https://doi.org/10.4081/gh.2022.1058
Habitat suitability map of Ixodes ricinus tick in France using multi-criteria analysis
Submitted: 22 November 2021
Accepted: 14 April 2022
Published: 17 May 2022
Accepted: 14 April 2022
Abstract Views: 4551
PDF: 1699
Appendix: 233
HTML: 133
Appendix: 233
HTML: 133
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
Authors
The tick Ixodes ricinus is widely distributed across Europe and is responsible for the transmission of several pathogens to humans and animals. In this study, we used a knowledge-based method to map variations in habitat suitability for I. ricinus ticks throughout continental France and Corsica. The multi-criteria decision analysis (MCDA) integrated four major biotic and abiotic factors known to influence tick populations: climate, land cover, altitude and the density of wild ungulates. For each factor, habitat suitability index (HSI) values were attributed to different locations based on knowledge regarding its impact on tick populations. For the MCDA, two methods of factor combination were tested, additive and multiplicative, both which were evaluated at the spatial scales of departments and local municipalities. The resulting habitat suitability maps (resolution=100x100 m) revealed that conditions are suitable for I. ricinus over most of France and Corsica. Particularly suitable habitats were located in central, north-eastern and south-western France, while less-suitable habitats were found in the Mediterranean and mountainous regions. To validate the approach, the HSI scores were compared to field data of I. ricinus nymph abundance. Regardless of scale, the correlation between abundance indicator and HSI score was stronger for the additive than for the multiplicative approach. Overall, this study demonstrates the value of MCDA for estimating habitat suitability maps for I. ricinus abundance, which could be especially useful in highlighting areas of the tick’s distribution where preventive measures should be prioritised.
Aenishaenslin C, Bouchard C, Koffi JK, Ogden NH, 2017. Exposure and preventive behaviours toward ticks and Lyme disease in Canada: Results from a first national survey. Ticks Tick-Borne Dis 8:112-8.
DOI: https://doi.org/10.1016/j.ttbdis.2016.10.006
Aenishaenslin C, Gern L, Michel P, Ravel A, Hongoh V, Waaub JP, Milord F, Belanger D, 2015. Adaptation and evaluation of a multi-criteria decision analysis model for Lyme disease prevention. PLoS One 10:e0135171.
DOI: https://doi.org/10.1371/journal.pone.0135171
Agoulon A, Butet A, Hoch T, Perez G, Plantard O, Verheyden H, Vourc’h G, 2016. 3. Dynamique des populations de tiques et liaison avec les facteurs environnementaux. In: Karen DM, Nathalie B (Eds.), Tiques et maladies à tiques : biologie, écologie évolutive, épidémiologie. IRD Editions, Marseille, France, pp. 85-112.
DOI: https://doi.org/10.4000/books.irdeditions.9027
Akl T, Bourgoin G, Souq M-L, Appolinaire J, Poirel M-T, Gibert P, Abi Rizk G, Garel M, Zenner L, 2019. Detection of tick-borne pathogens in questing Ixodes ricinus in the French Pyrenees and first identification of Rickettsia monacensis in France. Parasite 26:20.
DOI: https://doi.org/10.1051/parasite/2019019
Alfredsson M, Olafsson E, Eydal M, Unnsteinsdottir ER, Hansford K, Wint W, Alexander N, Medlock JM, 2017. Surveillance of Ixodes ricinus ticks (Acari: Ixodidae) in Iceland. Parasites Vectors 10:466.
DOI: https://doi.org/10.1186/s13071-017-2375-2
Asghar N, Petersson M, Johansson M, Dinnetz P, 2016. Local landscape effects on population dynamics of Ixodes ricinus. Geospat Health 11:487.
DOI: https://doi.org/10.4081/gh.2016.487
Aubry P, Guillemain M, 2019. Attenuating the nonresponse bias in hunting bag surveys: The multiphase sampling strategy. PLoS One 14:e0213670.
DOI: https://doi.org/10.1371/journal.pone.0213670
Beugnet F, Chalvet-Monfray K, Loukos H, 2009. FleaTickRisk: a meteorological model developed to monitor and predict the activity and density of three tick species and the cat flea in Europe. Geospat Health 4:97-113.
