Hostname: page-component-848d4c4894-cjp7w Total loading time: 0 Render date: 2024-06-21T19:58:49.989Z Has data issue: false hasContentIssue false
  • English
  • Français

Being successful in the world of narrow opportunities: transmission patterns of the trematode Ichthyocotylurus pileatus

Published online by Cambridge University Press:  07 August 2009

A. FALTÝNKOVÁ ,
A. KARVONEN ,
M. JYRKKÄ  and
E. T. VALTONEN
A. FALTÝNKOVÁ*
Affiliation:
Department of Biological and Environmental Science, University of Jyväskylä, PO Box 35 (YA), FI-40014 Jyväskylä, Finland Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, Branišovská 31, 370 05 České Budějovice, Czech Republic
A. KARVONEN
Affiliation:
Department of Biological and Environmental Science, Centre of Excellence in Evolutionary Research, P.O. Box 35, FI-40014University of Jyväskylä, Finland
M. JYRKKÄ
Affiliation:
Department of Biological and Environmental Science, University of Jyväskylä, PO Box 35 (YA), FI-40014 Jyväskylä, Finland
E. T. VALTONEN
Affiliation:
Department of Biological and Environmental Science, University of Jyväskylä, PO Box 35 (YA), FI-40014 Jyväskylä, Finland
*
*Corresponding author: Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, Branišovská 31, 370 05 České Budějovice, Czech Republic. Tel: +420 387775486. Fax: +420 385300388. E-mail: faltyn@paru.cas.cz
Get access Rights & Permissions [Opens in a new window]

Summary

Parasites with complex life cycles face 2 major challenges for transmission in northern latitudes. They have to cope with the general unpredictability associated with the series of transmission events required for completion of the cycle, and transmission has to be completed within a narrow temporal window because of strong seasonality. Despite this, some parasites show high transmission success, suggesting the operation of effective transmission mechanisms. We explored the transmission of Ichthyocotylurus pileatus (Trematoda) from its snail (Valvata macrostoma) to fish (Perca fluviatilis) hosts by examining some key characteristics in the dynamics of the cercarial emergence from snails. Transmission took place within a few weeks mainly in July, thus verifying the narrow temporal window for transmission. The output of the short-lived cercariae from the snails was low and variable in magnitude, but nevertheless resulted in a rapid and high rate of infection in newly hatched fish. The cercarial emergence showed a strong circadian rhythm with most of the cercariae emerging in early evening and night, which might represent the most likely mechanism underlying the high rate of transmission in this species. We emphasize the importance of holistic approaches combining aspects of multiple host species in studies on transmission of complex life-cycle parasites.

Keywords

host-parasite relationshipscomplex life cyclescommunity ecologytransmission windowcircadian patternhost exploitationDigeneacercarial emergence
Type
Research Article
Information
Parasitology , Volume 136 , Issue 11 , September 2009 , pp. 1375 - 1382
Copyright
Copyright © Cambridge University Press 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

