Hostname: page-component-76fb5796d-45l2p Total loading time: 0 Render date: 2024-04-30T04:07:05.972Z Has data issue: false hasContentIssue false
  • English
  • Français

Thermodynamics of cercarial development and emergence in trematodes

Published online by Cambridge University Press:  20 December 2012

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: Tel.: +44 (0)1784 443186. Fax: +44 (0)1784 414224. E-mail: n.morley@rhul.ac.uk
Get access Rights & Permissions [Opens in a new window]

Summary

Temperature is an important factor influencing the biology of ectothermic organisms and is intrinsically linked to climate change. Trematodes are potentially susceptible to temperature changes and in order to develop predictive frameworks of their responses to climate change large-scale analyses are needed. The present study, using the Q10 value, analyses experimental data from the scientific literature on the effects of temperature on cercarial development and emergence across a wide range of temperature in low (⩽35°) and mid-latitude (36–60°) species. Temperature appears to have no significant effect on the rate of development of cercariae within molluscan hosts. Data on cercarial emergence, corrected to incorporate the minimum emergence temperature threshold (METT) and acclimation status, was found to be largely unaffected by temperature over optimum ranges of ≈20 °C (15–25 °C) for mid-latitude species and ≈25 °C (20–30 °C) for low-latitude species. In addition, a decline in emergence rates was shown at higher temperatures. These results are contrary to a previous study on the meta-analysis of cercarial emergence. Some evidence of strain-specific differences and thermostability over a wide temperature range for both cercarial development and emergence was apparent. The significance of these results in furthering our understanding of cercarial biology under natural conditions is discussed.

Keywords

cercariaedevelopmentemergencesheddingtemperatureclimate change
Type
Research Article
Information
Parasitology , Volume 140 , Issue 10 , September 2013 , pp. 1211 - 1224
Copyright
Copyright © Cambridge University Press 2012 

