Climate‐driven changes to the spatio‐temporal distribution of the parasitic nematode, Haemonchus contortus, in sheep in Europe

Rose, Hannah; Caminade, Cyril; Bolajoko, Muhammad Bashir; Phelan, Paul; van Dijk, Jan; Baylis, Matthew; Williams, Diana; Morgan, Eric R.

doi:10.1111/gcb.13132

Climate‐driven changes to the spatio‐temporal distribution of the parasitic nematode, Haemonchus contortus, in sheep in Europe

Journal Article · Wed Jan 06 00:00:00 EST 2016 · Global Change Biology

DOI:https://doi.org/10.1111/gcb.13132· OSTI ID:1400729

Rose, Hannah ^[1]; Caminade, Cyril ^[2]; Bolajoko, Muhammad Bashir ^[3]; Phelan, Paul ^[4]; van Dijk, Jan ^[5]; Baylis, Matthew ^[6]; Williams, Diana ^[7]; Morgan, Eric R. ^[8]

School of Biological Sciences Life Sciences Building University of Bristol Tyndall Avenue Bristol BS8 1TQ UK, School of Veterinary Sciences University of Bristol Langford House Langford Bristol BS40 5DU UK, Cabot Institute University of Bristol Cantocks Close Bristol BS8 1TS UK
School of Environmental Sciences University of Liverpool Liverpool UK, Department of Epidemiology and Population Health The Farr Institute @HeRC University of Liverpool Liverpool L69 3GL UK
School of Biological Sciences Life Sciences Building University of Bristol Tyndall Avenue Bristol BS8 1TQ UK, National Veterinary Research Institute P.M.B. 01, Vom Plateau State Nigeria
Animal &, Grassland Research and Innovation Centre Teagasc Grange, Dunsanny Co. Meath Ireland
Department of Epidemiology and Population Health Institute of Infection and Global Health University of Liverpool, Leahurst Neston Cheshire CH64 7TE UK
School of Environmental Sciences University of Liverpool Liverpool UK, Health Protection Research Unit in Emerging and Zoonotic Infections University of Liverpool Neston UK
Department of Infection Biology Institute of Infection and Global Health University of Liverpool Liverpool L3 5RF UK
School of Veterinary Sciences University of Bristol Langford House Langford Bristol BS40 5DU UK, Cabot Institute University of Bristol Cantocks Close Bristol BS8 1TS UK

Abstract

Recent climate change has resulted in changes to the phenology and distribution of invertebrates worldwide. Where invertebrates are associated with disease, climate variability and changes in climate may also affect the spatio‐temporal dynamics of disease. Due to its significant impact on sheep production and welfare, the recent increase in diagnoses of ovine haemonchosis caused by the nematode Haemonchus contortus in some temperate regions is particularly concerning. This study is the first to evaluate the impact of climate change on H. contortus at a continental scale. A model of the basic reproductive quotient of macroparasites, Q ₀ , adapted to H. contortus and extended to incorporate environmental stochasticity and parasite behaviour, was used to simulate Pan‐European spatio‐temporal changes in H. contortus infection pressure under scenarios of climate change. Baseline Q ₀ simulations, using historic climate observations, reflected the current distribution of H. contortus in Europe. In northern Europe, the distribution of H. contortus is currently limited by temperatures falling below the development threshold during the winter months and within‐host arrested development is necessary for population persistence over winter. In southern Europe, H. contortus infection pressure is limited during the summer months by increased temperature and decreased moisture. Compared with this baseline, Q ₀ simulations driven by a climate model ensemble predicted an increase in H. contortus infection pressure by the 2080s. In northern Europe, a temporal range expansion was predicted as the mean period of transmission increased by 2–3 months. A bimodal seasonal pattern of infection pressure, similar to that currently observed in southern Europe, emerges in northern Europe due to increasing summer temperatures and decreasing moisture. The predicted patterns of change could alter the epidemiology of H. contortus in Europe, affect the future sustainability of contemporary control strategies, and potentially drive local adaptation to climate change in parasite populations.

View Accepted Manuscript (Publisher)

Sponsoring Organization:: USDOE

OSTI ID:: 1400729

Journal Information:: Global Change Biology, Journal Name: Global Change Biology Journal Issue: 3 Vol. 22; ISSN 1354-1013

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (52)

