The Macroalgae Ecological Quality Index (MEQI) in the Basin of Mexico: a proposal of aquatic bioindicators for peri-urban rivers
DOI:
https://doi.org/10.22201/ib.20078706e.2022.93.3899Palabras clave:
aquatic biomonitoring, ecological quality, macroalgae, mountain rivers, Mexican Biotic IndexResumen
We assessed macroalgal responses to anthropogenic pressures in the Basin of Mexico to examine whether these biological indicators exhibited a discriminatory and explanatory correlation for the ecological quality evaluation reflected in the Macroalgae Ecological Quality Index (MEQI). The proposal included three steps: i) characterization of trophic level and hydromorphological quality (HQ) in 49 sites collected between 2012 and 2016 with different conservation degrees; ii) calculation of the indicator value of 20 taxa and the algorithm proposal; and iii) validation of the algorithm in 26 new sites and its correlation with water quality and HQ. The ecological quality gradient to which the macroalgae responded was related to oxygen saturation, soluble reactive phosphorus, dissolved inorganic nitrogen, and hydromorphological quality. By assigning an indicator value to each group of species, we calculated the MEQI using the formula adapted from Pantle and Buck, indicating five different ecological quality classes. The MEQI index allowed to established good quality reference sites and also established altered sites in chemical composition and structure. Therefore, MEQI are recommended for biomonitoring in the Basin of Mexico and the registration of its multiple stressors.
Citas
Acosta, R. Ríos, B., Rieradevall, M., & Prat, N. (2009). Propuesta de un protocolo de evaluación de la calidad ecológica de ríos Andinos (CERA) y su aplicación a dos cuencas de Ecuador y Perú. Limnetica, 2, 35–64.
Anagnostidis, K., & Komárek, J. (2005). Oscillatoriales. In B. Budel, G. Gartner, L. Krienitz, & M. Schagerl (Eds.), Cyanoprokaryota (pp. 1–759). Freshwater flora of Central Europe 9/2. Berlin: Elsevier.
Ávila-Akerberg, V. D. (2010). Forest quality in the southwest of México City. Assessment towards ecological restoration of ecosystem services (Ph.D. Thesis). Faculty of Forest and Environmental Sciences, University of Freiburg. Germany.
Bojorge-García, M., Carmona-Jiménez, J., Beltrán, Y., & Cartajena, M. (2010). Temporal and spatial distribution of macroalgal communities of mountain streams in Valle de Bravo Basin, central Mexico. Hydrobiologia, 641, 59–169. https://doi.org/10.1007/s10750-009-0074-5
Bonilla-Lemus, P., Caballero-Villegas, A., Carmona-Jiménez,
J., & Lugo-Vázquez, A. (2014). Occurrence of free-living amoebae in streams of the Mexico Basin. Experimental Parasitology, 145, 28–33. https://doi.org/10.1016/j. exppara.2014.07.001
Borges, F. R., & Necchi, O. Jr. (2006). Patterns of spatial distribution in macroalgal communities from tropical lotic ecosystems. Brazilian Journal of Botany, 29, 669–680.
Branco, C. C. Z., Bispo, P. C., Peres, C. K., Tonetto, A. F., & Branco, L. H. Z. (2014). The roles of environmental conditions and spatial factors in controlling stream macroalgal communities. Hydrobiologia, 732, 123–132. https://doi.org/10.1007/s10750-014-1852-2
Carmona-Jiménez, J., & Caro-Borrero, A. (2017). The last peri-urban rivers of the Mexico Basin: establishment of the reference conditions through the evaluation of ecological quality and biological indicators. Revista Mexicana de Biodiversidad, 88, 425–436. https://doi.org/10.1016/j. rmb.2017.03.019
Carmona-Jiménez, J., & Necchi, O., Jr. (2002). Taxonomy and distribution of Paralemanea (Lemaneaceae, Rhodophyta) in Central Mexico. Cryptogamie Algologie, 23, 39–49.
Carmona-Jiménez, J., & Vilaclara, F. G. (2007). Survey and distribution of Batrachospermaceae (Rhodophyta) in high- altitude tropical streams from central Mexico. Cryptogamie Algologie, 28, 271–282.
