Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-27T08:51:57.216Z Has data issue: false hasContentIssue false
  • English
  • Français

Thermodynamics of egg production, development and hatching in trematodes

Published online by Cambridge University Press:  06 May 2016

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

Abstract

Temperature is a key factor influencing the rate of biological processes of ectothermic animals and is intrinsically linked to climate change. Trematode parasites may be potentially susceptible to temperature changes and, in order to develop a predictive framework of their response to climate change, large-scale analyses are needed. In particular, the biology of the egg of all species is at some time influenced by environmental conditions. The present study uses Arrhenius activation energy (E*), a common measure of temperature-mediated reaction rates, to analyse experimental data from the scientific literature on the effects of temperature on the production, development and hatching of trematode eggs. Egg production declines at high temperatures, with habitat-specific climatic factors determining the optimal thermal range. Egg development, as is typical of invertebrates, shows a simple response to temperature, with minimal differences between mid- (35–60°) and low-latitude (<35°) species. Egg hatching demonstrates variable thermodynamics with high E* values at low temperature ranges and thermostability at mid-temperatures, before declining at high temperature ranges, with wide thermostable zones being a common feature. Comparisons between development and hatching indicate that these two parameters demonstrate different thermodynamical responses. The significance of these results in furthering our understanding of trematode egg biology under natural conditions is discussed.

Type
Research Papers
Information
Journal of Helminthology , Volume 91 , Issue 3 , May 2017 , pp. 284 - 294
Copyright
Copyright © Cambridge University Press 2016 

