Emergence of Lyme disease on treeless islands in Scotland, UK

Millins, Caroline; Leo, Walter; MacInnes, Isabell; Ferguson, Johanne; Charlesworth, Graham; Nayar, Donald; Davison, Reece; Yardley, Jonathan; Kilbride, Elizabeth; Huntley, Selene J.; Gilbert, Lucy; Viana, Mafalda; Johnson, Paul C. D.; Biek, Roman

doi:10.1101/2020.08.31.263319

Cited by 3 publications

(5 citation statements)

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“…The small spatial scale of our plots, while a potential issue for con rming a link between rodent abundance and NIP, proved su cient to demonstrate effects of high deer density on DON, vegetation height and rodent activity, and ultimately, Lyme disease hazard. While a previous meta-analysis of deer exclusion effects on tick abundance (14) suggested that deer exclusion areas of at least 2.5 ha may be necessary to have an effect, our results show smaller plots sizes to be su cient for revealing strong spatial gradients and for testing impacts of deer on ticks, consistent with other more recent studies (Gilbert et Irrespective of the mechanisms driving NIP, the most critical parameter governing public health and policy importance for Lyme disease is the density of infected nymphs (DIN=NIP x DON), which is the key proxy for Lyme disease hazard in the environment (29). DIN was ve times higher in high deer density plots compared to exclosures due to deer having a strong positive effect on DON.…”

Section: Discussionsupporting

confidence: 90%

“…These different mechanisms are not mutually exclusive and the effect of high deer density on NIP will depend on the relative strength of the rst (transmission potential) mechanism compared to the other two (dilution and ecological cascade mechanisms) (Figure 1). A further key aim was to test the impact of high deer density on Lyme disease hazard, which is de ned as the density of infected nymphs (DIN) in the environment and is the product of NIP and DON (29). It is di cult to predict the effect of deer on Lyme disease hazard because it will depend on the relative strengths of the effect of deer on DON and the mechanisms driving NIP (Figure 1).…”

Section: Introductionmentioning

confidence: 99%

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Experimental Evidence for Opposing Effects of High Deer Density on Tick-Borne Pathogen Prevalence and Hazard

Gandy

Kilbride

Biek

et al. 2021

Preprint

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Background: Identifying the mechanisms driving disease risk is challenging for multi-host pathogens, such as Borrelia burgdorferi s.l., the tick-borne bacteria causing Lyme disease. Deer are tick reproduction hosts but do not transmit B. burgdorferi s.l., whereas rodents and birds are competent transmission hosts. Here, we use a long-term deer exclosure experiment to test three mechanisms for how high deer density might shape B. burgdorferi s.l. prevalence in ticks: increased prevalence due to higher larval tick densities facilitating high transmission on rodents (M1); alternatively, reduced B. burgdorferi s.l. prevalence because more larval ticks feed on deer rather than transmission-competent rodents (dilution effect) (M2), potentially due to ecological cascades, whereby higher deer grazing pressure lowers vegetation which decreases rodent abundance thus reducing transmission (M3).Methods: In a large enclosure where red deer stags were kept at high density (32.5 deer/km²), we used an experimental design consisting of eight plots of 0.23ha, four being fenced to simulate the absence of deer and four that were accessible to deer. In each plot we measured the density of questing nymphs and nymphal infection prevalence in spring, summer and autumn and quantified vegetation height and density, and small mammal abundance Results: Prevalence tended to be lower, though not conclusively so, in high deer density plots compared to exclosures (predicted prevalence of 1.0% vs 2.2%), suggesting that the dilution (M2) and cascade (M3) mechanisms might outweigh the increased opportunities for transmission (M1). Presence of deer at high density led to lower vegetation and fewer rodents, consistent with an ecological cascade. However, Lyme disease hazard (density of infected I. ricinus nymphs) was five times higher in high deer density plots due to tick density being 18 times higher.Conclusion: High densities of tick reproduction hosts such as deer can drive up vector-borne disease hazard, despite the potential to simultaneously reduce pathogen prevalence. This has implications for environmental pathogen management and for deer management, although the impact of intermediate deer densities now needs testing.

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Section: Discussionsupporting

confidence: 90%

Section: Introductionmentioning

confidence: 99%

Experimental Evidence for Opposing Effects of High Deer Density on Tick-Borne Pathogen Prevalence and Hazard

Gandy

Kilbride

Biek

et al. 2021

Preprint

Self Cite

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“…genospecies were found in all years, at both sites, with a minimum overall prevalence of 12.6%. This compares with overall Borrelia prevalences of I. ricinus of 1.7% (range 0–6.0%) detected in questing nymphs sampled at multiple sites across mainland Scotland and the Isle of Mull [ 25 ], 6.4% and 0.7% in questing nymphs at sites of, respectively, high and low Lyme disease incidence in the Outer Hebrides [ 26 ], 3.2% (range 0–5.6%) in questing nymphs and adults at four sites in England [ 27 ], 19.0% (range 0–24.5%) in questing nymphs collected over three years at sites in a single area of southern England [ 28 ] and 3.8% (range 0–24.0%) in questing ticks collected over six years at 20 sites in recreational areas of England and Wales [ 29 ]. In the two last-mentioned studies, significant variation was seen in tick infection rates between years [ 28 , 29 ]; on Brownsea Island, where ticks were sampled in both Spring and Autumn, the minimum overall prevalence of Borrelia infection was 9.9% in 2017 compared with 21.3% in 2018.…”

