Documenting Virginia s New Illegal Aliens Culex coronator and Culex nigripalpus Notes on recent expansions and US distributions

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Documenting Virginia s New Illegal Aliens Culex coronator and Culex nigripalpus Notes on recent expansions and US distributions Karen Akaratovic,

1 Documenting Virginia s New Illegal Aliens Culex coronator and Culex nigripalpus Notes on recent expansions and US distributions Karen Akaratovic, Jay Kiser, and Charles Abadam kakaratovic@suffolkva.us Suffolk Mosquito Control Suffolk, Virginia VMCA Annual Conference Portsmouth, VA January 25, 2018

Culex nigripalpus Bionomics Suffolk, Virginia collection

2 Contents Culex coronator Bionomics Suffolk, Virginia collection (2016) US distribution and recent expansions Culex nigripalpus Bionomics Suffolk, Virginia collection (2017) US distribution and recent expansions Future outlook

Culex coronator Neotropical Known range: Patagonia to southern US (no record in Chile) Previously thought to be complex of 5 species New data (2017)

3 Culex coronator Neotropical Known range: Patagonia to southern US (no record in Chile) Previously thought to be complex of 5 species New data (2017) suggests it is a single polymorphic species 1 Polymorphic = multiple phenotypes (forms) of same species Commons.wikimedia.org Example: sexual dimorphism

Culex coronator Habitat Larvae 2-8 Natural and

pools, rock pools, ditches Adults 3,9-11 Wooded

floodplains Corral/pasture areas Sand ridge,

gamosquito.org/resources/2008 meeting/moulis.

4 Culex coronator Habitat Larvae 2-8 Natural and artificial containers Woodland spring, flood pools, rock pools, ditches Adults 3,9-11 Wooded and cleared areas Campgrounds, cemeteries, floodplains Corral/pasture areas Sand ridge, cattail marsh, cypress swamp meeting/moulis.pdf o.org/resources/2008m eeting/moulis.pdf Goddard et al. 2006

5 Culex coronator Larval Morphology Harrison et al Siphon length 7-9 times width at base Distinctive crown of spines at apex of siphon

6 Culex coronator Adult Morphology Easily confused with Cx. tarsalis Hindtarsomeres banded across joints Proboscis- ventral median patch of pale scales (not a band) Palpus without pale scales Costal and subcostal veins all dark

7 Culex coronator Trapping Collected year-round where endemic Bioquip.com johnwhock.com Collected primarily late summer/fall for new discoveries Smith et al Smith Bioquip.com et al Most common trap types: CDC light & CDC gravid 3,4,9 Other trap types: UV-CDC, ABC light, ABC Mosquito Magnet X, Fay-Prince, Malaise, Hourly rotator, EVS Suffolk collection: BG-Sentinel 2 16

8 Culex coronator Hosts White-tailed deer Carolina chickadee Tufted titmouse Domestic cat Domestic dog Domestic horse Northern raccoon River otter Virginia opossum Human

9 Culex coronator Vector Competence WNV (in US) Field-collected females found 13,15,17 Highly susceptible in laboratory conditions (80-100%) Similar or higher transmission rates than Culex pipiens, Cx. quinquefasciatus and Cx. restuans 7 SLE (Trinidad and Brazil) 28,29 VEE (Mexico) 26 Ilheus virus (Peru) 27

10 Culex coronator Suffolk, VA collection New species state record November 1, 2016: collected 1 female specimen 16 No further specimens collected as of this report, despite increased trapping and larval surveying

11 Culex coronator Suffolk, VA Collection

12 Culex coronator Suffolk, VA Collection

14 Culex coronator US distribution/recent expansion 1906: first described, Trinidad 2 Mid-20 th Century: new in SW US- TX 18, AZ 19, NM 20 Early 2000s: significant expansions- 6 years, 8 new states 2003: OK : LA 9, MS : AL 11, FL : GA : SC : NC : VA 16

15 Culex coronator US distribution Akaratovic, K. I., & Kiser, J. P. (2017). First Record of Culex Coronator in Virginia, with Notes on Its Rapid Dispersal, Trapping Methods, and Biology. Journal of the American Mosquito Control Association, 33(3),

16 Culex nigripalpus Tropical/Neotropical Known range: Patagonia to southern US (no record in Chile) Indistinct adult morphology; easily confused with Cx. salinarius, Cx. pipiens complex, Cx. quinquefasciatus, and Cx. restuans Commons.wikimedia.org

even salt marsh Adults30, 40 Prefer high humidity conditions (> 90%); dense vegetation Found in diverse habitats, especially after

