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The influence of temperature on the development, hatching and survival of Nematodirus battus larvae

Published online by Cambridge University Press:  09 November 2007

J. van DIJK  and
E. R. MORGAN
J. van DIJK*
Affiliation:
School of Biological Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, UK
E. R. MORGAN
Affiliation:
School of Biological Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, UK
*
*Corresponding author: Present address: Liverpool University Climate and Infectious Diseases of Animals Group (LUCINDA), Veterinary Clinical Science, Leahurst, Neston, Cheshire CH64 7TE, UK. Tel: +44 (0) 1517946084. Fax: +44 (0) 1517946028. E-mail: Jan.van-Dijk@liverpool.ac.uk
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Summary

Although Nematodirus battus (Nematoda: Trichostrongyloidea) is an economically important and highly pathogenic parasite of sheep in the temperate regions, very little is known about the population dynamics of its free-living stages and their relationship with ambient temperature. Here we describe the temperature-related vital rates and thresholds of egg development, hatching and larval survival for the first time. N. battus eggs were able to develop between 11·5 and 27°C, but development at the lower end of this range was more successful. Embryonated eggs did not hatch below 11°C or above 17°C. This is the first description of an upper threshold for hatching in trichostrongyloids. In contrast with most previous studies, although some eggs hatched only after being chilled, substantial proportions of eggs were also found to hatch without the need for chilling. These proportions were lower with increasing, within-hatching range, temperatures. Larval death rates significantly increased at temperatures towards and above the upper hatching threshold. The peculiar hatching behaviour of N. battus may therefore be explained in terms of optimization of larval survival. We argue that our findings confirm the likelihood of an arctic origin of the parasite. Probable changes and adaptations of parasite behaviour in the temperate regions, and the driving forces behind them, are discussed, as well as factors affecting persistence and geographical spread against a background of climate change.

Keywords

parasitefree-living stagessheeparcticecologyclimate changeadaptationbet-hedging
Type
Research Article
Information
Parasitology , Volume 135 , Issue 2 , February 2008 , pp. 269 - 283
Copyright
Copyright © Cambridge University Press 2007

