Abstract
The human activities generate inputs of pollutants that exacerbate the natural tendency to eutrophication in estuaries. The goal of this study was to investigate the effects of anthropogenic pollution on tintinnid assemblages along the coast of the Río de la Plata Estuary. Our working hypothesis was that the abundance and size structure of tintinnid assemblages are significantly modified by the availability of differently sized food items due the organic pollution and eutrophication. Results showed that a high degree of water quality deterioration was negatively correlated with tintinnid abundance and diversity. Consequently, sites where the concentration of nutrients was still high showed the highest representation of tintinnids with small lorica oral diameter (LOD), especially Tintinnidium balechi, associated with small-sized prey (bacteria, pico-, and nanophytoplankton). Finally, diversity index was maximum at sites where water was less polluted and T. balechi dominance alternates with species with a larger LOD, a phenomenon which is related to the increased size of the available food (microphytoplankton). These results suggest that tintinnid species composition and distribution represent useful predictors of water quality.
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Acha, E. M., H. Mianzan, R. Guerrero, J. Carreto, D. Giberto, N. Montoya & M. Carignan, 2008. An overview of physical and ecological processes in the Rio de la Plata Estuary. Continental Shelf Research 28: 1579–1588.
Alder, V. A., 1999. Tintinnoinea. In Boltovskoy, D. (ed.), South Atlantic Zooplankton. Backhuys Publishers, Leiden: 321–384.
Alder, V. A. & G. Thompson, 2000. Spatial and temporal distribution of tintinnids (Protozoa, Ciliata) in relation to frontal systems and the general hydrologic dynamics of the Southern Ocean (SW Atlantic Sector; 50–64 S, 65–49 W). In Davidson, W., C. Howard-Williams & P. Broady (eds), Antarctic Ecosystems: Models for Wider Ecological Understanding. Caxton Press, Christchurch: 203–214.
American Public Health Association (APHA), 1998. Standard Methods for Examination of Water and Wastewater. American Public Health Association, American Water Works Association and Water Pollution Control Federation, Washington, DC.
Barría de Cao, M. S., 1981. Contribución al estudio de los Tintinnoineos (Ciliata, Protozoa) de la zona de Bahía Blanca. Contribución Científica IADO 61: 1–70.
Barría de Cao, M. S., 1992. Abundance and species composition of Tintinnina (Ciliophora) in Bahía Blanca Estuary, Argentina. Estuarine, Coastal and Shelf Science 34: 295–303.
Barría de Cao, M. S., R. Pettigrosso & C. Popovich, 1997. Planktonic ciliates during a diatom bloom in Bahía Blanca Estuary, Argentina. II Tintinnids. Oebalia 23: 21–31.
Barría de Cao, M. S., R. Pettigrosso, E. Parodi & R. Freije, 2003. Abundance and species composition of planktonic Ciliophora from the wastewater discharge zone in the Bahía Blanca Estuary, Argentina. Iheringia Série Zoologia 93: 229–236.
Barría de Cao, M. S., D. Beigt & M. Piccolo, 2005. Temporal variability of diversity and biomass of tintinnids (Ciliophora) in a southwestern Atlantic temperate estuary. Journal of Plankton Research 27: 1103–1111.
Barría de Cao, M. S., M. Abbate, R. Pettigrosso & M. Hoffmeyer, 2013. The planktonic ciliate community and its relationship with the environmental conditions and water quality in two bays of the Beagle Channel, Argentina. Journal of the Marine Biological Association of the UK 93: 1753–1760.
Bernard, C. & F. Rassoulzadegan, 1993. The role of picoplankton (cyanobacteria and plastidic picoflagellates) in the diet of tintinnids. Journal of Plankton Research 15: 361–373.
Bojanić, N., O. Vidjak, M. Šolić, N. Krstulović, I. Brautović, S. Matijević, G. Kuspilic, S. Sestanovic, Z. Gladan & I. Marasović, 2012. Community structure and seasonal dynamics of tintinnid ciliates in Kaštela Bay (Middle Adriatic Sea). Journal of Plankton Research 34: 510–530.
Boltovskoy, D. & V. A. Alder, 1992. Microzooplankton and tintinnid species-specific assemblage structures: patterns of distribution and year-to-year variations in the Weddell Sea (Antarctica). Journal of Plankton Research 14: 1405–1423.
