Pangloss revisited: A critique of the dilution effect and the biodiversity-buffers-disease paradigm

Parasitology

Volumn 139, Issue 7, 2012, Pages 847-863

  Randolph, S E ^a   Dobson, A D M ^a,b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF STIRLING   (United Kingdom)

Author keywords

biodiversity; community structure; dilution effect; disease risk; helminths; rodent borne infections; vector borne diseases

Indexed keywords

BUFFER;

BIODIVERSITY; BORRELIA; BORRELIA BURGDORFERI; COMMUNITY STRUCTURE; CONSERVATION BIOLOGY; DILUTION; DISEASE TRANSMISSION; ECOSYSTEM; EMPIRICAL RESEARCH; EVIDENCE BASED PRACTICE; HOST PATHOGEN INTERACTION; HUMAN; INFECTION PREVENTION; INFESTATION; LYME DISEASE; MALARIA; MOSQUITO; NONHUMAN; PARASITE; PARASITE PREVALENCE; PARASITE VECTOR; POPULATION DENSITY; PREVALENCE; PRIORITY JOURNAL; REVIEW; RISK ASSESSMENT; RISK FACTOR; TICK; TICK BORNE DISEASE; TICK BORNE ENCEPHALITIS; TICK BORNE ENCEPHALITIS FLAVIVIRUS; VECTOR CONTROL; WEST NILE FEVER; WEST NILE FLAVIVIRUS;

ANIMALS; ARACHNID VECTORS; BIODIVERSITY; BORRELIA BURGDORFERI; ECOSYSTEM; HOST-PARASITE INTERACTIONS; HUMANS; LYME DISEASE; TICK-BORNE DISEASES; TICKS;

HEXAPODA; IXODIDA; RODENTIA; VERMES;

EID: 84861873823     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182012000200     Document Type: Review

References (151)

1. Allan, B. F., Dutra, H. P., Goessling, L. S., Barnett, K., Chase, J. M., Marquis, R. J., Pang, G., Storch, G. A., Thach, R. E. and Orrock, J. L. (2011). Invasive honeysuckle eradication reduces tick-borne disease risk by altering host dynamics. Proceedings of the National Academy of Sciences, USA 107, 18523-18527.
2. Allan, B. F., Goessling, L. S., Storch, G. A. and Thach, R. E. (2010). Identification of reservoir hosts for Amblyomma americanum-associated zoonoses using bloodmeal analysis. Emerging Infectious Diseases 16, 433-440.
3. Allan, B. F., Keesing, F. and Ostfeld, R. S. (2003). Effect of forest fragmentation on Lyme disease risk. Conservation Biology 17, 267-272. (Pubitemid 36234419)
4. Allan, B. F., Langerhaus, R. B., Ryberg, W. A., Landesman, W. J., Griffin, N.W., Katz, R. S., Oberle, B. J., Schutzenhofer, M. R., Smyth, K. N., de St Maurice, A., Clark, L., Crooks, K. R., Hernandez, D. E., McLean, R. G., Ostfeld, R. S. and Chase, J.M. (2009). Ecological correlates of risk and incidence of West Nile virus in the United States. Oecologia 158, 699-708. (Pubitemid 50308893)
5. Apperson, C. S., Levine, J. F., Evans, T. L., Braswell, A. and Heller, J. (1993). Relative utilization of reptiles and rodents as hosts by immature Ixodes scapularis (Acari: Ixodidae) in the coastal plain of North Carolina, USA. Experimental and Applied Acarology 17, 719-731.
6. Begon, M. (2008). Effects of host diversity on disease dynamics. In Infectious Disease Ecology: Effects of Ecosystems on Disease and of Disease on Ecosystems. (ed. Ostfeld, R. S., Keesing, F. and Eviner, V. T.), pp. 12-29. Princeton University Press, Princeton. NJ, USA.
7. Bogh, C., Clarke, S. E., Walraven, G. E. L. and Lindsay, S.W. (2002). Zooprophylaxis, artefact or reality? A paired-cohort study of the effect of passive zooprophylaxis on malaria in The Gambia. Transactions of the Royal Society of Tropical Medicine and Hygiene 96, 593-596. (Pubitemid 36231475)
8. Borer, E. T., Mitchell, C. E., Power, A. G. and Seabloom, E.W. (2009). Consumers indirectly increase infection risk in grassland food webs. Proceedings of the National Academy of Sciences, USA 106, 503-506.
9. Bouma, M. J. and Rowland, M. (1995). Failure of passive zooprophylaxis: cattle ownership in Parkistan is associated with a higher prevalence of malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene 89, 351-353.
10. Brisson, D., Dykhuizen, D. E. and Ostfeld, R. S. (2008). Conspicuous impacts of inconspicuous hosts on the Lyme disease epidemic. Proceedings of the Royal Society of London, B 275, 227-235. (Pubitemid 350174590)
11. Bruemmer, C. M., Rushton, S. P., Gurnell, J., Lurz, P.W.W., Nettleton, P., Sainsbury, A.W., Duff, J. P., Gilray, J. and McInnes, C. J. (2010). Epidemiology of squirrelpox in grey squirrels in the UK. Epidemiology & Infection 138, 941-950.
