Pathogen persistence in the environment and insect-baculovirus interactions: Disease-density thresholds, epidemic burnout, and insect outbreaks

American Naturalist

Volumn 179, Issue 3, 2012, Pages

  Fuller, Emma ^a,c   Elderd, Bret D ^b   Dwyer, Greg ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b LOUISIANA STATE UNIVERSITY   (United States)

^c THE NATURE CONSERVANCY   (United States)

Author keywords

Complex dynamics; Environmental transmission; Host pathogen; Insect outbreaks; Lymantria dispar; Nucleopolyhedrovirus; Threshold theorem

Indexed keywords

DISEASE TRANSMISSION; EPIDEMIC; EXPERIMENTAL STUDY; FOLIAGE; HOST-PATHOGEN INTERACTION; MOTH; NUMERICAL MODEL; PERSISTENCE; PUPATION; SURVIVAL; THRESHOLD; VIRUS;

ANIMAL; ARTICLE; BACULOVIRUS; BIOLOGICAL MODEL; HOST PATHOGEN INTERACTION; LONGEVITY; MOTH; PHYSIOLOGY; POPULATION DYNAMICS; TIME; UNITED STATES; VIROLOGY;

ANIMALS; BACULOVIRIDAE; HOST-PATHOGEN INTERACTIONS; LONGEVITY; MICHIGAN; MODELS, BIOLOGICAL; MOTHS; POPULATION DYNAMICS; TIME FACTORS;

HEXAPODA; LYMANTRIA; LYMANTRIA DISPAR; NUCLEOPOLYHEDROVIRUS;

EID: 84857028161     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/664488     Document Type: Article

References (93)

