Hostname: page-component-77c89778f8-m8s7h Total loading time: 0 Render date: 2024-07-16T18:14:24.493Z Has data issue: false hasContentIssue false

Halocladius variabilis (Diptera: Chironomidae): a marine insect symbiotic with seaweeds from the White Sea, Russia

Published online by Cambridge University Press:  26 August 2009

Elena R. Tarakhovskaya
Affiliation:
Department of Plant Physiology and Biochemistry, St Petersburg State University, Universitetskaya nab. 7/9, St Petersburg 199034, Russia
David J. Garbary*
Affiliation:
Department of Biology, St Francis Xavier University, Antigonish, Nova Scotia, Canada, B2G 2W5
*
Correspondence should be addressed to: D.J. Garbary, Department of Biology, St Francis Xavier University, Antigonish, Nova Scotia, Canada, B2G 2W5 email: dgarbary@gmail.com

Abstract

The commensal (and possibly mutualistic) symbiosis between the marine chironomid, Halocladius variabilis, and brown algal epiphytes of Fucus vesiculosus and Ascophyllum nodosum is described for the first time from Europe, based on field studies from the White Sea, Russia. While the primary host, Elachista fucicola, and the secondary host, A. nodosum, are the same as in eastern Canada where the symbiosis was first described, White Sea populations have a wider range of primary hosts that include Pylaiella littoralis and Dictyosiphon foeniculaceus. About 64% of E. fucicola thalli on A. nodosum in the low intertidal zone were colonized. Significantly lower frequencies were found on E. fucicola when the latter was epiphytic on F. vesiculosus at the same tidal height or on either secondary host when they were in the subtidal zone. For a given tidal height, or secondary host, frequency of H. variabilis was reduced on P. littoralis and further reduced on D. foeniculaceus. We suggest that subtidal populations are colonized by dispersal of larvae from the intertidal zone on to suitable substrata, and that there is limited potential for these individuals to reach the intertidal zone as adults for reproduction.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Cheng, L. and Collins, J.D. (1980) Observations on behavior, emergence and reproduction of the marine midges Pontomyia (Diptera: Chironomidae). Marine Biology 58, 15.CrossRefGoogle Scholar
Colbo, M.H. (1996) Chironomidae from marine coastal environments near St John's, Newfoundland, Canada. Hydrobiologia 318, 117122.CrossRefGoogle Scholar
Cubit, C. (1982) Disturbance and predation in an assemblage of herbivorous Diptera and algae on rocky shores. Oecologia 54, 2331.Google Scholar
Deckert, R.J. and Garbary, D.J. (2005) Ascophyllum and its symbionts. VI. Microscopic characterization of the Ascophyllum nodosum (Phaeophyceae), Mycophycias ascophylli (Ascomycetes) symbiotum. Algae 20, 225232.CrossRefGoogle Scholar
Garbary, D.J., Burke, J. and Tian, Lining. (1991) The Ascophyllum–Polysiphonia–Mycosphaerella symbiosis. 2. Aspects of the ecology and distribution of Polysiphonia lanosa in Nova Scotia. Botanica Marina 3, 391401.Google Scholar
Garbary, D.J. and London, J.F. (1995) The Ascophyllum, Polysiphonia, Mycosphaerella symbiosis. 5. Fungal infection protects A. nodosum from desiccation. Botanica Marina 38, 529533.CrossRefGoogle Scholar
Garbary, D.J. and MacDonald, K.A. (1995) The Ascophyllum, Polysiphonia, Mycosphaerella symbiosis. 4. Mutualism in the Ascophyllum–Mycosphaerella interaction. Botanica Marina 38, 221225.CrossRefGoogle Scholar
Garbary, D.J. and Deckert, R.J. (2001) Three part harmony—Ascophyllum and its symbionts. In Seckbach, J. (ed.) Symbiosis: mechanisms and model systems. Dortrecht, The Netherlands: Kluwer, pp. 309321.Google Scholar
Garbary, D.J. Fraser, S., Ferguson, C. and Lauff, R.F. (2004) Use of eelgrass, Zostera marina, wrack by three species of ladybird beetles (Coleoptera: Coccinellidae) in Prince Edward Island. Canadian Field-Naturalist 118, 225228.CrossRefGoogle Scholar
Garbary, D.J., Deckert, R.J. and Hubbard, C.B. (2005a) Ascophyllum and its symbionts. VII. Three-way interactions among Ascophyllum nodosum (Phaeophyceae), Mycophycias ascophylli (Ascomycetes) and Vertebrata lanosa (Ceramiales, Rhodophyta). Algae 20, 353361.CrossRefGoogle Scholar
Garbary, D.J., Jamieson, M.M., Fraser, S.J. and Cranston, P.S. (2005b) Ascophyllum (Phaeophyceae) and its symbionts. IX. A novel symbiosis between Halocladius variabilis (Chironomidae, Insecta) and Elachista fucicola (Elachistaceae, Phaeophyceae) from marine rocky shores of Nova Scotia. Symbiosis 40, 6168.Google Scholar
