Mixotrophic ciliate dynamics in two zones of a temperate and highly turbid estuary in South America, Argentina
DOI:
https://doi.org/10.25260/EA.16.26.2.0.122Abstract
Mixotrophy is a feeding strategy by which some organisms combine autrotrophic and heterotrophic activities. The seasonal dynamics of the five most common mixotrophic ciliates were studied monthly in surface layers of the inner and middle zone of the Bahía Blanca estuary, a nutrient-rich, shallow and highly turbid environment in Argentina, from January to December 2009. Temperature, salinity, turbidity and chlorophyll a were recorded, as well as the abundance and biomass of Strombidium capitatum, Strombidium acutum, Cyrtostrombidium sp., Lohmanniella oviformis and Tontonia appendiculariformis. The highest mixotrophic ciliate abundance was recorded during the austral winter (June-July) in the inner zone, meanwhile in the middle zone of the estuary the presence of these ciliates was almost null. The highest chlorophyll contribution derived from mixotrophic ciliates to total chlorophyll a ranged from 6% in the inner zone to 23% in the middle zone, both registered in autumn. The low abundance of mixotrophs in the middle zone of the estuary during the winter, as is usually observed in other coastal ecosystems, could be explained through a higher grazing pressure in this zone (top-down control) by mesozooplankton (e.g., copepods) in comparison to the inner zone. The secondary bloom of phytoplankton consistently observed during the last summers dominated by small sized diatoms and nanoplankton phytoflagelates, could have sustained the high abundance of mixotrophic ciliates registered in the middle zone in autumn and summer.References
Agatha, S., and J. C. Riedel-Lorjé. 1997. Taxonomy and ecology of some Oligotrichea from brackish water basins at the west coast of Schleswig-Holstein (Northern Germany). Journal of Eukaryotic Microbiology 44:27A.
Agatha, S. 2011. Global diversity of aloricate Oligotrichea (Protista, Ciliophora, Spirotricha) in marine and brackish sea water. PLoS ONE 6:e22466.
Barría De Cao, M. S., R. E. Pettigrosso, E. R. Parodi, and H. Freije. 2003. Abundance and species composition of the planktonic ciliates from the waste water discharge zone in the Bahía Blanca Estuary, Argentina. Iheringia. Serie Zoologia 93:229-236.
Bernard, C., and F. Rassoulzadegan. 1995. Seasonal variations of mixotrophic ciliates in the northwest Mediterranean Sea. Marine Ecology Progress Series 108:295‑301.
Caron, D. A., and D. A. Hutchins. 2013. The effects of changing climate on microzooplankton grazing and community structure: drivers, predictions and knowledge gaps. Journal of Plankton Research 35:235-252.
Clarke, K. R., and R. M. Warwick (eds.). 1994. Change in Marine Communities: An Approach to Statistical Analysis and Interpretation. Natural Environment Research. Council. Plymouth. United Kingdom. Pp. 144.
Cloern, J. E. 1987. Turbidity as a control on phytoplankton biomass and productivity in estuaries. Continental Shelf Research 7:1367-1381.
Cole, J. J., N. F. Caraco, and B. L. Peierls. 1992. Can phytoplankton maintain a positive carbon balance in a turbid, freshwater, tidal estuary? Limnology and Oceanography 37:1608-1617.
Dolan, J. R., and C. Marrase. 1995. Planktonic ciliate distribution relative to a deep chlorophyll maximum: Catalan sea, NW Mediterranean, June 1993. Deep-Sea Research 42(I):1965-1987.
Dolan, J. R., and M. T. Pérez. 2000. Costs, benefits and characteristics of mixotrophy in marine oligotrichs. Freshwater Biology 45:227-238.
Dutz, J., and J. Peters. 2008. Importance and nutritional value of large ciliates for the Reproduction of Acartia clausi during the post spring-bloom period in the North Sea. Aquat Microb Ecol 50:261-277.
