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Global warming and temperature-mediated increases in cercarial emergence in trematode parasites

  • R. POULIN (a1)

Global warming can affect the world's biota and the functioning of ecosystems in many indirect ways. Recent evidence indicates that climate change can alter the geographical distribution of parasitic diseases, with potentially drastic consequences for their hosts. It is also possible that warmer conditions could promote the transmission of parasites and raise their local abundance. Here I have compiled experimental data on the effect of temperature on the emergence of infective stages (cercariae) of trematode parasites from their snail intermediate hosts. Temperature-mediated changes in cercarial output varied widely among trematode species, from small reductions to 200-fold increases in response to a 10 °C rise in temperature, with a geometric mean suggesting an almost 8-fold increase. Overall, the observed temperature-mediated increases in cercarial output are much more substantial than those expected from basic physiological processes, for which 2- to 3-fold increases are normally seen. Some of the most extreme increases in cercarial output may be artefacts of the methods used in the original studies; however, exclusion of these extreme values has little impact on the preceding conclusion. Across both species values and phylogenetically independent contrasts, neither the magnitude of the initial cercarial output nor the shell size of the snail host correlated with the relative increase in cercarial production mediated by rising temperature. In contrast, the latitude from which the snail-trematode association originated correlated negatively with temperature-mediated increases in cercarial production: within the 20 ° to 55 ° latitude range, trematodes from lower latitudes showed more pronounced temperature-driven increases in cercarial output than those from higher latitudes. These results suggest that the small increases in air and water temperature forecast by many climate models will not only influence the geographical distribution of some diseases, but may also promote the proliferation of their infective stages in many ecosystems.

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Combes, C., Fournier, A., Moné, H. and Théron, A. ( 1994). Behaviours in trematode cercariae that enhance parasite transmission: patterns and processes. Parasitology109 (Suppl.) S3S13.

Evans, N. A. ( 1985). The influence of environmental temperature upon transmission of the cercariae of Echinostoma liei (Digenea: Echinostomatidae). Parasitology90, 269275.

Felsenstein, J. ( 1985). Phylogenies and the comparative method. American Naturalist125, 115.

Fingerut, J. T., Zimmer, C. A. and Zimmer, R. K. ( 2003). Patterns and processes of larval emergence in an estuarine parasite system. Biological Bulletin205, 110120.

Fredensborg, B. L., Mouritsen, K. N. and Poulin, R. ( 2004). Intensity-dependent mortality of Paracalliope novizealandiae (Amphipoda: Crustacea) infected by a trematode: experimental infections and field observations. Journal of Experimental Marine Biology and Ecology311, 253265.

Fredensborg, B. L., Mouritsen, K. N. and Poulin, R. ( 2005). Impact of trematodes on host survival and population density in the intertidal gastropod Zeacumantus subcarinatus. Marine Ecology Progress Series290, 109117.

Fried, B., LaTerra, R. and Kim, Y. ( 2002). Emergence of cercariae of Echinostoma caproni and Schistosoma mansoni from Biomphalaria glabrata under different laboratory conditions. Journal of Helminthology76, 369371.

Galaktionov, K. V. and Dobrovolskij, A. A. ( 2003). The Biology and Evolution of Trematodes. Kluwer Academic Publishers, Dordrecht, The Netherlands.

Garland, T.Jr., Harvey, P. H. and Ives, A. R. ( 1992). Procedures for the analysis of comparative data using phylogenetically independent contrasts. Systematic Biology41, 1832.

Gumble, A., Otori, Y., Ritchie, L. S. and Hunter, G. W. ( 1957). The effect of light, temperature and pH on the emergence of Schistosoma japonicum cercariae from Oncomelania nosophora. Transactions of the American Microscopical Society76, 8792.

Harvell, C. D., Mitchell, C. E., Ward, J. R., Altizer, S., Dobson, A. P., Ostfeld, R. S. and Samuel, M. D. ( 2002). Climate warming and disease risks for terrestrial and marine biota. Science296, 21582162.

Jensen, K. T. and Mouritsen, K. N. ( 1992). Mass mortality in two common soft-bottom invertebrates, Hydrobia ulvae and Corophium volutator – the possible role of trematodes. Helgolander Meersuntersuchungen46, 329339.

Kuntz, R. E. ( 1947). Effect of light and temperature on emergence of Schistosoma mansoni cercariae. Transactions of the American Microscopical Society66, 3749.

Lee, C. G., Cho, S. H. and Lee, C. Y. ( 1995). Metacercarial production of Lymnaea viridis experimentally infected with Fasciola hepatica. Veterinary Parasitology58, 313318.

Lo, C.-T. and Lee, K.-M. ( 1996). Pattern of emergence and the effects of temperature and light on the emergence and survival of heterophyid cercariae (Centrocestus formosanus and Haplorchis pumilio). Journal of Parasitology82, 347350.

Lockyer, A. E., Olson, P. D., Østergaard, P., Rollinson, D., Johnston, D. A., Attwood, S. W., Southgate, V. R., Horak, P., Snyder, S. D., Le, T. H., Agatsuma, T., McManus, D. P., Carmichael, A. C., Naem, S. and Littlewood, D. T. J. ( 2003). The phylogeny of the Schistosomatidae based on three genes with emphasis on the interrelationships of Schistosoma Weinland, 1858. Parasitology126, 203224.

Loker, E. S. ( 1983). A comparative study of the life-histories of mammalian schistosomes. Parasitology87, 343369.