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References

REFERENCES

Ames, C. and Turner, B. (2003). Low temperature episodes in development of blowflies: implications for postmortem interval estimation. Medical and Veterinary Entomology 17, 178–186.CrossRefGoogle ScholarPubMed
Arneberg, P., Skorping, A., Grenfell, B. and Read, A. F. (1989). Host densities as determinants of abundance in parasite communities. Proceedings of the Royal Society of London, B 265, 1283–1289.CrossRefGoogle Scholar
Ash, C. P. J. and Atkinson, H. J. (1983). Evidence for a temperature-dependent conversion of lipid reserves to carbohydrate in quiescent eggs of the nematode Nematodirus battus. Comparative Biochemical Physiology 76B, 603–610.Google Scholar
Ash, C. P. J. and Atkinson, H. J. (1986). Nematodirus battus: development of cold hardiness in dormant eggs. Experimental Parasitology 62, 24–28.CrossRefGoogle ScholarPubMed
Barger, I. A. and Le Jambre, L. F. (1988). Regulation of Haemonchus contortus populations in sheep: mortality of established worms. International Journal for Parasitology 18, 269–273.CrossRefGoogle ScholarPubMed
Bauer, C. (1989). Infection with Nematodirus battus (Crofton and Thomas, 1951) and pasture eimeriosis in lambs in Germany. Deutsche Tierarzliche Wochenschrift 96, 382–384.Google Scholar
Besier, R. B. and Dunsmore, J. D. (1993). The ecology of Haemonchus contortus in a winter rainfall region in Australia: the development of eggs into infective larvae. Veterinary Parasitology 45, 275–292.CrossRefGoogle Scholar
Boag, B. and Thomas, R. J. (1975). Epidemiological studies on Nematodirus species in sheep. Research in Veterinary Science 19, 263–268.CrossRefGoogle ScholarPubMed
Borgsteede, F. H. M., Hendriks, J. and van den Burg, W. P. (1978). Nematodirus battus in Nederland. Tijdschrift voor Diergeneeskunde 103, 279–280.Google Scholar
Christie, M. G. (1962). On the hatching of Nematodirus battus, with some remarks on N. filicollis. Parasitology 52, 297–313.CrossRefGoogle Scholar
Christensen, C. M., Barnes, E. H. and Nansen, P. (1997). Experimental Oesophagostomum dentatum infections in the pig: worm populations at regular intervals during trickle infections with three dose levels of larvae. Parasitology 115, 545–552.CrossRefGoogle ScholarPubMed
Croffon, H. D. and Thomas, R. J. (1951). A new species of Nematodirus in sheep. Nature, London 29, 559.CrossRefGoogle Scholar
Dunn, A. M. (1978). Nematodiriasis. In Veterinary Helminthology, 2nd Edn. (ed. Dunn, A. M.), pp. 185–188. William Heineman Medical Books Ltd, London, UK.Google Scholar
Eysker, M. and Kooyman, F. N. J. (1993). Notes on necropsy and herbage processing techniques for gastrointestinal nematodes of ruminants. Veterinary Parasitology 46, 205–213.CrossRefGoogle ScholarPubMed
Fenton, A. and Hudson, P. J. (2002). Optimal infection strategies: should macroparasites hedge their bets? Oikos 96, 92–101.CrossRefGoogle Scholar
Fudalewicz-Niemczyk, W., Nowosad, B. and Skalska, M. (1996). Pierwsze doniesienie o Nematodirus battus – nicieniu pasozytniczym owiec w. Polski Przeglad Zoologiczny 40, 65–68.Google Scholar
Gibson, T. E. (1963). Experiments on the epidemiology of Nematodiriasis. Research in Veterinary Science 4, 258–268.CrossRefGoogle Scholar
Gibson, T. E. and Everett, G. (1963). The development of resistance by sheep to infection with the nematode Nematodirus battus. Bristish Veterinary Journal 119, 214–218.CrossRefGoogle Scholar
Gibson, T. E. and Everett, G. (1976). The ecology of the free-living stages of Haemonchus contortus. British Veterinary Journal 132, 50–59.CrossRefGoogle ScholarPubMed
Gibson, T. E. and Everett, G. (1981). The ecology of the free-living stages of Nematodirus battus. Research in Veterinary Science 31, 323–327.CrossRefGoogle ScholarPubMed
Graham, E. G., Harris, T. J. and Ollerenshaw, C. B. (1984). Some observations on the epidemiology of Nematodirus battus in Anglesey. Agricultural and Forest Meteorology 32, 121–132.CrossRefGoogle Scholar
Grenfell, B. T., Smith, G. and Anderson, R. M. (1987). The regulation of Ostertagia ostertagi populations in calves: the effect of past and current experience of infection on proportional establishment and parasite survival. Parasitology 95, 363–372.CrossRefGoogle ScholarPubMed
Helle, O. (1969). The introduction of Nematodirus battus (Crofton and Thomas 1951) into a new environment. Veterinary Record 84, 157–160.CrossRefGoogle Scholar