12. Brunner, J. L. and Ostfeld, R. S. (2008). Multiple causes of variable tick burdens on small-mammal hosts. Ecology 89, 2259-2272.
13. Burri, C., Bastic, V., Maeder, G., Patalas, E. and Gern, L. (2011). Microclimate and the zoonotic cycle of tick-borne encephalitis virus in Switzerland. Journal of Medical Entomology 48, 615-627.
14. Carlson, J. C., Dyer, L. A., Omlin, F. X. and Beier, J. C. (2009). Diversity cascades and malaria vectors. Journal of Medical Entomology 46, 460-464.
15. Civitello, D. J., Flory, S. L. and Clay, K. (2008). Exotic grass invasion reduces survival of Amblyomma americanum and Dermacentor variabilis ticks (Acari: Ixodidae). Journal of Medical Entomology 45, 867-872.
16. Clover, J. R. and Lane, R. S. (1995). Evidence implicating nymphal Ixodes pacificus (Acari: Ixodidae) in the epidemiology of Lyme disease in California. American Journal of Tropical Medicine and Hygiene 53, 237-240.
17. Costello, A., Abbas, M., Allen, A., Ball, S., Bellamy, R., Friel, S., Grace, N., Johnson, A., Kett, M., Lee, M., Levy, C., Maslin, M., McCoy, D., McGuire, B., Montgomery, H., Napier, D., Pagel, C., Patel, J., de Oliveira, J. A. P., Redclift, N., Rees, H., Rogger, D., Scott, J., Stephenson, J., Twigg, J., Wolff, J. and Patterson, C. (2009). Managing the health effects of climate change. The Lancet 373, 1693-1733.
18. Craine, N. G., Randolph, S. E. and Nuttall, P. A. (1995). Seasonal variation in the rôle of grey squirrels as hosts of Ixodes ricinus, the tick vector of the Lyme disease spirochaete, in a British woodland. Folia Parasitologica 42, 73-80.
19. Dalkvist, T., Sibly, R. M. and Topping, C. J. (2011). How predation and landscape fragmentation affect vole population dynamics. PLoS ONE 6, e22834.
20. Daszak, P., Cunningham, A. A. and Hyatt, A. D. (2001). Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Tropica 78, 103-116. (Pubitemid 32179644)
21. Diaz, S., Fargione, J., Chapin, F. S. I. and Tilman, D. (2006). Biodiversity loss threatens human well-being. PLoS Biology 4, 1300-1305.
22. Dizney, L. J. and Ruedas, L. A. (2009). Increased host species diversity and decreased prevalence of Sin Nombre virus. Emerging Infectious Diseases 15, 1012-1018.
23. Dobson, A. P. (2004). Population dynamics of pathogens with multiple host species. The American Naturalist 164 (Suppl.) S64-S78.
24. Dobson, A., Cattadori, I., Holt, R. D., Ostfeld, R. S., Keesing, F., Krichbaum, K., Rohr, J. R., Perkins, S. E. and Hudson, P. J. (2006). Sacred cows and sympathetic squirrels: the importance of biological diversity to human health. PLoS Medicine 3, 714-718.
25. Dobson, A., Lafferty, K. D., Kuris, A. M., Hechinger, R. F. and Jetz, W. (2008). Homage to Linneaus: How many parasites? How many hosts? Proceedings of the National Academy of Sciences, USA105, (Suppl. 1), 11482-11489.
26. Dobson, A. D. M., Finnie, T. J. R. and Randolph, S. E. (2011). A modified matrix model to describe the seasonal population ecology of the European tick Ixodes ricinus. Journal of Applied Ecology 48, 1017-1028.
27. Dobson, A. D. M. and Randolph, S. E. (2011). Modelling the effects of recent changes in climate, host density and acaricide treatments on population dynamics of Ixodes ricinus in the UK. Journal of Applied Ecology 48, 1029-1037.
28. Dowling, D. K. and Simmons, L.W. (2009). Reactive oxygen species as universal constraints in life-history evolution. Proceedings of Royal Society of London, B 276, 1737-1745.
29. Elias, S. P., Lubelczyk, C. B., Rand, P.W., Lacombe, E. H., Holman, M. S. and Smith, R. P. J. (2006). Deer browse resistant exoticinvasive understory: an indicator of elevated human risk of exposure to Ixodes scapularis (Acari: Ixodidae) in southern coastal Maine woodlands. Journal of Medical Entomology 43, 1142-1152. (Pubitemid 44862946)
