Characterization of the Long-distance Dispersal Kernel of White-Tailed Deer and Evaluating its Impact on Chronic Wasting Disease Spread in Wisconsin.

Mennatallah Gouda, Jim Powell, W Jacob McClure, Daniel P Walsh, Daniel Storm
Author Information
  1. Mennatallah Gouda: Department of Mathematics and Statistics, Utah State University, Logan, UT, 84321, USA. mennaasaad99@gmail.com.
  2. Jim Powell: Department of Mathematics and Statistics, Utah State University, Logan, UT, 84321, USA.
  3. W Jacob McClure: Department of Mathematics and Statistics, Utah State University, Logan, UT, 84321, USA.
  4. Daniel P Walsh: Wildlife Biology Program, Montana Cooperative Wildlife Research Unit, U.S. Geological Survey, University of Montana, Missoula, MT, 59812, USA.
  5. Daniel Storm: Wisconsin Department of Natural Resources, 101 S. Webster Street, Madison, WI, 53707, USA.

Abstract

Chronic wasting disease (CWD) is a fatal neurodegenerative disease infecting cervids. It is highly contagious and caused by misfolded prions that propagate via templated conformational conversion of the cervid's normal prion protein. Prevalence of CWD in free-ranging deer in North America is mostly low, but in some regions local prevalence has reached 80%. CWD prions can be transmitted via direct contact with infected individuals or indirectly through the environment. Infected individuals shed prions through feces, urine, saliva or carcasses, and prions have long environmental persistence. Long-distance dispersal of infected deer poses a significant risk for CWD spread. We propose an integrodifference equation (IDE) model to capture CWD dynamics and the consequences of long-distance dispersal behavior in white-tailed deer (WTD, Odocoileus virginianus). A diffusion-settling model characterizes long-distance dispersal kernels, accommodating hypothetical dispersal behaviors through time-dependent settling rate functions. Three new closed-form dispersal kernels are approximated using Laplace's method and parameterized with GPS location data collected from WTD in Wisconsin, USA. Settling rates reflecting ongoing sensitivity to stimuli which prompt deer to disperse from their natal home range give the most supported long-distance dispersal kernel. Impact of long-distance dispersal on CWD spread is quantified using the IDE model. At high population densities, long-distance dispersal can magnify CWD spread by a factor of four. At lower population densities single infected individuals cannot initiate an outbreak, but CWD may still spread due to the accumulation of environmental hazard from prions behind the wave of invasion, possibly presenting substantial management challenges.

