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Climate change and infectious disease: helminthological challenges to farmed ruminants in temperate regions

Published online by Cambridge University Press:  30 September 2009

J. van Dijk ,
N. D. Sargison ,
F. Kenyon  and
P. J. Skuce
J. van Dijk
Affiliation:
Liverpool University Climate and Infectious Diseases of Animals Group (LUCINDA), School of Veterinary Clinical Studies, Leahurst, Cheshire CH64 7TE, UK
N. D. Sargison
Affiliation:
Parasitology Division, Moredun Research Institute, Pentlands Science Park, Edinburgh EH26 0PZ, UK
F. Kenyon
Affiliation:
Parasitology Division, Moredun Research Institute, Pentlands Science Park, Edinburgh EH26 0PZ, UK
P. J. Skuce*
Affiliation:
Parasitology Division, Moredun Research Institute, Pentlands Science Park, Edinburgh EH26 0PZ, UK
*
†E-mail: [email protected]
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Abstract

In the UK, recent mean temperatures have consistently increased by between 1°C and 4°C compared to the 30-year monthly averages. Furthermore, all available predictive models for the UK indicate that the climate is likely to change further and feature more extreme weather events and a trend towards wetter, milder winters and hotter, drier summers. These changes will alter the prevalence of endemic diseases spatially and/or temporally and impact on animal health and welfare. Most notable among these endemic parasites are the helminths, which have been shown to be very strongly influenced by both the short-term weather and climate through effects on their free-living larval stages on pasture. In this review, we examine recent trends in prevalence and epidemiology of key helminth species and consider whether these could be climate-related. We identify likely effects of temperature and rainfall on the free-living stages and some key parasite traits likely to determine parasite abundance under changed climatic conditions. We find clear evidence that climate change, especially elevated temperature, has already changed the overall abundance, seasonality and spatial spread of endemic helminths in the UK. We explore some confounders and alternative explanations for the observed patterns. Finally, we explore the implications of these findings for policy makers and the livestock industry and make some recommendations for future research priorities.

Keywords

endemic diseaseparasiteecologyadaptationseasonality
Type
Full Paper
Information
animal , Volume 4 , Issue 3 , March 2010 , pp. 377 - 392
Copyright
Copyright © The Animal Consortium 2009

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References

Abrous, M, Rondelaud, D, Dreyfuss, G 1997. Paramphistomum daubneyi: the development of redial generations in the snail Lymnaea truncatula. Parasitology Research 83, 64–69.CrossRefGoogle ScholarPubMed
Abrous, M, Rondelaud, D, Dreyfuss, G 2000. Cercarial production of redial generations in single-miracidium infections of Lymnaea truncatula with Paramphistomum daubneyi of Fasciola hepatica. Journal of Helminthology 74, 1–5.CrossRefGoogle ScholarPubMed
Agyei, AD 1997. Seasonal changes in the level of infective strongylate nematode larvae on pasture in the coastal savanna regions of Ghana. Veterinary Parasitology 70, 175–182.CrossRefGoogle ScholarPubMed
Alcamo, J, Moreno, JM, Nováky, B, Bindi, M, Corobov, R, Devoy, RJN, Giannakopoulos, C, Martin, E, Olesen, JE, Shvidenko, A 2007. Europe. In Climate change 2007: impacts, adaptation and vulnerability. Contribution of working group II to the fourth assessment report of the intergovernmental panel on climate change (ed. ML Parry, OF Canziani, JP Palutikof, PJ van der Linden and CE Hanson), pp. 541–580. Cambridge University Press, Cambridge, UK.Google Scholar
Alizon, S, van Baalen, M 2008. Multiple infections, immune dynamics, and the evolution of virulence. The American Naturalist 172, E150–E168.CrossRefGoogle ScholarPubMed
Altizer, S, Dobson, A, Hosseini, P, Hudson, P, Pascual, M, Rohani, P 2006. Seasonality and the dynamics of infectious diseases. Ecology Letters 9, 467–484.Google Scholar
Andersen, FL, Wang, GT, Levine, ND 1966. Effect of temperature on survival of the free-living stages of Trichostrongylus colubriformis. Journal of Parasitology 52, 713–721.CrossRefGoogle ScholarPubMed
Andersen, FL, Levine, ND 1968. Effect of desiccation on survival of the free-living stages of Trichostrongylus colubriformis. Journal of Parasitology 54, 117–128.CrossRefGoogle ScholarPubMed
Andrews, SJ 1999. The life-cycle of Fasciola hepatica. In “Fasciolosis” (ed. JP Dalton), pp. 1–29. CABI International, Wallingford, UK.Google Scholar
