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EcoHealth

, Volume 9, Issue 2, pp 217–228 | Cite as

Impacts of Climate, Land Use, and Biological Invasion on the Ecology of Immature Aedes Mosquitoes: Implications for La Crosse Emergence

  • Paul T. LeisnhamEmail author
  • Steven A. Juliano
Review

Abstract

Arthropod-borne viruses (arboviruses) cause many diseases worldwide and their transmission is likely to change with land use and climate changes. La Crosse virus (LACV) is historically transmitted by the native mosquito Aedes triseriatus (Say) in the upper Midwestern US, but the invasive congeners Aedes albopictus (Skuse) and A. japonicus (Theobald), which co-occur with A. triseriatus in water-holding containers, may be important accessory vectors in the Appalachian region where La Crosse encephalitis is an emerging disease. This review focuses on evidence for how climate, land use, and biological invasions may have direct abiotic and indirect community-level impacts on immature developmental stages (eggs and larvae) of Aedes mosquitoes. Because vector-borne diseases usually vary in space and time and are related to the ecology of the vector species, we propose that the ecology of its mosquito vectors, particularly at their immature stages, has played an important role in the emergence of La Crosse encephalitis in the Appalachian region and represents a model for investigating the effects of environmental changes on other vector-borne diseases. We summarize the health effects of LACV and associated socioeconomic costs that make it the most important native mosquito-borne disease in the US. We review of the transmission of LACV, and present evidence for the impacts of climate, land use, and biological invasions on Aedes mosquito communities. Finally, we discuss important questions about the ecology of LACV mosquito vectors that may improve our understanding of the impacts of environmental changes on LACV and other arboviruses.

Keywords

Aedes albopictus Aedes triseriatus Culicidae disease ecology disease vectors interspecific competition predation invasion La Crosse encephalitis global change biology 

Notes

Acknowledgments

Development of this review was supported by a grant from the Maryland Agricultural Research Station to PTL, and by grants from NIAID (R01 AI-44793, ISU subaward, and R15 AI075306-01) to SAJ.

