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Integrating Landscape Hierarchies in the Discovery and Modeling of Ecological Drivers of Zoonotically Transmitted Disease from Wildlife

  • Douglas G. Goodin
  • Colleen B. Jonsson
  • Linda J. S. Allen
  • Robert D. Owen
Chapter
Part of the Advances in Environmental Microbiology book series (AEM, volume 5)

Abstract

Changes in landscape and land use can drive the emergence of zoonoses, and hence, there has been great interest in understanding how land cover change and the cascade of ecological effect associated with it are associated with emerging infectious diseases. In this chapter, we review how a spatially hierarchical approach can be used to guide research into the links between landscape properties and zoonotic diseases. Methodological advances have played a role in the revival of landscape epidemiology and we introduce the role of methodologies such as geospatial analysis and mathematical modeling. Importantly, we discuss cross-scale analysis and how this would provide a richer perspective of the ecology of zoonotic diseases. Finally, we will provide an overview of how hierarchical research strategies and modeling might be generally used in analyses of infectious zoonoses originating in wildlife.

Keywords

Hantaviruses Spill over Wildlife reservoirs Zoonoses Zoonotic RNA viruses Virus ecology Rodent borne viruses Landscape and the above 

Notes

Acknowledgments

CBJ and LJSA acknowledge the support of the National Science Foundation Grants (NSF) DMS-1516011 and DMS-1517719. CBJ and RDO acknowledge the support of the National Institutes of Health Grant (NIH) I103053. CBJ, LJSA, RDO, and DG acknowledge support from NIH R01 TW006986-01 through the NIH-NSF Ecology of Infectious Disease Program. RDO was partially supported by the Programa Nacional de Incentivo a los Investigadores (CONACYT, Paraguay).

Compliance with Ethical Standards

Funding

This study was funded by National Science Foundation grants (DMS-1516011 and DMS-1517719) and National Institutes of Health grant (R010AI103053). This work was supported by a grant from the Fogarty International Center (R01 TW006986-01) under the NIH-NSF Ecology of Infectious Diseases initiative.

Conflict of Interest

Douglas G. Goodin declares that he has no conflict of interest. Colleen B. Jonsson declares that she has no conflict of interest. Linda J. S. Allen declares that she has no conflict of interest. Robert D. Owen declares that he has no conflict of interest.

