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Environmental constraints influencing survival of an African parasite in a north temperate habitat: effects of temperature on egg development

Published online by Cambridge University Press:  27 April 2011

R. C. TINSLEY ,
J. E. YORK ,
A. L. E. EVERARD ,
L. C. STOTT ,
S. J. CHAPPLE  and
M. C. TINSLEY
R. C. TINSLEY*
Affiliation:
School of Biological Sciences, University of Bristol, Bristol BS8 1UG, UK
J. E. YORK
Affiliation:
School of Biological Sciences, University of Bristol, Bristol BS8 1UG, UK
A. L. E. EVERARD
Affiliation:
School of Biological Sciences, University of Bristol, Bristol BS8 1UG, UK
L. C. STOTT
Affiliation:
School of Biological Sciences, University of Bristol, Bristol BS8 1UG, UK
S. J. CHAPPLE
Affiliation:
School of Biological Sciences, University of Bristol, Bristol BS8 1UG, UK
M. C. TINSLEY
Affiliation:
School of Biological and Environmental Sciences, University of Stirling, Stirling FK9 4LA, UK
*
*Corresponding author: School of Biological Sciences, University of Bristol, Bristol BS8 1UG, UK. E-mail: [email protected]
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Summary

Factors affecting survival of parasites introduced to new geographical regions include changes in environmental temperature. Protopolystoma xenopodis is a monogenean introduced with the amphibian Xenopus laevis from South Africa to Wales (probably in the 1960s) where low water temperatures impose major constraints on life-cycle processes. Effects were quantified by maintenance of eggs from infections in Wales under controlled conditions at 10, 12, 15, 18, 20 and 25°C. The threshold for egg viability/ development was 15°C. Mean times to hatching were 22 days at 25°C, 32 days at 20°C, extending to 66 days at 15°C. Field temperature records provided calibration of transmission schedules. Although egg production continues year-round, all eggs produced during >8 months/ year die without hatching. Output contributing significantly to transmission is restricted to 10 weeks (May–mid-July). Host infection, beginning after a time lag of 8 weeks for egg development, is also restricted to 10 weeks (July–September). Habitat temperatures (mean 15·5°C in summer 2008) allow only a narrow margin for life-cycle progress: even small temperature increases, predicted with ‘global warming’, enhance infection. This system provides empirical data on the metrics of transmission permitting long-term persistence of isolated parasite populations in limiting environments.

Keywords

alien species introductionsXenopusProtopolystomaMonogeneatemperaturedevelopmentglobal warming
Type
Research Article
Information
Parasitology , Volume 138 , Issue 8 , July 2011 , pp. 1029 - 1038
Copyright
Copyright © Cambridge University Press 2011