Calbet, A. & E. Saiz, 2005. The ciliate–copepode link in marine ecosystems. Aquatic Microbial Ecology 38: 157–167.
Capriulo, G. M. & E. J. Carpenter, 1983. Abundance, species composition and feeding impact of tintinnid micro-zooplankton in Central Long Island Sound. Marine Ecology Progress Series 10: 277–288.
Capriulo, G. M. & D. V. Ninivaggi, 1982. A comparison of the feeding activities of field collected tintinnids and copepods fed identical natural particle assemblages. Annales de l’Institut océanographique 58: 325–334.
Cariou, J., J. Dolan & S. Dallot, 1999. A preliminary study of tintinnid diversity in the NW Mediterranean Sea. Journal of Plankton Research 21: 1065–1075.
Carsen, A., 2002. Aportes de contaminantes y sedimentos al río de la Plata interior. Franja costera: calidad de Agua, sedimentos y presencia de contaminantes en biota. Executive report, Programa de las Naciones Unidas para el Medio Ambiente, Argentina y Uruguay: 18 pp.
Clarke, K., 1993. Non parametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18: 117–143.
Clarke, K. & R. Warwick, 1994. Change in Marine Communities. Plymouth Marine Laboratory, Plymouth: 144 pp.
Cloern, J. E., 2001. Our evolving conceptual model of the coastal eutrophication problem. Marine Ecology Progress Series 210: 223–253.
Conforti, V., J. Alberghina & E. G. Urda, 1995. Structural changes and dynamics of the phytoplankton along a highly polluted lowland river of Argentina. Journal of Aquatic Ecosystem Health 4: 59–75.
Dolan, J. R., 2010. Morphology and ecology in tintinnid ciliates of the marine plankton: correlates of lorica dimensions. Acta Protozoologica 49: 235–244.
Dolan, J. R. & D. Coats, 1991. Changes in fine-scale vertical distributions of ciliate microzooplankton related to anoxia in Chesapeake Bay waters. Marine Microbial Food Webs 5: 81–93.
Dolan, J. R. & C. Gallegos, 2001. Estuarine diversity of tintinnids (planktonic ciliates). Journal of Plankton Research 23: 1009–1027.
Dolan, J. R. & C. Marassé, 1995. Planktonic ciliate distribution relative to a deep chlorophyll maximum: Catalan Sea, N. W. Mediterranean, June 1993. Deep-Sea Research 42: 1965–1987.
Dolan, J. R., H. Claustre, F. Carlotti, S. Plounevez & T. Moutin, 2002. Microzooplankton diversity: relationship of tintinnid ciliate with resources, competitors and predators from the Atlantic Coast of Morocco to the Eastern Mediterranean. Deep-Sea Research Part I: Oceanographic Research Papers 49: 1217–1232.
Dolan, J. R., S. Jacquet & J. Torréton, 2006. Comparing taxonomic and morphological biodiversity of tintinnids (planktonic ciliates) of New Caledonia. Limnology and Oceanography 51: 950–958.
Dolan, J. R., R. Pierce, E. Yang & S. Kim, 2012. Southern Ocean biogeography of tintinnid ciliates of the marine plankton. Journal of Eukaryotic Microbiology 59: 511–519.
Elliott, M. & V. Quintino, 2007. The estuarine quality paradox, environmental homeostasis and the difficulty of detecting anthropogenic stress in naturally stressed areas. Marine Pollution Bulletin 54: 640–645.
Fonda-Umani, S. & A. Beran, 2003. Seasonal variations in the dynamics of microbial plankton communities: first estimates from experiments in the Gulf of Trieste, Northern Adriatic Sea. Marine Ecology Progress Series 247: 1–16.
Framiñán, M. B. & O. B. Brown, 1996. Study of the Río de la Plata turbidity front, Part I: spatial and temporal distribution. Continental Shelf Research 16: 1259–1289.
Garcia, M. D. & N. Bonel, 2014. Environmental modulation of the plankton community composition and size-structure along the eutrophic intertidal coast of the Río de la Plata Estuary, Argentina. Journal of Limnology 73: 562–573.
Godhantaraman, N., 1994. Species composition and abundance of tintinnids and copepods in the Pichavaram Mangroves (South India). Ciencias Marinas 20: 371–391.
Godhantaraman, N., 2002. Seasonal variations in species composition, abundance, biomass and estimated production rates of tintinnids at tropical estuarine and mangrove waters, Parangipettai, southeast coast of India. Indian Journal of Marine Sciences 36: 161–171.