DOI: https://doi.org/10.4081/gh.2009.213
Boehnke D, Brugger K, Pfaffle M, Sebastian P, Norra S, Petney T, Oehme R, Littwin N, Lebl K, Raith J, Walter M, Gebhardt R, Rubel F, 2015. Estimating Ixodes ricinus densities on the landscape scale. Int J Health Geogr 14:23.
DOI: https://doi.org/10.1186/s12942-015-0015-7
Bonnet S, Huber K, Joncour G, René-Martellet M, Stachurski F, Zenner L, 2016. 2. Biologie des tiques. In: Karen DM, Nathalie B (Eds.), Tiques et maladies à tiques - Biologie, écologie évolutive, épidémiologie. IRD Editions, Marseille, France, pp. 53-84.
DOI: https://doi.org/10.4000/books.irdeditions.9020
Bord S, Dernat S, Ouillon L, René-Martellet M, Vourc’h G, Lesens O, Forestier C, Lebert I, 2022. Tick ecology and Lyme borreliosis prevention: a regional survey of pharmacists’ knowledge in Auvergne-Rhône-Alpes, France. Ticks Tick-Borne Dis 13:101932.
DOI: https://doi.org/10.1016/j.ttbdis.2022.101932
Bord S, Lebert I, René-Martellet M, Dernat S, Johany F, Bimonte S, Chalvet-Monfray K, Poux V, Cosson JF, Smoreda Z, Vourc’h G, 2019. Intérêt des données de téléphonie mobile et des sciences participatives pour l’estimation et la compréhension du risque de transmission de maladies liées à l’environnement: Application aux maladies transmises par les tiques. In Réunion Tiques & Maladies à Tiques - 22-23 may 2019, Montpellier, France.
Boyard C, Barnouin J, Bord S, Gasqui P, Vourc’h G, 2011. Reproducibility of local environmental factors for the abundance of questing Ixodes ricinus nymphs on pastures. Ticks Tick-Borne Dis 2:104-110.
DOI: https://doi.org/10.1016/j.ttbdis.2011.02.001
Boyard C, Vourc’h G, Barnouin J, 2008. The relationships between Ixodes ricinus and small mammal species at the woodland-pasture interface. Exp Appl Acarol 44:61-76.
DOI: https://doi.org/10.1007/s10493-008-9132-3
Brugger K, Boehnke D, Petney T, Dobler G, Pfeffer M, Silaghi C, Schaub GA, Pinior B, Dautel H, Kahl O, Pfister K, Suss J, Rubel F, 2016. A density map of the tick-borne encephalitis and Lyme borreliosis vector Ixodes ricinus (Acari: Ixodidae) for Germany. J Med Entomol 53:1292-302.
DOI: https://doi.org/10.1093/jme/tjw116
Butler AD, Sedghi T, Petrini JR, Ahmadi R, 2016. Tick-borne disease preventive practices and perceptions in an endemic area. Ticks Tick-Borne Dis 7:331-7.
DOI: https://doi.org/10.1016/j.ttbdis.2015.12.003
Cadenas FM, Rais O, Jouda F, Douet V, Humair P-F, Moret J, Gern L, 2007. Phenology of Ixodes ricinus and infection with Borrelia burgdorferi sensu lato along a North- and South-facing altitudinal gradient on Chaumont Mountain, Switzerland. J Med Entomol 44:683-93.
DOI: https://doi.org/10.1093/jmedent/44.4.683
Cat J, Beugnet F, Hoch T, Jongejan F, Prange A, Chalvet-Monfray K, 2017. Influence of the spatial heterogeneity in tick abundance in the modeling of the seasonal activity of Ixodes ricinus nymphs in Western Europe. Exp Appl Acarol 71:115-30.
DOI: https://doi.org/10.1007/s10493-016-0099-1
Chen D, Wong H, Belanger P, Moore K, Peterson M, Cunningham J, 2015. Analyzing the correlation between deer habitat and the component of the risk for Lyme disease in Eastern Ontario, Canada: A GIS-based approach. ISPRS Int J Geoinf 4:105-23.
DOI: https://doi.org/10.3390/ijgi4010105
Daniel M, Danielova V, Kriz B, Jirsa A, Nozicka J, 2003. Shift of the tick Ixodes ricinus and tick-borne encephalitis to higher altitudes in Central Europe. Eur J Clin Microbio Infect Dis 22:327-8.