Threshold quantities for helminth infections Heesterbeek, J. A. P.; Roberts, M. G. Journal of Mathematical Biology, Vol. 33, Issue 4 https://doi.org/10.1007/BF00176380	journal	February 1995
Regulation of Haemonchus contortus populations in sheep exposed to continuous infection Barger, I. A.; Le Jambre, L. F.; Georgi, J. R. International Journal for Parasitology, Vol. 15, Issue 5 https://doi.org/10.1016/0020-7519(85)90049-9	journal	October 1985
Vertical distribution of trichostrongylid larvae on herbage and in soil Callinan, A. P. L.; Westcott, J. M. International Journal for Parasitology, Vol. 16, Issue 3 https://doi.org/10.1016/0020-7519(86)90050-0	journal	June 1986
Regulation of Haemonchus contortus populations in sheep: Mortality of established worms Barger, I. A.; Le Jambre, L. F. International Journal for Parasitology, Vol. 18, Issue 2 https://doi.org/10.1016/0020-7519(88)90067-7	journal	March 1988
The development and mortality of the free-living stages of Haemonchus contortus in laboratory culture Coyne, Michael J.; Smith, Gary International Journal for Parasitology, Vol. 22, Issue 5 https://doi.org/10.1016/0020-7519(92)90013-B	journal	August 1992
A model for nematodiasis in New Zealand lambs Leathwick, D. M.; Barlow, N. D.; Vlassoff, A. International Journal for Parasitology, Vol. 22, Issue 6 https://doi.org/10.1016/0020-7519(92)90129-9	journal	September 1992
The mortality and fecundity of Haemonchus contortus in parasite-naive and parasite-exposed sheep following single experimental infections Coyne, Michael J.; Smith, Gary International Journal for Parasitology, Vol. 22, Issue 3 https://doi.org/10.1016/S0020-7519(05)80009-8	journal	May 1992
Hypobiosis of Haemonchus contortus in natural infections of sheep and goats in a semi-arid area of Kenya Gatongi, P. M.; Prichard, R. K.; Ranjan, S. Veterinary Parasitology, Vol. 77, Issue 1 https://doi.org/10.1016/S0304-4017(97)00207-0	journal	May 1998
GLOWORM-FL: A simulation model of the effects of climate and climate change on the free-living stages of gastro-intestinal nematode parasites of ruminants Rose, Hannah; Wang, Tong; van Dijk, Jan Ecological Modelling, Vol. 297 https://doi.org/10.1016/j.ecolmodel.2014.11.033	journal	February 2015
Understanding social resilience to climate variability in primary enterprises and industries Marshall, N. A. Global Environmental Change, Vol. 20, Issue 1 https://doi.org/10.1016/j.gloenvcha.2009.10.003	journal	February 2010
Modelling the impact of climate change on spatial patterns of disease risk: Sheep blowfly strike by Lucilia sericata in Great Britain Rose, Hannah; Wall, Richard International Journal for Parasitology, Vol. 41, Issue 7 https://doi.org/10.1016/j.ijpara.2011.01.012	journal	June 2011
Climate change and parasitic disease: farmer mitigation? Morgan, Eric R.; Wall, Richard Trends in Parasitology, Vol. 25, Issue 7 https://doi.org/10.1016/j.pt.2009.03.012	journal	July 2009
Frontiers in climate change–disease research Rohr, Jason R.; Dobson, Andrew P.; Johnson, Pieter T. J. Trends in Ecology & Evolution, Vol. 26, Issue 6 https://doi.org/10.1016/j.tree.2011.03.002	journal	June 2011
The epidemiology of abomasal nematodes of sheep in Sweden, with particular reference to over-winter survival strategies Waller, P. J.; Rudby-Martin, L.; Ljungström, B. L. Veterinary Parasitology, Vol. 122, Issue 3 https://doi.org/10.1016/j.vetpar.2004.04.007	journal	July 2004
Consequences of the unusually warm and dry summer of 2003 in The Netherlands: Poor development of free living stages, normal survival of infective larvae and long survival of adult gastrointestinal nematodes of sheep Eysker, M.; Bakker, N.; Kooyman, F. N. J. Veterinary Parasitology, Vol. 133, Issue 4 https://doi.org/10.1016/j.vetpar.2005.05.058	journal	November 2005
A computer model to simulate control of parasitic gastroenteritis in sheep on UK farms Learmount, J.; Taylor, M. A.; Smith, G. Veterinary Parasitology, Vol. 142, Issue 3-4 https://doi.org/10.1016/j.vetpar.2006.07.012	journal	December 2006
Ecology of the free-living stages of major trichostrongylid parasites of sheep O’Connor, Lauren J.; Walkden-Brown, Stephen W.; Kahn, Lewis P. Veterinary Parasitology, Vol. 142, Issue 1-2 https://doi.org/10.1016/j.vetpar.2006.08.035	journal	November 2006
