Naomi J. Fox

Predicting Impacts of Climate Change on Fasciola hepatica Risk

Fasciola hepatica (liver fluke) is a physically and economically devastating parasitic trematode whose rise in recent years has been attributed to climate change. Climate has an impact on the free-living stages of the parasite and its intermediate host Lymnaea truncatula, with the interactions between rainfall and temperature having the greatest influence on transmission efficacy. There have been a number of short term climate driven forecasts developed to predict the following seasons infection risk, with the Ollerenshaw index being the most widely used. Through the synthesis of a modified Ollerenshaw index with the UKCP09 fine scale climate projection data we have developed long term seasonal risk forecasts up to 2070 at a 25 km square resolution. Additionally UKCIP gridded datasets at 5 km square resolution from 1970-2006 were used to highlight the climate-driven increase to date. The maps show unprecedented levels of future fasciolosis risk in parts of the UK, with risk of serious epidemics in Wales by 2050. The seasonal risk maps demonstrate the possible change in the timing of disease outbreaks due to increased risk from overwintering larvae. Despite an overall long term increase in all regions of the UK, spatio-temporal variation in risk levels is expected. Infection risk will reduce in some areas and fluctuate greatly in others with a predicted decrease in summer infection for parts of the UK due to restricted water availability. This forecast is the first approximation of the potential impacts of climate change on fasciolosis risk in the UK. It can be used as a basis for indicating where active disease surveillance should be targeted and where the development of improved mitigation or adaptation measures is likely to bring the greatest benefits.

The status of tularemia in Europe in a one-health context: a review

The bacterium Francisella tularensis causes the vector-borne zoonotic disease tularemia, and may infect a wide range of hosts including invertebrates, mammals and birds. Transmission to humans occurs through contact with infected animals or contaminated environments, or through arthropod vectors. Tularemia has a broad geographical distribution, and there is evidence which suggests local emergence or re-emergence of this disease in Europe. This review was developed to provide an update on the geographical distribution of F. tularensis in humans, wildlife, domestic animals and vector species, to identify potential public health hazards, and to characterize the epidemiology of tularemia in Europe. Information was collated on cases in humans, domestic animals and wildlife, and on reports of detection of the bacterium in arthropod vectors, from 38 European countries for the period 1992-2012. Multiple international databases on human and animal health were consulted, as well as published reports in the literature. Tularemia is a disease of complex epidemiology that is challenging to understand and therefore to control. Many aspects of this disease remain poorly understood. Better understanding is needed of the epidemiological role of animal hosts, potential vectors, mechanisms of maintenance in the different ecosystems, and routes of transmission of the disease.

Livestock Helminths in a Changing Climate: Approaches and Restrictions to Meaningful Predictions.

Simple Summary Parasitic helminths represent one of the most pervasive challenges to livestock, and their intensity and distribution will be influenced by climate change. There is a need for long-term predictions to identify potential risks and highlight opportunities for control. We explore the approaches to modelling future helminth risk to livestock under climate change. One of the limitations to model creation is the lack of purpose driven data collection. We also conclude that models need to include a broad view of the livestock system to generate meaningful predictions. Abstract Climate change is a driving force for livestock parasite risk. This is especially true for helminths including the nematodes Haemonchus contortus, Teladorsagia circumcincta, Nematodirus battus, and the trematode Fasciola hepatica, since survival and development of free-living stages is chiefly affected by temperature and moisture. The paucity of long term predictions of helminth risk under climate change has driven us to explore optimal modelling approaches and identify current bottlenecks to generating meaningful predictions. We classify approaches as correlative or mechanistic, exploring their strengths and limitations. Climate is one aspect of a complex system and, at the farm level, husbandry has a dominant influence on helminth transmission. Continuing environmental change will necessitate the adoption of mitigation and adaptation strategies in husbandry. Long term predictive models need to have the architecture to incorporate these changes. Ultimately, an optimal modelling approach is likely to combine mechanistic processes and physiological thresholds with correlative bioclimatic modelling, incorporating changes in livestock husbandry and disease control. Irrespective of approach, the principal limitation to parasite predictions is the availability of active surveillance data and empirical data on physiological responses to climate variables. By combining improved empirical data and refined models with a broad view of the livestock system, robust projections of helminth risk can be developed.