DOI: https://doi.org/10.1007/s10096-003-0918-2
Daniel M, Danielova V, Kriz B, Ruzek D, Fialova A, Maly M, Materna J, Pejcoch M, Erhart J, 2016a. The occurrence of Ixodes ricinus ticks and important tick-borne pathogens in areas with high tick-borne encephalitis prevalence in different altitudinal levels of the Czech Republic Part I. Ixodes ricinus ticks and tick-borne encephalitis virus. Epidemiol Mikrobiol Imunol 65:118-28.
Daniel M, Rudenko N, Golovchenko M, Danielova V, Fialova A, Kriz B, Maly M, 2016b. The occurrence of Ixodes ricinus ticks and important tick-borne pathogens in areas with high tick-borne encephalitis prevalence in different altitudinal levels of the Czech Republic Part II. Ixodes ricinus ticks and genospecies of Borrelia burgdorferi sensu lato complex. Epidemiol Mikrobiol Imunol 65:182-92.
Danielova V, Daniel M, Schwarzova L, Materna J, Rudenko N, Golovchenko M, Holubova J, Grubhoffer L, Kilian P, 2010. Integration of a tick-borne encephalitis virus and Borrelia burgdorferi sensu lato into mountain ecosystems, following a shift in the altitudinal limit of distribution of their vector, Ixodes ricinus (Krkonose mountains, Czech Republic). Vector Borne Zoonotic Dis 10:223-30.
DOI: https://doi.org/10.1089/vbz.2009.0020
De Keukeleire M, Robert A, Kabamba B, Dion E, Luyasu V, Vanwambeke SO, 2016. Individual and environmental factors associated with the seroprevalence of Borrelia burgdorferi in Belgian farmers and veterinarians. Infect Ecol Epidemio l6:32793.
DOI: https://doi.org/10.3402/iee.v6.32793
De Keukeleire M, Vanwambeke SO, Somasse E, Kabamba B, Luyasu V, Robert A, 2015. Scouts, forests, and ticks: Impact of landscapes on human-tick contacts. Ticks Tick-Borne Dis 6:636-44.
DOI: https://doi.org/10.1016/j.ttbdis.2015.05.008
De Pelsmaeker N, Korslund L, Steifetten Ø, 2021. High-elevational occurrence of two tick species, Ixodes ricinus and I. trianguliceps, at their northern distribution range. Parasites Vectors 14:161.
DOI: https://doi.org/10.1186/s13071-021-04604-w
Derringer R, Suich R, 1980. Simultaneous optimization of several response variables. J Qual Technol 12:214-9.
DOI: https://doi.org/10.1080/00224065.1980.11980968
ECDC, 2019. A spatial modelling method for vector surveillance. European Centre for Disease Prevention and Control, Stockholm, 29 pp.
Estoque RC, 2012. Chapter 11: Analytic hierarchy process in geospatial analysis, In: Murayama Y (Ed.) Progress in Geospatial Analysis. Springler, Japan, pp. 157-181.
DOI: https://doi.org/10.1007/978-4-431-54000-7_11
Estoque RC, Murayama Y, 2010. Suitability analysis for beekeeping sites in La Union, Philippines, using GIS and multi-criteria evaluation techniques. Res J Appl Sci 5:242-53.
DOI: https://doi.org/10.3923/rjasci.2010.242.253
Estrada-Peña A, Alexander N, Wint GRW, 2016. Perspectives on modelling the distribution of ticks for large areas: so far so good? Parasites Vectors 9:179.
DOI: https://doi.org/10.1186/s13071-016-1474-9
Estrada-Peña A, Farkas R, Jaenson TG, Koenen F, Madder M, Pascucci I, Salman M, Tarres-Call J, Jongejan F, 2013. Association of environmental traits with the geographic ranges of ticks (Acari: Ixodidae) of medical and veterinary importance in the western Palearctic. A digital data set. Exp Appl Acaro l59:351-66.
DOI: https://doi.org/10.1007/s10493-012-9600-7
Estrada-Peña A, Venzal JM, 2007. Climate niches of tick species in the Mediterranean region: Modeling of occurrence data, distributional constraints, and impact of climate change. J Med Entomol 44:1130-8.
DOI: https://doi.org/10.1603/0022-2585(2007)44[1130:CNOTSI]2.0.CO;2
Estrada-Peña A, Venzal JM, Sanchez Acedo C, 2006. The tick Ixodes ricinus: distribution and climate preferences in the western Palaearctic. Med Vet Entomol 20:189-97.