Ethical Approval

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Abramson G, Kenkre VM (2002) Spatiotemporal patterns in the hantavirus infection. Phys Rev E Stat Nonlin Soft Matter Phys 66:011912CrossRefPubMedGoogle Scholar
  2. Abramson G, Kenkre VM, Yates TL, Parmenter RR (2003) Traveling waves of infection in the hantavirus epidemics. Bull Math Biol 65:519–534CrossRefPubMedGoogle Scholar
  3. Alexander KA, Lewis BL, Marathe M, Eubank S, Blackburn JK (2012) Modeling of wildlife-associated zoonoses: applications and caveats. Vector Borne Zoonotic Dis 12:1005–1018CrossRefPubMedPubMedCentralGoogle Scholar
  4. Allen TFH, Starr TB (eds) (1982) Hierarchy: perspectives for ecological complexity. University of Chicago Press, ChicagoGoogle Scholar
  5. Allen LJ, McCormack RK, Jonsson CB (2006a) Mathematical models for hantavirus infection in rodents. Bull Math Biol 68:511–524CrossRefPubMedGoogle Scholar
  6. Allen LJS, Allen EJ, Jonsson CB (2006b) The impact of environmental variation on hantavirus infection in rodents. In: Gumel AB, Castillo-Chavez C, Mickens RE, Clemence DP (eds) Modeling the dynamics of human diseases: emerging paradigms and challenges. AMS, Providence, RI, pp 1–15Google Scholar
  7. Allen LJS, Wesley CL, Owen RD, Goodin DG, Koch D, Jonsson CB, Chu Y-K, Hutchinson S, Paige R (2009) A habitat-based model for the spread of hantavirus between reservoir and spillover species. J Theor Biol 260:510–522CrossRefPubMedPubMedCentralGoogle Scholar
  8. Allen LJ, Brown VL, Jonsson CB, Klein SL, Laverty SM, Magwedere K, Owen JC, van den Driessche P (2012) Mathematical modeling of viral zoonoses in wildlife. Nat Resour Model 25:5–51CrossRefPubMedGoogle Scholar
  9. Arino J, Davis JR, Hartley D, Jordan R, Miller JM, van den Driessche P (2005) A multi-species epidemic model with spatial dynamics. Math Med Biol 22:129–142CrossRefPubMedGoogle Scholar
  10. Ashcroft MB, Chisholm LA, French KO (2009) Climate change at the landscape scale: predicting fine-grained spatial heterogeneity in warming and potential refugia for vegetation. Global Change Biol 15:656–667CrossRefGoogle Scholar
  11. Bohlman MC, Morzunov SP, Meissner J, Taylor MB, Ishibashi K, Rowe J, Levis S, Enria D, St Jeor SC (2002) Analysis of hantavirus genetic diversity in Argentina: S segment-derived phylogeny. J Virol 76:3765–3773CrossRefPubMedPubMedCentralGoogle Scholar
  12. Brownstein JS, Skelly DK, Holford TR, Fish D (2005) Forest fragmentation predicts local scale heterogeneity of Lyme disease risk. Oecologia 146:469–475CrossRefPubMedGoogle Scholar
  13. Buhnerkempe MG, Roberts MG, Dobson AP, Heesterbeek H, Hudson PJ, Lloyd-Smith JO (2015) Eight challenges in modelling disease ecology in multi-host, multi-agent systems. Epidemics 10:26–30CrossRefPubMedGoogle Scholar
  14. Chu YK, Milligan B, Owen RD, Goodin DG, Jonsson CB (2006) Phylogenetic and geographical relationships of hantavirus strains in Eastern and Western Paraguay. Am J Trop Med Hyg 75:1127–1134PubMedPubMedCentralCrossRefGoogle Scholar
  15. Chu YK, Goodin D, Owen RD, Koch D, Jonsson CB (2009) Sympatry of two hantavirus strains, Paraguay, 2003-2007. Emerg Infect Dis 15:1977–1980CrossRefPubMedPubMedCentralGoogle Scholar
  16. Csillag F, Fortin M-J, Dungan JL (2000) On the limits and extensions of the definition of scale. Bull Ecol Soc Am 81:230–232Google Scholar
  17. De Araujo J, Duré AIL, Negrão R, Ometto T, Thomazelli LM, Durigon EL (2015) Co-circulation in a single biome of the Juquitiba and Araraquara hantavirus detected in human sera in a sub-tropical region of Brazil. J Med Virol 87:725–732CrossRefPubMedGoogle Scholar
  18. De Beurs KM, Henebry GM (2004) Land surface phenology, climatic variation, and institutional change: analyzing agricultural land cover change in Kazakhstan. Remote Sens Environ 8:497–509CrossRefGoogle Scholar
