, Volume 22, Issue 2, pp 416–433 | Cite as

Contributions of Hydrology to Vesicular Stomatitis Virus Emergence in the Western USA

  • Emile EliasEmail author
  • D. Scott McVey
  • Debra Peters
  • Justin D. Derner
  • Angela Pelzel-McCluskey
  • T. Scott Schrader
  • Luis Rodriguez


Relationships between environmental variables associated with the spread of vector-borne pathogens, such as RNA viruses transmitted to humans and animals, remain poorly understood. Vesicular stomatitis (VS) is caused by a vector-borne, zoonotic RNA virus (VSV) and is the most common vesicular disease affecting livestock (domestic horses, cattle, pigs) throughout the Americas. This investigation focused on explaining patterns of more than 1500 VS-infected livestock premises in the western USA from 2004 to 2016 related to the ecology of the host-vector-virus-environment system. We investigated the relationship between VS incidents and habitat characteristics expected to be important to insect vectors: stream location, streamflow conditions, climate, and vegetation. Results show that VS incidents were distributed near the stream network with 72% located within 1 km of lotic habitat. Monthly incidents were closest to lotic habitat in April (x = 525 m) and furthest from lotic habitat in November, December and January (1843, 2141 and 4807 m) indicating that initial infection near streams may spread away from these locations. All first incidents (n = 35) occurred following peak annual streamflow, with 89% (31 of 35) of these occurring after streams returned to baseflow. This finding indicated that surveillance for VS could be targeted spatially in locally relevant geographic areas (that is, near streams) and temporally relative to local streamflow conditions which can be remotely monitored via existing web-accessible information networks. Habitat modeling of 11 subwatersheds revealed somewhat different models for each watershed with several factors important in multiple watersheds. In nine of the 11 watersheds, the highest model PC (31–71%) represented either higher-than-average long-term mean temperature or lower-than-average long-term mean precipitation. Approaching habitat modeling on a watershed basis reveals information to support additional research. These spatial and temporal relationships showcase the importance of hydrologic contributions to the emergence and distribution of an arthropod-borne disease in the western USA.


vesicular stomatitis vector-borne disease streamflow western USA livestock horses virus transmission MAXENT 



The authors thank Ryann Smith and Dustin Ward for data collection and mapping support. We also thank Dr. Mike Hobbins for providing Evaporative Demand Drought Index data. This work was supported by USDA-ARS CRIS Projects at the Jornada Experimental Range (#6235-11210-007), Plum Island Animal Disease Center (Project No. 8064-32000-058-00D), Center for Grain and Animal Health Research (#8064-32000-058-00D, #3020-32000-008-00D), and the Rangeland Resources and Systems Research Unit (#3012-21610-001-00D). Funding was provided by the National Science Foundation to New Mexico State University for the Jornada Basin Long Term Ecological Research Program (DEB 12-35828) and DEB 14-40166. We thank Mr. Darren James and Dr. Geovany Ramirez of NMSU for additional analyses in support of this study. We thank the USDA Office of the Chief Scientist for support of DPCP.

Supplementary material

10021_2018_278_MOESM1_ESM.docx (13 kb)
Supplementary material 1 (DOCX 12 kb)