Guerrero, M., M. Acha, M. Framiñan & C. Lasta, 1997. Physical oceanography of the Río de la Plata Estuary. Continental Shelf Research 17: 727–742.
Heinbokel, J. F., 1978. Studies on the functional role of tintinnids in the Southern California Bight. I. Grazing and growth rates in laboratory cultures. Marine Biology 47: 177–189.
Hlaili, S. A., B. Grami, N. Niquil, et al., 2008. The planktonic food web of the Bizerte Lagoon (south-western Mediterranean) during summer: I. Spatial distribution under different anthropogenic pressures. Estuarine, Coastal and Shelf Science 78: 61–77.
Huret, M., I. Dadou, F. Dumas, P. Lazure & V. Garçon, 2005. Coupling physical and biogeochemical processes in the Rio de la Plata plume. Continental Shelf Research 25: 629–653.
Jaime, P., A. Menéndez & O. Natale, 2001. Balance y dinámica de nutrientes principales en el Río de la Plata interior. Report in Spanish. Informe 01. Instituto Nacional del Agua 10–4.
Kamiyama, T. & M. Tsujino, 1996. Seasonal variation in the species composition of tintinnid ciliates in Hiroshima Bay, the Seto Inland Sea of Japan. Journal of Plankton Research 18: 2313–2327.
Karayanni, H., U. Christaki, F. Van Wambeke, et al., 2008. Heterotrophic nanoflagellate and ciliate bacterivorous activity and growth in the northeast Atlantic Ocean: a seasonal mesoscale study. Aquatic Microbial Ecology 51: 169–181.
Kchaou, N., J. Elloumi, Z. Drira, A. Hamza, H. Ayadi, A. Bouain & L. Aleya, 2009. Distribution of ciliates in relation to environmental factors along the coastline of the Gulf of Gabes, Tunisia. Estuarine, Coastal and Shelf Science 83: 414–424.
Kogan, M., 2005. Estudio de la composición específica, abundancia y distribución espacial del microzooplancton (Protozoos y micrometazoos) en el estuario del Río de La Plata (Argentina/Uruguay). PhD Thesis. Universidad de Buenos Aires, Argentina: 174 pp.
Kraus, T., B. Bergamaschi, P. Hernes, R. Spencer, R. Stepanauskas, C. Kendall, R. Losee & R. Fujii, 2008. Assessing the contribution of wetlands and subsided islands to dissolved organic matter and disinfection byproduct precursors in the Sacramento–San Joaquin River Delta: a geochemical approach. Organic Geochemistry 39: 1302–1318.
Kršinić, F., 2010. Tintinnids (Tintinnida, Choreotrichia, Ciliata) in the Adriatic Sea, Mediterranean. Part II. Ecology. Institute of Oceanography and Fisheries, Split: 113 pp.
Kruskal, J. & M. Wish, 1978. Multidimensional Scaling. Quantitative Applications in the social Sciences Series, Vol. 11. Sage Publications, Newbury Park.
Kurucz, A., A. Masello, S. Méndez, P. Cranston & P. Wells, 1998. Calidad ambiental del Río de La Plata. In Wells, P. & G. Daborn (eds), El Río de La Plata, una revisión ambiental. Informe de Antecedentes del Proyecto EcoPlata. Dalhousie University, Halifax: 71–86.
Laybourn-Parry, J., 1992. Protozoan Plankton Ecology. Chapman and Hall, London: 231 pp.
Legendre, P., 1993. Spatial autocorrelation: trouble or new paradigm? Ecology 74: 1659–1673.
Legendre, P., M. Dale, M. Fortin, J. Gurevitch, M. Hohn & D. Myers, 2002. The consequences of spatial structure for the design and analysis of ecological field surveys. Ecography 25: 601–615.
Lund, J., C. Kipling & E. Le Cren, 1958. The inverted microscope method of estimating algal numbers and the statistical basis of estimations by counting. Hydrobiologia 11: 143–170.
Margalef, R., 1955. Los organismos indicadores en la limnología. Biología de las aguas continentales. Ministerio de Agricultura, Instituto Forestal de Investigaciones y Experiencias: 300 pp.
McLusky, D. & M. Elliott, 2004. The Estuarine Ecosystem: Ecology, Threats and Management, 3rd edn. Oxford University Press, Oxford: 216 pp.