30. Elton, C. S. (1958). The Ecology of Invasions by Animals and Plants. Methuen, London, UK.
31. Ezenwa, V. O., Godsey, M. S., King, R. J. and Guptill, S. C. (2006). Avian diversity and West Nile virus: testing associations between biodiversity and infectious disease risk. Proceedings of Royal Society of London, B 273, 109-117. (Pubitemid 46768052)
32. Falco, R. C., McKenna, D. F., Daniels, T. J., Nadelman, R. B., Nowakowski, J., Fish, D. and Wormser, G. P. (1999). Temporal relation between Ixodes scapularis abundance and risk for Lyme disease associated with erythema migrans. American Journal of Epidemiology 149, 771-776. (Pubitemid 29180786)
33. Gern, L., Estrada-Peña, A., Frandsen, F., Gray, J., J. S., G., Jaenson, T.G. T., Jongejan, F., Kahl, O., Korenberg, E., Mehl, R. and Nuttall, P. A. (1998). European reservoir hosts of Borrelia burgdorferi sensu lato. Zentralblatt für Bakteriologie 287, 196-204. (Pubitemid 28202519)
34. Giardina, A. R., Schmidt, K. A., Schauber, E.M. and Ostfeld, R. S. (2000). Modeling the role of songbirds and rodents in the ecology of Lyme disease. Canadian Journal of Zoology 78, 2184-2197. (Pubitemid 32145112)
35. Gilbert, L., Norman, R., Laurenson, M. K., Reid, H.W. and Hudson, P. J. (2001). Disease persistence and apparent competition in a three-host community: an empirical and analytical study of large-scale, wild populations. Journal of Animal Ecology 70, 1053-1061. (Pubitemid 33146354)
36. Glass, G. E., Schwarz, B. S., Morgan III, J. M., Johnson, D. T., Noy, P. M. and Israel, E. (1995). Environmental risk factor for Lyme disease identified with geographic information systems. American Journal of Public Health 85, 944-948.
37. Gray, J. S., Kahl, O., Janetzki, C. and Stein, J. (1992). Studies on the ecology of Lyme disease in a deer forest in County Galway, Ireland. Journal of Medical Entomology 29, 915-920.
38. Guernier, V., Hochberg, M. E. and Guegan, J.-F. (2004). Ecology drives the worldwide distribution of human diseases. PLoS Biology 2, 0740.
39. Hamer, G. L., Chaves, L. F., Anderson, T. K., Kitron, U. D., Brawn, J. D., Ruiz, M. O., Loss, S. R., Walker, E. D. and Goldberg, T. L. (2011). Fine-scale variation in vector host use and force of infection drive localized patterns of West Nile virus transmission. PLoS ONE 6, e23767.
40. Hanincova, K., Ogden, N. H., Diuk-Wasser, M., Pappas, C. J., Iyer, R., Fish, D., Schwartz, I. and Kurtenbach, K. (2008). Fitness variation of Borrelia burgdorferi sensu stricto strains in mice. Applied and Environmental Microbiology 74, 153-157.
41. Hanski, I., Hansson, L. and Henttonen, H. (1991). Specialist predators, generalist predators, and the microtine rodent cycle. Journal of Animal Ecology 60, 353-367.
42. Hartemink, N. A., Davis, S. A., Reiter, P., Hubálek, Z. and Heesterbeek, J. A. P. (2007). Importance of bird-to-bird transmission for the establishment of West Nile virus. Vector-Borne and Zoonotic Diseases 7, 575-584.
43. Hawley, D.M. and Altizer, S. M. (2011). Disease ecology meets ecological immunology: understanding the links between organismal immunity and infection dynamics in natural populations. Functional Ecology 25, 48-60.
44. Hechinger, R. F. and Lafferty, K. D. (2005). Host diversity begets parasite diversity: bird final hosts and trematodes in snail intermediate hosts. Proceedings of the Royal Society of London, B 272, 1059-1066. (Pubitemid 40943956)
45. Hess, A. D. and Hayes, R. O. (1970). Relative potentials of domestic animals for zooprophylaxis against mosquito vectors of encephalitis. American Journal of Tropical Medicine and Hygiene 19, 327-334.
46. Holt, R. D. and Lawton, J. H. (1994). The ecological consequences of shared natural enemies. Annual Review of Ecology and Systematics 25, 495-520. (Pubitemid 24986129)
47. Hoodless, A. N., Kurtenbach, K., Nuttall, P. A. and Randolph, S. E. (2002). The impact of ticks on pheasant territoriality. Oikos 96, 245-250. (Pubitemid 34543908)
48. Hoogstraal, H. (1981). Changing patterns of tick-borne diseases in modern society. Annual Review of Entomology 26, 75-99.
49. Horobik, V., Keesing, F. and Ostfeld, R. S. (2007). Abundance and Borrelia burgdorferi-infection prevalence of nymphal Ixodes scapularis ticks along forest-field edges. EcoHealth 3, 262-268.
50. Horrocks, N. P. C., Matson, K. D. and Tieleman, B. I. (2011). Pathogen pressure puts immune defense into perspective. Integrative and Comparative Biology 51, 563-576.
