Invasive Species Impacting Native Disease Dynamics: A La Crosse virus case study M. Camille Harris DVM, MS, PhD Wildlife Disease Coordinator, U.S. Geological Survey Chair, Animal Pathogens Subcommittee, Federal Interagency Committee on Invasive Terrestrial Animals and Pathogens (ITAP) April 1, 2016 Zika isolated from at least 16 mosquito species “To assume that the main vector is Ae. aegypti in areas in which other mosquito species coexist is naive, and could be catastrophic if other species are found to have important roles in Zika virus transmission.” Constância F J Ayres Ayres, C.F., 2016. Identification of Zika virus vectors and implications for control. Lancet Infect Dis, 16: 278-279. Slide from Monath, T.P. 2016. Virus Reservoirs and Vectors. Research Priorities to Inform Public Health and Medical Practice for Domestic Zika Virus: A Workshop. National Academies of Sciences. Washington, DC. http://diseasemaps.usgs.gov/mapviewer/ USGS Ecosystems Overview Invasive Species & Disease La Crosse virus (LACV) • Family Bunyaviridae • Genus Orthobunyavirus • California encephalitis virus • Negative-sense single-stranded circular RNA virus Aedes triseriatus Borucki et al. 2002 La Crosse Virus & Forest Disturbance • Temperate forest mosquito community • LACV vectors • LACV vertebrate hosts • LACV prevalence • Mosquito LACV nucleic acid detection • Chipmunk LACV seroprevalence Southern Appalachian Silviculture and Biodiversity Project (SASAB) DISTURBANCE STAND AGE SW CCUT FCON Study Sites & Treatments BB3 BB1 BB2 NC Does forest disturbance influence the mosquito community? LACV Vectors • Cx. pipiens • Thompson et al. 1972 • Ae. canadensis • Berry et al. 1986 • Nasci et al. 2000 Ae. triseriatus Ae. japonicus Ae. albopictus Cx. pipiens/restuans Ae. canadensis Ae. vexans • Ae. vexans • Berry et al. 1983 Abundance of Primary LACV Vector and Recent Invasive Decline With Disturbance F3,380=28.1, p<0.0001 Ae. triseriatus F3,380=20.1, p<0.0001 Ae. japonicus Harris, MC. 2014. Forest Disturbance, Mosquito Vector Ecology and La Crosse Virus Dynamics in Southwestern Virginia An established invasive and floodwater mosquito increase in abundance with disturbance F3,380=3.5, p= 0.016 F3,380=6.2, p=0.0004 Ae. albopictus Ae. canadensis Harris, MC. 2014. Forest Disturbance, Mosquito Vector Ecology and La Crosse Virus Dynamics in Southwestern Virginia Culex spp. have no clear treatment preference Ae. vexans abundance was greatest on the CCUT F3,380=4.5, p= 0.0042 F3,380=3.2, p= 0.022 Ae. vexans Cx. pipiens/restuans Harris, MC. 2014. Forest Disturbance, Mosquito Vector Ecology and La Crosse Virus Dynamics in Southwestern Virginia Does forest disturbance influence LACV vector abundance? • Yes but in different ways: • • • • Ae. triseriatus and Ae. japonicus declined with disturbance Ae. albopictus and Ae. canadensis increased with disturbance Ae. vexans most abundant on the clearcut Cx. pipiens/restuans – no clear treatment preference La Crosse Virus & Forest Disturbance • Temperate forest mosquito community • LACV vectors • LACV vertebrate hosts • LACV prevalence • Mosquito LACV nucleic acid detection • Chipmunk LACV seroprevalence Does forest disturbance influence LACV detection in mosquito vectors? Most Mosquito LACV Detections on FCON 6 LACV Detected in 6 of 1,595 Vector Pools χ2=9.7, d.f.