Epilithic diatoms (Bacillariophyceae) as indicators of water quality in the Upper Lerma River, Mexico

Diatomeas epilíticas como indicadores de la calidad del agua en la cuenca alta del río Lerma, México

Virginia Segura–García,^1,2 Enrique A. Cantoral–Uriza,³ Isabel Israde⁴ and Nora Maidana⁵

¹ Facultad de Biología, Universidad Michoacana de San Nicolás de Hidalgo. Avenida Francisco J. Mujica s/n, Ciudad Universitaria, Col. Felicitas del Río, Morelia, Michoacán. 58040. México.

² Posgrado de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México (UNAM).

⁴ Departamento de Geología y Mineralogía, Instituto de Investigaciones Metalúrgicas, Edificio U. Universidad Michoacana de San Nicolás de Hidalgo. Ciudad Universitaria, Morelia, Michoacán. 58060. México.

⁵ Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires. Ciudad Universitaria, Pabellón 2, 4° piso, Laboratorio 15. C1428EHA–Buenos Aires, Argentina.

Recibido: 13 de mayo de 2010.
Aceptado: 7 de septiembre de 2011.

ABSTRACT

The upper Lerma River is the most economically important basin of Mexico because it is the region where 80 % of the commercial activity of the country takes place, with 3500 industries, 750,000 Ha of irrigated land and 14 cities with populations over 100,000 inhabitants. Despite this relevance, little or no waste water treatment is done in the basin, which results in high contamination levels. The present paper deals with the taxonomy and ecology of epilithic diatoms collected at 11 sites in the basin in the dry and post–rainy seasons of the 2003–2005 period. This is the first study in an environmental direction of the diatoms of the upper Lerma River basin and the information generated will be used to propose, in the short–term, a Lerma River diatom index (IDL), supporting water quality monitoring programs. 178 taxa were recognized, of which 112 taxa (63%) were cosmopolitan or widely distributed. The genera with most species were Nitzschia (34), Navicula (19), Gomphonema (15), and Pinnularia (11). The dominant species in the studied locations and study period were Eolimna subminuscula(Manguin) Moser, Lange–Bertalot etMetzeltin, Gomphonemaparvulum(Kützing) Kützing, Navicula veneta Kützing, Nitzschia capitellata Hustedt, N. sublinearis Hustedt, N. umbonata (Ehrenberg) Lange–Bertalot and Sellaphora pupula (Kützing) Mereschkowsky, which are characterized as tolerant to α–mesosaprobic to polysaprobic conditions, and to high nitrogen content. Trends in distribution of diatom species in the sampling sites were explained by variations in environmental parameters such as depth, conductivity, pH, temperature, and total dissolved solids.

Key words: Diatoms, Bacillariophyta, Lerma River, environmental quality, Mexico.

RESUMEN

La cuenca alta del río Lerma es la más importante de México desde el punto de vista económico, ya que en ella ocurren el 80 % de las actividades comerciales del país, con 3500 industrias diversas, 750,000 hectáreas de tierras de riego y 14 ciudades con poblaciones de más de 100,000 habitantes. El escaso o nulo tratamiento de las aguas residuales, trae como consecuencia una elevada contaminación. Este trabajo abordó el estudio taxonómico y ecológico de diatomeas epilíticas colectadas en 11 localidades de ésta cuenca, entre los años 2003–2005. Se trata del primer estudio con una orientación ambiental que se realiza sobre diatomeas de la cuenca alta de este río, y la información generada permitirá proponer en el corto plazo un índice diatomológico para el Río Lerma (IDL), que posibilite emprender programas de monitoreo de la calidad del agua. Se reconocieron 178 especies, de las cuales 112 taxones (63 %) fueron de amplia distribución. Los géneros con mayor número de especies fueron Nitzschia (34), Navicula (19), Gomphonema (15) y Pinnularia (11). Las especies dominantes en las localidades de estudio y en las épocas de recolecta fueron Eolimna subminuscula (Manguin) Moser, Lange–Bertalot et Metzeltin, Gomphonema parvulum (Kützing) Kützing, Navicula veneta Kützing, Nitzschia capitellata Hustedt, N. sublinearis Hustedt, N. umbonata (Ehrenberg) Lange–Bertalot y Sellaphora pupula (Kützing) Mereschkowsky, que se caracterizan por ser tolerantes a condiciones α–mesosapróbicas a polisapróbicas con alto contenido de nitrógeno. La distribución de las especies de diatomeas fueron explicadas por las variaciones en parámetros como profundidad, conductividad, pH, temperatura y sólidos disueltos totales.

Palabras clave: Diatomeas, Bacillariophyta, Río Lerma, calidad ambiental, México.

