Progress 10/01/02 to 09/30/09
Outputs
OUTPUTS: We have been studying the ecology, epidemiology and control of the Lyme disease spirochete (LDS), a tick-transmitted spirochete infection afflicting humans and other animals, for the past 28 years. The LDS is the most prevalent arthropod-borne disease in the United States with more than 56,000 cases reported for 2007 and 2008 alone. In the Far West, the western black-legged tick (WBLT) is the primary vector of the LDS to people. Since 2002, the broad objectives of this research were to clarify the role of the western gray squirrel as a keystone species for maintaining enzootic foci of the LDS; to investigate the host-seeking behavior of nymphs of the WBLT in relation to environmental parameters and to risk of human exposure to the LDS; to clarify the population structure of the LDS in host-seeking WBLT nymphs in dense woodlands in northwestern California; to ascertain what genotypes and species of LD group spirochetes infect humans; and to model the risk of human exposure to nymphs in woodlands of northwestern California. All these objectives were met, and the outputs were made available to the scientific community and public by means of articles and book chapters in peer-reviewed publications; by presentations at scientific conferences, public lectures or workshops; and by non-peer-reviewed publications or press releases. PARTICIPANTS: Not relevant to this project. TARGET AUDIENCES: Information gleaned during this project has been disseminated to the scientific community, the medical profession and the public via many publications in peer-reviewed international scientific journals, by outreach publications in regional or national magazines, by presentations at scientific conferences and public meetings, and by press releases. PROJECT MODIFICATIONS: Not relevant to this project.
Impacts
The outcomes and impacts have been reported annually since 2003. A few of the most significant earlier and current highlights are as follows. The western gray squirrel was found to be the primary host of the LDS in interior dense woodlands of northern California. As such, it is the primary source of spirochete infection for larvae and nymphs of the WBLT. The incidence of human LD in California mirrors the geographic distribution of this squirrel, and the prevalence of spirochete infection in squirrels is positively associated with a high incidence of human LD. Squirrels therefore are a keystone species driving the transmission cycle of the LDS in certain woodlands. Their terrestrial foraging behavior offers intriguing opportunities to reduce vector-tick populations and human-tick encounters by means of host-targeted methods, such as bait stations containing a pesticide-delivery system. The genetic population structure of the LDS in northwestern California was discovered to differ markedly from that in the northeastern United States. Twelve genotypes were identified, but 8 of the 20 known from the Northeast were absent. These include two genotypes that cause disseminated LD infection in humans. Also, a novel genotype having unknown pathogenicity for people comprised one-quarter of the genotypes identified from infected nymphal ticks. Taken together, these findings suggest that the lower genotypic diversity of the LDS in California, coupled with the absence of two types known to infect humans, may account in part for the lower incidence rate of human disease in this state. Polymerase chain reaction testing of human-serum specimens from a community at high risk for LD in northwestern California revealed that only one of the 12 genotypes found in ticks consistently infected people.
Publications
- Padgett, K. A., L. E. Casher, S. L. Stephens, and R. S. Lane. 2009. Effect of prescribed fire for tick control in California chaparral. J. Med. Entomol. 46: 1138-1145.
- Nieto, N. C., J. E. Foley, J. Bettaso, and R. S. Lane. 2009. Reptile infection with Anaplasma phagocytophilum, the causative agent of granulocytic anaplasmosis. J Parasitol. 95: 1165-1170.
- Girard, Y. A., B. Travinsky, A. Schotthoefer, N. Fedorova, R. J. Eisen, L. Eisen, A. G. Barbour, and R. S. Lane. 2009. Population structure of the Lyme borreliosis spirochete Borrelia burgdorferi in the western black-legged tick (Ixodes pacificus) in northern California. Appl. Environ. Microbiol. 75: 7243-7252.
- Lane, R. S., J. Mun, and H. A. Stubbs. 2009. Horizontal and vertical movements of host-seeking Ixodes pacificus (Acari: Ixodidae) nymphs in a hardwood forest. J. Vector Ecol. 34: 252-266.
- Nieto, N. C., Leonhard, S., Foley, J. E., and Lane, R. S. 2010. Coinfection of western gray squirrel (Sciurus griseus) and other sciurid rodents with Borrelia burgdorferi sensu stricto and Anaplasma phagocytophilum in California. J. Wildl. Dis. 46: 291-296.
- Lane, R. S. 2009. Lyme disease in the far-western United States: Outdoor enthusiasts beware. West. Outdoor News. February 11, 4 pp.
- Lane, R. S. 2009. Turkey hunters beware. Turkey Call. May/June: 96-97.
- Eisen, L., R. J. Eisen, J. Mun, D. J. Salkeld, and R. S. Lane. 2009. Transmission cycles of Borrelia burgdorferi and B. bissettii in relation to habitat type in northwestern California. J. Vector Ecol. 34: 81-91.
- Salkeld, D. J., and R. S. Lane. 2010. Community ecology and disease risk: lizards, squirrels, and the Lyme disease spirochete in California, USA. Ecology 91: 293-298.
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Progress 01/01/08 to 12/31/08
Outputs
OUTPUTS: We have been studying the ecology, epidemiology and control of the Lyme disease spirochete (LDS), a tick-transmitted spirochete infection, for the past 27 years. The LDS is the most prevalent arthropod-borne disease of public health importance in the United States with more than 20,000 cases reported annually to the national Centers for Disease Control and Prevention. Our main objectives include the identification of the primary reservoir hosts of this bacterium in natural settings where people work or recreate. A reservoir host is a vertebrate species that becomes infected naturally with the LDS following the bite of an infective tick, is bitten frequently by ticks that can acquire, maintain and transmit such spirochetes, and can serve as a source of infection for non-infected ticks that feed on it. In 2008, we completed and published a long-term study of the western gray squirrel and proved that, as hypothesized, it is a principal reservoir of the LDS in California. Additionally, we necropsied several naturally or experimentally infected squirrels to ascertain how the spirochete disseminates in this rodent. A related objective has been to further explore the role of birds in the ecology of the LDS in northern California. Nothing is known about the reservoir competence of birds in this region, and what has been published suggests that their role is minimal. Nevertheless, some birds are fed upon by vector ticks, and the possibility exists that a few ground-frequenting species may serve as reservoir hosts, a phenomenon that has been observed in Europe and the eastern United States. Finally, we continued our ongoing studies aimed at elucidating the genetic diversity of LDSs in nymphal ticks, and what particular genospecies or strains within a given genospecies, infect humans in northwestern California. The outputs of these investigations are being made available to the scientific community and the public by means of articles and book chapters in peer-reviewed publications; by presentations at scientific conferences, public lectures or workshops; and by non-peer- reviewed publications or press releases. PARTICIPANTS: Nothing significant to report during this reporting period. TARGET AUDIENCES: Nothing significant to report during this reporting period. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.