17 Larvae30, 31, 34 Culex nigripalpus Habitat Prefers fresh flooded, recent organic infusion, re-flooded every 10 d Tolerate a wide range of conditions Permanent, semi-permanent, and temporary pools Natural and artificial containers FW swamp, brackish water, even salt marsh Adults30, 40 Prefer high humidity conditions (> 90%); dense vegetation Found in diverse habitats, especially after heavy rainfall: Residential areas Pine forests Adjacent to salt marshes Floodplains Day & Curtis, 1994

usually single, 2x siphon width Mesothoracic seta 1-M tiny seta 2-M Carpenter

18 Culex nigripalpus Larval Morphology Head seta 5,6C with 3-4 branches Siphon length 6-7 times width at base 4 pairs of setae 1-S (siphon); basal pair usually single, 2x siphon width Mesothoracic seta 1-M tiny seta 2-M Carpenter and LaCasse 1955 Thoracic integument with tiny aciculae (spicules) Harrison et al. 2016

19 Culex nigripalpus Adult Morphology Features can be damaged in common adult traps Easily confused with : Cx. pipiens, Cx. quinquefasciatus Cx. restuans, Cx. salinarius Hindtarsomeres and proboscis dark, rarely with pale ventral scales Mid-lobe of scutellum with basal patch of fine dark brown scales Bugguide.net

20 Culex nigripalpus Adult Morphology Abdominal terga with indistinct/narrow pale bands and large basolateral patches on distal segments Segment VII mostly dark Sides of thorax appear glossy Mesepimeron without pale median patch

22 Culex nigripalpus Trapping Collected late summer and fall throughout range in US Strong correlation between emergence and humidity/rainfall Ideal: alternating heavy rain, drought conditions Bioquip.com Most commonly collected in New Jersey and CDC light traps, gravid traps Suffolk collection: CDC & BG-Sentinel 2

23 Culex nigripalpus Hosts Opportunistic feeder Seasonal transitions from avian to mammalian12, 39 Northern cardinal, common grackle, domestic chicken Northern raccoon, Virginia opossum, white-tailed deer Amplification and enzootic vector

24 Culex nigripalpus Vector Competence SLE 30 Primary enzootic and epidemic vector in FL 5 major epidemics in FL since 1959; most recent WNV30, 37, 38 One of the primary epizootic vectors in FL EEEV38, 41 Turkey malaria 36

25 Culex nigripalpus Suffolk, Virginia collection New species state record October 13, 2017: collected 4 females at 3 widely separated sites December 6, 2017: collected 1 female at far north site

26 Culex nigripalpus Suffolk, VA Collection

27 Culex nigripalpus US distribution and expansions 1901: first described in St. Lucia, Lesser Antilles Mid-20 th century: documented in southern US Darsie & Ward, 1981 and 2005 maps not entirely accurate depictions 1990s-2017: new findings, some difficult to find, some unpublished (NC,VA) New map needed

28 Culex nigripalpus US distribution and expansions 2005 map Darsie & Ward 2005

29 Culex nigripalpus US distribution and expansions map map Darsie & Ward 2005 Akaratovic et al. unpublished

30 Culex nigripalpus US distribution and expansions Akaratovic et al. unpublished

31 Cx. coronator & Cx. nigripalpus Possible causes of expansion Anthropogenic factors Increased travel, shipping, etc. Severe weather Habitat creation, strong wind displacement 8,11,25 Rising global temperatures Misidentification Cx. coronator Cx. tarsalis Cx. nigripalpus Cx. pipiens, Cx quinquefasciatus, Cx. restuans, Cx. salinarius

Severe weather Habitat creation, strong wind displacement 8,11,25 Rising global temperatures

32 Cx. coronator & Cx. nigripalpus Possible causes of expansion Anthropogenic factors Increased travel, shipping, etc. Severe weather Habitat creation, strong wind displacement 8,11,25 Rising global temperatures Misidentification Jason Williams Cx. coronator Cx. tarsalis Nathan D. Burkett- Cadena, 2013 Cx. nigripalpus Cx. pipiens, Cx quinquefasciatus, Cx. restuans, Cx. salinarius

33 Cx. coronator & Cx. nigripalpus Possible causes of expansion

34 Future Outlook Cx. coronator and Cx. nigripalpus will most likely continue crossing borders May become established in VA Arboviral potential More species expanding in the coming decades as global temperatures increase