References

  1. Aliabadi BW, Juliano SA (2002) Escape from gregarine parasites affects the competitive interactions of an invasive mosquito. Biological Invasions 4:283-297PubMedCrossRefGoogle Scholar
  2. Andreadis TG, Anderson JF, Vossbrinck CR, Main AJ (2004) Epidemiology of West Nile virus in Connecticut: A five-year analysis of mosquito data 1999–2003. Vector Borne Zoonotic Diseases 4:360-378CrossRefGoogle Scholar
  3. Andreadis TG (2007) Microsporidian parasites of mosquitoes. In: Biorational Control of Mosquitoes, Floore TG (editor), American Mosquito Control Association, Supplement to the Journal of the Mosquito Control Association, vol 23, pp 3–29Google Scholar
  4. Andreadis TG (2009) Failure of Aedes albopictus to overwinter following introduction and seasonal establishment at a tire recycling plant in the northeastern USA. Journal of the American Mosquito Control Association 25:25-31PubMedCrossRefGoogle Scholar
  5. Andreadis TG, Wolfe RJ (2010) Evidence for reduction of native mosquitoes with increased expansion of invasive Ochlerotatus japonicus japonicus (Diptera: Culicidae) in the northeastern United States. Journal of Medical Entomology 47:43-52.PubMedCrossRefGoogle Scholar
  6. Andreadis TG, Anderson JF, Munstermann LE, Wolfe RJ, Florin DA (2001) Discovery, distribution, and abundance of the newly introduced mosquito Ochlerotatus japonicus (Diptera: Culicidae) in Connecticut, USA. Journal of Medical Entomology 38:774-779PubMedCrossRefGoogle Scholar
  7. Armbruster P, Conn JE (2006) Geographic variation of larval growth in North American Aedes albopictus (Diptera: Culicidae). Annals of the Entomological Society of America 99:1234-1243CrossRefGoogle Scholar
  8. Armistead JS, Arias JR, Nishimura N, Lounibos LP (2008) Interspecific larval competition between Aedes albopictus and Aedes japonicus (Diptera: Culicidae) in northern Virginia. Journal of Medical Entomology 45:629–637Google Scholar
  9. Barker CM, Brewster CC, Paulson SL (2003a) Spatiotemporal oviposition and habitat preferences of Aedes triseriatus and Aedes albopictus in an emerging focus of La Crosse virus. Journal of the American Mosquito Control Association 19:382-391PubMedGoogle Scholar
  10. Barker CM, Paulson SL, Cantrell S, Davis BS (2003b) Habitat preferences and phenology of Aedes triseriatus and Aedes albopictus (Diptera: Culicidae) in southwestern Virginia. Journal of Medical Entomology 40:403-410PubMedCrossRefGoogle Scholar
  11. Barrett R, Kuzawa CW, McDade T, Armelagos GJ (1998) Emerging and re-emerging infectious diseases: The third epidemiologic transition. Annual Review of Anthropology 27:247-271CrossRefGoogle Scholar
  12. Becnel JJ, White SE (2007) Mosquito pathogenic viruses: the last 20 years. In: Biorational Control of Mosquitoes, Floore TG (editor), American Mosquito Control Association, Supplement to the Journal of the Mosquito Control Association, vol 23, pp 3–29Google Scholar
  13. Bevins SN (2007a) Establishment and abundance of a recently introduced mosquito species Ochlerotatus japonicus (Diptera : Culicidae) in the Southern Appalachians, USA. Journal of Medical Entomology 44:945-952PubMedCrossRefGoogle Scholar
  14. Bevins SN (2007b) Timing of resource input and larval competition between invasive and native container-inhabiting mosquitoes (Diptera: Culicidae). Journal Vector Ecology 32:252-262PubMedCrossRefGoogle Scholar
  15. Blackmore MS, Scoles GA, Craig GB (1995) Parasitism of Aedes aegypti and Ae. albopictus (Diptera: Culicidae) by Ascogregarina spp. (Apicomplexa: Lecudinidae) in Florida. Journal of Medical Entomology 32:847-852PubMedGoogle Scholar
  16. Bradshaw WE and Holzapfel CH (1983) Predator-mediated, non-equilibrium coexistence of tree-hole mosquitoes in southeastern North America. Oecologia 57:239-256CrossRefGoogle Scholar