DOI: https://doi.org/10.1111/j.1365-2915.2006.00622.x
Fabri ND, Sprong H, Hofmeester TR, Heesterbeek H, Donnars BF, Widemo F, Ecke F, Cromsigt JPGM, 2021. Wild ungulate species differ in their contribution to the transmission of Ixodes ricinus-borne pathogens. Parasites Vectors 14:360.
DOI: https://doi.org/10.1186/s13071-021-04860-w
Gilbert L, Maffey G, Ramsay S, Hester A, 2012. The effect of deer management on the abundance of Ixodes ricinus in Scotland. Ecol Appl 22:658-67.
DOI: https://doi.org/10.1890/11-0458.1
Gilot C, Deleigh B, Pichot J, Doche B, Guigen C, 1996. Prevalence of Borrelia burgdorferi (sensu lato) in Ixodes ricinus (L.) populations in France, according to a phytoecological zoning of the territory. Eur J Epidemiol 12:395-401.
DOI: https://doi.org/10.1007/BF00145304
Goldstein V, Boulanger N, Schwartz D, George J-C, Ertlen D, Zilliox L, Schaeffer M, Jaulhac B, 2018. Factors responsible for Ixodes ricinus nymph abundance: Are soil features indicators of tick abundance in a French region where Lyme borreliosis is endemic? Ticks Tick-Borne Dis 9:938-44.
DOI: https://doi.org/10.1016/j.ttbdis.2018.03.013
Hall JL, Alpers K, Bown KJ, Martin SJ, Birtles RJ, 2017. Use of mass-participation outdoor events to assess human exposure to tickborne pathogens. Emerg Infect Dis 23:463-7.
DOI: https://doi.org/10.3201/eid2303.161397
Hansford KM, Fonville M, Gillingham EL, Coipan EC, Pietzsch ME, Krawczyk AI, Vaux AGC, Cull B, Sprong H, Medlock JM, 2017. Ticks and Borrelia in urban and peri-urban green space habitats in a city in southern England. Ticks Tick-Borne Dis 8:353-61.
DOI: https://doi.org/10.1016/j.ttbdis.2016.12.009
Hofmeester TR, Sprong H, Jansen PA, Prins HHT, van Wieren SE, 2017. Deer presence rather than abundance determines the population density of the sheep tick, Ixodes ricinus, in Dutch forests. Parasites Vectors 10:433.
DOI: https://doi.org/10.1186/s13071-017-2370-7
Hongoh V, Hoen AG, Aenishaenslin C, Waaub JP, Belanger D, Michel P, Lyme MC, 2011. Spatially explicit multi-criteria decision analysis for managing vector-borne diseases. Int J Health Geogr 10:70.
DOI: https://doi.org/10.1186/1476-072X-10-70
Hönig V, Švec P, Marek L, Mrkvička T, Dana Z, Wittmann M, Masař O, Szturcová D, Růžek D, Pfister K, Grubhoffer L, 2019. Model of risk of exposure to Lyme borreliosis and tick-borne encephalitis virus-infected ticks in the border area of the Czech Republic (South Bohemia) and Germany (Lower Bavaria and Upper Palatinate). Int J Environ Res Public Health 16:1173.
DOI: https://doi.org/10.3390/ijerph16071173
Hönig V, Svec P, Masar O, Gribhoffer L, 2011. Tick-borne diseases risk model for south Bohemia (Czech Republic). GIS Ostrava 23-26.
Hook SA, Nelson CA, Mead PS, 2015. U.S. public’s experience with ticks and tick-borne diseases: results from national health styles surveys. Ticks Tick-Borne Dis 6: 483-8.
DOI: https://doi.org/10.1016/j.ttbdis.2015.03.017
Ishizaka A, Nemery P, 2013. Multi-criteria decision analysis: methods and software. Wiley, UK, 310 pp.
DOI: https://doi.org/10.1002/9781118644898
Joly D, Brossard T, Cardot H, Cavailhes J, Hilal M, Wavresky P, 2010. Les types de climats en France, une construction spatiale Cybergeo Eur J Geogr 501:1-26.
