Skip to main content

Advertisement

SpringerLink
Log in

Invasive Plants as Foci of Mosquito-Borne Pathogens: Red Cedar in the Southern Great Plains of the USA

  • Original Contribution
  • Published:
EcoHealth Aims and scope Submit manuscript

Abstract

West Nile virus (WNV) is the most significant mosquito-borne disease affecting humans in the United States. Eastern redcedar (ERC) is a native encroaching plant in the southern Great Plains that greatly alters abiotic conditions and bird and mosquito populations. This study tested the hypotheses that mosquito communities and their likelihood of WNV infection differ between ERC and other habitats in the southern Great Plains of the United States. We found support for our first hypothesis, with significantly more Culex tarsalis and Culex erraticus in ERC than deciduous and grass habitats. Mosquito communities in Central Oklahoma were more diverse (21 species) than western Oklahoma (11 species) but this difference was not associated with vegetation. Our second hypothesis was also supported, with significantly more WNV-infected Culex from ERC in both regions, as was our third hypothesis, with significantly more Culex tarsalis and Culex pipiens collected in ERC than other habitats in urban areas. The connection of mosquito-borne disease with invasive plants suggests that land management initiatives can affect human health and should be considered in light of public health impact. Evidence from other vector-borne disease suggests invasive plants, both in the Great Plains and globally, may facilitate the transmission of vector-borne pathogens.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3

Similar content being viewed by others

Data Availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reason request.

References

  • Acharya B, Kharel G, Zou C, Wilcox B, Halihan T (2018) Woody plant encroachment impacts on groundwater recharge: A review. Water 10:1466

    Article  Google Scholar 

  • Adalsteinsson SA, Shriver WG, Hojgaard A, Bowman JL, Brisson D, D’Amico V, Buler JJ (2018) Multiflora rose invasion amplifies prevalence of Lyme disease pathogen, but not necessarily Lyme disease risk. Parasites and Vectors 11:54

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 107:18523–18527

    Article  CAS  Google Scholar 

  • Allen T, Murray KA, Zambrana-Torrelio C, Morse SS, Rondinini C, Di Marco M, Breit N, Olival KJ, Daszak P (2017) Global hotspots and correlates of emerging zoonotic diseases. Nature Communications 8:1124

    Article  PubMed  PubMed Central  Google Scholar 

  • Archer SR, Andersen EM, Predick KI, Schwinning S, Steidl RJ, Woods SR (2017) Woody plant encroachment: causes and consequences. In: Rangeland systems Cham: Springer, pp 25–84

    Chapter  Google Scholar 

  • Bolling BG, Barker CM, Moore CG, Pape WJ, Eisen L (2009) Seasonal patterns for entomological measures of risk for exposure to Culex vectors and West Nile virus in relation to human disease cases in Northeastern Colorado. Journal of Medical Entomology 46:1519–1531

    Article  PubMed  Google Scholar 

  • Biggerstaff BJ (2006) PooledInfRate. Version 3.0: a Microsoft Excel Add-In to compute prevalence estimates from pooled samples. Fort Collins, CO: Centers for Disease Control and Prevention. Accessed at: https://www.cdc.gov/westnile/resourcepages/mosqSurvSoft.html

  • Bradt D, Wormington JD, Long JM, Hoback WW, Noden BH (2019) Differences in mosquito communities in six cities in Oklahoma. Journal of Medical Entomology 56:1395–1400

    Article  PubMed  Google Scholar 

  • Caterina GL, Will RE, Turton DJ, Wilson DS, Zou CB (2014) Water use of Juniperus virginiana trees encroached into mesic prairies in Oklahoma, USA. Ecohydrology 7:1124–1134

    Google Scholar 

  • Coppedge BR, Engle DM, Masters RE, Gregory MS (2001) Avian response to landscape change in fragmented southern Great Plains grasslands. Ecological Applications 11:47–59