35 References 1. Laurito, M., Briscoe, A. G., AlmirÓn, W. R., & Harbach, R. E. (2017). Systematics of the Culex coronator complex (Diptera: Culicidae): morphological and molecular assessment. Zoological Journal of the Linnean Society. 2. Dyar HG, Knab F The larvae of Culicidae classified as independent organisms. J NY Entomol Soc 14: , Varnado WC, Goddard J, Harrison BA New state record of Culex coronator Dyar and Knab (Diptera:Culicidae) from Mississippi. Proc Entomol Soc Wash107: Goddard J, Varnado WC, Harrison BA Notes on the ecology of Culex coronator Dyar and Knab, in Mississippi. J Am Mosq Control Assoc 22: Gray KM, Burkett-Cadena ND, Eubanks MD Pecor JE, Harbach RE, Peyton EL, Roberts DR, Rejmonkova E, Manguin S, Palanko J Mosquito studies in Belize, Central America: records, taxonomic notes, and a checklist of species. J Am Mosq Control Assoc 18: Gray KM, Burkett-Cadena ND, Eubanks MD Distribution expansion of Culex coronator in Alabama. J Am Mosq Control Assoc 24: Alto BW, Connelly CR, O Meara GF, Hickman D, Karr N Reproductive biology and susceptibility of Florida Culex coronator to infection with West Nile Virus. Vector Borne Zoonotic Dis 14: Connelly CR, Alto BW, O Meara GF The spread of Culex coronator (Diptera: Culicidae) throughout Florida. J Vector Ecol 41: Debboun M, Kuhr DD, Rueda LM, Pecor JE First record of Culex (Culex) coronator in Louisiana, USA. J Am Mosq Control Assoc 21: Smith JP, Walsh JD, Cope EH, Tennant RA, Kozak JA, Darsie RF Culex coronator Dyar and Knab: a new Florida species record. J Am Mosq Control Assoc 22: McNelly JR, Smith M, Micher-Stevens KM, Harrison BA First record of Culex coronator from Alabama. J Am Mosq Control Assoc 23: Mackay AJ, Kramer WL, Meece JK, Brumfield RT, Foil LD Host feeding patterns of Culex mosquitoes (Diptera: Culicidae) in East Baton Rouge Parish, Louisiana. J Med Entomol 47: Mackay AJ, Roy A, Yates MM, Foil LD West Nile Virus detection in mosquitoes in East Baton Rouge Parish, Louisiana, from November 2002 to October J Am Mosq Control Assoc 24: Easton ER, Price MA, Graham OH The collection of biting flies in West Texas with Malaise and animal baited traps. Mosq News 28: Brauch JE The integration of mosquito avian host preference with West Nile Virus activity in wild bird and mosquito populations in Baton Rouge, Louisiana [M.S. thesis]. Louisiana State University, Baton Rouge, LA. Available from: LSU Digital Commons (etd ). 16. Akaratovic, K. I., & Kiser, J. P. (2017). First Record of Culex Coronator in Virginia, with Notes on Its Rapid Dispersal, Trapping Methods, and Biology. Journal of the American Mosquito Control Association, 33(3), LMCA [Louisiana Mosquito Control Association] Le Maringouin Newsletter: December 2003 [Internet]. Hammond, LA: Louisiana Mosquito Control Association [accessed March 16, 2017]. Available from Randolph NM and O Neill K The mosquitoes of Texas Bulletin, Texas State Health Dept. 100p. 19. Richards CS, Nielsen LT, Rees DM Mosquito records from the Great Basin and the drainage of the lower Colorado River. Mosq News 16: Wolff TA, Nielsen LT, Hayes RO A current list and bibliography of the mosquitoes of New Mexico. Mosq Syst 7: Noden BH, Coburn L, Wright R, Bradely K An updated checklist of the mosquitoes of Oklahoma including new state records and West Nile Virus Vectors, J Am Mosq Control Assoc 31:

