Effect of deer density on tick infestation of rodents and the hazard of tick-borne encephalitis. II: Population and infection models

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Evidence of the Importance of Host Habitat Use in Predicting the Dilution Effect of Wild Boar for Deer Exposure to Anaplasma spp

Foci of tick-borne pathogens occur at fine spatial scales, and depend upon a complex arrangement of factors involving climate, host abundance and landscape composition. It has been proposed that the presence of hosts that support tick feeding but not pathogen multiplication may dilute the transmission of the pathogen. However, models need to consider the spatial component to adequately explain how hosts, ticks and pathogens are distributed into the landscape

Persistence of Pathogens with Short Infectious Periods in Seasonal Tick Populations: The Relative Importance of Three Transmission Routes

BACKGROUND: The flaviviruses causing tick-borne encephalitis (TBE) persist at low but consistent levels in tick populations, despite short infectious periods in their mammalian hosts and transmission periods constrained by distinctly seasonal tick life cycles. In addition to systemic and vertical transmission, cofeeding transmission has been proposed as an important route for the persistence of TBE-causing viruses. Because cofeeding transmission requires ticks to feed simultaneously, the timing of tick activity may be critical to pathogen persistence. Existing models of tick-borne diseases do not incorporate all transmission routes and tick seasonality. Our aim is to evaluate the influence of seasonality on the relative importance of different transmission routes by using a comprehensive mathematical model. METHODOLOGY/PRINCIPAL FINDINGS: We developed a stage-structured population model that includes tick seasonality and evaluated the relative importance of the transmission routes for pathogens with short infectious periods, in particular Powassan virus (POWV) and the related "deer tick virus," emergent encephalitis-causing flaviviruses in North America. We used the next generation matrix method to calculate the basic reproductive ratio and performed elasticity analyses. We confirmed that cofeeding transmission is critically important for such pathogens to persist in seasonal tick populations over the reasonable range of parameter values. At higher but still plausible rates of vertical transmission, our model suggests that vertical transmission can strongly enhance pathogen prevalence when it operates in combination with cofeeding transmission. CONCLUSIONS/SIGNIFICANCE: Our results demonstrate that the consistent prevalence of POWV observed in tick populations could be maintained by a combination of low vertical, intermediate cofeeding and high systemic transmission rates. When vertical transmission is weak, nymphal ticks support integral parts of the transmission cycle that are critical for maintaining the pathogen. We also extended the model to pathogens that cause chronic infections in hosts and found that cofeeding transmission could contribute to elevating prevalence even in these systems. Therefore, the common assumption that cofeeding transmission is not relevant in models of chronic host infection, such as Lyme disease, could lead to underestimating pathogen prevalence

Landscape structure affects the prevalence and distribution of a tick-borne zoonotic pathogen

Background Landscape structure can affect pathogen prevalence and persistence with consequences for human and animal health. Few studies have examined how reservoir host species traits may interact with landscape structure to alter pathogen communities and dynamics. Using a landscape of islands and mainland sites we investigated how natural landscape fragmentation affects the prevalence and persistence of the zoonotic tick-borne pathogen complex Borrelia burgdorferi(sensu lato), which causes Lyme borreliosis. We hypothesized that the prevalence of B. burgdorferi (s.l.) would be lower on islands compared to the mainland and B. afzelii, a small mammal specialist genospecies, would be more affected by isolation than bird-associated B. garinii and B. valaisiana and the generalist B. burgdorferi (sensu stricto). Methods Questing (host-seeking) nymphal I. Ricinus ticks (n = 6567) were collected from 12 island and 6 mainland sites in 2011, 2013 and 2015 and tested for B. burgdorferi(s.l.). Deer abundance was estimated using dung transects. Results The prevalence of B. burgdorferi (s.l.) was significantly higher on the mainland (2.5%, 47/1891) compared to island sites (0.9%, 44/4673) (P < 0.01). While all four genospecies of B. burgdorferi (s.l.) were detected on the mainland, bird-associated species B. garinii and B. valaisiana and the generalist genospecies B. burgdorferi(s.s.) predominated on islands. Conclusion We found that landscape structure influenced the prevalence of a zoonotic pathogen, with a lower prevalence detected among island sites compared to the mainland. This was mainly due to the significantly lower prevalence of small mammal-associated B. afzelii. Deer abundance was not related to pathogen prevalence, suggesting that the structure and dynamics of the reservoir host community underpins the observed prevalence patterns, with the higher mobility of bird hosts compared to small mammal hosts leading to a relative predominance of the bird-associated genospecies B. garinii and generalist genospecies B. burgdorferi (s.s.) on islands. In contrast, the lower prevalence of B. afzelii on islands may be due to small mammal populations there exhibiting lower densities, less immigration and stronger population fluctuations. This study suggests that landscape fragmentation can influence the prevalence of a zoonotic pathogen, dependent on the biology of the reservoir host