Fessenden, L., and T. J. Cowles. 1994. Copepod predation on phagotrophic ciliates in Oregon coastal waters. Marine Ecology Progress Series 107:103-111.
Figueiredo, G. M., R. D. M. Nash, and D. J. S. Montagnes. 2007. Do protozoa contribute significantly to the diet of larval fish in the Irish Sea? J Mar Biol Assoc UK 87:843-850.
Flynn, K. J., D. K. Stoecker, A. Mitra, J. A. Cuervo, P. M. Glibert, P. J. Hansen, E. Graneli, and J. M. Burkholder. 2012. Misuse of the phytoplankton-zooplankton dichotomy: the need to assign organisms as mixotrophs within plankton functional types. Journal Plankton Research 35:3-11.
Freije, R. H. & J. E. Marcovecchio. 2004. Oceanografía química. Pp. 69-78 in: M. C. Piccolo and M. Hoffmeyer (eds.). El ecosistema del estuario de Bahía Blanca. Instituto Argentino de Oceanografía, Bahía Blanca. Argentina.
Gismervik, I., Y. Olsen, and O. Vadstein. 2002. Micro- and mesozooplankton response to enhanced nutrient input-a mesocosm study. Hydrobiologia 484:75-87.
Grattepanche, J.D., E. Breton, J. M. Brylinski, E. Lecuyer, and U. Christaki. 2011. Succession of primary producers and micrograzers in a coastal ecosystem dominated by Phaeocystis globosa blooms. Journal of Plankton Research 33:37-50.
Guinder, V.A., C. A. Popovich, and G. Perillo. 2012. Phytoplankton and Physicochemical Analysis on the Water System of the Temperate Estuary in South America: Bahía Blanca Estuary, Argentina. International Journal of Environmental Research 6:547-556.
Guinder, V. A., C. A. Popovich, and G. M. E. Perillo. 2009. Particulate suspended matter concentrations in the Bahía Blanca Estuary, Argentina: Implication for the development of phytoplankton blooms. Estuarine Coastal and Shelf Science 85:157-165.
Hammer, A. C. & J. W. Pitchford. 2005. The role of mixotrophy in plankton bloom dynamics, and the consequences for productivity. Journal of Marine Science 62:833-840.
Hasle, G. R. 1978. Using the inverted microscope. Pp: 191-196 in: A. Sournia (ed.). Phytoplankton manual. UNESCO, Paris.
Hoffmeyer, M. S. 2004. Mesozooplancton. Pp. 133-141 in: M. C. Piccolo and M. S. Hoffmeyer. (eds.). El ecosistema del estuario de Bahía Blanca. Instituto Argentino de Oceanografía. Bahía Blanca, Argentina.
Johansson, M., E. Gorokhova, and U. Larsson. 2004. Annual variability in ciliate community structure, potential prey and predators in the open northern Baltic Sea proper. Journal Plankton Research 26:67-80.
Johnson, M.D. 2011a. Acquired phototrophy in ciliates: a review of cellular interactions and structural adaptations. Journal Eukaryotic Microbiology 58:185-195.
Johnson, M. D. 2011b. The acquisition of phototrophy: adaptive strategies of hosting endosymbionts and organelles. Photosynthesis Research 107:117-132.
Kocum, E., G. J. C. Underwood, and D. B. Nedwell. 2002. Simultaneous measurement of phytoplanktonic primary production, nutrient and light availability along a turbid, eutrophic UK east coast estuary (the Colne Estuary). Marine Ecology Progress Series 231:1-12.
López Abbate, M. C., J. C. Molinero, V. A. Guinder, M. S. Dutto, S. M. Barria De Cao, L. A. Ruiz Etcheverry, R. E. Pettigrosso, M. C. Carcedo, and M. S. Hoffmeyer. 2015. Microplankton dynamics under heavy anthropogenic pressure. The case of the Bahía Blanca Estuary, southwestern Atlantic Ocean Mar. Marine Pollution Bulletin 95:305-314.
