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Thermodynamics of trematode infectivity

Published online by Cambridge University Press:  29 October 2014

N. J. MORLEY  and
J. W. LEWIS
N. J. MORLEY*
Affiliation:
School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey TW20 0EX, UK
J. W. LEWIS
Affiliation:
School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey TW20 0EX, UK
*
*Corresponding author. School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey TW20 0EX, UK. E-mail: n.morley@rhul.ac.uk
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Summary

Temperature is an important factor influencing the biology of organisms and is intrinsically linked to climate change. The establishment of trematodes in target hosts is potentially susceptible to temperature changes effecting parasite infectivity or host susceptibility, and therefore in order to develop predictive frameworks of host–parasite dynamics under climate change large-scale analyses are required. The present study analyses the thermodynamics of the infectivity of larval trematodes including miracidia, cercariae and metacercariae from experimental data contained in the scientific literature using the Arrhenius critical incremental energy of activation (E*), an accurate measure of temperature-driven reaction rates. For miracidia and cercariae, infectivity increases as the temperature rises reaching a plateau over optimal thermal ranges before declining at higher temperatures. In contrast, metacercarial infectivity is at its greatest at low temperatures, declining with increasing temperature.

Keywords

miracidiacercariaemetacercariaetemperatureinfectivitytransmissionclimate change
Type
Research Article
Information
Parasitology , Volume 142 , Issue 4 , April 2015 , pp. 585 - 597
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Copyright
Copyright © Cambridge University Press 2014 