Keywords

References

  1. Allen LJ, Ernest RK (2002) The impact of long-range dispersal on the rate of spread in population and epidemic models. IMA Vol Math Its Appl 125:183���198
  2. Baeten LA, Powers BE, Jewell JE, Spraker TR, Miller MW (2007) A natural case of chronic wasting disease in a free-ranging moose (Alces alces shirasi). J Wildl Dis 43(2):309���314. https://doi.org/10.7589/0090-3558-43.2.309 [DOI: 10.7589/0090-3558-43.2.309]
  3. Bartz JC, Benavente R, Caughey B, Christensen S, Herbst A, Hoover EA, the NC1209: North American Interdisciplinary Chronic Wasting Disease Research Consortium Members. (2024). Chronic wasting disease: state of the science. Retrieved from https://www.mdpi.com/2076-0817/13/2/138
  4. Benestad SL, Mitchell G, Simmons M, Ytrehus B, Vik��ren T (2016) First case of chronic wasting disease in Europe in a Norwegian free-ranging reindeer. Vet Res 47(1):88. https://doi.org/10.1186/s13567-016-0375-4 [DOI: 10.1186/s13567-016-0375-4]
  5. Centers for Disease Control and Prevention (2021). Prion Diseases. Retrieved September 2. 2022, from https://www.cdc.gov/prions/index.html
  6. Denkers ND, Hoover CE, Davenport KA, Henderson DM, McNulty EE, Nalls AV, Mathiason CK, Hoover EA (2020) Very low oral exposure to prions of brain or saliva origin can transmit chronic wasting disease. PLoS ONE. https://doi.org/10.1371/journal.pone.0237410 [DOI: 10.1371/journal.pone.0237410]
  7. Edmunds DR, Kauffman MJ, Schumaker BA, Lindzey FG, Cook WE, Kreeger TJ, Grogan RG, Cornish TE (2016) Chronic wasting disease drives population decline of white-tailed deer. PLoS ONE. https://doi.org/10.1371/journal.pone.0161127 [DOI: 10.1371/journal.pone.0161127]
  8. Eghiaian F, Grosclaude J, Lesceu S, Debey P, Doublet B, Tr��guer E, Rezaei H, Knossow M (2004) Insight into the PrPC���>PrPSc conversion from the structures of antibody-bound ovine prion scrapie-susceptibility variants. Proc Natl Acad Sci USA 101(28):10254���10259. https://doi.org/10.1073/pnas.0400014101 [DOI: 10.1073/pnas.0400014101]
  9. Garlick MJ, Powell JA, Hooten MB, McFarlane LR (2011) 44 Homogenization of large-scale movement models in ecology. Bull Math Biol 73(9):2088���2108. https://doi.org/10.1007/s11538-0109612-6 [DOI: 10.1007/s11538-0109612-6]
  10. Garlick MJ, Powell JA, Hooten MB, MacFarlane LR (2014) Homogenization, sex, and differential motility predict spread of chronic wasting disease in mule deer in southern Utah. J Math Biol 69(2):369���399. https://doi.org/10.1007/s00285-013-0709-z [DOI: 10.1007/s00285-013-0709-z]
  11. Georgsson G, Sigurdarson S, Brown P (2006) Infectious agent of sheep scrapie may persist in the environment for at least 16 years. J Gen Virol 87(12):3737���3740. https://doi.org/10.1099/vir.0.82011-0 [DOI: 10.1099/vir.0.82011-0]
  12. Gilbertson MLJ, Ketz A, Hunsaker M, Jarosinski D, Ellarson W, Walsh DP, Storm DJ, Turner WC (2022) Agricultural land use shapes dispersal in white-tailed deer (Odocoileus virginianus). Mov Ecol 10:43. https://doi.org/10.1186/s40462-022-00342-5 [DOI: 10.1186/s40462-022-00342-5]
  13. Haley NJ, Seelig DM, Zabel MD, Telling GC, Hoover EA (2009) Detection of CWD prions in urine and saliva of deer by transgenic mouse bioassay. PLoS ONE. https://doi.org/10.1371/journal.pone.0004848 [DOI: 10.1371/journal.pone.0004848]
  14. Hefley TJ, Hooten MB, Russell RE, Walsh DP, Powell JA (2017) When mechanism matters: Bayesian forecasting using models of ecological diffusion. In Ecology Letters (Vol. 20, Issue 5, pp. 640���650). Blackwell Publishing Ltd. https://doi.org/10.1111/ele.12763
  15. Jacobson KH, Lee S, McKenzie D, Benson CH, Pedersen JA (2009) Transport of the pathogenic prion protein through landfill materials. Environ Sci Technol 43(6):2022���2028. https://doi.org/10.1021/es802632d45 [DOI: 10.1021/es802632d45]
  16. Jennelle CS, Henaux V, Wasserberg G, Thiagarajan B, Rolley RE, Samuel MD (2014) Transmission of chronic wasting disease in Wisconsin white-tailed deer: implications for disease spread and management. PLoS ONE. https://doi.org/10.1371/journal.pone.0091043 [DOI: 10.1371/journal.pone.0091043]
  17. Johnson CJ, Phillips KE, Schramm PT, McKenzie D, Aiken JM, Pedersen JA (2006) Prions adhere to soil minerals and remain infectious. PLoS Pathog 2(4):e32. https://doi.org/10.1371/journal.ppat.0020032 [DOI: 10.1371/journal.ppat.0020032]
  18. Johnson CJ, Pedersen JA, Chappell RJ, McKenzie D, Aiken JM (2007) Oral transmissibility of prion disease is enhanced by binding to soil particles. PLoS Pathog 3(7):e93. https://doi.org/10.1371/journal.ppat.0030093 [DOI: 10.1371/journal.ppat.0030093]
  19. Kocisko DA, Come JH, Priola SA, Chesebro B, Raymond GJ, Lansbury PT, Caughey B (1994) Cell-free formation of protease-resistant prion protein. Nature 370(6489):471���474. https://doi.org/10.1038/370471a0 [DOI: 10.1038/370471a0]
  20. Logan J (2013) Applied mathematics, 4th edn. John Wiley and Sons Inc., Hoboken, New Jersey
  21. Lutz CL, Diefenbach DR, Rosenberry CS (2015) Population density influences dispersal in female white-tailed deer. J Mammal 96(3):494���501. https://doi.org/10.1093/jmammal/gyv054 [DOI: 10.1093/jmammal/gyv054]
  22. Mathiason CK, Powers JG, Dahmes SJ, Osborn DA, Miller KV, Warren RJ, Mason GL, Hays SA, Hayes-Klug J, Seelig DM, Wild MA, Wolfe LL, Spraker TR, Miller MW, Sigurdson CJ, Telling GC, Hoover EA (2006) Infectious prions in the saliva and blood of deer with chronic wasting disease. Science (New York, N.y.) 314(5796):133���136. https://doi.org/10.1126/science.1132661 [DOI: 10.1126/science.1132661]
  23. May RM (1978) Host-parasitoid systems in patchy environments: a phenomenological model. J Animal Ecol 47:833���844 [DOI: 10.2307/3674]
  24. McGahan I, Powell J, Spencer E (2021) 28 Models later: model competition and the zombie apocalypse. Bull Math Biol 83(3):22. https://doi.org/10.1007/s11538-020-00845-5 [DOI: 10.1007/s11538-020-00845-5]
