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

Published online by Cambridge University Press:  13 September 2005

R. POULIN
R. POULIN
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56, Dunedin, New Zealand
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Abstract

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.

Keywords

cercariaecomparative analysislatitudephylogenyQ10snailstrematodes
Type
Research Article
Information
Parasitology , Volume 132 , Issue 1 , January 2006 , pp. 143 - 151
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

Ataev, G. L. ( 1991). Temperature influence on the development and biology of rediae and cercariae of Philophthalmus rhionica (Trematoda). Parazitologiya 25, 349–359.Google Scholar
Bossaert, K., Lonneux, J. F., Losson, B. and Peeters, J. ( 1999). Fasciolosis incidence forecasts in Belgium by means of climatic data. Annales de Médecine Vétérinaire 143, 201–211.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 (Suppl.) S3–S13.CrossRefGoogle Scholar
Evans, N. A. ( 1985). The influence of environmental temperature upon transmission of the cercariae of Echinostoma liei (Digenea: Echinostomatidae). Parasitology 90, 269–275.CrossRefGoogle Scholar
Felsenstein, J. ( 1985). Phylogenies and the comparative method. American Naturalist 125, 1–15.CrossRefGoogle Scholar
Fingerut, J. T., Zimmer, C. A. and Zimmer, R. K. ( 2003). Patterns and processes of larval emergence in an estuarine parasite system. Biological Bulletin 205, 110–120.CrossRefGoogle Scholar
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 Ecology 311, 253–265.CrossRefGoogle Scholar
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 Series 290, 109–117.CrossRefGoogle Scholar
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 Helminthology 76, 369–371.CrossRefGoogle Scholar
Fried, B. and Ponder, E. L. ( 2003). Effects of temperature on survival, infectivity and in vitro encystment of the cercariae of Echinostoma caproni. Journal of Helminthology 77, 235–238.CrossRefGoogle Scholar
Galaktionov, K. V. and Dobrovolskij, A. A. ( 2003). The Biology and Evolution of Trematodes. Kluwer Academic Publishers, Dordrecht, The Netherlands.CrossRef
Garland, T. Jr., Harvey, P. H. and Ives, A. R. ( 1992). Procedures for the analysis of comparative data using phylogenetically independent contrasts. Systematic Biology 41, 18–32.CrossRefGoogle Scholar
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 Society 76, 87–92.CrossRefGoogle Scholar
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. Science 296, 2158–2162.CrossRefGoogle Scholar
Harvey, P. H. and Pagel, M. D. ( 1991). The Comparative Method in Evolutionary Biology. Oxford University Press, Oxford.
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 Meersuntersuchungen 46, 329–339.CrossRefGoogle Scholar
Kuntz, R. E. ( 1947). Effect of light and temperature on emergence of Schistosoma mansoni cercariae. Transactions of the American Microscopical Society 66, 37–49.CrossRefGoogle Scholar
Lee, C. G., Cho, S. H. and Lee, C. Y. ( 1995). Metacercarial production of Lymnaea viridis experimentally infected with Fasciola hepatica. Veterinary Parasitology 58, 313–318.CrossRefGoogle Scholar
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 Parasitology 82, 347–350.CrossRefGoogle Scholar
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. Parasitology 126, 203–224.CrossRefGoogle Scholar
Loker, E. S. ( 1983). A comparative study of the life-histories of mammalian schistosomes. Parasitology 87, 343–369.CrossRefGoogle Scholar
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 Scholar
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 Organisms 25, 169–173.CrossRefGoogle Scholar
Mao, C. P., Li, L. and Wu, C. C. ( 1949). Studies on the emergence of cercariae of Schistosoma japonicum from their Chinese snail host, Oncomelania hupensis. American Journal of Tropical Medicine 29, 937–944.CrossRefGoogle Scholar
