David Pleydell

Drivers of Echinococcus multilocularis transmission in China: small mammal diversity, landscape or climate?

Background Human alveolar echinococcocosis (AE) is a highly pathogenic zoonotic disease caused by the larval stage of the cestode E. multilocularis. Its life-cycle includes more than 40 species of small mammal intermediate hosts. Therefore, host biodiversity losses could be expected to alter transmission. Climate may also have possible impacts on E. multilocularis egg survival. We examined the distribution of human AE across two spatial scales, (i) for continental China and (ii) over the eastern edge of the Tibetan plateau. We tested the hypotheses that human disease distribution can be explained by either the biodiversity of small mammal intermediate host species, or by environmental factors such as climate or landscape characteristics. Methodology/findings The distributions of 274 small mammal species were mapped to 967 point locations on a grid covering continental China. Land cover, elevation, monthly rainfall and temperature were mapped using remotely sensed imagery and compared to the distribution of human AE disease at continental scale and over the eastern Tibetan plateau. Infection status of 17,589 people screened by abdominal ultrasound in 2002–2008 in 94 villages of Tibetan areas of western Sichuan and Qinghai provinces was analyzed using generalized additive mixed models and related to epidemiological and environmental covariates. We found that human AE was not directly correlated with small mammal reservoir host species richness, but rather was spatially correlated with landscape features and climate which could confirm and predict human disease hotspots over a 200,000 km2 region. Conclusions/Significance E. multilocularis transmission and resultant human disease risk was better predicted from landscape features that could support increases of small mammal host species prone to population outbreaks, rather than host species richness. We anticipate that our study may be a starting point for further research wherein landscape management could be used to predict human disease risk and for controlling this zoonotic helminthic.

Landscape composition and spatial prediction of alveolar echinococcosis in Southern Ningxia, China

Background Alveolar echinococcosis (AE) presents a serious public health challenge within China. Mass screening ultrasound surveys can detect pre-symptomatic AE, but targeting areas identified from hospital records is inefficient regarding AE. Prediction of undetected or emerging hotspots would increase detection rates. Voles and lemmings of the subfamily Arvicolinae are important intermediate hosts in sylvatic transmission systems. Their populations reach high densities in productive grasslands where food and cover are abundant. Habitat availability is thought to affect arvicoline population dynamic patterns and definitive host–intermediate host interactions. Arvicoline habitat correlates with AE prevalence in Western Europe and southern Gansu Province, China. Methods and Findings Xiji County, Ningxia Hui Autonomous Region, borders southern Gansu. The aims of this study were to map AE prevalence across Xiji and test arvicoline habitat as a predictor. Land cover was mapped using remotely sensed (Landsat) imagery. Infection status of 3,205 individuals screened in 2002–2003 was related, using generalised additive mixed models, to covariates: gender; farming; ethnicity; dog ownership; water source; and areal cover of mountain pasture and lowland pasture. A Markov random field modelled additional spatial variation and uncertainty. Mountain pasture and lowland pasture were associated with below and above average AE prevalence, respectively. Conclusions Low values of the normalised difference vegetation index indicated sub-optimality of lowland pasture for grassland arvicolines. Unlike other known endemic areas, grassland arvicolines probably did not provide the principal reservoir for Echinococcus multilocularis in Xiji. This result is consistent with recent small mammal surveys reporting low arvicoline densities and high densities of hamsters, pikas and jerboas, all suitable intermediate hosts for E. multilocularis, in reforested lowland pasture. The risk of re-emergence is discussed. We recommend extending monitoring to: southern Haiyuan County, where predicted prevalence was high; southern Xiji County, where prediction uncertainty was high; and monitoring small mammal community dynamics and the infection status of dogs.

Using long-term monitoring of red fox populations to assess changes in rodent control practices

Pest control is a global issue for agriculture, health, biodiversity conservation and economy. Anticoagulant rodenticides are used over large areas to control rodent pests and can cause widespread poisoning of nontarget wildlife. In France, bromadiolone is the only pesticide authorized to control the water vole Arvicola terrestris Scherman, in grasslands. Since 2001, legislation has been in place to replace curative treatments by preventive ones and limit the quantity of rodenticide used. As the legislation took effect over time, the impact on red fox Vulpes vulpes populations was monitored. Fox populations and bromadiolone treatments were monitored in the Doubs Department (5000 km² area), France. Fox counts were carried out during spring, and vole control was primarily conducted in autumn. Relative fox densities (Kilometric Abundance Index: KAI) obtained per commune for year n (2004-2009) were related to treatments achieved during year n−1 (2003-2008). Treatments from year n−2 were used to investigate possible delayed responses in fox populations. Kilometric Abundance Index of foxes was significantly related to treatment intensities in years n−1 and n−2. The impact was greatest in a large area (>1000 km²), where intensive treatments were achieved in 2003. Fox KAI generally remained dramatically low in this area until 2005, after which a partial recovery was observed. The same area was treated again from 2006 to 2008 but with only half the amount of bait per hectare that was used in 2003. These treatments were followed by a moderate decrease in fox populations. Synthesis and applications: We have established, for the first time on a regional scale, the negative impact of a rodenticide on fox populations. We have shown that a shift to preventive treatments with reduced anticoagulant rodenticide use is less harmful to fox populations. However, to approach a zero impact, treatments should be reduced further by limitation of bait quantities authorized per hectare and per commune and using alternative methods to chemical control. Long-term monitoring of wildlife populations using index methods can provide valuable information about the adverse effects of pesticides; therefore, we recommend their inclusion in the assessment of pest management practices.