Hoberg, E. P. (2005). Coevolution and biogeography among nematodirinae (Nematoda: Trichostrongylina) Lagomorpha and Artiodactyla (Mammalia): Exploring determinants of history and structure for the northern fauna across the Holarctic. Journal of Parasitology 91, 358–369.CrossRefGoogle ScholarPubMed
Hoberg, E. P., Zimmerman, G. L. and Lichtenfels, J. R. (1986). First report of Nematodirus battus (Nematoda: Trichostrongyloidea) in North America: redescription and comparison to other species. Journal of the Helminthological Society of Washington 53, 80–88.Google Scholar
Jansen, J. (1973). Where does Nematodirus battus Crofton and Thomas, 1951, come from? Veterinary Record 92, 697–698.CrossRefGoogle Scholar
Jenkins, E. J., Kutz, S. J., Hoberg, E. P. and Polley, L. (2006 a). Bionomics of larvae of Parelaphostrongylus odocoilei (Nematoda: Protostrongylidae) in experimentally infected gastropod intermediate hosts. Journal of Parasitology 92, 298–305.CrossRefGoogle ScholarPubMed
Jenkins, E. J., Veitch, A. M., Kutz, S. J., Hoberg, E. P. and Polley, L. (2006 b). Climate change and the epidemiology of protostrongylid nematodes in northern ecosystems: Parelaphostrongylus odocoilei and Protostrongylus stilesi in Dall's sheep (Ovis d. dalli). Parasitology 132, 387–401.CrossRefGoogle ScholarPubMed
Kingsbury, P. A. (1953). Nematodirus infestation – A probable cause of losses amongst lambs. Veterinary Record 65, 167–169.Google Scholar
Kutz, S. J., Hoberg, E. P., Nishi, J. and Polley, L. (2002). Development of the muskox lungworm, Umingmakstrongylus pallikuukensis (Protostrongylidae), in gastropods in the Arctic. Canadian Journal of Zoology 80, 1977–1985.CrossRefGoogle Scholar
Kutz, S. J., Hoberg, E. P. and Polley, L. (2001). Umingmakstrongylus pallikuukensis (nematoda: protostrongylidae) in gastropods: larval morphology, morphometrics, and development rates. Journal of Parasitology 87, 527–535.CrossRefGoogle ScholarPubMed
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, 2571–2576.Google ScholarPubMed
Lichtenfels, J. R., Hoberg, E. P. and Zarlenga, D. S. (1997). Systematics of gastrointestinal nematodes of domestic ruminants: adavances between 1992 and 1995 and proposals for future research. Veterinary Parasitology 72, 225–238.CrossRefGoogle Scholar
Lindqvist, A., Ljungstrom, B. L., Nilsson, O. and Waller, P. J. (2001). The dynamics, prevalence and impact of nematode infections in organically raised sheep in Sweden. Acta Veterinaria Scandinavica 42, 337–389.CrossRefGoogle ScholarPubMed
McKellar, Q., Bairden, K., Duncan, J. L. and Armour, J. (1983). Change in N. battus epidemiology. Veterinary Record 112, 309.CrossRefGoogle ScholarPubMed
Meyers, L. A. and Bull, J. J. (2002). Fighting change with change: adaptive variation in an uncertain world. Trends in Ecology and Evolution 17, 551–557.CrossRefGoogle Scholar
Morgan, E. R., Milner-Gulland, E. J., Torgerson, P. R. and Medley, G. F. (2004). Ruminating on complexity: macroparasites of wildlife and livestock. Trends in Ecology and Evolution 19, 181–188.CrossRefGoogle ScholarPubMed
Morrissey, R. E. and Baust, J. G. (1976). The ontogeny of cold tolerance in the gall fly, Eurostata solidagensis. Journal of Insect Physiology 22, 431–437.CrossRefGoogle Scholar
Parkin, J. T. (1972). The ecology of Nematodirus battus with some observations on the hatching process. Ph.D. thesis, University of Newcastle-upon-Tyne.Google Scholar
Patel, M. N., Stolinski, M. and Wright, D. J. (1997). Neutral lipids and the assessment of infectivity in enthomopathogenic nematodes: observations on four Steinernema species. Parasitology 114, 489–496.CrossRefGoogle Scholar
Patel, M. N. and Wright, D. J. (1997). Glycogen: its importance in the infectivity of aged juveniles of Steinernema carpocapsae. Parasitology 114, 591–596.Google ScholarPubMed
Philipi, T. and Seger, J. (1989). Hedging one's evolutionary bets, revisited. Trends in Ecology and Evolution 4, 41–44.CrossRefGoogle Scholar
Rickard, L. G., Hoberg, E. P., Bishop, J. K. and Zimmerman, G. L. (1989). Epizootiology of Nematodirus battus, N. filicollis and N. spathiger (Nematoda: Trichostrongyloidea) in Western Oregon. Proceedings of the Helminthological Society of Washington 56, 104–115.Google Scholar