Impacts
A 3-year field survey of western gray squirrels in 8 northern Californian counties, and an accompanying series of laboratory transmission experiments, established conclusively that this rodent is a keystone species driving LD transmission cycles in some dense woodlands. Overall, 30% of 222 wild-caught or road-kill squirrels were PCR positive, and one-half of the squirrels derived from Humboldt and Mendocino counties were infected. In the laboratory, up to 86% of non-infected larval ticks placed on naturally infected squirrels acquired spirochetes and maintained them after molting to nymphs. We conclude that western gray squirrels frequently are infected with the LDS, they can retain their infections for prolonged periods, and they are able to infect, and be infected by, the Western Black-Legged Tick (WBLT). This tick is the primary vector of the spirochete to humans. Four wild-caught western gray squirrels were necropsied to evaluate dissemination of the LDS in their tissues. Blood, synovial and cerebrospinal fluid, and diverse tissue samples from skin and organs were taken and examined by culture, PCR and histology. Infection in these squirrels was highly localized inasmuch as spirochetes were confined mainly to the skin. In total, 760 blood samples collected from birds in Mendocino County were assayed by PCR to discover if they were infected with the LDS. Overall, 4.3% of individual birds were PCR positive for 3 or more genospecies of LDSs: the LDS (B. burgdorferi sensu stricto), B. bissettii and 1 or more unclassified genospecies, with B. bissettii being the most prevalent species. In contrast, larval and nymphal ixodid ticks collected from the same birds were almost exclusively infected with B. burgdorferi sensu stricto. Taken together, these results indicate that birds from this region are insignificant hosts of the LDS. Lastly, we completed PCR testing of 5,431 WBLTs collected throughout Mendocino County for the presence the LDS. A total of 264 (4.9%) ticks contained LDS DNA. To further characterize the spirochetes detected, we sequenced portions of two genes, the ribosomal RNA intergenic spacer (IGS) and the outer surface protein C (OspC) genes. The reason why sequence typing is important is because certain types are known to be associated with more severe forms of LD in humans. Our findings are stunning. Of the 18 OspC sequence types found in ticks and humans in the northeastern United States, only 10 were identified in I. pacificus ticks in California. Interestingly, two OspC types most commonly associated with serious and invasive forms of LD in the Northeast were not found in any of the ticks tested. California ticks, however, contained two completely novel OspC sequence types, one of which was the most common and represented about one-quarter of all ticks tested. Also exciting was our finding that the predominant novel OspC type is found in ticks in association with a novel IGS genotype. We hypothesize that the predominance of the novel LDS strain and the lack of two genotypes associated with severe disease on the East Coast, may contribute to the much lower incidence of LD among humans in California.
Publications
- Killilea, M. E., A. Swei, R. S. Lane, C. J. Briggs, and R. S. Ostfeld. 2008. Spatial dynamics of Lyme disease: a review. EcoHealth 5:167-195.
- Salkeld, D. J., S. Leonhard, Y. A. Girard, N. Hahn, J. M. Mun, K. A. Padgett, and R. S. Lane. 2008. Identifying the reservoir hosts of the Lyme disease spirochete Borrelia burgdorferi in California: the role of the western gray squirrel (Sciurus griseus). Am. J. Trop. Med. Hyg. 79:535-540.
- Lane, R.S. 2008. Lyme disease in California. Pest Notes Publ. 7485. Univ. Calif. Div. Ag. Nat. Res. 5 p.
- Kleinjan, J. E., and R. S. Lane. 2008. Larval keys to the genera of Ixodidae (Acari) and species of Ixodes (Latreille) ticks established in California. Pan-Pacif. Entomol. 84:121-142.
- Lane, R. S. 2008. Lyme disease in California. The California Yelper. Fall issue, pp. 9, 13. ixodid ticks (Acari) for avian, reptilian or rodent hosts. J. Med. Entomol. 46:115-122.
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Progress 01/01/06 to 12/31/06
Outputs
To determine if tree squirrels are serving as reservoir hosts of the Lyme Disease spirochete (LDS) in California, ear-tissue biopsy specimens obtained from 193 tree squirrels collected in 21 counties have been tested by polymerase chain reaction (PCR). These included 124 tissue specimens from native western gray squirrels, and 64 and 5 specimens from introduced fox squirrels and eastern gray squirrels, respectively. Up to 58% of the western gray squirrels collected from different localities, 1 (1.6%) of the fox squirrels, and none of the few eastern gray squirrels was PCR positive for the LDS. These data support the hypothesis that, at least in certain subtypes of dense woodlands, the western gray squirrel is serving as a keystone species in LD transmission cycles. An ongoing study of the diurnal host-seeking behavior of nymphal western black-legged (WBLT) ticks in a black-oak/madrone forest was continued for the third year, and a woodland-grass habitat was sampled
similarly in 2006 as a comparison area. The densities of nymphs were found to be greater on logs and tree trunks than in adjacent leaf litter or grass in both habitats, and the densities in all of these biotopes were greater in the dense woodland than in the woodland-grass habitat. Taken together, these findings expand our knowledge of the host-seeking activities of the nymphs, reconfirm earlier evidence that contact with wood is a greater risk factor for human exposure to the nymphs than contact with either leaf litter or grass, and demonstrate that people are more likely to encounter the nymphs in a dense woodland than in a woodland-grass habitat. To determine ecological and epidemiological factors that place humans at elevated risk of exposure to nymphs of the WBLT in dense woodlands, ecological and remotely-sensed characterizations of landscape composition in Mendocino County were used to develop risk-assessment models. Tick density was found to be elevated in forests having a
growing degree-day range of 2,600 to 3,000 (10 ?C base). All areas in California sharing this particular trait, and therefore projected to pose high human risk of exposure to nymphs, were identified by means of geographical information systems. A comparison of spatial LD incidence patterns based on county versus zip-code units for the period 1993-2005 revealed that zip-code units are much more useful than county units for detecting small, isolated areas with elevated disease risk, especially in southern California where LD is rare. Another model will be developed after all 5,500 nymphal WBLTs collected from 78 sites in Mendocino County in 2004 have been tested by PCR. To date, 2,156 nymphs have been tested; of these, 7% were PCR positive. When the testing has been completed, the density of infected nymphs will be used as the response variable to develop the final model. Ultimately, findings resulting from these field studies/modeling efforts will be incorporated into educational
materials (e.g., brochures, slide shows) to alert the public and medical community as to what subtypes of woodland in California pose elevated risk of exposure to people who either work or recreate in them.
