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      Climate, Deer, Rodents, and Acorns as Determinants of Variation in Lyme-Disease Risk

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          Abstract

          Risk of human exposure to vector-borne zoonotic pathogens is a function of the abundance and infection prevalence of vectors. We assessed the determinants of Lyme-disease risk (density and Borrelia burgdorferi-infection prevalence of nymphal Ixodes scapularis ticks) over 13 y on several field plots within eastern deciduous forests in the epicenter of US Lyme disease (Dutchess County, New York). We used a model comparison approach to simultaneously test the importance of ambient growing-season temperature, precipitation, two indices of deer (Odocoileus virginianus) abundance, and densities of white-footed mice (Peromyscus leucopus), eastern chipmunks (Tamias striatus), and acorns ( Quercus spp.), in both simple and multiple regression models, in predicting entomological risk. Indices of deer abundance had no predictive power, and precipitation in the current year and temperature in the prior year had only weak effects on entomological risk. The strongest predictors of a current year's risk were the prior year's abundance of mice and chipmunks and abundance of acorns 2 y previously. In no case did inclusion of deer or climate variables improve the predictive power of models based on rodents, acorns, or both. We conclude that interannual variation in entomological risk of exposure to Lyme disease is correlated positively with prior abundance of key hosts for the immature stages of the tick vector and with critical food resources for those hosts.

          Abstract

          A long-term study of tick dynamics simultaneously assesses the impact of multiple ecological variables on Lyme disease risk and strongly implicates a role for rodent hosts and their food resources.

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          Most cited references80

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          The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk.

          The extent to which the biodiversity and community composition of ecosystems affect their functions is an issue that grows ever more compelling as human impacts on ecosystems increase. We present evidence that supports a novel function of vertebrate biodiversity, the buffering of human risk of exposure to Lyme-disease-bearing ticks. We tested the Dilution Effect model, which predicts that high species diversity in the community of tick hosts reduces vector infection prevalence by diluting the effects of the most competent disease reservoir, the ubiquitous white-footed mouse (Peromyscus leucopus). As habitats are degraded by fragmentation or other anthropogenic forces, some members of the host community disappear. Thus, species-poor communities tend to have mice, but few other hosts, whereas species-rich communities have mice, plus many other potential hosts. We demonstrate that the most common nonmouse hosts are relatively poor reservoirs for the Lyme spirochete and should reduce the prevalence of the disease by feeding, but rarely infecting, ticks. By accounting for nearly every host species' contribution to the number of larval ticks fed and infected, we show that as new host species are added to a depauperate community, the nymphal infection prevalence, a key risk factor, declines. We identify important "dilution hosts" (e.g., squirrels), characterized by high tick burdens, low reservoir competence, and high population density, as well as "rescue hosts" (e.g., shrews), which are capable of maintaining high disease risk when mouse density is low. Our study suggests that the preservation of vertebrate biodiversity and community composition can reduce the incidence of Lyme disease.
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            Climate variability and change in the United States: potential impacts on vector- and rodent-borne diseases.

            Diseases such as plague, typhus, malaria, yellow fever, and dengue fever, transmitted between humans by blood-feeding arthropods, were once common in the United States. Many of these diseases are no longer present, mainly because of changes in land use, agricultural methods, residential patterns, human behavior, and vector control. However, diseases that may be transmitted to humans from wild birds or mammals (zoonoses) continue to circulate in nature in many parts of the country. Most vector-borne diseases exhibit a distinct seasonal pattern, which clearly suggests that they are weather sensitive. Rainfall, temperature, and other weather variables affect in many ways both the vectors and the pathogens they transmit. For example, high temperatures can increase or reduce survival rate, depending on the vector, its behavior, ecology, and many other factors. Thus, the probability of transmission may or may not be increased by higher temperatures. The tremendous growth in international travel increases the risk of importation of vector-borne diseases, some of which can be transmitted locally under suitable circumstances at the right time of the year. But demographic and sociologic factors also play a critical role in determining disease incidence, and it is unlikely that these diseases will cause major epidemics in the United States if the public health infrastructure is maintained and improved.
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              The biological and social phenomenon of Lyme disease.

              Lyme disease, unknown in the United States two decades ago, is now the most common arthropod-borne disease in the country and has caused considerable morbidity in several suburban and rural areas. The emergence of this disease is in part the consequence of the reforestation of the northeastern United States and the rise in deer populations. Unfortunately, an accurate estimation of its importance to human and animal health has not been made because of difficulties in diagnosis and inadequate surveillance activities. Strategies for prevention of Lyme disease include vector control and vaccines.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS Biol
                pbio
                PLoS Biology
                Public Library of Science (San Francisco, USA )
                1544-9173
                1545-7885
                June 2006
                9 May 2006
                : 4
                : 6
                Affiliations
                [1] 1Institute of Ecosystem Studies, Millbrook, New York, United States of America
                [2] 2Department of Biology, Bard College, Annandale-on-Hudson, New York, United States of America
                Princeton University United States of America
                Article
                10.1371/journal.pbio.0040145
                1457019
                16669698
                6ed954b8-6823-47ce-a5b4-04014ec4436c
                Copyright: © 2006 Ostfeld et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                Categories
                Research Article
                Ecology
                Infectious Diseases
                Zoology
                Epidemiology/Public Health
                Parasitology
                Arthropods

                Life sciences
                Life sciences

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