Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-23T07:10:37.181Z Has data issue: false hasContentIssue false
  • English
  • Français

Asynchrony in host and parasite phenology may decrease disease risk in livestock under climate warming: Nematodirus battus in lambs as a case study

Published online by Cambridge University Press:  19 June 2015

OWEN J. GETHINGS ,
HANNAH ROSE ,
SIÂN MITCHELL ,
JAN VAN DIJK  and
ERIC R. MORGAN
OWEN J. GETHINGS
Affiliation:
University of Bristol, School of Biological Sciences, Bristol Life Sciences Building, 24 Tyndall Avenue, Bristol, BS8 1TQ, UK Harper Adams University, Crop and Environment Sciences, Newport, Shropshire, TF10 8NB, UK
HANNAH ROSE
Affiliation:
University of Bristol, School of Biological Sciences, Bristol Life Sciences Building, 24 Tyndall Avenue, Bristol, BS8 1TQ, UK University of Bristol, Cabot Institute, Cantocks Close, Bristol, BS8 1TS, UK
SIÂN MITCHELL
Affiliation:
Animal and Plant Health Agency, Carmarthen Investigation Centre, Job's Well Rd, Johnstown, Carmarthen, SA31 3EZ, Wales, UK
JAN VAN DIJK
Affiliation:
Department of Epidemiology and Population Health, University of Liverpool, Institute of Infection and Global Health, Neston, Cheshire, CH64 7TE, UK
ERIC R. MORGAN*
Affiliation:
University of Bristol, Cabot Institute, Cantocks Close, Bristol, BS8 1TS, UK University of Bristol, School of Veterinary Science, Langford House, Langford, Somerset, BS40 5DU, UK
*
* Corresponding author. University of Bristol, Life Sciences Building, Tyndall Avenue, Bristol, BS8 1TQ, UK. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Mismatch in the phenology of trophically linked species as a result of climate warming has been shown to have far-reaching effects on animal communities, but implications for disease have so far received limited attention. This paper presents evidence suggestive of phenological asynchrony in a host-parasite system arising from climate change, with impacts on transmission. Diagnostic laboratory data on outbreaks of infection with the pathogenic nematode Nematodirus battus in sheep flocks in the UK were used to validate region-specific models of the effect of spring temperature on parasite transmission. The hatching of parasite eggs to produce infective larvae is driven by temperature, while the availability of susceptible hosts depends on lambing date, which is relatively insensitive to inter-annual variation in spring temperature. In southern areas and in warmer years, earlier emergence of infective larvae in spring was predicted, with decline through mortality before peak availability of susceptible lambs. Data confirmed model predictions, with fewer outbreaks recorded in those years and regions. Overlap between larval peaks and lamb availability was not reduced in northern areas, which experienced no decreases in the number of reported outbreaks. Results suggest that phenological asynchrony arising from climate warming may affect parasite transmission, with non-linear but predictable impacts on disease burden. Improved understanding of complex responses of host-parasite systems to climate change can contribute to effective adaptation of parasite control strategies.