  17. Bradshaw WE, Holzapfel CH (1985) The distribution and abundance of treehole mosquitoes in North America: Perspectives from north Florida. In: Ecology of Mosquitoes: Proceedings of a Workshop Florida Medical Entomology Laboratory, Lounibos LP, Rey JR, Frank JH (editors), Vero Beach, FL, pp 3-23Google Scholar
  18. Calisher CH (1994) Medically important arboviruses of the United States and Canada. Clinical Microbiology Reviews 7:89-116PubMedGoogle Scholar
  19. Carpenter SR (1983) Resource limitation of larval treehole mosquitoes subsisting on beech detritus. Ecology 64:219-223CrossRefGoogle Scholar
  20. CDC (2011) Arboviral encephalitis cases reported in humans, by type, United States, 1964–2010. Centers for Disease Control and Prevention. http://www.cdc.gov/ncidod/dvbid/arbor/arbocase.htm. Accessed 1 June, 2011
  21. Cully JF, Street TG, Heard PB (1992) Transmission of La Crosse virus by four strains of Aedes albopictus to and from the eastern chipmunk (Tamias striatus). Journal of American Mosquito Control Association 8:237-240Google Scholar
  22. Darsie RF, Ward RA (2005) Identification and Geographical Distribution of the Mosquitoes of North America, North of Mexico. University Press of Florida, Gainesville, FLGoogle Scholar
  23. Daszak P, Cunningham AA, Hyatt AD (2000) Wildlife ecology - Emerging infectious diseases of wildlife - Threats to biodiversity and human health. Science 287:443-449PubMedCrossRefGoogle Scholar
  24. Debboun M, Green TJ, Rueda LM, Hall RD (2005) Relative abundance of tree hole-breeding mosquitoes in Boone County, Missouri, USA, with emphasis on the vector potential of Aedes triseriatus for canine heartworm, Dirofilaria immitis (Spirurida: Filariidae). Journal of American Mosquito Control Association 21:274-278CrossRefGoogle Scholar
  25. Edgerly JS, Willey MS, Livdahl TP (1993) The community ecology of Aedes egg hatching: Implications for a mosquito invasion Ecological Entomology 18:123-128CrossRefGoogle Scholar
  26. Edgerly JS, Willey MS, Livdahl TP (1999) Intraguild predation among larval treehole mosquitoes, Aedes albopictus, Ae. aegypti, Ae. triseriatus (Diptera: Culicidae), in laboratory microcosms. Journal of Medical Entomology 36:394-399PubMedGoogle Scholar
  27. Estrada-Franco JG, Craig Jr GB (1995) Biology, Disease Relationships, and Control of Aedes albopictus. Pan American Health Organization, Technical Publication 42. PAHO, Washington, DCGoogle Scholar
  28. Fish D, Carpenter SR (1982) Leaf litter and larval mosquito dynamics in tree-hole ecosystems. Ecology 63:283-288CrossRefGoogle Scholar
  29. Frankino WA, Juliano SA (1999) Costs of reproduction and geographic variation in the reproductive tactics of the mosquito Aedes triseriatus Oecologia 120:59-68CrossRefGoogle Scholar
  30. Gerhardt RR, Gottfried KL, Apperson CS, Davis BS, Erwin PC et al. (2001) The first isolation of La Crosse virus from naturally occurring infected Aedes albopictus. Emerging Infectious Diseases 7:807-811PubMedGoogle Scholar
  31. Gray EW, Harrison BA, Womack ML, Kerce J, Neely CJ et al. (2005) Ochlerotatus japonicus japonicus (Theobald) in Georgia and North Carolina. Journal of the American Mosquito Control Association 21: 144-146.PubMedCrossRefGoogle Scholar
  32. Grim DC, Jackson BT, Paulson SL (2007) Abundance and bionomics of Ochlerotatus J. japonicus in two counties in southwestern Virginia. Journal of the American Mosquito Control Association 23:259-263PubMedCrossRefGoogle Scholar
  33. Grimstad PR (1988) California group virus disease. In: The Arboviruses: Epidemiology and Ecology, Vol. II, Monath TP (editor), Boca Raton, FL: CRC Press, pp 99-136Google Scholar
  34. Grimstad PR, Craig GB Jr, Ross QE, Yuill TM (1977) Aedes triseriatus and La Crosse virus: geographic variation in vector susceptibility and ability to transmit. American Journal of Tropical Medicine and Hygiene 26:990-6.PubMedGoogle Scholar