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References

REFERENCES

Bakke, T. A., Cable, J. and Harris, P. D. (2007). The biology of gyrodactylid monogeneans: the “Russian-doll killers”. Advances in Parasitology 64, 161–376.Google Scholar
Chubb, J. C. (1977). Seasonal occurrence of helminths in freshwater fishes. Part 1. Monogenea. Advances in Parasitology 15, 133–199.Google Scholar
Dunn, A. M. (2009). Parasites and biological invasions. Advances in Parasitology 68, 161–184.CrossRefGoogle ScholarPubMed
Fouquet, A. and Measey, G. J. (2006). Plotting the course of an African clawed frog invasion in Western France. Animal Biology 56, 95–102.Google Scholar
Jackson, H. C. and Tinsley, R. C. (1988). Environmental influences on egg production by the monogenean Protopolystoma xenopodis. Parasitology 97, 115–128.Google Scholar
Jackson, J. A. (1993). Systematic and ecological studies on the helminth parasites of Xenopus species. Ph.D. thesis. University of London, London, UK.Google Scholar
Jackson, J. A. and Tinsley, R. C. (1998 a). Effects of temperature on oviposition rate in Protopolystoma xenopodis (Monogenea: Polystomatidae). International Journal for Parasitology 28, 309–315.Google Scholar
Jackson, J. A. and Tinsley, R. C. (1998 b). Reproductive interference in concurrent infections of two Protopolystoma species (Monogenea: Polystomatidae). International Journal for Parasitology 28, 1201–1204.Google Scholar
Jackson, J. A. and Tinsley, R. C. (2001). Protopolystoma xenopodis (Polystomatidae: Monogenea) primary and secondary infections in Xenopus laevis. Parasitology 123, 455–463.Google Scholar
Jackson, J. A. and Tinsley, R. C. (2002). Effects of environmental temperature on the susceptibility of Xenopus laevis and X. wittei (Anura) to Protopolystoma xenopodis (Monogenea). Parasitology Research 88, 632–638.Google Scholar
Jackson, J. A. and Tinsley, R. C. (2003). Parasite infectivity to hybridizing host species: a link between hybrid resistance and allopolyploid speciation? International Journal for Parasitology 33, 137–144.Google Scholar
Jackson, J. A. and Tinsley, R. C. (2005). Geographic and within-population structure in variable resistance to parasite species and strains in a vertebrate host. International Journal for Parasitology 35, 29–37.Google Scholar
Jackson, J. A. and Tinsley, R. C. (2007). Evolutionary divergence in polystomatids infecting tetraploid and octoploid Xenopus in East African highlands: biological and molecular evidence. Parasitology 134, 1223–1235.Google Scholar
Jackson, J. A., Tinsley, R. C. and Hinkel, H. (1998). Mutual exclusion of congeneric monogenean species in a space-limited habitat. Parasitology 117, 563–569.CrossRefGoogle Scholar
Jackson, J. A., Tinsley, R. C. and Du Preez, L. H. (2001). Differentiation of two locally sympatric Protopolystoma (Monogenea: Polystomatidae) species by temperature-dependent larval development and survival. International Journal for Parasitology 31, 815–821.CrossRefGoogle ScholarPubMed
Jackson, J. A., Pleass, R. J., Cable, J., Bradley, J. E. and Tinsley, R. C. (2006). Heterogenous interspecific interactions in a host-parasite system. International Journal for Parasitology 36, 1341–1349.CrossRefGoogle Scholar
Kearn, G. C. (1986). The eggs of monogeneans. Advances in Parasitology 25, 175–273.CrossRefGoogle ScholarPubMed
Kennedy, C. R. (1994). The ecology of introductions. In Parasitic Diseases of Fish (ed. Pike, A. W. and Lewis, J. W.), pp. 189–208. Samara Publishing, Tresaith, UK.Google Scholar
Kennedy, C. R. and Fitch, D. J. (1990). Colonization, larval survival and epidemiology of the nematode Anguillicola crassus, parasitic in the eel, Anguilla anguilla, in Britain. Journal of Fish Biology 36, 117–131.Google Scholar
Lillo, F., Marrone, F., Sicilia, A. and Castelli, G. (2005). An invasive population of Xenopus laevis (Daudin, 1802) in Italy. Herpetozoa 18, 63–64.Google Scholar
Lobos, G. and Jaksic, F. M. (2005). The ongoing invasion of African clawed frogs (Xenopus laevis) in Chile: causes of concern. Biodiversity and Conservation 14, 429–439.CrossRefGoogle Scholar
