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Comparative Study
. 2018 Dec 4;11(1):621.
doi: 10.1186/s13071-018-3200-2.

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

Caroline Millins  1   2   3 , Eleanor R Dickinson  4 , Petra Isakovic  4   5 , Lucy Gilbert  6 , Agnieszka Wojciechowska  4   7 , Victoria Paterson  4 , Feng Tao  4   8 , Martin Jahn  4   9 , Elizabeth Kilbride  4 , Richard Birtles  10 , Paul Johnson  4   11 , Roman Biek  4   11
Affiliations
Comparative Study

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

Caroline Millins et al. Parasit Vectors. .

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.

Keywords: Borrelia burgdorferi (sensu lato); Habitat fragmentation; Host community; Pathogen persistence.

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Not applicable.

Competing interests

The authors declare that they have no competing interests.

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Figures

Fig. 1
Fig. 1
Map of the study sites within Loch Lomond and the Trossachs National Park, Scotland, is shown by the box on the map on the left side of the figure. Loch Lomond is represented by the shaded area on the map on the right, the 12 islands within the loch which were sampled for questing Ixodes ricinus and 6 mainland sites are labelled. Site descriptions are in Table 1. Maps were drawn in ArcMap, ArcGIS version 10 (Esri, Redlands, USA)
Fig. 2
Fig. 2
Prevalence and genospecies of Borrelia burgdorferi (sensu lato) sampled at Loch Lomond and the Trossachs National Park, Scotland in 2011, 2013 and 2015. Grey squares indicate sites which were sampled, white squares indicate sites which were not sampled. The size of the circle is proportional to the log-prevalence of B. burgdorferi (s.l.), the colour indicates the genospecies present
See this image and copyright information in PMC

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