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

Akpom, C.A. & Warren, K.S. (1975) Calorie and protein malnutrition in chronic murine Schistosomiasis mansoni: effect on the parasite and the host. Journal of Infectious Diseases 132, 6–14.Google Scholar
Akramova, F.D., Azimov, D.A. & Shakarboev, E.B. (2011) Morphology, biology and taxonomy of Dendritobilharzia loossi Skrjabin, 1924 (Trematoda: Bilharziellidae), a parasite of Pelecanus onocrotalus (Pelecanidae) and Anas plathyrinchos (Anatidae). Parasite 18, 39–48.CrossRefGoogle ScholarPubMed
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., Hassan, H.R. & Al-Mayah, S.H. (2010) Ecological factors affecting egg development and life span of miracidia of Fasciola gigantica . Kerbala Journal of Pharmaceutical Sciences 1, 74–80.Google Scholar
Amarasinghe, L.D. & Kumara, H.L.N.N. (2007) Effect of rainfall and temperature on liver and rumen fluke infestations of bovines in Sri Lanka. International Journal of Biological and Chemical Sciences 1, 229–236.Google Scholar
Ataev, G.L. (1993) [The temperature and elimination influence on the biology of Philophthalmus rhionica miracidia]. Parazitologiya 27, 134–139 (in Russian).Google Scholar
Barry, R.G. & Chorley, R.J. (2003) Atmosphere, weather and climate. 8th edn. London, Routledge.Google Scholar
Basch, P.F. (1991) Schistosomes: development, reproduction and host relations. New York, Oxford University Press.Google Scholar
Berkhout, B.W., Lloyd, M.M., Poulin, R. & Studer, A. (2014) Variation among genotypes in responses to increasing temperature in a marine parasite: evolutionary potential in the face of global warming? International Journal for Parasitology 44, 1019–1027.Google Scholar
Brandts, J.F. (1967) Heat effects on proteins and enzymes. pp. 25–72 in Rose, A.H (Ed.) Thermobiology. London, Academic Press.Google Scholar
Campbell, W.C. (1961) Notes on the egg and miracidium of Fascioloides magna (Trematoda). Transactions of the American Microscopical Society 80, 308–319.Google Scholar
Christensen, N.O., Frandsen, F. & Roushdy, M.Z. (1980) The influence of environmental conditions and parasite-intermediate host-related factors on the transmission of Echinostoma liei . Zeitschrift für Parasitenkunde 63, 47–63.Google Scholar
Chubb, J.C. (1979) Seasonal occurrence of helminths in freshwater fishes. Part II. Trematoda. Advances in Parasitology 17, 141–313.CrossRefGoogle Scholar
Cossins, A.R. & Bowler, K. (1987) Temperature biology of animals. London, Chapman & Hall.Google Scholar
Crozier, W.J. (1924) On biological oxidations as function of temperature. Journal of General Physiology 7, 189–216.Google Scholar
DeWitt, W.B. (1955) Influence of temperature on penetration of snail hosts by Schistosoma mansoni miracidia. Experimental Parasitology 4, 271–276.CrossRefGoogle ScholarPubMed
Fagbemi, B.O. (1984) The effects of environmental factors on the development, behaviour and survival of Paramphistomum microbothrium miracidia. Veterinary Parasitology 16, 71–81.CrossRefGoogle ScholarPubMed
Ginetsinskaya, T.A. (1988) Trematodes, their life cycles, biology and evolution. New Delhi, Amerind Publishing Company.Google Scholar
Gold, D. & Goldberg, M. (1976) Effect of light and temperature on hatching in Fasciola hepatica (Trematoda: Fasciolidae). Israel Journal of Zoology 25, 178–185.Google Scholar
Gonzalez-Langa, C., Manga-Gonzalez, Y., Del-Pozo-Carnero, P. & Hidalgo-Argüello, R. (1989) Dynamics of elimination of the eggs of Fasciola hepatica (Trematode, Digenea) in the faeces of cattle in the Porma Basin, Spain. Veterinary Parasitology 34, 35–43.CrossRefGoogle Scholar
Gonzalez-Langa, C., Manga-Gonzalez, Y. & Del-Pozo-Carnero, P. (1993) Coprological study of the Dicrocoelium dendriticum (Digenea) egg elimination by cattle in highland areas in León Province, Northwest Spain. Parasitology Research 79, 488–491.Google Scholar
Hanna, R.E., Williamson, D.S., Mattison, R.G. & Nizami, W.A. (1988) Seasonal reproduction in Paramphistomum epiclitum and Gastrothylax crumenifer, rumen paramphistomes of the Indian water buffalo, and comparison with the biliary paramphistome Gigantocotyle explanatum . International Journal for Parasitology 18, 513–521.CrossRefGoogle ScholarPubMed
Hira, P.R. (1967) Studies on the hatching of Schistosoma haematobium ova and some factors influencing the process. Journal of the West African Science Association 12, 95–102.Google Scholar
Hira, P.R. (1968) Studies on the miracidia and cercariae of Schistosoma haematobium Bilharz. Journal of the West African Science Association 13, 165–172.Google Scholar
Hoar, W.S. (1983) General and comparative physiology. Englewood Cliffs, Prentice-Hall.Google Scholar