51. Hubálek, Z. and Halouzka, J. (1998). Prevalence rates of Borrelia burgdorferi sensu lato in host-seeking Ixodes ricinus ticks in Europe. Parasitology Research 84, 167-172. (Pubitemid 28062547)
52. Hubálek, Z. and Halouzka, J. (1999). West Nile virus -a reemerging mosquito-borne viral disease in Europe. Emerging Infectious Diseases 5, 643-650. (Pubitemid 29493766)
53. Hudson, P. J., Rizzoli, A., Rosa, R., Chemini, C., Jones, L. D. and Gould, E. A. (2001). Tick-borne encephalitis virus in northern Italy: molecular analysis, relationships with density and seasonal dynamics of Ixodes ricinus. Medical and Veterinary Entomology 15, 304-313. (Pubitemid 32901369)
54. Humair, P.-F. and Gern, L. (1998). Relationship between Borrelia burgdorferi sensu lato species, red squirrels (Sciurus vulgaris) and Ixodes ricinus in enzootic areas in Switzerland. Acta Tropica 69, 213-227. (Pubitemid 28243244)
55. Humair, P.-F., Postic, D., Wallich, R. and Gern, L. (1998). An avian reservoir (Turdus merula) of the Lyme borreliosis spirochetes. Zentralblatt für Bakteriologie 287, 521-538. (Pubitemid 28271154)
56. Jensen, P.M. and Frandsen, F. (2000). Temporal risk assessment for Lyme borreliosis in Denmark. Scandinavian Journal of Infectious Diseases 35, 539-544.
57. Jensen, P. M., Hansen, H. and Frandsen, F. (2000). Spatial risk assessment for Lyme borreliosis in Denmark. Scandinavian Journal of Infectious Diseases 35, 545-550.
58. Johnson, P. T. J., Hartson, R. B., Larson, D. J. and Sutherland, D. R. (2008). Diversity and disease: community structure drives parasite transmission and host fitness. Ecology Letters 11, 1017-1026.
59. Johnson, P. T. J., Lund, P. J., Hartson, R. B. and Yoshino, T. P. (2009). Community diversity reduces Schistosoma mansoni transmission, host pathology and human infection risk. Proceedings of Royal Society of London, B 276, 1657-1663.
60. Johnson, P. T. J. and Thieltges, D.W. (2010). Diversity, decoys and the dilution effect: how ecological communities affect disease risk. Journal of Experimental Biology 213, 961-970.
61. Jones, K. E., Patel, N. G., Levy, M. A., Storeygard, A., Balk, D., Gittleman, J. L. and Daszak, P. (2008). Global trends in emerging infectious diseases. Nature, London 451, 990-994.
62. Keesing, F., Belden, L. K., Daszak, P., Dobson, A., Harvell, C. D., Holt, R. D., Hudson, P., Jolles, A., Jones, K. E., Mitchell, C. E., Myers, S. S., Bogich, T. and Ostfeld, R. S. (2010). Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature, London 468, 647-652.
63. Keesing, F., Brunner, J., Duerr, S., Killilea, M., LoGiudice, K., Schmidt, K., Vuong, H. and Ostfeld, R. S. (2009). Hosts as ecological traps for the vector of Lyme disease. Proceedings of the Royal Society, B 276, 3911-3919.
64. Keesing, F., Holt, R. D. and Ostfeld, R. S. (2006). Effects of species diversity on disease risk. Ecology Letters 9, 485-498.
65. Kilpatrick, M., Daszak, P., Jones, M. J., Marra, P. P. and Kramer, L. D. (2006). Host heterogeneity dominates West Nile virus transmission. Proceedings of the Royal Society of London, B 273, 2327-2333. (Pubitemid 44387340)
66. Kimura, K., Isogal, E., Isogal, H., Kamewaka, Y., Nishikawa, T., Ishii, N. and Fujii, N. (1995). Detection of Lyme disease spirochetes in the skin of naturally infected wild sika deer (Cervus nippon yesoensis) by PCR. Applied and Environmental Microbiology 61, 1641-1642.
67. Komar, N., Langevin, S., Hinten, S., Nemeth, N., Edwards, E., Hettler, D., Davis, B., Bowen, R. and Bunning, M. (2003). Experimental infection of North American birds with the New York 1999 strain of West Nile virus. Emerging Infectious Diseases 9, 311-322. (Pubitemid 36330872)
68. Kostiukov, M. A., Alekseev, A. N., Bulychev, V. P. and Gordeeva, Z. E. (1986). [Experimental evidence for infection of Culex pipiens L. mosquitoes by West Nile fever virus from Rana ridibunda Pallas and its transmission by bites]. Meditsinskaya Parazitologiya i Parazitarnye Bolezni 6, 76-78.
69. Kurtenbach, K., Carey, D., Hoodless, A. N., Nuttall, P. A. and Randolph, S. E. (1998a). Competence of pheasants as reservoirs for Lyme disease spirochetes. Journal of Medical Entomology 35, 77-81. (Pubitemid 128461098)
70. Kurtenbach, K., Hanincova, K., Tsao, J. I., Margos, G., Fish, D. and Ogden,N.H. (2006). Fundamental processes in the evolutionary ecology of Lyme borreliosis. Nature Reviews Microbiology 4, 660-669.