  35. Grimstad PR, Haramis LD (1984) Aedes triseriatus (Diptera: Culicidae) and La Crosse virus. III. Enhances oral transmission by nutrition-deprived mosquitoes. Journal of Medical Entomology 21:249-256PubMedGoogle Scholar
  36. Grimstad PR, Kobayashi JF, Zhang M, Craig Jr GB (1989) Recently introduced Aedes albopictus in the United States: Potential vector of La Crosse virus (Bunyaviridae: California serogroup). Journal of American Mosquito Control Association 5:422-427Google Scholar
  37. Grimstad PR, Walker ED (1991) Aedes triseriatus (Diptera: Culicidae) and La Crosse virus. IV. Nutritional deprivation of larvae affects the adult barriers to infection and transmission. Journal of Medical Entomology 28:378-386PubMedGoogle Scholar
  38. Griswold MW, Lounibos LP (2005a) Competitive outcomes of aquatic container Diptera depends on predation and resource levels. Annals of the Entomological Society of America 98:673-681PubMedCrossRefGoogle Scholar
  39. Haddow AD, Moulton JK, Gerhardt RR, McCuiston LJ. Jones CJ (2009) Description of the egg of Ochlerotatus japonicus japonicus (Diptera: Culicidae) using variable pressure scanning electron microscopy. Journal of Medical Entomology 46: 9-14PubMedCrossRefGoogle Scholar
  40. Haddow AD, Odai A (2009) The incidence risk, clustering, and clinical presentation of La Crosse virus infections in the eastern United States, 2003-2007. PLoS ONE 4: e6145PubMedCrossRefGoogle Scholar
  41. Hanson SM, Craig Jr GB (1994) Relationship between cold hardiness and supercooling point in Aedes albopictus eggs. Journal of the American Mosquito Control Association 11:35-38Google Scholar
  42. Hanson SM, Craig Jr GB (1995) Aedes albopictus (Diptera: Culicidae) eggs: Field survivorship during northern Indiana winters. Journal of Medical Entomology 32:599-604PubMedGoogle Scholar
  43. Hawley WA, Pumpuni CB, Brady RH, Craig Jr GB (1989) Overwintering survival of Aedes albopictus (Diptera, Culicidae) eggs in Indiana. Journal of Medical Entomology 26:122-129PubMedGoogle Scholar
  44. Hughes MT, Gonzalez JA, Reagan KL, Blair CD, Beaty BJ (2006) Comparative potential of Aedes triseriatus, Aedes albopictus, and Aedes aegypti (Diptera: Culicidae) to transovarially transmit La Crosse virus. Journal of Medical Entomology 43:757-761PubMedCrossRefGoogle Scholar
  45. Hughes TH, Irwin PM, Kaufman A, Sage H, Pagac BB Jr, Paskewitz SM. (2008) First records of Aedes japonicus japonicus in Wisconsin. Journal of the American Mosquito Control Association. 24:583-4.PubMedCrossRefGoogle Scholar
  46. IPCC (2007) Climate Change 2007: Synthesis Report. IPCC’s Fourth Assessment Report. Intergovernmental Panel on Climate Change. http://www.ipcc.ch/publications_and_data/publications_and_data.htm. Accessed 17 July 2011
  47. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL et al. (2008) Global trends in emerging infectious diseases. Nature 451:990-994PubMedCrossRefGoogle Scholar
  48. Jones TF, Craig AS, Nasci RS, Patterson LER, Erwin PC, Gerhardt RR et al. (1999) Newly recognized focus of La Crosse encephalitis in Tennessee. Clinical Infectious Diseases 28:93-97PubMedCrossRefGoogle Scholar
  49. Joy JE, Sullivan SN (2005) Occurrence of tire inhabiting mosquito larvae in different geographic regions of West Virginia. Journal of the American Mosquito Control Association 21:380-386PubMedCrossRefGoogle Scholar
  50. Juliano SA (1996) Geographic variation in Aedes triseriatus (Diptera: Culicidae): Temperature-dependent effects of a predator on survival of larvae. Environmental Entomology 25:624-631Google Scholar
  51. Juliano SA (2009) Species interactions among mosquitoes: Context dependence across habitat gradients. Annual Review of Entomology 54:37-56PubMedCrossRefGoogle Scholar
  52. Juliano SA, Lounibos LP (2005) Ecology of invasive mosquitoes: effects on resident species and on human health. Ecology Letters 8:558-574PubMedCrossRefGoogle Scholar