    Article  Google Scholar 

  • Curren EJ, Lehman J, Kolsin J, Walker WL, Martin SW, Staples JE, Hills SL, Gould CV, Rabe IB, Fischer M, Lindsey NP (2018) West Nile virus and other nationally notifiable arboviral diseases - United States, 2017. Morbidity Mortality Weekly Report 67:1137–1142

    Article  PubMed  PubMed Central  Google Scholar 

  • Darsie RF, Ward RA (2005) Identification and Geographical Distribution of the Mosquitoes of North America, North of Mexico, Gainesville, 2nd edn. Press of Florida: Univ

    Google Scholar 

  • Dusek RJ, McLean RG, Kramer LD, Ubico SR, Dupuis AP II, Ebel GD, Guptill SC (2009) Prevalence of West Nile virus in migratory birds during spring and fall migration. The American Journal of Tropical Medicine Hygiene 81:1151–1158

    Article  PubMed  Google Scholar 

  • Eldridge DJ, Bowker MA, Maestre FT, Roger E, Reynolds JF, Whitford WG (2011) Impacts of shrub encroachment on ecosystem structure and functioning: towards a global synthesis. Ecology Letters 14:709–722

    Article  PubMed  PubMed Central  Google Scholar 

  • Engle DM, Coppedge BR, Fuhlendorf SD (2008) From the dust bowl to the green glacier: Human activity and environmental change in Great Plains grasslands. In: Van Auken OW (ed) Western North American Juniperus Communities: A Dynamic Vegetation Typepp 253–271

    Chapter  Google Scholar 

  • Engle DM, Kulbeth JD (1992) Growth dynamics of crowns of eastern redcedar at 3 locations in Oklahoma. Journal of Range Management 45:301–305

    Article  Google Scholar 

  • Flonard M, Lo E, Levetin E (2018) Increasing Juniperus virginiana L. pollen in the Tulsa atmosphere: long-term trends, variability, and influence of meteorological conditions. International Journal of Biometeorology 62:229–241

    Article  PubMed  Google Scholar 

  • Foley JA, DeFries R, Asner GP, Barford C, Bonan G, Carpenter SR, Chapin FS, Coe MT, Daily GC, Gibbs HK, Helkowski JH, Holloway T, Howard EA, Kucharik CJ, Monfreda C, Patz JA, Prentice C, Ramankutty N, Snyder PK (2005) Global consequences of land use. Science 309:570–574

    Article  CAS  PubMed  Google Scholar 

  • Frost JS, Powell LA (2011) Cedar infestation impacts avian communities along the Niobrara river valley, Nebraska. Restoration Ecology 19:529–536

    Article  Google Scholar 

  • Fryxell RT, Lewis TT, Peace H, Hendricks BB, Paulsen D (2014) Identification of avian malaria (Plasmodium sp.) and canine heartworm (Dirofilaria immitis) in the mosquitoes of Tennessee. Journal of Parasitology 100:455–462

    Article  Google Scholar 

  • Gardner AM, Muturi EJ, Overmier LD, Allan BF (2017) Large-scale removal of invasive honeysuckle decreases mosquito and avian host abundance. Ecohealth 14:750–761

    Article  PubMed  Google Scholar 

  • Godsey Jr MS, Blackmore MS, Panella NA, Burkhalter K, Gottfried K, Halsey LA, Rutledge R, Langevin SA, Gates R, Lamonte KM, Lambert A, Lanciotti RS, Blackmore CGM, Loyless T, Stark L, Oliveri R, Conti L, Komar N ( 2005) West Nile virus epizootiology in the southeastern United States, 2001. Vector-Borne & Zoonotic Diseases 5:82-89

  • 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 transmission. The American Journal of Tropical Medicine and Hygiene 80:268–278

    Article  PubMed  Google Scholar 

  • Horncastle VJ, Hellgren EC, Mayer PM, Ganguli AC, Engle DM, Leslie DM Jr (2005) Implications of invasion by Juniperus virginiana on small mammals in the southern Great Plains. Journal of Mammalogy 86:1144–1155