  25. Medlock J, Kot M (2003) Spreading disease: integro-differential equations old and new. Math Biosci 182(2):201���222. https://doi.org/10.1016/S0025-5564(03)00041-5 [DOI: 10.1016/S0025-5564(03)00041-5]
  26. Miller MW, Williams ES (2003) Prion disease: horizontal prion transmission in mule deer. Nature 425(6953):35���36. https://doi.org/10.1038/425035a [DOI: 10.1038/425035a]
  27. Miller MW, Williams ES, Hobbs NT, Wolfe LL (2004) Environmental sources of prion transmission in mule deer. Emerg Infect Dis 10(6):1003���1006. https://doi.org/10.3201/eid1006.040010 [DOI: 10.3201/eid1006.040010]
  28. Miller MW, Hobbs NT, Tavener SJ (2006) Dynamics of prion disease transmission in mule deer. Ecol Appl 16(6):2208���2214. https://doi.org/10.1890/1051-0761(2006)016[2208:DOPDTI]2.0.CO;2 [DOI: 10.1890/1051-0761(2006)016[2208]
  29. Neupane RC, Powell JA (2015) Mathematical model of seed dispersal by frugivorous birds and migration potential of pinyon and juniper in Utah. Appl Math 06(09):1506���1523. https://doi.org/10.4236/am.2015.69135 [DOI: 10.4236/am.2015.69135]
  30. Neupane RC, Powell JA, Edwards TC (2021) Connecting regional-scale tree distribution models with seed dispersal kernels. Appl Math Comput. https://doi.org/10.1016/j.amc.2021.126591 [DOI: 10.1016/j.amc.2021.126591]
  31. O���Rourke KI, Spraker TR, Hamburg LK, Besser TE, Brayton KA, Knowles DP (2004) Polymorphisms in the prion precursor functional gene but not the pseudogene are associated with susceptibility to chronic wasting disease in white-tailed deer. J Gen Virol 85(5):1339���1346. https://doi.org/10.1099/vir.0.79785-0 [DOI: 10.1099/vir.0.79785-0]
  32. Pan KM, Baldwin M, Nguyen J, Gasset M, Serban A, Groth D, Mehlhorn I, Huang Z, Fletterick RJ, Cohen FE (1993) Conversion of alpha-helices into beta-sheets features in the formation of the scrapie prion proteins. Proc Natl Acad Sci USA 90(23):10962���10966. https://doi.org/10.1073/pnas.90.23.10962 [DOI: 10.1073/pnas.90.23.10962]
  33. Pritzkow S, Morales R, Moda F, Khan U, Telling GC, Hoover E, Soto C (2015) Grass plants bind, retain, uptake, and transport infectious prions. Cell Rep 11(8):1168���1175. https://doi.org/10.1016/j.celrep.2015.04.036 [DOI: 10.1016/j.celrep.2015.04.036]
  34. Safar J, Roller PP, Gajdusek DC, Gibbs CJ (1993) Conformational transitions, dissociation, and unfolding of scrapie amyloid (prion) protein. J Biol Chem 268(27):20276���20284. https://doi.org/10.1016/s0021-9258(20)80725-x [DOI: 10.1016/s0021-9258(20)80725-x]
  35. Safar JG, Lessard P, Tamg��ney G, Freyman Y, Deering C, Letessier F, DeArmond SJ, Prusiner SB (2008) Transmission and detection of prions in feces. J Infectious Diseases 198(1):81���89 [DOI: 10.1086/588193]
  36. Sigurdson CJ, Williams ES, Miller MW, Spraker TR, O���Rourke KI, Hoover EA (1999) Oral transmission and early lymphoid tropism of chronic wasting disease PrPres in mule deer fawns (Odocoileus hemionus). J Gen Virol 80(10):2757���2764. https://doi.org/10.1099/0022-1317-80-10-2757 [DOI: 10.1099/0022-1317-80-10-2757]
  37. Skuldt LH, Mathews NE, Oyer AM (2008) White-tailed deer movements in a chronic wasting disease area in South-Central Wisconsin. J Wildl Manag 72(5):1156���1160. https://doi.org/10.2193/2006-469 [DOI: 10.2193/2006-469]
  38. Tamg��ney G, Miller MW, Wolfe LL, Sirochman TM, Glidden DV, Palmer C, Lemus A, Dearmond SJ, Prusiner SB (2009) Asymptomatic deer excrete infectious prions in faeces. Nature 461(7263):529���532. https://doi.org/10.1038/nature08289 [DOI: 10.1038/nature08289]
  39. Tamg��ney G, Richt JA, Hamir AN, Greenlee JJ, Miller MW, Wolfe LL, Sirochman TM, Young AJ, Glidden DV, Johnson NL, Giles K, DeArmond SJ, Prusiner SB (2012) Salivary prions in sheep and deer. Prion 6(1):52���61. https://doi.org/10.4161/pri.6.1.16984 [DOI: 10.4161/pri.6.1.16984]
  40. U.S. Geological Survey: USGS (2024). Expanding distribution of chronic wasting disease. Retrieved from www.usgs.gov website: https://www.usgs.gov/centers/nwhc/science/expanding-distribution-chronic-wasting-disease
  41. Williams ES (2005) Chronic wasting disease. Vet Pathol 42(5):530���549. https://doi.org/10.1354/vp.42-5-530 [DOI: 10.1354/vp.42-5-530]
  42. Williams ES, Miller MW (2002) Chronic wasting disease in deer and elk in North America. Revue Scientifique Et Technique (International Office of Epizootics) 21(2):305���316. https://doi.org/10.20506/rst.21.2.1340 [DOI: 10.20506/rst.21.2.1340]
  43. Williams ES, Young S (1982) Spongiform encephalopathy of rocky mountain elk. J Wildl Dis 18(4):465���471. https://doi.org/10.7589/0090-3558-18.4.465 [DOI: 10.7589/0090-3558-18.4.465]
  44. Williams ES, Young S (1992) Spongiform encephalopathies in cervidae. Revue Scientifique Et Technique De L���OIE 11(2):551���567. https://doi.org/10.20506/rst.11.2.611 [DOI: 10.20506/rst.11.2.611]
  45. Wisconsin Department of Natural Resources [WIDNR] (2002). Arrival of CWD in Wisconsin biggest natural resources story of 2002. Chronic wasting disease alliance. https://cwd-info.org/arrival-of-cwd-in-wisconsin-biggest-natural-resources-story-of-2002/
  46. Wisconsin Department of Natural Resources [WIDNR] (2022). Deer health ��� disease. Retrieved October 10. 2022, from Deer Statistics (wi.gov)
  47. Wojcik R, Eichel J, Bradley JA, Benning LG (2021) How allogenicfactors affect succession in glacier forefields. Earth-Sci Rev 218:103642 [DOI: 10.1016/j.earscirev.2021.103642]
  48. Wright C, Howard A, Lim S, Lakshman P, Loo C (2018) PrPc: the normal prion. FASEB J 32:794.8. https://doi.org/10.1096/fasebj.2018.32.1_supplement.794.8 [DOI: 10.1096/fasebj.2018.32.1_supplement.794.8]
  49. Zabel M, Ortega A (2017) The ecology of prions. Microbiol Mol Biol Rev 81(3):e00001-17. https://doi.org/10.1128/MMBR.00001-17 [DOI: 10.1128/MMBR.00001-17]