INTRODUCTION

The research about algae in Mexico considering the diatoms in lotic environments has emphasized floristic aspects (Cantoral & Montejano, 1993; Cantoral et al., 1997; Valadez–Cruz et al., 1996; Ramírez et al., 2001; Novelo et al., 2007), taxonomy (Cantoral, 1997; Oliva et al., 2006, 2008; Segura–García et al., 2010), geographical distribution (Ramírez & Cantoral, 2003) and ecological topics, as well as their use as biological indicators (Bojorge & Cantoral–Uriza, 2007; Cantoral–Uriza & Mora, 2012; in press).

The Lerma–Chapala basin has had a remarkable economical growth and generates many products for the country. Furthermore, 80% of the national commercial activity takes place in the basin (Mestre–Rodríguez, 1997) in which 3500 diverse industries, 750,000 Ha of irrigated fields, and 14 cities with more than 100,000 inhabitants are located. All this makes it the more densely populated region in the country with over 9'000,000 inhabitants (INEGI, 1983; INE, 2003).

These agricultural, industrial, and urban activities taking place without adequate and integrated water management converted the Lerma River into one of the most polluted of Mexico, causing negative effects that have not been completely quantified such as the disappearance of flora and fauna in some regions (Medina–Nava, 2003).

Due to the importance of the basin both as a center of species origin and diversification (Díaz–Pardo et al., 1993; Moncayo et al., 2001), and as a site of abundant natural resources, it is a priority to propose methods for identifying bioindicator organisms that could reflect the prevailing environmental conditions, enable their monitoring, and allow for the evaluation of water quality; all of which would facilitate ecosystem management decision making.

MATERIALS AND METHODS

Study area. The Lerma–Chapala Basin, located in central Mexico between 19° 03' to 21° 34' N and 99° 16' to 103° 31' W, has an area of 53,591 Km² from the Lerma River headwaters in the Nevado de Toluca at 4600 m a.s.l. to its mouth in the Chapala Lake at 1600 m a.s.l., and covers territory from five states (State of México, Guanajuato, Querétaro, Michoacán and Jalisco; Cotler et al., 2004; Cotler et al., 2006).

The present research focused on the upper Lerma River sub–basin (19° 37' 30" to 20° 08' 32" N and 100° 35' 43" W) located in the Trans Mexican Volcanic Belt that was originated by the subduction of the Pacific and Cocos Plate under the North American Plate (Israde–Alcántara, 1999; Fig. 1, Table 1). It is formed by stratovolcanoes, cineritic cones and calderas that emitted volcanic breccias, tuffs and detrictic materials that accumulated since the Neogene and throughout the Holocene.

Different types of soils are distinguished in the sub–basin, the most abundant being Luvic Feozem, Luvisol, Planosol and Andosol, while Vertisol and Litosol are less represented (SPP, 1985). The climate is temperate with average temperatures of 18 °C in the valleys and plains and of 12.5 °C in the mountains (Mil Cumbres). The annual precipitations range between 646 to 1642 mm and the vegetation types include fir (Abies), pine (Pinus) and pineoak [Pinus–Quercus] forests, gallery forests (Salix bonplandiana Kunth, Taxodium mucronatum Ten.), and altered subtropical shrub (SPP, 1985).

Sample collection. Samples of water and epilithic diatoms were collected during the dry (April to June) and post–rainy (November–December) seasons of the 2003–2005 period. The chosen sampling sites were approximately 10 Km apart from each other and near populated areas, according to the criteria established by Israde–Alcántara et al. (2007). We considered the province division of the Lerma River proposed by Moncayo et al. (2001) based on the highly endemic ichthyofauna. Eight sites were sampled in the main course of the river, and three more in the tributaries.

The sampling sites were chosen taking into account the different human activities and land uses occurring in the basin, and attempting to obtain samples from sites located both upstream and downstream, and from villages or cities.

Depth was measured with an electric sounding line. Water temperature, specific conductivity (K₂₅) and pH were measured with a Conductronic (PC–18) potentiometer. Dissolved solids were recorded using a HORIBA Multiparameter meter and dissolved oxygen concentration, with a portable YSI (51–B) meter (Table 2).

Epilithic diatoms were collected according to the method proposed by Iserentant et al. (1999), by brushing 10 cm² area of submerged rocks with disposable tooth brushes. The samples were stored in plastic bottles and fixed in situ with 4% formaldehyde solution.