Impacts
This research aims to clarify the complex ecology and epidemiology of the LDS and other tick-transmitted bacterial agents in the Far West. Since 1995, we have directed most of our research effort towards elucidating what environmental and behavioral factors elevate the human risk of exposure to the nymphs of the WBLT in various habitat types, especially mixed hardwood forests. Our ongoing study of the western gray squirrel strongly suggests that this squirrel is a keystone species driving LD transmission cycles in certain subtypes of dense woodlands. We continue to explore the host-seeking behavior of nymphal WBLTs both spatially and temporally in woodland habitats, which have been identified as a moderate to high-risk habitat for a significant portion (12%) of rural Mendocino County. In 2006, we reconfirmed that prolonged contact with logs or tree trunks generally poses significantly higher risk than contact with adjacent leaf-litter or grassy areas, and we also
determined that dense woodlands pose greater risk than woodland-grass habitats. Additionally, we found that the use of finer scale zip-code units in LD risk-assessment modeling efforts is more likely to reveal areas of geographically restricted risk than models using county units as the spatial variable. Over 2,000 nymphs of the WBLT from Mendocino County have been tested for the LDS by PCR, and several genotypes were identified among the 7% of ticks that were positive. We now are trying to ascertain which of these genotypes infect humans and cause clinical LD in northwestern California.
Publications
- Mun, J., Eisen, R. J., Eisen, L. and Lane. R. S. 2006. Detection of a Borrelia miyamotoi sensu lato relapsing-fever group spirochete from Ixodes pacificus in California. J. Med. Entomol. 43:120-123.
- Eisen, R. J., Eisen, L. and Lane, R.S. 2006. Predicting density of Ixodes pacificus nymphs in dense woodlands in Mendocino County, California, based on geographic information systems and remote sensing versus field-derived data. Am. J. Trop. Med. Hyg. 74:632-640.
- Eisen, L., Eisen, R. J. and Lane, R.S. 2006. Geographical distribution patterns and habitat suitability models for presence of host-seeking ixodid ticks in dense woodlands of Mendocino County, California. J. Med. Entomol. 43:415-427.
- Brown, R. N., Peot, M.A. and Lane, R.S. 2006. Sylvatic maintenance of Borrelia burgdorferi (Spirochaetales) in northern California: Untangling the web of transmission. J. Med. Entomol. 43:743-751.
- Lane, R. S., Mun, J., Eisen, L. and Eisen, R. J. 2006. Refractoriness of the western fence lizard (Sceloporus occidentalis) to the Lyme disease spirochete Borrelia bissettii. J. Parasitol. 92:691-696.
- Eisen, R. J., Lane, R. S., Fritz, C. L. and Eisen, L. 2006. Spatial patterns of Lyme disease risk in California based on disease incidence data and modeling of vector-tick exposure. Am. J. Trop. Med. Hyg. 75:669-676.
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Progress 01/01/05 to 12/31/05
Outputs
Tick studies initiated several years ago in a black oak/madrone woodland and three other comparable dense woodlands at the University of California Hopland Research and Extension Center were continued in 2005. Systematic drag-sampling conducted bihourly revealed that nymphs of the western black-legged tick (WBLT) are active in leaf-litter areas throughout the daytime, and that the host-seeking behavior of nymphs was not correlated with either ambient temperature or relative humidity. The relative density of nymphs on logs and tree trunks was much greater than it was in adjacent leaf litter, and the infection prevalence with the Lyme disease spirochete (LDS) in nymphs collected from logs and tree trunks combined was greater than in nymphs collected from leaf litter. Mark-release-recapture experiments revealed that marked nymphs released atop logs and in adjoining leaf-litter areas up to 1.5-m away were just as likely to move on or off logs, or toward or away from logs.
Individually marked nymphs traveled up to 3.4-m before they were recaptured over periods ranging up to six weeks post-release. To evaluate the reservoir competence of the western gray squirrel and related squirrels for the LDS, ear-tissue biopsy specimens from 124 tree squirrels collected in approximately 20 counties throughout California were tested by PCR. These included 55 tissue specimens from western gray squirrels, and 64 and five from introduced fox squirrels and eastern gray squirrels, respectively. Infection rates in the different squirrel species ranged from zero to approximately 50%, and varied by geographical region. The western fence lizard has been demonstrated to be refractory to experimental infection with the LDS, one of several closely related spirochetes in the LD spirochetal complex that are pathogenic for humans. Another member of the this spirochetal complex, BORRELIA BISSETTII, is distributed widely throughout North America and a similar, if not identical,
spirochete has been implicated as a human pathogen in southern Europe. To determine the susceptibility of the western fence lizard to BORRELIA BISSETTII, six naive lizards were exposed to the feeding activities of nymphal WBLTs experimentally infected with this spirochete. None of the lizards developed detectable infections for up to eight weeks post-tick feeding, infected nymphs apparently lost their infections within two weeks after engorgement, and WBLT larvae placed on lizards during or after nymphal-tick feeding did not acquire and maintain spirochetes. In contrast, three of four naive deer mice exposed similarly to feeding by one or more B. BISSETTII-infected nymphs developed detectable infections within four weeks. These and previous findings suggest that the complement system of the western fenced lizard typically destroys LDSs present in tissues of attached and feeding nymphs, thereby potentially reducing the force of transmission of such bacteria to humans or other animals
by the resultant adult ticks.
