Morphological variability, spatial distribution and abundance of <em>Helicostomella</em> species (Ciliophora: Tintinnina) in relation to environmental factors (Argentine shelf; 40-55°S)

Luciana F. Santoferrara; Viviana A. Alder

doi:10.3989/scimar.2009.73n4701

Authors

Luciana F. Santoferrara Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires
Viviana A. Alder Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires

DOI:

https://doi.org/10.3989/scimar.2009.73n4701

Keywords:

tintinnids, genus Helicostomella, lorica polymorphism, abundance, shelf dynamics, fronts, environmental factors

Abstract

For the first time a taxonomic and ecological study of species belonging to Helicostomella was performed over a mesoscale spatial distribution by examining ca. 3000 loricae collected in Argentine shelf waters during the austral autumn. Microscopic and statistical analysis revealed that the general shape and the oral diameter remained practically constant in the whole area surveyed, despite a continuous length fluctuation of ca. 300 µm, which includes the entire range present in eight previously reported species. Consequently, we consider that the genus may be represented only by H. subulata, whose strong fluctuations in length (mostly attributed to an increase in the collar length), density and biomass seem to respond to temperature, food availability and front-related processes. In Buenos Aires coastal waters associated with a quasi permanent estuarine front (40-40.5°S), mixed conditions would favour moderate abundances of long loricae, whereas in northern (42.5-45.5°S) and southern (46-54.5°S) Patagonian waters, high (103 ind. L^-1) and low (< 5 ind. L^-1) densities of short loricae seem to be a consequence of stratification and encystment, respectively. The non-occurrence of the species at 41-42°S, together with a three-fold reduction in length-related parameters between specimens from Buenos Aires and Patagonian waters, suggests a disjunct distribution.

Downloads

Download data is not yet available.

Author Biographies

Luciana F. Santoferrara, Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires

Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires.

Viviana A. Alder, Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires

Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires. Instituto Antártico Argentino, Buenos Aires

References

Acha, E., H. Mianzan, R. Guerrero, M. Favero and J. Bava. – 2004. Marine fronts at the continental shelves of austral South America. Physical and ecological processes. J. Mar. Sist., 44: 83-105. doi:10.1016/j.jmarsys.2003.09.005

Agatha, S. and M. Struder-Kypke. – 2007. Phylogeny of the order Choreotrichida (Ciliophora, Spirotricha, Oligotrichea) as inferred from morphology, ultrastructure, ontogenesis, and SSr- RNA gene sequences. Eur. J. Protistol., 43(1): 37-63. doi:10.1016/j.ejop.2006.10.001 PMid:17166704

Alder, V. – 1999. Tintinnoinea. In: D. Boltovskoy (ed.), South Atlantic zooplankton, pp. 321-384. Backhuys Publishers, Leiden.

Alder, V. and C. Franzosi. – 2003. Bacterioplankton abundance in relation to environmental factors in the Argentine Sea during April 2002. Proc. IBMANT/ ANDEEP Int. Symp., Argentina.

Almandoz, G., M. Ferrario, G. Ferreyra, I. Schloss, J. Esteves and F. Paparazzo. – 2007. The genus Pseudo-nitzschia (Bacillariophyceae) in continental shelf waters of Argentina (Southwestern Atlantic Ocean, 38-55oS). Harmful Algae, 6: 93-103. doi:10.1016/j.hal.2006.07.003

Balech, E. – 1942. Tintinnoideos del estrecho Le Maire. Physis, XIX: 245-252.

Balech, E. – 1951. Nuevos datos sobre Tintinnoinea de Argentina y Uruguay. Physis, 20(58): 291-302.

Balech, E. – 1959. Tintinnoinea del Mediterraneo. Trab. Inst. Esp. Oceanogr., 28: 1-84.

Balkis, N. – 2004. Tintinnids (Protozoa: Ciliophora) of the Buyukcekmece Bay in the Sea of Marmara. Sci. Mar., 68(1): 33-44. doi:10.3989/scimar.2004.68n133

Barria de Cao, S. – 1986. Contribucion al conocimiento de Tintinnina (Protozoa, Ciliophora) de la zona de Bahia Blanca, II (Argentina). Bol. Inst. Esp. Oceanogr., 3(1): 143-150.