Diatoms were observed with light microscopes (LMs) (Reichert–Jung–Polivar and Olympus Bimax 50) equipped with Nomarski interference optics, and digital photographic cameras (Sony Cybershot and Olympus DP12). Apical and transapical axis lengths, and striae density were measured on at least 20 specimens for each species in the same locality. Minimum and maximum values, average, and standard deviation for each morphometric parameter were estimated to show the variation in populations. When necessary for taxonomic identification, the scanning electronic microscopes (SEMs) Phillips XL 30 (Museo Argentino de Ciencias Naturales, Buenos Aires, Argentina), and JEOL JSM 6400 (IIM–UMSNH) were used.

Taxonomic identifications were based on Patrick and Reimer (1966); Gasse (1980, 1986); Germain (1981); Ehrlich (1995); Cox (1996); Cantoral (1997); Krammer (1997); Krammer and Lange–Bertalot (1997a, b; 2004a, b); Metzeltin and Lange–Bertalot (1998, 2002); Novelo (1998); Rumrich et al. (2000); Lange–Bertalot (2001); Metzeltin and García–Rodríguez (2003); Werum and Lange–Berta–lot (2004); Díaz and Maidana (2005); Metzeltin et al. (2005); Oliva–Martinez et al. (2005), and Novelo et al. (2007). The environmental preferences of taxa were also consulted in the above–mentioned references.

For the statistical analysis, 400 valves were counted per slide (Kelly et al., 1998) in all samples for obtaining the relative abundance of taxa. To explore the relations between species and environmental variables a Canonic Correspondence Analysis (CCA) was performed considering the frequencies of the most abundant species (>3%) (CANOCO program; ter Braak, 1990). The significance of the canonical axes was tested using a Monte Carlo permutation test of samples.

RESULTS

The physicochemical characteristics of the Lerma River define it as a temperate waterbody with temperatures from 14 to 24.5 °C in the post–rainy season, and between 16–24.1 °C in the dry season. pH varies from 5 to 10.8, and the conductivity values are characteristic of freshwaters with low to moderate mineralization (117917 μS cm^–1). The dissolved oxygen concentration (OD mg L^–1) and oxygen saturation percent (OS %) range from hypoxic conditions (0.1 mg L^–1 and 1 OS %) in localities with industrial activity, agro–chemical drainage from farming areas and high eutrophication, to very well oxygenated waters (10 mg L^–1 and 115 OS %) in sites where geomorphological variations favor the increase of current velocity. The minimum depth was registered during the dry season (10 cm) and the maximum, in the post rainy season (220 cm, El Pedregal) (Table 2).

In the revision with LMs, 53 genera and 178 infrageneric taxa were identified, of which 112 (63%) are cosmopolitan or have wide distribution. The genera with higher number of species were Nitzschia (34), Navicula (19), Gomphonema (15), and Pinnularia (11). Cocconeis placentula var. euglypta, Eolimna subminuscula, Gomphonema parvulum, Navicula veneta, Nitzschia capitellata, N. umbonata, N. palea, and Sellaphora pupula were present throughout the period of study (Table 3).

As show in Table 3, the rivers Laja and Querétaro were characterized by low specific richness and the abundance of few taxa, such as Nitzschia amphibia and N. capitellata in the former, and N. capitellata and N. umbonata in the latter. In Pedregal Spring a high abundance of some species characteristic of oligotrophic and highly oxygenated waters was observed, such as Rhoicosphenia abbreviata and Eolimna tantula.

The CCA for the most abundant species (>3%) showed an environment–species correlation of 50.8%, the highest percentage of the explained variation (77.1%) being due to the first two canonical axis. The first eigen values in the Monte Carlo permutation test showed highly significant relations between the species and the chosen variables (p = 0.002). These results suggest that the distribution tendencies of the more abundant species in the sampling sites may be explained by the variables included in the model: depth, conductivity, pH, temperature, and total dissolved solids (Fig. 2).

Temperature was the variable that seemed to be more related with the distribution of Eolimna tantula, Nitzschia microcephala Grunow and Planothidium frequentissimum, while presence of Eolimna subminuscula, Gomphonema lagenula, G. parvulum, Navicula germainii Wallace, Nitzschia capitellata, N. palea, N. umbonata, N. levidensis (W.Smith) Grunow, Sellaphora pupula, and Stephanocyclus meneghiniana was positively and significantly correlated with conductivity. On the other side, Luticola goep–pertiana, L. mutica, Navicula antonii Lange–Bertalot, Nitzschia dissipata var. dissipata (Kützing) Rabenhorst, and N. frustulum were positively correlated with depth. In Fig. 3A–Z shows the main diatoms as indicators of water quality in the Lerma River.

DISCUSSION

The Lerma River was characterized as a highly polluted and eutrophic system due to a constant throughout the year drainage of high nutrient content wastewaters from industrial, agricultural, and urban activities.