Habitat properties are key drivers of Borrelia burgdorferi (s.l.) prevalence in Ixodes ricinus populations of deciduous forest fragments

Background: The tick Ixodes ricinus has considerable impact on the health of humans and other terrestrial animals because it transmits several tick-borne pathogens (TBPs) such as B. burgdorferi (sensu lato), which causes Lyme borreliosis (LB). Small forest patches of agricultural landscapes provide many ecosystem services and also the disservice of LB risk. Biotic interactions and environmental filtering shape tick host communities distinctively between specific regions of Europe, which makes evaluating the dilution effect hypothesis and its influence across various scales challenging. Latitude, macroclimate, landscape and habitat properties drive both hosts and ticks and are comparable metrics across Europe. Therefore, we instead assess these environmental drivers as indicators and determine their respective roles for the prevalence of B. burgdorferi in I. ricinus. Methods: We sampled I. ricinus and measured environmental properties of macroclimate, landscape and habitat quality of forest patches in agricultural landscapes along a European macroclimatic gradient. We used linear mixed models to determine significant drivers and their relative importance for nymphal and adult B. burgdorferi prevalence. We suggest a new prevalence index, which is pool-size independent. Results: During summer months, our prevalence index varied between 0 and 0.4 per forest patch, indicating a low to moderate disservice. Habitat properties exerted a fourfold larger influence on B. burgdorferi prevalence than macroclimate and landscape properties combined. Increasingly available ecotone habitat of focal forest patches diluted and edge density at landscape scale amplified B. burgdorferi prevalence. Indicators of habitat attractiveness for tick hosts (food resources and shelter) were the most important predictors within habitat patches. More diverse and abundant macro- and microhabitat had a diluting effect, as it presumably diversifies the niches for tick-hosts and decreases the probability of contact between ticks and their hosts and hence the transmission likelihood.[br/] Conclusions: Diluting effects of more diverse habitat patches would pose another reason to maintain or restore high biodiversity in forest patches of rural landscapes. We suggest classifying habitat patches by their regulating services as dilution and amplification habitat, which predominantly either decrease or increase B. burgdorferi prevalence at local and landscape scale and hence LB risk. Particular emphasis on promoting LB-diluting properties should be put on the management of those habitats that are frequently used by humans. In the light of these findings, climate change may be of little concern for LB risk at local scales, but this should be evaluated further

Modeling West Nile virus Ecology

The main objectives of the work-package "Modeling West Nile virus Ecology” are to evaluate the effect of temperature on West Nile virus (WNV) transmission potential and the emergence of new foci, to identify the primary reservoir host species and their relative competence to WNV transmission, to assess the impact of host heterogeneity on WNV amplification for various lineages and genotypes, to evaluate the interactions of WNV with other mosquito-infecting viruses, and to integrate these data into a mathematical model to determine how hosts, vectors and pathogens might interact dynamically. Here I present the results concerning the effect of some environmental variables on mosquito population dynamics. The mosquitoes dataset include longitudinal sampling of Culex pipiens adult females collected from 2000 to 2011 in Piedmont region, North-western Italy. We found that the onset of mosquito activity and total mosquito abundance are well explained by some early predictors that concern only climatic and environmental conditions that take place during the spring season. Specifically, the onset is well predicted by weekly cumulated temperature till half of May while total abundance is well predicted by the speed of temperature increase in spring and by total precipitation during spring. In addition, total mosquito abundance is also influenced by the distance of the mosquito trap to urban sites

Deer density drives tick infestation pattern on rodents and TBE hazard: empirical and theoretical investigations