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

Akramova, F. D., Azimov, D. A. and Shakarboev, E. B. (2010). The morphology and biology of the trematode Gigantobilharzia acotylea (Digena, Schistosomatidae). Vestnik Zoologii 44, e1–e10.CrossRefGoogle Scholar
Al-Habbib, W. M. S. and Al-Zako, S. S. (1981). The effect of different temperatures on the development of intra-molluscan stages of Fasciola gigantica. Journal of Thermal Biology 6, 373–377.CrossRefGoogle Scholar
Al-Habbib, W. M. S. and Grainger, J. N. R. (1983). The effect of constant and changing temperature on the rate of development of the eggs and the larval stages of Fasciola hepatica. Proceedings of the Royal Irish Academy 83B, 281–290.Google Scholar
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. and May, R. M. (1979). Prevalence of schistosome infections within molluscan populations: observed patterns and theoretical predictions. Parasitology 79, 63–94.CrossRefGoogle ScholarPubMed
Anderson, P. A., Nowsielski, J. W. and Croll, N. A. (1976). The emergence of cercariae of Trichobilharzia ocellata and its relationship to the activity of its snail host Lymnaea stagnalis. Canadian Journal of Zoology 54, 1481–1487.CrossRefGoogle Scholar
Aoki, Y., Sata, K., Muhoho, N. D., Noda, S. I. and Kimura, E. (2003). Cercariometry for detection of transmission sites for schistosomiasis. Parasitology International 52, 403–408.CrossRefGoogle ScholarPubMed
Asch, H. L. (1972). Rhythmic emergence of Schistosoma mansoni cercariae from Biomphalaria glabrata: Control by illumination. Experimental Parasitology 31, 350–355.CrossRefGoogle ScholarPubMed
Ataev, G. L. (1991). Development of rediae and cercariae of Philophthalmus rhionica (Trematoda) in starved molluscan hosts. Parazitologiya 25, 456–461. [In Russian.]Google Scholar
Awi, G. D. B. (1986). The pathogenesis of Diplostomum spathaceum (Rudolphi, 1819) in freshwater molluscs. Ph.D. thesis, University of Aberdeen, Aberdeen, UK.Google Scholar
Biswas, G. and Subramanian, G. (1988). Development pattern of Schistosoma nasale in experimentally reared Indoplanobis exustus. Indian Journal of Animal Health 27, 123–126.Google Scholar
Blankespoor, H. D., Babiker, S. M. and Blankespoor, C. L. (1989). Influence of temperature on the development of Schistosoma haematobium in Bulinus truncatus. Journal of Medical & Applied Malacology 1, 123–131.Google Scholar
Boissier, J., Rivera, E. R. and Mone, H. (2003). Altered behaviour of the snail Biomphalaria glabrata as a result of infection with Schistosoma mansoni. Journal of Parasitology 89, 429–433.CrossRefGoogle 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, UK.Google Scholar
Crozier, W. J. (1924). On biological oxidations as function of temperature. Journal of General Physiology 7, 189–216.CrossRefGoogle ScholarPubMed
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, USA 108, 10591–10596.CrossRefGoogle ScholarPubMed
Dinnik, J. A. and Dinnik, N. N. (1964). The influence of temperature on the succession of redial and cercarial generations of Fasciola gigantica in a snail host. Parasitology 54, 59–65.CrossRefGoogle Scholar
Dovgalev, A. S. (1987). The effects of temperature on the shedding times of Metagonimus yokogawai cercariae by molluscs. Meditsinskaya Parazitologiya i Parazitarnye Bolezni 1987, 47–50. [In Russian.]Google Scholar
Dutt, S. C. and Srivastava, H. D. (1962). Biological studies on Orientobilharzia dattai (Dutt and Srivastava, 1952) Dutt and Srivastava, 1955- a blood fluke of ruminants. Indian Journal of Veterinary Science & Animal Husbandry 32, 216–228.Google 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
Foster, R. (1964). The effect of temperature on the development of Schistosoma mansoni Sambon 1907 in the intermediate host. Journal of Tropical Medicine & Hygiene 67, 289–292.Google ScholarPubMed
Frandsen, F. and Christensen, N. O. (1984). An introductory guide to the identification of cercariae from African freshwater snails with special reference to cercariae of trematode species of medical and veterinary importance. Acta Tropica 41, 181–202.Google Scholar
Frank, G. H. (1966). The effect of temperature on the rate of development and emergence of Schistosome cercariae. Zoologica Africana 2, 211–221.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 ScholarPubMed
Gayevskaya, A. V. (1972). Effect of light and water temperature on the emergence of some species of cercariae from Black sea mollusks. Hydrobiological Journal 8, 84–85.Google Scholar
Ginetsinskaya, T. A. (1988). Trematodes, their Life Cycles, Biology and Evolution. Amerind Publishing Company, New Delhi, India.Google Scholar
Gordon, R. M., Davey, T. H. and Peaston, H. (1934). The transmission of human bilharziasis in Sierra Leone, with an account of the life-cycle of schistosomes concerned, S. mansoni and S. haematobium. Annals of Tropical Medicine & Parasitology 28, 323–418.CrossRefGoogle Scholar
Gumble, A., Otori, Y., Ritchie, L. S. and Hunter, G. W. III (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