The physicochemical data showed a clear discrimination of the studied sites having a high conductivity such as Puente Lerma, San Jerónimo Ixtapatango, San Lorenzo Tlacotepec, Pedregal, Uruétaro, and Laja River, in which the discharges of industrial and urban activity of sites within the State of México are very intense, as are those of sewage derived from agricultural activities located in the states of Michoacán and Guanajuato. Sampling sites with both high dissolved oxygen content and high oxygen saturation percent were San Jerónimo Ixtapatongo, Temazcalcingo Bridge, Pedregal Spring, Chamácuaro, and El Capulín, localities in which the river has zones with boulders or large rocks that increase the oxygenation of the system.

Known taxocenoses are dominated by species of the genera Nitzschia, Navicula and Gomphonema, similar to those observed in several lentic bodies named "bordos" in the state of Guanajuato near the Lerma River (Cantoral–Uriza & Mora, in press). The presence of a large number of Nitzschia species that are tolerant to a wide range of environmental conditions (Dere et al., 2006; Cantoral–Uriza & Mora, in press) evidenced the hypereutrophic conditions that predominated in the Lerma River during the research period.

The rivers Laja and Querétaro, considered as referents for highly disturbed conditions, have a low species diversity and are dominated by species characteristic of organic matter enriched waters such as Nitzschia capitellata present in both rivers, and N. amphibia and N. umbonata, occurring in the former and the latter water bodies, respectively. Pedregal Spring, dominated by Eolimna tantula, Amphora copulata (both exclusive of this location), and Rhoicosphenia abbreviata, was the referent for less disturbed waters in the Lerma River. The latter three taxa have been recorded for waters with low nutrient concentrations and conductivities, although E. tantula may tolerate hypereutrophic conditions (Lange–Bertalot, 2001; Ramírez & Plata–Díaz, 2008). A. copulata and R. abbreviata are sensitive to the increase of conductivity (Maidana et al., 2005) and may grow in places with high current velocity (Walker & Pan, 2006). R. abbreviata may also reflect the continual industrial and urban activity talking place in the basin (Walker & Pan, 2006).

CCA grouped some species that are sensitive to oxygen saturation percent (Fig. 2). This group includes high oxygen concentration demanding species such as Luticola mutica (100% saturation), Nitzschia dissipata (75%), and Nitzschia frustulum (50%) (van Dam et al., 1994).

Most of the dominant species (i.e., Eolimna subminuscula, Gomphonema parvulum, Luticola goeppertiana, Nitzschia amphibia, N. capitellata, N. palea, N. umbonata, and Sellaphorapupula) have been characterized in the literature as being tolerant to high electrolyte contents in rivers highly contaminated with industrial waste (Germain, 1981; van Dam et al., 1994; De Wolf, 1982; Lobo et al., 1995; Cox, 1996; Cantoral, 1997; Krammer & Lange–Bertalot, 1997b; Novelo, 1998; Lange–Bertalot, 2001; Dere et al., 2006; Ndiritu et al., 2006; Novelo et al., 2007), and thus, the presence of these species could be considered to be indicators of similar conditions in the upper Lerma River.

Gomphonema parvulum and Nitzschia palea, observed in areas of agricultural runoff such as San Jerónimo Ixtapatongo, Temazcalcingo Bridge, El Capulín, and Uruétaro, have also been found in rivers with high concentrations of nitrates and phosphates near agricultural land in the U.S., Japan, Poland, and Germany (Lobo et al., 1995; Leland & Porter, 2000; Köster & Hübener, 2001; Sczepocka & Szulc, 2006; Zampella etal., 2007).

Species such as Achnanthidium minutissimum, Rhoicosphenia abbreviata, and Navicula antonii indicate slightly better conditions of oxygenation whitin the Lerma River (Krammer & Lange–Bertalot, 1985, 2004b). While Nitzschia sublinearis, N. palea, and Luticola goeppertiana are species that may reflect conditions of intermediate pollution, in the present study they were observed to occur only in low relative abundances (Krammer & Lange–Bertalot, 1997b; Salomoni et al., 2006).

The observed decrease in biodiversity and the changes in species composition in the most altered zones of the river during the sampling years could be accounted for by changes in water quality due to the increase of pollution in the system given that, as has been shown by Stevenson (1997), communities may adapt themselves to environmental stress througth a change in species composition. Thus, in highly contaminated places of the upper Lerma River, medium to small sized species such as Eolimna subminuscula and Nitzschia palea were found, while medium to large size individuals of Ulnaria ulna, Nitzschia umbonata, and Sellaphora pupula were found in places with relatively less environmental perturbation; all of the above–mentioned species were found to be amply distributed in the study area, and the latter three are considered as tolerant to moderate organic pollution (Martinez de Fabricius et al., 2003).