1. Abbott, K. C., and G. Dwyer. 2008. Using mechanistic models to understand synchrony in forest insect populations: the North American gypsy moth as a case study. American Naturalist 172: 613-624.
2. Barbosa, P., and V. A. Krischik. 1987. Influence of alkaloids on the feeding preference of eastern deciduous forest trees by the gypsy moth, Lymantria dispar. American Naturalist 130:53-69.
3. Beisner, B., and J. Myers. 1999. Population density and transmission of virus in experimental populations of the western tent caterpillar (Lepidoptera: Lasiocampidae). Environmental Entomology 28: 1107-1113.
4. Berger, J., B. Liseo, and R. Wolpert. 1999. Integrated likelihood methods for eliminating nuisance parameters. Statistical Science 14:1-22.
5. Biever, K., and D. Hostetter. 1985. Field persistence of Trichoplusia ni (Lepidoptera, Noctuidae) single-embedded nuclear polyhedrosis virus on cabbage foliage. Environmental Entomology 14:579-581.
6. Bjornstad, O. N., C. Robinet, and A. M. Liebhold. 2010. Geographic variation in North American gypsy moth cycles: subharmonics, generalist predators, and spatial coupling. Ecology 91:106-118.
7. Bonsall, M., S. Sait, and R. Hails. 2005. Invasion and dynamics of covert infection strategies in structured insect-pathogen populations. Journal of Animal Ecology 74:464-474.
8. Boots, M., J. Greenman, D. Ross, R. Norman, R. Hails, and S. Sait. 2003. The population dynamical implications of covert infections in host-microparasite interactions. Journal of Animal Ecology 72: 1064-1072.
9. Breban, R., J. M. Drake, D. E. Stallknecht, and P. Rohani. 2009. The role of environmental transmission in recurrent avian influenza epidemics. PLoS Computational Biology 5:e1000346. doi:10.1371/journal.pcbi.1000346.
10. Broome, J. R., P. P. Sikorowski, and W. W. Neel. 1974. Effect of sunlight on activity of nuclear polyhedrosis virus fromMalacosoma disstria. Journal of Economic Entomology 67:135-136.
11. Burden, J., C. Nixon, A. Hodgkinson, R. Possee, S. Sait, L. King, and R. Hails. 2003. Covert infections as a mechanism for long-term persistence of baculoviruses. Ecology Letters 6:524-531.
12. Burden, J., R. Possee, S. Sait, L. King, and R. Hails. 2006. Phenotypic and genotypic characterisation of persistent baculovirus infections in populations of the cabbage moth (Mamestra brassicae) within the British Isles. Archives of Virology 151:635-649.
13. Burnham, K. P., and D. R. Anderson. 2002. Model selection and multimodel inference: a practical information-theoretic approach. 2nd ed. Springer New York.
14. Capinera, J. L., S. P. Kirouac, and P. Barbosa. 1976. Phagodeterrency of cadaver components to gypsy moth larvae, Lymantria dispar. Journal of Invertebrate Pathology 28:277-279.
15. Cory, J. S., and J. H. Myers. 2003. The ecology and evolution of insect baculoviruses. Annual Review of Ecological and Evolutionary Systems 34:239-272.
16. D'Amico, V., and J. S. Elkinton. 1995. Rainfall effects on transmission of gypsy moth (Lepidoptera, Lymantriidae) nuclear polyhedrosis virus. Environmental Entomology 24:1144-1149.
17. D'Amico, V., J. Elkinton, J. Podgwaite, J. Buonaccorsi, and G. Dwyer. 2005. Pathogen clumping: an explanation for non-linear transmission of an insect virus. Ecological Entomology 30:383-390.
18. Doane, C. 1969. Trans-ovum transmission of a nuclear-polyhedrosis virus in gypsy moth and inducement of virus susceptibility. Journal of Invertebrate Pathology 14:199-210.
19. Doane, C. 1970. Primary pathogens and their role in development of an epizootic in gypsy moth. Journal of Invertebrate Pathology 15: 21-33.
20. Dobson, A., and M. Meagher. 1996. The population dynamics of brucellosis in the Yellowstone National Park. Ecology 77:1026-1036.
21. Duffy, M. A., and L. Sivars-Becker. 2007. Rapid evolution and ecological host-parasite dynamics. Ecology Letters 10:44-53.
22. Duffy, M. A., C. E. Caceres, S. R. Hall, A. J. Tessier, and A. R. Ives. 2010. Temporal, spatial, and between-host comparisons of patterns of parasitism in lake zooplankton. Ecology 91:3322-3331.
23. Dwyer, G. 1991. The effects of density, stage and spatial heterogeneity on the transmission of an insect virus. Ecology 72:559-574.
24. Dwyer, G., and J. S. Elkinton. 1993. Using simple models to predict virus epizootics in gypsy moth populations. Journal of Animal Ecology 62:1-11.
