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Parasites in a man-made landscape: contrasting patterns of trematode flow in a fishpond area in Central Europe

Published online by Cambridge University Press:  28 April 2011

M. SOLDÁNOVÁ ,
A. FALTÝNKOVÁ ,
T. SCHOLZ  and
A. KOSTADINOVA
M. SOLDÁNOVÁ
Affiliation:
Institute of Parasitology, Biology Centre of the Academy of Sciences of the Czech Republic, Branišovská 31, 370 05 České Budějovice, Czech Republic
A. FALTÝNKOVÁ
Affiliation:
Institute of Parasitology, Biology Centre of the Academy of Sciences of the Czech Republic, Branišovská 31, 370 05 České Budějovice, Czech Republic
T. SCHOLZ
Affiliation:
Institute of Parasitology, Biology Centre of the Academy of Sciences of the Czech Republic, Branišovská 31, 370 05 České Budějovice, Czech Republic
A. KOSTADINOVA*
Affiliation:
Institute of Parasitology, Biology Centre of the Academy of Sciences of the Czech Republic, Branišovská 31, 370 05 České Budějovice, Czech Republic Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, 2 Gagarin Street, 1113 Sofia, Bulgaria
*
*Corresponding author: Institute of Parasitology, Biology Centre of the Academy of Sciences of the Czech Republic, Branišovská 31, 370 05 České Budějovice, Czech Republic. Tel: +420 38 5310351. Fax: +420 38 5310388. E-mail: Aneta.Kostadinova@uv.es; kostadinova@paru.cas.cz
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Summary

We have explored a large body of novel data focusing on small-scale temporal and spatial patterns in the composition and structure of larval trematode communities in Lymnaea stagnalis (L.) from a typical Central European agricultural landscape. The 5 eutrophic fishponds studied provide excellent environments for the development of species-rich and abundant trematode communities. Nine prevalent species were consistently present in component communities, but had differential contribution to the parasite flow in the 5 ponds resulting in significant contrasting patterns of community similarity and the prevalence of the 3 major transmission guilds driving this similarity. Component communities split into 2 groups: (i) those from the large pond dominated by anatid and larid generalists with active miracidial transmission; and (ii) those from the smaller ponds dominated by 2 plagiorchioideans infecting snails via egg ingestion. We put forward 3 hypotheses for the remarkable differences in larval trematode flow in the similar and closely located eutrophic ponds: (i) species-specific differences in parasite colonization potential displayed by an ‘active-passive’ dichotomy in miracidial transmission strategies of the species; (ii) top-down effects of pond context on transmission pathways of the trematodes; and (iii) competition as an important mechanism in eutrophic environments with a bottom-up effect on component community structure.

Keywords

Lymnaea stagnalistrematode community structurespatial variationparasite floweutrophic fishpondsCentral Europe
Type
Research Article
Information
Parasitology , Volume 138 , Issue 6 , May 2011 , pp. 789 - 807
Copyright
Copyright © Cambridge University Press 2011

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References

REFERENCES

Allgöwer, R. and Effelsberg, W. (1991). Badedermatitisepidemie im Baggersee – ein Anlaß zur Zustandsanalyse der Gewässer und Vorbereitung einer naturverträglichen Nutzungskonzeption. Öffentliche Gesundheitswesen 53, 115–156.Google Scholar
Beer, S. A. and German, S. M. (1993). Ecological prerequisites of worsening of the cercariosis situation in cities of Russia (Moscow Region as an example). Parazitologiya 27, 441–449. (In Russian.)Google Scholar
