Dilution Effect of the Refractory Lizard Host on the Transmission of the Lyme Disease Pathogen by Its Tick Vector in Northern California
Main Article Content
Abstract
A current model for Ixodes scapularis was revised and extended to represent the temperature dependent life cycle and host structure for Ixodes pacificus, the vector of the Lyme disease pathogen Borrelia burgdorferi in the Western United States. Parameters were adjusted to reflect data collected in Mendocino, CA. The hosts for I. pacificus include the Western Fence Lizard, which is not only an incompetent host for B. burgdorferi, but some studies claim that it eliminates it in ticks that feed on this lizard. The lizard host has been proposed as a reason for lower prevalence of Lyme disease in the West. This hypothesis was tested quantitatively by varying the number of lizard hosts. Model results suggest that the presence of refractory hosts produces a dilution effect for B. burgdorferi infection and is likely to be the reason for observed lower prevalence of Lyme disease in the Western United States.
Keywords:
Lyme disease, Borrelia burgdorferi, Ixodes pacificus, Western Fence Lizard, Dilution effect, Refractory host, Tick-borne disease, Mathematical modeling
Article Details
How to Cite
RATTI, Vardayani; WALLACE, Dorothy.
Dilution Effect of the Refractory Lizard Host on the Transmission of the Lyme Disease Pathogen by Its Tick Vector in Northern California.
Medical Research Archives, [S.l.], v. 11, n. 12, dec. 2023.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/4948>. Date accessed: 22 aug. 2026.
doi: https://doi.org/10.18103/mra.v11i12.4948.
Section
Research Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
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4. Padgett KA, Lane RS. Life cycle of Ixodes pacificus (Acari: Ixodidae): timing of developmental processes under field and laboratory conditions. J Med Entomol. 2001; 38(5):684–693. doi:10.1603/0022-2585-38.5.684
5. Troughton DR, Levin ML. Life cycles of seven ixodid tick species (Acari: Ixodidae) under standardized laboratory conditions. J Med Entomol. 2007; 44(5):732–740. doi:10.1603/0022-2585(2007)44[732:lcosit]2.0.co;2
6. Peavey CA, Lane RS. Field and laboratory studies on the timing of oviposition and hatching of the western black-legged tick, Ixodes pacificus (Acari: Ixodidae). Exp Appl Acarol. 1996; 20(12):695–711. doi:10.1007/BF00051555
7. Eisen L, Eisen RJ, Lane RS. The roles of birds, lizards, and rodents as hosts for the western black-legged tick Ixodes pacificus. J Vector Ecol. 2004; 29(2):295–308.
8. Castro MB, Wright SA. Vertebrate hosts of Ixodes pacificus (Acari: ixodidae) in California. J Vector Ecol. 2007; 32(1):140–149. doi:10.3376/1081-1710(2007)32[140:vhoipa]2.0.co;2
9. Westrom DR, Lane RS, Anderson JR. Ixodes pacificus (Acari: Ixodidae): population dynamics and distribution on Columbian black-tailed deer (Odocoileus hemionus columbianus). J Med Entomol. 1985;22(5):507–511. doi:10.1093/jmedent/22.5.507
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11. MacDonald AJ, McComb S, Sambado S. Linking Lyme disease ecology and epidemiology: Reservoir host identity, not richness, determines tick infection and human disease in California. Environ Res Lett. 2022; 17(11). DOI 10.1088/1748-9326/ac9ece
12. Salkeld DJ, Lane RS. Community ecology and disease risk: lizards, squirrels, and the Lyme disease spirochete in California, USA. Ecology. 2010; 91(1):293–298. https://doi.org/10.1890/08-2106.1
13. Salomon J, Lawrence A, Crews A, Sambado S, Swei A. Host infection and community composition predict vector burden. Oecologia. 2021; 196(2):305-316. https://doi.org/10.1007/s00442-021-04851-9
14. Hahn MB, Feirer S, Monaghan AJ, et al. Modeling future climate suitability for the western blacklegged tick, Ixodes pacificus, in California with an emphasis on land access and ownership. Ticks Tick Borne Dis. 2021; 12(5):101789. doi:10.1016/j.ttbdis.2021.101789.
