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      Distribution of ticks, tick-borne pathogens and the associated local environmental factors including small mammals and livestock, in two French agricultural sites: the OSCAR database

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          Abstract

          Background

          In Europe, ticks are major vectors of both human and livestock pathogens (e.g. Lyme disease, granulocytic anaplasmosis, bovine babesiosis). Agricultural landscapes, where animal breeding is a major activity, constitute a mosaic of habitat types of various quality for tick survival and are used at different frequencies by wild and domestic hosts across seasons. This habitat heterogeneity, in time and space, conditions the dynamics of these host-vector-pathogen systems and thus drives acarological risk (defined as the density of infected ticks). The principal objective of the OSCAR project (2011-2016) was to examine the links between this heterogeneity and acarological risk for humans and their domestic animals. Here, we present the data associated with this project.

          New information

          This paper reports a database on the distribution and densities of I. ricinus ticks - the most common tick species in French agricultural landscapes - and the prevalence of three tick-borne pathogens ( Anaplasma phagocytophilum , Borrelia spp. and Babesia spp.) in two sites in north-western (“Zone Atelier Armorique”: ZA site) and south-western (“Vallées et Coteaux de Gascogne”: VG site) France. The distribution and density of ticks along a gradient of wooded habitats, as well as biotic variables, such as the presence and abundance of their principal domestic (livestock) and wild hosts (small mammals), were measured from forest cores and edges to more or less isolated hedges, all bordering meadows. Ticks, small mammals and information on local environmental conditions were collected along 90 transects in each of the two sites in spring and autumn 2012 and 2013 and in spring 2014, corresponding to the main periods of tick activity. Local environmental conditions were recorded along each tick and small mammal transect: habitat type, vegetation type and characteristics, slope and traces of livestock presence. Samples consisted of questing ticks collected on the vegetation (mainly I. ricinus nymphs), biopsies of captured small mammals and ticks fixed on small mammals. In the VG site, livestock occurrence and abundance were recorded each week along each tick transect.

          A total of 29004 questing ticks and 1230 small mammals were captured during the study across the two sites and over the five field campaigns. All questing nymphs (N = 12287) and questing adults (N = 646) were identified to species. Ticks from small mammals (N = 1359) were also identified to life stage. Questing nymphs (N = 4518 I. ricinus ) and trapped small mammals (N = 908) were analysed for three pathogenic agents: A. phagocytophilum , Borrelia spp. and Babesia spp.

          In the VG site, the average prevalence in I. ricinus nymphs for A. phagocytophilum , Borrelia spp. and Babesia spp. were, respectively 1.9% [95% CI: 1.2-2.5], 2.5% [95% CI: 1.8-3.2] and 2.7% [95% CI: 2.0-3.4]. In small mammals, no A. phagocytophilum was detected, but the prevalence for Borrelia spp. was 4.2% [95% CI: 0.9-7.5]. On this site, there was no screening of small mammals for Babesia spp. In ZA site, the average prevalence in nymphs for A. phagocytophilum , Borrelia spp. and Babesia were, respectively 2.2% [95% CI: 1.6-2.7], 3.0% [95% CI: 2.3-3.6] and 3.1% [95% CI: 2.5-3.8]. In small mammals, the prevalence of A. phagocytophilum and Borrelia spp. were, respectively 6.9% [95% CI: 4.9-8.9] and 4.1% [95% CI: 2.7-5.9]. A single animal was found positive for Babesia microti at this site amongst the 597 tested.

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          Most cited references 32

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          The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk.

          The extent to which the biodiversity and community composition of ecosystems affect their functions is an issue that grows ever more compelling as human impacts on ecosystems increase. We present evidence that supports a novel function of vertebrate biodiversity, the buffering of human risk of exposure to Lyme-disease-bearing ticks. We tested the Dilution Effect model, which predicts that high species diversity in the community of tick hosts reduces vector infection prevalence by diluting the effects of the most competent disease reservoir, the ubiquitous white-footed mouse (Peromyscus leucopus). As habitats are degraded by fragmentation or other anthropogenic forces, some members of the host community disappear. Thus, species-poor communities tend to have mice, but few other hosts, whereas species-rich communities have mice, plus many other potential hosts. We demonstrate that the most common nonmouse hosts are relatively poor reservoirs for the Lyme spirochete and should reduce the prevalence of the disease by feeding, but rarely infecting, ticks. By accounting for nearly every host species' contribution to the number of larval ticks fed and infected, we show that as new host species are added to a depauperate community, the nymphal infection prevalence, a key risk factor, declines. We identify important "dilution hosts" (e.g., squirrels), characterized by high tick burdens, low reservoir competence, and high population density, as well as "rescue hosts" (e.g., shrews), which are capable of maintaining high disease risk when mouse density is low. Our study suggests that the preservation of vertebrate biodiversity and community composition can reduce the incidence of Lyme disease.
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            Multiplex real-time PCR for detection of anaplasma phagocytophilum and Borrelia burgdorferi.