DOI: https://doi.org/10.4000/cybergeo.23155
Klitgaard K, Højgaard J, Isbrand A, Madsen JJ, Thorup K, Bødker R, 2019. Screening for multiple tick-borne pathogens in Ixodes ricinus ticks from birds in Denmark during spring and autumn migration seasons. Ticks Tick-Borne Dis 10: 546-52.
DOI: https://doi.org/10.1016/j.ttbdis.2019.01.007
Lebert I, Agoulon A, Bastian S, Butet A, Cargnelutti B, Cèbe N, Chastagner A, Léger E, Lourtet B, Masseglia S, McCoy KD, Merlet J, Noël V, Perez G, Picot D, Pion A, Poux V, Rames J-L, Rantier Y, Verheyden H, Vourc’h G, Plantard O, 2020. 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. Biodivers Data J 8:e50123.
DOI: https://doi.org/10.3897/BDJ.8.e50123
Lees AD, 1946. The water balance in Ixodes ricinus L. and certain otherspecies of ticks. Parasitology 37:1-20.
DOI: https://doi.org/10.1017/S0031182000013093
Lejal E, Marsot M, Chalvet-Monfray K, Cosson J-F, Moutailler S, Vayssier-Taussat M, Pollet T, 2019. A three-years assessment of Ixodes ricinus-borne pathogens in a French peri-urban forest. Parasites Vectors 12:551.
DOI: https://doi.org/10.1186/s13071-019-3799-7
Li S, Gilbert L, Vanwambeke SO, Yu J, Purse BV, Harrison PA, 2019. Lyme disease risks in Europe under multiple uncertain drivers of change. Environ Health Perspect 127:067010.
DOI: https://doi.org/10.1289/EHP4615
Maetzel D, Maier WA, Kampen H, 2005. Borrelia burgdorferi infection prevalences in questing Ixodes ricinus ticks (Acari: Ixodidae) in urban and suburban Bonn, western Germany. Parasitol Res 95:5-12.
DOI: https://doi.org/10.1007/s00436-004-1240-3
Malczewski J, 2000. On the use of weighted linear combination method in GIS: common and best practice approaches. Trans GIS 4:5-22.
DOI: https://doi.org/10.1111/1467-9671.00035
Martello E, Mannelli A, Grego E, Ceballos LA, Ragagli C, Stella MC, Tomassone L, 2019. Borrelia burgdorferi sensu lato and spotted fever group rickettsiae in small rodents and attached ticks in the Northern Apennines, Italy. Ticks Tick-Borne Dis 10:862-7.
DOI: https://doi.org/10.1016/j.ttbdis.2019.04.005
Materna J, Daniel M, Metelka L, Harcarika J, 2008. The vertical distribution, density and the development of the tick Ixodes ricinus in mountain areas influenced by climate changes (The Krkonose Mts., Czech Republic). Int J Med Microbiol 298:25-37.
DOI: https://doi.org/10.1016/j.ijmm.2008.05.004
Mathews-Martin L, Namèche M, Vourc’h G, Gasser S, Lebert I, Poux V, Barry S, Bord S, Jachacz J, Chalvet Monfray K, Bourdoiseau G, Sepúlveda D, Chambon-Rouvier S, René-Martellet M, 2020. Questing tick abundance in urban and peri-urban parks in the French city of Lyon. Parasites Vectors 13:576.
DOI: https://doi.org/10.1186/s13071-020-04451-1
Medlock JM, Hansford KM, Bormane A, Derdakova M, Estrada-Pena A, George JC, Golovljova I, Jaenson TG, Jensen JK, Jensen PM, Kazimirova M, Oteo JA, Papa A, Pfister K, Plantard O, Randolph SE, Rizzoli A, Santos-Silva MM, Sprong H, Vial L, Hendrickx G, Zeller H, Van Bortel W, 2013. Driving forces for changes in geographical distribution of Ixodes ricinus ticks in Europe. Parasites Vectors 6:1.
DOI: https://doi.org/10.1186/1756-3305-6-1
Metzger MJ, Bunce RGH, Jongman RHG, Mücher CA, Watkins JW, 2005. A climatic stratification of the environment of Europe. Glob Ecol Biogeogr 14:549-63.
DOI: https://doi.org/10.1111/j.1466-822X.2005.00190.x
Millins C, Gilbert L, Medlock J, Hansford K, Thompson DB, Biek R, 2017. Effects of conservation management of landscapes and vertebrate communities on Lyme borreliosis risk in the United Kingdom. Philos Trans R Soc Lond B Biol Sci 372.