  1. Abdelnur OM. 1968. The biology of some black flies (Diptera: Simuliidae) of Alberta. Quaestiones Entomologicae 4:113–74.Google Scholar
  2. Adler PH, Cheke RA, Post RJ. 2010. Evolution, epidemiology, and population genetics of black flies (Diptera: Simuliidae). Infect Genet Evol 10(7):846–65. Scholar
  3. Bartrons M, Papeş M, Diebel MW, Gratton C, Vander Zanden MJ. 2013. Regional-level inputs of emergent aquatic insects from water to land. Ecosystems 16(7):1353–63. Scholar
  4. Bernotiene R, Bartkeviciene G. 2013. The relationship between water temperature and the development cycle beginning and duration in three black fly species. J Insect Sci 13:1. Scholar
  5. Black WCIV, Moore CG. 2005. Population biology as a tool to study vector-borne diseases. New York: Elsevier.Google Scholar
  6. Botto C, Escalona E, Vivas-Martinez S, Behm V, Delgado L, Coronel P. 2005. Geographical patterns of onchocerciasis in southern Venezuela: relationships between environment and infection prevalence. Parassitologia 47(1):145–50.Google Scholar
  7. Brannin MT, O’Donnell MK, Fingerut J. 2014. Effects of larval size and hydrodynamics on the growth rates of the black fly Simulium tribulatum. Integr Zool 9(1):61–9. Scholar
  8. Cheke RA. 1995. Cycles in daily catches of members of the Simulium damnosum species complex. Trop Med Parasitol 46(4):247–52.Google Scholar
  9. Cheke RA. 2012. The thermal constant of the onchocerciasis vector Simulium damnosum s.l. in West Africa. Med Vet Entomol 26(2):236–8. Scholar
  10. Cid N, Verkaik I, Garcia-Roger EM, Rieradevall M, Bonada N, Sanchez-Montoya MM, Prat N. 2016. A biological tool to assess flow connectivity in reference temporary streams from the Mediterranean Basin. Sci Total Environ 540:178–90. Scholar
  11. Cross WF, Baxter CV, Donner KC, Rosi-Marshall EJ, Kennedy TA, Hall RO Jr, Rogers RS. 2011. Ecosystem ecology meets adaptive management: food web response to a controlled flood on the Colorado River, Glen Canyon. Ecol Appl 21(6):2016–33.CrossRefGoogle Scholar
  12. Daly C, Halbleib M, Smith JI, Gibson WP, Doggett MK, Taylor GH, Pasteris PA. 2008. Physiographically-sensitive mapping of temperature and precipitation across the conterminous United States. International Journal of Climatology 28:2031–64. Scholar
  13. Docile TN, Figueiro R, Gil-Azevedo LH, Nessimian JL. 2015. Water pollution and distribution of the black fly (Diptera: Simuliidae) in the Atlantic Forest, Brazil. Rev Biol Trop 63(3):683–93.CrossRefGoogle Scholar
  14. Drolet BS, Campbell CL, Stuart MA, Wilson WC. 2005. Vector competence of Culicoides sonorensis (Diptera: Ceratopogonidae) for vesicular stomatitis virus. J Med Entomol 42(3):409–18.CrossRefGoogle Scholar
  15. Duarte PC, Morley PS, Traub-Dargatz JL, Creekmore LH. 2008. Factors associated with vesicular stomatitis in animals in the western United States. J Am Vet Med Assoc 232(2):249–56. Scholar
  16. Eyo JE, Ikechukwu EO, Ubachukwu PO, Ivoke N, Ekeh FN. 2014. Effects of climatic conditions on the biting density and relative abundance of Simulium damnosum complex in a rural Nigerian farm settlement. Ann Agric Environ Med 21(4):697–700. Scholar
  17. Figueiro R, Maia-Herzog M, Gil-Azevedo LH, Monteiro RF. 2014. Seasonal variation in black fly (Diptera: Simuliidae) taxocenoses from the Brazilian Savannah (Tocantins, Brazil). J Vector Ecol 39(2):321–7. Scholar
  18. Goodger WJ, Thurmond M, Nehay J, Mitchell J, Smith P. 1985. Economic impact of an epizootic of bovine vesicular stomatitis in California. J Am Vet Med Assoc 186:370–3.Google Scholar
  19. Gratton C, Donaldson J, Zanden M. 2008. Ecosystem linkages between lakes and the surrounding terrestrial landscape in Northeast Iceland. Ecosystems 11:764–74. Scholar
  20. Grillet ME, Villamizar NJ, Cortez J, Frontado HL, Escalona M, Vivas-Martinez S, Basanez MG. 2005. Diurnal biting periodicity of parous Simulium (Diptera: Simuliidae) vectors in the onchocerciasis Amazonian focus. Acta Trop 94(2):139–58. Scholar