Brown, R., Soldánová, M., Barrett, J. and Kostadinova, A. (2011). Small-scale to large-scale and back: larval trematodes in Lymnaea stagnalis and Planorbarius corneus in Central Europe. Parasitology Research 108, 137–150.CrossRefGoogle ScholarPubMed
Bush, A. O., Lafferty, K. D., Lotz, J. M. and Shostak, A. W. (1997). Parasitology meets ecology in its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.CrossRefGoogle Scholar
Chapman, G. and Fernando, C. H. (1994). The diets and related aspects of feeding of Nile tilapia (Oreochromis niloticus L.) and common carp (Cyprinus carpio L.) in lowland rice fields in northeast Thailand. Aquaculture 123, 281–307.CrossRefGoogle Scholar
Clarke, K. R. and Gorley, R. N. (2006). PRIMER v6: User Manual/Tutorial. PRIMER-E Ltd, Plymouth, Devon, UK.Google Scholar
Clarke, K. R., Somerfield, P. J. and Gorley, R. N. (2008). Testing of null hypotheses in exploratory community analyses: similarity profiles and biota-environment linkage. Journal of Experimental Marine Biology and Ecology 366, 56–69.CrossRefGoogle Scholar
Cort, W. W., McMullen, D. B. and Brackett, S. (1937). Ecological Studies on the Cercariae in Stagnicola emarginata angulata (Sowerby) in the Douglas Lake Region, Michigan. Journal of Parasitology 23, 504–532.CrossRefGoogle Scholar
Curtis, L. A. and Hubbard, K. M. (1990). Trematode infections in a gastropod host misrepresented by observing shed cercariae. Journal of Experimental Marine Biology and Ecology 143, 131–137.CrossRefGoogle Scholar
Esch, G. W. (1971). Impact of ecological succession on parasite fauna in centrarchids from oligotrophic and eutrophic ecosystems. American Midland Naturalist 86, 160–168.CrossRefGoogle Scholar
Esch, G. W., Barger, M. A. and Fellis, K. J. (2002). The transmission of digenetic trematodes: Style, elegance, complexity. Integrative and Comparative Biology 42, 304–312.CrossRefGoogle ScholarPubMed
Esch, G. W., Curtis, L. A. and Barger, M. A. (2001). A perspective on the ecology of trematode communities in snails. Parasitology 123, S57–S75.CrossRefGoogle ScholarPubMed
Esch, G. W., Wetzel, E. J., Zelmer, D. A. and Schotthoeffer, A. M. (1997). Long-term changes in parasite population and community structures: A case history. American Midland Naturalist 137, 369–387.CrossRefGoogle Scholar
Faltýnková, A. (2005). Larval trematodes (Digenea) in molluscs from small water bodies near České Budějovice, Czech Republic. Acta Parasitologica 50, 49–55.Google Scholar
Faltýnková, A. and Haas, W. (2006). Larval trematodes in freshwater molluscs from the Elbe to Danube rivers (Southeast Germany): before and today. Parasitology Research 99, 572–582.CrossRefGoogle ScholarPubMed
Faltýnková, A., Našincová, V. and Kablásková, L. (2007). Larval trematodes (Digenea) of the great pond snail, Lymnaea stagnalis (L.), (Gastropoda: Pulmonata) in Central Europe: a survey of species and key to their identification. Parasite 14, 39–51.CrossRefGoogle Scholar
Fernandez, J. and Esch, G. W. (1991). Guild structure of larval trematodes in the snail Helisoma anceps: patterns and processes at the individual host level. Journal of Parasitology 77, 528–539.CrossRefGoogle ScholarPubMed
Fredensborg, B. L., Mouritsen, K. N. and Poulin, R. (2006). Relating bird host distribution and spatial heterogeneity in trematode infections in an intertidal snail-from small to large scale. Marine Biology 149, 275–283.CrossRefGoogle Scholar
Galaktionov, K. V. and Dobrovolskij, A. A. (2003). The Biology and Evolution of Trematodes. An Essay on the Biology, Morphology, Life Cycles, Transmissions, and Evolution of Digenetic Trematodes. Kluwer Academic Publishers, Dordrecht, The Netherlands.Google Scholar