    Article  Google Scholar 

  • Johnson MG, Adams J, McDonald-Hamm C, Wendelboe A, Bradley KK (2015) Seasonality and survival associated with three outbreak seasons of West Nile virus disease in Oklahoma—2003, 2007, and 2012. Journal of Medical Virology 87:1633–1640

    Article  PubMed  Google Scholar 

  • Joshi O, Becerra TA, Engle DM, Fuhlendorf SD, Elmore RD (2017) Factors affecting public preferences for grassland landscape heterogeneity in the Great Plains. Environmental Management 60:922–930

    Article  PubMed  Google Scholar 

  • Kent R, Juliusson L, Weissmann M, Evans S, Komar N (2009) Seasonal blood-feeding behavior of Culex tarsalis (Diptera: Culicidae) in Weld County, Colorado, 2007. Journal of Medical Entomology 46:380–390

    Article  PubMed  Google Scholar 

  • Kilpatrick AM, Daszak P, Jones MJ, Marra PP, Kramer LD (2006a) Host heterogeneity dominates West Nile virus transmission. Proceedings of the Royal Society of London b: Biological Sciences 273:2327–2333

    Google Scholar 

  • Kilpatrick AM, Kramer LD, Jones MJ, Marra PP, Daszak P (2006) West Nile virus epidemics in North America are driven by shifts in mosquito feeding behavior. PLoS Biology 4:e82

    Article  PubMed  PubMed Central  Google Scholar 

  • Lanciotti RS, Kerst AJ, Nasci RS, Godsey MS, Mitchell CJ, Savage HM, Komar N, Panella NA, Allen BC, Volpe KE, Davis BS, Roehrig JT (2000) Rapid detection of West Nile virus from human clinical specimens, field-collected mosquitoes, and avian samples by a TaqMan reverse transcriptase-PCR assay. Journal of Clinical Microbiology 38:4066‐4071

  • Lindsey NP, Kuhn S, Campbell GL, Hayes EB (2008) West Nile virus neuroinvasive disease incidence in the United States, 2002–2006. Vector-Borne & Zoonotic Diseases 8:35–40

    Article  Google Scholar 

  • Lyimo IN, Ferguson HM (2009) Ecological and evolutionary determinants of host species choice in mosquito vectors. Trends Parasitology 25:189–196

    Article  Google Scholar 

  • Martins LMO, David MR, Maciel-de-Freitas R, Silva-do-Nascimento TF (2018) Diversity of Anopheles mosquitoes from four landscapes in the highest endemic region of malaria transmission in Brazil. Journal of Vector Ecology 43:235–244

    Article  CAS  PubMed  Google Scholar 

  • Nackley LL, West AG, Skowno AL, Bond WJ (2017) The nebulous ecology of native invasions. Trends in Ecology and Evolution 32:814–824

    Article  PubMed  Google Scholar 

  • Noden BH, Coburn L, Wright R, Bradley K (2015) An updated checklist of the mosquitoes of Oklahoma including new state records and West Nile Virus vectors, 2003–06. Journal of the American Mosquito Control Association 31:336–345

    Article  PubMed  Google Scholar 

  • Noden BH, Dubie T (2017) Involvement of invasive eastern red cedar (Juniperus virginiana) in the expansion of Amblyomma americanum in Oklahoma. Journal of Vector Ecology 42:178–183

    Article  PubMed  Google Scholar 

  • Noden BH, Tanner EP, Polo JA, Fuhlendorf SD (2021) Invasive woody plants as foci of tick-borne pathogens: eastern redcedar in the southern Great Plains. Journal of Vector Ecology 46:12–18

    Article  Google Scholar 

  • O’Brien VA, Reiskind MH (2013) Host-seeking mosquito distribution in habitat mosaics of southern Great Plains cross-timbers. Journal of Medical Entomology 50:1231–1239

    Article  PubMed  Google Scholar 

  • Oklahoma Climatological Survey (OCS) (2016) Oklahoma Climate. Accessed at: http://climate.ok.gov/index.php/climate.