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References

REFERENCES

Al-Jibouri, M. M., Al-Mayah, S. H. and Hassan, H. R. (2011). The factors affecting metacercarial production of Fasciola gigantica from Lymnaea auricularia snails. Journal of Basrah Researches (Sciences) 37, 9–16.Google Scholar
Anderson, R. M., Whitfield, P. J. and Dobson, A. P. (1978). Experimental studies on infection dynamics: infection of definitive host by cercariae of Transversotrema patialense . Parasitology 77, 189–200.CrossRefGoogle ScholarPubMed
Anderson, R. M., Mercer, J. G., Wilson, R. A. and Carter, N. P. (1982). Transmission of Schistosoma mansoni from man to snail: experimental studies of miracidial survival and infectivity in relation to larval age, water temperature, host size and host age. Parasitology 85, 339–360.Google Scholar
Bělehrádek, J. (1935). Temperature and living matter. Protoplasma Monographien 8, 1–277.Google Scholar
Boray, J. C. (1963). The ecology of Fasciola hepatica with particular reference to its intermediate host in Australia. Proceedings of the World Veterinary Congress 17, 709–715.Google Scholar
Brandts, J. F. (1967). Heat effects on proteins and enzymes. In Thermobiology (ed. Rose, A. H.), pp. 25–72. Academic Press, London.Google Scholar
Chadhri, S. S. and Gupta, R. P. (1985). Viability and infectivity of Paramphistomum metacercariae stored under different conditions. Indian Veterinary Journal 62, 470–472.Google Scholar
Christensen, N. O., Frandsen, F. and Nansen, P. (1979). The effect of some environmental conditions and final-host- and parasite-related factors on the penetrations of Schistosoma mansoni cercariae into mice. Zeitschrift fur Parasitenkunde 59, 267–275.CrossRefGoogle ScholarPubMed
Chu, K. Y., Massoud, J. and Sabbaghian, H. (1966). Host-parasite relationship of Bulinus truncates and Schistosoma haematobium in Iran. 3. Effect of water temperature on the ability of miracidia to infect snails. Bulletin of the World Health Organization 34, 131–133.Google Scholar
Colley, F. C. and Olson, A. C. Jr. (1963). Posthodiplostomum minimum (Trematoda: Diplostomidae) in fishes of Lower Otay Reservoir, San Diego County, California. Journal of Parasitology 49, 148.CrossRefGoogle Scholar
Costlow, J. D. Jr., Bookhout, C. G. and Monroe, R. (1960). The effect of salinity and temperature on larval development of Sesarma cinereum (Bosc) reared in the laboratory. Biological Bulletin 118, 183–202.CrossRefGoogle Scholar
Crozier, W. J. (1924). On biological oxidations as function of temperature. Journal of General Physiology 7, 189–216.Google Scholar
Dell, A. I., Pawar, S. and Savage, V. M. (2011). Systematic variation in the temperature dependence of physiological and ecological traits. Proceedings of the National Academy of Sciences of the United States of America 108, 10591–10596.CrossRefGoogle ScholarPubMed
DeWitt, W. B. (1955). Influence of temperature on penetration of snail hosts by Schistosoma mansoni miracidia. Experimental Parasitology 4, 271–276.Google Scholar
DeWitt, W. B. (1965). Effects of temperature on penetration of mice by cercariae of Schistosoma mansoni . American Journal of Tropical Medicine and Hygiene 14, 579–580.Google Scholar
Evans, A. S. and Stirewalt, M. A. (1951). Variations in infectivity of cercariae of Schistosoma mansoni . Experimental Parasitology 1, 19–33.CrossRefGoogle Scholar
Evans, N. A. (1985). Experimental observations on the transmission of Schistosoma margrebowiei miracidia. International Journal for Parasitology 15, 361–364.Google Scholar
Ferrell, D. L., Negovetich, N. J. and Wetzel, E. J. (2001). Effect of temperature on the infectivity of metacercariae of Zygocotyle lunata (Digenea: Paramphistomidae). Journal of Parasitology 87, 10–13.Google Scholar
Foster, R. (1964). The effect of temperature on the development of Schistosoma mansoni Sambon 1907 in the intermediate host. Journal of Tropical Medicine and Hygiene 67, 289–292.Google Scholar
Ghandour, A. M. (1976). A study of the relationship between temperature and the infectivity of Schistosoma mansoni and Schistosoma haematobium cercariae. Journal of Helminthology 50, 193–196.CrossRefGoogle ScholarPubMed
Ghandour, A. M. and Webbe, G. (1973). A study of the death of Schistosoma mansoni cercariae during penetration of mammalian host skin: the influence of the ages of the cercariae and of the host. International Journal for Parasitology 3, 789–794.CrossRefGoogle ScholarPubMed
Ginetsinskaya, T. A. (1988). Trematodes, their Life Cycles, Biology and Evolution. Amerind Publishing Company, New Delhi.Google Scholar
Gold, D. and Goldberg, M. (1979). Temperature effect on susceptibility of four species of Lymnaea snails to infection with Fasciola hepatica (Trematoda). Israel Journal of Zoology 28, 193–198.Google Scholar
Hoar, W. S. (1983). General and Comparative Physiology. Prentice-Hall, Englewood Cliffs.Google Scholar
Humiczewska, M. (2004). Some enzymes of respiratory chain in metacercariae of Fasciola hepatica . Zoologica Poloniae 49, 63–76.Google Scholar