15. Casher L, Lane R, Barrett R, Eisen L. Relative importance of lizards and mammals as hosts for ixodid ticks in northern California. Exp Appl Acarol. 2002; 26(1-2):127-143. doi:10.1023/a:1020911306291
16. Lane RS, Loye JE. Lyme disease in California: interrelationship of Ixodes pacificus (Acari: Ixodidae), the western fence lizard (Sceloporus occidentalis), and Borrelia burgdorferi. J Med Entomol. 1989; 26(4):272-278. doi:10.1093/jmedent/26.4.272
17. Lane RS, Quistad GB. Borreliacidal factor in the blood of the western fence lizard (Sceloporus occidentalis). J Parasitol. 1998; 84(1):29-34.
18. Lane RS, Mun J, Eisen L, Eisen RJ. Refractoriness of the western fence lizard (Sceloporus occidentalis) to the Lyme disease group spirochete Borrelia bissettii. J Parasitol. 2006;92(4):691-696. doi:10.1645/GE-738R1.1
19. Eisen L, Eisen RJ, Lane RS. Seasonal activity patterns of Ixodes pacificus nymphs in relation to climatic conditions. Med Vet Entomol. 2002;16(3):235-244. doi:10.1046/j.1365-2915.2002.00372.x
20. Eisen RJ, Eisen L, Lane RS. 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. 2006;74(4):632-640.
21. Eisen RJ, Clark RJ, Monaghan AJ, Eisen L, Delorey MJ, Beard CB. Host-seeking phenology of Ixodes pacificus (Acari: Ixodidae) nymphs in Northwestern California in relation to calendar week, woodland type, and weather conditions. J Med Entomol. 2017;54(1):125-131. doi:10.1093/jme/tjw155
22. Tälleklint-Eisen L, Lane RS. Variation in the density of questing Ixodes pacificus (Acari: Ixodidae) nymphs infected with Borrelia burgdorferi at different spatial scales in California. J Parasitol. 1999; 85(5):824–831.
23. Rose I, Yoshimizu MH, Bonilla DL, Fedorova N, Lane RS, Padgett KA. Phylogeography of Borrelia spirochetes in Ixodes pacificus and Ixodes spinipalpis ticks highlights differential acarological risk of tick-borne disease transmission in northern versus southern California. PLoS One. 2019; 14(4):e0214726. Published 2019 Apr 4. doi:10.1371/journal.pone.0214726
24. Wallace D, Ratti V, Kodali A, et al. Effect of rising temperature on Lyme disease: Ixodes scapularis population dynamics and Borrelia burgdorferi transmission and prevalence. Can J Infect Dis Med Microbiol. 2019;2019:9817930. Published 2019 Sep 16. doi:10.1155/2019/9817930
25. Winter JM, Partridge TF, Wallace D, et al. Modeling the sensitivity of blacklegged ticks (Ixodes scapularis) to temperature and land cover in the northeastern United States. J Med Entomol. 2021; 58(1):416–27. doi:10.1093/jme/tjaa179
26. Ratti V, Winter JM, Wallace DI. Dilution and amplification effects in Lyme disease: Modeling the effects of reservoir-incompetent hosts on Borrelia burgdorferi sensu stricto transmission. Ticks Tick Borne Dis. 2021;12(4):101724. doi:10.1016/j.ttbdis.2021.101724
27. Wittmer HU, Forrester TD, Allen ML, Marescot L, Casady DS. Black-tailed deer population assessment in the Mendocino National Forest, California final project report—December 2014. DOI:10.13140/2.1.3440.9764
28. Stafford III KC. Reduced abundance of Ixodes scapularis (Acari: Ixodidae) with exclusion of deer by electric fencing. J Med Entomol. 1993; 30:986–996. doi:10.1093/jmedent/30.6.986
29. Levi T, Keesing F, Holt RD, Barfield M, Ostfeld RS. Quantifying dilution and amplification in a community of hosts for tick-borne pathogens. Ecol Appl. 2016;26:484–498. doi:10.1890/15-0122
30. Ostfeld RS, Keesing F. Biodiversity and disease risk: the case of Lyme disease. Conservation biology 2000;14, 722–728. https://doi.org/10.1046/j.1523-1739.2000.99014.x
31. Ostfeld RS. Biodiversity loss and the rise of zoonotic pathogens. Clin Microbiol Infect. 2009;15 Suppl 1:40–43. doi:10.1111/j.1469-0691.2008.02691.x
32. Ogden N, Lindsay L, Beauchamp G, et al. Investigation of relationships between temperature and developmental rates of tick Ixodes scapularis (Acari: Ixodidae) in the laboratory and field. J Med Entomol. 2004;41(4):622–633. doi:10.1603/0022-2585-41.4.622
33. Lane RS, Kleinjan JE, Schoeler GB. Diel activity of nymphal Dermacentor occidentalis and Ixodes pacificus (Acari: Ixodidae) in relation to meteorological factors and host activity periods. J Med Entomol. 1995;32(3):290–299. doi:10.1093/jmedent/32.3.290
34. Gray JS, Kahl O, Lane RS, Levin ML, Tsao JI. Diapause in ticks of the medically important Ixodes ricinus species complex. Ticks Tick Borne Dis. 2016;7(5):992–1003. doi:10.1016/j.ttbdis.2016.05.006
35. Belozerov VN. New aspects in investigations of diapause and non-diapause dormancy types in insects and other arthropods. Entomol Rev. 2009;89: 127–136. https://doi.org/10.1134/S0013873809020018
36. Belozerov VN. Diapause and quiescence as two main kinds of dormancy and their significance in life cycles of mites and ticks (Chelicerata: Arachnida: Acari). Acarina. 2009; 17(1): 3–32.