McManus, G. & M. Ederington-Cantrell, 1992. Phytoplankton pigments and growth rates, and microzooplankton grazing in a large temperate estuary. Marine Ecology Progress Series 87: 77–85.
Menéndez, A. & M. Re, 2012. Antecedentes sobre la calidad del agua. Componente B: Modelación de Calidad del Agua. Planteo de aplicaciones y estudios adicionales. INA-FreplataII Informe 3: 32 pp.
Mianzan, H., C. Lasta, E. Acha, R. Guerrero, G. Macchi & C. Bremec, 2001. The Río de la Plata Estuary, Argentina–Uruguay. In Seeliger, U. & B. Kjerfve (eds), Coastal Marine Ecosystems of Latin America. Springer, Berlin: 185–204.
Mishra, S. & R. Panigrahy, 1999. The tintinnids (Protozoa: Ciliata) of the Bahuda Estuary, east coast of India. Indian Journal of Marine Sciences 28: 219–221.
Modigh, M., S. Castaldo, M. Saggiomo, et al., 2003. Distribution of tintinnid species from 428 N to 438 S through the Indian Ocean. Hydrobiologia 503: 251–262.
Montagnes, D., 2013. Ecophysiology and behaviour of tintinnids. In Dolan, J., D. Montagnes, S. Agatha, D. Coats & D. Stoecker (eds), Biology and Ecology of Tintinnid Ciliates: Models for Marine Plankton. Wiley-Blackwell, Oxford: 86–122.
Nagy, G. J., M. Gómez-Erache, C. H. López & A. C. Perdomo, 2002. Distribution patterns of nutrients and symptoms of eutrophication in the Rio de la Plata River Estuary System. In Nutrients and Eutrophication in Estuaries and Coastal Waters. Springer, Dordrecht: 125–139.
Nakata, K. & S. Koyama, 2003. Interannual changes of the winter to early spring biomass and composition of mesozooplankton in the Kuroshio region in relation to climatic factors. Journal of Oceanography 59: 225–234.
Paerl, H., L. Valdes, B. Peierls, J. Adolf & L. Harding Jr., 2006. Anthropogenic and climatic influences on the eutrophication of large estuarine ecosystems. Limnology and Oceanography 51: 448–462.
Pierce, R. W. & J. T. Turner, 1994. Plankton studies in Buzzards Bay, Massachusetts, USA: IV. Tintinnids, 1987 to 1988. Marine Ecology Progress Series 112: 235–240.
Planque, B. & A. Taylor, 1998. Long-term changes in zooplankton and the climate of the North Atlantic. ICES Journal of Marine Science 55: 644–654.
Porter, K. G. & Y. S. Feig, 1980. The use of DAPI for identifying and counting aquatic microflora. Limnology and Oceanography 25: 943–948.
Pratt, J. & J. Balczon, 1992. Biomonitoring using protozoans. In Lee, J. & A. Soldo (eds), Protocols in Protozoology. Society of Protozoologists: B-12.1–B-12.3.
Raffaelli, D. & C. Mason, 1981. Pollution monitoring with meiofauna, using the ratio of nematodes to copepods. Marine Pollution Bulletin 12: 158–163.
Rakshit, D., S. Biswas, S. Sarkar, B. Bhattacharya, N. Godhantaraman & K. Satpathy, 2014. Seasonal variations in species composition, abundance, biomass and production rate of tintinnids (Ciliata: Protozoa) along the Hooghly (Ganges) River Estuary, India: a multivariate approach. Environmental Monitoring and Assessment 186: 3063–3078.
Rives, C. V., 1997. Protozoos como indicadores de contaminación. Calidad de las aguas de la franja costera sur del Río de La Plata (San Fernando-Magdalena). Sec. Obras Públicas, Buenos Aires: 113–119.
Santoferrara, L. F. & V. A. Alder, 2009. Morphological variability, spatial distribution and abundance of Helicostomella species (Ciliophora: Tintinnina) in relation to environmental factors (Argentine shelf; 40-558S). Scientia Marina 73: 701–716.
Sarkar, S., A. Choudhuri & D. Choudhuri, 1985. Seasonal variations of zooplankton in a tidal creek (Mooriganga) of the Hooghly Estuary. University Science Journal, Burdwan 2: 113–121.