Modelling Parasite Transmission in a Grazing System: The Importance of Host Behaviour and Immunity

Parasitic helminths present one of the most pervasive challenges to grazing herbivores. Many macro-parasite transmission models focus on host physiological defence strategies, omitting more complex interactions between hosts and their environments. This work represents the first model that integrates both the behavioural and physiological elements of gastro-intestinal nematode transmission dynamics in a managed grazing system. A spatially explicit, individual-based, stochastic model is developed, that incorporates both the hosts’ immunological responses to parasitism, and key grazing behaviours including faecal avoidance. The results demonstrate that grazing behaviour affects both the timing and intensity of parasite outbreaks, through generating spatial heterogeneity in parasite risk and nutritional resources, and changing the timing of exposure to the parasites’ free-living stages. The influence of grazing behaviour varies with the host-parasite combination, dependent on the development times of different parasite species and variations in host immune response. Our outputs include the counterintuitive finding that under certain conditions perceived parasite avoidance behaviours (faecal avoidance) can increase parasite risk, for certain host-parasite combinations. Through incorporating the two-way interaction between infection dynamics and grazing behaviour, the potential benefits of parasite-induced anorexia are also demonstrated. Hosts with phenotypic plasticity in grazing behaviour, that make grazing decisions dependent on current parasite burden, can reduce infection with minimal loss of intake over the grazing season. This paper explores how both host behaviours and immunity influence macro-parasite transmission in a spatially and temporally heterogeneous environment. The magnitude and timing of parasite outbreaks is influenced by host immunity and behaviour, and the interactions between them; the incorporation of both regulatory processes is required to fully understand transmission dynamics. Understanding of both physiological and behavioural defence strategies will aid the development of novel approaches for control.

Climate-driven tipping-points could lead to sudden, high-intensity parasite outbreaks.

Parasitic nematodes represent one of the most pervasive and significant challenges to grazing livestock, and their intensity and distribution are strongly influenced by climate. Parasite levels and species composition have already shifted under climate change, with nematode parasite intensity frequently low in newly colonized areas, but sudden large-scale outbreaks are becoming increasingly common. These outbreaks compromise both food security and animal welfare, yet there is a paucity of predictions on how climate change will influence livestock parasites. This study aims to assess how climate change can affect parasite risk. Using a process-based approach, we determine how changes in temperature-sensitive elements of outbreaks influence parasite dynamics, to explore the potential for climate change to influence livestock helminth infections. We show that changes in temperate-sensitive parameters can result in nonlinear responses in outbreak dynamics, leading to distinct ‘tipping-points’ in nematode parasite burdens. Through applying two mechanistic models, of varying complexity, our approach demonstrates that these nonlinear responses are robust to the inclusion of a number of realistic processes that are present in livestock systems. Our study demonstrates that small changes in climatic conditions around critical thresholds may result in dramatic changes in parasite burdens.

Counterintuitive increase in observed Mycobacterium avium subspecies paratuberculosis prevalence in sympatric rabbits following the introduction of paratuberculosis control measures in cattle

Paratuberculosis (Johne’s disease) is caused by the bacterium Mycobacterium avium subspecies paratuberculosis (Map). Achieving herd-level control of mycobacterial infection is notoriously difficult, despite widespread adoption of test-and-cull-based control strategies. The presence of infection in wildlife populations could be contributing to this difficulty. Rabbits are naturally infected with the same Map strain as cattle, and can excrete high levels in their faeces. The aim of this study is to determine if implementation of paratuberculosis control in cattle leads to a decline in Map infection levels in rabbits. An island-wide, test-and-cull-based paratuberculosis control programme was initiated on a Scottish island in 2008. In this study annual tests were obtained from 15 cattle farms, from 2008 to 2011, totalling 2609 tests. Rabbits (1564) were sampled from the 15 participating farms, from 2008 to 2011, and Map was detected by faecal culture. Map seroprevalence in cattle decreased from 16 to 7.2 per cent, while Map prevalence in rabbits increased from 10.3 to 20.3 per cent. Results indicate that efforts to control paratuberculosis in cattle do not reduce Map levels in sympatric rabbits. This adds to mounting evidence that if Map becomes established in wild rabbit populations, rabbits represent a persistent and widespread source of infection, potentially impeding livestock control strategies.

Ubiquitous parasites drive a 33% increase in methane yield from livestock

Of anthropogenic methane emissions, 40% can be attributed to agriculture, the majority of which are from enteric fermentation in livestock. With international commitments to tackle drivers of climate change, there is a need to lower global methane emissions from livestock production. Gastrointestinal helminths (parasitic worms) are globally ubiquitous and represent one of the most pervasive challenges to the health and productivity of grazing livestock. These parasites influence a number of factors affecting methane emissions including feed efficiency, nutrient use, and production traits. However, their effects on methane emissions are unknown. This is to our knowledge the first study that empirically demonstrates disease-driven increases in methane (CH4) yield in livestock (grams of CH4 per kg of dry matter intake). We do this by measuring methane emissions (in respiration chambers), dry matter intake, and production parameters for parasitised and parasite-free lambs. This study shows that parasite infections in lambs can lead to a 33% increase in methane yield (g CH4/kg DMI). This knowledge will facilitate more accurate calculations of the true environmental costs of parasitism in livestock, and reveals the potential benefits of mitigating emission through controlling parasite burdens.