Horstmann, H.J. (1962) Sauerstoffverbrauch und glycogengehalt der eier von Fasciola hepatica wahrend der entwicklung der miricidien. Zeitschrift für Parasitenkunde 21, 437–445.Google Scholar
Ichii, S., Irie, Y. & Yasuraoka, K. (1990) Growth and fecundity of Schistosoma japonicum in mice maintained at different environmental temperatures. Japanese Journal of Experimental Medicine 60, 39–44.Google Scholar
Islam, K.M., Islam, M.S., Rauf, S.M.A., Khan, A., Hossain, M.K., Adhikary, G.N., Sarkar, S. & Rahman, M. (2014) Effects of climatic factors on prevalence of developmental stages of Fasciola gigantica infection in Lymnaea snails (Lymnaea auricularia var. rufescens) in Bangladesh. Journal of Chemical, Biological, and Physical Sciences, Section B 5, 301–310.Google Scholar
Ito, J. (1955) Studies on hatchability of Schistosoma japonicum eggs in several external environmental conditions. Japanese Journal of Medical Science and Biology 8, 175–184.Google Scholar
Jurberg, A.D., Pascarelli, B.M., Pelajo-Machado, M., Maldonado, A. Jr, Mota, E.M. & Lenzi, H.L. (2008) Trematode embryology: a new method for whole-egg analysis by confocal microscopy. Development Genes and Evolution 218, 267–271.Google Scholar
Khan, P., Abidi, S.M.A., Nizami, W.A., Irshadullah, M. & Ahmad, M. (1991) Biochemical changes during the development of the miracidium of Gigantocotyle explanatum . International Journal for Parasitology 21, 731–734.Google Scholar
Koehler, A.V., Brown, B., Poulin, R., Thieltges, D.W. & Fredensborg, B.L. (2012) Disentangling phylogenetic constraints from selective forces in the evolution of trematode transmission stages. Evolutionary Ecology 26, 1497–1512.Google Scholar
Lambrecht, F.L. (1967) The influence of certain environmental factors on the development of eggs and survival of miracidia of Echinostoma barbosai Lie and Bach, 1966. Revista do Instituto de Medicina Tropical de Sao Paulo 9, 11–17.Google 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
Lightner, L.K. (1976) Temperature stress and the development of schistosomiasis in mice. PhD thesis, Iowa State University, USA.Google Scholar
Lightner, L.K. (1977). Environmental heat stress and the development of Schistosoma mansoni in mice. Iowa State Journal of Research 52, 5–7.Google Scholar
Manga-González, M.Y., González-Lanza, C. & Cabanas, E. (2007) Dicrocoelium dendriticum primoinfection and kinetic egg elimination in marked lambs and ewes from the León Mountains (Spain). Revista Ibérica de Parasitologia 67, 15–25.Google Scholar
Manga-González, M.Y., Quiroz-Romero, H., González-Lanza, C., Minambres, B. & Ochoa, P. (2010) Strategic control of Dicrocoelium dendriticum (Digenea) egg excretion by naturally infected sheep. Veterinarni Medicina 55, 19–29.Google Scholar
McCarthy, A.M. (1989) The biology and transmission dynamics of Echinoparyphium recurvatum (Digenea: Echinostomatidae). PhD thesis, King's College, University of London, UK.Google Scholar
McKindsey, C.W. & McLaughlin, J.D. (1993) The viability of Sphaeridiotrema pseudoglobulus (Digenea) eggs following cold water storage as a possible overwintering strategy. Parasitology 107, 441–447.Google Scholar
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.Google 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.Google Scholar
Morley, N.J. & Lewis, J.W. (2013) Thermodynamics of cercarial development and emergence in trematodes. Parasitology 140, 1211–1224.Google Scholar
Morley, N.J. & 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. & Lewis, J.W. (2015) Thermodynamics of trematode infectivity. Parasitology 142, 585–597.Google Scholar
Nollen, P.M., Samizadeh-Yazd, A. & Snyder, D.E. (1979) The longevity and hatchability of Philophthalmus megalurus and Philophthalmus gralli miracidia in different environmental conditions. Journal of Parasitology 65, 772–776.Google Scholar
Ono, Y. & Isoda, M. (1951) Studies on fascioliasis. 1. Observations on the life history of Fasciola hepatica . Japanese Journal of Veterinary Science 13, 87–93 (in Japanese).Google Scholar
Pacenovsky, J., Krupicer, I. & Legeny, J. (1980a) Studium embryogonie Paramphistomum ichikawai Fukui 1922 (Trematode; Paramphistomata) v laboratornych a prirodzenych podmienkach CSSR. Folia Veterinaria 24, 279–308.Google Scholar
Pacenovsky, J., Krupicer, I. & Legeny, J. (1980b) Studium embryogonie Liochis scotiae Willmott 1950, Velichko 1966 (Trematode; Paramphistomata) v laboratornych a prirodzenych podmienkach CSSR. Folia Veterinaria 24, 329–355.Google Scholar