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 épizooties 27, 467–484.Google Scholar
Mas-Coma, S., Bargues, M. D., Valero, M. A. and Fuentes, M. V. (2003). Adaptation capacities of Fasciola hepatica and their relationships with human fascioliasis: from below sea level up to the very high altitude. In Taxonomy, Ecology and Evolution of Metazoan Parasites, Vol. II (ed. Combes, C. and Jourdane, J.), pp. 81–123. Presses Universitaires de Perpignan, Perpignan, France.Google Scholar
Mas-Coma, S., Valero, M. A. and Bargues, M. D. (2009). Fasciola, lymnaeids and human fascioliasis, with a global overview on disease transmission, epidemiology, evolutionary genetics, molecular epidemiology and control. Advances in Parasitology 69, 41–146.Google Scholar
Measey, G. J. and Tinsley, R. C. (1998). Feral Xenopus laevis in South Wales. Herpetological Journal 8, 23–27.Google Scholar
Ollerenshaw, C. B. (1974). Forecasting liver fluke disease. In The Effects of Meteorological Factors upon Parasites (ed. Taylor, A. E. R. and Muller, R.), pp. 33–52. Symposia of the British Society for Parasitology 12. Blackwell Scientific Publications, Oxford, UK.Google Scholar
Robinson, M. W. and Dalton, J. P. (2009). Zoonotic helminth infections with particular emphasis on fasciolosis and other trematodiases. Philosophical Transactions of the Royal Society of London, B 364, 2763–2776.Google Scholar
Taraschewski, H. (2006). Hosts and parasites as aliens. Journal of Helminthology 80, 99–128.CrossRefGoogle ScholarPubMed
Tinsley, R. C. (1996). Parasites of Xenopus. In The Biology of Xenopus (ed. Tinsley, R. C. and Kobel, H. R.), pp. 233–261. Oxford University Press, Oxford, UK.Google Scholar
Tinsley, R. C. (2004). Platyhelminth parasite reproduction: some general principles derived from monogeneans. Canadian Journal of Zoology 82, 270–291.CrossRefGoogle Scholar
Tinsley, R. C. (2005). Parasitism and hostile environments. In Parasitism and Ecosystems (ed. Thomas, F., Renaud, F. and Guégan, J-F.), pp. 85–112. Oxford University Press, Oxford, UK.Google Scholar
Tinsley, R. C. and Jackson, J. A. (1998). Speciation of Protopolystoma Bychowsky, 1957 (Monogenea: Polystomatidae) in hosts of the genus Xenopus (Anura: Pipidae). Systematic Parasitology 40, 93–141.Google Scholar
Tinsley, R. C. and McCoid, M. J. (1996). Feral populations of Xenopus outside Africa. In The Biology of Xenopus (ed. Tinsley, R. C. and Kobel, H. R.), pp. 81–94. Oxford University Press, Oxford, UK.Google Scholar
Tinsley, R. C., York, J. E., Stott, L. C., Everard, A. L. E., Chapple, S. J. and Tinsley, M. C. (2011). Environmental constraints influencing survival of an African parasite in a north temperate habitat: effects of temperature on development within the host. Parasitology 137, this issue.Google Scholar
Torgerson, P. and Claxton, J. (1999). Epidemiology and control. In Fascioliasis (ed. Dalton, J. P.), pp. 113–149. CABI Publishing, Wallingford, UK.Google Scholar
Tubbs, L. A., Poortenaar, C. W., Sewell, M. A. and Diggles, B. K. (2005). Effects of temperature on fecundity in vitro, egg hatching and reproductive development of Benedenia seriolae and Zeuxapta seriolae (Monogenea) parasitic on yellowtail kingfish Seriola lalandi. International Journal for Parasitology 35, 315–327.CrossRefGoogle Scholar
Van Dijk, J. and Morgan, E. R. (2008). The influence of temperature on the development, hatching and survival of Nematodirus battus larvae. Parasitology 135, 269–283.Google Scholar
Webster, B. L., Southgate, V. R. and Tchuem Tchuenté, L. A. (2003). On Schistosoma haematobium, S. intercalatum and occurrences of their natural hybridization in south west Cameroon. In Taxonomy, Ecology and Evolution of Metazoan Parasites, Vol. II (ed. Combes, C. and Jourdane, J.), pp. 319–337. Presses Universitaires de Perpignan, Perpignan, France.Google Scholar
Whittington, I. D., Chisholm, L. A. and Rhode, K. (2000). The larvae of Monogenea (Platyhelminthes). Advances in Parasitology 44, 139–232.Google Scholar