Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-24T23:32:52.508Z Has data issue: false hasContentIssue false
  • English
  • Français

Thermodynamics of cercarial survival and metabolism in a changing climate

Published online by Cambridge University Press:  08 August 2011

N. J. MORLEY
N. J. MORLEY*
Affiliation:
School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey TW20 0EX, UK
*
*Corresponding author: Tel: +44 (0)1784 443186. Fax: +44 (0)1784 414224. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Cercariae are non-feeding free-living stages in the life cycles of trematodes, highly influenced by temperature. Their life span is brief, limited by the depletion of a non-renewable glycogen store. Warmer temperatures under the influence of climate change may promote the transmission of parasites and therefore understanding their thermobiology forms an important step in discerning the future dynamics of parasite populations. An empirical relationship exists between cercarial mean expected life span and the half-life of the population (t0·5) and therefore t0·5 is a good indicator of glycogen utilization. In this study experimental data on the effects of temperature on cercarial survival is compiled from the scientific literature and evaluated in terms of metabolism using Q10 and Arrhenius activation energy (E* or μ), common measures of temperature-mediated reaction rates. Cercariae have a variable response to temperature, which does not appear to be influenced by their life-history attributes or size. There were little differences in Q10 and E* values between most temperature ranges. In almost half the studies examined (7 of 16) cercariae demonstrated a discrete zone of thermostability over a range equivalent to typical individual mean summer temperatures. Distinct intraspecific differences in temperature responses between 3 laboratory strains of Schistosoma mansoni and 2 natural strains of Echinoparyphium recurvatum sensu stricto were apparent. The importance of these results for cercarial biology under global climate change is discussed.

Keywords

cercariaetemperaturetrematodessurvivalmetabolismclimate change
Type
Research Article
Information
Parasitology , Volume 138 , Issue 11 , September 2011 , pp. 1442 - 1452
Copyright
Copyright © Cambridge University Press 2011