Impacts
This long-term research is elucidating the basic transmission cycles of the LDS and closely related spirochetes in the Far West. During the past decade, we have focused on various subtypes of dense woodlands in northwestern California, a moderately high-risk habitat for human exposure to spirochete-infected nymphal WBLTs. The western gray squirrel has been implicated as a primary reservoir host of the LDS, i.e., as a source of spirochetal infection for the WBLT over a broad geographical range. Further, the host-seeking behavior of nymphal WBLTs is being explored in-depth to further define the human risk of exposure to this life stage in dense woodlands. Significant findings to date demonstrated that people can be exposed to nymphs from dawn to dusk, that prolonged contact with wood (e.g., logs) is more risky than contact with leaf-litter, and that certain subtypes of dense woodlands pose greater risk than others. Finally, the western fence lizard fulfills the criteria
for a zooprophylactic host of BORRELIA BISSETTII. It is refractory to experimental infection with this spirochete, and its innate immune system probably destroys spirochetes present in infected nymphal WBLTs that engorge on it, presumably as a byproduct of complement proteins delivered with the blood-meal. To the extent that nymphal ticks feed preferentially on lizards rather than on reservoir-competent hosts like the western gray squirrel, humans or other animals bitten subsequently by adult WBLTs from the same tick population are less likely to be exposed to BORRELIA BISSETTII.
Publications
- Eisen, R. J., Eisen, L. and Lane, R. S. 2005. Remote sensing (Normalized Difference Vegetation Index) classification of risk versus minimal risk habitats for human exposure to Ixodes pacificus (Acari: Ixodidae) nymphs in Mendocino County, California. J. Med. Entomol. 42:75-81.
- Lane, R. S., Mun, J., Parker, J. M. and White, M. 2005. Columbian black-tailed deer (Odocoileus hemionus columbianus) as hosts for Borrelia spp. in northern California. J. Wildl. Dis. 41:115-124.
- Hahn, N., Eisen, R. J., Eisen, L. and Lane, R. S. 2005. Ketamine-medetomidine anesthesia with atipamezole reversal: practical anesthesia for rodents under field conditions. Lab Animal 34:48-51.
- Lane, R. S., Mun, J., Eisen, R. J. and Eisen, L. 2005. Western gray squirrel (Rodentia: Sciuridae): A primary reservoir host of Borrelia burgdorferi in Californian oak woodlands? J. Med. Entomol. 42:388-396.
- Francischetti, I. M. B., Pham, V. M., Mans, B. J., Anderson, J. F., Mather, T. N., Lane, R. S. and Ribeiro, J. M. C. 2005. The transcriptome of the salivary glands of the female western black-legged tick Ixodes pacificus (Acari: Ixodidae). Insect Biochem. Molecular Biol. 35:1142-1161.
- Schwan, T. G., Raffel, S. J., Schrumpf, M. E., Policastro, P. F., Rawlings, J. A., Lane, R. S., Breitschwerdt, E. B. and Porcella, S. F. 2005. Phylogenetic analysis of the spirochetes Borrelia parkeri and Borrelia turicatae and the potential for tick-borne relapsing fever in Florida. J. Clin. Microbiol. 43:3851-3859.
- Brown, R. N., Dennis, D. T. and Lane, R. S. 2005. Geographic distributions of tick-borne diseases and their vectors. Pages 363-391 in: Goodman, J. L., D. T. Dennis and D. E. Sonenshine. Tick-Borne Diseases of Humans. ASM Press, Washington, D. C.
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Progress 01/01/04 to 12/31/04
Outputs
In 2004, we sought to create a spatially explicit model of the density of nymphal western black-legged ticks (WBLT) in woodland-leaf habitats in Mendocino County, California. The WBLT is the primary vector of the Lyme disease spirochete to humans in the Far West. The primary objectives were, first, to identify suitable habitats for questing nymphs using remotely sensed variables such as brightness, greenness, wetness and the Normalized Difference Vegetation Index (NDVI) derived from Landsat TM imagery and, second, to model nymphal density within human-risk habitats. We began by creating a habitat model for the 5,300-acre Hopland Research and Extension Center (HREC). The NDVI from four seasons provided spectral signatures that could be used to uniquely identify the four predominant habitat types present there, i.e., woodland-leaf, woodland-grass, grasslands and chaparral. A maximum-likelihood algorithm, based on 4 seasons of NDVI, was used to classify Landsat TM
imagery for the area. The result was a habitat map of the HREC that correctly categorized the 4 habitat types with >83% accuracy and correctly categorized woodland-leaf with 93% accuracy. Similar methods were used to create a habitat model for the entire county. At this scale, habitats were best separated based on NDVI and Brightness from February and NDVI and Wetness from July. The resulting model correctly identified woodland leaf habitats with >93% user accuracy. Overall, 52.6% of the county was classified as nymphal risk habitat. To create a GIS model of tick density, nymphs were collected from 78 woodland sites throughout the county. Nymphs were present in or around each of the 78 sites; within sites, densities ranged from 0 to 24.6 nymphs per 100 m2. Using density data from 62 of the 78 sites, we created a model (based on forward-stepwise multiple regression) of density within all woodlands identified by remote sensing. The final model explained 77% of the variation in nymphal
density within the 16 field sites that were not used to create the model. Overall, the risk surface showed that 11.9% of the county was classified as habitat posing moderate to high risk of human exposure to nymphs (>6.4 nymphs per 100 m2). Further, the highest risk class (>10.5 nymphs per 100 m2) tended to cluster in the central interior portion of the county and coincides with some of the most heavily populated areas.
Impacts
This research is intended to identify specific subtypes of woodland-leaf habitats and related environmental factors that are associated with elevated risk of human exposure to nymphs of the WBLT in northwestern California. This life stage avidly bites people who recreate or work outdoors in woodlands during the spring or summer, and it typically has a much higher prevalence of spirochetal infection (~5-15%) than do the adult ticks (~1-4%). Development of the aforementioned risk model, and a supplementary model in which the density of spirochete-infected nymphs will be substituted for the density of nymphs per se, should contribute significantly to our fundamental knowledge of the landscape ecology and epidemiology of Lyme disease in the Far West. Ultimately, this information will be disseminated to state and local health authorities, as well as to the media, to educate the laity and medical profession about the types of habitats and specific human behaviors that
increase the risk of exposure to the Lyme disease spirochete.
Publications
- Lane, R. S., Steinlein, D. B., and Mun, J. 2004. Human behaviors elevating exposure to Ixodes pacificus (Acari: Ixodidae) nymphs and their associated bacterial zoonotic agents in a hardwood forest. J. Med. Entomol. 41: 239-248.
