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

Author(s):  
Sara Louise Gandy ◽  
Elizabeth Kilbride ◽  
Roman Biek ◽  
Caroline Millins ◽  
Lucy Gilbert

Abstract 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.

2021 ◽  
Vol 14 (1) ◽  
Author(s):  
Sara Gandy ◽  
Elizabeth Kilbride ◽  
Roman Biek ◽  
Caroline Millins ◽  
Lucy Gilbert

Abstract 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


2021 ◽  
Author(s):  
Sara Louise Gandy ◽  
Elizabeth Kilbride ◽  
Roman Biek ◽  
Caroline Millins ◽  
Lucy Gilbert

Abstract 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., resulting in potentially opposing effects on transmission. Here, we use a deer exclosure experiment to test three hypotheses for how high deer density shapes B. burgdorferi s.l. prevalence in ticks: (H1) high transmission on rodents due to higher tick densities; alternatively, (H2) low B. burgdorferi s.l. prevalence because more ticks feed on deer rather than transmission-competent rodents (dilution effect); (H3) ecological cascades, whereby lower vegetation decreases rodent abundance thus reducing transmission. Although we found support for all three mechanisms, prevalence was reduced almost 3-fold in high deer density plots compared to exclosures, suggesting that the dilution (H2) and cascade (H3) mechanisms outweighed the increased opportunities for transmission (H1). High deer density led to lower vegetation and fewer rodents, providing evidence for an ecological cascade. However, Lyme disease hazard (density of infected ticks) was increased 5-fold at high deer densities due to an 18-fold rise in tick density. This demonstrates that reproduction hosts like deer can drive up vector-borne disease hazard at high densities, despite simultaneously reducing pathogen prevalence.


2000 ◽  
Vol 78 (12) ◽  
pp. 2061-2078 ◽  
Author(s):  
Richard S Ostfeld ◽  
Felicia Keesing

This is a critical evaluation of the influence of species diversity within communities of vertebrates on the risk of human exposure to vector-borne zoonoses. Vertebrates serve as natural reservoirs of many disease agents (viral, bacterial, protozoal) that are transmitted to humans by blood-feeding arthropod vectors. We describe the natural history of the Lyme disease zoonosis to illustrate interactions among pathogens, vectors, vertebrate hosts, and risk to humans. We then describe how the presence of a diverse assemblage of vertebrates can dilute the impact of the principal reservoir (the white-footed mouse, Peromyscus leucopus) of Lyme disease spirochetes (Borrelia burgdorferi), thereby reducing the disease risk to humans. Exploring the logic of what we call the dilution effect reveals four conditions that are necessary for it to apply generally to vector-borne zoonoses: (1) the feeding habits of the vector are generalized; (2) the pathogen is acquired by the vector from hosts (as opposed to exclusively transovarial transmission); (3) reservoir competence (the ability of a particular host species to infect a vector) varies among host species; and (4) the most competent reservoir host tends to be a community dominant, as defined by the proportion of the tick population fed by that species. When these conditions are met, vertebrate communities with high species diversity will contain a greater proportion of incompetent reservoir hosts that deflect vector meals away from the most competent reservoirs, thereby reducing infection prevalence and disease risk. Incorporating the likelihood that the abundance of competent reservoirs is reduced in more diverse communities, owing to the presence of predators and competitors, reinforces the impact of the dilution effect on the density of infected vectors. A review of the literature reveals the generality, though not the universality, of these conditions, which suggests that the effects of diversity on disease risk may be widespread. Issues in need of further exploration include (i) the relative importance of diversity per se versus fluctuating numbers of particular species; (ii) the relevance of species richness versus evenness to the dilution effect; (iii) whether the dilution effect operates at both local and regional scales; and (iv) the shape of empirically determined curves relating diversity to measures of disease risk. Further studies linking community ecology with epidemiology are warranted.


Parasitology ◽  
2016 ◽  
Vol 143 (10) ◽  
pp. 1310-1319 ◽  
Author(s):  
SANNE C. RUYTS ◽  
EVY AMPOORTER ◽  
ELENA C. COIPAN ◽  
LANDER BAETEN ◽  
DIETER HEYLEN ◽  
...  