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

Atkinson, D. (1994). Temperature and organism size: a biological law for ectotherms? Advances in Ecological Research 25, 1–58.CrossRefGoogle Scholar
Brandts, J. F. (1967). Heat effects on proteins and enzymes. In Thermobiology (ed. Rose, A. H.), pp. 25–72. Academic Press, London, UK.Google Scholar
Combes, C. and Theron, A. (1981). Les densites cercariennes. Memoires du Museum National d'Histoire Naturelle, Serie A, Zoologie 119, 186–196.Google Scholar
Crozier, W. J. (1924). On biological oxidations as function of temperature. Journal of General Physiology 7, 189–216.CrossRefGoogle ScholarPubMed
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
Evans, N. A. and Gordon, D. M. (1983). Experimental studies on the transmission dynamics of the cercariae of Echinoparyphium recurvatum (Digenea: Echinostomatidae). Parasitology 87, 167–174.CrossRefGoogle Scholar
Gammermaister, T. P. (1977). Data on the heat resistance of cercariae of some species of trematodes. Parazitologiya 11, 24–28. [In Russian].Google Scholar
Ginetsinskaya, T. A. (1960). The relationship between the distribution of glycogen in the bodies of different cercariae and their biological peculiarities. Doklady Biological Sciences 135, 949–951.Google Scholar
Ginetsinskaya, T. A. (1988). Trematodes, their life cycles, biology and evolution. Amerind Publishing Company, New Delhi, India.Google Scholar
Harris, A. L. (1986). Larval trematode infections of the freshwater snail Lymnaea peregra (Muller). M. Phil. thesis, Queen Mary and Westfield College, University of London, London, UK.Google Scholar
Hoar, W. S. (1983). General and Comparative Physiology. Prentice-Hall, Englewood Cliffs, USA.Google Scholar
Koprivnikar, J. and Poulin, R. (2009). Interspecific and intraspecific variation in cercariae release. Journal of Parasitology 95, 14–19.CrossRefGoogle ScholarPubMed
Lawson, J. R. and Wilson, R. A. (1980). The survival of the cercariae of Schistosoma mansoni in relation to water temperature and glycogen utilization. Parasitology 81, 337–348.CrossRefGoogle ScholarPubMed
Lee, R. S. (1990). The development of Sanguinicola inermis Plehn, 1905 (Digenea: Sanguinicolidae) in Common Carp, Cyprinus carpio L. Ph.D. thesis, Royal Holloway College, University of London, London, UK.Google 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 ScholarPubMed
Mas-Coma, S., Valero, M. A. and Bargues, M. D. (2009). Climate change effects on trematodiases, with emphasis on zoonotic fascioliasis and schistosomiasis. Veterinary Parasitology 163, 264–280.CrossRefGoogle ScholarPubMed
McCarthy, A. M. (1989). The biology and transmission dynamics of Echinoparyphium recurvatum (Digenea: Echinostomatidae). Ph.D. thesis, King's College, University of London, London, UK.Google 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 ScholarPubMed
Möller, H. (1978). The effects of salinity and temperature on the development and survival of fish parasites. Journal of Fish Biology 12, 311–323.CrossRefGoogle Scholar
Morley, N. J. (2011). Inbred laboratory cultures and natural trematode transmission under climate change. Trends in Parasitology 27, 286–287.CrossRefGoogle ScholarPubMed
Morley, N. J., Crane, M. and Lewis, J. W. (2001). Toxicity of cadmium and zinc to Diplostomum spathaceum (Trematoda: Diplostomidae) cercarial survival. International Journal for Parasitology 31, 1211–1217.CrossRefGoogle ScholarPubMed
Morley, N. J., Adam, M. E. and Lewis, J. W. (2007). Effects of temperature on the transmission and establishment of Echinoparyphium recurvatum (Trematoda: Echinostomatidae) metacercariae in Lymnaea peregra (Gastropoda: Pulmonata). Journal of Helminthology 81, 311–315.CrossRefGoogle Scholar
Morley, N. J., Adam, M. E. and Lewis, J. W. (2010). The effects of host size and temperature on the emergence of Echinoparyphium recurvatum cercariae from Lymnaea peregra under natural light conditions. Journal of Helminthology 84, 317–326.CrossRefGoogle ScholarPubMed
Newell, R. C. (1973). Environmental factors affecting the acclimatory responses of ectotherms. In Effects of Temperature on Ectothermic Organisms (ed. Wieser, W.), pp. 151–164. Springer-Verlag, Berlin, Germany.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
Pietrock, M. and Marcogliese, D. J. (2003). Free-living endohelminth stages: at the mercy of environmental conditions. Trends in Parasitology 19, 293–299.CrossRefGoogle ScholarPubMed
Poulin, R. (2006). Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parasitology 132, 143–151.CrossRefGoogle ScholarPubMed
Poulin, R. and Latham, A. D. M. (2003). Effects of initial (larval) size and host body temperature on growth in trematodes. Canadian Journal of Zoology 81, 574–581.CrossRefGoogle Scholar
Prosser, C. L. (1973). Comparative Animal Physiology, Saunders, Philadelphia, PA, USA.Google Scholar
Purnell, R. E. (1966). Host parasite relationships in schistosomiasis. III. The effect of temperature on the survival of Schistosoma mansoni miracidia and on the survival and infectivity of Schistosoma mansoni cercariae. Annals of Tropical Medicine & Parasitology 60, 182–186.CrossRefGoogle Scholar
Raffel, T. R., Rohr, J. R., Paull, S. H. and Johnson, P. T. J. (2010). Toward a general theory for how climate change will affect infectious disease. Bulletin of the Ecological Society of America 91, 467–473.Google Scholar
Ramajo-Martin, V. and Simon-Martin, F. (1984). Supervivencia e infectividad de las cercarias de Schistosoma bovis en relacion con la edad y la temperatura. Revista Iberica de Parasitologia 44, 399–407.Google Scholar
Ramajo-Martin, V. and Simon-Vicente, F. (1988). Variaciones estacionales de Planorbarius metidjensis en un arroyo de corriente temporal e infeccion de los moluscos por Schistosoma bovis. Revista Iberica de Parasitologia 48, 379–386.Google Scholar
Randall, D., Burggren, W. and French, K. (2001). Eckert Animal Physiology. 5th Edn, Freeman and Company, New York, USA.Google Scholar
Sirag, S. B. and James, E. R. (1982). The effect of different maintenance temperatures of Schistosoma mansoni cercariae. Part 1. Sudan Journal of Veterinary Research 4, 119–123.Google Scholar
Shostak, A. W. and Esch, G. W. (1990). Temperature effects on survival and excystment of cercariae of Halipegus occidualis (Trematoda). International Journal for Parasitology 20, 95–99.CrossRefGoogle ScholarPubMed
Vernberg, W. B. (1963). Respiration of digenetic trematodes. Annals of the New York Academy of Sciences 113, 261–271.CrossRefGoogle ScholarPubMed
Vernberg, W. B. and Hunter, W. S. (1959). Studies on oxygen consumption in digenetic trematodes. III. The relationship of body nitrogen to oxygen uptake. Experimental Parasitology 8, 76–82.CrossRefGoogle ScholarPubMed
Vernberg, W. B. and Vernberg, F. J. (1965). Interrelationships between parasites and their hosts- I. Comparative metabolic patterns of thermal acclimation of larval trematodes with that of their host. Comparative Biochemistry & Physiology 14, 557–566.CrossRefGoogle ScholarPubMed
Walker, R. W. and Barrett, J. (1983). Mitochondrial adenosine triphosphatase activity and temperature adaptation in Schistocephalus solidus (Cestoda: Pseudophyllidea). Parasitology 87, 307–326.CrossRefGoogle Scholar
Whitfield, P. J., Bartlett, A., Khammo, N. and Clothier, R. H. (2003). Age-dependent survival and infectivity of Schistosoma mansoni cercariae. Parasitology 127, 29–35.CrossRefGoogle ScholarPubMed
Wieser, W. (1973). Temperature relations of ectotherms: a speculative review. In Effects of Temperature on Ectothermic Organisms (ed. Wieser, W.), pp. 1–23. Springer-Verlag, Berlin, Germany.CrossRefGoogle Scholar
West, G. B., Woodruff, W. H. and Brown, J. H. (2002). Allometric scaling of metabolic rate from molecules and mitochondria to cells and mammals. Proceedings of the National Academy of Sciences, USA 99, 2473–2478.CrossRefGoogle ScholarPubMed
Xiang, X., Cheng Tai, L., Guo Ren, F., Tian Ping, W., Dabing, L. and Wei Duo, W. (2000). Studies on biology of Echinochasmus liliputanus cercariae. Chinese Journal of Parasitic Disease Control 13, 199–204. [In Chinese].Google Scholar
Yacoubi, B., Zekhnini, A., Rondelaud, D., Vignoles, P., Dreyfuss, G., Cabaret, J. and Moukrim, A. (2007). Habitats of Bulinus truncatus and Planorbarius metidjensis, under a semiarid or an arid climate. Parasitology Research 101, 311–316.CrossRefGoogle ScholarPubMed
Young, R. E., Bundy, D. A. P. and Taylor, N. (1984). A thermostable zone in survivorship and metabolism of a tropical marine cercaria. Comparative Biochemistry & Physiology 78A, 793–798.CrossRefGoogle Scholar