  • Paull SH, Horton DE, Ashfaq M, Rastogi D, Kramer LD, Diffenbaugh NS, Kilpatrick AM (2017) Drought and immunity determine the intensity of West Nile virus epidemics and climate change impacts. Proceedings of the Royal Society of London b: Biological Sciences 284:20162078

    Google Scholar 

  • Pavlovsky N (1966) The natural nidality of transmissible disease with special reference to the landscape ecology of zooanthroposes. Urbana: University of Illinois Press

    Google Scholar 

  • Petersen LR, Carson PJ, Biggerstaff BJ, Custer B, Borchardt SM, Busch MP (2013) Estimated cumulative incidence of West Nile virus infection in US adults, 1999–2010. Epidemiology & Infection 141:591–595

    Article  CAS  Google Scholar 

  • Ratajczak Z, Nippert JB, Collins SL (2012) Woody encroachment decreases diversity across North American grasslands and savannas. Ecology 93:697–703

    Article  PubMed  Google Scholar 

  • Reimann CA, Hayes EB, DiGuiseppi C, Hoffman R, Lehman JA, Lindsey NP, Campbell GL, Fischer M (2008) Epidemiology of neuroinvasive arboviral disease in the United States, 1999–2007. The American Journal of Tropical Medicine Hygiene 79:974–979

    Article  PubMed  Google Scholar 

  • Reisen WK (2010) Landscape epidemiology of vector-borne diseases. Annual Review of Entomology 55:461–483

    Article  CAS  PubMed  Google Scholar 

  • Reiskind MH, Griffin RH, Janairo MS, Hopperstad KA (2017) Mosquitoes of field and forest: the scale of habitat segregation in a diverse mosquito assemblage. Medical and Veterinary Entomology 31:44–54

    Article  CAS  PubMed  Google Scholar 

  • Reiskind MH, Zarrabi AA (2011) The importance of an invasive tree fruit as a resource for mosquito larvae. Journal of Vector Ecology 36:197–203

    Article  PubMed  Google Scholar 

  • Reiskind MH, Zarrabi AA, Lounibos LP (2010) Invasive leaf resources alleviate density dependence in the invasive mosquito, Aedes albopictus. Biological Invasions 12:2319–2328

    Article  PubMed  Google Scholar 

  • Rosenberg R, Lindsey NP, Fischer M, Gregory CJ, Hinckley AF, Mead PS, Paz-Bailey G, Waterman SH, Drexler NA, Kersh GJ, Hooks H, Partridge SK, Visser SN, Beard CB, Petersen LR (2018) Vital Signs: Trends in reported vectorborne disease cases - United States and Territories, 2004–2016. Morbidity Mortality Weekly Report 67:496–501

    Article  PubMed  PubMed Central  Google Scholar 

  • Sherrill KK (2019) The influence of eastern red cedar on Tabanidae populations in Oklahoma. Master’s degree: Oklahoma State University. Accessed at: https://shareok.org/bitstream/handle/11244/321612/Sherrill_okstate_0664M_16279.pdf?sequence=1&isAllowed=y

  • Spence Beaulieu MR, Hopperstad K, Dunn RR, Reiskind MH (2019) Simplification of vector communities during suburban succession. PLoS One 14:e0215485

    Article  PubMed  PubMed Central  Google Scholar 

  • Spence Beaulieu MR, Reiskind MH (2020) Comparative vector efficiency of two prevalent mosquito species for dog heartworm in North Carolina. Journal of Medical Entomology 57:608–614

    PubMed  Google Scholar 

  • Symstad AJ, Leis SA (2017) Woody encroachment in northern great plains grasslands: perceptions, actions, and needs. Natural Areas Journal 37:118–127