Lorenzen, C. J., and S. W. Jeffrey. 1980. Determination of chlorophyll in seawater. UNESCO Technical Papers in Marine Science 35:1-20.
Lynn, D. H., D. J. S. Montagnes, T. Dale, G. L. Gilron, and S. L. Strom. 1991. A reassessment of the genus Strombidinopsis (Ciliophora, Choreotrichida) with descriptions of four new planktonic species and remarks on its taxonomy and phylogeny. Journal of the Marine Biological Association UK 71:597-602.
Maeda, M., and P. Carey. 1985. An illustrated guide to the species of the family Strombiidae (Oligotrichida, Ciliophora), free swimming protozoa common in the aquatic environment. Bulletin of the Ocean Research Institute, University of Tokyo 19:1-68.
Maeda, M. 1986. An illustrated guide to the species of the families Halteriidae and Strobilidiidae (Oligotrichida, Ciliophora), free swimming protozoa common in the aquatic environment. Bulletin of the Ocean Research Institute, University of Tokyo 21:1-67.
Mclusky, D. S., and M. Elliott (eds.). 2004. The Estuarine Ecosystem: Ecology, Threats and Management, 3rd ed. University Press, Oxford. Pp. 214.
Mironova, E., I. Telesh, and S. Skarlato. 2011. Diversity and seasonality in structure of ciliate communities in the Neva Estuary (Baltic Sea). Journal Plankton Research 34:208-220.
Mironova, E., I. Telesh & S. Skarlato. 2013. Planktonic Ciliates of the Neva Estuary (Baltic Sea): Community Structure and Spatial Distribution. Acta Protozoology 52:13-23.
Mironova, E., I. Telesh, and S. Skarlato. 2014. Ciliates in plankton of the Baltic Sea. Protistology 8:81-124.
Modigh, M. 2001. Seasonal variations of photosynthetic ciliates at a Mediterranean coastal site. Aquatic Microbiol Ecology 23:163-175.
Montagnes, D. J. S., and D. H. Lynn. 1991. Taxonomy of the major groups of marine planktonic ciliates, with emphasis on the aloricate forms. Marine Microbial Food Webs 5:59-74.
Montagnes, D. J. S., and F. J. R. Taylor. 1994. The salient features of five marine ciliates in the class Spirotrichea (Oligotrichia), with notes on their culturing and behaviour. Journal of Eukaryotic Microbiology 41:569-586.
Ota, T., and A. Taniguchi. 2003. Standing crop of planktonic ciliates in the East China Sea and their potential grazing impact and contribution to nutrient regeneration. Deep-Sea Research 50:423-442.
Pérez, M. T., J. R. Dolan, and E. Fukai. 1997. Planktonic oligotrich ciliates in the NW Mediterranean: growth rates and consumption by copepods. Marine Ecology Progress Series 155:89-101.
Pérez, M. T., J. R. Dolan, F. Vidussi, and E. Fukai. 2000. Diel vertical distribution of planktonic ciliates within the surface layer of the NW Mediterranean (May 1995). Deep-Sea Research 47:479-503.
Perillo, G. M. E., M. C. Piccolo, E. R. Parodi, and R. H. Freije. 2001. The Bahía Blanca Estuary ecosystem: a review. Pp. 205-217 in: U. Seelinger, L. Lacerda, and B. Kjerve (eds.). Coastal Marine Ecosystems of Latin America. Springer Verlag, Heidelberg, Germany.
Perillo, G. M. E., and M. C. Piccolo. 1991. Tidal response in the Bahía Blanca estuary, Argentina. Journal of Coastal Research 7:437-449.
Pettigrosso, R. E., and C. A. Popovich. 2009. Phytoplankton- aloricate ciliate community in the Bahía Blanca Estuary (Argentina): Seasonal patterns and trophic groups. Brazilian Journal of Oceanography 57:215-227.