Sellner, K., 1987. Phytoplankton in Chesapeake Bay: role in carbon, oxygen and nutrient dynamics. In Majumdar, S., L. Hall & H. Austin (eds), Contaminant Problems and Management of Living Chesapeake Bay Resources. Pennsylvania Academy of Science, Philadelphia: 134–157.
Shekhar, T., B. Kiran, E. Puttaiah, Y. Shivaraj & K. Mahadevan, 2008. Phytoplankton as index of water quality with reference to industrial pollution. Journal of Environmental Biology 29: 233–236.
Simionato, C., D. Moreira, I. Piedra-Cueva, M. Fossati, M. Re, M. Sabarots Gerbec, A. Menendez & F. Cayocca, 2011. Proyecto FREPLATA-FFEM Modelado numérico y mediciones in situ y remotas de las transferencias de sedimentos finos a través del Río de la Plata. Parte B: Simulaciones numéricas. Revista Frente Marítimo 22: 265–304.
Sitran, R., A. Bergamasco, F. Decembrini & L. Guglielmo, 2007. Temporal succession of tintinnids in the Northern Ionian Sea, Central Mediterranean. Journal of Plankton Research 29: 495–508.
Souto, S., 1973. Contribución al conocimiento de los tintínidos de agua dulce de la República Argentina. I. Río de la Plata y delta del Paraná. Physis 32: 249–254.
Souto, S., 1974. Tintinnidos del Río de la Plata y su zona de influencia (Protozoa, Ciliata). Physis 33: 201–205.
Souto, S., 1981. Tintinnina. In Boltovskoy, D. (ed.), Atlas del zooplancton del Atlántico Sudoccidental y métodos de trabajo con el zooplancton marino. Instituto Nacional de Desarrollo Pesquero, Mar del Plata: 353–381.
Telesh, I. & V. Khlebovich, 2010. Principal processes within the estuarine salinity gradient: a review. Marine Pollution Bulletin 61: 149–155.
Urrutxurtu, I., E. Orive & A. Sota, 2003. Seasonal dynamics of ciliated protozoa and their potential food in a eutrophic estuary (Bay of Biscay). Estuarine, Coastal and Shelf Science 57: 1169–1182.
Verity, P. G., 1987. Abundance, community composition, size distribution, and production rates of tintinnids in Narragansett Bay, Rhode Island. Estuarine, Coastal and Shelf Science 24: 671–690.
Verity, P. G. & C. Langdon, 1984. Relationships between lorica volume, carbon, nitrogen, and ATP content of tintinnids in Narragansett Bay. Journal of Plankton Research 6: 859–868.
Wang, X. L., Y. L. Lu, J. Y. Han, G. Z. He & T. Y. Wang, 2007. Identification of anthropogenic influences on water quality of rivers in Taihu Watershed. Journal of Environmental Sciences 19: 475–481.
Wiadnyana, N. & F. Rassoulzadegan, 1989. Selective feeding of Acartia clausi and Centropages typicus on microzooplankton. Marine Ecology Progress Series 53: 37–45.
Wiegner, T., S. Seitzinger, D. Breitburg & J. Sanders, 2003. The effects of multiple stressors on the balance between autotrophic and heterotrophic processes in an estuarine system. Estuaries 26: 352–364.
Xu, M., H. Cao, P. Xie, D. Deng, W. Feng & J. Xu, 2005. The temporal and spatial distribution, composition and abundance of Protozoa in Chaohu Lake, China: relationship with eutrophication. European Journal of Protistology 41: 183–192.
Acknowledgements
We want to express our gratitude to Dr. Sofía Dutto for her help in the statistical analyses and to Dr. Mónica Hoffmeyer for her detailed comments and corrections. We are also thankful to Certified Translator Viviana Soler for her technical assistance in controlling the use of the English language in this paper. Finally, we would like to express our thanks to the anonymous reviewers for improvements in this manuscript. Financial support for this study was provided by the Agencia Nacional de Promoción Científica y Tecnológica (FONCYT-PICT 32077) to Dr. Nora Gómez, Head of the Laboratory of Plankton and Biofilms from the Instituto de Limnología “Dr. Raúl A. Ringuelet,” CONICET-UNLP.
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Garcia, M.D., Barría de Cao, M.S. Anthropogenic pollution along the coast of a temperate estuary: effects on tintinnid assemblages. Hydrobiologia 809, 201–219 (2018). https://doi.org/10.1007/s10750-017-3465-z
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DOI: https://doi.org/10.1007/s10750-017-3465-z