25. Dwyer, G., J. S. Elkinton, and J. P. Buonaccorsi. 1997. Host heterogeneity in susceptibility and disease dynamics: tests of a mathematical model. American Naturalist 150:685-707.
26. Dwyer, G., J. Dushoff, J. S. Elkinton, and S. A. Levin. 2000. Pathogendriven outbreaks in forest defoliators revisted: building models from experimental data. American Naturalist 156:105-120.
27. Dwyer, G., J. Dushoff, and S. Yee. 2004. The combined effects of pathogens and predators on insect outbreaks. Nature 430:341-345.
28. Dwyer, G., J. Firestone, and T. E. Stevens. 2005. Should models of disease dynamics in herbivorous insects include the effects of varatiability in host-plant foliage quality? American Naturalist 165: 16-31.
29. Ebert, D., O. Rainey, T. M. Embley, and D. Scholz. 1996. Development, life cycle, ultrastructure and phylogenetic position of Pasteuria ramosa Metchnikoff 1888: rediscovery of an obligate endoparasite of Daphnia magna Straus. Philosophical Transactions of the Royal Society B: Biological Sciences 351:1689-1701.
30. Efron, B., and R. J. Tibshirani. 1994. An introduction to the bootstrap. Chapman & Hall/CRC, New York.
31. Elderd, B. D., J. Dushoff, and G. Dwyer. 2008. Host-pathogen interactions, insect outbreaks, and natural selection for disease resistance. American Naturalist 172:829-842.
32. Elkinton, J. S., and A. M. Liebhold. 1990. Population dynamics of gypsy moth in North America. Annual Review of Entomology 35: 571-596.
33. Elnagar, S., and S. Abul-Nasr. 1980. Effect of direct sunlight on the virulence of NPV (nuclear polyhedrosis-virus) of the cotton leafworm, Spodoptera littoralis (boisd). Journal of Applied Entomology 90:75-80.
34. Entwistle, P. F., and P. H. W. Adams. 1977. Prolonged retention of infectivity in nuclear polyhedrosis virus of Gilpinia hercyniae (Hymenoptera, Diprionidae) on foliage of spruce species. Journal of Invertebrate Pathology 29:392-394.
35. Fuxa, J. R., and A. R. Richter. 2007. Effect of nucleopolyhedrovirus concentration in soil on viral transport to cotton (Gossypium hirsutum L.) plants. Biocontrol 52:821-843.
36. Georgievska, L., R. S. M. De Vries, P. Gao, X. Sun, J. S. Cory, J. M. Vlak, and W. Van Der Werf. 2010. Transmission of wild-type and recombinant HaSNPV among larvae of Helicoverpa armigera (Lepidoptera: Noctuidae) on cotton. Environmental Entomology 39: 459-467.
37. Goulson, D., R. Hails, T. Williams, M. Hirst, S. Vasconcelos, B. Green, T. Carty, and J. Cory. 1995. Transmission dynamics of a virus in a stage-structured insect population. Ecology 76:392-401.
38. Grove, M. J., and K. Hoover. 2007. Intrastadial developmental resistance of third instar gypsy moths (Lymantria dispar L.) to L. dispar nucleopolyhedrovirus. Biological Control 40:355-361.
39. Hails, R., P. Hernandez-Crespo, S. Sait, C. Donnelly, B. Green, and J. Cory. 2002. Transmission patterns of natural and recombinant baculoviruses. Ecology 83:906-916.
40. Hall, S. R., M. A. Duffy, A. J. Tessier, and C. E. Caceres. 2005. Spatial heterogeneity of daphniid parasitism within lakes. Oecologia (Berlin) 143:635-644.
41. Hall, S. R., C. R. Becker, M. A. Duffy, and C. E. Caceres. 2010. Variation in resource acquisition and use among host clones creates key epidemiological trade-offs. American Naturalist 176:557-565.
42. Hochberg, M. E. 1989. The potential role of pathogens in biological control. Nature 337:262-265.
43. Hunter, A. 1991. Traits that distinguish outbreaking and nonoutbreaking macrolepidoptera feeding on northern hardwood trees. Oikos 60:275-282.
44. Hunter-Fujita, F., P. Entwistle, H. Evans, and N. Crook. 1998. Insect viruses and pest management. Wiley, Chichester.
45. Ignoffo, C. M., D. L. Hostetter, P. P. Sikorowski, G. Sutter, and W. M. Brooks. 1977. Inactivation of representative species of entomopathogenic viruses, a bacterium, fungus, and protozoan by an UV light-source. Environmental Entomology 6:411-415.
46. Il'inykh, A., and E. Ul'yanova. 2005. Latency of baculoviruses. Biology Bulletin 32:496-502.
47. Ilyinykh, A., M. Shternshis, and S. Kuzminov. 2004. Exploration into a mechanism of transgenerational transmission of nucleopolyhe drovirus in Lymantria dispar L. in western Siberia. Biocontrol 49: 441-454.
48. Jaques, R. P. 1967. Persistence of a nuclear polyhedrosis virus in habitat of host insect Trichoplusia ni. I. Polyhedra deposited on foliage. Canadian Entomologist 99:785-794.