Bernard, C. and F. Rassoulzadegan. – 1993. The role of picoplankton (cyanobacteria and plastidic picoflagellates) in the diet of tintinnids. J. Plankton Res., 15(4): 361-374. doi:10.1093/plankt/15.4.361

Bianchi, A., L. Bianucci, A. Piola, D. Ruiz Pino, I. Schloss, A. Poisson and C. Balestrini. – 2005. Vertical stratification and airsea CO2 fluxes in the Patagonian shelf. J. Geophis. Res., 110: C07003. doi:10.1029/2004JC002488

Bojanic´, N. – 2001. Seasonal distribution of the ciliated protozoa in Kastela Bay. J. Mar. Biol. Ass. U.K., 81: 383-390. doi:10.1017/S002531540100399X

Bojanic´, N., M. Šolic´, N. Krstulovic´, S. Sestanovic´, Z. Nincˇevic´ Gladan, I. Marasovic´ and I. Brautovic´. – 2006. The role of ciliates within the microbial food web in the eutrophicated part of Kastela Bay (middle Adriatic Sea). Sci. Mar., 70(3): 431-442. doi:10.3989/scimar.2006.70n3431

Boschi, E. – 1998. El Mar Argentino y sus recursos pesqueros, Vol. 2. INIDEP, Mar del Plata.

Capriulo, G. and E. Carpenter. – 1983. Abundance, species composition and feeding impact of tintinnid microzooplankton in central Long Island sound. Mar. Ecol. Prog. Ser., 10: 277-288. doi:10.3354/meps010277

Cordeiro, T. and R. Sassi. – 1997. Tintinnina (Ciliophora, Protista) of the North Sea during the spring of 1986. Helgol. Meeresunters, 5: 155-172. doi:10.1007/BF02908705

Dolan, J. and C. Gallegos. – 2001. Estuarine diversity of tintinnids (planktonic ciliates). J. Plankton Res., 23(9): 1009-1027. doi:10.1093/plankt/23.9.1009

Dolan, J., H. Claustre, F.Carlotti, S. Plounevez and T. Moutin. – 2002. Microzooplankton diversity: relationship of tintinnid ciliates with resources, competitors and predators from the Atlantic Coast of Morocco to the Eastern Mediterranean. Deep-Sea Res. Part I, 49: 1217-1232. doi:10.1016/S0967-0637(02)00021-3

Fernandes, L. – 1998. Taxonomia, distribuicao e biomassa dos tintininos (Ciliophora, Tintinnina) e microplâncton associado no Atlântico Sul Ocidental. Ph.D. thesis, Univ. Parana. Field, J., K. Clarke and R. Warwick. – 1982. A practical strategy for analysing multispecies distribution patterns. Mar. Ecol. Prog. Ser., 8: 37-52.

Godhantaraman, N. – 2002. Seasonal variations in species composition, abundance, biomass and estimated production rates of tintinnids at tropical estuarine and mangrove waters, Parangipettai region, southeast coast of India. J. Mar. Syst., 36: 161-171. doi:10.1016/S0924-7963(02)00185-9

Godhantaraman, N. and S. Uye. – 2003. Geographical and seasonal variations in taxonomic composition, abundance and biomass of microzooplancton across a brackish-water lagoonal system of Japan. J. Plankton Res., 25(5): 465-482. doi:10.1093/plankt/25.5.465

Gold, K. and E. Morales. – 1975. Seasonal changes in lorica sizes and the species of Tintinnina in the New York Bight. J. Protozool., 22(4): 520-528.

Hada, Y. – 1970. The protozoan plankton of the Antarctic and Subantarctic seas. Jare Scientific Reports Series 31, National Science Museum, Tokyo.

Hargraves, P. – 1981. Seasonal variation of tintinnids (Ciliophora: Oligotrichida) in Narragansett Bay, Rhode Island, USA. J. Plankton Res., 3(1): 81-91. doi:10.1093/plankt/3.1.81

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. J. Plankton Res., 26: 67-80. doi:10.1093/plankt/fbg115

Kamiyama, T. – 1994. Effects of extracellular products from phytoplankton on the excystment of tintinnids from marine sediments. Mar. Ecol. Prog. Ser., 105: 199-201. doi:10.3354/meps105199

Kamiyama, T. – 1995. Change in the microzooplankton community during decay of a Heterosigma akashiwo bloom. J. Oceanogr., 51: 279-287. doi:10.1007/BF02285166

Kamiyama, T. – 1997. Effect of phytoplankton abundance on excystment of tintinnid ciliates from marine sediments. J. Oceanogr., 53: 299-302.

Kamiyama, T. and Y. Aizawa. – 1992. Effects of temperature and light on tintinnid excystment from marine sediments. Nippon Suisan Gakk, 58: 877-844.