SUMMARYLyme disease is caused by bacteria of theBorrelia burgdorferigenospecies complex and transmitted by Ixodid ticks. In North America only one pathogenic genospecies occurs, in Europe there are several. According to the dilution effect hypothesis (DEH), formulated in North America, nymphal infection prevalence (NIP) decreases with increasing host diversity since host species differ in transmission potential. We analysedBorreliainfection in nymphs from 94 forest stands in Belgium, which are part of a diversification gradient with a supposedly related increasing host diversity: from pine stands without to oak stands with a shrub layer. We expected changing tree species and forest structure to increase host diversity and decrease NIP. In contrast with the DEH, NIP did not differ between different forest types. Genospecies diversity however, and presumably also host diversity, was higher in oak than in pine stands. Infected nymphs tended to harbourBorrelia afzeliiinfection more often in pine stands whileBorrelia gariniiandBorrelia burgdorferiss. infection appeared to be more prevalent in oak stands. This has important health consequences, since the latter two cause more severe disease manifestations. We show that the DEH must be nuanced for Europe and should consider the response of multiple pathogenic genospecies.


2011 ◽  
Vol 278 (1720) ◽  
pp. 2970-2978 ◽  
Author(s):  
Andrea Swei ◽  
Richard S. Ostfeld ◽  
Robert S. Lane ◽  
Cheryl J. Briggs

The distribution of vector meals in the host community is an important element of understanding and predicting vector-borne disease risk. Lizards (such as the western fence lizard; Sceloporus occidentalis ) play a unique role in Lyme disease ecology in the far-western United States. Lizards rather than mammals serve as the blood meal hosts for a large fraction of larval and nymphal western black-legged ticks ( Ixodes pacificus —the vector for Lyme disease in that region) but are not competent reservoirs for the pathogen, Borrelia burgdorferi . Prior studies have suggested that the net effect of lizards is to reduce risk of human exposure to Lyme disease, a hypothesis that we tested experimentally. Following experimental removal of lizards, we documented incomplete host switching by larval ticks (5.19%) from lizards to other hosts. Larval tick burdens increased on woodrats, a competent reservoir, but not on deer mice, a less competent pathogen reservoir. However, most larvae failed to find an alternate host. This resulted in significantly lower densities of nymphal ticks the following year. Unexpectedly, the removal of reservoir-incompetent lizards did not cause an increase in nymphal tick infection prevalence. The net result of lizard removal was a decrease in the density of infected nymphal ticks, and therefore a decreased risk to humans of Lyme disease. Our results indicate that an incompetent reservoir for a pathogen may, in fact, increase disease risk through the maintenance of higher vector density and therefore, higher density of infected vectors.


Author(s):  
Julia E Poje ◽  
Jose F Azevedo ◽  
Nisha Nair ◽  
Kurayi Mahachi ◽  
Lexi E Frank ◽  
...  

Abstract Lyme disease, caused by Borrelia burgdorferi sensu stricto and most commonly transmitted by Ixodes scapularis Say (Ixodida: Ixodidae), is the most common tick-borne disease in Maryland. Because B. burgdorferi s.s. is maintained in enzootic cycles among wild mice (Peromyscus spp) and Ixodes spp ticks, differing patterns of parasitism of ticks on mice could impact the infection prevalence with B. burgdorferi. We determined the infection prevalence of Peromyscus spp as well as questing and partially engorged nymphal ticks collected at six sites on private land in five counties in Maryland from May to August 2020. Questing nymph infection prevalence (NIP) was 14%. We trapped 1258 mice and collected 554 ticks and 413 ear tissue samples. The prevalence of infested Peromyscus spp varied based on host age and sex, with older and male mice more likely to be infested. We detected a significant difference amongst the proportion of attached Ixodes and the location of trapping. Similarly, the prevalence of B. burgdorferi infected Peromyscus spp mice varied between locations (average mouse infection prevalence was 40%), with the highest prevalence in locations where Ixodes were the most commonly found ticks. The B. burgdorferi infection prevalence in partially engorged I. scapularis nymphs retrieved from Peromyscus spp was ~36% which lends further support to the host infection prevalence. Local differences in distribution of infected vectors and reservoirs are important factors to consider when planning interventions to reduce Lyme disease risk.