We concluded that the environmental information based on a precise taxonomic description from the epilithic diatoms and understanding of ecological preferences that was generated in the present study may represent a relevant constribution for a region of great economic importance in Mexico.

As show by the results of CCA, the distribution of epilithic diatoms species in the study area is closely linked to chemical and physical characteristics of water (particularly to depth, conductivity, pH, temperature, and total dissolved solids), and is also associated to the different types and the intensities of human activities taking place along the upper Lerma River sub–basin.

The environmental and taxonomic information of this study will be of aid for designing water quality monitoring programs using epilithic diatoms species that were shown by our study to be bioindicators, and because they provide tools to develop a series of management activities aimed at improving water quality, therefore bettering the quality of life of people that depend on this resource.

ACKNOWLEDGMENTS

This project was financed by CONACyT (SEP–2003–CO2–44693/A–1). The authors acknowledge Rodrigo Velásquez for his help during field work and Salvador Almanza for his aid in the elaboration of diatom figures.

REFERENCES

Bojorge, M. & E. Cantoral–Uriza. 2007. Estructura comunitaria de diatomeas asociadas a talos de Prasiola mexicana (Chlorophyta) en el río Magdalena, D.F. Hidrobiológica 17 (1): 11–22.         [ Links ]

Cantoral, E. A. 1997. Diatomeas (Bacillariophyceae) de ambientes lóticos en la cuenca baja de la Huasteca Potosina. Tesis de Doctorado. Facultad de Ciencias. División de Estudios de Posgrado. Universidad Nacional Autónoma de México. 201 p.         [ Links ]

Cantoral, E. & G. Montejano. 1993. Las algas de la localidad El Salto (San Luis Potosí, México), un ejemplo de estudios florísticos en ambientes cambiantes. Boletín de la Sociedad Botánica de México 53: 3–20.         [ Links ]

Cantoral–Uriza, E., J. Carmona & G. Montejano. 1997. Diatoms of calcareous tropical springs in the central region of Mexico. Cryptogamie Algologie 18 (1): 19–46.         [ Links ]

Cantoral–Uriza, E. & L. Mora. Diatomeas en bordos de la subcuenca San Miguel Allende, Guanajuato. In: Estudio de Estado sobre la Biodiversidad de Guanajuato. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (CONABIO) – Instituto de Ecología del Estado de Guanajuato. (In press).         [ Links ]

Cotler, H., A. Priego, C. Rodríguez, C. Enríquez & J. C. Fernández. 2004. Determinación de zonas prioritarias para la eco–rehabilitación de la cuenca Lerma–Chapala. Dirección de Manejo Integral de Cuencas Hídricas. Dirección General de Investigación de Ordenamiento Ecológico y Conservación de Ecosistemas. Instituto Nacional de Ecología. Ciudad de México, 29 p.         [ Links ]

Cotler, A, H., M. Mazarí & J. de Anda (Eds.). 2006. Atlas de la Cuenca Lerma–Chapala, construyendo una visión conjunta. Secretaría de Medio Ambiente y Recursos Naturales, Instituto Nacional de Ecología, Universidad Nacional Autónoma de México, Instituto de Ecología. México, 196 p.         [ Links ]

Cox, E. 1996. Identification of freshwater diatoms from live material. Chapman & Hall. Oxford. 158 p.         [ Links ]

De Wolf, H. 1982. Method of coding of ecological data from diatoms for computer utilization. Mededelingen Rijks Geologische Dienst. 36 (2): 95–98.         [ Links ]

Dere, S., N. Dalkiron, D. Karacaoglu, A. Elmaci, B. Dúlger & E. Sentúrk. 2006. Relationship among epipelic diatom taxa, bacterial abundances and water quality in a highly polluted stream catchment, Bursa–Turkey. Environmental Monitoring and Assessment 112: 1–22.         [ Links ]

Díaz–Pardo, E., M. A. Godínez–Rodríguez, E. López–López & E. Soto–Galera. 1993. Ecología de los peces de la cuenca del río Lerma, México. Anales de la Escuela Nacional de Ciencias Biológicas 39: 103–127.         [ Links ]

Díaz, P. C. & N. I. Maidana. 2005. Diatomeas de los salares. Atacama y Punta Negra. II Región Chile. Centro de Ecología Aplicada. Minera Escondida Ltda. Santiago de Chile. 146 p.         [ Links ]

Ehrlich, A. 1995. Atlas of the inland–water diatom flora of Israel; Flora Palaestina. The Geological Survey of Israel. The Israel Academy of Sciencies and Humanities. Israel. 166 p.         [ Links ]