Caro-Borrero, A., Carmona-Jiménez, J., Varley, A., De Garay- Arellano, G., Mazari-Hiriart, M., & Adams, D. (2017). The potential of local and scientific ecological knowledge as a source of information in a periurban sub-basin: a case study from Mexico City. Applied Ecology and Environmental Research, 15, 541–562. http://dx.doi.org/10.15666/aeer/1501_541562
Dodds, W. K., Jones, J. R., & Welch, E. B. (1998). Suggested classification of stream trophic state: distributions of temperate stream types by chlorophyll, total nitrogen, and phosphorus. Water Research, 32, 1455–1462. https://doi. org/10.1016/S0043-1354(97)00370-9
Dodds, W. K. (2003). Misuse of inorganic N and soluble reactive P concentrations to indicate nutrient status of surface waters. Journal of the North American Benthological Society, 22, 171–181.
DOF (Diario Oficial de la Federación). (2003). Norma Oficial Mexicana NOM-001-SEMARNAT-1996 (aclaración a la NOM-001-ECOL-1996), que establece los límites máximos permisibles de contaminantes en las descargas de aguas residuales en aguas y bienes nacionales. Retrieved on August 20th, 2019. http://dof.gob.mx/nota_detalle.php?codigo=486 3829&fecha=06/01/1997
Dufrené, M., & Legendre, P. (1997). Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecological Monographs, 67, 345–366. https://doi. org/10.1890/0012-9615(1997)067[0345:SAAIST]2.0.CO;2
Ettl, H., & Gartner, G. (1988). Chlorophyta II. In A. Pascher, H. Ettl, J. Gerloff, H. Heynig, & D. Mollenhauer (Eds.),Tetrasporales, Chlorococclales, Gloeodendrales. Subwasserflora von Mitteleuropa (pp. 1–807). Berlin: Gustav Fischer Verlag.
European Commission (2000). Directive 2000/60/EC of The European Parliament and of the Council- Establishing a framework for community action in the field of water policy. Official Journal of the European Communities. Brussels, Belgium. Retrieved on June 9th, 2019. https://www.eea. europa.eu/policy-documents/directive-2000-60-ec-of
Ferrusquía-Villafranca, F. (1998). Geología de México: una sinopsis. In T. P. Ramamoorthy, R. Bye, A. Lot, & J. Fa (Eds.), Diversidad biológica de México. Orígenes y distribución (pp. 3–108), Ciudad de México: Instituto de Biología, UNAM.
Flor-Arnau, N., Real, M., González, G., Cambra, J., Moreno, J. L., Solá, C. et al. (2015). Índice de macrófitos fluviales (IMF), una nueva herramienta para evaluar el estado ecológico de los ríos mediterráneos. Limnetica, 34, 95–114.
García, E. (2004). Modificaciones al sistema de clasificación climática de Köppen. Ciudad de México: Instituto de Geografía, Universidad Nacional Autónoma de México. Ciudad de México, México.
GDF (Gobierno del Distrito Federal). (2012). Atlas geográfico del suelo de conservación del Distrito Federal. Ciudad de México: GDF. Ciudad de México, México.
Hach Company. (2003). Water analysis handbook, 4th ed. Loveland, Colorado, USA: Hach Co.
Hammer, Ø., Harper, D. A. T., & Ryan, P. D. (2001). PAST. Paleontologia Electronica, 4, 1–9.
INEGI (Instituto Nacional de Estadística y Geografía). (2013). Conjunto de datos vectoriales de uso del suelo y vegetación, escala 1:250 000, Serie V. Mapa. Cd. de México: INEGI.
Karr, J. (1993). Defining and assessing ecological integrity: Beyond water quality. Environmental Toxicology and Chemistry, 12, 1521–1531. https://doi.org/10.1002/ etc.5620120902
Kelly, M. G. (2013). Data rich, information poor? Phytobenthos assessment and the Water Framework Directive. European Journal of Phycology, 48, 437–450. https://doi.org/10.1080/ 09670262.2013.852694
Komárek, A. (2013). Heterocytous Genera, Vol. 19/3rd part. In B. Budel, G. Gartner, L. Krienitz, & M. Schagerl (Eds.), Cyanoprokaryota (pp. 1–1131). Freshwater flora of Central Europe. Berlin: Springer Spektrum.