  19. de Oliveira RC, Padula PJ, Gomes R, Martinez VP, Bellomo C, Bonvicino CR, Freire E Lima DI, Bragagnolo C, Caldas ACS, D’Andrea PS, de Lemos ERS (2011) Genetic characterization of hantaviruses associated with sigmodontine rodents in an endemic area for hantavirus pulmonary syndrome in southern Brazil. Vector Borne Zoonotic Dis 11:301CrossRefPubMedGoogle Scholar
  20. de Sousa RL, Moreli ML, Borges AA, Campos GM, Livonesi MC, Figueiredo LT, Pinto AA (2008) Natural host relationships and genetic diversity of rodent-associated hantaviruses in Southeastern Brazil. Intervirology 51:299–310CrossRefPubMedGoogle Scholar
  21. Delfraro A, Tomé L, D’Elía G, Clara M, Achával F, Russi JC, Rodonz JRA (2008) Juquitiba-like hantavirus from 2 nonrelated rodent species, Uruguay. Emerg Infect Dis 14:1447–1451CrossRefPubMedPubMedCentralGoogle Scholar
  22. Diffenbaugh NS, Pal JS, Trapp RJ, Giorgi F (2005) Fine-scale processes regulate the response of extreme events to global climate change. Proc Natl Acad Sci U S A 102:15774–15778CrossRefPubMedPubMedCentralGoogle Scholar
  23. Dobson A (2004) Population dynamics of pathogens with multiple host species. Am Nat 164(Suppl 5):S64–S78CrossRefPubMedGoogle Scholar
  24. Epstein JH, Field HE, Luby S, Pulliam JR, Daszak P (2006) Nipah virus: impact, origins, and causes of emergence. Curr Infect Dis Rep 8:59–65CrossRefPubMedGoogle Scholar
  25. Estrada-Peña A, Oteo JA (1991) Vectors of Lyme disease in Spain. Res Rev Parasitol 51:101–102Google Scholar
  26. Estrada-Peña A, Venzal JM, Acebedo Sanchez C (2006) The tick Ixodes ricinus: distribution and climate preferences in the Western Palaearctic. Med Vet Entomol 20:350–359CrossRefGoogle Scholar
  27. Feng Z, Velasco-Hernandez J, Tapia-Santos B (2013) A mathematical model for coupling within-host and between-host dynamics in an environmentally-driven infectious disease. Math Biosci 241:49–55CrossRefPubMedGoogle Scholar
  28. Fulhorst CF, Cajimat MNB, Utrera A, Milazzo ML, Duno GM (2004) Maporal virus, a hantavirus associated with the fulvous pygmy rice rat (Oligoryzomys fulvescens) in Western Venezuela. Virus Res 104:139–144CrossRefPubMedGoogle Scholar
  29. Gilchrist MA, Coombs D (2006) Evolution of virulence: interdependence, constraints, and selection using nested models. Theor Popul Biol 69:145–153CrossRefPubMedGoogle Scholar
  30. Giraudoux P, Craig PS, Delattre P, Bartholomot B, Harraga S, Quere JP, Raoul F, Wang Y, Shi D, Vuitton DA (2003) Interactions between landscape changes and host communities can regulate Echinococcus multilocularis transmission. Parasitology 127:121–131CrossRefGoogle Scholar
  31. Glass GE, Cheek JE, Patz JA, Shields TM, Doyle TJ, Thoroughman DA, Hunt DK, Enscore RE, Gage KL, Irland C, Peters CJ, Bryan R (2000) Using remotely sensed data to identify areas at risk for hantavirus pulmonary syndrome. Emerg Infect Dis 6:238–247CrossRefPubMedPubMedCentralGoogle Scholar
  32. Glass GE, Yates TL, Fine JB, Shields TM, Kendall JB, Hope AG, Parmenter CA, Peters CJ, Ksiazek TG, Li CS, Patz JA, Mills JN (2002) Satellite imagery characterizes local animal reservoir populations of Sin Nombre virus in the Southwestern United States. Proc Natl Acad Sci U S A 99:16817–16822CrossRefPubMedPubMedCentralGoogle Scholar
  33. González-Ittig RE, Rivera PC, Levis SC, Calderón GE, Gardenal CN (2014) The molecular phylogenetics of the genus Oligoryzomys (Rodentia: C ricetidae) clarifies rodent host–hantavirus associations. Zool J Linnean Soc 171:457–474CrossRefGoogle Scholar
  34. Goodin DG, Koch DE, Owen RD, Chu Y-K, Hutchinson JMS, Jonsson CB (2006) Land cover associated with hantavirus presence in Paraguay. Global Ecol Biogeogr 15:519CrossRefGoogle Scholar
  35. Goodin DG, Paige R, Owen RD, Ghimire K, Koch DE, Chu YK, Jonsson CB (2009) Microhabitat characteristics of Akodon montensis, a reservoir for hantavirus, and hantaviral seroprevalence in an Atlantic forest site in Eastern Paraguay. J Vector Ecol 34:104–113CrossRefPubMedGoogle Scholar