Small-mammal assemblage response to deforestation and afforestation in central China

Abstract Deforestation is a major environmental issue driving the loss of animal and plant species. Afforestation has recently been promoted to conserve and restore Chinese forest ecosystems. We investigated the distribution of small-mammal assemblages in an area where forest and associated deforestation habitats dominate, and in an agricultural area where afforestation is ongoing in the Loess Plateau of southern Ningxia Autonomous Region, P.R. China. Multiple trapping was used. Assemblages were defined based on the multinomial probability distribution and information theory. Species turnover between assemblages of deforested and afforested habitats was high, although no clear effect on species richness was observed. The two assemblages described along the deforestation gradient displayed higher diversity, whereas diversity was lower in assemblages identified in afforested habitats where Cricetulus longicaudatus, a known agricultural pest in various areas of China, clearly dominated. The threatened Sorex cylindricauda and Eozapus setchuanus were recorded along the deforestation gradient but not in plantations. Therefore, habitats present along a deforestation succession in this part of Ningxia sustain a high diversity of small mammals and include species of conservation concern. At the present stage of its process (maximum 15 years), afforestation in southern Ningxia favours the dominance of an agricultural pest.

Parapatric distribution and sexual competition between two tick species, Amblyomma variegatum and A. hebraeum (Acari, Ixodidae), in Mozambique

BackgroundAmblyomma variegatum and A. hebraeum are two ticks of veterinary and human health importance in south-east Africa. In Zimbabwe they occupy parapatric (marginally overlapping and juxtaposed) distributions. Understanding the mechanisms behind this parapatry is essential for predicting the spatio-temporal dynamics of Amblyomma spp. and the impacts of associated diseases. It has been hypothesized that exclusive competition between these species results from competition at the levels of male signal reception (attraction-aggregation-attachment pheromones) or sexual competition for mates. This hypothesis predicts that the parapatry described in Zimbabwe could also be present in other countries in the region.MethodsTo explore this competitive exclusion hypothesis we conducted field surveys at the two species’ range limits in Mozambique to identify areas of sympatry (overlapping areas) and to study potential interactions (communicative and reproductive interference effects) in those areas. At sympatric sites, hetero-specific mating pairs were collected and inter-specific attractiveness/repellent effects acting at long and short distances were assessed by analyzing species co-occurrences on co-infested herds and co-infested hosts.ResultsCo-occurrences of both species at sampling sites were infrequent and localized in areas where both tick and host densities were low. At sympatric sites, high percentages of individuals of both species shared attachment sites on hosts and inter-specific mating rates were high. Although cross-mating rates were not significantly different for A. variegatum and A. hebraeum females, attraction towards hetero-specific males was greater for A. hebraeum females than for A. variegatum females and we observed small asymmetrical repellent effects between males at attachment sites.ConclusionsOur observations suggest near-symmetrical reproductive interference between A. variegatum and A. hebraeum, despite between-species differences in the strength of reproductive isolation barriers acting at the aggregation, fixation and partner contact levels. Theoretical models predict that sexual competition coupled with hybrid inviability, greatly reduces the probability of one species becoming established in an otherwise suitable location when the other species is already established. This mechanism can explain why the parapatric boundary in Mozambique has formed within an area of low tick densities and relatively infrequent host-mediated dispersal events.

Did Vaccination Slow the Spread of Bluetongue in France

Vaccination is one of the most efficient ways to control the spread of infectious diseases. Simulations are now widely used to assess how vaccination can limit disease spread as well as mitigate morbidity or mortality in susceptible populations. However, field studies investigating how much vaccines decrease the velocity of epizootic wave-fronts during outbreaks are rare. This study aimed at investigating the effect of vaccination on the propagation of bluetongue, a vector-borne disease of ruminants. We used data from the 2008 bluetongue virus serotype 1 (BTV-1) epizootic of southwest France. As the virus was newly introduced in this area, natural immunity of livestock was absent. This allowed determination of the role of vaccination in changing the velocity of bluetongue spread while accounting for environmental factors that possibly influenced it. The average estimated velocity across the country despite restriction on animal movements was 5.4 km/day, which is very similar to the velocity of spread of the bluetongue virus serotype 8 epizootic in France also estimated in a context of restrictions on animal movements. Vaccination significantly reduced the propagation velocity of BTV-1. In comparison to municipalities with no vaccine coverage, the velocity of BTV-1 spread decreased by 1.7 km/day in municipalities with immunized animals. For the first time, the effect of vaccination has been quantified using data from a real epizootic whilst accounting for environmental factors known to modify the velocity of bluetongue spread. Our findings emphasize the importance of vaccination in limiting disease spread across natural landscape. Finally, environmental factors, specifically those related to vector abundance and activity, were found to be good predictors of the velocity of BTV-1 spread, indicating that these variables need to be adequately accounted for when evaluating the role of vaccination on bluetongue spread.