Marcogliese, D. J. ( 2001). Implications of climate change for parasitism of animals in the aquatic environment. Canadian Journal of Zoology 79, 1331–1352.CrossRefGoogle Scholar
McCarthy, A. M. ( 1999). The influence of temperature on the survival and infectivity of the cercariae of Echinoparyphium recurvatum (Digenea: Echinostomatidae). Parasitology 118, 383–388.CrossRefGoogle Scholar
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 Parasitology 97, 617–627.CrossRefGoogle Scholar
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 Parasitology 33, 977–985.CrossRefGoogle Scholar
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 Helminthology 76, 341–347.CrossRefGoogle Scholar
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 Series 151, 123–134.CrossRefGoogle Scholar
Mouritsen, K. N. and Poulin, R. ( 2002 a). Parasitism, climate oscillations and the structure of natural communities. Oikos 97, 462–468.Google Scholar
Mouritsen, K. N. and Poulin, R. ( 2002 b). Parasitism, community structure and biodiversity in intertidal ecosystems. Parasitology 124, S101–S117.Google Scholar
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 Parasitology 33, 733–755.CrossRefGoogle Scholar
Ottersen, G., Planque, B., Belgrano, A., Post, E., Reid, P. C. and Stenseth, N. C. ( 2001). Ecological effects of the North Atlantic Oscillation. Oecologia 128, 1–14.CrossRefGoogle Scholar
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. Parasitology 111, 373–378.CrossRefGoogle Scholar
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 Parasitenkunde 63, 159–169.Google Scholar
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 Parasitenkunde 70, 95–103.CrossRefGoogle Scholar
Purvis, A. and Rambaut, A. ( 1994) Comparative Analysis by Independent Contrasts (C.A.I.C.), version 2.0. Oxford University, Oxford.
Rees, G. ( 1948). A study of the effect of light, temperature and salinity on the emergence of Cercaria purpurae Lebour from Nucella lapillus (L.). Parasitology 38, 228–242.CrossRefGoogle Scholar
Rojo-Vázquez, F. A. and Simón-Martin, F. ( 1985). Algunos aspectos de la biologia de las cercarias de Trichobilharzia sp. del Rio Cañedo (Provincia de Salamanca, España). Revista Iberica de Parasitologia 45, 141–148.Google Scholar
Schmidt, K. A. and Fried, B. ( 1996). Emergence of cercariae of Echinostoma trivolvis from Helisoma trivolvis under different conditions. Journal of Parasitology 82, 674–676.CrossRefGoogle Scholar
Schmidt-Nielsen, K. ( 1997). Animal Physiology: Adaptation and Environment, 5th Edn. Cambridge University Press, Cambridge.
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 Parasitology 76, 790–795.CrossRefGoogle Scholar
Sousa, W. P. ( 1991). Can models of soft-sediment community structure be complete without parasites? American Zoologist 31, 821–830.Google Scholar
Stenseth, N. C., Mysterud, A., Ottersen, G., Hurrell, J. W., Chan, K.-S. and Lima, M. ( 2002). Ecological effects of climate fluctuations. Science 297, 1292–1296.CrossRefGoogle Scholar
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, B 270, 2087–2096.CrossRefGoogle Scholar
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 Aquaculture 64, 70–74.2.0.CO;2>CrossRefGoogle Scholar
Umadevi, K. and Madhavi, R. ( 1997). Effects of light and temperature on the emergence of Haplorchis pumilio cercariae from the snail host, Thiara tuberculata. Acta Parasitologica 42, 12–16.Google Scholar
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 Physiology A 100, 413–418.CrossRefGoogle Scholar
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, London 416, 389–395.CrossRefGoogle Scholar
Willmer, P., Stone, G. and Johnston, I. ( 2000). Environmental Physiology of Animals. Blackwell Science, Oxford.
Yilma, J. M. and Malone, J. B. ( 1998). A geographic information system forecast model for strategic control of fasciolosis in Ethiopia. Veterinary Parasitology 78, 103–127.CrossRefGoogle Scholar