Anonymous 2004. PGE an increasing problem in Scottish sheep – SAC organises a discussion forum. SAC Veterinary Services – Surveillance Report. Veterinary Record 154, 773–775.Google Scholar
Anonymous 2005a. Nematodirosis a major problem in Scottish flocks in June. SAC Veterinary Services – Surveillance Report. Veterinary Record 157, 273–276.CrossRefGoogle Scholar
Anonymous 2005b. Increase in parasitic gastroenteritis in sheep related to this year’s autumn weather. VLA Surveillance Report. Veterinary Record 157, 757–760.CrossRefGoogle Scholar
Anonymous 2006a. Increased incidence of parasitic gastroenteritis and pasteurellosis in lambs. VLA Surveillance Report. Veterinary Record 158, 39–42.CrossRefGoogle Scholar
Anonymous 2006b. Fasciolosis in pigs in Scotland. SAC Veterinary Services – Surveillance Report. Veterinary Record 158, 646–648.Google Scholar
Anonymous 2006c. Severe March weather causes problems for Scottish hill farmers. SAC Veterinary Services – Surveillance Report. Veterinary Record 158, 813–816.CrossRefGoogle Scholar
Anonymous 2007a. Dictyocaulosis frequently diagnosed in Scottish dairy cattle in October. SAC Veterinary Services – Surveillance Report. Veterinary Record 160, 37–40.CrossRefGoogle Scholar
Anonymous 2007b. Acute fasciolosis diagnosed in young Scottish calves. SAC Veterinary Services – Surveillance Report. Veterinary Record 161, 249–252.CrossRefGoogle Scholar
Anonymous 2007c. Vets in a changing world. Editorial. Veterinary Record 161, 637.CrossRefGoogle Scholar
Anonymous 2007d. Fall in the number of outbreaks of systemic pasteurellosis in sheep. SAC Veterinary Services – Surveillance Report. Veterinary Record 161, 837–840.Google Scholar
Anonymous 2007e. Animal diseases and global warming. Veterinary Record 161, 833.Google Scholar
Anonymous 2008. Further cases of Paramphistomum species infection in cattle and reindeer. Veterinary Record 163, 7–10.CrossRefGoogle Scholar
Ash, CPJ, Atkinson, HJ 1986. Nematodirus battus: Development of cold hardiness in dormant eggs. Experimental Parasitology 62, 24–28.CrossRefGoogle ScholarPubMed
Bartley, DJ, Jackson, E, Johnston, K, Coop, RL, Mitchell, GB, Sales, J, Jackson, F 2003. A survey of anthelmintic resistant nematode parasites in Scottish sheep flocks. Veterinary Parasitology 117, 61–71.CrossRefGoogle ScholarPubMed
Behnke, JM, Barnard, CJ, Wakelin, D 1992. Understanding chronic nematode infections: evolutionary considerations, current hypotheses and the way forward. International Journal for Parasitology 22, 861–907.CrossRefGoogle ScholarPubMed
Bennett, R, IJpelaar, J 2005. Updated estimates of the costs associated with thirty four endemic livestock diseases in Great Britain: a note. Journal of Agricultural Economics 56, 135–144.CrossRefGoogle Scholar
Beveridge, I, Pullman, AL, Martins, RR, Barelds, A 1989. Effects of temperature and relative humidity on development and survival of the free-living stages of Trichstrongylus colubriformis, T. rugatus and T. vitrinus. Veterinary Parasitology 33, 143–153.CrossRefGoogle ScholarPubMed
Blouin, MS, Yowell, CA, Courtney, CH, Dame, JB 1995. Host movement and the genetic structure of populations of parasitic nematodes. Genetics 141, 1007–1014.CrossRefGoogle ScholarPubMed
Boag, B, Lello, J, Fenton, A, Tompkins, DM, Hudson, PJ 2001. Patterns of parasite aggregation in the wild European rabbit (Oryctolagus cuniculus). International Journal for Parasitology 31, 1421–1428.CrossRefGoogle ScholarPubMed
Boag, B, Thomas, RJ 1985. The effect of temperature on the survival of infective larvae of nematodes. Journal of Parasitology 71, 383–384.CrossRefGoogle ScholarPubMed
Boes, J, Medley, GF, Eriksen, L, Roepstorff, A, Nansen, P 1998. Distribution of Ascaris suum in experimentally and naturally infected pigs and comparison with Ascaris lumbicoides infections in humans. Parasitology 117, 589–596.Google Scholar
Brennan, GP, Fairweather, I, Trudgett, A, Hoey, E, McCoy, MA, McConville, M, Meaney, M, Robinson, M, McFerran, N, Ryan, L, Lanusse, C, Mottier, L, Alvarez, L, Solana, H, Virkel, G, Brophy, PM 2007. Understanding triclabendazole resistance. Experimental and Molecular Pathology 82, 104–109.CrossRefGoogle ScholarPubMed
Brownlie, J, Peckham, C, Waage, J, Woolhouse, M, Lyall, C, Meagher, L, Tait, J, Baylis, M, Nicoll, A 2006. Foresight. Infectious Diseases: preparing for the future. Future threats. Prepared for the Foresight Project Detection and Identification of Infectious Diseases. Office of Science and Innovation, London.Google Scholar
Brunsdon, RV 1988. The economic impact of nematode infection in sheep: implications for future research and control. In The economic importance of parasites of livestock in New Zealand (ed. ACG Heath), Miscellaneous Publication no. 1, pp. 4–16. New Zealand Society for Parasitology, Palmerston North, New Zealand.Google Scholar
