Blood meal analysis reveals sources of tick-borne pathogens and differences in host utilization of juvenile Ixodes ricinus across urban and sylvatic habitats.
Borrelia
Ixodes ricinus
blood meal
host
tick-borne pathogens
urban green space
Journal
Zoonoses and public health
ISSN: 1863-2378
Titre abrégé: Zoonoses Public Health
Pays: Germany
ID NLM: 101300786
Informations de publication
Date de publication:
14 Mar 2024
14 Mar 2024
Historique:
revised:
22
02
2024
received:
25
01
2024
accepted:
06
03
2024
medline:
15
3
2024
pubmed:
15
3
2024
entrez:
14
3
2024
Statut:
aheadofprint
Résumé
Urban green spaces are locations of maximal human activity, forming areas of enhanced risk for tick-borne disease (TBD) transmission. Being also limited in spatial scale, green spaces form prime targets for control schemes aiming to reduce TBD risk. However, for effective control, the key species maintaining local tick and tick-borne pathogen (TBP) populations must be identified. To determine how patterns of host utilization vary spatially, we utilized blood meal analysis to study the contributions of voles, shrews, squirrels, leporids and cervids towards blood meals and the acquisition of TBPs of juvenile Ixodes ricinus in urban and sylvatic areas in Finland. A total of 1084 nymphs were collected from the capital city of Finland, Helsinki and from a sylvatic island in southwestern Finland, and subjected to qPCR analysis to identify DNA remnants of the previous host. We found significant differences in host contributions between urban and sylvatic environments. Specifically, squirrels and leporids were more common hosts in urban habitats, whereas cervids and voles were more common in sylvatic habitats. In addition to providing 18.4% of larval blood meals in urban habitats, red squirrels were identified as the source of 28.6% (n = 48) of Borrelia afzelii detections and 58.1% (n = 18) of Borrelia burgdorferi sensu stricto detections, indicating an important role for local enzootic cycles. Our study highlights that the key hosts maintaining tick and TBP populations may be different in urban and sylvatic habitats. Likewise, hosts generally perceived as important for upkeep may have limited importance in urban environments. Consequently, targeting control schemes based on off-site data of host importance may lead to suboptimal results.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Maj ja Tor Nesslingin Säätiö
Organisme : Suomen Kulttuurirahasto
Organisme : Sakari Alhopuron Säätiö
Informations de copyright
© 2024 The Authors. Zoonoses and Public Health published by Wiley-VCH GmbH.
Références
Andersson, M., Bartkova, S., Lindestad, O., & Råberg, L. (2013). Co-infection with ‘Candidatus Neoehrlichia mikurensis’ and Borrelia afzelii in Ixodes ricinus ticks in southern Sweden. Vector Borne and Zoonotic Diseases, 13, 438-442. https://doi.org/10.1089/vbz.2012.1118
Andersson, M., & Råberg, L. (2011). Wild rodents and novel human pathogen Candidatus Neoehrlichia mikurensis, southern Sweden. Emerging Infectious Diseases, 17, 1716-1718. https://doi.org/10.3201/eid1709.101058
Borland, E. M., & Kading, R. C. (2021). Modernizing the toolkit for arthropod bloodmeal identification. Insects, 12(37), 1-27. https://doi.org/10.3390/insects12010037
Bown, K. J., Lambin, X., Telford, G., Heyder-Bruckner, D., Ogden, N. H., & Birtles, R. J. (2011). The common shrew (Sorex araneus): A neglected host of tick-borne infections? Vector Borne and Zoonotic Diseases, 11, 947-953. https://doi.org/10.1089/vbz.2010.0185
Casjens, S. R., Fraser-Liggett, C. M., Mongodin, E. F., Qiu, W. G., Dunn, J. J., Luft, B. J., & Schutzer, S. E. (2011). Whole genome sequence of an unusual Borrelia burgdorferi sensu lato isolate. Journal of Bacteriology, 193, 1489-1490.
Collini, M., Albonico, F., Hauffe, H. C., & Mortarino, M. (2015). Identifying the last bloodmeal of questing sheep tick nymphs (Ixodes ricinus L.) using high resolution melting analysis. Veterinary Parasitology, 210, 194-205.
Dolan, M. C., Schulze, T. L., Jordan, R. A., Schulze, C. J., Ullmann, A. J., Hojgaard, A., Williams, M. A., & Piesman, J. (2017). Evaluation of doxycycline-laden oral bait and topical fipronil delivered in a single bait box to control Ixodes scapularis (Acari: Ixodidae) and reduce Borrelia burgdorferi and Anaplasma phagocytophilum infection in small mammal reservoirs and host-seeking ticks. Journal of Medical Entomology, 54, 403-410. https://doi.org/10.1093/jme/tjw194
ECDC. (2020). Tick-borne encephalitis Annual Epidemiological Report for 2020 key facts.