            A multiplex real-time PCR assay was developed for the simultaneous detection of Anaplasma phagocytophilum and Borrelia burgdorferi. The assay was tested on various Anaplasma, Borrelia, Erhlichia, and Rickettsia species, as well as on Bartonella henselae and Escherichia coli, and the assay was found to be highly specific for A. phagocytophilum and the Borrelia species tested (B. burgdorferi, B. parkeri, B. andersonii, and B. bissettii). The analytical sensitivity of the assay is comparable to that of previously described nested PCR assays (A. phagocytophilum, 16S rRNA; B. burgdorferi, fla gene), amplifying the equivalent of one-eighth of an A. phagocytophilum-infected cell and 50 borrelia spirochetes. The dynamic range of the assay for both A. phagocytophilum and B. burgdorferi was >/=4 logs of magnitude. Purified DNA from A. phagocytophilum and B. burgdorferi was spiked into DNA extracted from uninfected ticks and from negative control mouse and human bloods, and these background DNAs were shown to have no significant effect on sensitivity or specificity of the assay. The assay was tested on field-collected Ixodes scapularis ticks and shown to have 100% concordance compared to previously described non-probe-based PCR assays. To our knowledge, this is the first report of a real-time multiplex PCR assay that can be used for the simultaneous and rapid screening of samples for A. phagocytophilum and Borrelia species, two of the most common tick-borne infectious agents in the United States.
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              Detection and identification of Ehrlichia, Borrelia burgdorferi sensu lato, and Bartonella species in Dutch Ixodes ricinus ticks.

              A sensitive and specific PCR hybridization assay was developed for the simultaneous detection and identification of Ehrlichia and Borrelia burgdorferi sensu lato. In separate assays the 16S rRNA gene of Ehrlichia species and the 23S-5S rRNA spacer region of B. burgdorferi sensu lato were amplified and labeled by PCR. These PCR products were used in a reverse line blot hybridization assay in which oligonucleotide probes are covalently linked to a membrane in parallel lines. Hybridization of the samples with the oligonucleotide probes on this membrane enabled the simultaneous detection and identification of Ehrlichia, B. burgdorferi, and Bartonella species in 40 different samples. The application of the assay to DNA extracts from 121 Ixodes ricinus ticks collected from roe deer demonstrated that 45% of these ticks carried Ehrlichia DNA. More than half of these positive ticks carried species with 16S rRNA gene sequences closely related to those of E. phagocytophila and the human granulocytic ehrlichiosis agent. The majority of the other positive ticks were infected with a newly identified Ehrlichia-like species. In addition, 13% of the ticks were infected with one or more B. burgdorferi genospecies. In more than 70% of the ticks 16S rRNA gene sequences for Bartonella species or other species closely related to Bartonella were found. In five of the ticks both Ehrlichia and B. burgdorferi species were detected.
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                Author and article information

                Contributors
                Journal
                Biodivers Data J
                Biodivers Data J
                1
                urn:lsid:arphahub.com:pub:F9B2E808-C883-5F47-B276-6D62129E4FF4
                urn:lsid:zoobank.org:pub:245B00E9-BFE5-4B4F-B76E-15C30BA74C02
                Biodiversity Data Journal
                Pensoft Publishers
                1314-2836
                1314-2828
                2020
                05 May 2020
                : 8
                Affiliations
                [1 ] Université Clermont Auvergne, INRAE, VetAgro Sup, UMR EPIA, F-63122, Saint-Genès Champanelle, France Université Clermont Auvergne, INRAE, VetAgro Sup, UMR EPIA F-63122, Saint-Genès Champanelle France
                [2 ] INRAE, BIOEPAR, Oniris, F-44307, Nantes, France INRAE, BIOEPAR, Oniris F-44307, Nantes France
                [3 ] Université Rennes, CNRS, ECOBIO (Ecosystèmes, biodiversité, évolution) - UMR 6553, 35000 Rennes, France Université Rennes, CNRS, ECOBIO (Ecosystèmes, biodiversité, évolution) - UMR 6553 35000 Rennes France
                [4 ] CEFS, Université de Toulouse, INRAE, F-31326, Castanet-Tolosan, France CEFS, Université de Toulouse, INRAE F-31326, Castanet-Tolosan France
                [5 ] MIVEGEC, Université Montpellier-CNRS-IRD, 911 Avenue Agropolis, 34394 Montpellier, France MIVEGEC, Université Montpellier-CNRS-IRD, 911 Avenue Agropolis 34394 Montpellier France
                Author notes
                Corresponding authors: Isabelle Lebert ( isabelle.lebert@ 123456inrae.fr ), Alain Butet ( alain.butet@ 123456univ-rennes1.fr ), Karen D. McCoy ( karen.mccoy@ 123456ird.fr ), Hélène Verheyden ( helene.verheyden@ 123456inra.fr ).

                Academic editor: Jenő Kontschán

                Article
                50123 8481
                10.3897/BDJ.8.e50123
                7217980
                Isabelle Lebert, Albert Agoulon, Suzanne Bastian, Alain Butet, Bruno Cargnelutti, Nicolas Cèbe, Amélie Chastagner, Elsa Léger, Bruno Lourtet, Sébastien Masseglia, Karen D. McCoy, Joël Merlet, Valérie Noël, Grégoire Perez, Denis Picot, Angélique Pion, Valérie Poux, Jean-Luc Rames, Yann Rantier, Hélène Verheyden, Gwenael Vourc'h, Olivier Plantard

                This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                Page count
                Figures: 10, Tables: 17, References: 33
                Categories
                Data Paper (Biosciences)
                Apicomplexa
                Rickettsiales
                Spirochaetes
                Protozoa
                Mammalia
                Bovidae
                Cervidae
                Ixodidae
                Arthropoda
                Agriculture and Forestry
                Ecology & Environmental sciences
                France

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