49. Jaques, R. P. 1968. Inactivation of nuclear polyhedrosis virus of Trichoplusia ni by gamma and ultraviolet radiation. Canadian Journal of Microbiology 14:1161-1163.
50. Jaques, R. P. 1972. Inactivation of foliar deposits of virus of Trichoplusia ni (Lepidoptera: Noctuidae) and Pieris rapae (Lepidoptera: Pieridae) and tests on protectant additives. Canadian Entomologist 104:1985-1994.
51. Johnson, D. M., A. M. Liebhold, and O. N. Bjørnstad. 2005. Circumpolar variation in periodicity and synchrony among gypsy moth populations. Journal of Animal Ecology 74:882-892.
52. Keeling, M. J. and P. Rohani. 2007. Modeling infectious diseases in humans and animals. Princeton University Press, Princeton, NJ.
53. Kermack, W. O., and A. G. McKendrick. 1927. Contributions to the mathematical theory of epidemics. Bulletin of Mathematical Biology 53:33-55.
54. King, A. A., E. L. Ionides, M. Pascual, and M. J. Bouma. 2008. Inapparent infections and cholera dynamics. Nature 454:877-881.
55. Kouassi, L. N., K. Tsuda, C. Goto, S. Mukawa, Y. Sakamaki, K. Kusigemati, and M. Nakamura. 2009. Prevalence of latent virus in Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae) and its activation by a heterologous virus. Applied Entomology and Zoology 44:95-102.
56. Lipman, N., B. Corning, and M. Coiro. 1992. The effects of intracage ventilation on microenvironmental conditions in filter-top cages. Laboratory Animals 26:206-210.
57. Lloyd-Smith, J. O., P. C. Cross, C. J. Briggs, M. Daugherty, W. M. Getz, J. Latto, M. S. Sanchez, A. B. Smith, and A. Swei, A. 2005. Should we expect population thresholds for wildlife disease? Trends in Ecology & Evolution 20:511-519.
58. Mathiason, C. K., S. A. Hays, J. Powers, J. Hayes-Klug, J. Langenberg, S. J. Dahmes, D. A. Osborn, et al. 2009. Infectious prions in preclinical deer and transmission of chronic wasting disease solely by environmental exposure. PLoS ONE 4:e5916.
59. McCullagh, P., and J. Nelder. 1989. Generalized linear models. Chapman & Hall/CRC, Boca Raton, FL.
60. Miller, L. K. 1997. The baculoviruses. Plenum, New York.
61. Moreau, G., and C. J. Lucarotti. 2007. A brief review of the past use of baculoviruses for the management of eruptive forest defoliators and recent developments on a sawfly virus in Canada. Forestry Chronicle 83:105-112.
62. Moreau, G., C. J. Lucarotti, E. G. Kettela, G. S. Thurston, S. Holmes, C. Weaver, D. B. Levin, and B. Morin. 2005. Aerial application of nucleopolyhedrosis induces decline in increasing and peaking populations of neodiprion abietis. Biological Control 33:65-73.
63. Morgan, B. J. T. 1992. Analysis of quantal response data. Chapman & Hall, New York.
64. Murray, K. D., and J. S. Elkinton. 1989. Environmental contamination of egg masses as a major component of transgenerational transmission of gypsy-moth nuclear polyhedrosis-virus (Ld- MNPV). Journal of Invertebrate Pathology 53:324-334.
65. Myers, J., R. Malakar, and J. Cory. 2000. Sublethal nucleopolyhedrovirus infection effects on female pupal weight, egg mass size, and vertical transmission in gypsy moth (Lepidoptera: Lymantriidae). Environmental Entomology 29:1268-1272.
66. Olofsson, E. 1988. Persistence and dispersal of the nuclear polyhedrosis virus of Neodiprion sertifer (Geoffroy) (Hymenoptera: Diprionidae) in a virus-free lodgepole pine plantation in Sweden. Canadian Entomologist 120:887-892.
67. Otvos, I. S., J. C. Cunningham, and L. M. Friskie. 1987. Aerial application of nuclear polyhedrosis virus against Douglas-fir tussock moth, Orgyia pseudostugata (Mcdunnough) (Lepidoptera: Lymantriidae). 1. Impact in the year of application. Canadian Entomologist 119:697-706.
68. Park, E. J., C. M. Yin, and J. P. Burand. 1996. Baculovirus replication alters hormone-regulated host development. Journal of General Virology 77:547-554.
69. Parker, B. J., B. D. Elderd, and G. Dwyer. 2010. Host behaviour and exposure risk in an insect-pathogen interaction. Journal of Animal Ecology 79:863-870.
70. Pascual, M., M. Bouma, and A. Dobson. 2002. Cholera and climate: revisiting the quantitative evidence. Microbes and Infection 4:237-245.
71. Peltonen, M., A. M. Liebhold, O. N. Bjornstad, and D. W. Williams. 2002. Spatial synchrony in forest insect outbreaks: roles of regional stochasticity and dispersal. Ecology 83:3120-3129.
72. Podgwaite, J. D., K. S. Shields, R. T. Zerillo, and R. B. Bruen. 1979. Environmental persistence of the nucleopolyhedrosis virus of the gypsy moth, Lymantria dispar. Environmental Entomology 8:528-536.