  21. Hadi UK, Takaoka H. 1995. Effects of constant temperatures on oviposition and immature development of Simulium bidentatum (Diptera: Simuliidae), a vector of bovine Onchocerca (Nematoda: Onchocercidae) in central Kyushu, Japan. J Med Entomol 32(6):801–6.CrossRefGoogle Scholar
  22. Howerth EW, Mead DG, Stallknecht DE. 2002. Immunolocalization of vesicular stomatitis virus in black flies (Simulium vittatum). Ann N Y Acad Sci 969:340–5.CrossRefGoogle Scholar
  23. Hurd HS, McCluskey BJ, Mumford EL. 1999. Management factors affecting the risk for vesicular stomatitis in livestock operations in the western United States. J Am Vet Med Assoc 215(9):1263–8.Google Scholar
  24. Ivkovic M, Kesic M, Mihaljevic Z, Kudela M. 2014. Emergence patterns and ecological associations of some haematophagous blackfly species along an oligotrophic hydrosystem. Med Vet Entomol 28(1):94–102. Scholar
  25. Jessen JI. 1977. Black flies (Dipter: Simuliidae) which affect sheep in southern Idaho. (PhD), University of Idaho, Moscow, Idaho.Google Scholar
  26. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P. 2008. Global trends in emerging infectious diseases. Nature 451(7181):990–3.CrossRefGoogle Scholar
  27. Kompas T, Nguyen TPL, Van Ha P. 2015. Food and biosecurity: livestock production and towards a world free of FMD. Food Security 7(2):375–82. Scholar
  28. LaDeau SL, Glass GE, Hobbs NT, Latimer A, Ostfeld RS. 2011. Data–model fusion to better understand emerging pathogens and improve infectious disease forecasting. Ecological Applications 21(5):1443–60. Scholar
  29. Liang X. 1994. A two-layer variable infiltration capacity land surface representation for general circulation models. Washington: Retrieved from Seattle.Google Scholar
  30. Lim KJ, Engel BA, Tang Z, Choi J, Kim K, Muthukrishnan S, Tripathy D. 2005. Automated web GIS based hydrograph analysis tool, WHAT. Journal of the American Water Resources Association 41(6):1407–16.CrossRefGoogle Scholar
  31. Lundberg J, Moberg F. 2003. Mobile link organisms and ecosystem functioning: implications for ecosystem resilience and management. Ecosystems 6(1):0087–98. Scholar
  32. McCall PJ. 1995. Oviposition aggregation pheromone in the Simulium damnosum complex. Med Vet Entomol 9(2):101–8.CrossRefGoogle Scholar
  33. McCall PJ, Cheke RA, Wilson MD, Post RJ, Flook PK, Mank R, Mas J. 1998. Distribution of the Simulium damnosum complex on Bioko island, Equatorial Guinea, and the potential for onchocerciasis elimination by vector eradication. Med Vet Entomol 12(3):267–75.CrossRefGoogle Scholar
  34. McCall PJ, Trees AJ. 1993. Onchocerciasis in British cattle: a study of the transmission of Onchocerca sp. in north Wales. J Helminthol 67(2):123–35.CrossRefGoogle Scholar
  35. McCluskey B, Hurd B, Mumford EL. 1999. Review of the 1997 outbreak of vesicular stomatitis in the western United States. J Am Vet Med Assoc 215(9):1259–62.Google Scholar
  36. McEvoy DJ, Huntington JL, Mejia JF, Hobbins MT. 2016. Improved seasonal drought forecasts using reference evapotranspiration anomalies. Geophysical Research Letters 43(1):377–85. Scholar
  37. Mead DG, Mare CJ, Cupp EW. 1997. Vector competence of select black fly species for vesicular stomatitis virus (New Jersey serotype). Am J Trop Med Hyg 57(1):42–8.CrossRefGoogle Scholar
  38. Mead DG, Mare CJ, Ramberg FB. 1999. Bite transmission of vesicular stomatitis virus (New Jersey serotype) to laboratory mice by Simulium vittatum (Diptera: Simuliidae). J Med Entomol 36(4):410–13.CrossRefGoogle Scholar
  39. Mead DG, Ramberg FB, Besselsen DG, Mare CJ. 2000a. Transmission of vesicular stomatitis virus from infected to noninfected black flies co-feeding on nonviremic deer mice. Science 287(5452):485–7. Scholar
  40. Mead DG, Ramberg FB, Mare CJ. 2000b. Laboratory vector competence of black flies (Diptera: Simuliidae) for the Indiana serotype of vesicular stomatitis virus. Ann N Y Acad Sci 916:437–43.CrossRefGoogle Scholar
  41. Merow C, Smith MJ, Silander JA. 2013. A practical guide to MaxEnt for modeling species’ distributions: what it does, and why inputs and settings matter. Ecography 36(10):1058–69. Scholar
