, Lawrence, Kansas, pp. 1-7.
Lopes H.E. and Heckman C.W. 1996. The seasonal sucession of biotic communities in wetlands of the Tropical wet-and-dry climatic zone: IV. The free-living sarcodines and ciliates of the Pantanal ofMato Grosso, Brazil. Int. Rev. gesamten Hydrobiol. Hydrogr. 81, 367-384.
Lugo A., Alcocer J., Sánchez M.A. and Escobar E. 1998. Littoral protozoan assemblages from two Mexican hyposaline lakes. Hydrobiologia 381, 9-13.
Luna-Pabello V.M. 2006. Atlas de ciliados y otros microorganismos frecuentes en sistemas de tratamiento aerobio de aguas residuales. Facultad de Química, Universidad Nacional Autónoma de México, México.
Lynn D.H. 2008. The ciliated protozoa. Characterization, classification, and guide for the literature. Springer, New York.
Madoni P. 1991. Community structure and distribution of the ciliate protozoa in a freshwater pond covered by Lemna minor. Boll. Zool. 58, 273-279.
Madoni P. 2005. Ciliated protozoan communities and saprobic evaluation of water quality in the hilly zone of some tributaries of the Po River (northern Italy). Hydrobiologia. 541, 55-69.
Madoni P. and Giuseppa M. 2006. Acute toxicity of heavy metals towards to freshwater ciliated protists. Environ. Pollut. 141, 1-7.
Madrazo-Garibay M. and López-Ochoterena E. 1985. Protozoarios ciliados de México XXV. Estomatogénesis en Glaucoma dragescui Corliss,
1971 (Oligohymenophorea, Hymenostomatida). Rev. Lat-amer. Microbiol. 27, 45-48.
Magurran A.E. 2004. Measuring biological diversity. Blackwell Publishing, Oxford.
Mieczan T. 2007a. Epiphytic protozoa (testate amoeba and ciliates) associated with Sphagnum in peatbogs: relationship to chemical parameters. Pol. J. Ecol. 55, 79-90.
Mieczan T. 2007b. Seasonal patterns of testate amoeba and ciliates in three peatbogs: relationship to bacteria and flagellates (Poleski National Park, Eastern Poland). Ecohydrol. Hydrobiol. 7, 79-88.
Mieczan T. 2008. Diversity and vertical distribution ofplanktonic ciliates in a stratified mesotrophic lake: relationship to environmental conditions. Oceanol. Hydrobiol. Stud. 37, 83-95.
Mieczan T. 2009. Ciliates in Sphagnum peat-lands: vertical micro-distribution, and relationship of species assemblages with environmental parameters. Zool. Stud. 48, 33-48.
Mieczan T., Adamczuk M. and Pogorzelec M. 2018. Ciliates as restoration indicators in peatbogs - 10 years of study. Eur. J. Protistol. 62,11-23.
Mitsch W.J. and Gosselink J.G. 2015. Wetlands. Wiley, New Jersey.
Pfister G., Auer B., Arndt H. 2002. Pelagic ciliates (Protozoa: Ciliophora) of different brackish and freshwater lakes - a community analysis at the species level. Limnologica. 32, 147-168.
SEMARNAT. 2002. Decreto por el que se declara área natural protegida, con el carácter de área de protección de flora y fauna, la región conocida como Ciénegas de Lerma en el Estado de México, con una superficie total de 3,023-95-74.005 hectáreas. Diario Oficial de la Federación 27 de Noviembre 2002, Secretaría de Medio Ambiente y Recursos Naturales, México. pp. 4-12.
Sipaúba-Tavares L.H. and Dias S.G. 2014. Water quality and communities associated with macrophytes in a shallow water-supply reservoir on an aquaculture farm. Braz. J. Biol. 74 (2), 420—428.
Song B. 2000. A comparative study on planktonic ciliates in two shallow mesotrophic lakes (China): species composition, distribution and quantitative importance. Hydrobiologia. 427, 143—153.
Tirjaková E. and Vdacny P. 2013. Analysis and evolution ofwater quality ofthe upper Váh river (northern Slovakia) by long-term changes in the community structure of ciliates (Protista: Ciliophora). Biologia. 68, 667-678.
Weisse T. 2002. The significance of inter- and intraspecific variation in bacterivorous and herbivorous protists. Antonie van Leeuwenhoek. 81, 327-341.
Weisse T. 2017. Functional diversity of aquatic ciliates. Eur. J. Protistol. 61, 331-358.
Zarazúa G., Ávila-Pérez P., Tejeda S., Valdivia-Barrientos M., Zepeda-Gómez C. and Macedo-Miranda G. 2013. Evaluación de los metales pesados Cr, Mn, Fe, Cu, Zn y P en sombrerillo de agua (Hydrocotyle ranunculoides) del curso Alto del Río Lerma, México. Rev. Int. Contam. Ambient. 29, 17-24.
Zepeda-Gómez C., Lot-Helgueras A., Nemiga X.A. and Madrigal-Uribe D. 2012a. Florística y diversidad de las Ciénegas del Río Lerma Estado de México, México. Acta Bot. Mex. 98, 23-49.
Zepeda-Gómez C., Nemiga X.A., Lot-Holgue-ras A. and Madrigal-Uribe D. 2012b. Análisis del cambio del uso de suelo en las ciénegas de Lerma (1973-2008) y su impacto en la vegetación acuática. Invest. Geog. 78, 48-61.
Address for correspondence: Daniel Méndez-Sánchez. Facultad de Ciencias, Universidad Autónoma del Estado de México, campus El Cerrillo, Piedras Blancas, Desviación Tlachaloya, Carretera Toluca -Atlacomulco Kilómetro 15.5, C.P. 50200, Toluca, Edo. de México, Mexico; e-mail: [email protected], [email protected].
