EcoHealth

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Large-Scale Removal of Invasive Honeysuckle Decreases Mosquito and Avian Host Abundance

  • Allison M. Gardner
  • Ephantus J. Muturi
  • Leah D. Overmier
  • Brian F. Allan
Original Contribution

Abstract

Invasive species rank second only to habitat destruction as a threat to native biodiversity. One consequence of biological invasions is altered risk of exposure to infectious diseases in human and animal populations. The distribution and prevalence of mosquito-borne diseases depend on the complex interactions between the vector, the pathogen, and the human or wildlife reservoir host. These interactions are highly susceptible to disturbance by invasive species, including terrestrial plants. We conducted a 2-year field experiment using a Before–After/Control–Impact design to examine how removal of invasive Amur honeysuckle (Lonicera maackii) in a forest fragment embedded within a residential neighborhood affects the abundance of mosquitoes, including two of the most important vectors of West Nile virus, Culex pipiens and Cx. restuans. We also assessed any potential changes in avian communities and local microclimate associated with Amur honeysuckle removal. We found that (1) removal of Amur honeysuckle reduces the abundance of both vector and non-vector mosquito species that commonly feed on human hosts, (2) the abundance and composition of avian hosts is altered by honeysuckle removal, and (3) areas invaded with honeysuckle support local microclimates that are favorable to mosquito survival. Collectively, our investigations demonstrate the role of a highly invasive understory shrub in determining the abundance and distribution of mosquitoes and suggest potential mechanisms underlying this pattern. Our results also give rise to additional questions regarding the general impact of invasive plants on vector-borne diseases and the spatial scale at which removal of invasive plants may be utilized to effect disease control.

Keywords

Invasive plants Culex pipiens Culex restuans Lonicera maackii Conservation West Nile virus 

