Hannah Rose

Modelling the impact of climate change on spatial patterns of disease risk: sheep blowfly strike by Lucilia sericata in Great Britain.

Understanding the spatial scale and temporal pattern of disease incidence is a fundamental prerequisite for the development of appropriate management and intervention strategies. It is particularly critical, given the need to understand the elevated risks linked to climate change, to allow the most likely changes in the distribution of parasites and disease vectors to be predicted under a range of climate change scenarios. Using statistical models, the spatial distribution and climatic correlates of a range of parasites and diseases have been mapped previously, but their development into dynamic, predictive tools is less common. The aim of the work described here, was to use a species distribution model to characterise the environmental determinants of the monthly occurrence of ovine cutaneous myiasis (blowfly strike) by Lucilia sericata, the most frequent primary agent of northern European myiasis, and to then use this model to describe the potential spatial changes that might be expected in response to predicted climate change in Great Britain. The model predicts that the range of elevated temperatures predicted by current climate change scenarios will result in an increase in the risk of strike and an elongated blowfly season. However, even for the most rapid warming scenario predictions over the next 70 years, strike is not predicted to occur throughout the winter. Nevertheless, in this latter case, parts of central and southern England are likely to become too hot and dry for strike by L. sericata, to persist in mid-summer. Under these conditions, it is possible that other, more pathogenic Mediterranean agents of myiasis, such as Wolfhartia magnifica, could potentially replace L. sericata. Where the phenology of strike is altered by climate change, as predicted here, significant changes to the timing and frequency of parasite treatments and husbandry practices, such as shearing, will be required to manage the problem. The results suggest that the modelling approach adopted here could be usefully applied to a range of disease systems.

Mapping risk foci for endemic sheep scab.

Psoroptic mange in sheep, resulting from infestation by the astigmatid mite Psoroptes ovis, is increasingly prevalent in Europe and other parts of the world. As a step towards improved national control, regional or local scab management programmes that target high-risk areas and aim to maintain the number of outbreaks below an acceptable level may be an effective initial use of time and resource. To facilitate such a management approach, in this paper scab outbreak farms are identified using a questionnaire survey of sheep farmers, the data from which are then used to build a national scab risk model for Great Britain. The questionnaire results indicate a national prevalence of scab, between March 2007 and February 2008, of 8.6% (+/-1.98). However, previous exposure to sheep scab significantly affected the respondents probability of reporting a scab outbreak during the survey period (chi(2)=53.2, d.f.=1, P<0.001); 85% of the farms that reported at least one scab outbreak had experienced outbreaks in previous years, 27% had experienced outbreaks in more than five of the previous 10 years. In contrast, 76% of farms that did not report scab had not had a previous outbreak. The highest prevalence areas were in Northern England, Wales, Southwest England and Scotland. Modelling the distribution of the reported scab outbreaks identified height above sea level, temperature and rainfall as significant predictors of the probability of an outbreak, superimposed on an underlying pattern of sheep abundance. It is argued that scab management programmes directed at these foci have the potential to allow a more targeted approach to scab control and significantly reduce the prevalence of scab in the UK and other European countries.