2017 ◽  
Vol 372 (1722) ◽  
pp. 20160173 ◽  
Author(s):  
Christina L. Faust ◽  
Andrew P. Dobson ◽  
Nicole Gottdenker ◽  
Laura S. P. Bloomfield ◽  
Hamish I. McCallum ◽  
...  

As biodiversity declines with anthropogenic land-use change, it is increasingly important to understand how changing biodiversity affects infectious disease risk. The dilution effect hypothesis, which points to decreases in biodiversity as critical to an increase in infection risk, has received considerable attention due to the allure of a win–win scenario for conservation and human well-being. Yet some empirical data suggest that the dilution effect is not a generalizable phenomenon. We explore the response of pathogen transmission dynamics to changes in biodiversity that are driven by habitat loss using an allometrically scaled multi-host model. With this model, we show that declining habitat, and thus declining biodiversity, can lead to either increasing or decreasing infectious-disease risk, measured as endemic prevalence. Whether larger habitats, and thus greater biodiversity, lead to a decrease (dilution effect) or increase (amplification effect) in infection prevalence depends upon the pathogen transmission mode and how host competence scales with body size. Dilution effects were detected for most frequency-transmitted pathogens and amplification effects were detected for density-dependent pathogens. Amplification effects were also observed over a particular range of habitat loss in frequency-dependent pathogens when we assumed that host competence was greatest in large-bodied species. By contrast, only amplification effects were observed for density-dependent pathogens; host competency only affected the magnitude of the effect. These models can be used to guide future empirical studies of biodiversity–disease relationships across gradients of habitat loss. The type of transmission, the relationship between host competence and community assembly, the identity of hosts contributing to transmission, and how transmission scales with area are essential factors to consider when elucidating the mechanisms driving disease risk in shrinking habitat. This article is part of the themed issue ‘Conservation, biodiversity and infectious disease: scientific evidence and policy implications'.


2019 ◽  
Vol 57 (1) ◽  
pp. 273-280 ◽  
Author(s):  
Alison E Simmons ◽  
Anna B Manges ◽  
Tashi Bharathan ◽  
Shannon L Tepe ◽  
Sara E McBride ◽  
...  

Abstract Lyme disease is the most commonly reported vector-borne illness and sixth most commonly reported notifiable infectious disease in the United States. The majority of cases occur in the Northeast and upper-Midwest, and the number and geographic distribution of cases is steadily increasing. The blacklegged tick (Ixodes scapularis Say) is the principal vector of the Lyme disease spirochete (Borrelia burgdorferi sensu stricto) in eastern North America. Although Lyme disease risk has been studied in residential and recreational settings across rural to urban landscapes including metropolitan areas, risk within U.S. cities has not been adequately evaluated despite the presence of natural and undeveloped public parkland where visitors could be exposed to B. burgdorferi-infected I. scapularis. We studied the occurrence of I. scapularis and infection prevalence of B. burgdorferi in four insular regional parks within the city of Pittsburgh to assess Lyme disease risk of exposure to infected adults and nymphs. We found that the density of I. scapularis adults (1.16 ± 0.21 ticks/100 m2) and nymphs (3.42 ± 0.45 ticks/100 m2), infection prevalence of B. burgdorferi in adults (51.9%) and nymphs (19.3%), and density of infected adults (0.60 ticks/100 m2) and nymphs (0.66 ticks/100 m2) are as high in these city parks as nonurban residential and recreational areas in the highly endemic coastal Northeast. These findings emphasize the need to reconsider, assess, and manage Lyme disease risk in greenspaces within cities, especially in high Lyme disease incidence states.


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