- Eisen, R. J., Eisen, L., and Lane, R. S., 2004. Habitat-related variation in infestation of lizards and rodents by Ixodes ticks in dense woodlands in Mendocino County, California. Exp. Appl. Acarol. 33: 215-233.
- Eisen, R. J., Mun, J., Eisen, L., and Lane, R. S. 2004. Life-stage related differences in density of questing ticks and infection with Borrelia burgdorferi s.l. within a single cohort of Ixodes pacificus (Acari: Ixodidae). J. Med. Entomol. 41: 768-773.
- Foley, J. E., Foley, P., Brown, R. N., Lane, R. S., Dumler, J. S., and Madigan, J. E. 2004. Ecology of Anaplasma phagocytophilum and Borrelia burgdorferi in the western United States. J. Vector Ecol. 29: 41-50.
- Eisen, L., Eisen, R. J., and Lane, R. S. 2004. The roles of birds, lizards and rodents as hosts for the western black-legged tick, Ixodes pacificus. J. Vector Ecol. 29: 295-308.
- Eisen, L., Eisen, R. J., Chang, C. C., Mun, J., and Lane, R. S. 2004. Acarological risk of exposure to Borrelia burgdorferi spirochaetes: Long-term evaluations in north-western California, with implications for Lyme borreliosis risk assessment models. Med. Vet. Entomol. 18: 38-49.
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Progress 01/01/03 to 12/31/03
Outputs
Dense woodlands have been identified as the primary habitat of the nymphal stage of the western black-legged tick (WBLT) in northwestern California. This tick is the primary vector of the Lyme disease spirochete (LDS) and the agent of human anaplasmosis in the Far West. Since 2002, studies have been conducted in Mendocino County, California, to determine the principal reservoir host of the LDS in dense woodlands. In 2003, lizards, birds and small mammals were collected in 8 woodlands and contiguous chaparral and grassland habitats in the Hopland area. In total, 157 lizards, 209 birds, 302 ground-dwelling rodents, and 10 western gray squirrels were examined for presence of the WBLT. Birds were separated into guilds based on their foraging and nesting behavior, with perceived risk of exposure to tick host-seeking substrate highest for Guild I and lowest for Guild IV. Overall mean larval-tick loads were highest on western fence and alligator lizards (18.0-35.3 per
animal), followed by squirrels (9.2), a guild I bird and dusky-footed wood rat grouping (3.5-5.2), PEROMYSCUS spp. mice (1.1), and guild II-IV birds (0.08-0.5). Average nymphal-tick loads ranged from 5.4-6.0 for alligator lizards, western fence lizards and squirrels to 1.0 for guild I birds, 0.1-0.3 for guild II-III birds, 0.05-0.06 for guild IV birds and wood rats, and 0 for PEROMYSCUS spp. mice. A crude analysis of host usage demonstrated that western fence lizards and alligator lizards accounted for 84.1% of all larval ticks and 91.1% of the nymphal ticks. These results reconfirm earlier findings that, on an area-wide basis, lizards are far more important hosts of immature WBLTs than birds and mammals combined. Ear-punch biopsies and whole-blood specimens taken from small mammals and birds, respectively, were tested for presence of the LDS with a nested PCR assay and by sequencing analyses. Overall, 80% of squirrels versus just 5.8% of the PEROMYSCUS spp. mice and wood rats caught
in woodlands were infected with the LDS or closely related spirochetes. In contrast, 17.4% (55 of 316) birds were found to contain spirochetes, but only one of the infected birds, an oak titmouse, was infected with the LDS. The remaining infected birds contained BORRELIA BISSETTII or other uncharacterized spirochetes belonging to the diverse LD spirochetal complex.
Impacts
This research helps to clarify the basic transmission cycle of the LDS in dense woodlands in northwestern California, a potentially high-risk habitat for human exposure to spirochete-infected nymphal WBLTs. The western gray squirrel was implicated for the first time as a primary reservoir host of the LDS, and as an important host of both the larval and nymphal stages of the WBLT. A reservoir is a vertebrate that helps to maintain an animal disease agent in a given area by serving as a source of infection for uninfected blood-sucking arthropods that feed on it. Although nearly 20% of the birds tested were found to contain spirochetes, the fact that only one of them actually was infected with the LDS suggests that birds generally may be relatively unimportant in the ecology and epidemiology of Lyme disease in this region.
Publications
- Eisen, R. J., Eisen, L., Castro, M. B., and Lane, R. S. 2003. Environmentally related variability in risk of exposure to Lyme disease spirochetes in northern California: Effect of climatic conditions and habitat type. Environ. Entomol. 32: 1010-1018.
- Eisen, L, Dolan, M. C., Piesman, J., and Lane, R. S. 2003. Vector competence of Ixodes pacificus and I. spinipalpis (Acari: Ixodidae), and reservoir competence of the dusky-footed woodrat (Neotoma fuscipes) and the deer mouse (Peromyscus maniculatus), for Borrelia bissettii. J. Med. Entomol. 40: 311-320.
- Ullman, A. J., Lane, R. S., Kurtenbach, K., Miller, M., Schriefer, M. E., Zeidner, N., and Piesman, J. 2003. Bacteriolytic activity of selected vertebrate sera for Borrelia burgdorferi sensu stricto and Borrelia bissettii. J. Parasitol. 89: 1256-1257.
