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Parasite adaptation to extreme conditions in a desert environment

Published online by Cambridge University Press:  16 October 2009

R. C. Tinsley
Affiliation:
School of Biological Sciences, University of Bristol, Bristol BS8 1UG, UK

Summary

Deserts represent universally recognized extreme environments for animal life. This paper documents the highly specialized adaptations of Pseudodiplorchis americanus, a monogenean parasite of the desert toad, Scaphiopus couchii. Building on a long-term record of parasite population ecology (continuing since the early 1980s), field studies focus on the effects of severe drought in the Sonoran Desert, Arizona, in the mid 1990s. This provides a test of the ability of the host-parasite system to tolerate exceptional perturbation. The analysis provides new insight into parasite infection dynamics in a natural wildlife system through integration of host and parasite population age structure. The environmental check interrupted host recruitment in 1993–95 and parasite recruitment in 1995–97. This produced an imprint in age structure and infection levels recognizable over several years: parasite recruitment failure reduced transmission 2–3 years later. The host (maximum life span 17 years) tolerated the disruption but the impact was more serious for the parasite (life span 3 years) leading to extinction of some previously stable populations. Despite this demonstration of a rare event exacerbating external environmental constraints, experimental studies suggest that the internal (host) environment normally creates the most severe conditions affecting P. americanus. Only about 3 % of parasites survive from invasion until first reproduction. Post-invasion factors including host immunity, characteristic of most parasite life cycles, constitute a greater constraint upon survival than external conditions, even in a desert environment.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1999