Pettigrosso, R. E. 2003. Planktonic Ciliates Choreotrichida and Strombidiida from the Inner zone of the Bahía Blanca Estuary, Argentina. Iheringia Serie Zoologia 93:117-126.
Piccolo, M. C., and M. E. Perillo. 1990. Physical characteristics of the Bahía Blanca estuary Argentina. Estuarine, Coastal and Shelf Science 31:303-317.
Pierce, W. R., and J. T. Turner. 1992. Ecology of planktonic ciliates in marine food webs. Florida, Reviews in Aquatic Science 6(2):139-181.
Popovich, C. A., and J. E. Marcovecchio. 2008. Spatial and temporal variability of phytoplankton and environmental factors in a temperate estuary of South America (Atlantic coast, Argentina). Continental Shelf Research 28:236-244.
Popovich, C. A., C. V. Spetter, R. H. Freije, and J. E. Marcovecchio. 2008. Dissolved Nutrients Availability during winter diatom bloom in a turbid and shallow estuary (Bahía Blanca, Argentina). Journal of Coastal Research 24:95-102.
Putt, M., and D. Stoecker. 1989. An experimentally determined carbon:volume ratio for marine 'oligotrichous' ciliates from estuarine coastal waters. Limnology Oceanography 34:1097-1103.
Putt, M. 1990. Abundance, chlorophyll content and photosynthetic rates of ciliates in the Nordic Seas during summer. Deep-Sea Res A 37:1713-1731.
Sanders, R. W. 1995. Seasonal distributions of the photosynthesizing ciliates Laboea strobila and Myrionecta rubra (=Mesodinium rubrum) in an estuary of the Gulf of Maine. Aquatic Microbial Ecology 9:237-242.
Smayda, T. J. 1983. The phytoplankton of estuaries. Pp. 65-102 in: B. H. Ketchum (ed.). Estuaries and Enclosed Seas. Elsevier, Amsterdam.
Sokal, R. R., and F. J. Rohlf (eds.). 1999. Introducción a la Bioestadística. Editorial Reverté SA, Barcelona, España. Pp. 362.
Stelfox-Widdicombe, C. E., S. D. Archera, P. H. Burkilla, and J. Stefelsc. 2004. Microzooplankton grazing in Phaeocystis and diatom-dominated waters in the southern North Sea in spring. Journal of Sea Research 51:37-51.
Stoecker, D. K., D. J. Gifford, and M. Putt. 1994. Preservation of marine planktonic ciliates: losses and cell shrinkage during fixation. Marine Ecology Progress Series 110:293-299.
Stoecker, D. K., D. E. Gustafson, and P. G. Verity. 1996. Micro- and mesoprotozooplankton at 140°W in the equatorial Pacific: heterotrophs and mixotrophs. Aquatic Microbial Ecology 10:273-282.
Stoecker, D, K., M. D. Johnson, C. De Vargas & F. Not. 2009. Acquired Phototrophy in Aquatic Protists. Aquatic Microbial Ecology 57:279-310.
Stoecker, D.K., M. W. Silver, A. E. Michaels, and L. H. Davis. 1988-1989. Enslavement of algal chloroplasts by four Strombidium spp. (Ciliophora, Oligotrichida). Marine Microbial Food Webs 3:79-100.
Stoecker, D. K., A. C. Weigel, D. A. Stockwell, and M. W. Lomas. 2014. Microzooplankton: Abundance, biomass and contribution To chlorophyll in the Eastern Bering Sea in summer. Deep-Sea Research II 109:134-144.
Urrutxurtu, I., E. Orive, and A. Sota. 2003. Seasonal dynamics of ciliated protozoa and their potential food in an eutrophic estuary (Bay of Biscay). Estuarine Coastal and Shelf Science 57:1169-1182.
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Copyright (c) 2016 Rosa E. Pettigrosso, Maximiliano D. García, Román Ruibrig, M. Sofía Dutto, María López Morales, Mónica S. Hoffmeyer
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