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

Abstract

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 bymore » 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.« less

Authors:
 [1];  [2];  [3];  [4];  [5];  [6];  [7];  [8]
  1. 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
  2. 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
  3. 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
  4. Animal &, Grassland Research and Innovation Centre Teagasc Grange, Dunsanny Co. Meath Ireland
  5. Department of Epidemiology and Population Health Institute of Infection and Global Health University of Liverpool, Leahurst Neston Cheshire CH64 7TE UK
  6. School of Environmental Sciences University of Liverpool Liverpool UK, Health Protection Research Unit in Emerging and Zoonotic Infections University of Liverpool Neston UK
  7. Department of Infection Biology Institute of Infection and Global Health University of Liverpool Liverpool L3 5RF UK
  8. 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
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1400729
Resource Type:
Publisher's Accepted Manuscript
Journal Name:
Global Change Biology
Additional Journal Information:
Journal Name: Global Change Biology Journal Volume: 22 Journal Issue: 3; Journal ID: ISSN 1354-1013
Publisher:
Wiley-Blackwell
Country of Publication:
United Kingdom
Language:
English

Citation Formats

Rose, Hannah, Caminade, Cyril, Bolajoko, Muhammad Bashir, Phelan, Paul, van Dijk, Jan, Baylis, Matthew, Williams, Diana, and Morgan, Eric R. Climate‐driven changes to the spatio‐temporal distribution of the parasitic nematode, Haemonchus contortus, in sheep in Europe. United Kingdom: N. p., 2016. Web. doi:10.1111/gcb.13132.
Rose, Hannah, Caminade, Cyril, Bolajoko, Muhammad Bashir, Phelan, Paul, van Dijk, Jan, Baylis, Matthew, Williams, Diana, & Morgan, Eric R. Climate‐driven changes to the spatio‐temporal distribution of the parasitic nematode, Haemonchus contortus, in sheep in Europe. United Kingdom. https://doi.org/10.1111/gcb.13132
Rose, Hannah, Caminade, Cyril, Bolajoko, Muhammad Bashir, Phelan, Paul, van Dijk, Jan, Baylis, Matthew, Williams, Diana, and Morgan, Eric R. Wed . "Climate‐driven changes to the spatio‐temporal distribution of the parasitic nematode, Haemonchus contortus, in sheep in Europe". United Kingdom. https://doi.org/10.1111/gcb.13132.
@article{osti_1400729,
title = {Climate‐driven changes to the spatio‐temporal distribution of the parasitic nematode, Haemonchus contortus, in sheep in Europe},
author = {Rose, Hannah and Caminade, Cyril and Bolajoko, Muhammad Bashir and Phelan, Paul and van Dijk, Jan and Baylis, Matthew and Williams, Diana and Morgan, Eric R.},
abstractNote = {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.},
doi = {10.1111/gcb.13132},
journal = {Global Change Biology},
number = 3,
volume = 22,
place = {United Kingdom},
year = {Wed Jan 06 00:00:00 EST 2016},
month = {Wed Jan 06 00:00:00 EST 2016}
}

Journal Article:
Free Publicly Available Full Text
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https://doi.org/10.1111/gcb.13132

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Cited by: 42 works
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Works referenced in this record:

Ecology of the free-living stages of major trichostrongylid parasites of sheep
journal, November 2006

  • O’Connor, Lauren J.; Walkden-Brown, Stephen W.; Kahn, Lewis P.
  • Veterinary Parasitology, Vol. 142, Issue 1-2
  • DOI: 10.1016/j.vetpar.2006.08.035

Haemonchosis and teladorsagiosis in a Scottish sheep flock putatively associated with the overwintering of hypobiotic fourth stage larvae
journal, July 2007


Observations on the free-living stages of the stomach worm Haemonchus contortus
journal, November 1963


A Non-Stationary Relationship between Global Climate Phenomena and Human Plague Incidence in Madagascar
journal, October 2014

  • Kreppel, Katharina S.; Caminade, Cyril; Telfer, Sandra
  • PLoS Neglected Tropical Diseases, Vol. 8, Issue 10
  • DOI: 10.1371/journal.pntd.0003155