Bryan, RP, Kerr, JD 1989. Factors affecting the survival and migration of the free-living stages of gastrointestinal nematode parasites of cattle in central Queensland. Veterinary Parasitology 30, 315–326.CrossRefGoogle ScholarPubMed
Callinan, APL, Westcott, JM 1986. Vertical distribution of trichostrongylid larvae on herbage and in soil. International Journal for Parasitology 16, 241–244.CrossRefGoogle ScholarPubMed
Chiejina, SN, Fakae, BB 1989. The ecology of infective larvae of bovine gastrointestinal trichostrongylids in dry season contaminated pastures in the Nigerian derived savanna. Journal of Helminthology 63, 127–139.CrossRefGoogle ScholarPubMed
Christie, MG 1962. On the hatching of Nematodirus battus, with some remarks on N. filicollis. Parasitology 52, 297–313.Google Scholar
Claxton, JR, Sutherst, J, Ortiz, P, Clarkson, MJ 1999. The effect of cyclic temperatures on the growth of Fasciola hepatica and Lymnaea viatrix. The Veterinary Journal 157, 166–171.CrossRefGoogle ScholarPubMed
Colebrook, E, Wall, R 2004. Ectoparasites of livestock in Europe and the Mediterranean region. Veterinary Parasitology 120, 251–274.Google Scholar
Connan, RM 1986. Ostertagiosis in young lambs in spring. Veterinary Record 119, 359–360.CrossRefGoogle Scholar
Conwill-Jenkins, D, Phillipson, RF 1971. The kinetics of repeated low-level infections of Nippostrongylus barasiliensis in the laboratory rat. Parasitology 62, 457–465.CrossRefGoogle Scholar
Cornell, SJ, Bjornstad, ON, Cattadori, IM, Boag, B, Hudson, PJ 2008. Seasonality, cohort-dependence and the development of immunity in a natural host-nematode system. Proceedings of the Royal Society of London. Series B. Biological Sciences 275, 511–518.Google Scholar
Coyne, MJ, Smith, G 1992. The development and mortality of the free-living stages of Haemonchus contortus in laboratory culture. International Journal for Parasitology 22, 641–650.CrossRefGoogle ScholarPubMed
Crofton, HD 1948. The ecology of immature phases of trichostrongyle nematodes. Parasitology 39, 17–25.CrossRefGoogle ScholarPubMed
Crofton, HD 1965. Ecology and biological plasticity of sheep nematodes 1. The effect of temperature on the hatching of eggs of some nematode parasites of sheep. Cornell Veterinarian 55, 242–250.Google Scholar
Crofton, HD, Whitlock, JH, Glazer, RA 1965. Ecology and biological plasticity of sheep nematodes 2. Genetic x environmental plasticity in Haemonchus contortus (Rud. 1803). Cornell Veterinarian 55, 251–258.Google Scholar
David, GP 1997. Survey on lungworm in adult cattle. Veterinary Record 141, 343–344.Google ScholarPubMed
Davis, MB, Shaw, RG, Etterson, JR 2005. Evolutionary responses to changing climate. Ecology 86, 1704–1714.Google Scholar
Dobson, RJ, Barnes, EH 1995. Interaction between Ostertagia circumcincta and Haemonchus contortus infections in young lambs. International Journal for Parasitology 25, 495–501.CrossRefGoogle ScholarPubMed
Dobson, RJ, Barnes, EH, Windon, RG 1992. Population dynamics of Trichostrongylus colubriformis and Ostertagia circumcincta in single and concurrent infections. International Journal for Parasitology 22, 997–1004.CrossRefGoogle ScholarPubMed
El-Azazy, OME 1990. Absense of hypobiosis in abomasal nematodes of sheep and goats in Egypt. Veterinary Parasitology 37, 55–60.CrossRefGoogle Scholar
Eriksen, L, Nansen, P, Roepstorff, A, Lind, P, Nilsson, O 1992. Response to repeated inoculations with Ascaris suum eggs in pigs during the fattening period. 1. Studies on worm population kinetics. Parasitology Research 78, 241–246.CrossRefGoogle Scholar
Fakae, BB, Chiejina, SN 1988. Further studies on the development and availability of infective larvae of bovine gastrointestinal trichostrongylids on pasture in eastern Nigeria. Veterinary Parasitology 28, 143–152.CrossRefGoogle ScholarPubMed
Fenton, A, Hudson, PJ 2002. Optimal infection strategies: should macroparasites hedge their bets? Oikos 96, 92–101.CrossRefGoogle Scholar
Fernandez, AS, Fiel, CA, Steffan, PE 1999. Study on inductive factors of hypobiosis of Ostertagia ostertagi in cattle. Veterinary Parasitology 81, 295–307.Google Scholar
Fischlin, A, Midgley, GF, Price, JT, Leemans, R, Gopal, B, Turley, C, Rounsevell, MDA, Dube, OP, Tarazona, J, Velichko, AA 2007. Ecosystems, their properties, goods, and services. In Climate change 2007: impacts, adaptation and vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (ed. ML Parry, OF Canziani, JP Palutikof, PJ van der Linden and CE Hanson), pp. 211–272. Cambridge University Press, Cambridge.Google Scholar