Haemonchosis and teladorsagiosis in a Scottish sheep flock putatively associated with the overwintering of hypobiotic fourth stage larvae Sargison, N. D.; Wilson, D. J.; Bartley, D. J. Veterinary Parasitology, Vol. 147, Issue 3-4 https://doi.org/10.1016/j.vetpar.2007.04.011	journal	July 2007
Interaction between the effects of evaporation rate and amount of simulated rainfall on development of the free-living stages of Haemonchus contortus O’Connor, Lauren J.; Kahn, Lewis P.; Walkden-Brown, Stephen W. Veterinary Parasitology, Vol. 155, Issue 3-4 https://doi.org/10.1016/j.vetpar.2008.05.010	journal	August 2008
Back to the future: Developing hypotheses on the effects of climate change on ovine parasitic gastroenteritis from historical data van Dijk, J.; David, G. P.; Baird, G. Veterinary Parasitology, Vol. 158, Issue 1-2 https://doi.org/10.1016/j.vetpar.2008.08.006	journal	November 2008
Sheep helminth parasitic disease in south eastern Scotland arising as a possible consequence of climate change Kenyon, F.; Sargison, N. D.; Skuce, P. J. Veterinary Parasitology, Vol. 163, Issue 4 https://doi.org/10.1016/j.vetpar.2009.03.027	journal	August 2009
Effect of simulated rainfall timing on faecal moisture and development of Haemonchus contortus and Trichostrongylus colubriformis eggs to infective larvae Khadijah, S.; Kahn, L. P.; Walkden-Brown, S. W. Veterinary Parasitology, Vol. 192, Issue 1-3 https://doi.org/10.1016/j.vetpar.2012.10.015	journal	February 2013
Moisture requirements for the migration of Haemonchus contortus third stage larvae out of faeces Wang, Tong; van Wyk, J. A.; Morrison, A. Veterinary Parasitology, Vol. 204, Issue 3-4 https://doi.org/10.1016/j.vetpar.2014.05.014	journal	August 2014
Predictions of future grazing season length for European dairy, beef and sheep farms based on regression with bioclimatic variables Phelan, P.; Morgan, E. R.; Rose, H. The Journal of Agricultural Science, Vol. 154, Issue 5 https://doi.org/10.1017/S0021859615000830	journal	October 2015
The dynamics of nematode infections of farmed ruminants Roberts, M. G.; Heesterbeek, J. A. P. Parasitology, Vol. 110, Issue 4 https://doi.org/10.1017/S0031182000064830	journal	May 1995
Observations on the free-living stages of the stomach worm Haemonchus contortus Rose, J. H. Parasitology, Vol. 53, Issue 3-4 https://doi.org/10.1017/S0031182000073923	journal	November 1963
The influence of water on the migration of infective trichostrongyloid larvae onto grass van DIJK, J.; Morgan, E. R. Parasitology, Vol. 138, Issue 6 https://doi.org/10.1017/S0031182011000308	journal	April 2011
Nematode parasites of sheep: a survey of epidemiological parameters and their application in a simple model Kao, R. R.; Leathwick, D. M.; Roberts, M. G. Parasitology, Vol. 121, Issue 1 https://doi.org/10.1017/S0031182099006095	journal	July 2000
A European daily high-resolution gridded data set of surface temperature and precipitation for 1950–2006 Haylock, M. R.; Hofstra, N.; Klein Tank, A. M. G. Journal of Geophysical Research, Vol. 113, Issue D20 https://doi.org/10.1029/2008JD010201	journal	January 2008
A globally coherent fingerprint of climate change impacts across natural systems Parmesan, Camille; Yohe, Gary Nature, Vol. 421, Issue 6918 https://doi.org/10.1038/nature01286	journal	January 2003
The next generation of scenarios for climate change research and assessment Moss, Richard H.; Edmonds, Jae A.; Hibbard, Kathy A. Nature, Vol. 463, Issue 7282 https://doi.org/10.1038/nature08823	journal	February 2010
Effects of elevated temperature on multi-species interactions: the case of Pedunculate Oak, Winter Moth and Tits Buse, A.; Dury, S. J.; Woodburn, R. J. W. Functional Ecology, Vol. 13, Issue s1 https://doi.org/10.1046/j.1365-2435.1999.00010.x	journal	June 1999
Prevalence and Seasonal Pattern of Caprine Trichostrongyles in a Dry Area of Central Spain: Valc& aacute; rcel and G arc& iacute; a R omero Valcárcel, F.; Romero, C. García Journal of Veterinary Medicine, Series B, Vol. 46, Issue 10 https://doi.org/10.1046/j.1439-0450.1999.00297.x	journal	December 1999
The Inter-Sectoral Impact Model Intercomparison Project (ISI–MIP): Project framework Warszawski, Lila; Frieler, Katja; Huber, Veronika Proceedings of the National Academy of Sciences, Vol. 111, Issue 9 https://doi.org/10.1073/pnas.1312330110	journal	December 2013