Mixtures of GAMs for habitat suitability analysis with overdispersed presence/absence data

A new approach to species distribution modelling based on unsupervised classification via a finite mixture of GAMs incorporating habitat suitability curves is proposed. A tailored EM algorithm is outlined for computing maximum likelihood estimates. Several submodels incorporating various parameter constraints are explored. Simulation studies confirm, that under certain constraints, the habitat suitability curves are recovered with good precision. The method is also applied to a set of real data concerning presence/absence of observable small mammal indices collected on the Tibetan plateau. The resulting classification was found to correspond to species-level differences in habitat preference described in previous ecological work.

Towards understanding the impacts of environmental variation on Echinococcus multilocularis transmission

A key element in disease emergence/re-emergence is ecosystem disruption as a result of anthropogenic effects which may be as rapid as in forestry and agricultural changes. There is however difficulty in developing suitable models to study ecology of infectious diseases, wherein spatial determinants that meaningfully characterize wildlife reservoir habitat, can be linked in turn to host ecology and to dynamics of pathogen/parasite transmission. Spatial variables in the form of landscape and socio-economic characteristics should be linked to parasite transmission dynamics using an integrated modeling approach that takes into account multi-level heterogeneity at habitat, host and parasite domains and deterministic transmission parameters. The diversity of small mammals host communities and landscape worldwide offer a number of systems that sustain transmission of E. multilocularis at various time-space scales. It is expected that further advances will come from methods combining quantification of host communities from field surveys, landscape via remote sensing and parasite transmission via population screenings conducted on definitive hosts (e.g. dogs in villages in China or foxes in Europe) and humans, in a spatially explicit context. The combination of multi-level field approaches with modern regression techniques coupled with traditional transmission models provide a unique opportunity of investigating how a diversity of small mammal communities and anthropogenic landscapes can regulate parasite transmission.

Estimation of the dispersal distances of an aphid-borne virus in a patchy landscape

Characterising the spatio-temporal dynamics of pathogens in natura is key to ensuring their efficient prevention and control. However, it is notoriously difficult to estimate dispersal parameters at scales that are relevant to real epidemics. Epidemiological surveys can provide informative data, but parameter estimation can be hampered when the timing of the epidemiological events is uncertain, and in the presence of interactions between disease spread, surveillance, and control. Further complications arise from imperfect detection of disease and from the huge number of data on individual hosts arising from landscape-level surveys. Here, we present a Bayesian framework that overcomes these barriers by integrating over associated uncertainties in a model explicitly combining the processes of disease dispersal, surveillance and control. Using a novel computationally efficient approach to account for patch geometry, we demonstrate that disease dispersal distances can be estimated accurately in a patchy (i.e. fragmented) landscape when disease control is ongoing. Applying this model to data for an aphid-borne virus (Plum pox virus) surveyed for 15 years in 605 orchards, we obtain the first estimate of the distribution of flight distances of infectious aphids at the landscape scale. About 50% of aphid flights terminate beyond 90 m, which implies that most infectious aphids leaving a tree land outside the bounds of a 1-ha orchard. Moreover, long-distance flights are not rare–10% of flights exceed 1 km. By their impact on our quantitative understanding of winged aphid dispersal, these results can inform the design of management strategies for plant viruses, which are mainly aphid-borne.

A framework for estimating the effects of sequential reproductive barriers: implementation using Bayesian models with field data from cryptic species

Determining how reproductive barriers modulate gene flow between populations represents a major step towards understanding the factors shaping the course of speciation. Although many indices quantifying reproductive isolation (RI) have been proposed, they do not permit the quantification of cross direction-specific RI under varying species frequencies and over arbitrary sequences of barriers. Furthermore, techniques quantifying associated uncertainties are lacking, and statistical methods unrelated to biological process are still preferred for obtaining confidence intervals and p-values. To address these shortcomings, we provide new RI indices that model changes in gene flow for both directions of hybridization, and we implement them in a Bayesian model. We use this model to quantify RI between two species of the psyllid Cacopsylla pruni based on field genotypic data for mating individuals, inseminated spermatophores and progeny. The results showed that pre-insemination isolation was strong, mildly asymmetric and undistinguishably different between study sites despite large differences in species frequencies; that post-insemination isolation strongly affected the more common hybrid type; and that cumulative isolation was close to complete. In the light of these results, we discuss how these developments can strengthen comparative RI studies. Author contributions JP and NS initiated the study and obtained biological data. JP and DRJP developed the porosity-based approach. DRJP conceived the Bayesian implementation and code. JP, DRJP and NS wrote the manuscript. Data availability Mitochondrial sequence data will be available at Genbank, source code is available at xxx.