Fletcher, HL, Hoey, EM, Orr, N, Trudgett, A, Fairweather, I, Robinson, MW 2004. The occurrence and significance of triploidy in the liver fluke, Fasciola hepatica. Parasitology 128, 69–72.CrossRefGoogle ScholarPubMed
Foster, AP, Otter, A, O’Sullivan, T, Cranwell, MP, Twomey, DF, Millar, MF, Taylor, MA 2008. Rumen fluke (paramphistomosis) in British cattle. Veterinary Record 162, 528.CrossRefGoogle ScholarPubMed
Gaba, S, Gourbiere, S 2008. To delay once or twice: the effect of hypobiosis and free-living stages on the stability of host–parasite interactions. Journal of the Royal Society Interface 5, 919–928.Google Scholar
Garcia Romero, C, Valcarcel, F, Rojo Vazquez, FA 1997. Influence of climate on pasture infectivity of ovine trichostrongyles in dry pastures. Journal of Veterinary Medicine 44, 437–443.CrossRefGoogle ScholarPubMed
Gasnier, N, Rondelaud, D, Abrous, M, Carreras, F, Boulard, C, Diez-Banos, P, Cabaret, J 2000. Allopatic combination of Fasciola hepatica and Lymnaea truncatula is more efficient than sympatric ones. International Journal for Parasitology 30, 573–578.Google Scholar
Giangaspero, MFA, Bahhady, FA, Orita, G, Gruner, L 1992. Summer-arrested development of abomasal trichostrongylids in Awassi sheep in semi-arid areas of North-West Syria. Parasitology Research 78, 594–597.CrossRefGoogle ScholarPubMed
Gibson, TE, Everett, G 1976. The ecology of the free-living stages of Haemonchus contortus. British Veterinary Journal 132, 50–59.CrossRefGoogle ScholarPubMed
Gordon, HM 1948. The epidemiology of parasitic disease, with special reference to studies with nematode parasites of sheep. Australian Veterinary Journal 24, 17–45.CrossRefGoogle Scholar
Gould, EA, Higgs, S, Buckley, A, Gritsun, TS 2006. Potential arbovirus emergence and implications for the United Kingdom. Emerging Infectious Diseases 12, 549–555.CrossRefGoogle ScholarPubMed
Greer, AW 2008. Trade-offs and benefits: implications of promoting a strong immunity to gastrointestinal nematodes in sheep. Parasite Immunology 30, 123–132.CrossRefGoogle Scholar
Hennessy, KJ, Gregory, JM, Mitchell, JFB 1997. Changes in daily precipitation under enhanced greenhouse conditions. Climate Dynamics 13, 667–680.CrossRefGoogle Scholar
Hoberg, EP 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, EP, Lichtenfels, JR, Gibbons, L 2004. Phylogeny for species of Haemonchus (Nematoda: Trichostrongyloidea): considerations of their evolutionary history and global biogeography among Camelidae and Pecora. Journal of Parasitology 90, 1085–1102.CrossRefGoogle ScholarPubMed
Hoberg, EP, Monsen, KJ, Kutz, S, Blouin, MS 1999. Structure, biodiversity and historical biogeography of nematode faunas in Holarctic ruminants: morphological and molecular diagnoses for Teladorsagia boreoarcticus (Nematoda: Ostertagiinae), a dimorphic cryptic species in muskoxen. Journal of Parasitology 85, 910–934.CrossRefGoogle ScholarPubMed
Hodasi, JKM 1976. The effects of low temperature on Lymnaea truncatula. Zeitschrift für Parasitenkunde 48, 281–286.CrossRefGoogle ScholarPubMed
Hsu, CK, Levine, ND 1977. Degree-day concept in development of infective larvae of Haemonchus contortus and Trichostrongylus colubriformis under constant and cyclic conditions. American Journal of Veterinary Research 138, 1115–1119.Google Scholar
Hudson, PJ, Cattadori, IM, Boag, B, Dobson, AP 2006. Climate disruption and parasite-host dynamics: patterns and processes associated with warming and the frequency of extreme climatic events. Journal of Helminthology 80, 175–182.CrossRefGoogle ScholarPubMed
IPCC 2007. Climate change 2007: impacts, adaptation and vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change, pp. 1–986. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Jackson, F, Coop, RL 2000. The development of anthelmintic resistance in sheep nematodes. Parasitology 120, 95–107.CrossRefGoogle ScholarPubMed
Jackson, F, Jackson, E, Coop, RL, Huntley, J 1992. Interactions between Teladorsagia circumcincta and Trichostrongylus vitrinus infections in young lambs. Research in Veterinary Science 53 3, 363–370.CrossRefGoogle ScholarPubMed
Jacobs, DE, Rose, CH 1990. Studies on Ostertagia spp. from Greenlandic sheep – arrested development and worm length. Acta Veterinaria Scandinavica 31, 333–337.CrossRefGoogle ScholarPubMed
Jarrett, JN 2008. Inter-population variation in shell morphology of the barnacle Chthamalus fissus. Journal of Crustacean Biology 28, 16–20.CrossRefGoogle Scholar
Jehan, M, Gupta, V 1974. The effects of temperature on the survival and development of the free-living stages of twisted wireworm Haemonchus contortus, Rudolphi 1803, of sheep and other ruminants. Zeitschrift für Parasitenkunde 43, 197–208.CrossRefGoogle ScholarPubMed