73. R Development Core Team. 2009. Ra language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.
74. Raymond, B., S. Hartley, J. Cory, R. and R. Hails. 2005. The role of food plant and pathogen-induced behaviour in the persistence of a nucleopolyhedrovirus. Journal of Invertebrate Pathology 88:49-57.
75. Reardon, R. C., J. D. Podgwaite, and R. T. Zerillo. 1996. Gypcheck, the gypsy moth nucelopolyhedrosis virus product. USDA Forest Service, FHTET-96-16.
76. Roland, J., and W. J. Kaupp. 1995. Reduced transmission of foresttent caterpillar (Lepidoptera, Lasiocampidae) nuclear polyhedrosis virus at the forest edge. Environmental Entomology 24:1175-1178.
77. Ross, S. M. 2002. Simulation. 3rd ed. Academic Press, London.
78. Shapiro, M., J. R. Robertson, and R. A. Bell. 1979. Quantitative and qualitative differences in gypsy moth (Lepidoptera: Lymantriidae) nuclear polyhedrosis virus produced in different-aged larvae. Journal of Economic Entomology 79:1174-1177.
79. Shepherd, R. F., I. S. Otvos, R. J. Chorney, and J. C. Cunningham. 1984. Pest-management of Douglas-fir tussock moth (Lepidoptera: Lymantriidae): prevention of an outbreak through early treatment with a nuclear polyhedrosis-virus by ground and aerial applications. Canadian Entomologist 116:1533-1542.
80. Sorrell, I., A. White, A. B. Pedersen, R. S. Hails, and M. Boots. 2009. The evolution of covert, silent infection as a parasite strategy. Proceedings of the Royal Society B: Biological Sciences 276:2217-2226.
81. Sun, X., X. Sun, W. Van Der Werf, J. Vlak, and Z. Hu. 2004. Field inactivation of wild-type and genetically modified Helicoverpa armigera single nucleocapsid nucleopolyhedrovirus in cotton. Biocontrol Science and Technology 14:185-192.
82. Tanada, Y., and E. Omi. 1974. Persistence of insect viruses in field populations of alfalfa insects. Journal of Invertebrate Pathology 23:360-365.
83. Thieme, H. 2003. Mathematics in population biology. Princeton University Press, Princeton, NJ.
84. Thompson, C., D. Scott, and B. Wickman. 1981. Long-term persistence of the nuclear polyhedrosis virus of the Douglas-fir tussock moth, Orgyia pseudostugata (Lepidoptera, Lymantriidae) in forest soil. Environmental Entomology 10:254-255.
85. Thorpe, K. W., S. P. Cook, R. E. Webb, J. D. Podgwaite, and R. C. Reardon. 1999. Aerial application of the viral enhancer blankophor BBH with reduced rates of gypsy moth (Lepidoptera: Lymantriidae) nucleopolyhedrovirus. Biological Control 16:209-216.
86. Vilaplana, L., K. Wilson, E. M. Redman, and J. S. Cory. 2010. Pathogen persistence in migratory insects: high levels of verticallytransmitted virus infection in field populations of the African armyworm. Evolutionary Ecology 24:147-160.
87. Webb, R., R. Peiffer, R. Fuester, M. Valenti, K. Thorpe, G. White, and M. Shapiro. 1999. Effects of blankophor BBH, a virusenhancing adjuvant, on mortality of gypsy moth (Lepidoptera: Lymantriidae). Journal of Entomological Science 34:391-403.
88. Webb, R., M. Shapiro, K. Thorpe, R. Peiffer, R. Fuester, M. Valenti, G. White, and J. Podgwaite. 2001. Potentiation by a granulosis virus of Gypchek, the gypsy moth (Lepidoptera: Lymantriidae) nuclear polyhedrosis virus product. Journal of Entomological Science 36:169-176.
89. Woods, S. A., and J. S. Elkinton. 1987. Bimodal patterns of mortality from nuclear polyhedrosis virus in gypsy moth (Lymantria dispar) populations. Journal of Invertebrate Pathology 50:151-157.
90. Woods, S., J. Elkinton, and J. Podgwaite. 1989. Acquisition of nuclear polyhedrosis virus from tree stems by newly emerged gypsy-moth (Lepidoptera, Lymantriidae) larvae. Environmental Entomology 18:298-301.
91. Woods, S. A., J. S. Elkinton, and K. D. Murray. 1991. Transmission dynamics of a nuclear polyhedrosis-virus and predicting mortality in gypsy-moth (Lepidoptera, Lymnatriidae) populations. Journal of Economic Entomology 84:423-430.
92. Young, S., W. Yearian, and K. Kim. 1977. Effect of dew from cotton and soybean foliage on activity of Heliothis nuclear polyhedrosis virus. Journal of Invertebrate Pathology 29:105-111.
93. Zhou, M., X. Sun, X. Sun, J. Vlak, Z. Hu, and W. Van Der Werf. 2005. Horizontal and vertical transmission of wild-type and recombinant Helicoverpa armigera single-nucleocapsid nucleopolyhedrovirus. Journal of Invertebrate Pathology 89:165-175.