Keywords

Climate changenon-linearNematodirus battusnematodeepidemiologyspringanthelminticsheepfood securitydisease
Type
Research Article
Information
Parasitology , Volume 142 , Issue 10 , September 2015 , pp. 1306 - 1317
Check for updates
Copyright
Copyright © Crown 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Altizer, S., Dobson, A., Hosseini, P., Hudson, P., Pascual, M. and Rohani, P. (2006). Seasonality and the dynamics of infectious diseases. Ecology Letters 9, 467–484.CrossRefGoogle ScholarPubMed
Altizer, S., Ostfeld, R. S., Johnson, P. T. J., Kutz, S. and Harvell, C. D. (2013). Climate change and infectious diseases: from evidence to a predictive framework. Science 341, 514–519.CrossRefGoogle ScholarPubMed
Andre, J., Haddon, M. and Pecl, G. T. (2010). Modelling climate-change-induced nonlinear thresholds in cephalopod population dynamics. Global Change Biology 16, 2866–2875.CrossRefGoogle Scholar
Bolajoko, M. B., Rose, H., Musella, V., Bosco, A., Rinaldi, L., Van Dijk, J., Cringoli, G. and Morgan, E. R. (2015). The basic reproduction quotient (Q0) as a potential spatial predictor of the seasonality of ovine haemonchosis. Geospatial Health 9, 333–350.Google Scholar
Both, C., van Asch, M., Bijlsma, R. G., van den Burg, A. B. and Visser, M. E. (2009). Climate change and unequal phenological changes across four trophic levels: constraints or adaptations? Journal of Animal Ecology 78, 73–83.Google Scholar
Bradshaw, W. E. and Holzapfel, C. M. (2008). Genetic response to rapid climate change: it's seasonal timing that matters. Molecular Ecology 17, 157–166.CrossRefGoogle ScholarPubMed
Brooks, D. R. and Hoberg, E. P. (2007). How will global climate change affect parasite-host assemblages? Trends in Parasitology 23, 571–574.CrossRefGoogle ScholarPubMed
Brown, V. L. and Rohani, P. (2012). The consequences of climate change at an avian influenza ‘hotspot’. Biology Letters 8, 1036–1039.CrossRefGoogle ScholarPubMed
Cameron, J., Malpaux, B. and Castonguay, F. W. (2010). Accelerated lambing achieved by a photoperiod regimen consisting of alternating 4-month sequences of long and short days applied year-round. Journal of Animal Science 88, 3280–3290.CrossRefGoogle ScholarPubMed
Dobson, A. P. and Carper, R. (1992). Global warming and potential changes in host-parasite and disease vector relationships. In Global Warming and Biological Diversity (ed. Peters, R. L. and Lovejoy, T.), pp. 201–220. Yale University Press, New Haven, USA.Google Scholar
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.Google Scholar
Hernandez, A. D., Poole, A. and Cattadori, I. M. (2013). Climate changes influence free-living stages of soil-transmitted parasites of European rabbits. Global Change Biology 19, 1028–1042.Google Scholar
Hoar, B. M., Ruckstuhl, K. and Kutz, S. (2012). Development and availability of the free-living stages of Ostertagia gruehneri, an abomasal parasite of barrenground caribou (Rangifer tarandus tarandus), on the Canadian tundra. Parasitology 139, 1093–1100.CrossRefGoogle ScholarPubMed
Kaplan, R. M. and Vidyashankar, A. N. (2012). An inconvenient truth: global worming and anthelmintic resistance. Veterinary Parasitology 186, 70–78.Google Scholar
Kenyon, F., Sargison, N. D., Skuce, P. J. and Jackson, F. (2009). Sheep helminth parasitic disease in south eastern Scotland arising as a possible consequence of climate change. Veterinary Parasitology 163, 293–297.Google Scholar
Klapwijk, M. B., Grobler, C., Ward, K. and Wheeler, D. (2010). Influence of experimental warming and shading on host-parasitoid synchrony. Global Change Biology 16, 102–112.CrossRefGoogle Scholar
Kreyling, J., Wiesenberg, G. L. B., Thiel, D., Wohlfart, C., Huber, G., Walter, J., Jentsch, A., Konnert, M. and Beierkuhnlein, C. (2012). Cold hardiness of Pinus nigra Arnold as influenced by geographic origin, warming and extreme summer drought. Environmental and Experimental Botany 78, 99–108.CrossRefGoogle Scholar