García-Berthou, E. (2001). Size- and depth-dependent variation in habitat and diet of the common carp (Cyprinus carpio). Aquatic Sciences 63, 466–476.CrossRefGoogle Scholar
Gillespie, G. and Hero, J.-M. (1999). Potential impacts of introduced fish and fish translocations on Australian amphibians. In: Declines and Disappearances of Australian Frogs (ed. Campbell, A.), pp. 131–144. Environment Australia, Camberra, Australia.Google Scholar
Glöer, P. (2002). Die Süßwassergastropoden Nord- und Mitteleuropas. Bestimmungschlüssel, Lebensweise, Verbreitung. Die Tierwelt Deutschlands 73, 1–327.Google Scholar
Hanski, I. (1982). Communities of bumblebees: testing the core-satellite hypothesis. Annales Zoologici Fennici 19, 65–73.Google Scholar
Hechinger, R. F. and Lafferty, K. D. (2005). Host diversity begets parasite diversity: Bird final hosts and trematodes in snail intermediate hosts. Proceedings of the Royal Society of London, B 272, 1059–1066.Google ScholarPubMed
Holmes, J. C. and Price, P. W. (1986). Communities of parasites. In Community Ecology: Pattern and Process (ed. Kikkawa, J. and Anderson, D. J.), pp. 186–213. Blackwell Scientific Publications, Oxford, UK.Google Scholar
Hong, Q.-B., Zhou, X.-N., Sun, L.-P., Yang, G.-J., Huang, Y.-X., Yang, K. et al. (2002). Impact of global warming on the transmission of schistosomiasis in China. 1. The hibernation and lethal temperature on Oncomelania hupensis in laboratory. Chinese Journal of Schistosomiasis Control 14, 192–195.Google Scholar
Johnson, P. T. J. and Chase, J. M. (2004). Parasites in the food web: linking amphibian malformations and aquatic eutrophication. Ecology Letters 7, 521–526.CrossRefGoogle Scholar
Johnson, P. T. J., Chase, J. M., Dosch, K. L., Hartson, R. B., Gross, J. A., Larson, D. J., Sutherland, D. R. and Carpenter, S. R. (2007). Aquatic eutrophication promotes pathogenic infection in amphibians. Proceedings of the National Academy of Sciences, USA 104, 15781–15786.CrossRefGoogle ScholarPubMed
Johnson, P. T. J., Lunde, K. B., Thurman, E. M., Ritchie, E. G., Wray, S. N., Sutherland, D. R., Kapfer, J. M., Frest, T. J., Bowerman, J. and Blaustein, A. R. (2002). Parasite (Ribeiroia ondatrae) infection linked to amphibian malformations in the western United States. Ecological Monographs 72, 151–168.CrossRefGoogle Scholar
Johnson, P. T. J. and McKenzie, V. J. (2009). Effects of environmental change on helminth infections in amphibians: Exploring the emergence of Ribeiroia and Echinostoma infections in North America. In The Biology of Echinostomes. From the Molecule to the Community (ed. Fried, B. and Toledo, R.), pp. 249–280. Springer Science + Business Media, New York, USA.CrossRefGoogle Scholar
Johnson, P. T. J., Sutherland, D. R., Kinsella, J. M. and Lunde, K. B. (2004). Review of the trematode genus Ribeiroia (Psilostomidae): Ecology, life history, and pathogenesis with special emphasis on the amphibian malformation problem. Advances in Parasitology 57, 191–253.CrossRefGoogle ScholarPubMed
Kavetska, K. M., Rząd, I. and Sitko, J. (2008). Taxonomic structure of Digenea in wild ducks (Anatinae) from West Pomerania. Wiadomosci Parazytologiczne 54, 131–136.Google ScholarPubMed
Kolářová, L., Horák, P. and Skírnisson, K. (2010). Methodical approaches in the identification of areas with a potential risk of infection by bird schistosomes causing cercarial dermatitis. Journal of Helminthology 84, 327–335.CrossRefGoogle ScholarPubMed
Kořínek, V., Fott, J., Fuksa, J., Lellák, J. and Pražáková, M. (1987). Carp ponds of central Europe. In Managed Aquatic Ecosystems (ed. Michael, R. G.), pp. 29–62. Elsevier Science B. V., Amsterdam, The Netherlands.Google Scholar