  42. Millest AL, Cheke RA, Greenwood R. 1999. Distribution of the Simulium metallicum complex in Mexico in relation to selected environmental variables. Med Vet Entomol 13(2):139–49.CrossRefGoogle Scholar
  43. Moore RB, Dewald TG. 2016. The road to NHDPlus—advancements in digital stream networks and associated catchments. JAWRA Journal of the American Water Resources Association 52(4):890–900. Scholar
  44. Mullens BA. 1989. A quantitative survey of Culicoides variipennis (Diptera: Ceratopogonidae) in dairy wastewater ponds in southern California. J Med Entomol 26(6):559–65.CrossRefGoogle Scholar
  45. Mullens BA, Rodriguez JL. 1988. Colonization and response of Culicoides variipennis (Diptera: Ceratopogonidae) to pollution levels in experimental dairy wastewater ponds. J Med Entomol 25(6):441–51.CrossRefGoogle Scholar
  46. Murdock CC, Foufopoulos J, Simon CP. 2013. A transmission model for the ecology of an avian blood parasite in a temperate ecosystem. PLoS ONE 8(9):e76126. Scholar
  47. NASS. 2013. National Agricultural Statistics Service. Retrieved from
  48. NHDPlus Team. 2016. NHDPlus Version 2. Retrieved from:
  49. Olea PP, Mateo-Tomás P, de Frutos Á. 2010. Estimating and modelling bias of the hierarchical partitioning public-domain software: implications in environmental management and conservation. PLoS ONE 5(7):e11698. Scholar
  50. Opara KN, Fagbemi BO. 2005. Physico-chemical indices of breeding sites of Simulium damnosum in the lower Cross River Basin, Nigeria. J Environ Sci (China) 17(3):511–17.Google Scholar
  51. Pachon RT, Walton WE. 2011. Seasonal occurrence of black flies (Diptera: Simuliidae) in a desert stream receiving trout farm effluent. J Vector Ecol 36(1):187–96. Scholar
  52. Parham PE, Waldock J, Christophides GK, Hemming D, Agusto F, Evans KJ, Michael E. 2015. Climate, environmental and socio-economic change: weighing up the balance in vector-borne disease transmission. Philosophical Transactions of the Royal Society B: Biological Sciences . Scholar
  53. Paton DJ, Sumption KJ, Charleston B. 2009. Options for control of foot-and-mouth disease: knowledge, capability and policy. Philos Trans R Soc Lond B Biol Sci 364(1530):2657–67. Scholar
  54. Perez AM, Pauszek SJ, Jimenez D, Kelley WN, Whedbee Z, Rodriguez LL. 2010. Spatial and phylogenetic analysis of vesicular stomatitis virus over-wintering in the United States. Prev Vet Med 93(4):258–64. Scholar
  55. Peters DPC, Burruss N, Rodriguez LL, McVey DS, Elias E, Pelzel-McCluskey A, Derner JD, Schrader TS, Yao J, Pauszek SJ, Lombard J, Archer AR, Bestlemeyer B, Browning DM, Brungaard CW, Hatfield JL, Hannan NP, Herrick JE, Okin GS, Sala OE, Savoy H, Vivoni ER. 2018. An integrated view of complex landscapes: a big data-model integration approach to transdisciplinary science. Bioscience (accepted).Google Scholar
  56. Peters DPC, Rodriguez L, McVey DS, Elias EH, Pelzel-McCluskey A, Derner JD, Yao J, Pauszek SJ, Schrader TS, Burruss N. 2017. Towards a theory of ecological catastrophes based on cross-scale interactions: insights from long-term data. Paper presented at the Ecological Society of America, Portland, Oregon.
  57. Pfannenstiel RS, Mullens BA, Ruder MG, Zurek L, Cohnstaedt LW, Nayduch D. 2015. Management of North American culicoides biting midges: current knowledge and research needs. Vector Borne Zoonotic Dis 15(6):374–84. Scholar
  58. Pfannenstiel RS, Ruder MG. 2015. Colonization of bison (Bison bison) wallows in a tallgrass prairie by Culicoides spp (Diptera: Ceratopogonidae). J Vector Ecol 40(1):187–90.CrossRefGoogle Scholar
  59. Phillips SJ, Anderson RP, Schapire RE. 2006. Maximum entropy modeling of species geographic distributions. Ecol Model 190:231–59.CrossRefGoogle Scholar
  60. Plowright RK, Sokolow SH, Gorman ME, Daszak P, Foley JE. 2008. Causal inference in disease ecology: investigating ecological drivers of disease emergence. Frontiers in Ecology and the Environment 6(8):420–9. Scholar
  61. Preston DL, Mischler JA, Townsend AR, Johnson PTJ. 2016. Disease ecology meets ecosystem science. Ecosystems 19(4):737–48. Scholar