Livestock ectoparasites: Integrated management in a changing climate

The prevalence of livestock ectoparasites is the result of a complex interaction of factors such as parasite and host abundance, host susceptibility, climate and, critically, farmer husbandry and intervention strategies, all of which change seasonally in space and time. Given the complexity of the interacting factors, the effects of any climate change on disease incidence are hard to predict, as accordingly are the optimal husbandry responses required to ameliorate any effects. Here cutaneous myiasis in sheep, by the blowfly Lucilia sericata in the United Kingdom, is used to highlight the impact of a range of such issues. Cutaneous myiasis would be expected to be highly sensitive to even small changes in climate and therefore provides a good model to illustrate the problems inherent in attempting to predict the effect of climate change on livestock disease incidence. Both simulation and spatial species distribution models, show that the range of elevated temperatures predicted by current climate change scenarios are likely to result in an elongated blowfly season with earlier spring emergence and a higher cumulative incidence of strike. Strike incidence would be expected to increase, particularly for ewes in early summer. However, under higher IPCC emissions senarios (+3 °C), parts of central and southern England may become too hot and dry for strike by L. sericata to persist in mid-summer. Under these conditions, it is possible that other, more pathogenic Mediterranean agents of myiasis, such as Wohlfahrtia magnifica could replace L. sericata. Nevertheless, the models suggest that simple changes in some husbandry practices, such as shearing or trap use, could have an important effect in reducing early season ewe strike incidences by L. sericata. The work reviewed here, suggests that climate warming is likely to increase the risk of fly strike incidence, with consequent animal welfare and economic problems. However, practical measures exist which, with modest changes in husbandry practices, should be able to manage expected increases in strike, under the range of climate changes currently predicted. The work demonstrates that attempts to predict the likely impact of climate change on disease incidence must take into account changes in farmer behaviour and animal management practices as well as parasite biology.

The parasitic phase of Ostertagia ostertagi: quantification of the main life history traits through systematic review and meta-analysis.

Predictive models of parasite life cycles increase our understanding of how parasite epidemiology is influenced by global changes and can be used to support decisions for more targeted worm control. Estimates of parasite population dynamics are needed to parameterize such models. The aim of this study was to quantify the main life history traits of Ostertagia ostertagi, economically the most important nematode of cattle in temperate regions. The main parameters determining parasite density during the parasitic phase of O. ostertagi are (i) the larval establishment rate, (ii) hypobiosis rate, (iii) adult mortality and (iv) female fecundity (number of eggs laid per day per female). A systematic review was performed covering studies from 1962 to 2007, in which helminth-naïve calves were artificially infected with O. ostertagi. The database was further extended with results of unpublished trials conducted at the Laboratory for Parasitology of Ghent University, Belgium. Overall inverse variance weighted estimates were computed for each of the traits through random effects models. An average establishment rate (±S.E.) of 0.269±0.022 was calculated based on data of 27 studies (46 experiments). The establishment rate declined when infection dose increased and was lower in younger animals. An average proportion of larvae entering hypobiosis (±S.E.) of 0.041 (±0.009) was calculated based on 27 studies (54 experiments). The proportion of ingested larvae that went into hypobiosis was higher in animals that received concomitant infections with nematode species other than O. ostertagi (mixed infections). An average daily adult mortality (±S.E.) of 0.028 (±0.002) was computed based on data from 28 studies (70 experiments). Adult mortality was positively correlated with infection dose. A daily fecundity (±S.E.) of 284 (±45) eggs per female was found based on nine studies (10 experiments). The average female sex ratio of O. ostertagi based on individual animal data (n=75) from six different studies was estimated to be 0.55. We believe that this systematic review is the first to summarise the available data on the main life history traits of the parasitic phase of O. ostertagi. In conclusion, this meta-analysis provides novel estimates for the parameterization of life cycle-based transmission models, explicitly reports measures of variance around these estimates, gives evidence for density dependence of larval establishment and adult mortality, shows that host age affects larval establishment and, to our knowledge, provides the first evidence for O. ostertagi of a female-biased sex ratio.

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

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.

Exploiting parallels between livestock and wildlife: Predicting the impact of climate change on gastrointestinal nematodes in ruminants

Global change, including climate, policy, land use and other associated environmental changes, is likely to have a major impact on parasitic disease in wildlife, altering the spatio-temporal patterns of transmission, with wide-ranging implications for wildlife, domestic animals, humans and ecosystem health. Predicting the potential impact of climate change on parasites infecting wildlife will become increasingly important in the management of species of conservation concern and control of disease at the wildlife-livestock and wildlife-human interface, but is confounded by incomplete knowledge of host-parasite interactions, logistical difficulties, small sample sizes and limited opportunities to manipulate the system. By exploiting parallels between livestock and wildlife, existing theoretical frameworks and research on livestock and their gastrointestinal nematodes can be adapted to wildlife systems. Similarities in the gastrointestinal nematodes and the life-histories of wild and domestic ruminants, coupled with a detailed knowledge of the ecology and life-cycle of the parasites, render the ruminant-GIN host-parasite system particularly amenable to a cross-disciplinary approach.