Eötvös, C. B., Magura, T., & Lövei, G. L. (2018). A meta-analysis indicates reduced predation pressure with increasing urbanization. Landscape and Urban Planning, 180, 54-59. https://doi.org/10.1016/j.landurbplan.2018.08.010
Estrada-Peña, A., Mihalca, A. D., & Petney, T. N. (2018). Ticks of Europe and North Africa: A guide to species identification. Springer.
Gering, J. C., & Blair, R. B. (1999). Predation on artificial bird nests along an urban gradient: Predatory risk or relaxation in urban environments? Ecography, 22, 532-541.
Goethert, H. K., Mather, T. N., Buchthal, J., & Telford, S. R., III. (2021). Retrotransposon-based blood meal analysis of nymphal deer ticks demonstrates spatiotemporal diversity of Borrelia burgdorferi and Babesia microti reservoirs. Applied and Environmental Microbiology, 87, 1-15.
Grochowska, A., Milewski, R., Pancewicz, S., Dunaj, J., Czupryna, P., Milewska, A. J., Róg-Makal, M., Grygorczuk, S., & Moniuszko-Malinowska, A. (2020). Comparison of tick-borne pathogen prevalence in Ixodes ricinus ticks collected in urban areas of Europe. Scientific Reports, 10(1), 6975. https://doi.org/10.1038/s41598-020-63883-y
Hanincova, K., Schäfer, S. M., Etti, S., Sewell, H. S., Taragelová, V., Ziak, D., Labuda, M., & Kurtenbach, K. (2003). Association of Borrelia afzelii with rodents in Europe. Parasitology, 126, 11-20.
Hansford, K. M., Fonville, M., Gillingham, E. L., Coipan, E. C., Pietzsch, M. E., Krawczyk, A. I., Vaux, A. G. C., Cull, B., Sprong, H., & Medlock, J. M. (2017). Ticks and Borrelia in urban and peri-urban green space habitats in a city in southern England. Ticks and Tick-borne Diseases, 8, 353-361.
Hansford, K. M., Wheeler, B. W., Tschirren, B., & Medlock, J. M. (2022). Questing Ixodes ricinus ticks and Borrelia spp. in urban green space across Europe: A review. Zoonoses and Public Health, 69, 153-166.
Hauck, D., Jordan, D., Springer, A., Schunack, B., Pachnicke, S., Fingerle, V., & Strube, C. (2020). Transovarial transmission of Borrelia spp., Rickettsia spp. and Anaplasma phagocytophilum in Ixodes ricinus under field conditions extrapolated from DNA detection in questing larvae. Parasites & Vectors, 13, 176. https://doi.org/10.1186/s13071-020-04049-7
Hayes, S. F., Burgdorfer, W., & Aeschlimann, A. (1980). Sexual transmission of spotted fever group rickettsiae by infected male ticks: Detection of rickettsiae in immature spermatozoa of Ixodes ricinus. Infection and Immunity, 27(2), 638-642.
Humair, P.-F., & Gern, L. (1998). Relationship between Borrelia burgdorferi sensu lato species, red squirrels (Sciurus vulgaris) and Ixodes ricinus in enzootic areas in Switzerland. Acta Tropica, 69, 213-227.
Jaenson, T. G. T., & Talleklint, L. (1996). Lyme borreliosis spirochetes in Ixodes ricinus (Acari: Ixodidae) and the varying hare on isolated islands in the Baltic Sea. Journal of Medical Entomology, 33(3), 339-343. https://doi.org/10.1093/jmedent/33.3.339
Jędrzejewski, W., Rychlik, L., & Jędrzejewska, B. (1993). Responses of bank voles to odours of seven species of predators: Experimental data and their relevance to natural predator-vole relationships. Oikos, 68(2), 251-257. https://doi.org/10.2307/3544837
Jokimäki, J., Selonen, V., Lehikoinen, A., & Kaisanlahti-Jokimäki, M. L. (2017). The role of urban habitats in the abundance of red squirrels (Sciurus vulgaris, L.) in Finland. Urban Forestry & Urban Greening, 27, 100-108.
Kahl, O., & Gray, J. S. (2023). The biology of Ixodes ricinus with emphasis on its ecology. Ticks and Tick-borne Diseases, 14(2), 102114. https://doi.org/10.1016/j.ttbdis.2022.102114
Kim, H. H. (1992). Urban heat island. International Journal of Remote Sensing, 13, 2319-2336.
Kokkonen, A. (2022). Valkohäntäpeurojen (Odocoileus virginianus) ja metsäkauriiden (Capreolus capreolus) tiheyden vaikutus alueen puutiaisten (Ixodes ricinus) määrään ja puutiaisten kantamien taudinaiheuttajien esiintyvyyteen riistaruokintapaikkojen läheisyydessä ja kontrollialueilla [The effect of population densities of white-tailed deer and roe deer on Ixodes ricinus tick prevalence and tick-borne pathogen prevalence near feeding and control areas] (Master's thesis). University of Turku (Finnish).