71. Kurtenbach, K., Peacey, M. F., Rijpkema, S. G. T., Hoodless, A. N., Nuttall, P. A. and Randolph, S. E. (1998b). Differential transmission of the genospecies of Borrelia burgdorferi sensu lato by game birds and small rodents in England. Applied and Environmental Microbiology 64, 1169-1174. (Pubitemid 28188367)
72. Kurtenbach, K., Sewell, H., Ogden, N. H., Randolph, S. E. and Nuttall, P. A. (1998c). Serum complement as a key factor in Lyme disease ecology. Infection and Immunity 66, 1248-1251. (Pubitemid 28101172)
73. Lane, R. S. and Quistad, G. B. (1998). Borreliacidal factor in the blood of the western fence lizard (Sceloporus occidentalis). Journal of Parasitology 84, 29-34. (Pubitemid 28125427)
74. Larigauderie, A. and Mooney, H. A. (2010). The Intergovernmental science-policy Platform on Biodiversity and Ecosystems Services: moving a step closer to an IPCC-like mechanism for biodiversity. Current Opinion in Environmental Sustainability 2, 9-14.
75. Lee, K. A., Martin, L. B., Hasselquist, D., Ricklefs, R. E. and Wikelski, M. (2006). Contrasting adaptive immune defenses and blood parasite prevalence in closely related Passer sparrows. Oecologia 150, 383-392. (Pubitemid 44748895)
76. Lee, K. A., Wikelski, M., Robinson, W. D., Robinson, T. R. and Klasing, K. C. (2008). Constitutive immune defences correlate with life-history variables in tropical birds. Journal of Animal Ecology 77, 356-363. (Pubitemid 351191060)
77. Linard, C., Lamarque, P., Heyman, P., Ducoffre, G., Lutasu, V., Tersago, K., Vanwambeke, S. O. and Lambin, E. F. (2007). Determinants of the geographic distribution of Puumala virus and Lyme borreliosis infections in Belgium. International Journal of Health Geographics 6, 15-29.
78. LoGiudice, K., Duerr, S. T. K., Newhouse, M. J., Schmidt, K. A., Killilea, M. E. and Ostfeld, R. S. (2008). Impact of host community composition on Lyme disease risk. Ecology 89, 2841-2849.
79. LoGiudice, K., Ostfeld, R. S., Schmidt, K. A. and Keesing, F. (2003). The ecology of infectious disease: Effects of host diversity and community composition on Lyme disease risk. Proceedings of the National Academy of Sciences, USA 100, 567-571. (Pubitemid 36126092)
80. Loss, S. R., Hamer, G. L., Walker, E. D., Ruiz,M. O., Goldberg, T. L., Kitron, U. and Brawn, J.D. (2009). Avian host community structure and prevalence of West Nile virus in Chicago, Illinois. Oecologia 159, 415-424.
81. Macdonald, G. (1956). Epidemiological basis of malaria control. Bulletin of the World Health Organization 15, 613-626.
82. Marina, C. F., Bond, J. G., Casas, M., Munoz, J., Orozco, A., Valle, J. and Williams, T. (2011). Spinosad as an effective larvicide for control of Aedes albopictus and Aedes aegypti, vectors of dengue in southern Mexico. Pest Management Science 67, 114-121.
83. Marris, E. (2010). UN body will assess ecosystems and biodiversity. Nature, London 465, 859-859.
84. Martin, L. B., Hasselquist, D. and Wikelski, M. (2006). Investment in immune defense is linked to pace of life in house sparrows. Oecologia 147, 565-575.
85. Martin, L. B., Weil, Z. M. and Nelson, R. J. (2007). Immune defense and reproductive pace of life in Peromyscus mice. Ecology 88, 2516-2528. (Pubitemid 351345109)
86. Matuschka, F.-R., Fischer, P., Heiler, M., Richter, D. and Spielman, A. (1992). Capacity of European animals as reservoir hosts for the Lyme disease spirochete. Journal of Infectious Diseases 165, 479-483.
87. Matuschka, F.-R., Heiler, M., Eiffert, H., Fischer, P., Lotter, H. and Spielman, A. (1993). Diversionary role of hoofed game in the transmission of Lyme-disease spirochetes. American Journal of Tropical Medicine and Hygiene 48, 693-699. (Pubitemid 23187201)
88. Matuschka, F.-R., Schinkel, T.W., Klug, B., Spielman, A. and Richter, D. (2000). Relative importance of European rabbits for Lyme disease spirochaetes. Parasitology 121, 297-302.
89. Miller, D. L., Mauel, M. J., Baldwin, C. L., Burtle, G., Ingram, D., Hines, M. E. and Frazier, K. S. (2003). West Nile virus in farmed alligators. Emerging Infectious Diseases 9, 794-799. (Pubitemid 36801578)
90. Murgue, B., Murri, S., Zientara, S., Durand, B., Durand, J.-P. and Zeller, H. (2001). West Nile outbreak in horses in southern France, 2000: the return after 35 years. Emerging Infectious Diseases 7, 692-696. (Pubitemid 32845261)
91. Nah, K., Kim, Y. and Lee, J. M. (2010). The dilution effect of the domestic animal population on the transmission of P. vivax malaria. Journal of Theoretical Biology 266, 299-306.