37. MathWorks. 2016. Natick, MA.
38. Xu G, Pearson P, Dykstra E, Andrews ES, Rich SM. Human-biting Ixodes ticks and pathogen prevalence from California, Oregon, and Washington. Vector Borne Zoonotic Dis. 2019; 19(2):106–114. doi:10.1089/vbz.2018.2323
39. Eisen RJ, Eisen L, Ogden NH, Beard CB. Linkages of weather and climate with Ixodes scapularis and Ixodes pacificus (Acari: Ixodidae), enzootic transmission of Borrelia burgdorferi, and Lyme disease in North America. J Med Entomol. 2016; 53(2):250–261. doi:10.1093/jme/tjv199
40. Eisen L, Eisen RJ, Lane RS. Geographical distribution patterns and habitat suitability models for presence of host-seeking ixodid ticks in dense woodlands of Mendocino County, California. J Med Entomol. 2006; 43(2):415–427. doi:10.1603/0022-2585(2006)043[0415:gdpahts]2.0.co;2
41. Swei A, Ostfeld RS, Lane RS, Briggs CJ. Impact of the experimental removal of lizards on Lyme disease risk. Proceedings of the Royal Society B: Biological Sciences. 2011; 278(1720):2970–2978.
42. Benth JŠ, Benth FE, Jalinskas P. A spatial-temporal model for temperature with seasonal variance. J Appl Stat. 2007; 34(7):823–841.
2. Dizon C, Lysyk TJ, Couloigner I, Cork SC. Ecology and epidemiology of Lyme disease in Western North America. Zoonotic Dis. 2023; 3(1):20–37. https://doi.org/10.3390/zoonoticdis3010004
3. Maggi RG, Toliver M, Richardson T, Mather T, Breitschwerdt EB. Regional prevalences of Borrelia burgdorferi, Borrelia bissettiae, and Bartonella henselae in Ixodes affinis, Ixodes pacificus and Ixodes scapularis in the USA. Ticks Tick Borne Dis. 2019; 10(2):360-364. doi:10.1016/j.ttbdis.2018.11.015
4. Padgett KA, Lane RS. Life cycle of Ixodes pacificus (Acari: Ixodidae): timing of developmental processes under field and laboratory conditions. J Med Entomol. 2001; 38(5):684–693. doi:10.1603/0022-2585-38.5.684
5. Troughton DR, Levin ML. Life cycles of seven ixodid tick species (Acari: Ixodidae) under standardized laboratory conditions. J Med Entomol. 2007; 44(5):732–740. doi:10.1603/0022-2585(2007)44[732:lcosit]2.0.co;2
6. Peavey CA, Lane RS. Field and laboratory studies on the timing of oviposition and hatching of the western black-legged tick, Ixodes pacificus (Acari: Ixodidae). Exp Appl Acarol. 1996; 20(12):695–711. doi:10.1007/BF00051555
7. Eisen L, Eisen RJ, Lane RS. The roles of birds, lizards, and rodents as hosts for the western black-legged tick Ixodes pacificus. J Vector Ecol. 2004; 29(2):295–308.