The basic reproduction quotient (Q0) as a potential spatial predictor of the seasonality of ovine haemonchosis.

Haemonchus contortus is a gastrointestinal nematode parasite of small ruminants, which feeds on blood and causes significant disease and production loss in sheep and goats, especially in warmer parts of the world. The life cycle includes free-living immature stages, which are subject to climatic influences on development, survival and availability, and this species therefore exhibits spatio-temporal heterogeneity in its infection pressure based on the prevailing climate. Models that better explain this heterogeneity could predict future epidemiological changes. The basic reproduction quotient (Q0) was used as a simple process-based model to predict climate-driven changes in the potential transmission of H. contortus across widely different geo-climatic zones, and showed good agreement with the observed frequency of this species in the gastrointestinal nematode fauna of sheep (r = 0.81, P <0.01). Averaged monthly Q0 output was further used within a geographical information system (GIS) to produce preliminary haemonchosis risk maps for the United Kingdom (UK) over a four-year historical span and under future climate change scenarios. Prolonged transmission seasons throughout the UK are predicted, especially in the south although with restricted transmission in peak summer due to rainfall limitation. Additional predictive ability might be achieved if information such as host density and distribution, grazing pattern and edaphic conditions were included as risk layers in the GIS-based risk map. However, validation of such risk maps presents a significant challenge, with georeferenced observed data of sufficient spatial and temporal resolution rarely available and difficult to obtain.

Cattle and Nematodes Under Global Change: Transmission Models as an Ally

Nematode infections are an important economic constraint to cattle farming. Future risk levels and transmission dynamics will be affected by changes in climate and farm management. The prospect of altered parasite epidemiology in combination with anthelmintic resistance requires the adaptation of current control approaches. Mathematical models that simulate disease dynamics under changing climate and farm management can help to guide the optimization of helminth control strategies. Recent efforts have increasingly employed such models to assess the impact of predicted climate scenarios on future infection pressure for gastrointestinal nematodes (GINs) in cattle, and to evaluate possible adaptive control measures. This review aims to consolidate progress in this field to facilitate further modeling and application.

Modelling Cooperia oncophora: Quantification of key parameters in the parasitic phase.

Cooperia oncophora is one of the most common intestinal nematodes in cattle. It is also the dose-limiting species for the most frequently used anthelmintics, and consequently, the species usually involved in reports of anthelmintic resistance. However, little information is available on its population dynamics, hindering the parameterisation of transmission models to support understanding of the impact of anthelmintic resistance, climate change and alternative control strategies on nematode epidemiology. This systematic review and meta-analysis provides estimates for key life history traits of the parasitic phase of C. oncophora and investigates potential influences of acquired immunity on these traits.

Pathogenicity of biological control agents for livestock ectoparasites: a simulation analysis.

The management of arthropod ectoparasites of livestock currently relies largely on the use of neurotoxic chemicals. However, concerns over the development of resistance, as well as operator and environmental contamination, have stimulated research into alternative approaches to their control, including the use of biological pathogens. The search for suitable pathogens often focuses on identifying the most highly virulent agents for application. However, practical issues such as the ability of a pathogen to penetrate to the skin through hair or wool, tolerance of high skin surface temperatures and high residual activity may mean that the most virulent pathogens are not necessarily the most appropriate for commercial application. Here, a simulation model is constructed and used to highlight a range of key features which characterize suitable pathogens for such application. Sensitivity analysis shows that even a relatively low probability of infection following contact between infectious and susceptible individuals may give acceptable control, providing it is counterbalanced by higher survival of both infected and infectious parasite hosts in order to allow the rate of transmission to exceed the threshold required to suppress parasite population growth. The model highlights the need for studies attempting to identify sustainable biocontrol agents to explore the use of pathogens which have a range of the characteristics that contribute to overall pathogenicity, but which are also most compatible with practical application systems.