92. Nupp, T. E. and Swihart, R. K. (1996). Effect of forest patch area on population attributes of white-footed mice (Peromyscus leucopus) in fragmented landscapes. Canadian Journal of Zoology 74, 467-472.
93. Nupp, T. E. and Swihart, R. K. (1998). Effects of forest fragmentation on population attributes of white-footed mice and eastern chipmunks. Journal of Mammalogy 79, 1234-1243. (Pubitemid 128485078)
94. Ogden, N. H., Nuttall, P. A. and Randolph, S. E. (1997). Natural Lyme disease cycles maintained via sheep by co-feeding ticks. Parasitology 115, 591-599. (Pubitemid 28078655)
95. Ogden, N.H. and Tsao, J. I. (2009). Biodiversity and Lyme disease: dilution or amplification? Epidemics 1, 196-206.
96. Orrock, J. L., Allan, B. F. and Drost, C. A. (2011). Biogeographic and ecological regulation of disease: prevalence of Sin Nombre virus in island mice is related to island area, precipitation, and predator richness. American Naturalist 177, 691-697.
97. Ostfeld, R. S. (2009). Biodiversity loss and the rise of zoonotic pathogens. Clinical Infectious Diseases 15, 40-43.
98. Ostfeld, R. S., Canham, C. D., Oggenfuss, K., Winchcombe, R. J. and Keesing, F. (2006). Climate, deer, rodents, and acorns as determinants of variation in Lyme-disease risk. PLoS Biology 4, e145.
99. Ostfeld, R. S. and Holt, R. D. (2004). Are predators good for your health? Evaluating evidence for top-down regulation of zoonotic disease reservoirs. Frontiers in Ecology and the Environment 2, 13-20.
100. Ostfeld, R. S. and Keesing, F. (2000a). Biodiversity and disease risk: the case of Lyme disease. Conservation Biology 14, 722-728. (Pubitemid 30390728)
101. Ostfeld, R. S. and Keesing, F. (2000b). The function of biodiversity in the ecology of vector-borne zoonotic diseases. Canadian Journal of Zoology 78, 2061-2078. (Pubitemid 32145098)
102. Ostfeld, R. S. and LoGiudice, K. (2003). Community disassembly, biodiversity loss, and the erosion of an ecosystem service. Ecology 84, 1421-1427. (Pubitemid 37435729)
103. Packer, C., Holt, R. D., Hudson, P. J., Lafferty, K. D. and Dobson, A. P. (2003). Keeping herds healthy and alert: implications of predator control for infectious disease. Ecology Letters 6, 797-802. (Pubitemid 37105907)
104. Paddock, C. D. and Yabsley, M. J. (2007). Ecological havoc, the rise of white-tailed deer, and the emergence of Amblyomma americanum-associated zoonoses in the United States. Current Topics in Microbiology and Immunology 315, 289-324.
105. Peixoto, I. D. and Abramson, G. (2006). The effect of biodiversity on the hantavirus epizootic. Ecology 87, 873-879.
106. Perkins, S. E., Cattadori, I. M., Tagliapietra, V., Rizzoli, A. and Hudson, P. J. (2006). Localized deer absence leads to tick amplification. Ecology 87, 1981-1986. (Pubitemid 44215723)
107. Piesman, J. (2002). Ecology of Borrelia burgdorferi sensu lato in North America. In Lyme Borreliosis Biology, Epidemiology and Control (ed. Gray, J. S., Kahl, O., Lane, R. S. and Stanek, G.), pp. 223-250. Cabi Wallingford U.K.
108. CABI, Wallingford, UK. Piesman, J. and Gern, L. (2008). Lyme borreliosis in Europe and North America. In Ticks: Biology, Disease and Control (ed. Bowman, A. S. and Nuttall, P. A.), pp. 220-252. Cambridge University Press Cambridge U.K.
109. Cambridge University Press, Cambridge, UK. Plyusnina, A., Krajinovic, L. C., Margaletic, J., Niemimaa, J., Nemirov, K., Lundkvist, A., Markotic, A., Miletic-Medved, M., Avsic-Zupanc, T., Henttonen, H. and Plyusnin, A. (2011). Genetic evidence for the presence of two distinct hantaviruses associated with Apodemus mice in Croatia and analysis of local strains. Journal of Medical Virology 83, 108-114.
110. Pongsiri, M. J. and Roman, J. (2007). Examining the links between biodiversity and human health: an interdisciplinary research intiative at the U.S. Environmental Protection Agency. EcoHealth 4, 82-85. (Pubitemid 46625431)
111. Pongsiri, M. J., Roman, J., Ezenwa, V. O., Goldberg, T. L., Koren, H. S., Newbold, S. C., Ostfeld, R. S., Pattanayak, S. K. and Salkeld, D. J. (2009). Biodiversity loss affects global disease ecology. BioScience 59, 945-954.
