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

Published online by Cambridge University Press:  27 June 2011

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
L. C. STOTT
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
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]

Summary

The monogenean Protopolystoma xenopodis has been established in Wales for >40 years following introduction with Xenopus laevis from South Africa. This provides an experimental system for determining constraints affecting introduced species in novel environments. Parasite development post-infection was followed at 15, 20 and 25°C for 15 weeks and at 10°C for ⩾1 year and correlated with temperatures recorded in Wales. Development was slowed/arrested at ⩽10°C which reflects habitat conditions for >6 months/year. There was wide variation in growth at constant temperature (body size differing by >10 times) potentially attributable in part to genotype-specific host-parasite interactions. Parasite density had no effect on size but host sex did: worms in males were 1·8 times larger than in females. Minimum time to patency was 51 days at 25°C and 73 days at 20°C although some infections were still not patent at both temperatures by 105 days p.i. In Wales, fastest developing infections may mature within one summer (about 12 weeks), possibly accelerated by movements of hosts into warmer surface waters. Otherwise, development slows/stops in October–April, delaying patency to about 1 year p.i., while wide variation in developmental rates may impose delays of 2 years in some primary infections and even longer in secondary infections.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2011

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References

REFERENCES

Barber, I. (2005). Parasites grow larger in faster growing fish hosts. International Journal for Parasitology 35, 137143.Google Scholar
Barré, N. and Uilenberg, G. (2010). Spread of parasites transported with their hosts: case study of two species of cattle tick. Revue scientifique et technique, Office international des épizooties 29, 149160.Google Scholar
Brooks, D. R. and Hoberg, E. P. (2007). How will global climate change affect parasite-host assemblages? Trends in Parasitology 23, 571574.Google Scholar
Carey, C., Cohen, N. and Rollins-Smith, L. (1999). Amphibian declines: an immunological perspective. Developmental and Comparative Immunology 23, 459472.Google Scholar
Drake, J. M. (2003). The paradox of the parasites: implications for biological invasion. Proceedings of the Royal Society of London, B 270, S133S135.Google Scholar
Jackson, J. A. and Tinsley, R. C. (1998). Effects of temperature on oviposition rate in Protopolystoma xenopodis (Monogenea: Polystomatidae). International Journal for Parasitology 28, 309315.Google Scholar
Jackson, J. A. and Tinsley, R. C. (2001). Protopolystoma xenopodis (Polystomatidae: Monogenea) primary and secondary infections in Xenopus laevis. Parasitology 123, 455463.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, 632638.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, 137144.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, 2937.CrossRefGoogle 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, 12231235.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, 13411349.Google 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, 815821.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, 563569.Google Scholar
Karvonen, A., Rintamäki, P., Jokela, J. and Valtonen, E. T. (2010). Increasing water temperature and disease risks in aquatic systems: climate change increases the risk of some, but not all, diseases. International Journal for Parasitology 40, 14831488.Google Scholar
Krasnov, B. R. and Matthee, S. (2010). Spatial variation in gender-based parasitism: host-related, parasite-related and environment-related effects. Parasitology 137, 15271536.Google Scholar
Kutz, S. J., Hoberg, E. P., Polley, L. and Jenkins, E. J. (2005). Global warming is changing the dynamics of Arctic host-parasite systems. Proceedings of the Royal Society of London, B 272, 25712576.Google ScholarPubMed
Le Morvan, C., Troutaud, D. and Deschaux, P. (1998). Differential effects of temperature on specific and nonspecific immune defences in fish. Journal of Experimental Biology 201, 165168.Google 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, 467484.CrossRefGoogle ScholarPubMed
Measey, G. J. and Tinsley, R. C. (1998). Feral Xenopus laevis in South Wales. Herpetological Journal 8, 2327.Google Scholar
Mitchell, J. B. (1973). The effect of temperature on the development of Gorgoderina vitelliloba in Rana temporaria. International Journal for Parasitology 3, 545548.Google Scholar
Moret, Y., Bollache, L., Wattier, R. and Rigaud, T. (2007). Is the host or the parasite the most locally adapted in an amphipod-acanthocephalan relationship? A case study in a biological invasion context. International Journal for Parasitology 37, 637644.CrossRefGoogle ScholarPubMed
Poulin, R. (1996). Helminth growth in vertebrate hosts: does host sex matter? International Journal for Parasitology 26, 13111315.Google Scholar
R Development Core Team (2010). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org.Google Scholar
Tinsley, R. C. (1973). Ultrastructural studies on the form and function of the gastrodermis of Protopolystoma xenopi (Monogenoidea: Polyopisthocotylea). Biological Bulletin 144, 541555.Google Scholar
Tinsley, R. C. (2004). Platyhelminth parasite reproduction: some general principles derived from monogeneans. Canadian Journal of Zoology 82, 270291.Google Scholar
Tinsley, R. C. (2005). Parasitism and hostile environments. In Parasitism and Ecosystems (ed. Thomas, F., Renaud, F. and Guégan, J.-F.), pp. 85112. Oxford University Press, Oxford, UK.Google Scholar
Tinsley, R. C. (2010). Amphibians, with special reference to Xenopus. In The UFAW Handbook on the Care and Management of Laboratory and other Research Animals, 8th Edn (ed. Hubrecht, R. and Kirkwood, J.), pp. 741760. Wiley-Blackwell, 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, 93141.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. 8194. Oxford University Press, Oxford, UK.Google Scholar
Tinsley, R. C. and Owen, R. W. (1975). Studies on the biology of Protopolystoma xenopodis (Monogenoidea): the oncomiracidium and life cycle. Parasitology 71, 445463.Google Scholar
Tinsley, R. C., York, J. E., Everard, A. L. E., Stott, L. C., 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 egg development. Parasitology 138 (this issue).Google Scholar
Viney, M. E., Steer, M. D. and Wilkes, C. P. (2006). The reversibility of constraints on size and fecundity in the parasitic nematode Strongyloides ratti. Parasitology 133, 477483.Google Scholar
Wilkes, C. P., Thompson, F. J., Gardner, M. P., Paterson, S. and Viney, M. E. (2004). The effect of the host immune response on the parasitic nematode Strongyloides ratti. Parasitology 128, 661669.Google Scholar