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

Millins, C. et al. (2018) Landscape structure affects the prevalence and distribution of a tick-borne zoonotic pathogen. Parasites and Vectors, 11, 621. (doi:10.1186/s13071-018-3200-2) (PMID:30514350) (PMCID:PMC6278045)

Millins, C. et al. (2018) Landscape structure affects the prevalence and distribution of a tick-borne zoonotic pathogen. Parasites and Vectors, 11, 621. (doi:10.1186/s13071-018-3200-2) (PMID:30514350) (PMCID:PMC6278045)

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Abstract

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.

Item Type:Articles
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Paterson, Dr Victoria and Isakovic, Miss Petra and Dickinson, Miss Eleanor and Biek, Dr Roman and Johnson, Dr Paul and Kilbride, Mrs Elizabeth and Gilbert, Dr Lucy and Millins, Dr Caroline
Authors: Millins, C., Dickinson, E. R., Isakovic, P., Gilbert, L., Wojciechowska, A., Paterson, V., Tao, F., Jahn, M., Kilbride, E., Birtles, R., Johnson, P., and Biek, R.
College/School:College of Medical Veterinary and Life Sciences > Institute of Biodiversity Animal Health and Comparative Medicine
College of Medical Veterinary and Life Sciences > School of Veterinary Medicine
Journal Name:Parasites and Vectors
Publisher:BioMed Central
ISSN:1756-3305
ISSN (Online):1756-3305
Copyright Holders:Copyright © 2018 The Authors
First Published:First published in Parasites and Vectors 11: 621
Publisher Policy:Reproduced under a Creative Commons License

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Project CodeAward NoProject NamePrincipal InvestigatorFunder's NameFunder RefLead Dept
500194BBSRC Doctoral Training Grant 2009-15Massimo PalmariniBiotechnology and Biological Sciences Research Council (BBSRC)BB/F016786/1MVLS III - CENTRE FOR VIRUS RESEARCH
482721Effects of host population size and isolation on parasite distribution in a naturally fragmented host-metapopulationRoman BiekNatural Environment Research Council (NERC)NE/G000786/1RI BIODIVERSITY ANIMAL HEALTH & COMPMED