Impact of the experimental removal of lizards on Lyme disease risk

Department of Integrative Biology, University of California, 3060 Valley Life Sciences Building, Berkeley, CA 94720-3140, USA.
Proceedings of the Royal Society B: Biological Sciences (Impact Factor: 5.05). 02/2011; 278(1720):2970-8. DOI: 10.1098/rspb.2010.2402
Source: PubMed


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.

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    • "Juvenile ticks carrying Borrelia that feed on these lizards are cleansed of infection through complement-mediated innate immunity (Kuo et al. 2000). Recent attention has therefore focused on the role of S. occidentalis in Lyme disease ecology, and studies have shown that removal of S. occidentalis from oak woodland communities can have dramatic and complex effects on the prevalence of the bacteria (Swei et al. 2011). Studying the fine details of the Ixodes feeding mechanisms and the responses of the host may help elucidate the complexities inherent in this host–parasite relationship. "
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    ABSTRACT: The western black-legged tick (Ixodes pacificus) is a common tick species throughout the western USA and is the major vector for Borrelia burgdorferi, the Lyme disease causing bacterium. Western fence lizards (Sceloporus occidentalis) are a major host for juvenile I. pacificus, but are incompetent hosts for B. burgdorferi, which makes this host-parasite relationship of particular interest. In order to shed further light on this complex host-parasite relationship, we investigated the effects of temperature on feeding duration (number of days to repletion), success (number feeding to repletion), and efficiency (replete tick mass) of larval I. pacificus. Western fence lizards were experimentally infested with larval ticks and exposed to three constant temperatures (21, 27, 33 °C). Larvae feeding at 21 °C took approximately twice as long as larvae at 27 and 33 °C. Effects of temperature on feeding duration are likely mediated through effects on host blood circulation and functionality of tick salivary proteins. Our results here suggest temperature is another important factor influencing the feeding dynamics of I. pacificus, and likely other tick species. Future research is needed to clarify the exact mechanisms behind temperature effects on tick feeding.
    Experimental and Applied Acarology 07/2015; 67(2). DOI:10.1007/s10493-015-9950-z · 1.62 Impact Factor
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    • "This effect has been demonstrated empirically for western fence lizards (Sceloporus occidentalis ), which are non-competent hosts for Borrelia burgdorferi in California. Because lizards provide meals for ticks, experimental removal of lizards reduces infected tick density (Swei et al. 2011), which suggests that this non-competent host increases disease risk for humans. "
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    ABSTRACT: Control of human infectious disease has been promoted as a valuable ecosystem service arising from the conservation of biodiversity. There are two commonly discussed mechanisms by which biodiversity loss could increase rates of infectious disease in a landscape. First, loss of competitors or predators could facilitate an increase in the abundance of competent reservoir hosts. Second, biodiversity loss could disproportionately affect non-competent, or less competent reservoir hosts, which would otherwise interfere with pathogen transmission to human populations by, for example, wasting the bites of infected vectors. A negative association between biodiversity and disease risk, sometimes called the "dilution effect hypothesis," has been supported for a few disease agents, suggests an exciting win-win outcome for the environment and society, and has become a pervasive topic in the disease ecology literature. Case studies have been assembled to argue that the dilution effect is general across disease agents. Less touted are examples in which elevated biodiversity does not affect or increases infectious disease risk for pathogens of public health concern. In order to assess the likely generality of the dilution effect, we review the association between biodiversity and public health across a broad variety of human disease agents. Overall, we hypothesize that conditions for the dilution effect are unlikely to be met for most important diseases of humans. Biodiversity probably has little net effect on most human infectious diseases but, when it does have an effect, observation and basic logic suggest that biodiversity will be more likely to increase than to decrease infectious disease risk.
    Ecology 04/2014; 95(4):817-32. DOI:10.1890/13-1041.1 · 4.66 Impact Factor
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    • "Due to the host generalist behaviour of I. scapularis, increasing diversity of animal host species increases the possibility that ticks are diverted away from P. leucopus onto animals that are less efficient reservoirs of B. burgdorferi, which could result in a dilution effect [24]. However, the increased abundance of hosts associated with increasing biodiversity would likely boost abundance of ticks (which are obligate parasites at all feeding life stages), which calls into question the existence of a consistent inverse relationship between host biodiversity and tick and tick-borne pathogen abundance [25,26]. "
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    ABSTRACT: It has been suggested that increasing biodiversity, specifically host diversity, reduces pathogen and parasite transmission amongst wildlife (causing a "dilution effect"), whereby transmission amongst efficient reservoir hosts, (e.g. Peromyscus spp. mice for the agent of Lyme disease Borrelia burgdorferi) is reduced by the presence of other less efficient host species. If so, then increasing biodiversity should inhibit pathogen and parasite invasion. We investigated this hypothesis by studying invasion of B. burgdorferi and its tick vector Ixodes scapularis in 71 field sites in southeastern Canada. Indices of trapped rodent host diversity, and of biodiversity of the wider community, were investigated as variables explaining the numbers of I. scapularis collected and B. burgdorferi infection in these ticks. A wide range of alternative environmental explanatory variables were also considered. The observation of low I. scapularis abundance and low B. burgdorferi infection prevalence in sites where I. scapularis were detected was consistent with early-stage invasion of the vector. There were significant associations between the abundance of ticks and season, year of study and ambient temperature. Abundance of host-seeking larvae was significantly associated with deer density, and abundance of host-seeking larvae and nymphs were positively associated with litter layer depth. Larval host infestations were lower where the relative proportion of non-Peromyscus spp. was high. Infestations of hosts with nymphs were lower when host species richness was higher, but overall nymphal abundance increased with species richness because Peromyscus spp. mouse abundance and host species richness were positively correlated. Nymphal infestations of hosts were lower where tree species richness was higher. B. burgdorferi infection prevalence in ticks varied significantly with an index of rates of migratory bird-borne vector and pathogen invasion. I. scapularis abundance and B. burgdorferi prevalence varied with explanatory variables in patterns consistent with the known biology of these species in general, and in the study region in particular. The evidence for a negative effect of host biodiversity on I. scapularis invasion was mixed. However, some evidence suggests that community biodiversity beyond just host diversity may have direct or indirect inhibitory effects on parasite invasion that warrant further study.
    Parasites & Vectors 07/2013; 6(1):195. DOI:10.1186/1756-3305-6-195 · 3.43 Impact Factor
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