Gasse, F. 1980. Les diatomées lacustres plio–pléistocènes du Gadeb (Éthiopie). Systématique, paléoécologie, biostratigraphie. Revue Algologique, Memoire Hors–Série 3: 249.         [ Links ]

Gasse, F. 1986. East african diatoms, Taxonomy, ecological, distribution. Bibliotheca Diatomologica, Vol. 011. 292 p.         [ Links ]

Germain, H. 1981. Flore des Diatomées, Diatomophycées, eux douces et saumâtres du Massif Armoricain et des contrées voisines d'Europe occidentale. Boubée. Paris. 444 p.         [ Links ]

Instituto Nacional de Ecología (INE). 2003. Diagnóstico bio–físico y socioeconómico de la Cuenca Lerma–Chapala. Dirección de Investigación de Ordenamiento Ecológico y Conservación de Ecosistemas. Dirección de Manejo Integral de Cuencas Hídricas. 258 p.         [ Links ]

Instituto Nacional de Estadística, Geografía e Informática (INEGI). 1983. X Censo General de Población y Vivienda 1980. Resumen. México. 395 p.         [ Links ]

Iserentant R., L. Ector, F. Straub & D. U. Hernández–Becerril. 1999. Méthodes et techniques de préparation des échantillons de diatomées. Cryptogamie Algology 20: 143–148.         [ Links ]

Israde–Alcántara, I. 1999. Lagos tectónicos y volcánicos de Michoacán. In: Corona Chávez, P. & I. Israde–Alcántara (Eds.). Carta geológica del estado de Michoacán. Escala 1:250,000. Instituto de Investigaciones Metalúrgicas; Departamento de Geología y Mineralogía. Secretaría de Difusión Cultural y Extensión Universitaria. Universidad Michoacana de San Nicolás de Hidalgo, Michoacán, México, pp. 46–74.         [ Links ]

Israde–Alcántara, I., V. Segura–García, N. Abarca, L. Ector, E. Cantoral–Uriza & M. Mendoza–Cantú. 2007. Diatomeas del Río Lerma, estimación de la calidad del agua de un río fuertemente contaminado. Resultados preliminares. Memorias del Congreso Nacional y Reunión Mesoamericana de Manejo de Cuencas Hidrográficas, Querétaro. Disco compacto.         [ Links ]

Kelly, M. G., A. Cazaubon, E. Coring, A. Dell'Uomo, L. Ector, B. Goldsmith, H. Guasch, J. Hürlimann, A. Jarlman, B. Kawecka, J. Kwandrans, R. Laugaste, E.–A. Lindstrøm, M. Leitao, P. Marvan, J. Padisák, E. Pipp, J. Prygiel, E. Rott, S. Sabater, H. van Dam & J. Vizinet. 1998. Recommendations for the routine sampling of diatoms for water quality assessments in Europe. Journal of Applied Phycology 10: 215–224.         [ Links ]

Köster, D. & T. Hübener. 2001. Application of Diatom Indices in a planted ditch constructed for tertiary sewage treatment in Schwaan, Germany. Internationale Revue der Gesamten. Hidrobiology 86: 241–252.         [ Links ]

Krammer, K. 1997. Die cymbelloiden Diatomeen; Eine Monographie der weltweit bekannten Taxa. Teil 2, Encyonema part., Encyonopsis and Cymbellopsis. Bibliotheca Diatomologica. Band 37. J. Cramer. Berlin. 469 p.         [ Links ]

Krammer, K. & H. Lange–Bertalot. 1985. Naviculaceae. Neue und wenig bekannte Taxa, neue Kombinationen und Synonyme sowie Bemer–kungen zu einigen Gattungen. Bibliotheca Diatomologica 9: 1–230.         [ Links ]

Krammer, K. & H. Lange–Bertalot. 1997a. Bacillariophyceae 2/1. Teil: Na–viculaceae. In: Ettl, H., J. Gerloff, H. Heynig & D. Mollenhauer (Eds.). Süßbwasserflora von Mitteleuropa. Gustav Fisher Verlag. Stuttgart, Germany. 876 p.         [ Links ]

Krammer, K. & H. Lange–Bertalot. 1997b. Bacillariophyceae 2/2. Teil: Ba–cillariaceae, Epithemiaceae, Surirellaceae. In: Ettl, H., J. Gerloff, H. Heynig & D Mollenhauer (Eds.). Süßbwasserflora von Mitteleuropa. Gustav Fisher Verlag. Stuttgart, Germany. 437 p.         [ Links ]