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References

REFERENCES

Armstrong, E. P., Halton, D. W., Tinsley, R. C., Cable, J., Johnston, R. N., Johnston, C. F. & Shaw, C. (1997). Immunocytochemical evidence for the involvement of an FMRFamide-related peptide in egg production in the flatworm parasite Polystoma nearcticum. Journal of Comparative Neurology 377, 41–8.3.0.CO;2-J>CrossRefGoogle ScholarPubMed
Bush, A. O., Lafferty, K. D., Lotz, J. M. & Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–83.CrossRefGoogle Scholar
Cable, J., Harris, P. D. & Tinsley, R. C. (1998). Life history specializations of monogenean flatworms: a review of experimental and microscopical studies. Microscopy Research and Technique 42, 186–99.3.0.CO;2-R>CrossRefGoogle ScholarPubMed
Cable, J. & Tinsley, R. C. (1991 a). Intra-uterine larval development in the polystomatid monogeneans Pseudodiplorchis americanus and Neodiplorchis scaphiopodis. Parasitology 103, 253–66.CrossRefGoogle ScholarPubMed
Cable, J. & Tinsley, R. C. (1991 b). The ultrastructure of photoreceptors in Pseudodiplorchis americanus and Neodiplorchis scaphiopodis (Monogenea: Polystomatidae). International Journal for Parasitology 21, 8190.CrossRefGoogle Scholar
Cable, J. & Tinsley, R. C. (1992 a). Tegumental ultrastructure of Pseudodiplorchis americanus larvae (Monogenea: Polystomatidae). International Journal for Parasitology 22, 819–29.CrossRefGoogle Scholar
Cable, J. & Tinsley, R. C. (1992 b). Unique ultrastructural adaptations of Pseudodiplorchis americanus (Polystomatidae: Monogenea) to a sequence of hostile conditions following host infection. Parasitology 105, 229–41.CrossRefGoogle Scholar
Cable, J. & Tinsley, R. C. (1992 c). Microsporidean hyperparasites and bacteria associated with Pseudodiplorchis americanus (Monogenea: Polystomatidae). Canadian Journal of Zoology 70, 523–29.CrossRefGoogle Scholar
Cable, J., Tocque, K. & Tinsley, R. C. (1997). Histological analysis of the egg capsule of the ovoviviparous polystomatid monogenean, Pseudodiplorchis americanus. International Journal for Parasitology 27, 1075–80.CrossRefGoogle ScholarPubMed
Dimmitt, M. A. & Ruibal, R. (1980). Environmental correlates of emergence in spadefoot toads ( Scaphiopus). Journal of Herpetology 14, 21–9.CrossRefGoogle Scholar
Gannicott, A. M. & Tinsley, R. C. (1998 a). Larval survival characteristics and behaviour of the gill monogenean Discocotyle sagittata. Parasitology 117, 491–8.CrossRefGoogle ScholarPubMed
Gannicott, A. M. & Tinsley, R. C. (1998 b). Environmental control of transmission of Discocotyle sagittata (Monogenea): egg production and development. Parasitology 117, 499504.CrossRefGoogle Scholar
Harris, P. D. & Tinsley, R. C. (1987). The biology of Gyrdicotylus gallieni (Gyrodactylidea), an unusual viviparous monogenean from the African clawed toad, Xenopus laevis. Journal of Zoology (London) 212, 325–46.CrossRefGoogle Scholar
Jackson, J. A. & Tinsley, R. C. (1994). Infrapopulation dynamics of Gyrdicotylus gallieni (Monogenea: Gyrodactylidae). Parasitology 108, 447–52.CrossRefGoogle ScholarPubMed
Rodgers, L. O. & Kuntz, R. E. (1940). A new polystomatid monogenean fluke from a spadefoot. The Wasmann Collector 4, 3740.Google Scholar
Ruibal, R., Tevis, L. & Roig, v. (1969). The terrestrial ecology of the spadefoot toad Scaphiopus hammondii. Copeia 1969, 571–84.CrossRefGoogle Scholar
Seymour, R. S. (1973). Energy metabolism of dormant spadefoot toads. Copeia 1973, 435–45.CrossRefGoogle Scholar
Tinsley, R. C. (1983). Ovoviviparity in platyhelminth life cycles. Parasitology 86, 161196.CrossRefGoogle ScholarPubMed
Tinsley, R. C. (1989). Effects of host sex on transmission success. Parasitology Today 5, 190–5.CrossRefGoogle ScholarPubMed
Tinsley, R. C. (1990 a). Host behaviour and opportunism in parasite life cycles. In Parasitism and host behaviour, (ed. Barnard, C. J. & Behnke, J. M.), pp. 158–92. London: Taylor & Francis.Google Scholar
Tinsley, R. C. (1990 b). The influence of parasite infection on mating success in Spadefoot toads, Scaphiopus couchii. American Zoologist 30, 313–24.CrossRefGoogle Scholar
Tinsley, R. C. (1993). The population biology of polystomatid monogeneans. Bulletin Français de la Pêche et de la Pisciculture, 328, 120–36.CrossRefGoogle Scholar
Tinsley, R. C. (1995). Parasitic disease in amphibians: control by the regulation of worm burdens. Parasitology 111, S15378.CrossRefGoogle ScholarPubMed
Tinsley, R. C. (1996). Parasites of Xenopus. In The Biology of Xenopus, (ed. Tinsley, R. C. & Kobel, H. R.), pp. 233–61. Oxford: Oxford University Press.Google Scholar
Tinsley, R. C. & Earle, C. M. (1983). Invasion of vertebrate lungs by the polystomatid monogeneans Pseudodiplorchis americanus and Neodiplorchis scaphiopodis. Parasitology 86, 501–17.CrossRefGoogle Scholar
Tinsley, R. C. & Jackson, H. C. (1986). Intestinal migration in the life cycle of Pseudodiplorchis americanus (Monogenea). Parasitology 93, 451–69.CrossRefGoogle Scholar
Tinsley, R. C. & Jackson, H. C. (1988). Pulsed transmission of Pseudodiplorchis americanus (Monogenea) between desert hosts (Scaphiopus couchii). Parasitology 97, 437–52.CrossRefGoogle Scholar
Tinsley, R. C. & Tocque, K. (1995). The population dynamics of a desert anuran, Scaphiopus couchii. Australian Journal of Ecology 20, 376–84.CrossRefGoogle Scholar
Tocque, K. (1990). The reproductive strategy of a monogenean parasite in a desert environment. PhD. thesis. London University.Google Scholar
Tocque, K. (1993). The relationship between parasite burden and host resources in the desert toad (Scaphiopus couchii), under natural environmental conditions. Journal of Animal Ecology 62, 683–93.CrossRefGoogle Scholar
Tocque, K. & Tinsley, R. C. (1991 a). The influence of desert temperature cycles on the reproductive biology of Pseudodiplorchis americanus (Monogenea). Parasitology 103, 111–20.CrossRefGoogle Scholar
Tocque, K. & Tinsley, R. C. (1991 b). Asymmetric reproductive output by the monogenean Pseudodiplorchis americanus. Parasitology 102, 213–30.CrossRefGoogle ScholarPubMed
Tocque, K. & Tinsley, R. C. (1992). Ingestion of host blood by the monogenean Pseudodiplorchis americanus: a quantitative analysis. Parasitology 104, 283–9.CrossRefGoogle Scholar
Tocque, K. & Tinsley, R. C. (1994 a). Survival of Pseudodiplorchis americanus (Monogenea) under controlled environmental conditions. Parasitology 108, 185–94.CrossRefGoogle ScholarPubMed
Tocque, K. & Tinsley, R. C. (1994 b). The relationship between Pseudodiplorchis americanus (Monogenea) density and host resources under controlled environmental conditions. Parasitology 108, 175–83.CrossRefGoogle ScholarPubMed
Tocque, K., Tinsley, R. C. & Lamb, T. (1995). Ecological constraints on feeding and growth of Scaphiopus couchii. Herpetological Journal 5, 257–65.Google Scholar