8. Castro MB, Wright SA. Vertebrate hosts of Ixodes pacificus (Acari: ixodidae) in California. J Vector Ecol. 2007; 32(1):140–149. doi:10.3376/1081-1710(2007)32[140:vhoipa]2.0.co;2
9. Westrom DR, Lane RS, Anderson JR. Ixodes pacificus (Acari: Ixodidae): population dynamics and distribution on Columbian black-tailed deer (Odocoileus hemionus columbianus). J Med Entomol. 1985;22(5):507–511. doi:10.1093/jmedent/22.5.507
10. MacDonald AJ, Hyon DW, Brewington JB, O'Connor KE, Swei A, Briggs CJ. Lyme disease risk in southern California: abiotic and environmental drivers of Ixodes pacificus (Acari: Ixodidae) density and infection prevalence with Borrelia burgdorferi. Parasit Vectors. 2017;10(1):1–6. Published 2017 Jan 5. doi:10.1186/s13071-016-1938-y
11. MacDonald AJ, McComb S, Sambado S. Linking Lyme disease ecology and epidemiology: Reservoir host identity, not richness, determines tick infection and human disease in California. Environ Res Lett. 2022; 17(11). DOI 10.1088/1748-9326/ac9ece
12. Salkeld DJ, Lane RS. Community ecology and disease risk: lizards, squirrels, and the Lyme disease spirochete in California, USA. Ecology. 2010; 91(1):293–298. https://doi.org/10.1890/08-2106.1
13. Salomon J, Lawrence A, Crews A, Sambado S, Swei A. Host infection and community composition predict vector burden. Oecologia. 2021; 196(2):305-316. https://doi.org/10.1007/s00442-021-04851-9
14. Hahn MB, Feirer S, Monaghan AJ, et al. Modeling future climate suitability for the western blacklegged tick, Ixodes pacificus, in California with an emphasis on land access and ownership. Ticks Tick Borne Dis. 2021; 12(5):101789. doi:10.1016/j.ttbdis.2021.101789.
15. Casher L, Lane R, Barrett R, Eisen L. Relative importance of lizards and mammals as hosts for ixodid ticks in northern California. Exp Appl Acarol. 2002; 26(1-2):127-143. doi:10.1023/a:1020911306291
16. Lane RS, Loye JE. Lyme disease in California: interrelationship of Ixodes pacificus (Acari: Ixodidae), the western fence lizard (Sceloporus occidentalis), and Borrelia burgdorferi. J Med Entomol. 1989; 26(4):272-278. doi:10.1093/jmedent/26.4.272
17. Lane RS, Quistad GB. Borreliacidal factor in the blood of the western fence lizard (Sceloporus occidentalis). J Parasitol. 1998; 84(1):29-34.
18. Lane RS, Mun J, Eisen L, Eisen RJ. Refractoriness of the western fence lizard (Sceloporus occidentalis) to the Lyme disease group spirochete Borrelia bissettii. J Parasitol. 2006;92(4):691-696. doi:10.1645/GE-738R1.1
19. Eisen L, Eisen RJ, Lane RS. Seasonal activity patterns of Ixodes pacificus nymphs in relation to climatic conditions. Med Vet Entomol. 2002;16(3):235-244. doi:10.1046/j.1365-2915.2002.00372.x
20. Eisen RJ, Eisen L, Lane RS. 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. 2006;74(4):632-640.
21. Eisen RJ, Clark RJ, Monaghan AJ, Eisen L, Delorey MJ, Beard CB. Host-seeking phenology of Ixodes pacificus (Acari: Ixodidae) nymphs in Northwestern California in relation to calendar week, woodland type, and weather conditions. J Med Entomol. 2017;54(1):125-131. doi:10.1093/jme/tjw155
22. Tälleklint-Eisen L, Lane RS. Variation in the density of questing Ixodes pacificus (Acari: Ixodidae) nymphs infected with Borrelia burgdorferi at different spatial scales in California. J Parasitol. 1999; 85(5):824–831.