Bagge, A. M., Poulin, R. and Valtonen, E. T. (2004). Fish population size, and not density, as the determining factor of parasite infection: a case study. Parasitology 128, 305–313.CrossRefGoogle Scholar
Balling, T. E. and Pfeiffer, W. (1997). Frequency distributions of fish parasites in the perch Perca fluviatilis L. from Lake Constance. Parasitology Research 83, 370–373.Google Scholar
Bell, A. S., Sommerville, C. and Gibson, D. I. (1999). Cercarial emergence of Ichthyocotylurus erraticus (Rudolphi, 1809), I. variegatus (Creplin, 1825) and Apatemon gracilis (Rudolphi, 1819) (Digenea: Strigeidae): contrasting responses to light:dark cycling. Parasitology Research 85, 387–392.Google Scholar
van den Berg, M. S., Coops, H., Noordhuis, R., van Schie, J. and Simons, J. (1997). Macroinvertebrate communities in relation to submerged vegetation in two Chara-dominated lakes. Hydrobiologia 342/343, 143–150.Google Scholar
Brown, S. P., Renaud, F., Guegan, J. F. and Thomas, F. (2001). Evolution of trophic transmission in parasites: the need to reach a mating place? Journal of Evolutionary Biology 14, 815–820.Google Scholar
Choisy, M., Brown, S. P., Lafferty, K. D. and Thomas, F. (2003). Evolution of trophic transmission in parasites: Why add intermediate hosts? American Naturalist 162, 172–181.Google Scholar
Combes, C. (1980). Atlas Mondial des Cercaires. Mémoires du Muséum National d'Histoire Naturelle, Série A, Zoologie 115, 5–235.Google Scholar
Combes, C., Bartoli, P. and Théron, A. (2002). Trematode transmission strategies. In The Behavioural Ecology of Parasites (ed. Lewis, E. E., Campbell, J. F. and Sukhdeo, M. V. K.), pp. 1–12. CAB International Wallingford, UK.Google Scholar
Combes, C., Fournier, A., Moné, H. and Théron, A. (1994). Behaviours in trematode cercariae that enhance parasite transmission: patterns and processes. Parasitology 109, 3–13.CrossRefGoogle ScholarPubMed
Cribb, T. H., Bray, R. A., Olson, P. D. and Littlewood, D. T. J. (2003). Life cycle evolution in the Digenea: a new perspective from phylogeny. Advances in Parasitology 54, 197–254.Google Scholar
Faltýnková, A., Niewiadomska, K., Santos, M. J. and Valtonen, E. T. (2007). Furcocercous cercariae (Trematoda) from freshwater snails in Central Finland. Acta Parasitologica 52, 310–317.Google Scholar
Faltýnková, A., Valtonen, E. T. and Karvonen, A. (2008). Spatial and temporal structure of the trematode component community in Valvata macrostoma (Gastropoda, Prosobranchia). Parasitology 135, 1691–1699.Google Scholar
Faulkner, M., Halton, D. W. and Montgomery, W. I. (1989). Sexual, seasonal and tissue variation in the encystment of Cotylurus variegatus metacercariae in perch, Perca fluviatilis. International Journal for Parasitology 19, 285–290.Google Scholar
Grigorovich, I. A., Mills, E. L., Richards, C. B., Breneman, D. and Ciborowski, J. J. H. (2005). European valve snail Valvata piscinalis (Muller) in the Laurentian Great Lakes basin. Journal of Great Lakes Research 31, 135–143.Google Scholar
Harrod, C. and Griffiths, D. (2005). Ichthyocotylurus erraticus (Digenea: Strigeidae): factors affecting infection intensity and the effects of infection on pollan (Coregonus autumnalis), a glacial relict fish. Parasitology 131, 511–519.Google Scholar
Heitkamp, U. (1982). Phänologie und Ökologie der Mollusken stagnierender Kleingewässer Süd-Niedersachsens. Faunistische Mitteilungen Süd-Niedersachsens 4/5, 1–39.Google Scholar
Huusko, A., Vuorimies, O. and Sutela, T. (1996). Temperature and light mediated predation by perch on vendace larvae. Journal of Fish Biology 49, 441–447.Google Scholar
Jokela, J., Lively, C. M., Taskinen, J., and Peters, A. D. (1999). Effect of starvation on parasite-induced mortality in a freshwater snail (Potamopyrgus antipodarum). Oecologia 119, 320–325.Google Scholar
Jokela, J., Taskinen, J., Mutikainen, P. and Kopp, K. (2005). Virulence of parasites in hosts under environmental stress: experiments with anoxia and starvation. Oikos 108, 156–164.Google Scholar
Karvonen, A., Cheng, G. H. and Valtonen, E. T. (2005). Within-lake dynamics in the similarity of parasite assemblages of perch (Perca fluviatilis). Parasitology 131, 817–823.Google Scholar
Karvonen, A., Kirsi, S., Hudson, P. J. and Valtonen, E. T. (2004). Patterns of cercarial production from Diplostomum spathaceum: terminal investment or bet hedging? Parasitology 129, 87–92.Google Scholar