    Article  Google Scholar 

  • Thiemann TC, Wheeler SS, Barker CM, Reisen WK (2011) Mosquito host selection varies seasonally with host availability and mosquito density. PLoS Neglected Tropical Diseases 5:e1452

    Article  PubMed  PubMed Central  Google Scholar 

  • Turell MJ, Spring AR, Miller MK, Cannon CE (2002) Effect of holding conditions on the detection of West Nile viral RNA by reverse transcriptase-polymerase chain reaction from mosquito (Diptera: Culicidae) pools. Journal of Medical Entomology 39:1–3

    Article  PubMed  Google Scholar 

  • Twidwell D, Rogers WE, Fuhlendorf SD, Wonkka CL, Engle DM, Ukawuba I, Shaman J (2018) Association of spring-summer hydrology and meteorology with human West Nile virus infection in West Texas, USA, 2002–2016. Parasites and Vectors 11:224

    Article  Google Scholar 

  • Venter ZS, Cramer MD, Hawkins HJ (2018) Drivers of woody plant encroachment over Africa. Nature Communications 9:2272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang J, Xiao X, Qin Y, Doughty RB, Dong J, Zou Z (2018) Characterizing the encroachment of juniper forests into sub-humid and semi-arid prairies from 1984 to 2010 using PALSAR and Landsat data. Remote Sensing of Environment 205:166–179

    Article  Google Scholar 

  • 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 39:1911–1921

    Article  PubMed  Google Scholar 

  • Zou CB, Twidwell D, Bielski CH, Fogarty DT, Mittelstet AR, Starks PJ, Will RE, Zhong Y, Acharya BS (2018) Impact of Eastern redcedar proliferation on water resources in the great plains USA- current state of knowledge. Water (switzerland) 10:1768

    Google Scholar 

Download references

Acknowledgements

We thank the landowners who allowed free access and trapping to occur on their land and Alexandra Spring and personnel in the Army Public Health Command for assistance in WNV testing. NMC was supported by the United States Navy Medical Service Corps In-service Procurement Program. Partial support was provided by funding from NIFA/USDA Hatch Grant funds through the Oklahoma Agricultural Experiment Station [BHN (OKL-03085); JLT (OKL 003036)] and USDA Multistate Projects [BHN (OKL03186); JLT (OKL 03110) MHR (NC-01943)].

Author information

Authors and Affiliations

  1. Department of Entomology and Plant Pathology, Oklahoma State University, 127 Noble Research Center, Stillwater, OK, 74078, USA

    Bruce H. Noden, Noel M. Cote & Justin L. Talley

  2. Department of Entomology and Plant Pathology, North Carolina State University, 2310 Gardner Hall, Raleigh, NC, 27696, USA

    Michael H. Reiskind

Authors
  1. Bruce H. Noden
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Noel M. Cote
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michael H. Reiskind
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Justin L. Talley
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bruce H. Noden.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary Information

Below is the link to the electronic supplementary material.

10393_2021_1562_MOESM1_ESM.tif

Mean trap night abundance for Cx. tarsalis in urban and rural landscapes by region and canopy. In each boxplot, the mean is represented as a black line with the upper and lower quartiles making the box and whiskers being within 1.5x the interquartile range (TIF 3697 KB)

10393_2021_1562_MOESM2_ESM.tif

Open eastern redcedar canopy sites where pools WNV-infected Culex tarsalis were collected in urban Okeene (A) and rural Fairview (B) (TIF 3763 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Noden, B.H., Cote, N.M., Reiskind, M.H. et al. Invasive Plants as Foci of Mosquito-Borne Pathogens: Red Cedar in the Southern Great Plains of the USA. EcoHealth 18, 475–486 (2021). https://doi.org/10.1007/s10393-021-01562-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10393-021-01562-8

Keywords

Search

Navigation