Pfukenyi, D.M., Mukaratirwa, S., Willingham, A.L. & Monrad, J. (2005) Epidemiological studies of amphistome infections in cattle in the highveld and lowveld communal grazing areas of Zimbabwe. Onderstepoort Journal of Veterinary Research 72, 67–86.Google Scholar
Pfukenyi, D.M., Mukaratirwa, S., Willingham, A.L. & Monrad, J. (2006a) Epidemiological studies of Fasciola gigantica infections in cattle in the highveld and lowveld communal grazing areas of Zimbabwe. Onderstepoort Journal of Veterinary Research 73, 37–51.Google Scholar
Pfukenyi, D.M., Mukaratirwa, S., Willingham, A.L. & Monrad, J. (2006b) Epidemiological studies of Schistosoma mattheei infections in cattle in the highveld and lowveld communal grazing areas of Zimbabwe. Onderstepoort Journal of Veterinary Research 73, 179–191.Google Scholar
Polozowski, A. & Czeszczyszyn, T. (2004) Wplyw różnych czynników fizykochemicznych na embriogenezę I wyląg miracidiów Fasciola hepatica . Acta Scientiarum Polonorum, Medicina Veterinaria 3, 45–51.Google Scholar
Poulin, R. (1997) Egg production in adult trematodes: adaptation or constraint? Parasitology 114, 195–204.Google Scholar
Prosser, C.L. (1973) Comparative animal physiology, Philadelphia, Saunders.Google Scholar
Rowcliffe, S.A. & Ollerenshaw, C.B. (1960) Observations on the bionomics of the egg of Fasciola hepatica . Annals of Tropical Medicine and Parasitology 54, 172–181.CrossRefGoogle ScholarPubMed
Samuelson, J.C., Quinn, J.J. & Caulfield, J.P. (1984) Hatching, chemokinesis, and transformation of miracidia of Schistosoma mansoni . Journal of Parasitology 70, 321–331.CrossRefGoogle ScholarPubMed
Shirai, M. (1925) The supplementary studies on the infection with Fasciola hepatica . Jikken Igaku Zasshi 11, 194–233 (in Japanese).Google Scholar
Smyth, J.D. & Halton, D.W. (1983) The physiology of trematodes. 2nd edn. Cambridge, Cambridge University Press.Google Scholar
Srivastava, H.D. & Dutt, S.C. (1962) Studies on Schistosoma indicum . ICAR Research Series 34, 1–91.Google Scholar
Studer, A. & 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
Sugiura, S., Sasaki, T., Hosaka, Y. & Ono, R. (1954) A study of several factors influencing hatching of Schistosoma japonicum eggs. Journal of Parasitology 40, 381–386.Google Scholar
Thomas, C., Jacquiet, P. & Dorchies, P. (2007) La prevalence des helminthoses bovines a-t-elle été modifiée par la canicule de l’été 2003 dans le sud-ouest de la France? Parasite 14, 265–268.Google Scholar
Toledo, R. (2009) Echinostomes in the definitive host: a model for the study of host–parasite relationships. pp. 89–109 in Fried, B. & Toledo, R. (Eds) The biology of echinostomes: from molecules to the community. New York, Springer.Google Scholar
Vanoverschelde, R. (1981) Studies on the life-cycle of Himasthla militaris (Trematoda: Echinostomatidae): influence of salinity and temperature on egg development and miracidial emergence. Parasitology 82, 459–465.Google Scholar
Vladimirov, V.L. (1961) Morphology and development of eggs of Posthodiplostomum cuticola (Nordmann, 1832) Dubois, 1936 – causative agent of black spot in fish. Doklady Biological Sciences 140, 892–893.Google Scholar
Warren, K.S. (1978) The pathology, pathobiology and pathogenesis of schistosomiasis. Nature 273, 609–612.CrossRefGoogle ScholarPubMed
Watanabe, S. (1965) A revision of genus Fasciola in Japan, with particular reference to F. hepatica and F. gigantica . Progress of Medical Parasitology in Japan 2, 359–381.Google Scholar
Whitfield, P.J. & Evans, N.A. (1983) Parthenogenesis and asexual multiplication among parasitic platyhelminths. Parasitology 86, 121–160.Google Scholar
Williams, E.A. (1980) The morphology and development of larval digeneans from the freshwater snail Lymnaea peregra (Muller). PhD thesis, Royal Holloway, University of London, UK.Google Scholar
Wilson, R.A., Smith, G. & Thomas, M.R. (1982) Facioliasis. pp. 262–361 in Anderson, R.M. (Ed.) The population dynamics of infectious diseases: theory and applications. London, Chapman & Hall.CrossRefGoogle Scholar
Xu, Y.Z. & Dresden, M.H. (1990) The hatching of schistosome eggs. Experimental Parasitology 70, 236–240.CrossRefGoogle ScholarPubMed
Ye, X.-P., Fu, Y.-L., Wu, Z.-X., Anderson, R.M. & Agnew, A. (1997) The effects of temperature, light and water upon the hatching of the ova of Schistosoma japonicum . Southeast Asian Journal of Tropical Medicine and Public Health 28, 575–580.Google Scholar
Supplementary material: File

Morley and Lewis supplementary material S1

Supplementary Table

Download Morley and Lewis supplementary material S1(File)
File 75.8 KB
Supplementary material: File

Morley and Lewis supplementary material S2

Supplementary Table

Download Morley and Lewis supplementary material S2(File)
File 57.9 KB