  36. Grenfell BT, Dobson AP (1995) Ecology of disease in natural populations. Cambridge University Press, Cambridge, UKCrossRefGoogle Scholar
  37. Haydon DT, Cleaveland S, Taylor LH, Laurenson MK (2002) Identifying reservoirs of infection: a conceptual and practical challenge. Emerg Infect Dis 8:1468–1473CrossRefPubMedGoogle Scholar
  38. Heesterbeek H, Anderson RM, Andreasen V, Bansal S, De Angelis D, Dye C, Eames KT, Edmunds WJ, Frost SD, Funk S, Hollingsworth TD, House T, Isham V, Klepac P, Lessler J, Lloyd-Smith JO, Metcalf CJ, Mollison D, Pellis L, Pulliam JR, Roberts MG, Viboud C, Isaac Newton Institute, I.D.D.C. (2015) Modeling infectious disease dynamics in the complex landscape of global health. Science 347:4339CrossRefGoogle Scholar
  39. Hudson PJ, Rizzoli A, Grenfell BT, Heesterbeek H, Dobson AP (2002) The ecology of wildlife diseases. Oxford University Press, OxfordGoogle Scholar
  40. Jenerette GD, Wu J (2000) On the definitions of scale. Bull Ecol Soc Am 81:104–105Google Scholar
  41. Johnson AM, Bowen MD, Ksiazek TG, Williams RJ, Bryan RT, Mills JN, Peters CJ, Nichol ST (1997) Laguna Negra Virus associated with HPS in Western Paraguay and Bolivia. Virology 238:115–127CrossRefGoogle Scholar
  42. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P (2008) Global trends in emerging infectious diseases. Nature 451:990CrossRefPubMedPubMedCentralGoogle Scholar
  43. Jones BA, Grace D, Kock R, Alonso S, Rushton J, Said MY, McKeever D, Mutua F, Young J, McDermott J, Pfeiffer DU (2013) Zoonosis emergence linked to agricultural intensification and environmental change. Proc Natl Acad Sci USA 110:8399CrossRefPubMedGoogle Scholar
  44. Jonsson CB, Figueiredo LT, Vapalahti O (2010) A global perspective on hantavirus ecology, epidemiology, and disease. Clin Microbiol Rev 23:412–441CrossRefPubMedPubMedCentralGoogle Scholar
  45. Kilgore PE, Peters CJ, Mills JN, Rollin PE, Armstrong L, Khan AS, Ksiazek TG (1995) Prospects for the control of Bolivian hemorrhagic fever. Emerg Infect Dis 1:97–100CrossRefPubMedPubMedCentralGoogle Scholar
  46. Kitron U, Clennon JA, Cecere MC, Gürtler RE, King CH, Vazquez-Prokopec G (2006) Upscale or downscale: applications of fine scale remotely sensed data to Chagas disease in Argentina and schistosomiasis in Kenya. Geospatial Health 1:49–58CrossRefPubMedPubMedCentralGoogle Scholar
  47. Langlois JP, Fahrig L, Merriam G, Artsob H (2001) Landscape structure influences continental distribution of hantavirus in deer mice. Landsc Ecol 16:255–266CrossRefGoogle Scholar
  48. Lidicker WZ (1995) Landscape approaches in mammalian ecology and conservation. University of Minnesota Press, MinneapolisGoogle Scholar
  49. Lloyd-Smith JO, George D, Pepin KM, Pitzer VE, Pulliam JR, Dobson AP, Hudson PJ, Grenfell BT (2009) Epidemic dynamics at the human-animal interface. Science 326:1362–1367CrossRefPubMedPubMedCentralGoogle Scholar
  50. Londoño AF, Díaz FJ, Agudelo-Flórez P, Levis S, Rodas JD (2011) Genetic evidence of hantavirus infections in wild rodents from northwestern Colombia. Vector Borne Zoonotic Dis 11:701CrossRefPubMedGoogle Scholar
  51. Lozada M, Guthmann N (1998) Microhabitat selection under experimental conditions of three sigmodontine rodents. Ecoscience 5:51–55CrossRefGoogle Scholar
  52. McCormack RK, Allen LJS (2007a) Disease emergence in multi-host epidemic models. Math Med Biol 24:17–34CrossRefPubMedGoogle Scholar
  53. McCormack RK, Allen LJS (2007b) Multi-patch deterministic and stochastic models for wildlife diseases. J Biol Dyn 1:63–85CrossRefPubMedGoogle Scholar
  54. McFarlane RA, Sleigh AC, McMichael AJ (2013) Land-use change and emerging infectious disease on an island continent. Int J Environ Res Public Health 10:2699–2719CrossRefPubMedPubMedCentralGoogle Scholar