  62. Racloz V, Ramsey R, Tong S, Hu W. 2012. Surveillance of dengue fever virus: a review of epidemiological models and early warning systems. PLOS Neglected Tropical Diseases 6(5):e1648. Scholar
  63. Rainwater-Lovett K, Pauszek SJ, Kelley WN, Rodriguez LL. 2007. Molecular epidemiology of vesicular stomatitis New Jersey virus from the 2004–2005 US outbreak indicates a common origin with Mexican strains. J Gen Virol 88(Pt 7):2042–51. Scholar
  64. Rodríguez LL, Fitch WM, Nichol ST. 1996. Ecological factors rather than temporal factors dominate the evolution of vesicular stomatitis virus. Proc Natl Acad Sci U S A 93(23):13030–5.CrossRefGoogle Scholar
  65. Rodriguez LL, Pauszek SJ, Bunch TA, Schumann KR. 2002. Full-length genome analysis of natural isolates of vesicular stomatitis virus (Indiana 1 serotype) from North, Central and South America. J Gen Virol 83(Pt 10):2475–83.CrossRefGoogle Scholar
  66. Rozendaal JA. 1997. Vector control: methods for use by individuals and communities. Retrieved from Geneva, Switzerland:
  67. Soil Survey Staff. 2016. Web Soil Survey. Retrieved from:
  68. Thomson JR, Clark BD, Fingerut JT, Hart DD. 2004. Local modification of benthic flow environments by suspension-feeding stream insects. Oecologia 140(3):533–42. Scholar
  69. Timoney PJ. 2000. The increasing significance of international trade in equids and its influence on the spread of infectious diseases. Annals New York Academy of Sciences 916:55–60. Scholar
  70. Tucker CJ. 1979. Red and photographic infrared linear combinations for monitoring vegetation. Remote Sens Environ 8(2):127–50.CrossRefGoogle Scholar
  71. U.S. Geological Survey. 2001. National water information system data. Retrieved from
  72. U.S. Geological Survey. 2012. Surface Water for USA: Peak Streamflow. Retrieved from
  73. USGS. 2014. National Map Small Scale, One-million scale county boundaries of the United States. Retrieved from
  74. Vanleeuwen JA, Rodriguez LL, Waltner-Toews D. 1995. Cow, farm, and ecologic risk factors of clinical vesicular stomatitis on Costa Rican dairy farms. Am J Trop Med Hyg 53(4):342–50.CrossRefGoogle Scholar
  75. Velazquez-Salinas L, Pauszek SJ, Zarate S, Basurto-Alcantara FJ, Verdugo-Rodriguez A, Perez AM, Rodriguez LL. 2014. Phylogeographic characteristics of vesicular stomatitis New Jersey viruses circulating in Mexico from 2005 to 2011 and their relationship to epidemics in the United States. Virology 449:17–24. Scholar
  76. Ya’cob Z, Takaoka H, Pramual P, Low VL, Sofian-Azirun M. 2016a. Breeding habitat preference of preimaginal black flies (Diptera: Simuliidae) in Peninsular Malaysia. Acta Trop 153:57–63. Scholar
  77. Ya’cob Z, Takaoka H, Pramual P, Low VL, Sofian-Azirun M. 2016b. Distribution pattern of black fly (Diptera: Simuliidae) assemblages along an altitudinal gradient in Peninsular Malaysia. Parasit Vectors 9:219. Scholar
  78. Zarroug IM, Elaagip AH, Abuelmaali SA, Mohamed HA, ElMubarak WA, Hashim K, Higazi TB. 2014. The impact of Merowe Dam on Simulium hamedense vector of onchocerciasis in Abu Hamed focus—Northern Sudan. Parasit Vectors 7:168. Scholar
  79. Zarroug IM, Hashim K, Elaagip AH, Samy AM, Frah EA, ElMubarak WA, Higazi TB. 2016. Seasonal Variation in Biting Rates of Simulium damnosum sensu lato, Vector of Onchocerca volvulus. Two Sudanese Foci. PLoS One 11(3):e0150309. Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Jornada Experimental Range UnitUS Department of Agriculture, Agricultural Research ServiceLas CrucesUSA
  2. 2.Arthropod-Borne Animal Diseases Research Unit, Center for Grain and Animal Health ResearchUS Department of Agriculture, Agricultural Research ServiceManhattanUSA
  3. 3.Rangeland Resources and Systems Research UnitUS Department of Agriculture, Agricultural Research ServiceCheyenneUSA
  4. 4.Animal and Plant Health Inspection Service, Veterinary ServicesUS Department of AgricultureFort CollinsUSA
  5. 5.Foreign Animal Disease Research Unit, Plum Island Animal Disease CenterUS Department of Agriculture, Agricultural Research ServiceOrient PointUSA

Personalised recommendations