Jenkins, GJ, Perry, MC, Prior, MJO 2007. The climate of the United Kingdom and recent trends. Met Office Hadley Centre, Exeter, UK.Google Scholar
Kao, RR, Leathwick, DM, Roberts, MG, Sutherland, IA 2000. Nematode parasites of sheep: a survey of epidemiological parameters and their application in a simple model. Parasitology 121, 85–103.CrossRefGoogle ScholarPubMed
Kaplan, RM 2004. Drug resistance in nematodes of veterinary importance: a status report. Trends in Parasitology 20, 477–481.CrossRefGoogle ScholarPubMed
Kendall, SB 1949. Bionomics of Lymnaea truncatula and the parthenitae of Fasciola hepatica under drought conditions. Journal of Helminthology 23, 57–68.CrossRefGoogle Scholar
Kendall, SB, McCullough, FS 1951. The emergence of cercariae of Fasciola hepatica from the snail Lymnaea truncatula. Journal of Helminthology 25, 77–92.CrossRefGoogle Scholar
Keymer, A 1982. Density-dependant mechanisms in regulation of intestinal helminth populations. Parasitology 84, 573–587.Google Scholar
Khasnis, AA, Nettleman, MD 2005. Global warming and infectious disease. Archives of Medical Research 36, 689–696.CrossRefGoogle ScholarPubMed
Krecek, RC, Murrell, KD, Douglass, LW 1990. Effects of microclimatic variables on the availability and movement of third-stage larvae of Ostertagia ostertagi on herbage. Onderstepoort Journal of Veterinary Research 57, 133–135.Google ScholarPubMed
Kutz, SJ, Hoberg, EP, Polley, L, Jenkins, EJ 2005. Global warming is changing the dynamics of Arctic host-parasite systems. Proceedings of the Royal Society of London. Series B. Biological Sciences 272, 2571–2576.Google Scholar
Langrova, I, Janskova, I 2004. Arrested development of Trichostrongylus colubriformis in experimentally infected rabbits. Effect of decreasing photoperiod, low temperature and desiccation. Helminthologia 41, 85–90.Google Scholar
Langrova, I, Janskovska, I, Borovsky, M, Fiala, T 2003. Effect of climatic influences on the migrations of infective larvae of cyathostominae. Veterinarni Medicina 48, 18–24.CrossRefGoogle Scholar
Lello, J, Boag, B, Fenton, A, Stevenson, IR, Hudson, PJ 2004. Competition and mutualism among the gut helminths of a mammalian host. Nature 428, 840–844.CrossRefGoogle ScholarPubMed
Levine, ND, Todd, KS 1975. Micrometeorological factors involved in development and survival of free-living stages of the sheep nematodes Haemonchus contortus and Trichostrongylus colubriformis. A review. International Journal of Biometeorology 19, 174–183.CrossRefGoogle ScholarPubMed
Louie, K, Vlassoff, A, Mackay, AD 2007. Gastrointestinal nematode parasites of sheep: a dynamic model for their effect on live weight gain. International Journal for Parasitology 37, 233–241.CrossRefGoogle Scholar
Lutzelschwab, CM, Fiel, CA, Pedonesse, SI, Najle, R, Rodriquez, E, Steffan, PE, Saumell, C, Fuse, L, Iglesias, L 2005. Arrested development of Ostertagia ostertagi: effect of the exposure of infective larvae to natural spring conditions of the humid pampa (Argentinia). Veterinary Parasitology 127, 253–262.CrossRefGoogle Scholar
Luzon-Pena, M, Rojo-Vazquez, FA, Gomez-Bautista, M 1994. The overwintering of eggs, intramolluscal stages and metacercariae of Fasciola hepatica under the temperatures of a Mediterranean area (Madrid, Spain). Veterinary Parasitology 55, 143–148.CrossRefGoogle ScholarPubMed
Mangal, TD, Paterson, S, Fenton, A 2008. Predicting the impact of long-term temperature changes on the epidemiology and control of schistosomiasis: a mechanistic model. PLoS ONE 3 1, e1438. doi:10.1371/journal.pone.0001438.CrossRefGoogle ScholarPubMed
Mapes, CJ, Coop, RL 1973. The effect of various periods of infection with the nematode Haemonchus contortus on the development of the nematode Nematodirus battus. Parasitology 66, 85–94.Google Scholar
Martin, PJ, Le Jambre, LF, Claxton, JH 1981. The impact of refugia on the development of thiabendazole resistance in Haemonchus contortus. International Journal for Parasitology 11, 35–41.Google Scholar
Medley, GF 2002. The epidemiological consequences of optimisation of the individual host immune response. Parasitology 125, S61–S70.CrossRefGoogle ScholarPubMed
Menzel, A, Fabian, P 1999. Growing season extended in Europe. Nature 397, 659.CrossRefGoogle Scholar
Meyers, LA, Bull, JJ 2002. Fighting change with change: adaptive variation in an uncertain world. Trends in Ecology and Evolution 17, 551–557.CrossRefGoogle Scholar
Michel, JF 1974. Arrested development of nematodes and some related phenomena. Advances in Parasitology 12, 279–366.CrossRefGoogle ScholarPubMed