36 References Kelly R, Mead D, Harrison BA Discovery of Culex coronator Dyar and Knab (Diptera: Culicidae) in Georgia. Proc Entomol Soc Wash 110: Moulis RA, Russell JD, Lewandowski HB, Thompson PS, Heusel JL Culex coronator in coastal Georgia and South Carolina. J Am Mosq Control Assoc 24: Harrison BA, Byrd BD, Sither CB, Whitt PB The mosquitoes of the Mid-Atlantic region: an identification guide. Mosquito and Vector-borne Infectious Diseases Laboratory Publication , Western Carolina University, Cullowhee, NC, 201 pp NCMVCA [North Carolina Mosquito and Vector Control Association] The Biting Times Newsletter. March 2017 [Internet]. Greenville, North Carolina: North Carolina Mosquito and Vector Control Association [accessed March 20, 2017]. Available from Scherer WF, Dickerman RW, Diaz-Najera A, Ward BA, Miller MH, Schaffer PA Ecologic studies of Venezuelan encephalitis virus in southeastern Mexico. III. Infection of mosquitoes. Am J Trop Med Hyg 20: Turell, M. J., M. L. O Guinn, J. W. Jones, M. R. Sardelis, D. J. Dohm, D. M. Watts, R. Fernandez, A. Travassos da Rosa, H. Guzman, R. Tesh, C. A. Rossi, G. V. Ludwig, J. A. Mangiafico, J. Kondig, L. P. Wasieloski, Jr., J. Pecor, M. Zyzak, G. Schoeler, C. N. Mores, C. Calampa, J. S. Lee, and T. A. Klein Isloation of viruses from mosquitoes (Diptera: Culicidae) collected in the Amazon Basin region of Peru. J. Med. Entomol. 42: Aitken, T. H. G., W. G. Downs, L. Spence, and A. H. Jonkers St. Louis encephalitis virus isolations in Trinidada, West Indies, Am. J. Trop. Med. Hyg. 13(3): Vasconcelos, P. F. da C., J. F. S. Travassos da Rosa, A. P. de A. Travassos da Rosa, N. Dégallier, F. de P. Pinheiro, G. C. Sá Filho Epidemiologia das encefalites por arbavírus na Amazônia brasileira. Rev. Inst. Med. Trop. S. Paulo. 33: Day, J. F., & Curtis, G. A. (1994). When it rains, they soar and that makes Culex nigripalpus a dangerous mosquito. American Entomologist, 40(3), O'Meara, G. F., Cutwa-Francis, M., & Rey, J. R. (2010). Seasonal variation in the abundance of Culex nigripalpus and Culex quinquefasciatus in wastewater ponds at two Florida dairies. Journal of the American Mosquito Control Association, 26(2), Dow, R. P., & Gerrish, G. M. (1970). Day-to-day change in relative humidity and the activity of Culex nigripalpus (Diptera: Culicidae). Annals of the Entomological Society of America, 63(4), Shaman, J., & Day, J. F. (2007). Reproductive phase locking of mosquito populations in response to rainfall frequency. PLoS One, 2(3), e Wright, J. P. (2017). Geospatial and Negative Binomial Regression Analysis of Culex nigripalpus, Culex erraticus, Coquillettidia perturbans, and Aedes vexans Counts and Precipitation and Land use Land cover Covariates in Polk County, Florida (Doctoral dissertation, University of South Florida) Mackay, A. J., Kramer, W. L., Meece, J. K., Brumfield, R. T., & Foil, L. D. (2010). Host feeding patterns of culex mosquitoes (Diptera: culicidae) in east baton rouge parish, Louisiana. Journal of medical entomology, 47(2), FORRESTER, D. J., NAYAR, J. K., & FOSTER, G. W. (1980). Culex nigripalpus: A natural vector of wild turkey malaria (Plasmodium hermani) in Florida. Journal of Wildlife Diseases, 16(3), Sardelis, M. R., Turell, M. J., Dohm, D. J., & O'Guinn, M. L. (2001). Vector competence of selected North American Culex and Coquillettidia mosquitoes for West Nile virus. Emerging infectious diseases, 7(6), Turell, M. J., Dohm, D. J., Sardelis, M. R., O guinn, M. L., Andreadis, T. G., & 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(1), Edman, J. D., & Taylor, D. J. (1968). Culex nigripalpus: seasonal shift in the bird-mammal feeding ratio in a mosquito vector of human encephalitis. Science, 161(3836), Xue R., Qualls W.A., & Kline D.L. (2016). Population reduction of mosquitoes and biting midges after deployment of mosquito magnet traps at a golf course adjacent to saltmarsh habitats in St. Augustine Beach, Florida. Technical Bulletin of the Florida Mosquito Control Association (10), Zyzak, M., Loyless, T., Cope, S., Wooster, M., & Day, J. F. (2002). Seasonal abundance of Culex nigripalpus Theobald and Culex salinarius Coquillett in north Florida, USA. Journal of vector ecology, 27,

37 Acknowledgements City of Suffolk, VA Beaufort County Mosquito Control Environmental Health Dept Jay Kiser Ann Herring Eugene McRoy Charles Abadam Alyx Riley Janice Gardner Richard White Brunswick County, NC Ashley Byers Junior Harrell Mosquito Control Amber Rymer Jeff Brown Western Carolina University Dr. Bruce A. Harrison NCMVCA / East Carolina University Dr. Stephanie L. Richards WRBU / New Hanover County, NC Mosquito Control Marie Hemmen Smithsonian Institute James E. Pecor

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