23. Rose I, Yoshimizu MH, Bonilla DL, Fedorova N, Lane RS, Padgett KA. Phylogeography of Borrelia spirochetes in Ixodes pacificus and Ixodes spinipalpis ticks highlights differential acarological risk of tick-borne disease transmission in northern versus southern California. PLoS One. 2019; 14(4):e0214726. Published 2019 Apr 4. doi:10.1371/journal.pone.0214726
24. Wallace D, Ratti V, Kodali A, et al. Effect of rising temperature on Lyme disease: Ixodes scapularis population dynamics and Borrelia burgdorferi transmission and prevalence. Can J Infect Dis Med Microbiol. 2019;2019:9817930. Published 2019 Sep 16. doi:10.1155/2019/9817930
25. Winter JM, Partridge TF, Wallace D, et al. Modeling the sensitivity of blacklegged ticks (Ixodes scapularis) to temperature and land cover in the northeastern United States. J Med Entomol. 2021; 58(1):416–27. doi:10.1093/jme/tjaa179
26. Ratti V, Winter JM, Wallace DI. Dilution and amplification effects in Lyme disease: Modeling the effects of reservoir-incompetent hosts on Borrelia burgdorferi sensu stricto transmission. Ticks Tick Borne Dis. 2021;12(4):101724. doi:10.1016/j.ttbdis.2021.101724
27. Wittmer HU, Forrester TD, Allen ML, Marescot L, Casady DS. Black-tailed deer population assessment in the Mendocino National Forest, California final project report—December 2014. DOI:10.13140/2.1.3440.9764
28. Stafford III KC. Reduced abundance of Ixodes scapularis (Acari: Ixodidae) with exclusion of deer by electric fencing. J Med Entomol. 1993; 30:986–996. doi:10.1093/jmedent/30.6.986
29. Levi T, Keesing F, Holt RD, Barfield M, Ostfeld RS. Quantifying dilution and amplification in a community of hosts for tick-borne pathogens. Ecol Appl. 2016;26:484–498. doi:10.1890/15-0122
30. Ostfeld RS, Keesing F. Biodiversity and disease risk: the case of Lyme disease. Conservation biology 2000;14, 722–728. https://doi.org/10.1046/j.1523-1739.2000.99014.x
31. Ostfeld RS. Biodiversity loss and the rise of zoonotic pathogens. Clin Microbiol Infect. 2009;15 Suppl 1:40–43. doi:10.1111/j.1469-0691.2008.02691.x
32. Ogden N, Lindsay L, Beauchamp G, et al. Investigation of relationships between temperature and developmental rates of tick Ixodes scapularis (Acari: Ixodidae) in the laboratory and field. J Med Entomol. 2004;41(4):622–633. doi:10.1603/0022-2585-41.4.622
33. Lane RS, Kleinjan JE, Schoeler GB. Diel activity of nymphal Dermacentor occidentalis and Ixodes pacificus (Acari: Ixodidae) in relation to meteorological factors and host activity periods. J Med Entomol. 1995;32(3):290–299. doi:10.1093/jmedent/32.3.290
34. Gray JS, Kahl O, Lane RS, Levin ML, Tsao JI. Diapause in ticks of the medically important Ixodes ricinus species complex. Ticks Tick Borne Dis. 2016;7(5):992–1003. doi:10.1016/j.ttbdis.2016.05.006
35. Belozerov VN. New aspects in investigations of diapause and non-diapause dormancy types in insects and other arthropods. Entomol Rev. 2009;89: 127–136. https://doi.org/10.1134/S0013873809020018
36. Belozerov VN. Diapause and quiescence as two main kinds of dormancy and their significance in life cycles of mites and ticks (Chelicerata: Arachnida: Acari). Acarina. 2009; 17(1): 3–32.
37. MathWorks. 2016. Natick, MA.
38. Xu G, Pearson P, Dykstra E, Andrews ES, Rich SM. Human-biting Ixodes ticks and pathogen prevalence from California, Oregon, and Washington. Vector Borne Zoonotic Dis. 2019; 19(2):106–114. doi:10.1089/vbz.2018.2323
39. Eisen RJ, Eisen L, Ogden NH, Beard CB. Linkages of weather and climate with Ixodes scapularis and Ixodes pacificus (Acari: Ixodidae), enzootic transmission of Borrelia burgdorferi, and Lyme disease in North America. J Med Entomol. 2016; 53(2):250–261. doi:10.1093/jme/tjv199
40. Eisen L, Eisen RJ, Lane RS. Geographical distribution patterns and habitat suitability models for presence of host-seeking ixodid ticks in dense woodlands of Mendocino County, California. J Med Entomol. 2006; 43(2):415–427. doi:10.1603/0022-2585(2006)043[0415:gdpahts]2.0.co;2
41. Swei A, Ostfeld RS, Lane RS, Briggs CJ. Impact of the experimental removal of lizards on Lyme disease risk. Proceedings of the Royal Society B: Biological Sciences. 2011; 278(1720):2970–2978.
42. Benth JŠ, Benth FE, Jalinskas P. A spatial-temporal model for temperature with seasonal variance. J Appl Stat. 2007; 34(7):823–841.