Kuris, A. M. (1990). Guild structure of larval trematodes in molluscan hosts: prevalence, dominance and significance of competition. In Parasite Communities: Patterns and Processes (ed. Esch, G. W., Bush, A. O. and Aho, J. M.), pp. 69–100. Chapman & Hall, London, UK.CrossRefGoogle Scholar
Lafferty, K. D. (1997). Environmental Parasitology: What can parasites tell us about human impacts on the environment? Parasitology Today 13, 251–255.CrossRefGoogle ScholarPubMed
Lafferty, K. D. and Holt, R. D. (2003). How should environmental stress affect the population dynamics of disease? Ecology Letters 6, 654–664.CrossRefGoogle Scholar
Lafferty, K. D. and Kuris, A. M. (1999). How environmental stress affects the impacts of parasites. Limnology and Oceanography 44, 925–931.CrossRefGoogle Scholar
Legendre, P., Lapointe, F.-J. and Casgrain, P. (1994). Modelling brain evolution from behavior: a permutational regression approach. Evolution 48, 1487–1499.CrossRefGoogle ScholarPubMed
Lowenberger, C. A. and Rau, M. E. (1994). Plagiorchis elegans: emergence, longevity and infectivity of cercariae, and host behavioural modifications during cercarial emergence. Parasitology 109, 65–72.CrossRefGoogle ScholarPubMed
Loy, C. and Haas, W. (2001). Prevalence of cercariae from Lymnaea stagnalis snails in a pond system in Southern Germany. Parasitology Research 87, 878–882.Google Scholar
Manly, B.F.J. (1997). Randomization, Bootstrap and Monte Carlo Methods in Biology. 2nd Edn. Chapman & Hall, London, UK.Google Scholar
Marcogliese, D. J. (2005). Parasites of the superorganism: Are they indicators of ecosystem health?. International Journal for Parasitology 35, 705–716.CrossRefGoogle ScholarPubMed
Marcogliese, D. J., Goater, T. M. and Esch, G. W. (1990). Crepidostomum cooperi (Allocreadidae) in the burrowing mayfly, Hexagenia limbata (Ephemeroptera) related to trophic status of a lake. American Midland Naturalist 124, 309–317.CrossRefGoogle Scholar
Michel, P. and Oberdorff, T. (1995). Feeding habits of fourteen European freshwater fish species. Cybium 19, 5–46.Google Scholar
Mouritsen, K. N. and Poulin, R. (2002). Parasitism, community structure and biodiversity in intertidal ecosystems. Parasitology 124, S101–S117.CrossRefGoogle ScholarPubMed
Musil, P., Janda, J. and Denie, H. (1995). Changes in abundance and selection of foraging habitat in cormorants Phalacrocorax carbo in South Bohemia (Czech Republic). Ardea 83, 247–253.Google Scholar
Pechar, L. (2000). Impacts of long-term changes in fishery management on the trophic level water quality in Czech fish ponds. Fisheries Management and Ecology 7, 23–31.CrossRefGoogle Scholar
Pokorný, J. and Hauser, V. (2002). The restoration of fish ponds in agricultural landscapes. Ecological Engineering 18, 555–574.CrossRefGoogle Scholar
Poulíčková, A., Neustupa, J., Špačková, J. and Škaloud, P. (2009). Distribution of epipelic diatoms in artificial fishponds along environmental and spatial gradients. Hydrobiologia 624, 81–90.CrossRefGoogle Scholar
Rudolfová, J., Littlewood, D. T. J., Sitko, J. and Horák, P. (2007). Bird schistosomes of wildfowl in the Czech Republic and Poland. Folia Parasitologica 54, 88–93.CrossRefGoogle ScholarPubMed
Sharpilo, V. P. and Iskova, N. I. (1989). [Fauna of Ukraine, Vol. 34, Issue 3. Trematodes. Plagiorhiates.] Naukova Dumka, Kiev (In Russian).Google Scholar
Shigin, A. A. (1980). [Trematodes of genus Diplostomum in the biocenosis of the fish farm ‘Skhodnya’]. Trudy GELAN 30, 140–202 (In Russian).Google Scholar
Sitko, J., Faltýnková, A. and Scholz, T. (2006). Checklist of the trematodes (Digenea) of birds of the Czech and Slovak Republics. Academia, Prague, Czech Republic.Google Scholar