Kamiyama, T. and M.Tsujino. – 1996. Seasonal variation in the species composition of tintinnid cilates in Hiroshima Bay, the Seto Inland Sea of Japan. J. Plankton Res., 18(12): 2313-2327. doi:10.1093/plankt/18.12.2313

Kim, Y-O. and A. Taniguchi. – 1995. Excystment of the oligotrich ciliate Strombidium conicum. Aquat. Microb. Ecol., 9: 149-156. doi:10.3354/ame009149

Kim, S., M. Gil Park, C. Moon, K. Shin and M. Chang. – 2007. Seasonal variations in phytoplankton growth and microzooplankton grazing in a temperate coastal embayment, Korea. Est. Coast. Shelf Sci., 71: 159-169. doi:10.1016/j.ecss.2006.07.011

Kofoid, C. and A. Campbell. – 1929. A conspectus of the marine and freshwater Ciliata belonging to the suborder Tintinnoinea, with description of new species principally from the Agassiz Expedition to the Eastern Tropical Pacific 1904-1905. Univ. Calif. Publ. Zool., 34: 1-403.

Kofoid, C. and A. Campbell. – 1939. Reports on the scientific results of the expedition to the Eastern Tropical Pacific. The Ciliata: the Tintinnoinea. Bull. Mus. comp. Zool. Harvard Univ., 34: 1-473.

Kogan, M. – 2005. Estudio de la composicón especifica, abundancia y distribución espacial del microzooplancton en el estuario del Río de La Plata. Ph.D. thesis, Univ. Buenos Aires.

Kršinic´, F. – 1987a. On the ecology of tintinnines in the bay of Mali Ston (Eastern Adriatic). Est. Coast. Shelf Sci., 24(4): 401-418.

Kršinic´, F. – 1987b. Tintinnines (Ciliophora, Oligotrichida, Tintinnina) in eastern Adriatic bays. Est. Coast. Shelf Sci., 24(4): 527-538. doi:10.1016/0272-7714(87)90132-6

Largier, J. – 1993. Estuarine fronts: how important are they? Estuaries, 16(1): 1-11. doi:10.2307/1352760

Laval-Peuto, M. – 1981. Construction of the lorica in Ciliata Tintinnina. In vivo study of Favella ehrenbergii: variability of the phenotypes during the cycle, biology, statistics, biometry. Protistologica, 17(2): 249-272.

Laval-Peuto, M. and D. Bronwlee. – 1986. Identification and systematics of the Tintinnina (Ciliophora): evaluation and surges tion for improvement. Ann. Inst. Oceanogr., 62(1): 69-84.

Lipej, L. – 1992. The tintinnid fauna (Tintinnina, Choreotrichida, Ciliophora) in Slovenian coastal waters. Razprave IV, Razreda Sasu, XXXIII(4): 93-113.

Marshall, S. – 1969. Protozoa Order Tintinnida. In: J. Fraser and V. Hansen (eds.), Fishes d’ identification du zooplancton. Cons. Per. Int. Explor. Mer., Charlottenlund, 120: 1-6.

Modigh, M. and S. Castaldo. – 2002. Variability and persistence in tintinnid assemblages at a Mediterranean coastal site. Aquat. Microb. Ecol., 28: 299-311. doi:10.3354/ame028299

Moscatello, S., F. Rubino, O. Saracino, G. Fanelli, G. Belmonte and F. Boero. – 2004. Plankton biodiversity around the Salento Peninsula (Southeast Italy): an integrated water/ sediment approach. Sci. Mar., 68(1): 85-102.

Muller, H. – 2000. Evidence of dormancy in planktonic oligotrich ciliates. Verh. Internat. Verein. Limnol., 27: 3206-3209.

Nakamachi, M. and N. Iwasaki. – 1998. List of tintinnids (Protozoa: Ciliata) in Uranouchi Inlet, Kochi, Japan. Bull. Mar. Sci. Fish., Kochi Univ., 18: 65-76.

Nakane, T., K. Nakaka, H. Bouman, T. Platt. – 2008. Environmental control of short-term variation in the plankton community of inner Tokyo Bay, Japan. Est. Coast. Shelf Sci., 78: 796-810. doi:10.1016/j.ecss.2008.02.023

Paranjape, M. – 1980. Occurrence and significance of resting cysts in a hyaline tintinnid Helicostomella subulata (Ehre.) Jorgensen. J. Exp. Mar. Biol. Ecol., 48: 23-33. doi:10.1016/0022-0981(80)90004-0

Paranjape, M. – 1987. Seasonal cycle and vertical distribution of tintinnids in the Bedford Basin, Nova Scotia, Canada. Can. J. Zool., 65(1): 41-48. doi:10.1139/z87-007

Pierce, R. – 1996. Morphology and infraciliature of selected species of Tintinnina with a philogenetic analysis of the Tintinnina based on infraciliature. Ph.D. thesis, Univ. Rhode Island.

Pierce, R. and J. Turner. – 1992. Ecology of planktonic ciliates in marine food webs. Rev. Aquat. Sci., 6(2): 139-181.