Tick-borne encephalitis (TBE) is an emerging zoonotic disease reported in several European and Asiatic countries with complex transmission routes that involve various host species. Understanding and quantifying the contribution of the different hosts involved in the TBE virus (TBEV) cycle is crucial to estimating the threshold conditions for virus emergence and spread. Some hosts, such as rodents, act as both feeding host for ticks and reservoir of the infection. Other species, such as deer, provide important sources of blood for feeding ticks, but they do not support TBEV transmission, acting instead as dead-end (i.e. incompetent) hosts. The aim of this study was to estimate the contribution of the main ungulate tick hosts to the pattern of tick infestation on rodents, and to TBEV occurrence in rodents and questing adult ticks. In the empirical study, we compared areas where endemic human TBE occurs, with control sites having no reported human TBE cases. In these six sample sites located in Italy and Slovakia, we assessed deer density using the pellet group count-plot sampling technique, collected questing ticks by dragging, live-trapped rodents (primarily Apodemus flavicollis and Myodes glareolus) and counted ticks feeding on rodents. Both rodents and adult ticks were screened for TBEV infection. TBEV infection in ticks and rodents was positively associated with the number of co-feeding ticks on rodents and negatively correlated with deer density. We hypothesize that the negative relationship between deer density and TBEV occurrence could be attributed to deer (non competent hosts) diverting questing ticks from rodents (competent hosts). In fact, we observed that, after an initial increase, the number of ticks feeding on rodents reaches a peak for an intermediate value of deer density and then decreases. In order to validate and interpret in a robust theoretical framework the empirical findings regarding the effect of deer density on tick infestation on rodents and TBEV occurrence, we introduce an eco-epidemiological model to explore the dynamics of tick population and TBEV infection. Model results show hump-shaped relationships between deer density and both feeding tick on rodents and the basic reproduction number for TBEV. This suggests that deer may act as tick amplifiers, but may also divert tick bites from competent hosts, thus diluting pathogen transmission. However, our model shows that the mechanism responsible for the dilution effect is more complex than the simple reduction of tick burden on competent hosts. In fact, while the number of feeding ticks on rodents may increase with deer density, the proportion of blood meals on competent compared to incompetent hosts may decrease, triggering infection decline. As a consequence, using just the number of ticks per rodent as a TBE risk predictor could be misleading if competent hosts share habitat with incompetent hosts

Effects of tick population dynamics and host densities on the persistence of tick-borne infections

The transmission and the persistence of tick-borne infections are strongly influenced by the densities and the structure of host populations. By extending previous models and analysis, in this paper we analyse how the persistence of ticks and pathogens, is affected by the dynamics of tick populations, and by their host densities. The effect of host densities on infection persistence is explored through the analysis and simulation of a series of models that include different assumptions on tick–host dynamics and consider different routes of infection transmission. Ticks are assumed to feed on two types of host species which vary in their reservoir competence. Too low densities of competent hosts (i.e., hosts where transmission can occur) do not sustain the infection cycle, while too high densities of incompetent hosts may dilute the competent hosts so much to make infection persistence impossible. A dilution effect may occur also for competent hosts as a consequence of reduced tick to host ratio; this is possible only if the regulation of tick populations is such that tick density does not increase linearly with host densitie

Modelling the impact of helminth parasite on rock partridge population dynamics

The aim of this work was to explore the effect of helminth parasites on rock partridge (Alectoris graeca saxatilis) population dynamics in the Dolomitic Alps (northern Italy). Specifically, we investigated the hypothesis that the nematode parasite Ascaridia compar can drive population cycles in rock partridge dynamics. In order to support this hypothesis, we compared the predictions obtained from a hostmacroparasite interaction model with multi-annual empirical data of A. compar infection in natural host populations. We estimated host demographic parameters from rock partridge census data, and the parasitological parameters from a series of experimental infections in a rock partridge captive population. Our model predicts higher levels of A. compar infestation for rock partridge population with a cyclic dynamics respect to those with a non-cyclic dynamics. In addition, for populations exhibiting cyclic dynamics, the model predicts a positive correlation between the mean parasite burden and the length of cycle period. Model predictions are well-supported by field data; in fact, a significant differences in parasite infection between cyclic and non cyclic populations and within cyclic populations with different oscillation periods were observed. On the basis of these results, we conclude that helminth parasites can be a possible driver for rock partridge population dynamics and must be considered when planning conservation strategies of this threatened species