Hansen, E. L. (1975). Secondary daughter sporocysts of Schistosoma mansoni: Their occurrence and cultivation. Annals of the New York Academy of Sciences 266, 426–436.CrossRefGoogle ScholarPubMed
Harris, A. L. (1986). Larval trematode infections of the freshwater snail Lymnaea peregra (Muller). M.Phil. thesis, Queen Mary & Westfield College, University of London, London, UK.Google Scholar
Hoar, W. S. (1983). General and Comparative Physiology. Prentice-Hall, Englewood Cliffs, NJ, USA.Google Scholar
Karvonen, A., Kirsi, S., Hudson, P. J. and Valtonen, E. T. (2004). Patterns of cercarial production from Diplostomum spathaceum: terminal investment or bet hedging? Parasitology 129, 87–92.CrossRefGoogle ScholarPubMed
Kendall, S. B. (1964). Some factors influencing the development and behaviour of trematodes in their molluscan hosts. In Host-Parasite Relationships in Invertebrate Hosts (Second Symposium of the British Society for Parasitology) (ed. Taylor, A. E. R.), pp. 51–73, Blackwell Scientific Publications, Oxford, UK.Google Scholar
Koprivnikar, J. and Poulin, R. (2009 a). Interspecific and intraspecific variation in cercariae release. Journal of Parasitology 95, 14–19.CrossRefGoogle ScholarPubMed
Koprivnikar, J. and Poulin, R. (2009 b). Effects of temperature, salinity, and water level on the emergence of marine cercariae. Parasitology Research 105, 957–965.CrossRefGoogle ScholarPubMed
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 ScholarPubMed
Lee, F. O. and Cheng, T. C. (1971). Schistosoma mansoni infection in Biomphalaria glabrata: Alterations in heart rate and thermal tolerance in the host. Journal of Invertebrate Pathology 18, 412–418.CrossRefGoogle ScholarPubMed
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 ScholarPubMed
Lewis, J. W. (1976). Studies on the biology of Phyllodistomum folium from the Worcester-Birmingham canal and the Water Gardens, Winterbourne. Ph.D. thesis, University of Birmingham, 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
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
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
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
Mangal, T. D. (2009). Developing spatio-temporal models of schistosomiasis transmission with climate change. Ph.D. thesis, University of Liverpool, Liverpool, UK.Google 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.Google ScholarPubMed
Marcogliese, D. J. (2008). The impact of climate change on the parasites and infectious diseases of aquatic animals. Revue Scientifique et Technique (Office international des Epizooties) 27, 467–484.CrossRefGoogle ScholarPubMed
Martin, S. and Vazquez, R. (1984). Biology and behaviour of the cercariae of a Sanguinicola sp. in the River Cilloruelo (Salamanca, Spain). Annales de Parasitologie Humaine et Comparee 59, 231–236.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
McDaniel, S. J. (1969). Littorina littorea: Lowered heat tolerance due to Cryptocotyle lingua. Experimental Parasitology 25, 13–15.CrossRefGoogle ScholarPubMed
Mills, C. A. (1980). Temperature-dependent survival and reproduction within populations of the ectoparasitic digenean Transversotrema patialense on the fish host. Parasitology 81, 91–102.CrossRefGoogle Scholar
Moravec, F., Barus, V., Rysavy, B. and Yousif, F. (1974). Observations on the development of two echinostomes, Echinoparyphium recurvatum and Echinostoma revolutum, the antagonists of human schistosomes in Egypt. Folia Parasitologica 21, 107–126.Google ScholarPubMed
Morley, N. J. (2011 a). Thermodynamics of cercarial survival and metabolism in a changing climate. Parasitology 138, 1442–1452.CrossRefGoogle Scholar
Morley, N. J. (2011 b). Inbred laboratory cultures and natural trematode transmission under climate change. Trends in Parasitology 27, 286–287.CrossRefGoogle ScholarPubMed
Morley, N. J. (2012 a). Thermodynamics of miracidial survival and metabolism. Parasitology 139, 1640–1651.CrossRefGoogle ScholarPubMed
Morley, N. J. (2012 b). Cercariae (Platyhelminthes: Trematoda) as neglected components of zooplankton communities in freshwater habitats. Hydrobiologia 691, 7–19.CrossRefGoogle 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.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
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 ScholarPubMed
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
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
Nice, N. G. (1979). Some aspects of the biology of Fasciola hepatica and its intermediate snail host Lymnaea truncatula. D.Phil. Thesis, University of York, York, UK.Google Scholar
Nojima, H. and Sato, A. (1978). The emergence of schistosome cercariae from snails. Part 1. Hourly response of cercarial emergence of Schistosoma mansoni and Schistosoma haematobium and effect of light cut on their emergence. Japanese Journal of Parasitology 27, 197–214. [In Japanese.]Google Scholar
Ollerenshaw, C. B. (1971). Some observations on the epidemiology of fascioliasis in relation to the timing of molluscicide applications in the control of the disease. Veterinary Record 88, 152–164.CrossRefGoogle Scholar