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Progress 01/01/02 to 12/31/02
Outputs
The western black-legged tick (WBLT), especially the nymphal stage, is the primary transmitter of the Lyme disease spirochete (LDS) to humans in the Far West. In spring 2002, the relative importance of lizards versus rodents as hosts for subadults (larvae, nymphs) of this tick was investigated at 14 sites in widely spaced inland areas of Mendocino County. These included 6 sites in oak woodlands, 5 sites in oak woodlands with influence of Douglas fir, and 3 sites in redwood/tanoak habitats. For all sites examined, western fence lizards carried signficantly heavier loads of larval and nymphal WBLTs than did rodents. In fact, on a county-wide basis, 85% of the larvae and 99.8% of the nymphs of the WBLT were removed from lizards. Previous research has demonstrated that lizards are refractory to infection with the LDS and contain proteins in their blood that destroy spirochetes present in the midguts of infected nymphs that attach to them. Thus, to the extent that nymphal
ticks feed on lizards and not on reservoir-competent hosts like certain species of rodents, the force of transmission of the LDS is reduced and people are less likely to be bitten by infected adult ticks. Not surprisingly, spirochetal infection prevalences in adult ticks that occur in areas where lizards are plentiful typically are only 1-2%. A long-term study of the ability of the WBLT and a nonhuman-biting tick in the same genus to acquire, maintain and transmit the spirochete BORRELIA BISSETTII was completed. This spirochete, which is a member of the LDS complex (11 species have been described to date), is suspected of causing an illness resembling LD in Europe. Both species of ticks were determined to be efficient experimental transmitters of B. BISSETTII and two species of wild rodents, the dusky-footed wood rat and the deer mouse, were found to be capable of serving as a source of infection for these ticks. Although the WBLT occasionally is infected naturally with B. BISSETTII
in northern California, molecular and immunological studies produced no evidence that any of approximately 200 patients with confirmed LD contained antibodies against this spirochete. Finally, 6 different behaviors were evaluated as potential risk factors for acquiring host-seeking nymphs of the WBLT in an oak-woodland in Mendocino County. Activities involving contact with wood resulted in greater acquisition of nymphs on either clothing or skin than those involving exclusive exposure to leaf litter. Sitting on logs and gathering wood were the riskiest behaviors with 30% and 23%, respectively, of such encounters yielding one or more ticks, whereas sitting on leaf litter (8.3%) and walking through it (1.7%) were the least risky activities. This is the first study in which acquisition of nymphs of the WBLT has been associated with specific kinds of behaviors.
Impacts
This ongoing research (now in its 21st year) further expands our knowledge of both the ecology and epidemiology of the LDS in the Far West. The basic transmission cycles of this spirochete and closely related tick-borne spirochetes are gradually being clarified, and specific behaviors that elevate exposure to the dangerous nymphal stage of the WBLT have been identified. Ultimately, the data gleaned from these studies will be used to develop and implement strategies for preventing and controlling LD.
Publications
- Gray, J., Kahl, O., Lane, R. S., and Stanek, G. (eds.). 2002. Lyme borreliosis: Biology, epidemiology and control. CABI Publishing, United Kingdom.
- Eisen, L. and Lane, R. S. 2002. Vectors of Borrelia burgdorferi sensu lato. Pages 91-115 in Gray, J., Kahl, O., Lane, R. S., and Stanek, G. (eds.). Lyme borreliosis: Biology, epidemiology and control. CABI Publishing, United Kingdom.
- Kahl, O., Gern, L., Eisen, L., and Lane, R. S. 2002. Ecological research on Borrelia burgdorferi sensu lato: Terminology and some methodological pitfalls. Pages 29-46 in Gray, J., Kahl, O., Lane, R. S., and Stanek, G. (eds.). Lyme borreliosis: Biology, epidemiology and control. CABI Publishing, United Kingdom.
- Eisen, L., Eisen, R. J., and Lane, R. S. 2002. Seasonal activity patterns of Ixodes pacificus nymphs in relation to climatic conditions. Med. Vet. Entomol. 16: 235-244.
- Casher, L., Lane, R., Barrett, R., and Eisen, L. 2002. Relative importance of lizards and mammals as hosts for ixodid ticks in northern California. Exp. Appl. Acarol. 26: 127-143.
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Progress 01/01/01 to 12/31/01
Outputs
In 2001, a 5-year study of the density of nymphal western black-legged ticks (WBLT) infected with the Lyme disease spirochete (LDS) in mixed hardwood forests in Mendocino County, California was concluded. Seven oak/madrone woodland sites at the 5,300-acre Hopland Research and Extension Center (HREC) and 9 oak /madrone/ Douglas fir sites at a 5,300-acre private ranch community at high risk for LD (CHR) were sampled in spring. Overall, the density of infected nymphs was 5-10 times higher at the CHR versus the HREC from 1997 to 1999, but only 1.5-1.8 times higher in 2000 and 2001. Also, the density of infected nymphs varied dramatically between sampling sites within both the CHR and HREC as well as between years for individual sites. These data demonstrate that the risk of human exposure to infected nymphs is highly variable within both properties, and that assessing LD risk based on the density of spirochete-infected nymphs must be carried out in multiple sites over a
period of several years. Further studies are under way to clarify what biotic and abiotic environmental factors are associated with the density of infected nymphs. In a related investigation, the seasonality of nymphal ticks and the peak density of infected nymphs were evaluated in 12 sites scattered throughout inland areas of Mendocino County. These included 3 broad habitat types, i.e., dry, warm oak/madrone woodlands, oak/madrone/Douglas fir, and cool, moist redwood/tanoak areas. Infected nymphs were detected in all sites, but the density of infected nymphs typically was much lower in redwood/tanoak than in the other 2 habitat types. Warm and dry oak/madrone woodlands, as compared with areas containing conifers, were characterized by a shorter duration of total and peak nymphal activity periods and an earlier peak density (i.e., late April versus mid-May). Redwoods, which appeared to comprise the lowest risk areas for human exposure to the LDS, exhibited a longer seasonal period of
tick host-seeking activity (spring to fall) in which peak densities occurred during the summer. Finally, California kangaroo rats and other small mammals have been implicated as reservoirs of the LDS and closely related spirochetes in northern California. A long-term investigation of the capacity of the kangaroo rat for maintaining and distributing such spirochetes has been nearly completed. We found that kangaroo rats can be infected simultaneously with several different kinds of spirochetes and that an individual animal can serve as a source of spirochetal infection for uninfected vector ticks throughout its lifetime. The significance of these findings is that they help to explain how spirochetes can be maintained and distributed within a particular habitat type between seasons as well as from year-to-year.
Impacts
This research has contributed to our understanding of the basic mechanisms whereby the Lyme disease spirochete is maintained and distributed in nature. It also has identified specific environmental and behavioral factors that are likely to increase human exposure to spirochete-infected ticks.
Publications
- Slowik, T.J., Lane, R.S., and Davis, R.M. 2001. Field trial of systemically delivered arthropod development-inhibitor (fluazuron) used to control woodrat fleas (Siphonaptera: Ceratophyllidae) and ticks (Acari: Ixodidae). J. Med. Entomol. 38:75-84.
- Slowik, T.J. and Lane, R.S. 2001. Birds and their ticks in northwestern California: Minimal contribution to Borrelia burgdorferi enzootiology. J. Parasitol. 87:755-761.