Skelly, D. K., Bolden, S. R., Holland, M. P., Friedenburg, L. K., Friedenfelds, N. A. and Malcom, T. R. (2006). Urbanization and disease in amphibians. In Disease Ecology: Community Structure and Pathogen Dynamics (ed. Collinge, S.K. and Ray, C.), pp. 153–167. Oxford University Press, Cary, NC, USA.CrossRefGoogle Scholar
Smith, N. F. (2001). Spatial heterogeneity in recruitment of larval trematodes to snail intermediate hosts. Oecologica 127, 115–122.CrossRefGoogle ScholarPubMed
Snyder, S. D. and Esch, G. W. (1993). Trematode community structure in the pulmonate snail Physa gyrina. Journal of Parasitology 79, 205–215.CrossRefGoogle ScholarPubMed
Soldánová, M., Selbach, C., Sures, B., Kostadinova, A. and Pérez-del-Olmo, A. (2010). Trematode communities in Radix auricularia and Lymnaea stagnalis in a reservoir system of the Ruhr River. Parasites & Vectors 3, 56.CrossRefGoogle Scholar
Sousa, W. P. (1990). Spatial scale and the processes structuring a guild of larval trematode parasites. In Parasite Communities: Patterns and Processes (ed. Esch, G.W., Bush, A. O. and Aho, J. M.), pp. 41–67. Chapman & Hall, London, UK.CrossRefGoogle Scholar
Suter, W. (1994). Overwintering waterfowl on Swiss lakes: how are abundance and species richness influenced by trophic status and lake morphology? Hydrobiologia 279/280, 1–14.CrossRefGoogle Scholar
Thieltges, D. W., Ferguson, M-N. A. D., Jones, C. S., Noble, L. R. and Poulin, R. (2009). Biogeographical patterns of marine larval trematode parasites in two intermediate snail hosts in Europe. Journal of Biogeography 36, 1493–1501.CrossRefGoogle Scholar
Ugland, K., Gray, J. G. and Ellingsen, K. (2003). The species–accumulation curve and estimation of species richness. Journal of Animal Ecology 72, 888–897.CrossRefGoogle Scholar
Väyrynen, T., Siddal, R., Valtonen, E. T. and Taskinen, J. (2000). Patterns of trematode parasitism in lymnaeid snails from northern and central Finland. Annales Zoologici Fennici 37, 189–199.Google Scholar
Vojtková, L. (1974 a). [Trematoda of amphibia in CSSR. I. Adult trematodes.] Folia Facultatis Scientiarum Naturalium Universitatis Purkynianae Brunensis, Biologia 15, 3–132 (In Czech).Google Scholar
Vojtková, L. (1974 b). [Trematoda of amphibia in CSSR. I. Adult trematodes.] Folia Facultatis Scientiarum Naturalium Universitatis Purkynianae Brunensis, Biologia 16, 7–86 (In Czech).Google Scholar
Williams, J. A. and Esch, G. W. (1991). Infra- and component community dynamics in the pulmonate snail Helisoma anceps with special emphasis on the hemiurid trematode Halipegus occidualis. Journal of Parasitology 77, 246–253.CrossRefGoogle Scholar
Wiśniewski, W. L. (1958). Characterization of the parasitofauna of an eutrophic lake. Acta Parasitologica Polonica 6, 1–64.Google Scholar
Zakikhani, M. and Rau, M. E. (1999). Plagiorchis elegans (Digenea: Plagiorchiidae) infections in Stagnicola elodes (Pulmonata: Lymnaeidae): host susceptibility, growth, reproduction, mortality, and cercarial production. Journal of Parasitology 85, 454–463.CrossRefGoogle ScholarPubMed
Żbikowska, E. (2007). Digenea species in chosen populations of freshwater snails in northern and central part of Poland. Wiadomosci Parazytologiczne 4, 301–308.Google Scholar
Żbikowska, E., Kobak, J., Żbikowski, J. and Kąklewski, J. (2006). Infestation of Lymnaea stagnalis by digenean flukes in the Jeziorak Lake. Parasitology Research 99, 434–439.CrossRefGoogle ScholarPubMed
Żbikowska, E. and Nowak, A. (2009). One hundred years of research on the natural infection of freshwater snails by trematode larvae in Europe. Parasitology Research 105, 301–311.CrossRefGoogle ScholarPubMed