Legorreta, J. (2009). Ríos, lagos y manantiales del valle de México. Universidad Autónoma Metropolitana. Ciudad de México, México.
Loza, V., Perona, E., Carmona-Jiménez, J., & Mateo, P. (2013). Phenotypic and genotypic characteristics of Phormidium- like cyanobacteria inhabiting microbial mats are correlated with the trophic status of running waters. European Journal of Phycology, 48, 235–252. https://doi.org/10.1080/096702 62.2013.799715
Mazari-Hiriart, M., Pérez-Ortíz, G., Orta-Ledesma, M. T., Armas- Vargas, F., Tapia, M. A., Solano-Ortiz, R. et al. (2014). Final opportunity to rehabilitate an urban river as a water source for Mexico City. Plos One, 9, 1–17. https://doi.org/10.1371/journal.pone.0102081
Mehta, S. K., & Gaur, J. P. (2005). Use of algae for removing
heavy metals ions from wastewater: progress and prospects. Critical Reviews Biotechnology, 25,113–152. https://doi.org/10.1080/07388550500248571
Nardini, A., Sansoni, G., Schipani, I., Conte, G., Goltara, A., Boz, B. et al. (2008). The Water Framework Directive: a soap bubble? An integrative proposal: FLEA (Fluvial Ecosystem Assessment). Venice: Centro Italiano per la Riqualificazione Fluviale.
Necchi, O., Branco, L. H. Z., & Branco, C. C. Z. (1995). Comparison of three techniques for estimating periphyton abundance in bedrock streams. Archiv für Hydrobiologie, 134, 393–402.
Oksanen, J., Blanchet, F. G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D. et al. (2019). vegan: Community Ecology Package. R package version 2.5-6. https://CRAN.R-project. org/package=vegan
Pantle, R., & Buck, H. (1955). Die biologische Überwachung der Gewässer und die Darstellung der Ergebnisse. Gas- und Wasserfach Wasser und Abwasser, 96, 609–620.
Pawlik-Skowrońska, B. (2003). When adapted to high zinc concentrations the periphytic green alga Stigeoclonium tenue produces high amounts of novel phytochelatin-related peptides. Aquatic Toxicology, 62, 155–163. https://doi. org/10.1016/S0166-445X(02)00080-2
Poikane, S., Kelly, M., & Cantonati, M. (2016). Benthic algal assessment of ecological status in European lakes and rivers: Challenges and opportunities. Science of the Total Environment, 568, 603–613.https://doi.org/10.1016/j. scitotenv.2016.02.027
Rice, E. W., Baird, R. B., & Eaton, A. D. (2017). Standard methods for examination of water and wastewater, 23rd. Ed. American Public Health Association (APHA), American Water Works Association, Water Environment Federation. Washington, D.C.: Port City Press.
Rieth, A. (1980). Xathophyceae, 2. Teil. In H. Ettl, J. Gerloff, & H. Heynig (Eds.), Subwasserflora von Mitteleuropa (pp. 1–147). Stuttgart: G. Fischer Verlag.
Rocha, J. C., Peres, C. K., Buzzo, J. L. L., de Souza, V., Krause, E. A., Bispo, P. C. et al. (2017). Modeling the species richness and abundance of lotic macroalgae based on habitat characteristics by artificial neural networks: a potentially useful tool for stream biomonitoring programs. Journal of Applied Phycology, 29, 2145–2153. https://doi.org/10.1007/ s10811-017-1107-5
Rodríguez-Flores, R., & Carmona-Jiménez, J. (2018). Ecology and distribution of macroscopic algae communities in streams from the Basin of Mexico. Botanical Science, 96, 63–75. https://doi.org/10.17129/botsci.1237
RStudio Team. (2019). RStudio: integrated development for R. RStudio, Inc., Boston, MA, USA. http://www.rstudio.com
Sánchez, O. (2007). Ecosistemas acuáticos: diversidad, procesos, problemática y conservación. In O. Sánchez, M. Herzig, E. Peters, V. Márquez-Huitzil, & L. Zambrano (Eds.), Perspectivas sobre conservación de ecosistemas acuáticos en México (pp. 11–36). Ciudad de México. Ciudad de México: Instituto Nacional de Ecología-Secretaría de Medio Ambiente y Recursos Naturales.