DOI: https://doi.org/10.1098/rstb.2016.0123
Ministère des Solidarités et de la Santé, 2016. Plan national de lutte contre la maladie de Lyme et les maladies transmissibles par les tiques. Available from: https://solidarites-sante.gouv.fr/IMG/pdf/plan_lyme_180117.pdf
Mücher CA, Klijn JA, Wascher DM, Schaminée JHJ, 2010. A new European landscape classification (LANMAP): a transparent, flexible and user-oriented methodology to distinguish landscapes. Ecol Indic 10:87-103.
DOI: https://doi.org/10.1016/j.ecolind.2009.03.018
Mysterud A, Hügli C, Viljugrein H, 2021. Tick infestation on medium–large-sized mammalian hosts: are all equally suitable to Ixodes ricinus adults? Parasites Vectors 14:254.
DOI: https://doi.org/10.1186/s13071-021-04775-6
Paul MC, Goutard FL, Roulleau F, Holl D, Thanapongtharm W, Roger FL, Tran A, 2016a. Quantitative assessment of a spatial multicriteria model for highly pathogenic avian influenza H5N1 in Thailand, and application in Cambodia. Sci Rep 6:31096.
DOI: https://doi.org/10.1038/srep31096
Paul RE, Cote M, Le Naour E, Bonnet SI, 2016b. Environmental factors influencing tick densities over seven years in a French suburban forest. Parasites Vectors 9:309.
DOI: https://doi.org/10.1186/s13071-016-1591-5
Perez D, Kneubuhler Y, Rais O, Gern L, 2012. Seasonality of Ixodes ricinus ticks on vegetation and on rodents and Borrelia burgdorferi sensu lato genospecies diversity in two Lyme borreliosis-endemic areas in Switzerland. Vector Borne Zoonotic Dis 12:633-44.
DOI: https://doi.org/10.1089/vbz.2011.0763
Perez G, Bastian S, Agoulon A, Bouju A, Durand A, Faille F, Lebert I, Rantier Y, Plantard O, Butet A, 2016. Effect of landscape features on the relationship between Ixodes ricinus ticks and their small mammal hosts. Parasites Vectors 9:20.
DOI: https://doi.org/10.1186/s13071-016-1296-9
Pfeiffer DU, Robinson TP, Stevenson M, Stevens KB, Rogers DJ, Clements ACA, 2008. Spatial analysis in epidemiology. Oxford University Press, New york, NY, USA, 160 pp.
DOI: https://doi.org/10.1093/acprof:oso/9780198509882.001.0001
R Core Team 2017. R: A language and environment for statistical computing, R Foundation for Statistical Computing, ed. Vienna, Austria. Available from: https://www.R-project.org/
Radolf J, Caimano M, Stevenson B, Hu L, 2012. Of ticks, mice and men: understanding the dual-host lifestyle of Lyme disease spirochaetes. Nat Rev Microbiol 10:87-99.
DOI: https://doi.org/10.1038/nrmicro2714
Ragagli C, Mannelli A, Ambrogi C, Bisanzio D, Ceballos LA, Grego E, Martello E, Selmi M, Tomassone L, 2016. Presence of host-seeking Ixodes ricinus and their infection with Borrelia burgdorferi sensu lato in the Northern Apennines, Italy. Exp Appl Acarol 69:167-78.
DOI: https://doi.org/10.1007/s10493-016-0030-9
Ramsey PH, 1989. Critical values for Spearman’s rank order correlation. J Educ Stat 14:245-53.
DOI: https://doi.org/10.3102/10769986014003245
Réseau sentinelles, 2021. Bilan annuel d’activités 2020, Janvier à décembre 2020, Veille sanitaire et recherche en soins primaires, Inserm, Médecine Sorbonne Université. Available from: https://www.sentiweb.fr/document/5361
Rizzoli A, Silaghi C, Obiegala A, Rudolf I, Hubalek Z, Foldvari G, Plantard O, Vayssier-Taussat M, Bonnet S, Spitalska E, Kazimirova M, 2014. Ixodes ricinus and its transmitted pathogens in urban and peri-urban areas in Europe: new hazards and relevance for public health. Front Public Health 2:251.