Pierce, R. and J.Turner. – 1993. Global biogeography of marine tintinnids. Mar. Ecol. Prog. Ser., 94: 11-26. doi:10.3354/meps094011

Piola, A. and A. Rivas. – 1997. Corrientes en la plataforma continental. In: E. Boschi (ed.), El mar argentino y sus recursos pesqueros. Antecedentes históricos de las exploraciones en el mar y las características ambientales. Vol. 1, pp. 119-132. Publicaciones Especiales INIDEP, Mar del Plata.

Ramirez, F. – 1996. Composicion, abundancia y variacion estacional del zooplancton de red del golfo San Matias. Frente Marit., 16(A): 157-167.

Romero, S., A. Piola, M. Charo and C.Garcia. – 2006. Chlorophylla variability off Patagonia based on SeaWiFS data. J. Geophys. Res., 111: C05021, doi:10.1029/2005JC003244

Sabatini, M. and G. Alvarez Colombo. – 2001. Seasonal pattern of zooplankton biomass in the Argentinian shelf off southern Patagonia (45°-55°S). Sci. Mar., 65(1): 21-31. doi:10.3989/scimar.2001.65n121

Sabatini, M. and P. Martos. – 2002. Mesozooplankton features in a frontal area off northern Patagonia (Argentina) during spring 1995 and 1998. Sci. Mar., 66(3): 215-232. doi:10.3989/scimar.2002.66n3215

Sanders, R. – 1987. Tintinnids and other microzooplankton-seasonal distributions and relationships to resources and hydrography in Maine estuary. J. Plankton Res., 9(1): 65-77. doi:10.1093/plankt/9.1.65

Santoferrara, L. – 2007. Estudio sistemático y ecológico de los ciliados (Protista, Ciliophora) planctónicos del Mar Argentino y Pasaje Drake. Ph.D. thesis. Univ. Buenos Aires.

Souto, S. – 1970a. Tintinnidos de la costa brasilera colectados por el Walther Herwig (Protozoa, Ciliata). Physis, XXX(80): 209-224.

Souto, S. – 1970b. Tintinnidos de la costa atlantica entre los 31° y 35° de latitud sur (Uruguay y sur de Brasil) (Protozoa, Ciliata). Physis, XXX(80): 187-208.

Souto, S. – 1979. Tintínnidos del Atlántico Sudoccidental y Antártica Argentina (Protozoa, Ciliata). Estudio taxonómico, distribucional y ecológico. Ph.D. thesis, Univ. Buenos Aires.

Strickland, J. and T. Parsons. – 1972. A practical handbook of seawater analysis. J. Fish. Res. Board. Can., 167: 1-311.

Struder-Kypke, M., E. Kypke, S. Agatha, J. Warwick and D. Montagnes. – 2002. The user-friendly guide to coastal planktonic ciliates. http://www.liv.ac.uk/ciliate/site/pages/h_subu/.

Thompson, G. and V. Alder. – 2005. Patterns in tintinnid species composition and abundance in relation to hydrological conditions of the Southwestern Atlantic during austral spring. Aquat. Microb. Ecol., 40: 85-101. doi:10.3354/ame040085

Thompson, G., V. Alder and D. Boltovskoy. – 2001. Tintinnids (Ciliophora) and other microzooplankton in Southwestern Atlantic Shelf break waters. Mar. Ecol., 22(4): 343-355. doi:10.1046/j.1439-0485.2001.01723.x

Urrutxurtu, I. – 2004. Seasonal succession of tintinnids in the Nervion River estuary, Basque Country, Spain. J. Plankton Res., 26(3): 307-314. doi:10.1093/plankt/fbh034

Utermohl, H. – 1958. Zur vervolkommung der quantitativen phytoplankton- methodik. Mitt. Int. Ver. Theor. Angew. Limnol., 9: 1-38.

Verity, P. and C. Langdon. – 1984. Relationship between lorica volume, carbon, nitrogen, and ATP content of tintinnids in Narragansett Bay. J. Plankton Res., 6: 859-868. doi:10.1093/plankt/6.5.859

Wasik, A. and E. Mikolajczyc. – 1996. The seasonal succession of hyaline Helicostomella subulata and aglutinated Tintinnopsis lobiancoi-dominants of the Baltic Tintinnina (Ciliophora). Oceanologia, 38(3): 405-418.

Yoo, K-I., Y-O. Kim and D-Y. Kim. – 1988. Taxonomic Studies on Tintinnids (Protozoa: Ciliata) in Korean Coastal Waters. 1. Chinhae Bay. Korean J. Syst. Zool., 4(1): 67-90.