Ittiprasert, W. and Knight, M. (2012). Reversing the resistance phenotype of the Biomphalaria glabrata snail host Schistosoma mansoni infection by temperature modulation. PLoS Pathogens 8, e1002677.Google Scholar
Jamjoom, M. B. and Banaja, A. E. A. (2007). Comparative studies on the susceptible and non-susceptible Biomphalaria alexandrina the intermediate snail host of Schistosoma mansoni in western Saudi Arabia. World Journal of Medical Sciences 2, 108–114.Google Scholar
Kellogg, S. J. and Olson, A. C. Jr. (1963). Some factors influencing the infectivity of the metacercariae of Posthodiplostomum minimum (Trematoda: Diplostomidae). Journal of Parasitology 49, 744.Google Scholar
Kruatrachue, M., Chitramvong, Y. P., Upatham, E. S., Vichasri, S. and Viyanant, V. (1982). Effects of physico-chemical factors on the infection of hamsters by metacercariae of Opisthorchis viverrini . Southeast Asian Journal of Tropical Medicine and Public Health 13, 614–617.Google Scholar
Landis, S. H., Kalbe, M., Reusch, T. B. H. and Roth, O. (2012). Consistent pattern of local adaptation during an experimental heat wave in a pipefish-trematode host–parasite system. PLoS ONE 7, e30658.CrossRefGoogle Scholar
Lewis, J. W. (1976). Studies on the biology of Phyllodistomum folium from the Worcester–Birmingham canal and the Water Gardens, Winterbourne. PhD thesis, University of Birmingham, UK.Google Scholar
Lo, C. T. (1972). Compatibility and host–parasite relationships between species of the genus Bulinus (Basommatophora: Planorbidae) and an Egyptian strain of Schistosoma haematobium (Trematoda: Digenea). Malacologia 11, 225–280.Google Scholar
Lwambo, N. J. S., Upatham, E. S., Kruatrachue, M. and Viyanant, V. (1987). The host–parasite relationship between the Saudi Arabian Schistosoma mansoni and its intermediate and definitive hosts. 2. Effects of temperature, salinity and pH on the infection of mice by S. mansoni cercariae. Southeast Asian Journal of Tropical Medicine and Public Health 18, 166–170.Google Scholar
Maldonado, J. F. and Acosta-Matienzo, J. (1948). Biological studies on the miracidium of Schistosoma mansoni . American Journal of Tropical Medicine and Hygiene 28, 645–657.Google Scholar
Mangum, C. P., Oakes, M. J. and Shick, J. M. (1972). Rate-temperature responses in scyphozoan medusa and polyps. Marine Biology 15, 298–303.Google Scholar
McCarthy, A. M. (1989). The biology and transmission dynamics of Echinoparyphium recurvatum (Digenea: Echinostomatidae) . Ph.D. thesis. King's College, University of 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.Google Scholar
McKindsey, C. W. and McLaughlin, J. D. (1995). Species- and size-specific infection of snails by Cyclocoelum mutabile (Digenea: Cyclocoelidae). Journal of Parasitology 81, 513–519.Google Scholar
Marples, M. J. (1965). The Ecology of Human Skin. Springfield, Illinois.Google Scholar
Meyrowitsch, D., Christensen, N. O. and Hindsbo, O. (1991). Effects of temperature and host density on the snail-finding capacity of cercariae of Echinostoma caproni (Digena: Echinostomatidae). Parasitology 102, 391–395.CrossRefGoogle Scholar
Morley, N. J. (2011). Thermodynamics of cercarial survival and metabolism in a changing climate. Parasitology 138, 1442–1452.Google Scholar
Morley, N. J. (2012). Thermodynamics of miracidial survival and metabolism. Parasitology 139, 1640–1651.CrossRefGoogle ScholarPubMed
Morley, N. J. and Lewis, J. W. (2013). Thermodynamics of cercarial development and emergence in trematodes. Parasitology 140, 1211–1224.CrossRefGoogle ScholarPubMed
Morley, N. J. and Lewis, J. W. (2014). Temperature stress and parasitism of endothermic hosts under climate change. Trends in Parasitology 30, 221–227.Google Scholar
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.Google 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.Google 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. (2010 a). The scaling of dose with host body mass and the determinants of success in experimental cercarial infections. International Journal for Parasitology 40, 371–377.CrossRefGoogle ScholarPubMed
Poulin, R. (2010 b). The selection of experimental doses and their importance for parasite success in metacercarial infection studies. Parasitology 137, 889–898.Google Scholar
Prah, S. K. and James, C. (1977). The influence of physical factors on the survival and infectivity of miracidia of Schistosoma mansoni and S. haematobium I. Effect of temperature and ultra-violet light. Journal of Helminthology 51, 73–85.CrossRefGoogle ScholarPubMed
Prosser, C. L. (1973). Comparative Animal Physiology. Saunders, Philadelphia.Google Scholar
Precht, H., Laudien, H. and Havsteen, B. (1973). The normal temperature range. In Temperature and Life (ed. Precht, H., Christophersen, J., Hensel, H. and Larcher, W.), pp. 302–399, Springer-Verlag, New York.Google Scholar
Purnell, R. E. (1966 a). Host–parasite relationships in schistosomiasis. I.: the effect of temperature on the infection of Biomphalaria sudanica tanganyicensis with Schistosoma mansoni miracidia and of laboratory mice with Schistosoma mansoni cercariae. Annals of Tropical Medicine and Parasitology 60, 90–93.Google Scholar