DOI: https://doi.org/10.3389/fpubh.2014.00251
Rousseau R, McGrath G, McMahon BJ, Vanwambeke SO, 2017. Multi-criteria decision analysis to model Ixodes ricinus habitat suitability. Ecohealth 14:591-602.
DOI: https://doi.org/10.1007/s10393-017-1247-8
Saint-Andrieux C, Barboiron A, 2014. Tableaux de chasse ongulés sauvages saison 2013-2014. Faune Sauvage Suppl:I-VIII.
Sandor AD, D’Amico G, Gherman CM, Dumitrache MO, Domsa C, Mihalca AD, 2017. Mesocarnivores and macroparasites: altitude and land use predict the ticks occurring on red foxes (Vulpes vulpes). Parasites Vectors 10:173.
DOI: https://doi.org/10.1186/s13071-017-2113-9
Semenza J, Suk J, 2018. Vector-borne diseases and climate change: a European perspective. FEMS Microbiol Lett 365.
DOI: https://doi.org/10.1093/femsle/fnx244
Stafford KC, 2004. Tick management handbook; an integrated guide for homeowners, pest control operators, and public health officials for the prevention of tick-associated disease. Connecticut Agricultural Experiment Station, 71 pp.
Svec P, Honig V, Zubrikova D, Wittmann M, Pfister K, Grubhoffer L, 2019. The use of multi-criteria evaluation for the selection of study plots for monitoring of I. ricinus ticks - Example from Central Europe. Ticks Tick-Borne Dis 10:905-10.
DOI: https://doi.org/10.1016/j.ttbdis.2019.04.014
Swart A, Ibanez-Justicia A, Buijs J, van Wieren SE, Hofmeester TR, Sprong H, Takumi K, 2014. Predicting tick presence by environmental risk mapping. Front Public Health 2:238.
DOI: https://doi.org/10.3389/fpubh.2014.00238
Tack W, Madder M, Baeten L, Vanhellemont M, Gruwez R, Verheyen K, 2012. Local habitat and landscape affect Ixodes ricinus tick abundances in forests on poor, sandy soils. For Ecol Manag 265:30-6.
DOI: https://doi.org/10.1016/j.foreco.2011.10.028
Taragel’ova VR, Mahrikova L, Selyemova D, Vaclav R, Derdakova M, 2016. Natural foci of Borrelia lusitaniae in a mountain region of Central Europe. Ticks Tick-Borne Dis 7:350-6.
DOI: https://doi.org/10.1016/j.ttbdis.2015.12.006
Thorin C, Rigaud E, Capek I, Andre-Fontaine G, Oster B, Gastinger G, Abadia G, 2008. Seroprevalence of Lyme borreliosis and tick-borne encephalitis in workers at risk, in eastern France. Med Mal Infect 38:533-42.
DOI: https://doi.org/10.1016/j.medmal.2008.06.008
Tsao JI, Hamer SA, Han S, Sidge JL, Hickling GJ, 2021. The contribution of wildlife hosts to the rise of ticks and tick-borne diseases in North America. J Med Entomol 58:1565-87.
DOI: https://doi.org/10.1093/jme/tjab047
Uusitalo R, Siljander M, Dub T, Sane J, Sormunen JJ, Pellikka P, Vapalahti O, 2020. Modelling habitat suitability for occurrence of human tick-borne encephalitis (TBE) cases in Finland. Ticks Tick-Borne Dis 11:101457.
DOI: https://doi.org/10.1016/j.ttbdis.2020.101457
Vanwambeke SO, Van Doninck J, Artois J, Davidson RK, Meyfroidt P, Jore S, 2016. Forest classes and tree cover gradient: tick habitat in encroached areas of southern Norway. Exp Appl Acarol 68:375-85.
DOI: https://doi.org/10.1007/s10493-015-0007-0
Vassallo M, Pichon B, Cabaret J, Figureau C, Pérez-Eid C, 2000. Methodology for sampling questing nymphs of Ixodes Ricinus(Acari: Ixodidae), the principal vector of Lyme disease in Europe. J Med Entomol 37:335-339.
DOI: https://doi.org/10.1093/jmedent/37.3.335
Vial L, Ducheyne E, Filatov S, Gerilovych A, McVey DS, Sindryakova I, Morgunov S, Pérez de León AA, Kolbasov D, De Clercq EM, 2018. Spatial multi-criteria decision analysis for modelling suitable habitats of Ornithodoros soft ticks in the Western Palearctic region. Vet Parasitol 249:2-16.