Krammer, K. & H. Lange–Bertalot. 2004a. Bacillariophyceae. 2/3. Teil : Centrales, Fragilariaceae, Eunotiaceae. In: Ettl, H., J. Gerloff, H. Heynig & D Mollenhauer (Eds.). Süßbwasserflora von Mitteleuropa. Gustav Fisher Verlag. Stuttgart, Germany. 598 p.         [ Links ]

Krammer, K. & H. Lange–Bertalot. 2004b. Bacillariophyceae. 2/4. Teil : Achnanthaceae Kritische Erganzungen zu Achnanthes s. l., Navicula s. str., Gomphonema. In: Ettl, H., J. Gerloff, H. Heynig & D Mollenhauer (Eds.). Süßbwasserflora von Mitteleuropa. Gustav Fisher Verlag. Stuttgart, Germany. 468 p.         [ Links ]

Lange–Bertalot, H. 2001. Diatoms of Europe. Diatoms of the European inland waters and comparable habitats. Navicula sensu stricto; 10 genera separated from Navicula sensu lato Frustulia. Vol. 2. Gantner Verlag. K. G. 526 p.         [ Links ]

Lobo, E. A., K. Katoh & Y. Aruga. 1995. Response of epilithic diatom assemblages to water pollution in rivers in the Tokyo Metropolitan area, Japan. Freshwater Biology 34: 191–204.         [ Links ]

Leland, H. V. & S. D. Porter. 2000. Distribution of benthic algae in the upper Illinois River basin in relation to geology and land use. Freshwater Biology 44: 279–301.         [ Links ]

Maidana, N., I. Izaguirre, A. Vinocur, G. Mateloni & H. A. Pizarro. 2005. Diatomeas en una transecta patagónico–antártica. Ecología Austral 15: 159–176.         [ Links ]

Martínez de Fabricius, A. L., N. Maidana, N. Gómez & S. Sabater. 2003. Distribution patterns of benthic diatoms in a Pampean river exponed to seasonal floods: the Cuarto River (Argentina). Biodiversity and Conservation 12: 2443–2454.         [ Links ]

Medina–Nava, M. 2003. Utilización del Índice de Integridad Biótica (IIB) para determinar áreas de conservación de peces en la cuenca Lerma–Chapala en Michoacán. Tesis de Maestría. Universidad Michoacana de San Nicolás de Hidalgo. Morelia, México. 86 p.         [ Links ]

Mestre–Rodríguez, J. E. 1997. Case study VIII–Lerma–Chapala Basin, Mexico. In: Helmer R, Hespanhol I (Ed.) Water pollution control – a guide to the use of water quality management principles. WHO–UNEP, pp. 1–15.         [ Links ]

Metzeltin, D & H. Lange–Bertalot. 1998. Tropical diatoms of the South America I. Iconographia Diatomologica 5: 1–695.         [ Links ]

Metzeltin, D. & H. Lange–Bertalot. 2002. Diatoms from the "Island Continent" Madagascar. Gantner Verlag K. G. Germany. 286 p.         [ Links ]

Metzeltin, D. & García–Rodríguez. 2003. Diatomeas uruguayas. Facultad de Ciencias, Universidad de la República. 207 p.         [ Links ]

Metzeltin, D., H. Lange–Bertalot & F. García–Rodríguez. 2005. Diatoms of Uruguay. Iconographia Diatomologica 15: 1–730.         [ Links ]

Moncayo, R, I. Israde–Alcántara & V. H. Garduño. 2001. La cherehuita Hubbsina turneri De Buen (1941) (Pisces: Goodeidae). Origen, distribución y su uso en la regionalIzación de la Cuenca del Río Lerma. Hidrobiológica 11 (1): 1–18.         [ Links ]

Ndiritu, G. G., N. N. Gichuki & L. Triest. 2006. Distribution of epilithic diatoms in response to environmental conditions in an urban tropical stream, Central Kenya. Biodiversity and Conservation 15: 3267–3293.         [ Links ]

Novelo, E. 1998. Floras ficológicas del Valle de Tehuacán, Puebla. Tesis de Doctorado. Facultad de Ciencias, División de Estudios de Posgrado. Universidad Nacional Autónoma de México. México, D.F., 599 p.         [ Links ]

Novelo, E., R. Tavera & C. Ibarra. 2007. Bacillariophyceae from karstic wetlands in Mexico. Bibliotheca Diatomologica. Vol. XX. J. Cramer. Germany. 136 p.         [ Links ]

Oliva–Martínez, G., J. G. Ramírez–Martínez, G. Garduño–Solórzano, J. Cañetas–Ortega & M. Ortega. 2005. Caracterización diatomológica en tres cuerpos de agua de los humedales de Jilotepec–Ixtlahuaca, Estado de México. Hidrobiológica 15 (1): 1–26.         [ Links ]