Rickard, L. G., Hoberg, E. P., Zimmerman, G. L. and Erno, J. K. (1987). Late fall transmission of Nematodirus battus (Nematoda: Trichostrongyloidea) in Western Oregon. Journal of Parasitology 73, 244–247.CrossRefGoogle ScholarPubMed
Rodger, J. L. (1983). Change in N.battus epidemiology. Veterinary Record 112, 261–262.CrossRefGoogle Scholar
Rose, C. H. and Jacobs, D. E. (1990). Epidemiology of sheep nematodes in Sub-Arctic Greenland: sources of infection on rangeland grazing. Acta Veterinaria Scandinavica 31, 339–345.CrossRefGoogle ScholarPubMed
Salih, N. E. and Grainger, J. N. R. (1982). The effect of constant and changing temperatures on the development of the eggs and larvae of Ostertagia circumcincta. Journal of Thermal Biology 7, 35–38.CrossRefGoogle Scholar
Samson, J. and Holmes, J. C. (1985). The effect of temperature on rates of development of larval Protostrongylus spp. (Nematoda: Metastrongyloidea) from bighorn sheep, Ovis canadensis canadensis, in the snail Vallonia pulchella. Canadian Journal of Zoology 63, 1445–1448.CrossRefGoogle Scholar
Sanchez, S. G. and Quiroz Romero, H. (1993). Frequency of gastroenteric lungworms and hepatic parasites in Magdalena Soltepec, Tlaxcala, Mexico. Veterinaria-Mexico 24, 195–198.Google Scholar
Saunders, L. M., Tompkins, D. M. and Hudson, P. J. (2002). Stochasticity accelerates nematode egg development. Journal of Parasitology 88, 1271–1272.CrossRefGoogle ScholarPubMed
Schjetlein, J. and Skorping, A. (1995). The temperature threshold for development of Elaphostrongylus rangiferi in the intermediate host: an adaption to winter survival? Parasitology 111, 103–110.CrossRefGoogle ScholarPubMed
Taylor, D. M. and Thomas, R. J. (1986). The development of immunity to Nematodirus battus in lambs. International Journal for Parasitology 16, 43–46.CrossRefGoogle ScholarPubMed
Thamsborg, S. M., Githigia, S. M., Larsen, M., Nansen, P. and Henriksen, S. A. (1996). Infection with Nematodirus battus, a new lamb parasite for Denmark. Dansk Veterinaertidsskrift 79, 231–232.Google Scholar
Thomas, D.RH. (1991). The epidemiology of Nematodirus battus- is it changing? Parasitology 102, 147–155.CrossRefGoogle ScholarPubMed
Thomas, R. J. (1959). Field studies on the seasonal incidence of Nematodirus battus and N. filicollis in sheep. Parasitology 49, 387–410.CrossRefGoogle Scholar
Thomas, R. J. and Stevens, A. J. (1956). Some observations on Nematodirus disease in Northumberland and Durham. Veterinary Record 68, 471–475.Google Scholar
Thomas, R. J. and Stevens, A. J. (1960). Ecological studies on the development of the pasture stages of Nematodirus battus and N. filicollis, nematode parasites of sheep. Parasitology 50, 31–49.CrossRefGoogle Scholar
Torina, A., Dara, S., Marino, A. M. F., Sparagano, O. A. E., Vitale, F., Reale, S. and Caracappa, S. (2004). Study of gastrointestinal nematodes in sicilian sheep and goats. Annals of the New York Academy of Sciences 1026, 187–194.CrossRefGoogle ScholarPubMed
Troell, K., Mattsson, J. G., Alderborn, A. and Hoglund, J. (2003). Pyrosequencing analysis identifies discrete populations of Haemonchus contortus from small ruminants. International Journal for Parasitology 33, 765–771.CrossRefGoogle ScholarPubMed
Troell, K., Tingstedt, C. and Hoglund, J. (2006). Phenotypic characterisation of Haemonchus contortus: a study of isolates from Sweden and Kenya in experimentally infected sheep. Parasitology 132, 403–409.CrossRefGoogle ScholarPubMed
Troell, K., Waller, P. and Hoglund, J. (2005). The development and overwintering survival of free-living larvae of Haemonchus conctortus in Sweden. Journal of Helminthology 79, 373–379.CrossRefGoogle ScholarPubMed
Wall, R., French, N. and Morgan, K. L. (1992). Effects of temperature on the development and abundance of the sheep blowfly Lucilia sericata (Diptera: Calliphoridae). Bulletin of Entomological Research 82, 125–131.CrossRefGoogle Scholar
Williams, H. and Richardson, A. M. (1984). Growth energies in relation to temperature for larvae of four species of necrophageous flies (Diptera: Calliphoridae). Australian Journal of Ecology 9, 141–152.CrossRefGoogle Scholar
Young, R. R., Anderson, N., Overend, D., Tweedie, R. L., Malafant, K. W. J. and Preston, G. A. N. (1980). The effect of temperature on times to hatching of eggs of the nematode Ostertagia circumcincta. Parasitology 81, 477–491.CrossRefGoogle ScholarPubMed