An Overview of CMIP5 and the Experiment Design
journal, April 2012

  • Taylor, Karl E.; Stouffer, Ronald J.; Meehl, Gerald A.
  • Bulletin of the American Meteorological Society, Vol. 93, Issue 4
  • DOI: 10.1175/BAMS-D-11-00094.1

Invasion, establishment, and range expansion of two parasitic nematodes in the Canadian Arctic
journal, September 2013

  • Kutz, Susan J.; Checkley, Sylvia; Verocai, Guilherme G.
  • Global Change Biology
  • DOI: 10.1111/gcb.12315

Climate change and parasitic disease: farmer mitigation?
journal, July 2009


Reference Crop Evapotranspiration from Temperature
journal, January 1985

  • George H. Hargreaves,
  • Applied Engineering in Agriculture, Vol. 1, Issue 2
  • DOI: 10.13031/2013.26773

Effect of simulated rainfall timing on faecal moisture and development of Haemonchus contortus and Trichostrongylus colubriformis eggs to infective larvae
journal, February 2013


The basic reproduction quotient (Q0) as a potential spatial predictor of the seasonality of ovine haemonchosis
journal, March 2015

  • Bolajoko, Muhammad-Bashir; Rose, Hannah; Musella, Vincenzo
  • Geospatial Health, Vol. 9, Issue 2
  • DOI: 10.4081/gh.2015.356

The next generation of scenarios for climate change research and assessment
journal, February 2010

  • Moss, Richard H.; Edmonds, Jae A.; Hibbard, Kathy A.
  • Nature, Vol. 463, Issue 7282
  • DOI: 10.1038/nature08823

Haemonchus contortus: spatial risk distribution for infection in sheep in Europe
journal, March 2015

  • Rinaldi, Laura; Catelan, Dolores; Musella, Vincenzo
  • Geospatial Health, Vol. 9, Issue 2
  • DOI: 10.4081/gh.2015.355

Modelling recent and future climatic suitability for fasciolosis in Europe
journal, March 2015

  • Caminade, Cyril; Van Dijk, Jan; Baylis, Matthew
  • Geospatial Health, Vol. 9, Issue 2
  • DOI: 10.4081/gh.2015.352

Effects of elevated temperature on multi-species interactions: the case of Pedunculate Oak, Winter Moth and Tits
journal, June 1999


The epidemiology of abomasal nematodes of sheep in Sweden, with particular reference to over-winter survival strategies
journal, July 2004


Climate Change and Infectious Diseases: From Evidence to a Predictive Framework
journal, August 2013


A trend-preserving bias correction – the ISI-MIP approach
journal, January 2013

  • Hempel, S.; Frieler, K.; Warszawski, L.
  • Earth System Dynamics Discussions, Vol. 4, Issue 1
  • DOI: 10.5194/esdd-4-49-2013

Moisture requirements for the migration of Haemonchus contortus third stage larvae out of faeces
journal, August 2014


Regulation of Haemonchus contortus populations in sheep: Mortality of established worms
journal, March 1988


The development and mortality of the free-living stages of Haemonchus contortus in laboratory culture
journal, August 1992


Regulation of Haemonchus contortus populations in sheep exposed to continuous infection
journal, October 1985


Prevalence and Seasonal Pattern of Caprine Trichostrongyles in a Dry Area of Central Spain: Valc& aacute; rcel and G arc& iacute; a R omero
journal, December 1999


Climate changes influence free-living stages of soil-transmitted parasites of European rabbits
journal, January 2013

  • Hernandez, Alexander D.; Poole, Adam; Cattadori, Isabella M.
  • Global Change Biology, Vol. 19, Issue 4
  • DOI: 10.1111/gcb.12106

Sheep helminth parasitic disease in south eastern Scotland arising as a possible consequence of climate change
journal, August 2009


Predictions of future grazing season length for European dairy, beef and sheep farms based on regression with bioclimatic variables
journal, October 2015


A globally coherent fingerprint of climate change impacts across natural systems
journal, January 2003