  53. Juliano SA, Lounibos LP, Nishimura N, Greene K (2010) Your worst enemy could be your best friend: Predator contributions to invasion resistance and persistence of natives. Oecologia. 162:709-718PubMedCrossRefGoogle Scholar
  54. Kappus KD, Calisher CH, Baron RC, Davenport J, Francy DB, et al. (1982) La Crosse virus infection and disease in western North Carolina. American Journal of Tropical Medicine and Hygiene 31:556–560.PubMedGoogle Scholar
  55. Kaufman MG, Bland SN, Worthen ME, Walker ED, Klug MJ (2001) Bacterial and fungal biomass responses to feeding by larval Aedes triseriatus (Diptera: Culicidae). Journal of Medical Entomology 38:711-719PubMedCrossRefGoogle Scholar
  56. Kesavaraju B, Juliano SA (2004) Differential behavioral responses to water-borne cues to predation in two container dwelling mosquitoes. Annals of the Entomological Society of America 97:194-201PubMedCrossRefGoogle Scholar
  57. Kesavaraju B, Damal K, Juliano SA (2008) Do natural container habitats impede invader dominance? Predator-mediated coexistence of invasive and native container-dwelling mosquitoes. Oecologia 155:631–639PubMedCrossRefGoogle Scholar
  58. Kesavaraju B, Alto BW, Lounibos LP, Juliano SA (2007) Behavioural responses of larval container mosquitoes to a size-selective predator. Ecological Entomology, 32, 262–272.PubMedCrossRefGoogle Scholar
  59. Kesavaraju B, Khan DF, Gaugler R (2011) Behavioral differences of invasive container-dwelling mosquitoes to a native predator. Journal of Medical Entomology 48: 526-532.PubMedCrossRefGoogle Scholar
  60. Kitching RL (2000) Food Webs and Container Habitats: The Natural History and Ecology of Phytotelmata, New York: Cambridge University PressCrossRefGoogle Scholar
  61. Kitching RL (2001) Food webs in phytotelmata: “Bottomup” and “top-down” explanations for community structure. Annual Review of Entomology 46:729-760PubMedCrossRefGoogle Scholar
  62. Kling LJ, Juliano SA, Yee DA (2007) Larval mosquito communities in discarded vehicle tires in a forested and unforested site: Detritus type, amount, and water nutrient differences. Journal of Vector Ecology 32:207-217PubMedCrossRefGoogle Scholar
  63. Lambert AJ, Blair CD, D’Anton M, Ewing W, Harborth M, Seiferth R et al. (2010) La Crosse Virus in Aedes albopictus Mosquitoes, Texas, USA, 2009. Emerging Infectious Diseases 16:856-858PubMedGoogle Scholar
  64. Leisnham P, Towler L, Juliano SA (2011) Geographic variation of photoperiodic diapause but not adult survival or reproduction of the invasive mosquito Aedes albopictus (Diptera: Culicidae) in North America. Annals of the Entomological Society of America 104:1309-1318PubMedCrossRefGoogle Scholar
  65. Leisnham PT, Lounibos LP, O’Meara GF, Juliano SA (2009) Interpopulation divergence in competitive interactions of the mosquito Aedes albopictus. Ecology 90:2405-2413PubMedCrossRefGoogle Scholar
  66. Livdahl TP, Willey MS (1991) Prospects for an invasion: competition between Aedes albopictus and native Aedes triseriatus. Science 253:189-191PubMedCrossRefGoogle Scholar
  67. Lounibos LP, Escher RL, Lourenco-de-Oliveria R (2003a) Asymmetric evolution of photoperiodic diapause in temperate and tropical invasive populations of Aedes albopictus (Diptera: Culicidae). Annals of the Entomological Society of America 96:512-518CrossRefGoogle Scholar
  68. Lounibos LP, O’Meara GF, Nishimura N, Escher RL (2003b). Interactions with native mosquito larvae regulate the production of Aedes albopictus from bromeliads in Florida. Ecological Entomology 28:551–558CrossRefGoogle Scholar
  69. Lounibos LP, O’Meara GF, Escher RL, Nishimura N, Cutwa M et al. (2001) Testing predictions of displacement of native Aedes by the invasive Asian Tiger Mosquito Aedes albopictus in Florida, USA. Biological Invasions 3:151-166CrossRefGoogle Scholar