Kreyling, J., Jentsch, A. and Beier, C. (2014). Beyond realism in climate change experiments: gradient approaches identify thresholds and tipping points. Ecology Letters 17, 125–e1.Google Scholar
Kutz, S., Checkley, S., Verocai, G. G., Dumond, M., Hoberg, E. P., Peacock, R., Wu, J. P., Orsel, K., Seegers, K., Warren, A. L. and Abrams, A. (2013). Invasion, establishment, and range expansion of two parasitic nematodes in the Canadian Arctic. Global Change Biology 19, 3254–3262.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 B: Biological Sciences 272, 2571–2576.Google Scholar
Lawler, J. J., White, D., Neilson, R. P. and Blaustein, A. R. (2006). Predicting climate-induced range shifts: model differences and model reliability. Global Change Biology 12, 1568–1584.Google Scholar
Lof, M. E., Reed, T. E., McNamara, J. M. and Visser, M. E. (2012). Timing in a fluctuating environment: environmental variability and asymmetric fitness curves can lead to adaptively mismatched avian reproduction. Proceedings of the Royal Society; Series B 279, 3161–3169.Google Scholar
Marshall, N. A., Park, S., Howden, S. M., Dowd, A. B. and Jakku, E. S. (2013). Climate change awareness is associated with enhanced adaptive capacity. Agricultural Systems 117, 30–34.Google Scholar
McMahon, C., Gordon, A. W., Edgar, H. W. J., Hanna, R. E. B., Brennan, G. P. and Fairweather, I. (2012). The effects of climate change on ovine parasitic gastroenteritis determined using veterinary surveillance and meteorological data for Northern Ireland over the period 1999–2009. Veterinary Parasitology 190, 67–177.Google Scholar
Molnar, P. K., Kutz, S. J., Hoar, B. M. and Dobson, A. P. (2013). Metabolic approaches to understanding climate change impacts on seasonal host-macroparasite dynamics. Ecology Letters 16, 9–21.Google Scholar
Mooney, H., Larigauderie, A., Cesario, M., Elmquist, T., Hoegh-Guldberg, O., Lavorel, S., Mace, G. M., Palmer, M., Scholes, R. and Yahara, T. (2009). Biodiversity, climate change, and ecosystem services. Current Opinion in Environmental Sustainability 1, 46–54.Google Scholar
Morgan, E. R. and van Dijk, J. (2012). Climate and the epidemiology of gastrointestinal nematode infections of sheep in Europe. Veterinary Parasitology 189, 8–14.CrossRefGoogle ScholarPubMed
Morgan, E. R. and Wall, R. (2009). Climate change and parasitic disease: farmer mitigation? Trends in Parasitology 25, 308–313.Google Scholar
Morgan, E. R., Hosking, B. C., Burston, S., Carder, K. M., Hyslop, A. C., Pritchard, L. J. and Whitmarsh, A. K. (2012). A survey of helminth control practices on sheep farms in Great Britain and Ireland. Veterinary Journal 192, 390–397.CrossRefGoogle ScholarPubMed
O'Connor, L. J., Walkden-Brown, S. W. and Kahn, L. P. (2006). Ecology of the free-living stages of major trichostrongylid parasites of sheep. Veterinary Parasitology 142, 1–15.CrossRefGoogle ScholarPubMed
Ollerenshaw, C. B. and Smith, L. P. (1966). An empirical approach to forecasting the incidence of nematodiriasis over England and Wales. Veterinary Record 79, 536–540.Google Scholar
Parmesan, C. and Yohe, G. (2003). A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37–42.Google Scholar
Paull, S. H. and Johnson, P. T. J. (2014). Experimental warming drives a seasonal shift in the timing of host-parasite dynamics with consequences for disease risk. Ecology Letters 17, 445–453.Google Scholar
Paull, S. H., LaFonte, B. E. and Johnson, P. T. J. (2012). Temperature-driven shifts in a host-parasite interaction drive nonlinear changes in disease risk. Global Change Biology 18, 3558–3567.Google Scholar
Perry, M., Hollis, D. and Elms, M. (2009). The Generation of Daily Gridded Datasets of Temperature and Rainfall for the UK. Met Office National Climate Information Centre. http://www.metoffice.gov.uk/climatechange/science/downloads/generation_of_daily_gridded_datasets.pdf.Google Scholar