Purnell, R. E. (1966 b). 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 and Parasitology 60, 182–186.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
Rea, J. G. and Irwin, S. W. B. (1995). The effects of age, temperature and shadow stimuli on activity patterns of the cercariae of Cryptocotyle lingua (Digenea: Heterophyidae). Parasitology 111, 95–101.Google Scholar
Richards, C. S. and Shade, P. C. (1987). The genetic variation of compatibility in Biomphalaria glabrata and Schistosoma mansoni . Journal of Parasitology 73, 1146–1151.Google Scholar
Samnaliev, P. and Vassilev, I. (1976). Ecology of the larval and parthenite stages of Paramphistomum microbothrium. I. Effect of the temperature, UV rays and X-ray irradiation on the development of eggs. Khelmintologiia 1, 88–98 [In Bulgarian]Google Scholar
Samnaliev, P. and Vassilev, I. (1979). Ecology of the larval and parthenite stages of Paramphistomum microbothrium. III. The effect of temperature on the invasiveness of miracidia. Khelmintologiia 7, 77–81 [In Bulgarian]Google Scholar
Sirag, S. B. and James, E. R. (1982). The effects of temperature and age on the infectivity of Schistosoma mansoni cercariae. Part II. Sudan Journal of Veterinary Research 4, 125–127.Google Scholar
Stables, J. N. and Chappell, L. H. (1986). Diplostomum spathaceum (Rud. 1819) – Effects of physical factors on the infection of rainbow trout (Salmo gairdneri) by cercariae. Parasitology 93, 71–79.Google Scholar
Stek, M. Jr. and Sulaiman, S. M. (1984). Thermal effects on Schistosoma mansoni irradiation-attenuated vaccine production and administration. Proceedings of the Helminthological Society of Washington 51, 287–292.Google Scholar
Stirewalt, M. A. and Fregeau, W. A. (1965). Effect of selected experimental conditions on penetration and maturation of Schistosoma mansoni in mice. I. Environmental. Experimental Parasitology 17, 168–179.Google Scholar
Studer, A. and Poulin, R. (2014). Analysis of trait mean and variability versus temperature in trematode cercariae: is there scope for adaptation to global warming? International Journal for Parasitology 44, 403–413.Google Scholar
Studer, A., Thieltges, D. W. and Poulin, R. (2010). Parasites and global warming: net effects of temperature on an intertidal host-parasite system. Marine Ecology Progress Series 415, 11–22.Google Scholar
Thieltges, D. W. and Rick, J. (2006). Effect of temperature on emergence, survival and infectivity of cercariae of the marine trematode Renicola roscovita (Digenea: Renicolidae). Diseases of Aquatic Organisms 73, 63–68.Google Scholar
Ubelaker, J. E. and Olsen, O. W. (1970). Influence of temperature on survival rate and infectivity of miracidia of two species of Phyllodistomum trematoda to pelecypods. Journal of Invertebrate Pathology 16, 363–366.Google Scholar
Upatham, E. S. (1973). The effect of water temperature on the penetration and development of St. Lucian Schistosoma mansoni miracidia in local Biomphalaria glabrata . Southeast Asian Journal of Tropical Medicine and Public Health 4, 367–370.Google Scholar
Upatham, E. S., Kruatrachue, M. and Khunborivan, V. (1984). Effects of physico-chemical factors on the infection of mice with Schistosoma japonicum and S. mekongi cercariae. Southeast Asian Journal of Tropical Medicine and Public Health 15, 254–260.Google Scholar
Vernberg, F. J. and Vernberg, W. B. (1964). Metabolic adaptation of animals from different latitudes. Helgolander Meeresuntersuchungen 9, 476–487.Google Scholar
Vladimirova, I. G. (2000). Relationship between respiration rate and temperature in Gastropods. Biology Bulletin 27, 383–392.Google Scholar
Vladimirova, I. G., Kleimenov, S. Yu. and Radzinskaya, L. I. (2003). The relationship of energy metabolism and body weight in bivalves (Mollusca: bivalvia). Biology Bulletin 30, 392–399.Google Scholar
Waadu, G. D. B. and Chappell, L. H. (1991). Effect of water temperature on the ability of Diplostomum spathaceum miracidia to establish in Lymnaeid snails. Journal of Helminthology 65, 179–185.Google Scholar
Wakelin, D. (1978). Genetic control of susceptibility and resistance in parasitic infection. Advances in Parasitology 16, 219–308.Google Scholar
Wen, S.-T. (1961). The behaviour of the free-living stages of the larvae – miracidium and cercaria – of Schistosoma mansoni and S. haematobium, with special reference to their modes of host-finding and host-penetration . Ph.D. thesis. External, University of London.Google Scholar
Wilson, R. A. and Denison, J. (1970). Studies on the activity of the miracidium of the common liver fluke, Fasciola hepatica . Comparative Biochemistry and Physiology 32, 301–313.Google Scholar
Yvon-Durocher, G., Caffrey, J. M., Cescatti, A., Dossena, M., Giorgio, P. D., Gasol, J. M., Montoya, J. M., Pumpanen, J., Staehr, P. A., Trimmer, M., Woodward, G. and Allen, A. P. (2012). Reconciling the temperature dependence of respiration across timescales and ecosystem types. Nature 487, 472–476.Google Scholar