Forest fragmentation predicts local scale heterogeneity of Lyme disease risk

Fragmentation of the landscape has been proposed to play an important role in defining local scale heterogeneity in Lyme disease risk through influence on mammalian host density and species composition. We tested this observed relationship in a suburban region around Lyme, Connecticut, where we collected data on the density of the tick vector, Ixodes scapularis and prevalence of the Lyme bacterium, Borrelia burgdorferi at 30 sites. Analysis of the landscape pattern of forest patches was performed using satellite imagery. The calculated landscape indices, which included patch size and isolation, revealed a positive link between fragmentation and both tick density and infection prevalence in ticks. In spite of higher entomologic risk, human incidence of Lyme disease is lower in fragmented contexts suggesting that entomologic risk is not the critical driver of human infections. These results represent a departure from the prior claims that fragmentation and human Lyme disease risk are positively linked. A complete understanding of the influence of landscape fragmentation will allow for improved risk mapping and potential environmental management of Lyme disease.

[1]  A. Spielman,et al.  Role of deer in the epizootiology of Babesia microti in Massachusetts, USA. , 1979, Journal of medical entomology.

[2]  A. Milne The comparison of sheep-tick populations (Ixodes ricinus L.) , 1943 .

[3]  R. Ostfeld,et al.  Biodiversity and Disease Risk: the Case of Lyme Disease , 2000 .

[4]  R D Holt,et al.  Diverse and Contrasting Effects of Habitat Fragmentation , 1992, Science.

[5]  A. Spielman,et al.  Ecology of Ixodes dammini-borne human babesiosis and Lyme disease. , 1985, Annual review of entomology.

[6]  H. Ginsberg,et al.  Habitat distribution of Ixodes dammini (Acari: Ixodidae) an Lyme disease spirochetes on Fire Island, New York. , 1989, Journal of medical entomology.

[7]  K. McGarigal,et al.  FRAGSTATS: spatial pattern analysis program for quantifying landscape structure. , 1995 .

[8]  S. Telford,et al.  Incompetence of deer as reservoirs of the Lyme disease spirochete. , 1988, The American journal of tropical medicine and hygiene.

[9]  R. Ostfeld,et al.  Effect of Forest Fragmentation on Lyme Disease Risk , 2003 .

[10]  M. Turner,et al.  LANDSCAPE ECOLOGY : The Effect of Pattern on Process 1 , 2002 .

[11]  D. Dennis,et al.  Surveillance for Lyme disease--United States, 1992-1998. , 2000, MMWR. CDC surveillance summaries : Morbidity and mortality weekly report. CDC surveillance summaries.

[12]  Bruce T. Milne,et al.  Indices of landscape pattern , 1988, Landscape Ecology.

[13]  L. Magnarelli,et al.  Spatial and temporal patterns of Ixodes scapularis (Acari: Ixodidae) in southeastern Connecticut. , 1993, Journal of medical entomology.

[14]  H. Kilpatrick,et al.  Reduced Abundance of Ixodes scapularis (Acari: Ixodidae) and the Tick Parasitoid Ixodiphagus hookeri (Hymenoptera: Encyrtidae) with Reduction of White-Tailed Deer , 2003, Journal of medical entomology.

[15]  D. Fish,et al.  Host associations of ticks (Acari: Ixodidae) parasitizing medium-sized mammals in a Lyme disease endemic area of southern New York. , 1989, Journal of medical entomology.

[16]  D. Fish,et al.  The biological and social phenomenon of Lyme disease. , 1993, Science.

[17]  Kurt H. Riitters,et al.  Landscape pattern metrics and regional assessment , 1999 .

[18]  D. Fish,et al.  Prevalence of Ixodes dammini near the homes of Lyme disease patients in Westchester County, New York. , 1988, American journal of epidemiology.

[19]  R. Ostfeld,et al.  BIODIVERSITY AND THE DILUTION EFFECT IN DISEASE ECOLOGY , 2001 .

[20]  D. Brillinger,et al.  The natural variability of vital rates and associated statistics. , 1986, Biometrics.

[21]  R. Swihart,et al.  EFFECT OF FOREST PATCH AREA ON POPULATION ATTRIBUTES OF WHITE-FOOTED MICE (PEROMYSCUS LEUCOPUS) IN FRAGMENTED LANDSCAPES , 1996 .

[22]  Felicia Keesing,et al.  The ecology of infectious disease: Effects of host diversity and community composition on Lyme disease risk , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[23]  Durland Fish,et al.  Landscape features associated with lyme disease risk in a suburban residential environment , 1998, Landscape Ecology.

[24]  A. Steere,et al.  Erythema chronicum migrans and Lyme arthritis: epidemiologic evidence for a tick vector. , 1978, American journal of epidemiology.

[25]  A. Spielman,et al.  Correlation between Abundance of Deer and That of the Deer Tick, Ixodes dammini (Acari: Ixodidae) , 1985 .

[26]  S. Stehman,et al.  Landscape Trends in Mid-Atlantic and Southeastern United States Ecoregions , 2003, Environmental management.

[27]  J. P. Davis,et al.  Lyme disease: A tick-borne spirochetosis , 1983 .

[28]  B. Wood,et al.  Landscape characterization of peridomestic risk for Lyme disease using satellite imagery. , 1997, The American journal of tropical medicine and hygiene.

[29]  James E. Vogelmann,et al.  Assessment of Forest Fragmentation in Southern New England Using Remote Sensing and Geographic Information Systems Technology , 1995 .

[30]  D. Fish,et al.  Landscape ecology of Lyme disease in a residential area of Westchester County, New York. , 1991, American journal of epidemiology.

[31]  D. Fish,et al.  Estimating Population Size and Drag Sampling Efficiency for the Blacklegged Tick (Acari: Ixodidae) , 2000, Journal of medical entomology.

[32]  P. Legendre Spatial Autocorrelation: Trouble or New Paradigm? , 1993 .

[33]  D. Fish,et al.  THE ROLE OF MEDIUM-SIZED MAMMALS AS RESERVOIRS OF BORRELIA BURGDORFERI IN SOUTHERN NEW YORK , 1990, Journal of wildlife diseases.

[34]  D. Fish,et al.  Relative importance of bird species as hosts for immature Ixodes dammini (Acari: Ixodidae) in a suburban residential landscape of southern New York State. , 1993, Journal of medical entomology.