Michel, JF, Lancaster, MB, Hong, C 1976. The resumed development of Ostertagia ostertagi in experimentally infected calves. Journal of Comparative Pathology 86, 615–619.CrossRefGoogle ScholarPubMed
Mitchell, GB, Maris, L, Bonniwell, MA 1998. Triclabendazole-resistant liver fluke in Scottish sheep. Veterinary Record 143, 399.Google ScholarPubMed
Morgan, ER, Medley, GF, Torgerson, PR, Shaikenov, BS, Milner-Gulland, EJ 2007. Parasite transmission in a migratory multiple host system. Ecological Modelling 200, 511–520.CrossRefGoogle Scholar
Morgan, ER, Milner-Gulland, EJ, Torgerson, PR, Medley, GF 2004. Ruminating on complexity: macroparasites of wildlife and livestock. Trends in Ecology and Evololution 19, 181–188.CrossRefGoogle ScholarPubMed
Morgan, ER, Wall, R 2009. Climate change and parasitic disease: farmer mitigation? Trends in Parasitology 25, 308–313.CrossRefGoogle ScholarPubMed
Murphy, TM, Power, EP, Sanchez-Miguel, C, Casey, MJ, Toolan, DP, Fagan, JG 2008. Paramphistomosis in Irish cattle. Veterinary Record 162, 831.CrossRefGoogle ScholarPubMed
Ndamukong, KJN, Ngone, MM 1996. Development and survival of Haemonchus contortus and Trichostrongylus spp. on pasture in Cameroon. Tropical Animal Health and Production 28, 193–197.Google Scholar
Nieuwhof, GJ, Bishop, SC 2005. Costs of the major endemic diseases in Great Britain and the potential benefits of reduction in disease impact. Animal Science 81, 23–29.CrossRefGoogle Scholar
Niven, P, Anderson, N, Vizard, AL 2002. Trichostrongylid infections in sheep after rainfall during summer in southern Australia. Australian Veterinary Journal 80, 567–570.CrossRefGoogle ScholarPubMed
O’Connor, LJ, Walkden-Brown, SW, Kahn, LP 2006. Ecology of the free-living stages of major trichostrongylid parasites of sheep. Veterinary Parasitology 142, 1–15.Google Scholar
Ollerenshaw, CB 1959. The ecology of the liver fluke (Fasciola hepatica). Veterinary Record 71, 957–965.Google Scholar
Ollerenshaw, CB, Rowlands, WT 1959. A method of forecasting the incidence of fascioliasis in Anglesey. Veterinary Record 71, 591–598.Google Scholar
Onyali, IO, Onwurili, COE, Ajayi, JA 1990. Development and survival of Haemonchus contortus larvae on pasture at Vom, Plateau State, Nigeria. Veterinary Research Communications 14, 211–216.Google Scholar
Pandey, VS, Chaer, A, Dakkak, A 1989. Effect of temperature on development of the free-living stages of Ostertagia circumcincta. Veterinary Parasitology 32, 193–197.Google Scholar
Pandey, VS, Chaer, A, Dakkak, A 1993. Effect of temperature and relative humidity on survival of eggs and infective larvae of Ostertagia circumcincta. Veterinary Parasitology 49, 219–227.CrossRefGoogle ScholarPubMed
Papadopoulos, E, Himonas, C, Coles, GC 2001. Drought and flock isolation may enhance the development of anthelmintic resistance in nematodes. Veterinary Parasitology 97, 253–259.CrossRefGoogle ScholarPubMed
Parkin, JT 1975. The effect of moisture stress upon the hatching of Nematodirus battus larvae. Parasitology 70, 149–155.CrossRefGoogle ScholarPubMed
Parkin, JT 1976. The effect of moisture supply upon the development and hatching of the eggs of Nematodirus battus. Parasitology 73, 343–354.CrossRefGoogle ScholarPubMed
Paterson, S, Viney, ME 2002. Host immune responses are necessary for density dependence in nematode infections. Parasitology 125, 283–292.CrossRefGoogle ScholarPubMed
Philip, DJ 1983. Effects of environment on survival of free-living stages of Haemonchus contortus and Ostertagia circumcincta. PhD, Washington State University, WA, USA.Google Scholar
Poulin, R 2006. Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parasitology 132, 143–151.CrossRefGoogle ScholarPubMed
Poulin, R 2007. Evolutionary ecology of parasites, 2nd edition. Princeton University Press, Princeton and Oxford.CrossRefGoogle Scholar
Pritchard, GC, Forbes, AB, Williams, DJL, Salimi-Bejestani, MR, Daniel, RG 2005. Emergence of fasciolosis in cattle in East Anglia. Veterinary Record 157, 578–582.CrossRefGoogle ScholarPubMed
Purse, BV, Mellor, PS, Rogers, DJ, Samuel, AR, Mertens, PC, Baylis, M 2005. Climate change and the recent emergence of bluetongue in Europe. Nature Reviews Microbiology 3, 171–181.CrossRefGoogle ScholarPubMed
Randolph, SE 2004. Evidence that climate change has caused ‘emergence’ of tick-borne diseases in Europe. International Journal of Medical Microbiology 293, 5–15.Google ScholarPubMed
Rees, G 1950. Observations on the vertical migration of the third-stage larva of Haemonchus contortus (Rud.) on experimental plots of Lilium perenne S24, in relation to meteorological and micrometeorological factors. Parasitology 40, 127–143.Google Scholar