Karvonen, A., Paukku, S., Valtonen, E. T. and Hudson, P. J. (2003). Transmission, infectivity and survival of Diplostomum spathaceum cercariae. Parasitology 127, 217–224.CrossRefGoogle ScholarPubMed
Karvonen, A., Terho, P., Seppälä, O., Jokela, J. and Valtonen, E. T. (2006). Ecological divergence of closely related Diplostomum (Trematoda) parasites. Parasitology 133, 229–235.Google Scholar
Karvonen, A. and Valtonen, E. T. (2004). Helminth assemblages of whitefish (Coregonus lavaretus) in interconnected lakes: Similarity as a function of species specific parasites and geographical separation. Journal of Parasitology 90, 471–476.CrossRefGoogle ScholarPubMed
Krieger, K. A. (1985). Snail distributions in Lake Erie: the influence of anoxia in the southern Central Basin nearshore zone. Ohio Journal of Science 85, 230–244.Google Scholar
Lorke, A., Weber, A., Hofmann, H. and Peeters, F. (2008). Opposing diel migration of fish and zooplankton in the littoral zone of a large lake. Hydrobiologia 600, 139–146.Google Scholar
McCarthy, H. O., Fitzpatrick, S. M. and Irwin, S. W. B. (2002). Life history and life cycles: production and behavior of trematode cercariae in relation to host exploitation and next-host characteristics. Journal of Parasitology 88, 910–918.Google Scholar
Mouthon, J. and Daufresne, M. (2006). Effects of the 2003 heatwave and climatic warming on mollusc communities of the Saône: a large lowland river and of its two main tributaries (France). Global Change Biology 12, 441–449.Google Scholar
Niewiadomska, K. (2003). Parasites of Fishes in Poland. Polskie Towarzystwo Parazitologiczne, Warsaw (in Polish).Google Scholar
Niewiadomska, K. and Kozicka, J. (1970). Remarks on the occurrence and biology of Cotylurus erraticus (Rudolphi, 1809) (Strigeidae) from the Mazurian lakes. Acta Parasitologica Polonica 18, 487–496.Google Scholar
Odening, K. and Bockhardt, I. (1971). Der Lebenszyklus des Trematoden Cotylurus variegatus im Spree-Havel-Seengebiet. Biologisches Zentralblatt 90, 49–84.Google Scholar
Odening, K., Mattheis, T. and Bockhardt, I. (1970). Der Lebenszyklus von Cotylurus c. cucullus (Thoss) (Trematoda, Strigeida) im Raum Berlin. Zoologische Jahrbücher. Abteilung für Systematik 97, 125–198.Google Scholar
Parker, G. A., Chubb, J. C., Ball, M. A. and Roberts, G. N. (2003). Evolution of complex life cycles in helminth parasites. Nature, London 425, 480–484.Google Scholar
Price, P. W. (1990). Host populations as resources defining parasite community organization. In Parasite Communities. Patterns and Processes (ed. Esch, G. W., Bush, A. O. and Aho, J. M.), pp. 21–40. Chapman and Hall, New York, USA.Google Scholar
Swennen, C., Heessen, H. J. L. and Höcker, A. W. M. (1979). Occurrence and biology of the trematodes Cotylurus (Ichthyocotylurus) erraticus, C. (I.) variegatus and C. (I.) platycephalus (Digenea: Strigeidae) in the Netherlands. Netherlands Journal of Sea Research 13, 161–191.Google Scholar
Taskinen, J. (1998). Cercarial production of the trematode Rhipidocotyle fennica in clams kept in the field. Journal of Parasitology 84, 345–349.Google Scholar
Taskinen, J., Valtonen, E. T. and Mäkelä, T. (1994). Quantity of sporocysts and seasonality of two Rhipidocotyle species (Digenea, Bucephalidae) in Anodonta piscinalis (Mollusca, Bivalvia). International Journal for Parasitology 24, 877–886.Google Scholar
Tielens, A. G. M. (1997). Biochemistry of trematodes. In Advances in Trematode Biology (ed. Fried, B. and Graczyk, T. K.), pp. 309–343. CRC Press, New York, USA.Google Scholar
Valtonen, E. T., Holmes, J. C., Aronen, J. and Rautalahti, I. (2003). Parasite communities as indicators of recovery from pollution: parasites of roach (Rutilus rutilus) and perch (Perca fluviatilis) in Central Finland. Parasitology 126, S43–S52.Google Scholar
Valtonen, E. T., Holmes, J. C. and Koskivaara, M. (1997). Eutrophication, pollution, and fragmentation: Effects on parasite communities in roach (Rutilus rutilus) and perch (Perca fluviatilis) in four lakes in central Finland. Canadian Journal of Fisheries and Aquatic Sciences 54, 572–585.CrossRefGoogle Scholar
Zamora, L. and Moreno-Amich, R. (2002). Quantifying the activity and movement of perch in a temperate lake by integrating acoustic telemetry and a geographic information system. Hydrobiologia 482, 209–218.CrossRefGoogle Scholar