Modelling the impact of climate change on spatial patterns of disease risk: Sheep blowfly strike by Lucilia sericata in Great Britain
journal, June 2011


Threshold quantities for helminth infections
journal, February 1995

  • Heesterbeek, J. A. P.; Roberts, M. G.
  • Journal of Mathematical Biology, Vol. 33, Issue 4
  • DOI: 10.1007/BF00176380

Frontiers in climate change–disease research
journal, June 2011

  • Rohr, Jason R.; Dobson, Andrew P.; Johnson, Pieter T. J.
  • Trends in Ecology & Evolution, Vol. 26, Issue 6
  • DOI: 10.1016/j.tree.2011.03.002

Nematode parasites of sheep: a survey of epidemiological parameters and their application in a simple model
journal, July 2000


Hypobiosis of Haemonchus contortus in natural infections of sheep and goats in a semi-arid area of Kenya
journal, May 1998


A computer model to simulate control of parasitic gastroenteritis in sheep on UK farms
journal, December 2006


A model for nematodiasis in New Zealand lambs
journal, September 1992


Metabolic approaches to understanding climate change impacts on seasonal host-macroparasite dynamics
journal, November 2012

  • Molnár, Péter K.; Kutz, Susan J.; Hoar, Bryanne M.
  • Ecology Letters, Vol. 16, Issue 1
  • DOI: 10.1111/ele.12022

The ecology of climate change and infectious diseases
journal, April 2009


Widespread anthelmintic resistance in European farmed ruminants: a systematic review
journal, March 2015

  • Rose, H.; Rinaldi, L.; Bosco, A.
  • Veterinary Record, Vol. 176, Issue 21
  • DOI: 10.1136/vr.102982

Interaction between the effects of evaporation rate and amount of simulated rainfall on development of the free-living stages of Haemonchus contortus
journal, August 2008

  • O’Connor, Lauren J.; Kahn, Lewis P.; Walkden-Brown, Stephen W.
  • Veterinary Parasitology, Vol. 155, Issue 3-4
  • DOI: 10.1016/j.vetpar.2008.05.010

The mortality and fecundity of Haemonchus contortus in parasite-naive and parasite-exposed sheep following single experimental infections
journal, May 1992


Back to the future: Developing hypotheses on the effects of climate change on ovine parasitic gastroenteritis from historical data
journal, November 2008


The dynamics of nematode infections of farmed ruminants
journal, May 1995


Vertical distribution of trichostrongylid larvae on herbage and in soil
journal, June 1986


Modelling the effects of past and future climate on the risk of bluetongue emergence in Europe
journal, June 2011

  • Guis, Helene; Caminade, Cyril; Calvete, Carlos
  • Journal of The Royal Society Interface, Vol. 9, Issue 67
  • DOI: 10.1098/rsif.2011.0255

The influence of water on the migration of infective trichostrongyloid larvae onto grass
journal, April 2011


To delay once or twice: the effect of hypobiosis and free-living stages on the stability of host–parasite interactions
journal, December 2007

  • Gaba, Sabrina; Gourbière, Sébastien
  • Journal of The Royal Society Interface, Vol. 5, Issue 25
  • DOI: 10.1098/rsif.2007.1282

Understanding social resilience to climate variability in primary enterprises and industries
journal, February 2010


The development and overwintering survival of free-living larvae of Haemonchus contortus in Sweden
journal, December 2005

  • Troell, K.; Waller, P.; Höglund, J.
  • Journal of Helminthology, Vol. 79, Issue 4
  • DOI: 10.1079/JOH2005286

A European daily high-resolution gridded data set of surface temperature and precipitation for 1950–2006
journal, January 2008

  • Haylock, M. R.; Hofstra, N.; Klein Tank, A. M. G.
  • Journal of Geophysical Research, Vol. 113, Issue D20
  • DOI: 10.1029/2008JD010201

The Inter-Sectoral Impact Model Intercomparison Project (ISI–MIP): Project framework
journal, December 2013

  • Warszawski, Lila; Frieler, Katja; Huber, Veronika
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 9
  • DOI: 10.1073/pnas.1312330110