Section: Discussionmentioning

confidence: 84%

Bacterial Pathogens and Symbionts Harboured by Ixodes ricinus Ticks Parasitising Red Squirrels in the United Kingdom

et al. 2021

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Red squirrels (Sciurus vulgaris) are native to most of Eurasia; in much of the United Kingdom, they have been supplanted by the non-native grey squirrel, and are considered an endangered species. Very little is known about the range of tick-borne pathogens to which UK red squirrels are exposed. As part of trap-and-release surveys examining prevalence of Mycobacterium spp. in red squirrel populations on two UK islands, Ixodes ricinus ticks were removed from squirrels and PCR screened for Borrelia spp., intracellular arthropod-borne bacteria and the parasitic wasp Ixodiphagus hookeri. At both sites, the most commonly encountered tick-transmitted bacterium was Borrelia burgdorferi sensu lato (overall minimum prevalence 12.7%), followed by Anaplasma phagocytophilum (overall minimum prevalence 1.6%). Single ticks infected with Spiroplasma were found at both sites, and single ticks infected with Borrelia miyamotoi or an Ehrlichia sp. at one site. Ticks harbouring Wolbachia (overall minimum prevalence 15.2%) were all positive for I. hookeri. Our study shows that UK red squirrels are potentially exposed to a variety of bacterial pathogens via feeding ticks. The effects on the health and survival of this already vulnerable wildlife species are unknown, and further studies are needed to evaluate the threat posed to red squirrels by Borrelia and other tick-borne pathogens.

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“…Irrespective of the mechanisms driving NIP, the most critical parameter governing public health and policy importance for Lyme disease is the DIN (= NIP × DON), which is the key proxy for Lyme disease hazard in the environment [29]. DIN was five times higher in high deer density plots compared to exclosures due to deer having a strong positive effect on DON.…”

Section: Discussionmentioning

confidence: 99%

“…1). A further key aim was to test the impact of high deer density on Lyme disease hazard, which is defined as the DIN in the environment and is the product of NIP and DON [29]. It is difficult to predict the effect of deer on Lyme disease hazard because it will depend on the relative strengths of the effect of deer on DON and the mechanisms driving NIP (Fig.…”

Section: Introductionmentioning

confidence: 99%

Experimental evidence for opposing effects of high deer density on tick-borne pathogen prevalence and hazard

et al. 2021

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Background Identifying the mechanisms driving disease risk is challenging for multi-host pathogens, such as Borrelia burgdorferi sensu lato (s.l.), the tick-borne bacteria causing Lyme disease. Deer are tick reproduction hosts but do not transmit B. burgdorferi s.l., whereas rodents and birds are competent transmission hosts. Here, we use a long-term deer exclosure experiment to test three mechanisms for how high deer density might shape B. burgdorferi s.l. prevalence in ticks: increased prevalence due to higher larval tick densities facilitating high transmission on rodents (M1); alternatively, reduced B. burgdorferi s.l. prevalence because more larval ticks feed on deer rather than transmission-competent rodents (dilution effect) (M2), potentially due to ecological cascades, whereby higher deer grazing pressure shortens vegetation which decreases rodent abundance thus reducing transmission (M3). Methods In a large enclosure where red deer stags were kept at high density (35.5 deer km−2), we used an experimental design consisting of eight plots of 0.23 ha, four of which were fenced to simulate the absence of deer and four that were accessible to deer. In each plot we measured the density of questing nymphs and nymphal infection prevalence in spring, summer and autumn, and quantified vegetation height and density, and small mammal abundance. Results Prevalence tended to be lower, though not conclusively so, in high deer density plots compared to exclosures (predicted prevalence of 1.0% vs 2.2%), suggesting that the dilution and cascade mechanisms might outweigh the increased opportunities for transmission mechanism. Presence of deer at high density led to shorter vegetation and fewer rodents, consistent with an ecological cascade. However, Lyme disease hazard (density of infected I. ricinus nymphs) was five times higher in high deer density plots due to tick density being 18 times higher. Conclusions High densities of tick reproduction hosts such as deer can drive up vector-borne disease hazard, despite the potential to simultaneously reduce pathogen prevalence. This has implications for environmental pathogen management and for deer management, although the impact of intermediate deer densities now needs testing. Graphical abstract

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Emergence of Lyme disease on treeless islands in Scotland, UK

Cited by 3 publications

References 43 publications

Experimental Evidence for Opposing Effects of High Deer Density on Tick-Borne Pathogen Prevalence and Hazard

Experimental Evidence for Opposing Effects of High Deer Density on Tick-Borne Pathogen Prevalence and Hazard

Bacterial Pathogens and Symbionts Harboured by Ixodes ricinus Ticks Parasitising Red Squirrels in the United Kingdom

Experimental evidence for opposing effects of high deer density on tick-borne pathogen prevalence and hazard

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