Habitat properties are key drivers of Borrelia burgdorferi (s.l.) prevalence in Ixodes ricinus populations of deciduous forest fragments
Abstract 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...
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| Format: | Article |
| Language: | English |
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BMC
2018-01-01
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| Series: | Parasites & Vectors |
| Subjects: | |
| Online Access: | http://link.springer.com/article/10.1186/s13071-017-2590-x |
| _version_ | 1818356420703158272 |
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| author | Steffen Ehrmann Sanne C. Ruyts Michael Scherer-Lorenzen Jürgen Bauhus Jörg Brunet Sara A. O. Cousins Marc Deconchat Guillaume Decocq Pieter De Frenne Pallieter De Smedt Martin Diekmann Emilie Gallet-Moron Stefanie Gärtner Karin Hansen Annette Kolb Jonathan Lenoir Jessica Lindgren Tobias Naaf Taavi Paal Marcus Panning Maren Prinz Alicia Valdés Kris Verheyen Monika Wulf Jaan Liira |
| author_facet | Steffen Ehrmann Sanne C. Ruyts Michael Scherer-Lorenzen Jürgen Bauhus Jörg Brunet Sara A. O. Cousins Marc Deconchat Guillaume Decocq Pieter De Frenne Pallieter De Smedt Martin Diekmann Emilie Gallet-Moron Stefanie Gärtner Karin Hansen Annette Kolb Jonathan Lenoir Jessica Lindgren Tobias Naaf Taavi Paal Marcus Panning Maren Prinz Alicia Valdés Kris Verheyen Monika Wulf Jaan Liira |
| author_sort | Steffen Ehrmann |
| collection | DOAJ |
| description | Abstract 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. 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. |
| first_indexed | 2024-12-13T19:56:56Z |
| format | Article |
| id | doaj.art-68ee9b467a6f4f72918475c63575c1a6 |
| institution | Directory Open Access Journal |
| issn | 1756-3305 |
| language | English |
| last_indexed | 2024-12-13T19:56:56Z |
| publishDate | 2018-01-01 |
| publisher | BMC |
| record_format | Article |
| series | Parasites & Vectors |
| spelling | doaj.art-68ee9b467a6f4f72918475c63575c1a62022-12-21T23:33:17ZengBMCParasites & Vectors1756-33052018-01-0111111510.1186/s13071-017-2590-xHabitat properties are key drivers of Borrelia burgdorferi (s.l.) prevalence in Ixodes ricinus populations of deciduous forest fragmentsSteffen Ehrmann0Sanne C. Ruyts1Michael Scherer-Lorenzen2Jürgen Bauhus3Jörg Brunet4Sara A. O. Cousins5Marc Deconchat6Guillaume Decocq7Pieter De Frenne8Pallieter De Smedt9Martin Diekmann10Emilie Gallet-Moron11Stefanie Gärtner12Karin Hansen13Annette Kolb14Jonathan Lenoir15Jessica Lindgren16Tobias Naaf17Taavi Paal18Marcus Panning19Maren Prinz20Alicia Valdés21Kris Verheyen22Monika Wulf23Jaan Liira24Geobotany, Faculty of Biology, University of FreiburgForest & Nature Lab, Ghent UniversityGeobotany, Faculty of Biology, University of FreiburgFaculty of Environment and Natural Resources, University of FreiburgSouthern Swedish Forest Research Centre, Swedish University of Agricultural SciencesLandscape Ecology, Department of Geography and Quaternary Geology, Stockholm UniversityDYNAFOR, Université de Toulouse, INRA, INPTUR “Ecologie et Dynamique des Systèmes Anthropisés” (EDYSAN, FRE 3498 CNRS-UPJV), Jules Verne University of PicardieForest & Nature Lab, Ghent UniversityForest & Nature Lab, Ghent UniversityFaculty of Biology/Chemistry (FB 02), Institute of Ecology, Vegetation Ecology and Conservation Biology, University of BremenUR “Ecologie et Dynamique des Systèmes Anthropisés” (EDYSAN, FRE 3498 CNRS-UPJV), Jules Verne University of PicardieFaculty of Environment and Natural Resources, University of FreiburgNatural Resources & Environmental Effects, IVL Swedish Environmental Research InstituteFaculty of Biology/Chemistry (FB 02), Institute of Ecology, Vegetation Ecology and Conservation Biology, University of BremenUR “Ecologie et Dynamique des Systèmes Anthropisés” (EDYSAN, FRE 3498 CNRS-UPJV), Jules Verne University of PicardieLandscape Ecology, Department of Geography and Quaternary Geology, Stockholm UniversityInstitute of Land Use Systems, Leibniz-ZALF (e.V.)Institute of Ecology and Earth Sciences, University of TartuInstitute of Virology, University Medical Center FreiburgInstitute of Virology, University Medical Center FreiburgUR “Ecologie et Dynamique des Systèmes Anthropisés” (EDYSAN, FRE 3498 CNRS-UPJV), Jules Verne University of PicardieForest & Nature Lab, Ghent UniversityInstitute of Land Use Systems, Leibniz-ZALF (e.V.)Institute of Ecology and Earth Sciences, University of TartuAbstract 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. 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.http://link.springer.com/article/10.1186/s13071-017-2590-xClimate gradientDilution habitatDisease ecologyEcosystem disserviceFunctional ecologyLandscape epidemiology |
| spellingShingle | Steffen Ehrmann Sanne C. Ruyts Michael Scherer-Lorenzen Jürgen Bauhus Jörg Brunet Sara A. O. Cousins Marc Deconchat Guillaume Decocq Pieter De Frenne Pallieter De Smedt Martin Diekmann Emilie Gallet-Moron Stefanie Gärtner Karin Hansen Annette Kolb Jonathan Lenoir Jessica Lindgren Tobias Naaf Taavi Paal Marcus Panning Maren Prinz Alicia Valdés Kris Verheyen Monika Wulf Jaan Liira Habitat properties are key drivers of Borrelia burgdorferi (s.l.) prevalence in Ixodes ricinus populations of deciduous forest fragments Parasites & Vectors Climate gradient Dilution habitat Disease ecology Ecosystem disservice Functional ecology Landscape epidemiology |
| title | Habitat properties are key drivers of Borrelia burgdorferi (s.l.) prevalence in Ixodes ricinus populations of deciduous forest fragments |
| title_full | Habitat properties are key drivers of Borrelia burgdorferi (s.l.) prevalence in Ixodes ricinus populations of deciduous forest fragments |
| title_fullStr | Habitat properties are key drivers of Borrelia burgdorferi (s.l.) prevalence in Ixodes ricinus populations of deciduous forest fragments |
| title_full_unstemmed | Habitat properties are key drivers of Borrelia burgdorferi (s.l.) prevalence in Ixodes ricinus populations of deciduous forest fragments |
| title_short | Habitat properties are key drivers of Borrelia burgdorferi (s.l.) prevalence in Ixodes ricinus populations of deciduous forest fragments |
| title_sort | habitat properties are key drivers of borrelia burgdorferi s l prevalence in ixodes ricinus populations of deciduous forest fragments |
| topic | Climate gradient Dilution habitat Disease ecology Ecosystem disservice Functional ecology Landscape epidemiology |
| url | http://link.springer.com/article/10.1186/s13071-017-2590-x |
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