Robinson, SE, Christley, RM 2006. Identifying temporal variation in reported births, deaths and movements of cattle in Britain. BMC Veterinary Research 2, 11.CrossRefGoogle ScholarPubMed
Rondelaud, D, Abrous, M, Dreyfuss, G 2002. The influence of different food sources on cercarial production in Lymnaea truncatula experimentally infected with Digenea. Veterinary Research 33, 95–100.CrossRefGoogle ScholarPubMed
Rose, JH 1963. Observations on the free-living stages of the stomach worm Haemonchus contortus. Parasitology 53, 469–481.Google Scholar
Rose, JH, Small, AJ 1984. Observations on the bionomics of the free-living stages of Trichostrongylus vitrinus. Journal of Helminthology 58, 49–58.Google Scholar
Rosenzweig, C, Casassa, G, Karoly, DJ, Imeson, A, Liu, C, Menzel, A, Rawlins, S, Root, TL, Seguin, B, Tryjanowski, P 2007. Assessment of observed changes and responses in natural and managed systems. In Climate change 2007: impacts, adaptation and vulnerability. Contribution of working group II to the fourth assessment report of the intergovernmental panel on climate change (ed. ML Parry, OF Canziani, JP Palutikof, PJ van der Linden and CE Hanson), pp. 79–131. Cambridge University Press, Cambridge, UK.Google Scholar
Ross, JG 1970. The Stormont ‘Wet Day’ forecasting system for fascioliasis. British Veterinary Journal 126, 401–408.CrossRefGoogle ScholarPubMed
Rossanigo, CE, Gruner, L 1995. Moisture and temperature requirements in faeces for the development of free-living stages of gastrointestinal nematodes of sheep, cattle and deer. Journal of Helminthology 69, 357–362.CrossRefGoogle ScholarPubMed
Rothwell, TLW 1989. Immune expulsion of parasitic nematodes from the alimentary tract. International Journal for Parasitology 19, 139–168.CrossRefGoogle ScholarPubMed
Rowcliffe, SA, Ollerenshaw, CB 1960. Observations on the bionomics of the egg of Fasciola hepatica. Annals of Tropical Medicine and Parasitology 54, 172–181.CrossRefGoogle ScholarPubMed
Sargison, ND, Jackson, F, Bartley, DJ, Moir, A 2005. Failure of moxidectin to control benzimidazole-, levamisole- and ivermectin-resistant Teladorsagia circumcincta in a sheep flock. Veterinary Record 156, 105–109.Google Scholar
Sargison, ND, Scott, PR, Jackson, F 2002. Telodorsagiosis in young lambs and extended postparturient susceptibility in moxidectin-treated ewes grazing heavily contaminated pastures. Veterinary Record 151, 353–355.CrossRefGoogle ScholarPubMed
Sargison, ND, Wilson, DJ, Bartley, DJ, Penny, CD, Jackson, F 2007. Haemonchosis and teladorsagiosis in a Scottish sheep flock putatively associated with the overwintering of hypobiotic fourth stage larvae. Veterinary Parasitology 147, 326–331.Google Scholar
Silangwa, SM, Todd, AC 1964. Vertical migration of trichostrongylid larvae on grasses. Journal of Parasitology 50, 278–285.CrossRefGoogle ScholarPubMed
Sissay, MM, Asefa, A, Uggla, A, Waller, PJ 2006. Anthelmintic resistance of nematode parasites of small ruminants in eastern Ethiopia: Exploitation of refugia to restore anthelmintic efficacy. Veterinary Parasitology 135, 337–346.CrossRefGoogle ScholarPubMed
Sissay, MM, Uggla, A, Waller, PJ 2007. Epidemiology and seasonal dynamics of gastrointestinal nematode infections of sheep in a semi-arid region of eastern Ethiopia. Veterinary Parasitology 143, 311–321.CrossRefGoogle Scholar
Skelly, DK, Joseph, LN, Possingham, HP, Feidenburg, LK, Farrugia, TJ, Kinnison, MT, Hendry, AP 2007. Evolutionary responses to climate change. Conservation biology 21, 1353–1355.CrossRefGoogle ScholarPubMed
Skinner, WD, Todd, KS 1980. Lateral migration of Haemonchus contortus larvae on pasture. American Journal of Veterinary Research 41, 395–398.Google Scholar
Skuce, PJ, Sargison, ND, Kenyon, F, Jackson, F, Mitchell, GB 2008. New challenges for the control of helminth parasites of Scottish livestock in the face of climate change. In Proceedings of ‘Livestock and Global Climate Change’ Conference, 17–20 May 2008, Hammamet, Tunisia, p. 97.Google Scholar
Smith, G, Wilson, RA 1980. Seasonal variations in the microclimate of Lymnaea truncatula habitats. Journal of Applied Ecology 17, 329–342.CrossRefGoogle Scholar
Stearns, SC 1992. The evolution of life histories. Oxford University Press, Oxford.Google Scholar
Steel, JW, Jones, WO, Symons, LEA 1982. Effect of a concurrent infection of Trichostrongylus colubriformis on the productivity and physiological and metabolic responses of lambs infected with Ostertagia circumcincta. Australian Journal of Agricultural Research 33, 131–140.CrossRefGoogle Scholar
Stromberg, BE 1997. Environmental factors influencing transmission. Veterinary Parasitology 72, 247–264.CrossRefGoogle ScholarPubMed