Grants

  1. G21AC10553/U.S. Geological Survey
  2. 2022-67015-38060/National Institute of Food and Agriculture

MeSH Term

Wasting Disease, Chronic
Animals
Deer
Wisconsin
Mathematical Concepts
Models, Biological
Prevalence
Prions
Computer Simulation
Animal Distribution
Epidemiological Models

Chemicals

Prions

Word Cloud

Created with Highcharts 10.0.0dispersalCWDprionslong-distancedeerspreadChronicdiseaseinfectedindividualsLong-distancemodelkernelswastingviacanenvironmentalequationIDEWTDusingWisconsinImpactpopulationdensitiesDispersalfatalneurodegenerativeinfectingcervidshighlycontagiouscausedmisfoldedpropagatetemplatedconformationalconversioncervid'snormalprionproteinPrevalencefree-rangingNorthAmericamostlylowregionslocalprevalencereached80%transmitteddirectcontactindirectlyenvironmentInfectedshedfecesurinesalivacarcasseslongpersistenceposessignificantriskproposeintegrodifferencecapturedynamicsconsequencesbehaviorwhite-tailedOdocoileusvirginianusdiffusion-settlingcharacterizesaccommodatinghypotheticalbehaviorstime-dependentsettlingratefunctionsThreenewclosed-formapproximatedLaplace'smethodparameterizedGPSlocationdatacollectedUSASettlingratesreflectingongoingsensitivitystimulipromptdispersenatalhomerangegivesupportedkernelquantifiedhighmagnifyfactorfourlowersingleinitiateoutbreakmaystilldueaccumulationhazardbehindwaveinvasionpossiblypresentingsubstantialmanagementchallengesCharacterizationKernelWhite-TailedDeerEvaluatingWastingDiseaseSpreadIntegrodifference

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