Oliva, M. G., A. Lugo, J. Alcocer & E. A. Cantoral–Uriza. 2006. Cyclotella alchichicana sp. nov. from a saline Mexican lake. Diatom Research 21 (1): 81–89.         [ Links ]

Oliva, G., A. Lugo, J. Alcocer & E. A. Cantoral–Uriza. 2008. Morphological study of Cyclotella choctawhatcheeana Prasad (Stephanodiscaceae) from a saline Mexican lake. Saline systems 4: 17–25.         [ Links ]

Patrick, R. & Ch. W. Reimer. 1966. The diatoms of The United States, exclusive of Alaska and Hawaii. Monographic Series of Academy of Natural Sciences of Philadelphia 13 (1): 1–688.         [ Links ]

Ramírez, M. & E. Cantoral. 2003. Flora algal de ríos templados en la zona occidental de la cuenca del Valle de México. Anales Instituto de Biología, Universidad Nacional Autónoma de México, Serie Botánica 74 (2): 143–194.         [ Links ]

Ramírez, A. & Y. Plata–Díaz. 2008. Diatomeas perifíticas en diferentes tramos de dos sistemas lóticos de alta montaña (Páramo de Santurbán, N de Santander, Colombia) y su relación con las variables ambientales. Acta Biológica de Colombia 13 (1): 199–216.         [ Links ]

Ramírez, M., Y. Beltrán, M. Bojorge, J. Carmona, E.A. Cantoral–Uriza & F. Valadez Cruz. 2001. Flora algal del Río La Magdalena, Distrito Federal, México. Boletín de la Sociedad Botánica de México 68: 51–73.         [ Links ]

Rumrich, U., H. Lange–Bertalot & M. Rumrich. 2000. Diatoms of the Andes, from Venezuela to Patagonia/Tierra del Fuego; and two additional contributions. A. R. G. Gantner Verlag K. G. 672 p.         [ Links ]

Salomoni, S. E., O. Rocha, V. L. Callegaro & E. A. Lobo. 2006. Epilithic diatoms as indicators of water quality in the Gravataí river, Rio Grande do Sul, Brazil. Hydrobiologia 559: 233–246.         [ Links ]

Segura–García V., I. Israde & N. Maidana. 2010. The genus Navicula sensu stricto in the Upper Lerma basin, Mexico. Diatom research 25 (2): 367–383.         [ Links ]

Sczepocka, E. & B. Szulc. 2006. Benthic diatoms in the central section of the Pilica river and Sulejów reservoir. International Journal of Oceanography and Hydrobiology 35 (2): 171–178.         [ Links ]

Secretaría de Programación y Presupuesto (SSP). 1985. Síntesis Geográfica del Estado de Michoacán. 316 p.         [ Links ]

Stevenson, R. J. 1997. Scale–dependent determinants and consequences of benthic algal heterogeneity. Journal North American Benthological Society 16: 248–262.         [ Links ]

ter Braak, C. J. F. 1990. CANOCO–a Fortran program for canonical community ordination by partial, detrended, canonical correspondence analysis, principal components analysis and redundancy analysis (version 3.11). Agricultural Mathematics Group, Wageningen, The Netherlands.         [ Links ]

Valadez–Cruz, F., J. Carmona–Jiménez & E. Cantoral–Uriza. 1996. Algas de ambientes lóticos en el estado de Morelos, México. Anales Instituto de Biología, Universidad Nacional Autónoma de México, Serie Botánica 67 (2): 227–282.         [ Links ]

van Dam, H., A. Mertens & J. Sinkel. 1994. A code checlist and ecological indicator values of freshwater diatoms from the Netherlands. Netherlands Journal of Aquatic Ecology 28 (1): 117–133.         [ Links ]

Walker, C. & Y. Pan. 2006. Using diatom assemblages to asses urban stream conditions. Hydrobiologia 561: 179–189.         [ Links ]

Weilhoefer, C. & Y. Pan. 2006. Diatom assemblages and their associations with environmental variables in Oregon Coast Range streams, USA. Hydrobiologia 561: 207–219.         [ Links ]

Werum, M. & H. Lange–Bertalot. 2004. Annotated Diatom Micrographs; Ecology–Hydrogeology–Taxonomy. Iconographia Diatomologica 13: 1–479.         [ Links ]

Zampella, R. A., K. J. Laidig & R. L. Lowe. 2007. Distribution of diatoms in relation to land use and pH in blackwater coastal plain streams. Environmental Management 39: 369–384.         [ Links ]