Sykes, AR, Poppi, DP, Elliot, DC 1988. Effect of concurrent infection with Ostertagia circumcincta and Trichostrongylus colubriformis on the performance of growing lambs consuming fresh herbage. Journal of Agricultural Science 110, 531–541.CrossRefGoogle Scholar
Tapiador, FJ, Sanchez, E, Gaertner, MA 2007. Regional changes in precipitation in Europe under an increased greenhouse emission scenario. Geophysical Research Letters 34, L06701.CrossRefGoogle Scholar
Thieltges, DW, Jensen, KT, Poulin, R 2008. The role of biotic factors in transmission of free-living endohelminth stages. Parasitology 135, 407–426.Google Scholar
Todd, KS, Levine, ND, Boatman, PA 1976. Effect of temperature on survival of free-living stages of Haemonchus contortus. American Journal of Veterinary Research 37, 991–992.Google ScholarPubMed
Troell, K, Waller, P, 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
Vallat, B 2008. Preface to ‘Climate change: impact on the epidemiology and control of animal diseases’. Revue Scientifique et Technique de l’Office International des Epizooties (OIE) 27, 297–298.CrossRefGoogle ScholarPubMed
van Dijk, J 2004. The epidemiology and control of dictyocaulosis in cattle. Cattle Practice 12, 133–145.Google Scholar
van Dijk, J, Morgan, ER 2006. Haemonchosis on organic farms. Veterinary Record 159, 642.Google Scholar
van Dijk, J 2008. Climate change and the epidemiology of gastrointestinal nematodes of sheep. PhD, University of Bristol.Google Scholar
van Dijk, J, Morgan, ER 2008. The effect of temperature on the development, hatching and survival of Nematodirus battus larvae. Parasitology 135, 269–283.CrossRefGoogle Scholar
van Dijk, J, David, GP, Baird, G, Morgan, ER 2008. Back to the future: developing hypotheses on the effects of climate change on ovine parasitic gastroenteritis from historical data. Veterinary Parasitology 158, 73–84.Google Scholar
van Dijk, J, Morgan, ER 2009. Hatching behaviour of Nematodirus filicollis in a flock co-infected with Nematodirus battus. Parasitology 136, 805–811.CrossRefGoogle Scholar
van Dijk, J, De Louw, MDE, Kalis, LPA, Morgan, ER 2009. Ultraviolet light increases mortality of nematode larvae and can explain patterns of larval availability at pasture. International Journal for Parasitology 39, 1151–1156.CrossRefGoogle ScholarPubMed
Visser, ME 2008. Keeping up in a warming world; assessing the rate of adaptation to climate change. Proceedings of the Royal Society of London. Series B. Biological Sciences 275, 649–659.Google Scholar
Walker, SM, Hoey, E, Fletcher, H, Brennan, G, Fairweather, I, Trudgett, A 2006. Stage-specific differences in fecundity over the life-cycle of two characterized isolates of the liver fluke, Fasciola hepatica. Parasitology 133, 209–216.CrossRefGoogle ScholarPubMed
Waller, PJ 1986. Anthelmintic resistance in Australia. Parasitology Today 2, S16–S18.CrossRefGoogle ScholarPubMed
Wang, GT 1967. Effect of temperature and culture methods on development of the free-living stages of Trichostrongylus colubriformis. American Journal of Veterinary Research 28, 1085–1090.Google ScholarPubMed
Ward, CJ 2006. Mathematical models to assess strategies for the control of gastrointestinal roundworms in cattle. 1. Construction. Veterinary Parasitology 138, 247–267.Google Scholar
Waruiru, RM, Thamsborg, SM, Nansen, P, Kyvsgaard, NC, Bogh, HO, Munyua, WK, Gathuma, JM 2001. The epidemiology of gastrointestinal nematodes of dairy cattle in central Kenya. Tropical Animal Health and Production 33, 173–187.CrossRefGoogle ScholarPubMed
Wharton, DA 1981. The effect of temperature on the behaviour of the infective larvae of Trichostrongylus colubriformis. Parasitology 82, 269–279.CrossRefGoogle ScholarPubMed
Williams, JC, Bilkovich, FR 1973. Distribution of Ostertagia ostertagi infective larvae on pasture herbage. American Journal of Veterinary Research 34, 1337–1344.Google ScholarPubMed
Wittmann, EJ, Baylis, M 2000. Climate change: effects on Culicoides-transmitted viruses and implications for the UK. Veterinary Journal 160, 107–117.CrossRefGoogle ScholarPubMed
Wolstenholme, AJ, Fairweather, I, Prichard, RK, von Samson-Himmelstjerna, G, Sangster, NC 2004. Drug resistance in veterinary helminths. Trends in Parasitology 20, 469–476.Google Scholar
Woolley, H 1997. The economic impact of ‘Husk’ in dairy cattle. Cattle Practice 5, 315–318.Google Scholar
Yamada, Y, Oshima, Y 2003. Distribution and movement of Caenorhabditis elegans on a thermal gradient. Journal of Experimental Biology 206, 2581–2593.Google Scholar
Yoder, HR, Coggins, JR 1998. Larval trematode assemblages in the snail Lymnaea stagnalis from south-eastern Wisconsin. Journal of Parasitology 84, 259–268.CrossRefGoogle Scholar