Korpimaki, E., Koivunen, V., & Hakkarainen, H. (1995). Microhabitat use and behavior of voles under weasel and raptor predation risk: Predator facilitation? Behavioral Ecology, 7(1), 30-34. https://doi.org/10.1093/beheco/7.1.30
Kurtenbach, K., De Michelis, S., Etti, S., Schäfer, S. M., Sewell, H. S., Brade, V., & Kraiczy, P. (2002). Host association of Borrelia burgdorferi sensu lato-The key role of host complement. Trends in Microbiology, 10(2), 74-79.
Mancini, F., Di Luca, M., Toma, L., Vescio, F., Bianchi, R., Khoury, C., Marini, L., Rezza, G., & Ciervo, A. (2014). Prevalence of tick-borne pathogens in an urban park in Rome, Italy. Annals of Agricultural and Environmental Medicine, 21, 723-727.
Marques, A. R., Strle, F., & Wormser, G. P. (2021). Comparison of Lyme disease in the United States and Europe. Emerging Infectious Diseases, 27, 2017-2024.
Mather, T. N., Nicholson, M. C., Donnelly, E. F., & Matyas, B. T. (1996). A brief original contribution entomologic index for human risk of Lyme disease. American Journal of Epidemiology, 144, 1066-1069. https://doi.org/10.1093/oxfordjournals.aje.a008879
Mysterud, A., Byrkjeland, R., Qviller, L., & Viljugrein, H. (2015). The generalist tick Ixodes ricinus and the specialist tick Ixodes trianguliceps on shrews and rodents in a northern forest ecosystem - A role of body size even among small hosts. Parasites & Vectors, 8, 639. https://doi.org/10.1186/s13071-015-1258-7
Olsén, B., Jaenson, T. G. T., & Bergström, S. (1995). Prevalence of Borrelia burgdorferi sensu lato-infected ticks on migrating birds. Applied and Environmental Microbiology, 61(8), 3082-3087. https://doi.org/10.1128/aem.61.8.3082-3087.1995
Pisanu, B., Chapuis, J. L., Dozières, A., Basset, F., Poux, V., & Vourc'h, G. (2014). High prevalence of Borrelia burgdorferi s.l. in the European red squirrel Sciurus vulgaris in France. Ticks and Tick-borne Diseases, 5, 1-6.
Plumer, L., Davison, J., & Saarma, U. (2014). Rapid urbanization of red foxes in Estonia: Distribution, behaviour, attacks on domestic animals, and health-risks related to zoonotic diseases. PLoS One, 9(12), e115124. https://doi.org/10.1371/journal.pone.0115124
Rizzoli, A., Silaghi, C., Obiegala, A., Rudolf, I., Hubálek, Z., Földvári, G., Plantard, O., Vayssier-Taussat, M., Bonnet, S., Spitalská, E., & Kazimírová, M. (2014). Ixodes ricinus and its transmitted pathogens in urban and peri-urban areas in Europe: New hazards and relevance for public health. Frontiers in Public Health, 2(251), 1-26. https://doi.org/10.3389/fpubh.2014.00251
Schulze, T. L., Jordan, R. A., Williams, M., & Dolan, M. C. (2017). Evaluation of the SELECT tick control system (TCS), a host-targeted bait box, to reduce exposure to Ixodes scapularis (Acari: Ixodidae) in a Lyme disease endemic area of New Jersey. Journal of Medical Entomology, 54, 1019-1024. https://doi.org/10.1093/jme/tjx044
Sonenshine, D. E., & Roe, M. R. (2013). Biology of ticks (p. 2). Oxford University Press, Incorporated.
Sormunen, J. J., Kulha, N., Klemola, T., Mäkelä, S., Vesilahti, E. M., & Vesterinen, E. J. (2020). Enhanced threat of tick-borne infections within cities? Assessing public health risks due to ticks in urban green spaces in Helsinki, Finland. Zoonoses and Public Health, 67, 823-839. https://doi.org/10.1111/zph.12767
Sormunen, J. J., Mäkelä, S., Klemola, T., Alale, T. Y., & Vesterinen, E. J. (2023). Voles, shrews and red squirrels as sources of tick blood meals and tick-borne pathogens on an island in southwestern Finland. Ticks and Tick-borne Diseases, 14, 102134. https://doi.org/10.1016/j.ttbdis.2023.102134
Strnad, M., Hönig, V., Růžek, D., Grubhoffer, L., & Rego, R. O. M. (2017). Europe-wide meta-analysis of Borrelia burgdorferi sensu lato prevalence in questing Ixodes ricinus ticks. Applied and Environmental Microbiology, 83(15), e00609-17. https://doi.org/10.1128/AEM.00609-17
Tapper, S. C., & Barnes, R. F. W. (1986). Influence of farming practice on the ecology of the brown hare (Lepus europaeus). Journal of Applied Ecology, 23(1), 39-52.
Tazerji, S. S., Nardini, R., Safdar, M., Shehata, A. A., & Duarte, P. M. (2022). An overview of anthropogenic actions as drivers for emerging and re-emerging zoonotic diseases. Pathogens, 11, 1-26. https://doi.org/10.3390/pathogens11111376
Voordouw, M. J. (2015). Co-feeding transmission in Lyme disease pathogens. Parasitology, 142, 290-302.