Garbary, D.J., Jamieson, M. and Taylor, B.R. (2009) Population ecology of the marine insect Halocladius variabilis (Diptera: Chironomidae) in the rocky intertidal zone of Nova Scotia, Canada. Marine Ecology Progress Series 376, 193202.CrossRefGoogle Scholar
Giberson, D.J., Bilyj, B. and Burgess, N. (2001) Species diversity and emergence patterns of nematocerous flies (Insecta: Diptera) from three coastal salt marshes in Prince Edward Island, Canada. Estuaries 24, 862874.CrossRefGoogle Scholar
Guiry, M.D. and Guiry, G.M. (2008) AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. http://www.algaebase.org; accessed 7 November 2008.Google Scholar
Gullan, P.J. and Cranston, P.S. (2004) The insects: an outline of entomology, 3rd edition. London: Blackwell.Google Scholar
Hashimoto, H. (1976) Non-biting midges of marine habitats (Diptera: Chironomidae). In Cheng, L. (ed.) Marine insects 1. Amsterdam: North Holland Publishing, pp. 377414.Google Scholar
Hirvenoja, M. (1973) Revision der Gattung Cricotopus van der Wulp und ihrer Vervandten. Annales Zoologici Fennici 10, 1363.Google Scholar
Hirvenoja, M. (1975) Species of the genus Cricotopus van der Wulp (Diptera, Chironomidae) and its closest relatives in Fenoscandia, especially in Finland. Annales Entomologici Fennici 41, 1937.Google Scholar
Hirvenoja, M., Palmén, E. and Hirvenoja, E. (2006) The emergence of Halocladius variabilis (Staeger) (Diptera: Chironomidae) in the surroundings of the Tvärminne Biological Station in the northern Baltic Sea. Entomologica Fennica 17, 8789.CrossRefGoogle Scholar
Johnson, S.C. and Scheibling, R.E. (1987) Structure and dynamics of epifaunal assemblages of intertidal rock weeds (Ascophyllum nodosum and Fucus vesiculosus) in Nova Scotia, Canada. Marine Ecology Progress Series 37, 209227.CrossRefGoogle Scholar
Khaitov, V.M., Fokin, M.V. and Nicolaeva, A.M. (1999) Structure of communities associated with dense assemblages of the tube-dwelling polychaete Polydora quadrilobata Jacobi (Spionidae) in the White Sea. Hydrobiologia 393, 221226.CrossRefGoogle Scholar
Kuz'mina, Ya. (2001) Chironomidae (Diptera) from north-east of the European part of Russia. Vestnik Instituta Biologii of KOMI Scientific Center, Russian Academy of Science 12, 5054.Google Scholar
Levington, J.S. (1995) Marine biology: function, biodiversity, ecology. New York: Oxford University Press.Google Scholar
McAllen, R. (1999) Enteromorpha intestinalis—a refuge for the supralittoral rockpool harpacticoid copepod Tigriopus brevicornis. Journal of the Marine Biological Association of the United Kingdom 79, 11251126.CrossRefGoogle Scholar
Neuman, D. (1976) Adaptations of chironomids to intertidal environments. Annual Review of Entomology 21, 387414.CrossRefGoogle Scholar
Neumann, D. (1986) Diel eclosion rhythm on a sublittoral population of the marine nsect Pontomyia pacifica. Marine Biology 90, 461465.CrossRefGoogle Scholar
Neumann, D., Kaminsky, R. and Heimbach, F. (1997) Timing of eclosion in marine insects on Mediterranean shores—studies on Clunio mediterraneus, C. ponticus and Thalassomyia frauenfeldi (Diptera: Chironomidae). Marine Biology 129, 513521.CrossRefGoogle Scholar
Robles, C.D. and Cubit, J. (1981) Influence of biotic factors in an upper intertidal community: dipteran larvae grazing on algae. Ecology 62, 15361547.CrossRefGoogle Scholar
Santhakumaran, L.N., Sneli, J.-A. and Sundnes, G. (1984) The larvae of Halocladius (Halocladius) variabilis (Diptera: Chironomidae) from the fouling assemblages on wooden test panels submerged in Trondheimsfjorden. Sarsia 69, 155158.CrossRefGoogle Scholar
Tian, Lining and Garbary, D.J. (1992) The Ascophyllum/Polysiphonia/Mycosphaerella symbiosis. III. Experimental studies on the interactions between P. lanosa and A. nodosum. Botanica Marina 35, 341349.Google Scholar
Tokunaga, M. (1932) Morphological and biological studies on a new marine chironomid fly, Pontomyia pacifica, from Japan. Memoirs of the College of Agriculture of Kyoto Imperial University 19, 155.Google Scholar
Vozzhinskaya, V.B. (1986) Benthic macrophytes of the White Sea. Moscow: Nauka.Google Scholar
Willis, L.D. and Hendricks, A.C. (1992) Life history, growth, survivorship, and production of Hydropsyche slossonae in Mill Creek, Virginia. Journal of the North American Benthological Society 11, 290303.CrossRefGoogle Scholar
Xu, H., Deckert, R.J. and Garbary, D.J. (2008) Ascophyllum and its symbionts. X. Ultrastructure of the interaction between A. nodosum (Phaeophyceae) and Mycophycias ascophylli (Ascomycetes). Canadian Journal of Botany 86, 185193.CrossRefGoogle Scholar
Zinova, A.D. (1953) Keys to the brown algae of northern seas of USSR. Moscow, Leningrad: Academy of Science of USSR.Google Scholar