References

  1. Allan BF, Dutra HP, Goessling LS, Barnett K, Chase JM, Marquis RJ, Pang G, Storch GA, Thach RE, Orrock JL (2010) Invasive honeysuckle eradication reduces tick-borne disease risk by altering host dynamics. Proceedings of the National Academy of Sciences USA 107:18523-18527CrossRefGoogle Scholar
  2. Anderson DB (1936) Relative humidity or vapor pressure deficit. Ecology 17:277-282CrossRefGoogle Scholar
  3. Arthur MA, Bray SR, Kuchle CR, McEwan RW (2012) The influence of the invasive shrub, Lonicera maackii, on leaf decomposition and microbial community dynamics. Plant Ecology 213:1571-1582CrossRefGoogle Scholar
  4. Bara JJ, Montgomery A, Muturi EJ (2014) Sublethal effects of atrazine and glyphosate on life history traits of Aedes aegypti and Aedes albopictus (Diptera: Culicidae). Parasitology Research 113:2879-2886CrossRefPubMedGoogle Scholar
  5. Bibby CJ (2000) Bird census techniques, Philadelphia: ElsevierGoogle Scholar
  6. Bradley CA, Gibbs SEJ, Altizer S (2008) Urban land use predicts West Nile virus exposure in songbirds. Ecological Applications 18:1083-1092CrossRefPubMedGoogle Scholar
  7. Brown HE, Childs JE, Diuk-Wasser MA, Fish D (2008) Ecological factors associated with West Nile virus transmission, northeastern United States. Emerging Infectious Diseases 14:1539-1545CrossRefPubMedPubMedCentralGoogle Scholar
  8. Castellano SM, Gorchov DL (2013) White-tailed deer (Odocoileus virginianus) disperse seeds of the invasive shrub, Amur honeysuckle (Lonicera maackii). Natural Areas Journal 33:78-80CrossRefGoogle Scholar
  9. Chazdon RL (2008) Beyond deforestation: restoring forests and ecosystem services on degraded lands. Science 320:1458-1460CrossRefPubMedGoogle Scholar
  10. Ciota AT, Drummond CL, Ruby MA, Drobnack J, Ebel GD, Kramer LD (2012) Dispersal of Culex mosquitoes (Diptera: Culicidae) form a wastewater treatment facility. Journal of Medical Entomology 49:35-42CrossRefPubMedPubMedCentralGoogle Scholar
  11. Civitello DJ, Flory SL, Clay K (2008) Exotic grass invasion reduces survival of Amblyomma americanum and Dermacentor variabilis ticks (Acari: Ixodidae). Journal of Medical Entomology 45:867-872CrossRefPubMedGoogle Scholar
  12. Conley AK, Watling JI, Orrock JL (2011) Invasive plant alters ability to predict disease vector distribution. Ecological Applications 21:329-334CrossRefPubMedGoogle Scholar
  13. Darsie RF, Ward RA (1981) Identification and geographical distribution of the mosquitoes of North America, north of Mexico, Washington: Walter Reed Army Institute of ResearchGoogle Scholar
  14. Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife – threats to biodiversity and human health. BioScience 287:443-449Google Scholar
  15. Delatte H, Gimonneau G, Triboire A, Fontenille D (2009) Influence of temperature on immature development, survival, longevity, fecundity, and gonotrophic cycles of Aedes albopictus, vector of chikungunya and dengue in the Indian Ocean. Journal of Medical Entomology 46:33-41CrossRefPubMedGoogle Scholar
  16. Diuk-Wasser MA, Molaei G, Simpson JE, Folsom-O’Keefe CM, Armstrong PM, Andreadis TG. (2010) Avian communal roosts as amplification foci for West Nile virus in urban areas in northeastern United States. American Journal of Tropical Medicine and Hygiene 82:337-343CrossRefPubMedPubMedCentralGoogle Scholar
  17. Dorning M, Cipollini D (2006) Leaf and root extracts of the invasive shrub, Lonicera maackii, inhibit seed germination of three herbs with no autotoxic effects. Plant Ecology 184:287-296CrossRefGoogle Scholar
  18. Ehrenfeld JG, Kourtev P, Huang W (2001) Changes in soil functions following invasions of exotic understory plants in deciduous forests. Ecological Applications 11:1287-1300CrossRefGoogle Scholar
  19. Elias SP, Lubelczyk CB, Rand PW, Lacombe EH, Holman MS, Smith RP (2006) Deer browse resistant exotic-invasive understory: an indicator of elevated human risk of exposure to Ixodes scapularis (Acari: Ixodidae) in southern coastal Maine woodlands. Journal of Medical Entomology 43:1142-1152CrossRefPubMedGoogle Scholar
  20. Fiedler AK, Landis DA, Wratten SD (2008) Maximizing ecosystem services from conservation biological control: the role of habitat management. Biological Control 45:254-271CrossRefGoogle Scholar
  21. Fish D, Carpenter SR (1982) Leaf litter and larval mosquito dynamics in tree-hole ecosystems. Ecology 63:283-288CrossRefGoogle Scholar
  22. Foster WA (1995) Mosquito sugar feeding and reproductive energetics. Annual Review of Entomology 40:443-474CrossRefPubMedGoogle Scholar
  23. Gardner AM, Allan BF, Frisbie LA, Muturi EJ (2015) Asymmetric effects of native and exotic invasive shrubs on ecology of the West Nile Virus vector Culex pipiens (Diptera: Culicidae). Parasites and Vectors 16:329CrossRefGoogle Scholar
  24. Hamer GL, Kitron UD, Goldberg TL, Brawn JD, Loss SR, Ruiz MO, Hayes DB, Walker ED (2009) Host selection by Culex pipiens mosquitoes and West Nile virus amplification. American Journal of Tropical Medicine and Hygiene 80:268-278PubMedGoogle Scholar
  25. Hartman KM, McCarthy BC (2004) Restoration of a forest understory after the removal of an invasive shrub, Amur honeysuckle (Lonicera maackii). Restoration Ecology 12:154-165CrossRefGoogle Scholar
  26. Hellmann JJ, Byers JE, Bierwagen BG, Dukes JS (2008) Five potential consequences of climate change for invasive species. Conservation Biology 22:534-543CrossRefPubMedGoogle Scholar
  27. Hutchinson TF, Vankat JL (1997) Invasibility and effects of Amur honeysuckle in southwestern Ohio forests. Conservation Biology 11:1117-1124CrossRefGoogle Scholar
  28. Ingold JL, Craycraft MJ (1983) Avian frugivory on honeysuckle (Lonicera) in soutwestern Ohio in fall. Ohio Journal of Science 83:256-258Google Scholar