- Padgett, K.A. and Lane, R.S. 2001. Life cycle of Ixodes pacificus (Acari: Ixodidae): Timing of developmental processes under field and laboratory conditions. J. Med. Entomol. 38:684-693.
- Lane, R.S. and Anderson, J.R. 2001. Research on animal-borne parasites and pathogens helps prevent human disease. Calif. Agric. 55(6):13-18.
- Slowik, T.J. and Lane, R.S. 2001. Nymphs of the western black-legged tick (Ixodes pacificus) collected from tree trunks in woodland-grass habitat. J. Vector Ecol. 26:165-171.
- Eisen, R.J., Eisen, L., and Lane, R.S. 2001. Prevalence and abundance of Ixodes pacificus immatures (Acari: Ixodidae) infesting western fence lizards (Sceloporus occidentalis) in northern California: Temporal trends and environmental correlates. J. Parasitol. 87:1301-1307.
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Progress 01/01/00 to 12/31/00
Outputs
The abundance of, and the prevalence of infection with the Lyme disease spirochete (LDS) in, the western black-legged tick (WBLT) were determined for the fourth consecutive year in a LD-endemic area of northwestern California. This tick is the primary vector of the LDS (and of the rickettsia causing human granulocytic ehrlichiosis) in the Far West. Knowledge of the density of spirochete-infected ticks can be used epidemiologically as an indirect measure of risk for acquiring LD. The density of ticks and their associated infection rates in some leaf-litter areas were found again to be as high as they are in certain highly endemic areas of the northeastern United States. Environmental factors having some potential to predict the density of nymphal ticks include climatic conditions, topographic exposure, and the presence of habitat edges or logs. For example, it appears that nymphal densities may be positively correlated with the amount of rainfall and negatively
correlated with temperature maximums from March to May. The efficiency of the tick-drag method used for sampling populations of nymphal WBLT ticks in leaf litter was determined to be only 6%, which suggests that the actual risk of exposure to ticks may be 15-20 times higher than estimated previously. Environmental correlates of the density and spatial distribution of the WBLT also were assessed in heavily-used recreational areas in Alameda and Marin counties. Adult-tick abundance was associated with the density of brush, the width of hiking trails, and the presence of an uphill slope. Although the risk for contracting LD was judged to be low in both recreational areas, risk varied significantly among trails, seasons, and from year-to-year. Another tick, Ixodes angustus, which occasionally bites humans, was shown to be a competent experimental vector of the LDS. This finding, coupled with earlier epidemiologic evidence, suggest that I. angustus could serve as a secondary vector of such
spirochetes to humans. Two tick-derived isolates of Borrelia coriaceae, a relapsing-fever group spirochete, were characterized genetically and found to be similar to the type strain. These represent only the second and third isolates of this little known spirochete since it was first isolated in the mid-1980s. Borrelia coriaceae has been suspected of infecting and causing clinical illness in rangeland cattle and possibly in humans as well. The physiologic mechanism in lizard blood responsible for eliminating spirochetes from the midguts of attached and feeding nymphal WBLTs was elucidated. Specifically, the complex series of enzymatic proteins comprising the alternative complement pathway of the reptilian immune system was implicated as the active spirochete-killing principle. After an infected nymphal tick feeds fully on the western fence lizard, detaches and then molts, all of the resulting adult ticks are spirochete-free. Consequently, host-seeking adult ticks have, on average, a
much lower spirochetal infection rate (1-4%) than do host-seeking nymphal ticks (2-15%) in California, and the likelihood of a person being bitten by an infected adult tick is reduced accordingly.
Impacts
(N/A)
Publications
- Kuo, M.M., Lane, R.S., and Giclas, P.C. 2000. A comparative study of mammalian and reptilian alternative pathway of complement-mediated killing of the Lyme disease spirochete (Borrelia burgdorferi). J. Parasitol. 86:1223-1228.
- Talleklint-Eisen, L. and Lane, R.S. 2000. Spatial and temporal variation in the density of Ixodes pacificus (Acari: Ixodidae) nymphs. Environ. Entomol. 29:272-280.
- Li, X., Peavey, C.A., and Lane, R.S. 2000. Density and spatial distribution of Ixodes pacificus (Acari: Ixodidae) in two recreational areas in north coastal California. Am. J. Trop. Med. Hyg. 62:415-422.
- Talleklint-Eisen, L. and Lane, R.S. 2000. Efficiency of drag sampling for estimating population sizes of Ixodes pacificus (Acari: Ixodidae) nymphs in leaf litter. J. Med. Entomol. 37:484-487.
- Peavey, C.A., Lane, R.S., and Damrow, T. 2000. Vector competence of Ixodes angustus (Acari: Ixodidae) for Borrelia burgdorferi sensu stricto. Exp. Appl. Acarol. 23:77-84.
- Hendson, M. and Lane, R.S. 2000. Genetic characteristics of Borrelia coriaceae isolates from the soft tick Ornithodoros coriaceus (Acari: Argasidae). J. Clin. Microbiol. 38:2678-2682.
- Lane, R.S. 2000. Lyme disease in California. Pest Notes Publ. 7485. Univ. Calif. Div. Ag. Nat. Res. 3 p.
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Progress 01/01/99 to 12/31/99
Outputs
A total of 130 isolates of Lyme disease spirochetes (LDS) and closely related spirochetes from field-derived ticks or small mammals was genetically characterized by polymerase chain reaction. Twelve restriction fragment length polymorphism groups identified among these isolates comprised the LDS, the recently described Borrelia bissettii, and one or more as yet uncharacterized borrelial genospecies. Notably, over 90% of the isolates from the western black-legged tick, Ixodes pacificus, a vicious human-biter, were identified as the LDS. This spirochete is by far the most important vector-borne pathogen afflicting humans in temperate regions worldwide. A serologic assay was used to assess the degree of association between human seropositivity for the LDS and anti-I. pacificus antibodies, as well as antibodies to 3 other human-biting arthropods (1 tick, 1 bug, 1 mosquito), among members of a community at high risk (CHR) for LD. This assay, which proved to be a useful
epidemiologic tool for elucidating the primary vector of the LDS, yielded potent new evidence corroborating previously published circumstantial evidence that I. pacificus indeed is the bridging vector from wildlife reservoirs to humans. The spatial variation in the density of spirochete-infected I. pacificus nymphs was determined at the CHR and a nearby comparison area. The area-wide prevalence of LDS-infection in I. pacificus nymphs, the mean densities of infected nymphs, and the mean densities of nymphs at the CHR were comparable to those in highly endemic areas of the East. The facts that the abundance of infected I. scapularis nymphs have been correlated with the number of LD cases in the northeastern USA and that nymphal density alone may predict temporal or spatial LD risk strongly suggest that, in northwestern California, the local risk of contracting LD may be as high as it is in some areas of the Northeast.