Nematode parasites of vertebrates: their development and transmission. Anderson, R. C. CABI LIbrary https://doi.org/10.1079/9780851994215.0000	book	January 2000
The development and overwintering survival of free-living larvae of Haemonchus contortus in Sweden Troell, K.; Waller, P.; Höglund, J. Journal of Helminthology, Vol. 79, Issue 4 https://doi.org/10.1079/JOH2005286	journal	December 2005
To delay once or twice: the effect of hypobiosis and free-living stages on the stability of host–parasite interactions Gaba, Sabrina; Gourbière, Sébastien Journal of The Royal Society Interface, Vol. 5, Issue 25 https://doi.org/10.1098/rsif.2007.1282	journal	December 2007
Modelling the effects of past and future climate on the risk of bluetongue emergence in Europe Guis, Helene; Caminade, Cyril; Calvete, Carlos Journal of The Royal Society Interface, Vol. 9, Issue 67 https://doi.org/10.1098/rsif.2011.0255	journal	June 2011
Metabolic approaches to understanding climate change impacts on seasonal host-macroparasite dynamics Molnár, Péter K.; Kutz, Susan J.; Hoar, Bryanne M. Ecology Letters, Vol. 16, Issue 1 https://doi.org/10.1111/ele.12022	journal	November 2012
Climate changes influence free-living stages of soil-transmitted parasites of European rabbits Hernandez, Alexander D.; Poole, Adam; Cattadori, Isabella M. Global Change Biology, Vol. 19, Issue 4 https://doi.org/10.1111/gcb.12106	journal	January 2013
Invasion, establishment, and range expansion of two parasitic nematodes in the Canadian Arctic Kutz, Susan J.; Checkley, Sylvia; Verocai, Guilherme G. Global Change Biology https://doi.org/10.1111/gcb.12315	journal	September 2013
Climate change and livestock parasites: integrated management of sheep blowfly strike in a warmer environment: INTEGRATED MANAGEMENT OF SHEEP BLOWFLY STRIKE Wall, Richard; Ellse, Lauren S. Global Change Biology, Vol. 17, Issue 5 https://doi.org/10.1111/j.1365-2486.2010.02361.x	journal	November 2010
Climate Change and Infectious Diseases: From Evidence to a Predictive Framework Altizer, S.; Ostfeld, R. S.; Johnson, P. T. J. Science, Vol. 341, Issue 6145 https://doi.org/10.1126/science.1239401	journal	August 2013
Widespread anthelmintic resistance in European farmed ruminants: a systematic review Rose, H.; Rinaldi, L.; Bosco, A. Veterinary Record, Vol. 176, Issue 21 https://doi.org/10.1136/vr.102982	journal	March 2015
An Overview of CMIP5 and the Experiment Design Taylor, Karl E.; Stouffer, Ronald J.; Meehl, Gerald A. Bulletin of the American Meteorological Society, Vol. 93, Issue 4 https://doi.org/10.1175/BAMS-D-11-00094.1	journal	April 2012
Reference Crop Evapotranspiration from Temperature No authors listed Applied Engineering in Agriculture, Vol. 1, Issue 2 https://doi.org/10.13031/2013.26773	journal	January 1985
A Non-Stationary Relationship between Global Climate Phenomena and Human Plague Incidence in Madagascar Kreppel, Katharina S.; Caminade, Cyril; Telfer, Sandra PLoS Neglected Tropical Diseases, Vol. 8, Issue 10 https://doi.org/10.1371/journal.pntd.0003155	journal	October 2014
The ecology of climate change and infectious diseases Lafferty, Kevin D. Ecology, Vol. 90, Issue 4 https://doi.org/10.1890/08-0079.1	journal	April 2009
Modelling recent and future climatic suitability for fasciolosis in Europe Caminade, Cyril; Van Dijk, Jan; Baylis, Matthew Geospatial Health, Vol. 9, Issue 2 https://doi.org/10.4081/gh.2015.352	journal	March 2015
Haemonchus contortus: spatial risk distribution for infection in sheep in Europe Rinaldi, Laura; Catelan, Dolores; Musella, Vincenzo Geospatial Health, Vol. 9, Issue 2 https://doi.org/10.4081/gh.2015.355	journal	March 2015
The basic reproduction quotient (Q0) as a potential spatial predictor of the seasonality of ovine haemonchosis Bolajoko, Muhammad-Bashir; Rose, Hannah; Musella, Vincenzo Geospatial Health, Vol. 9, Issue 2 https://doi.org/10.4081/gh.2015.356	journal	March 2015
A trend-preserving bias correction – the ISI-MIP approach Hempel, S.; Frieler, K.; Warszawski, L. Earth System Dynamics Discussions, Vol. 4, Issue 1 https://doi.org/10.5194/esdd-4-49-2013	journal	January 2013

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