DOI: https://doi.org/10.1016/j.vetpar.2017.10.022
Vourc’h G, Abrial A, Bord S, Jacquot M, Masséglia S, Poux V, Pisanu B, Bailly X, Chapuis JL, 2016. Mapping human risk of infection with Borrelia burgdorferi sensu lato, the agent of Lyme borreliosis, in a periurban forest in France. Ticks Tick-Borne Dis 7:644-52.
DOI: https://doi.org/10.1016/j.ttbdis.2016.02.008
Wierzbicka A, Raczka G, Skorupski M, Michalik J, Lane RS, 2016. Human behaviors elevating the risk of exposure to Ixodes ricinus larvae and nymphs in two types of lowland coniferous forests in west-central Poland. Ticks Tick-Borne Dis 7:1180-5.
DOI: https://doi.org/10.1016/j.ttbdis.2016.07.018
Wongnak P, Bord S, Donnet S, Hoch T, Beugnet F, Chalvet-Monfray K, 2022a. A hierarchical Bayesian approach for incorporating expert opinions into parametric survival models: A case study of female Ixodes ricinus ticks exposed to various temperature and relative humidity conditions. Ecol Model 464:109821.
DOI: https://doi.org/10.1016/j.ecolmodel.2021.109821
Wongnak P, Jacquot M, Bord S, Agoulon A, Beugnet F, Bournez L, Cèbe N, Chevalier A, Cosson J-F, Dambrine N, Hoch T, Huard F, Huber K, Korboulewsky N, Lebert I, Madouasse A, Marell A, Moutailler S, Plantard O, Pollet T, Poux V, René-Martellet M, Stachurski F, Vayssier-Taussat M, Verheyden H, Vial L, Vourc’h G, Chalvet-Monfray K 2022. Dataset of Ixodes ricinus ticks in mainland France (CLIMATICK and CC-EID projects), Chalvet-Monfray K, ed. Portail Data INRAE 2022. doi:10.15454/ZSYGUM
Wongnak P, Bord S, Jacquot M, Agoulon A, Beugnet F, Bournez L, Cèbe N, Chevalier A, Cosson JF, Dambrine N, Hoch T, Huard F, Korboulewsky N, Lebert I, Madouasse A, Mårel A, Moutailler S, Plantard O, Pollet T, Poux V, René Martellet M, Vayssier Taussat M, Verheyden H, Vourc’h G, Chalvet Monfray K, 2022. Meteorological and climatic variables predict the phenology of Ixodes ricinus nymph activity in France, accounting for habitat heterogeneity. Sci Rep 12:7833. doi:10.1038/s41598-022-11479-z.
DOI: https://doi.org/10.1038/s41598-022-11479-z
Zeimes CB, Olsson GE, Hjertqvist M, Vanwambeke SO, 2014. Shaping zoonosis risk: landscape ecology vs. landscape attractiveness for people, the case of tick-borne encephalitis in Sweden. Parasites Vectors 7:370.
DOI: https://doi.org/10.1186/1756-3305-7-370
Zubriková D, Wittmann M, Hönig V, Švec P, Víchová B, Essbauer S, Dobler G, Grubhoffer L, Pfister K, 2020. Prevalence of tick-borne encephalitis virus and Borrelia burgdorferi sensu lato in Ixodes ricinus ticks in Lower Bavaria and Upper Palatinate, Germany. Ticks Tick-Borne Dis 11:101375.
DOI: https://doi.org/10.1016/j.ttbdis.2020.101375
How to Cite
Lebert, I., Bord, S. ., Saint-Andrieux, C., Cassar, E., Gasqui, P., Beugnet, F., Chalvet-Monfray, K., Vanwambeke, S. O., Vourc’h, G., & René-Martellet, M. (2022). Habitat suitability map of <em>Ixodes ricinus</em> tick in France using multi-criteria analysis. Geospatial Health, 17(1). https://doi.org/10.4081/gh.2022.1058
Copyright (c) 2022 the Author(s)
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
PAGEPress has chosen to apply the Creative Commons Attribution NonCommercial 4.0 International License (CC BY-NC 4.0) to all manuscripts to be published.
List of Cited By :