  70. McGaw MM., Chandler LJ, Wasieloski LP, Blair CD, Beaty BJ (1998) Effect of La Crosse virus infection on overwintering of Aedes triseriatus. American Journal of Tropical Medicine and Hygiene 58:168-175PubMedGoogle Scholar
  71. McIntyre NE (2000) Ecology of urban arthropods: A review and a call to action. Annals of the Entomological Society of America 93:825-835CrossRefGoogle Scholar
  72. Mercer DR, Anderson JR (1994) Tannins in treehole habitats and their effects on Aedes sierrensis (Diptera: Culicidae) production and parasitism by Lambornella clarki (Ciliophera: Tetrahymenidae). Journal of Medical Entomology 31:159-167PubMedGoogle Scholar
  73. Merritt RW, Dadd RH, Walker ED (1992) Feeding-behavior, natural food, and nutritional relationships of larval mosquitoes. Annual Review of Entomology 37:349-376PubMedCrossRefGoogle Scholar
  74. Morris JA, Lampman RL, Ballmes G, Funes J, Halvorsen J, Novak RJ. (2007) First record of Aedes japonicus japonicus in Illinois: defining its spatial distribution and associated mosquito species. Journal of the American Mosquito Control Association. 23:243-51.PubMedCrossRefGoogle Scholar
  75. Munstermann LE, Wesson DM (1990) First record of Ascogregarina taiwanensis (Apiomplexa: Lecudinidae) in North American Aedes albopictus. Journal of the American Mosquito Control Association 6:235-243PubMedGoogle Scholar
  76. Murrell EG, Juliano SA (2008) Detritus type alters the outcome of interspecific competition between Aedes aegypti and Aedes albopictus (Diptera: Culicidae). Journal of Medical Entomology 45:375–83Google Scholar
  77. Nasci RS, Moore CG, Biggerstaff BJ, Panella NA, Liu HQ, et al. (2000) La Crosse encephalitis virus habitat associations in Nicholas County, West Virginia. Journal of Medical Entomology 37:559-570PubMedCrossRefGoogle Scholar
  78. Nawrocki SJ, Hawley WA (1987) Estimation of the northern limits of distribution of Aedes albopictus in North America. Journal of the American Mosquito Control Association 3: 314-317PubMedGoogle Scholar
  79. Novak MG, Higley LG, Christianssen CA, Rowley W (1993) Evaluating larval competition between Aedes albopictus and A. triseriatus (Diptera: Culicidae) through replacement series experiments. Environmental Entomology 22:311-318Google Scholar
  80. Peterson RG, Cummins KW (1974) Leaf processing in a woodland stream. Freshwater Biology 4: 343–368CrossRefGoogle Scholar
  81. Reinert JF (2000) New classification for the composite genus Aedes (Diptera: Culicidae: Aedini), elevation of subgenus Ochlerotatus to generic rank, reclassification of the other subgenera, and notes on certain subgenera and species. Journal of the American Mosquito Control Association 16:175–188PubMedGoogle Scholar
  82. Reisen WK (2010) Landscape Epidemiology of Vector-Borne Diseases. Annual Review of Entomology 55:461-483PubMedCrossRefGoogle Scholar
  83. Reiskind MH, Greene KL, Lounibos LP (2009) Leaf species identity and combination affect performance and oviposition choice of two container mosquito species. Ecological Entomology 34:447-456.PubMedCrossRefGoogle Scholar
  84. Rust RS, Thompson WH, Matthews CG, Beaty BJ, Chun RWM (1999) La Crosse and other forms of California encephalitis. Journal of Child Neurology 14:1-14PubMedCrossRefGoogle Scholar
  85. Sardelis MR, Turell MJ, Andre RG (2002) Laboratory transmission of La Crosse virus by Ochlerotatus j. japonicus (Diptera: Culicidae). Journal of Medical Entomology 39: 635-639PubMedCrossRefGoogle Scholar
  86. Shroyer DA and Craig Jr GB (1983) Egg diapause in Aedes triseriatus (Diptera, Culicidae): geographic variation in photoperiodic response and factors influencing diapause termination. Journal of Medical Entomology 20:601-607PubMedGoogle Scholar
  87. Sokol DK, Kleiman MB, Garg BP (2001) La Crosse viral encephalitis mimics herpes simplex viral encephalitis. Pediatric Neurology 25:413-415PubMedCrossRefGoogle Scholar