=3, p=0.02 5 4 3 2 1 0 CCON FCON CCUT SW Treatment Harris, MC. 2014. Forest Disturbance, Mosquito Vector Ecology and La Crosse Virus Dynamics in Southwestern Virginia LACV Detected in Accessory Vectors Only Ae. japonicus Cx. pipiens/restuans Ae. vexans Ae. triseriatus 3 LACV+ Pools 452 2 LACV+ Pools 375 1 LACV+ Pool 65 0 LACV+ Pools 590 Harris, MC. 2014. Forest Disturbance, Mosquito Vector Ecology and La Crosse Virus Dynamics in Southwestern Virginia Invasive Mosquitoes and LACV Photo Credit: CDC Public Health Image Library Invasive Mosquitoes and LACV • Vector Competence & TOT • Hughes et al. 2006 • Field LACV Detections & Isolations • Gerhardt et al. 2001 • Lambert et al. 2010 • Westby et al. 2011; 2015 Invasive Mosquitoes and LACV • Vector Competence • Sardelis et al. 2002 • Field LACV detections & isolations • Harris et al. 2015 • Detection in eggs • Westby et al. 2015 Photo Credit: CDC Public Health Image Library Harris et al. 2015. Detection and isolation of La Crosse virus in field-collected Aedes japonicus japonicus (Diptera: Culicidae) in the Appalachian Region, USA. Emerging Infectious Diseases. 21(4): http://dx.doi.org/10.3201/eid2104.140734 Harris et al. 2015. Detection and isolation of La Crosse virus in field-collected Aedes japonicus japonicus (Diptera: Culicidae) in the Appalachian Region, USA. Emerging Infectious Diseases. 21(4): http://dx.doi.org/10.3201/eid2104.140734 Harris et al. 2015. Detection and isolation of La Crosse virus in field-collected Aedes japonicus japonicus (Diptera: Culicidae) in the Appalachian Region, USA. Emerging Infectious Diseases. 21(4): http://dx.doi.org/10.3201/eid2104.140734 Harris et al. 2015. La Crosse virus field detection and vector competence of Culex mosquitoes. American Journal of Tropical Medicine & Hygiene. 93(3): 461-467. doi:10.4269/ajtmh.14-0128 LACV & Culex Mosquitoes • Both Cx. restuans and Cx. pipiens were susceptible to infection • Based on salivary expectorate, their ability to transmit LACV was poor in comparison to Ae. triseriatus • Nutritionally-stressed Cx. restuans larvae were significantly more likely to disseminate and transmit LACV Cx. pipiens/restuans Does forest disturbance influence LACV detection in mosquito vectors? • Most mosquito LACV detections were on undisturbed treatments • All LACV detections were in accessory vectors Summary • Mosquito vector populations were affected by forest disturbance in different ways • The primary LACV vector declined with disturbance • Mosquito LACV detection declined with disturbance • LACV was only detected in accessory vectors LACV Risk and Forest Disturbance • Ae. triseriatus abundance and mosquito LACV detections were greatest in undisturbed forest • Suspect greatest LACV vertical transmission • Greatest risk to humans • Complicated by multiple vectors • Other vertical transmitters • Link between mosquito community ecology and vector-borne disease dynamics needs to be explored Acknowledgements • Dana Hawley, Sally Paulson, Francois Elvinger, XJ Meng, Robert Jones • Co-Authors: Bryan L. Brown, Bryan Jackson, Dorian Jackson, Fan Yang, Steven Zink, Laura Kramer, Eric Dotseth, Paul Marek • SASAB Researchers (esp. Travis Belote, Carola Haas), Jesse Overcash (USFS) • Lab: Laila Kirkpatrick, Jennifer Miller, Kevin Myles, Noah Thrope, Kylie Perkins, Lindsey McAlexander, Genevieve Dudzinsky, Courtney Scarborough, Bryan Tims, Andrew Luna, Dee Petit, Sean Kelly, Alexander Ciota • Field: Nate Lambert, Allen Patton, RJ Wilding, Jake Bova, Bonnie Fairbanks, Cari Lynn Squibb • CDC: Amy Lambert, Jason Velez, Olga Kosoy, Marvin Godsey, Robert Lanciotti, Roger Nasci • VT: Jack Cranford, Bryan Jackson, Nancy Troyano, Jake Bova, Fan Yang, James Adelman, Cassandra Nunez, Sahnzi Moyers, Ariel Leon, Laura Schoenle Thomas, Michelle Jusino, Vicki Garci, Olya Milenkaya Thank you!
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