Impacts
(N/A)
Publications
- Lane, R.S., Peavey, C.A., Padgett, K.A., and Hendson, M. 1999. The life history of Ixodes (Ixodes) Jellisoni (Acari: Ixodidae) and its vector competence for Borrelia burgdorferi sensu lato. J. Med. Entomol. 36:329-340.
- Postic, D., Ras, N.M., Lane, R.S., Humair, P.-F., Wittenbrink, M.M., and Baranton, G. 1999. Common ancestry of Borrelia burgdorferi sensu lato strains from North America and Europe. J. Clin. Microbiol. 37:3010-3012.
- Tallekint-Eisen, L. and Lane, R.S. 1999. Variation in the density of questing Ixodes pacificus (Acari: Ixodidae) nymphs infected with Borrelia burgdorferi at different spatial scales in California. J. Parasitol. 85:824-831.
- Lane, R.S., Moss, R.B., Hsu, Y.-P., Wei, T., Mesirow, M.L. and Kuo, M.M. 1999. Anti-arthropod saliva antibodies among residents of a community at high risk for Lyme disease in California. Am. J. Trop. Med. Hyg. 61:850-859.
- Kain, D.E., Sperling, F.A.H., Daly, H.V., and Lane, R.S. 1999. Mitochondrial DNA sequence variation in Ixodes pacificus (Acari: Ixodidae). Heredity 83:378-386.
- Lane, R.S. and Keirans, J.E. 1999. Ixodes spinipalpis: A probable enzootic vector of Borrelia burgdorferi in California. Pages 395-399 in Needham, G.R., Mitchell R., Horn, D.J., and Welbourn, W.C., editors. Acarology IX: Volume 2, Symposia. Ohio Biological Survey, Columbus, Ohio.
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Progress 01/01/98 to 12/01/98
Outputs
The blood of the western fence lizard (SCELOPORUS OCCIDENTALIS) and the southern alligator lizard (ELGARIA MULTICARINATA) were found to contain a spirochete-killing factor, probably a protein or complex series of proteins, that kills the Lyme disease spirochete (LDS). Experimental studies revealed that the active principle in S. OCCIDENTALIS kills the LDS in the midguts of attached, feeding nymphal IXODES PACIFICUS ticks. Consequently, the prevalences of spirochetal infection in some populations of adult I. PACIFICUS are only 0.2 to 0.3 what they are in the preceding (nymphal) feeding stage. Eliminating spirochetal infections from human-biting ticks like I. PACIFICUS reduces the force of transmission of the LDS to humans and other animals. Genetic studies of spirochetal isolates from Californian ticks or small mammals disclosed that the complex comprising the LDS is heterogeneous. One cluster of isolates was different from all others worldwide and was named BORRELIA
BISSETTII. Studies are under way to determine the infectivity of this spirochete for ticks, rodents and humans. A little known tick, IXODES JELLISONI, was found to be a competent experimental vector of two novel groups of spirochetes related to the LDS. Notably, this tick was shown to be parthenogenetic, a phenomenon that has been reported only once before for a member of the large (234 species) and cosmopolitan tick genus IXODES.
Impacts
(N/A)
Publications
- OLIVER, JR., J. H., KOLLARS, JR., T. M., CHANDLER, JR., F. W., JAMES, A. M., MASTERS, E. J., LANE, R. S., and HUEY, L. O. 1998. First isolation and cultivation of BORRELIA BURGDORFERI sensu lato from Missouri. J. Clin. Microbiol. 36:1-5.
- LANE, R.S. and QUISTAD, G.B. 1998. Borreliacidal factor in the blood of the western fence lizard (SCELOPORUS OCCIDENTALIS). J. Parasitol.
- LANE, R.S., CASHER, L.E., PEAVEY, C.A., and PIESMAN, J. 1998. Modified bait tube controls disease-carrying ticks and fleas. Calif.
- WRIGHT, S.A. and LANE, R.S. 1998. Infestation of the southern alligator lizard (Squamata: Anguidae) by IXODES PACIFICUS (Acari: Ixodidae) and its susceptibility to BORRELIA BURGDORFERI. J. Med.
- POSTIC, D., RAS, N.M., LANE, R.S., HENDSON, M., and BARANTON, G. 1998. Expanded diversity among Californian BORRELIA isolates and description of BORRELIA BISSETTII sp. nov. (formerly BORRELIA group DN127). J. Clin. Microbiol. 36:3497-3504.
- LANE, R.S., PEAVEY, C.A., PADGETT, K.A., and HENDSON, M. 1999. The life history of IXODES (IXODES) JELLISONI (Acari: Ixodidae) and its vector competence for BORRELIA BURGDORFERI sensu lato. J. Med.
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Progress 10/01/97 to 12/01/97
Outputs
We found two ticks that feed on woodrats and other small mammals but rarely on humans, IXODES NEOTOMAE and I. SPINIPALPIS, have been implicated as maintenance vectors of Lyme disease spirochetes in the western United States. These ticks are similar morphologically, they share many of the same vertebrate hosts, and their geographical distributions overlap. New morphological and mitochondrial DNA evidence now suggest that these ticks are in fact conspecific and that I. NEOTOMAE should be made a junior synonym of I. SPINIPALPIS. These findings underscore the need for accurate taxonomic determinations when vector ecologists are conducting ecological studies of ticks and tick-transmitted agents of disease.
Impacts
(N/A)
Publications
- NORRIS, D.E., KLOMPEN, J.S.H., KEIRANS, J.E., LANE, R.S., PIESMAN, J., and BLACK IV, W.C. 1997. Taxonomic status of IXODES NEOTOMAE and I. SPINIPALPIS (Acari: Ixodidae) based on mitochondrial DNA evidence. J. Med. Entomol. 34:696-703.
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