112. Power, A. G. and Mitchell, C. E. (2004). Pathogen spillover in disease epidemics. American Naturalist 164, S79-S89. (Pubitemid 39509007)
113. Pugliese, A. and Rosa, R. (2008). Effect of host populations on the intensity of ticks and the prevalence of tick-borne pathogens: how to interpret the results of deer exclosure experiments. Parasitology 135, 1531-1544.
114. Randolph, S. E. (2004). Tick ecology: processes and patterns behind the epidemiological risk posed by ixodid ticks as vectors. Parasitology 129, S37-66.
115. Randolph, S. E. and Steele, G.M. (1985). An experimental evaluation of conventional control measures against the sheep tick Ixodes ricinus (L) (Acari: Ixodidae). II. The dynamics of the tick-host interaction. Bulletin of Entomological Research 75, 501-518.
116. Randolph, S. E. and Storey, K. (1999). Impact of microclimate on immature tick-rodent interactions (Acari: Ixodidae): implications for parasite transmission. Journal of Medical Entomology 36, 741-748. (Pubitemid 129559038)
117. Reiter, P. (2008). Global warming and malaria: knowing the horse before hitching the cart. Malaria Journal 7, S3.
118. Rizzoli, A., Hauffe, H. C., Tagliapietra, V., Neteler, M. and Rosa, R. (2009). Forest structure and roe deer abundance predict tick-borne encephalitis risk in Italy. PLoS ONE 4, e4336.
119. Roche, B. and Guégan, J.-F. (2011). Ecosystem dynamics, biological diversity and emerging infectious diseases. Comptes Rendus Biologies 334, 385-392.
120. Rosa, R., Pugliese, A., Norman, R. and Hudson, P. J. (2003). Thresholds for disease persistence in models for tick-borne infections including non-viraemic transmission, extended feeding and tick aggregation. Journal of Theoretical Biology 224, 359-376. (Pubitemid 37297432)
121. Ruedas, L. A., Salazar-Bravo, J., Tinnin, D. S., Armien, B., Caceres, L., Garcia, A., Diaz, M. A., Gracia, F., Suzán, G., Peters, C. J., Yates, T. L. and Mills, J. N. (2004). Community ecology of small mammal populations in Panama following an outbreak of Hantavirus pulmonary syndrome. Journal of Vector Ecology 29, 177-191. (Pubitemid 39008161)
122. Saul, A. (2003). Zooprophylaxis or zoopotentiation: the outcome of introduced animals on vector transmission is highly dependent on the mosquito mortality while searching. Malaria Journal 2, 32.
123. Sbrana, E., Tonry, J. H., Xiao, S. Y., da Rosa, A. P., Higgs, S. and Tesh, R. B. (2005). Oral transmission ofWest Nile virus in a hamster model. American Journal of Tropical Medicine and Hygiene 72, 325-329. (Pubitemid 41278885)
124. Sota, T. and Mogi, M. (1989). Effectiveness of zooprophylaxis in malaria control -a theoretical enquiry, with a model for mosquito populations with two bloodmeal hosts. Medical and Veterinary Entomology 3, 337-345.
125. Spielman, A., Wilson, M. L., Levine, J. F. and Piesman, J. (1985). Ecology of Ixodes dammini-borne human babesiosis and Lyme disease. Annual Review of Entomology 30, 439-460.
126. Stafford (III), K. C., Cartter, M. L., Magarelli, L. A., Ertel, S.-H. and Mshar, P. A. (1998). Temporal correlations between tick abundance and prevalence of ticks infected with Borrelia burgdorferi and increasing incidence of Lyme disease. Journal of Clinical Microbiology 36, 1240-1244. (Pubitemid 28208006)
127. Steinbach Elwell, L. C., Kerans, B. L. and Zickovich, J. (2009). Hostparasite interactions and competition between tubificid species in a benthic community. Freshwater Biology 54, 1616-1628.
128. Suzán, G., Armien, N., Mills, J. N., Marce, E., Ceballos, G., Avila, M., Salazar-Bravo, J., Ruedas, L. A., Armien, B. and Yates, T. L. (2008). Epidemiological considerations of rodent community composition in fragmented landsacpes in Panama. Journal of Mammalogy 89, 634-690.
129. Suzán, G., Marce, E., Giermakowski, J. T., Mills, J. N., Ceballos, G., Ostfeld, R. S., Armien, B., Pascale, J. M. and Yates, T. L. (2009). Experimental evidence for reduced rodent diversity causing increased hantavirus prevalence. PLoS ONE 4, e5461.
130. Swaddle, J. P. and Calos, S. E. (2008). Increased avian diversity is associated with lower incidence of human West Nile infection: observation of the dilution effect. PLoS ONE 3, e2488.
131. Swei, A., Ostfeld, R. S., Lane, R. S. and Briggs, C. J. (2011). Impact of the experimental removal of lizards on Lyme disease risk. Proceedings of the Royal Society of London, B 278, 2970-2978.