Santos-Cerquera, C., & Aguilar, A. G. (2016). Expansión urbana en el suelo de conservación. In Conabio, SEDEMA (Eds.), La biodiversidad en la Ciudad de México, Vol. I. (pp. 127– 138). Ciudad de México: Conabio/ SEDEMA.
Schneider, S. C., & Lindstrøm, E. A. (2009). Bioindication in Norwegian rivers using non-diatomaceous benthic algae: the acidification index periphyton (AIP). Ecological Indicators, 9, 1206–1211. https://doi.org/10.1016/j.ecolind.2009.02.008
Schneider, S. C., & Lindstrøm, E. A. (2011). The periphyton index of trophic status PIT: a new eutrophication metric based on non-diatomaceous benthic algae in Nordic rivers. Hydrobiologia, 665, 143–155. https://doi.org/10.1007/ s10750-011-0614-7
Segnini, S. E. (2002). El uso de los macroinvertebrados bentónicos como indicadores de la condición ecológica de los cuerpos de agua corriente. Ecotropicos, 16, 45–63.
Sheath, R. G., & Cole, K. M. (1992). Biogeography of stream macroalgae in North America. Journal of Phycology, 28, 448–460. https://doi.org/10.1111/j.0022-3646.1992.00448.x
Stancheva, R., & Sheath, R. G. (2016). Benthic soft-bodied algae as bioindicators of stream water quality. Knowledge and Management of Aquatic Ecosystems, 417, 15. https://doi. org/10.1051/kmae/2016002
Stoddard, J. L., Larsen, D. P., Hawkins, C. P., Johnson, R. K., & Norris, R. H. (2006). Setting expectations for the ecological condition of streams: the concept of reference condition. Ecological Applications, 16, 1267–1276. https://doi.org/10.1890/1051-0761(2006)016[1267:SEFTEC]2.0.
CO;2
Strunecký, O., Komárek, J., Johansen, J., Lukešová, A., & Elster,
J. (2013). Molecular and morphological criteria for revision of the genus Microcoleus (Oscillatoriales, Cyanobacteria). Journal of Phycology, 49, 1167–1180. https://doi.org/10. 1111/jpy.12128
Tornés, E., Cambra, J., Gomà, J., Leira, M., Ortiz, R., & Sabater S. (2007). Indicator taxa of benthic diatom communities: a case study in Mediterranean streams. Journal of Limnology, 43, 1–11. https://doi.org/10.1051/limn/2007023
Wallin, M., Wiederholm, T., & Johnson, R. K. (2003). Guidance on establishing reference conditions and ecological status class boundaries for inland surface waters. Final Report to the European Commission from CIS Working Group 2.3– REFCOND. CIS Working Group, 2, 93.
WFD (Water Framework Directive) (2000). Directive 2000/60/ EC of the European Parliament and of the Council of 23 October 2000 establishing a framework for Community action in the field of water policy. Official Journal of the European Communities L, 327, 1–73.
Wher, J. D., & Sheath, R. G. (2003). Freshwater algae of North America: ecology and classification. Amsterdam, Boston: Academic Press.
Wickham, H. (2016). ggplot2: Elegant graphics for data analysis. New York: Springer-Verlag.
Zuccarello, G. C., & Lokhorst, G. M. (2005). Molecular phylogeny of the genus Tribonema (Xanthophyceae) using rbcL gene sequence data: monophyly of morphologically simple algal species. Phycologia, 44, 384–392. https://doi. org/10.2216/0031-8884(2005)44[384:MPOTGT]2.0.CO;2