  88. Sota T (1993) Performance of Aedes albopictus and A. riversi larvae (Diptera: Culicidae) in waters that contain tannic acid and decaying leaves: is the treehole species better adapted to treehole water? Annals of Entomological Society of America 86:450-457Google Scholar
  89. Strand M, Herms DA, Ayres MP, Kubiske ME, Kaufman MG, Walker ED, et al. (1999) Effects of atmospheric CO2, light availability and tree species on the quality of leaf detritus as a resource for treehole mosquitoes. Oikos 84:277-283CrossRefGoogle Scholar
  90. Sudia WD, Newhouse VF, Calisher CH, Chamberlain RW (1971) California group arboviruses: Isolation from mosquitoes in North America. Mosquito News 31:576-600Google Scholar
  91. Sunahara T, Mogi M (2002) Priority effects of bamboo-stump mosquito larvae: influences of water exchange and leaf litter input. Ecological Entomology 27:346-354CrossRefGoogle Scholar
  92. Swanson J, Lancaster M, Anderson J, Crandell M, Haramis L, Grimstad P (2000) Overwintering and establishment of Aedes albopictus (Diptera: Culicidae) in an urban La Crosse virus enzootic site in Illinois. Journal of Medical Entomology 37:454-460PubMedCrossRefGoogle Scholar
  93. Szumlas DE, Apperson CS, Powell EF, Hartig P, Francy DB, Karabotsos N (1996) Relative abundance and species composition of mosquito populations (Diptera: Culicidae) in a La Crosse virus-endemic area in western North Carolina. Journal of Medical Entomology 33:598-607PubMedGoogle Scholar
  94. Teng HJ, Apperson CS (2000) Development and survival of immature Aedes albopictus and Aedes triseriatus (Diptera: Culicidae) in the laboratory: Effects of density, food, and competition on response to temperature. Journal of Medical Entomology 37:40-52PubMedCrossRefGoogle Scholar
  95. Tesh RB, Gubler DJ (1975) Laboratory studies of transovarial transmission of La Crosse and other arboviruses by Aedes albopictus and Culex fatigans. American Journal of Tropical Medicine and Hygiene 24:876-880PubMedGoogle Scholar
  96. Thielman A, Hunter FF (2006) Establishment of Ochlerotatus japonicus (Diptera: Culicidae) in Ontario, Canada. Journal of Medical Entomology 43:138–142Google Scholar
  97. Thompson WH, Evans AS (1965) California encephalitis virus studies in Wisconsin. American Journal of Epidemiology 81:230-244PubMedGoogle Scholar
  98. Thuiller W, Albert C, Araujo MB, Berry PM, Cabeza M, Guisan A, Hickler T, Midgely GF, Paterson J, Schurr FM, Sykes MT, Zimmermann NE (2008) Predicting global change impacts on plant species’ distributions: Future challenges. Perspectives in Plant Ecology Evolution and Systematics 9:137-152CrossRefGoogle Scholar
  99. Torres MI (1997) Impact of an outbreak of dengue fever: a case study from rural Puerto Rico. Human Organization 56:19-27Google Scholar
  100. Tsai TF (1991) Arboviral infections in the United States. Infectious Disease Clinics of North America 5:73-102PubMedGoogle Scholar
  101. Tseng M (2007) Ascogregarine parasites as possible biocontrol agents of mosquitoes. In: Biorational Control of Mosquitoes, Floore TG (editor), American Mosquito Control Association, Supplement to the Journal of the Mosquito Control Association, vol 23, pp 3–29Google Scholar
  102. Tuchman NC, Wahtera KA, Wetzel RG, Russo NM, Kilbane GM, Sasso LM, et al. (2003) Nutritional quality of leaf detritus altered by elevated atmospheric CO2: effects on development of mosquito larvae. Freshwater Biology 48:1432-1439CrossRefGoogle Scholar
  103. Utz JT, Apperson CS, MacCormack JN, Salyers M, Dietz EJ, McPherson JT (2003) Economic and social impacts of La Crosse encephalitis in western North Carolina. American Journal of Tropical Medicine and Hygiene 69:509-518PubMedGoogle Scholar