132. Talleklint, L. and Jaenson, T. G. T. (1994). Transmission of Borrelia burgdorferi s.l. from mammal reservoirs to the primary vector of Lyme borreliosis, Ixodes ricinus (Acari: Ixodidae), in Sweden. Journal of Medical Entomology 31, 880-886. (Pubitemid 2163473)
133. Talleklint, L. and Jaenson, T. G. T. (1996). Relationship between Ixodes ricinus density and prevalence of infection with Borrelia-like spirochetes and density of infected ticks. Journal of Medical Entomology 33, 805-811. (Pubitemid 126429452)
134. Tersago, K., Schreurs, A., Linard, C., Verhagen, R., Van Dongen, S. and Leirs, H. (2008). Population, environmental, and community effects on local bank vole (Myodes glareolus) Puumala virus infection in an area with low human incidence. Vector-Borne and Zoonotic Diseases 8, 235-244. (Pubitemid 351630136)
135. Tersago, K., Verhagen, R. and Leirs, H. (2011a). Temporal variation in individual factors associated with hantavirus infection in bank voles during an epizootic: implications for Puumala virus transmission dynamics. Vector-Borne and Zoonotic Diseases 11, 715-721.
136. Tersago, K., Verhagen, R., Servais, A., Heyman, P., Ducoffre, G. and Leirs, H. (2009). Hantavirus disease (nephropathia epidemica) in Belgium: effects of tree seed production and climate. Epidemiology and Infection 137, 250-256.
137. Tersago, K., Verhagen, R., Vapalahti, O., Heyman, P., Ducoffre, G. and Leirs, H. (2011b). Hantavirus outbreak in Western Europe: reservoir host infection dynamics related to human disease patterns. Epidemiology and Infection 139, 381-390.
138. Thieltges, D.W., Bordalo, M. D., Cabalerro Hernandez, A., Prinz, K. and Jensen, K. T. (2009a). Ambient fauna impairs parasite transmission in a marine parasite-host system. Parasitology 135, 1111-1116.
139. Thieltges, D.W., Reise, K., Prinz, K. and Jensen, K. T. (2009b). Invaders interfere with native parasite-host interactions. Biological Invasions 11, 1421-1429.
140. Tilman, D., Knops, J.M. H., Wedin, D., Reich, P. B., Ritchie, S. A. and Siemann, E. (1997). Influence of functional diversity and composition on ecosystem processes. Science 277, 1300-1302. (Pubitemid 27449081)
141. Tilman, D., Reich, P. B. and Knops, J. M. H. (2006). Biodiversity and ecosystem stability in a decade-long grassland experiment. Nature, London 441, 629-632. (Pubitemid 43927293)
142. Tsao, J. I., Wootton, J. T., Bunikis, J., Luna, M. G., Fish, D. and Barbour, A. G. (2004). An ecological approach to preventing human infection: vaccinating wild mouse reservoirs intervenes in the Lyme disease cycle. Proceedings of the National Academy of Sciences, USA 101, 18159-18164. (Pubitemid 40054090)
143. Turell, M. J., Dohm, D. J., Sardelis, M. R., O'Guinn, M. L., Andreadis, T. G. and Blow, J. A. (2005). An update on the potential of North American mosquitoes (Diptera: Culicidae) to transmit West Nile virus. Journal of Medical Entomology 42, 57-62. (Pubitemid 40171915)
144. van Buskirk, J. and Ostfeld, R. S. (1995). Controlling Lyme disease by modifying the density and species composition of tick hosts,. Ecological Applications 5, 1133-1140. (Pubitemid 3004275)
145. Vapalahti, O., Mustonen, J., Lundkvist, A., Henttonen, H., Plyusnin, A. and Vaheri, A. (2003). Hantavirus infections in Europe. Lancet Infectious Diseases 3, 653-661. (Pubitemid 37210229)
146. Voltaire (1759). Candide (edn. Bair L.), Bantam Dell, New York, USA.
147. Ward, J. S. and Mervosh, T. L. (2008). Strategies to reduce browse damage on eastern white pine (Pinis strobus) in southern New England, USA. Forest Ecology and Management 255, 1559-1567.
148. Williams, S. C., Ward, J. S., Worthley, T. E. and Stafford (III), K. C. (2009). Managing Japanese barberry (Ranunculales: Berberidaceae) infestations reduces black-legged tick (Acari: Ixodidae) abundance and infection prevalence with Borrelia burgdorferi (Spirochaetales: Spirochaetaceae). Environmental Entomology 38, 977-984.
149. Wilson, M. L., Litwin, T. S., Gavin, T. A., Capkanis, M. C., Maclean, D. C. and Spielman, A. (1990). Host-dependent differences in feeding and reproduction of Ixodes dammini (Acari: Ixodidae). Journal of Medical Entomology 27, 945-954.
150. Woolhouse, M. E. J. and Gowtage-Sequeria, S. (2005). Host range and emerging and reemerging pathogens. Emerging Infectious Diseases 11, 1842-1847. (Pubitemid 43356078)
151. Zeman, P. and Januska, J. (1999). Epizootiologic background of dissimilar distribution of human cases of Lyme borreliosis and tick-borne encephalitis in a joint endemic area. Comparative Immunology, Microbiology and Infectious Diseases 22, 247-260. (Pubitemid 29333114)