Paull, S. H. and Johnson, P. T. J. (2011). High temperature enhances host pathology in a snail-trematode system: possible consequences of climate change for the emergence of disease. Freshwater Biology 56, 767–778.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.CrossRefGoogle ScholarPubMed
Pflüger, W. (1981). Experimental epidemiology of schistosomiasis. II. Prepatency of Schistosoma mansoni in Biomphalaria glabrata at diurnally fluctuating temperatures. Zeitschrift für Parasitenkunde 66, 2221–229.Google ScholarPubMed
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 ScholarPubMed
Poulin, R. (2006). Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parasitology 132, 143–151.CrossRefGoogle ScholarPubMed
Prosser, C. L. (1973). Comparative Animal Physiology. Saunders, Philadelphia, PA, USA.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, USA.CrossRefGoogle Scholar
Prinz, K., Kelly, T. C., O'Riordan, R. M. and Culloty, S. C. (2011). Factors influencing cercarial emergence and settlement in the digenean trematode Parorchis acanthus (Philophthalmidae). Journal of the Marine Biological Association of the UK 91, 1673–1679.CrossRefGoogle Scholar
Raišyté, D. (1968). On the biology of Apatemon gracilis (Rud., 1819), a trematode parasitic in domestic and wild ducks. Acta Parasitologica Lithuanica 7, 71–84.Google Scholar
Randall, D., Burggren, W. and French, K. (2001). Eckert Animal Physiology. 5th Edn. Freeman and Company, New York, USA.Google Scholar
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 ScholarPubMed
Riel, A. (1975). Effect of trematodes on survival of Nassarius obsoletus (Say). Proceedings of the Malacological Society of London 41, 527–528.Google Scholar
Rojo-Vazquez, F. A. and Simon-Martin, F. (1985). Algunos aspectos de la biologia de las cercarias de Trichobilharzia sp. del Rio Canedo (Provincia de Salamanca, Espana). Revista Iberica de Parasitologia 45, 141–148.Google Scholar
Roushdy, M. Z. (1984). The effect of diurnal fluctuating temperature on the development of Schistosoma haematobium in Bulinus truncatus. Journal of the Egyptian Society of Parasitology 14, 507–514.Google Scholar
Šarounová, P. (2011). Effect of temperature on emergence of cercariae of model freshwater trematodes. Bc.Thesis, University of South Bohemia in České Budějovice, Czech Republic.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 ScholarPubMed
Shalaby, I. M., Hassan, M. G., Soliman, M. F. M. and Sherif, N. E. (2004). Factors affecting dynamics of metacercarial productivity of Fasciola gigantica from its snail host. Pakistan Journal of Biological Sciences 7, 393–398.CrossRefGoogle Scholar
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
Soliman, M. F. M. (2009). Fasciola gigantica: Cercarial shedding pattern from Lymnaea natalensis after long-term exposure to cadmium at different temperatures. Experimental Parasitology 121, 307–311.CrossRefGoogle ScholarPubMed
Sous, S. M. (1992). Influence of abiotic factors on emission and survival of cercariae of Diplostomum chromatophorum (Brown, 1931) (Trematoda, Diplostomidae). Ecological Parasitology 1, 154–159.Google Scholar
Stirewalt, M. (1954). Effect of snail maintenance temperatures on development of Schistosoma mansoni. Experimental Parasitology 3, 504–516.CrossRefGoogle ScholarPubMed
Stirewalt, M. (1981). Schistosoma mansoni: Conditions contributing to maximal cercarial harvests. Journal of Parasitology 67, 582–583.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Terhune, J. S., Wise, D. J. and Khoo, L. H. (2002). Bolbophorus confuses 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
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 ScholarPubMed
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
Vernberg, W. B. (1961). Studies on oxygen consumption in digenetic trematodes. VI. The influence of temperature on larval trematodes. Experimental Parasitology 11, 270–275.CrossRefGoogle ScholarPubMed
Vernberg, W. B. (1969). Adaptations of host and symbionts in the intertidal zone. American Zoologist 9, 357–365.CrossRefGoogle Scholar
Vernberg, W. B. and Vernberg, F. J. (1963). Influence of parasitism on thermal resistance of the mud-flat snail, Nassarius obsoleta Say. Experimental Parasitology 14, 330–332.CrossRefGoogle ScholarPubMed
Vladimirova, I. G. (2000). Relationship between respiration rate and temperature in Gastropods. Biology Bulletin 27, 383–392.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.CrossRefGoogle ScholarPubMed
Wagner, E. D. and Moore, B. (1959). The development of Schistosoma mansoni in snails kept at certain constant temperatures. Transactions of the American Microscopical Society 78, 424–428.CrossRefGoogle Scholar
Watertor, J. L. (1968). Effects of temperature stress on growth and development of larval and adult Telorchis bonnerensis (Trematoda: Telorchiidae). Journal of Parasitology 54, 506–508.CrossRefGoogle Scholar
Yang, G.-J., Utzinger, J., Sun, L.-P., Hong, Q.-B., Vounatsou, P., Tanner, M. and Zhou, X.-N. (2007). Effect of temperature on the development of Schistosoma japonicum within Oncomelania hupensis, and hibernation of O. Hupensis. Parasitology Research 100, 695–700.CrossRefGoogle ScholarPubMed