  29. Kitching RL (2001) Food webs in phytotelmata: “bottom-up” and “top-down” explanations for community structure. Annual Review of Entomology 46:729-760CrossRefPubMedGoogle Scholar
  30. Komar N, Langevin S, Hinten S, Nemeth N, Edwards E, Hettler D, Davis B, Bowen R, Bunning M (2003) Experimental infection of North American birds with the New York 1999 strain of West Nile virus. Emerging Infectious Diseases 9:311-322CrossRefPubMedPubMedCentralGoogle Scholar
  31. Loomis J, Kent P, Strange L, Fausch K, Covich A (2000) Measuring the total economic value of restoring ecosystem services in an impaired river basin: results from a contingent valuation survey. Ecological Economics 33:103-117CrossRefGoogle Scholar
  32. Loomis JD, Cameron GN (2014) Impact of the invasive shrub Amur honeysuckle (Lonicera maackii) on shrub-layer insects in a deciduous forest in the eastern United States. Biological Invasions 16:89-100CrossRefGoogle Scholar
  33. Luken JO, Thieret JW (1996) Amur honeysuckle, its fall from grace. BioScience 46:18-24CrossRefGoogle Scholar
  34. Mattos KJ, Orrock JL (2010) Behavioral consequences of plant invasion: an invasive plant alters rodent antipredator behavior. Behavioral Ecology 21:556-561CrossRefGoogle Scholar
  35. McCardle PW, Webb RE, Norden BB, Aldrich JR (2004) Evaluation of five trapping systems for the surveillance of gravid mosquitoes in Prince Georges County, Maryland. Journal of the American Mosquito Control Association 20:254-260PubMedGoogle Scholar
  36. McCusker CE, Ward MP, Brawn JD (2010) Seasonal responses of avian communities to invasive bush honeysuckles (Lonicera spp.). Biological Invasions 12:2459-2470CrossRefGoogle Scholar
  37. McNeish RE, Benbow ME, McEwan RW (2012) Riparian forest invasion by a terrestrial shrub (Lonicera maackii) impacts aquatic biota and organic matter processing in headwater streams. Biological Invasions 14:1881-1893CrossRefGoogle Scholar
  38. Miller KE, Gorchov DL (2004) The invasive shrub, Lonicera maackii, reduces growth and fecundity of perennial forest herbs. Oecologia 139:359-375CrossRefPubMedGoogle Scholar
  39. Molaei G, Andreadis TG, Armstrong PM, Anderson JF, Vossbrinck CR (2006) Host feeding patterns of Culex mosquitoes and West Nile virus transmission, northeastern United States. Emerging Infectious Diseases 12:468CrossRefPubMedPubMedCentralGoogle Scholar
  40. Muturi EJ, Gardner AM, Bara JJ (2015) Impact of an alien invasive shrub on ecology of native and alien invasive mosquito species (Diptera: Culicidae). Environmental Entomology 44:1308-1315CrossRefPubMedGoogle Scholar
  41. Pejchar L, Mooney HA (2009) Invasive species, ecosystem services and human well-being. Trends in Ecology and Evolution 24:497-504CrossRefPubMedGoogle Scholar
  42. Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecological Economics 52:273-288CrossRefGoogle Scholar
  43. Racelis AE, Davey RB, Goolsby JA, Pérez de León AA, Varner K, Duhaime R (2012) Facilitative ecological interactions between invasive species: Arundo donax stands as favorable habitat for cattle ticks (Acari: Ixodidae) along the U.S.-Mexico border. Journal of Medical Entomology 49:410-417CrossRefPubMedGoogle Scholar
  44. Reichard SH, White P (2001) Horticulture as a pathway of invasive plant introductions in the United States. BioScience 51:103-113CrossRefGoogle Scholar
  45. Schmidt KA, Whelan CJ (1999) Effects of exotic Lonicera and Rhamnus on songbird nest predation. Conservation Biology 13:1502-1506CrossRefGoogle Scholar
  46. Shewhart L, McEwan RW, Benbow ME (2014) Evidence for facilitation of Culex pipiens (Diptera: Culicidae) life history traits by the nonnative invasive shrub Amur honeysuckle (Lonicera maackii). Environmental Entomology 43:1584-1593CrossRefPubMedGoogle Scholar
  47. Smith EP (2002) BACI design. Encyclopedia of Environmetrics, New York: WileyGoogle Scholar
  48. Smokorowski KE, Randall RG (2017) Cautions on using the Before-After-Control-Impact design in environmental effects monitoring programs. FACETS 2:212-232CrossRefGoogle Scholar
  49. Turell MJ, O’Guinn ML, Dohm DJ, Jones JW (2001) Vector competence of North American mosquitoes (Diptera: Culicidae) for West Nile virus. Journal of Medical Entomology 38:130-134CrossRefPubMedGoogle Scholar
  50. 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
  51. White MA, Beurs D, Kirsten M, Didan K, Inouye DW, Richardson AD, Jensen OP, O’Keefe J, Zhang G, Nemani RR, Leeuwen V (2009) Intercomparison, interpretation, and assessment of spring phenology in North America estimated from remote sensing for 1982-2006. Global Change Biology 15:2335-2359CrossRefGoogle Scholar
  52. Wilcove DS, Rothstein D, Dubow J, Phillips A, Losos E (1998) Quantifying threats to imperiled species in the United States. BioScience 48:607-615CrossRefGoogle Scholar
  53. Williams SC, Ward JS, Worthley TE, Stafford KC (2009) Managing Japanese barberry (Ranunculales: Berberidaceae) infestations reduces blacklegged tick (Acari: Ixodidae) abundance and infection prevalence with Borrelia burgdorferi (Spirochaetales: Spirochaetaceae). Environmental Entomology 38:977-984CrossRefPubMedGoogle Scholar
  54. Williams SC, Ward JS (2010) Effects of Japanese barberry (Ranunculales: Berberidaceae) removal and resulting microclimatic changes on Ixodes scapularis (Acari: Ixodidae) abundances in Connecticut, USA. Environmental Entomology 39:1911-1921CrossRefPubMedGoogle Scholar

Copyright information

© EcoHealth Alliance 2017

Authors and Affiliations

  • Allison M. Gardner
    • 1
    • 2
  • Ephantus J. Muturi
    • 3
    • 4
  • Leah D. Overmier
    • 2
  • Brian F. Allan
    • 2
  1. 1.School of Biology and EcologyUniversity of MaineOronoUSA
  2. 2.Department of EntomologyUniversity of IllinoisUrbanaUSA
  3. 3.Illinois Natural History SurveyChampaignUSA
  4. 4.Crop Bioprotection Research UnitUSDA, ARSPeoriaUSA

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