Lowenberger, C. A. and Rau, M. E. ( 1994). Plagiorchis elegans: emergence, longevity and infectivity of cercariae, and host behavioural modifications during cercarial emergence. Parasitology109, 6572.

Lyholt, H. C. K. and Buchmann, K. ( 1996). Diplostomum spathaceum: effects of temperature and light on cercarial shedding and infection of rainbow trout. Diseases of Aquatic Organisms25, 169173.

Marcogliese, D. J. ( 2001). Implications of climate change for parasitism of animals in the aquatic environment. Canadian Journal of Zoology79, 13311352.

McCarthy, A. M. ( 1999). The influence of temperature on the survival and infectivity of the cercariae of Echinoparyphium recurvatum (Digenea: Echinostomatidae). Parasitology118, 383388.

Moodley, I., Kleinschmidt, I., Sharp, B., Craig, M. and Appleton, C. ( 2003). Temperature-suitability maps for schistosomiasis in South Africa. Annals of Tropical Medicine and Parasitology97, 617627.

Morgan, J. A. T., DeJong, R. J., Kazibwe, F., Mkoji, G. M. and Loker, E. S. ( 2003). A newly-identified lineage of Schistosoma. International Journal for Parasitology33, 977985.

Mouritsen, K. N. ( 2002). The Hydrobia ulvae Maritrema subdolum association: influence of temperature, salinity, light, water-pressure and secondary host exudates on cercarial emergence and longevity. Journal of Helminthology76, 341347.

Mouritsen, K. N. and Jensen, K. T. ( 1997). Parasite transmission between soft-bottom invertebrates: temperature mediated infection rates and mortality in Corophium volutator. Marine Ecology Progress Series151, 123134.

Mouritsen, K. N. and Poulin, R. ( 2002a). Parasitism, climate oscillations and the structure of natural communities. Oikos97, 462468.

Mouritsen, K. N. and Poulin, R. ( 2002b). Parasitism, community structure and biodiversity in intertidal ecosystems. Parasitology124, S101S117.

Olson, P. D., Cribb, T. H., Tkach, V. V., Bray, R. A. and Littlewood, D. T. J. ( 2003). Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology33, 733755.

Ottersen, G., Planque, B., Belgrano, A., Post, E., Reid, P. C. and Stenseth, N. C. ( 2001). Ecological effects of the North Atlantic Oscillation. Oecologia128, 114.

Pechenik, J. A. and Fried, B. ( 1995). Effect of temperature on survival and infectivity of Echinostoma trivolvis cercariae: a test of the energy limitation hypothesis. Parasitology111, 373378.

Pflüger, W. ( 1980). Experimental epidemiology of schistosomiasis. I. The prepatent period and cercarial production of Schistosoma mansoni in Biomphalaria snails at various constant temperatures. Zeitschrift für Parasitenkunde63, 159169.

Pflüger, W., Roushdy, M. Z. and El Emam, M. ( 1984). The prepatent period and cercarial production of Schistosoma haematobium in Bulinus truncatus (Egyptian field strains) at different constant temperatures. Zeitschrift für Parasitenkunde70, 95103.

Rees, G. ( 1948). A study of the effect of light, temperature and salinity on the emergence of Cercaria purpurae Lebour from Nucella lapillus (L.). Parasitology38, 228242.

Schmidt, K. A. and Fried, B. ( 1996). Emergence of cercariae of Echinostoma trivolvis from Helisoma trivolvis under different conditions. Journal of Parasitology82, 674676.

Shostak, A. W. and Esch, G. W. ( 1990). Photocycle-dependent emergence by cercariae of Halipegus occidualis from Helisoma anceps, with special reference to cercarial emergence patterns as adaptations for transmission. Journal of Parasitology76, 790795.

Sousa, W. P. ( 1991). Can models of soft-sediment community structure be complete without parasites? American Zoologist31, 821830.

Stenseth, N. C., Mysterud, A., Ottersen, G., Hurrell, J. W., Chan, K.-S. and Lima, M. ( 2002). Ecological effects of climate fluctuations. Science297, 12921296.

Stenseth, N. C., Ottersen, G., Hurrell, J. W., Mysterud, A., Lima, M., Chan, K.-S., Yoccoz, N. G. and Adlandsvik, B. ( 2003). Studying climate effects on ecology through the use of climate indices: the North Atlantic Oscillation, El Niño Southern Oscillation and beyond. Proceedings of the Royal Society of London, B270, 20872096.

Terhune, J. S., Wise, D. J. and Khoo, L. H. ( 2002). Bolbophorus confusus infections in channel catfish in northwestern Mississippi and effects of water temperature on emergence of cercariae from infected snails. North American Journal of Aquaculture64, 7074.

Van Aardt, W. J. and De Kock, K. N. ( 1991). Oxygen-consumption and hemocyanin function in the freshwater snail Marisa cornuarietis (L.). Comparative Biochemistry and PhysiologyA100, 413418.

Walther, G.-R., Post, E., Convey, P., Menzel, A., Parmesan, C., Beebee, T. J. C., Fromentin, J.-M., Hoegh-Guldberg, O. and Bairlein, F. ( 2002). Ecological responses to recent climate change. Nature, London416, 389395.

Yilma, J. M. and Malone, J. B. ( 1998). A geographic information system forecast model for strategic control of fasciolosis in Ethiopia. Veterinary Parasitology78, 103127.

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