  104. Van Rhein SL, Flanary BE, Juliano SA (2000) Effects of habitat type and drying on Ascogregarina barretti (Eugregarinida: Lecudinidae) infection in Aedes triseritatus (Diptera: Culicidae). Journal of Medical Entomology 37: 950-956PubMedCrossRefGoogle Scholar
  105. Von Allmen SD, Lopez-Correa RH, Woodall JP, Morens DM, Chiriboga J, Caste-Velez A (1977) Epidemic dengue fever in Puerto Rico, 1977: a cost analysis. American Journal of Tropical Medicine and Hygiene 59:265-271Google Scholar
  106. Walker ED, Lawson DL, Merritt RW, Morgan WT, Klug MJ (1991) Nutrient dynamics, bacterial populations, and mosquito productivity in tree hole ecosystems and microcosms. Ecology 72:1529-1546CrossRefGoogle Scholar
  107. Watts DM, Morris CD, Wright RE, DeFoliart GR, Hanson RP (1972) Transmission of La Crosse virus (California encephalitis group) by the mosquito, Aedes triseriatus. Journal of Medical Entomology 9:125-127PubMedGoogle Scholar
  108. Watts DM, Pantuwatana S, DeFoliart GR, Yuill TM, Thompson WH (1973) Transovarial transmission of La Crosse virus (California encephalitis group) in the mosquito Aedes triseriatus. Science 182:1140-1143PubMedCrossRefGoogle Scholar
  109. Watts DM, Thompson WH, Yuill TM, DeFoliart GR, Hanson RP (1974) Overwintering of La Crosse virus in Aedes triseriatus. American Journal of Tropical Medicine and Hygiene 23:694-700PubMedGoogle Scholar
  110. Weaver SC, Reisen WK (2010) Present and future arboviral threats. Antiviral Research 85:328-345PubMedCrossRefGoogle Scholar
  111. Weiss RA, McMichael AJ (2004) Social and environmental risk factors in the emergence of infectious diseases. Nature Medicine 10:S70-S76PubMedCrossRefGoogle Scholar
  112. Westby K, Fritzen C, Huang J, Jaske E, Paulsen D, Jones C, Moncayo AC. (2011) La Crosse encephalitis in Eastern Tennessee: Evidence of invasive mosquito (Aedes albopictus and Ochlerotatus japonicus) involvement in the transmission of an indigenous disease. American Journal of Tropical Medicine and Hygiene 85(supplement): 374Google Scholar
  113. Wilcox BA, Colwell RR (2005) Emerging and reemerging infectious diseases: Biocomplexity as an interdisciplinary paradigm. Ecohealth 2:244-257CrossRefGoogle Scholar
  114. Woodring J, Chandler LJ, Oray CT, McGaw MM, Blair CD, Beaty BJ (1998) Short Report: Diapause, transovarial transmission, and filial infection rates in geographic strains of La Crosse virus-infected Aedes triseriatus. American Journal of Tropical Medicine and Hygiene 58:587-588PubMedGoogle Scholar
  115. Wright RE, DeFoliart GR (1970) Associations of Wisconsin mosquitoes and woodland vertebrate hosts. Annals of the Entomological Society of America 63:777-786PubMedGoogle Scholar
  116. Yee DA (2008) Tires as habitats for mosquitoes: A review of studies within the eastern United States. Journal of Medical Entomology 45:581-593PubMedCrossRefGoogle Scholar
  117. Yee DA, Juliano SA (2006) Consequences of detritus type in an aquatic microsystem: effects on water quality, micro-organisms and performance of the dominant consumer. Freshwater Biology 51:448-459PubMedCrossRefGoogle Scholar
  118. Yee DA, Kaufman MG, Juliano SA (2007) The significance of ratios of detritus types and microorganism productivity to competitive interactions between aquatic insect detritivores. Journal of Animal Ecology 76:1105-1115PubMedCrossRefGoogle Scholar
  119. Yasuoka J, Levins R (2007) Impacts of deforestation and agricultural development on anopheline ecology and malaria epidemiology. Journal of Tropical Medicine and Hygiene 76:450-460Google Scholar

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© International Association for Ecology and Health 2012

Authors and Affiliations

  1. 1.Department of Environmental Science and TechnologyUniversity of MarylandCollege ParkUSA
  2. 2.School of Biological Sciences, Behavior, Ecology, Evolution, and Systematics SectionIllinois State UniversityNormalUSA

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