Phelan, P., Morgan, E. R., Rose, H., Grant, J. and O'Kiely, P. (in review). Future grazing season length predictions for European dairy, beef and sheep farms based on current regression with bioclimatic variables.Google Scholar
Polley, L. and Thompson, R. C. A. (2009). Parasite zoonoses and climate change: molecular tools for tracking shifting boundaries. Trends in Parasitology 25, 285–291.CrossRefGoogle ScholarPubMed
Rivington, M., Matthews, K. B., Bellochi, G., Buchan, K., Stockle, C. O. and Donatelli, M. (2007). An integrated assessment approach to conduct analyses of climate change impacts on whole-farm systems. Environmental Modelling and Software 22, 202–210.Google Scholar
Rose, H., Rinaldi, L., Bosco, A., Mavrot, F., de Waal, T., Skuce, P., Charlier, J., Torgerson, P. R., Hertzberg, H., Hendrickx, G., Vercruysse, J. and Morgan, E. R. (2015 a). Widespread spatial distribution of anthelmintic resistance in European farmed ruminants: a systematic review. Veterinary Record 176, 546.Google Scholar
Rose, H., Wang, T., van Dijk, J. and Morgan, E. R. (2015 b). GLOWORM-FL: a simulation model of the effects of climate and climate change on the free-living stages of gastrointestinal nematode parasites of ruminants. Ecological Modelling 297, 232–245.Google Scholar
Sargison, N. D., Wilson, D. J. and Scott, P. R. (2012). Observations on the epidemiology of autumn nematodirosis in weaned lambs in a Scottish sheep flock. Veterinary Record 15, 391.CrossRefGoogle Scholar
Singer, M. C. and Parmesan, C. (2010). Phenological asynchrony between herbivorous insects and their hosts: signal of climate change or pre-existing adaptive strategy. Philosophical Transactions of the Royal Society B 365, 3161–3176.CrossRefGoogle ScholarPubMed
Skuce, P. J., Morgan, E. R., van Dijk, J. and Mitchell, M. (2013). Animal health aspects of adaptation to climate change: beating the heat and parasites in a warming Europe. Animal 7, 333–345.Google Scholar
Smith, L. P. and Thomas, R. J. (1972). Forecasting the spring hatch of Nematodirus battus by use of soil temperature data. Veterinary Record 90, 388–392.Google Scholar
Thackeray, S. J., Henrys, P. A., Feuchtmayr, H., Jones, I. D., Maberly, S. C. and Winfield, I. J. (2013). Food web de-synchronisation in England's largest lake: an assessment based upon multiple phonological metrics. Global Change Biology 19, 3568–3580.Google Scholar
Thomas, D. Rh. (1991). The epidemiology of Nematodirus battus – is it changing? Parasitology 102, 147–155.Google Scholar
Van Dijk, J. and Morgan, E. R. (2008). The influence of temperature on the development, hatching and survival of Nematodirus battus larvae. Parasitology 135, 269–283.Google Scholar
Van Dijk, J. and Morgan, E. R. (2010). Variation in the hatching behaviour of Nematodirus battus: polymorphic bet hedging? International Journal for Parasitology 40, 675–681.CrossRefGoogle ScholarPubMed
Van Dijk, J. and Morgan, E. R. (2012). The influence of water and humidity on the hatching of Nematodirus battus eggs. Journal of Helminthology 86, 287–292.Google Scholar
Van Dijk, J., David, G. P., Baird, G. and Morgan, E. R. (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.CrossRefGoogle Scholar
Van Dijk, J., de Louw, M. D. E., Kalis, L. P. A. and Morgan, E. R. (2009). Ultraviolet light increases mortality of nematode larvae and can explain patterns of larval availability at pasture. International Journal for Parasitology 39, 1151–1156.Google Scholar
Van Dijk, J., Sargison, N. D., Kenyon, F. and Skuce, P. (2010). Climate change and infectious disease: helminthological challenges to ruminants in temperate regions. Animal 4, 377–392.Google Scholar
Visser, M. E. and Both, C. (2005). Shifts in phenology due to global climate change: the need for a yardstick. Proceedings of the Royal Society; Series B 272, 2561–2569.Google Scholar
Visser, M. E., van Noordwijk, J., Tinbergen, J. M. and Lessells, C. M. (1998). Warmer springs lead to mistimed reproduction in great tits (Parus major). Proceedings of the Royal Society; Series B 263, 1867–1870.Google Scholar