  55. Meentemeyer V (1989) Geographical perspectives of space, time, and scale. Landsc Ecol 3:163–173CrossRefGoogle Scholar
  56. Meentemeyer RK, Haas SE, Vaclavik T (2012) Landscape epidemiology of emerging infectious diseases in natural and human-altered ecosystems. Annu Rev Phytopathol 50:379–402CrossRefPubMedGoogle Scholar
  57. Meyer BJ, Schmaljohn CS (2000) Persistent hantavirus infections: characteristics and mechanisms. Trends Microbiol 8:61–67CrossRefPubMedGoogle Scholar
  58. Mideo N, Alizon S, Day T (2008) Linking within- and between-host dynamics in the evolutionary epidemiology of infectious diseases. Trends Ecol Evol 23:511–517CrossRefPubMedGoogle Scholar
  59. Olson DM, Dinerstein E, Wikramanayake ED, Burgess ND, Powell GVN, Underwood EC, D’Amico JA, Itoua I, Strand HE, Morrison JC, Loucks CJ, Allnutt TF, Ricketts TH, Kura Y, Lamoreux JF, Wettengel WW, Hedao P, Kassem KR (2001) Terrestrial ecoregions of the world: a new map of life on Earth. Bioscience 51:933–938CrossRefGoogle Scholar
  60. Ostfeld RS, Glass GE, Keesing F (2005) Spatial epidemiology: an emerging (or re-emerging) discipline. Trends Ecol Evol 20:328–336CrossRefPubMedGoogle Scholar
  61. Owen RD, Goodin DG, Koch DE, Chu Y-K, Jonsson CB (2010) Spatiotemporal variation in Akodon montensis (Cricetidae: Sigmodontinae) and hantaviral seroprevalence in a subtropical forest ecosystem. J Mammal 91:467CrossRefGoogle Scholar
  62. Palma RE, Polop JJ, Owen RD, Mills JN (2012) Ecology of rodent-associated hantaviruses in the Southern Cone of South America: Argentina, Chile, Paraguay, and Uruguay. J Wildl Dis 48:267–281CrossRefPubMedGoogle Scholar
  63. Parratt SR, Numminen E, Laine A-L (2016) Infectious disease dynamics in heterogeneous landscapes. Annu Rev Ecol Evol Syst 47:281–306CrossRefGoogle Scholar
  64. Patz JA, Olson SH, Uejio CK, Gibbs HK (2008) Disease emergence from global climate and land use change. New Emerg Infect Dis 92:1473–1491Google Scholar
  65. Pavlovskiĭ EN (1966) Natural nidality of transmissible diseases, with special referece to the landscape epidemiology of zooanthroponoses. University of Illinois Press, Urbana, ILGoogle Scholar
  66. Pellis L, Ball F, Bansal S, Eames K, House T, Isham V, Trapman P (2015) Eight challenges for network epidemic models. Epidemics 10:58–62CrossRefPubMedGoogle Scholar
  67. Peterson AT (2014) Mapping disease transmission risk in geographic and ecological contexts. John Hopkins University Press, Baltimore, MDGoogle Scholar
  68. Pinzon JE, Wilson JM, Tucker CJ, Arthur R, Jahrling PB, Formenty P (2004) Trigger events: enviroclimatic coupling of Ebola hemorrhagic fever outbreaks. Am J Trop Med Hyg 71:664–674PubMedCrossRefGoogle Scholar
  69. Poindexter CJ, Schnell GD, Sánchez-Hernández C, Romero-Almaraz MdL, Kennedy ML, Best TL, Wooten MC, Owen RD (2012) Variation in habitat use of coexisting rodent species in a tropical dry deciduous forest. Mammal Biol 77:249–257CrossRefGoogle Scholar
  70. Potter KA, Woods A, Pincebourde S (2013) Microclimatic challenges in global change biology. Global Change Biol 19:2932–2939CrossRefGoogle Scholar
  71. Pulliam JR, Epstein JH, Dushoff J, Rahman SA, Bunning M, Jamaluddin AA, Hyatt AD, Field HE, Dobson AP, Daszak P, Henipavirus Ecology Research G (2012) Agricultural intensification, priming for persistence and the emergence of Nipah virus: a lethal bat-borne zoonosis. J R Soc Interface 9:89–101CrossRefPubMedGoogle Scholar
  72. Real LA, Biek R (2007) Spatial dynamics and genetics of infectious diseases on heterogeneous landscapes. J R Soc 4:935–948Google Scholar
  73. Reed BC, Schwartz MD, Xiao X (2009) Remote sensing phenology. In: Noormets A (ed) Phenology of ecosystem processes: applications in global change research. Springer, New York, NY, pp 231–246CrossRefGoogle Scholar
  74. Rees EE, Pond BA, Tinline RR, Bélanger D (2013) Modelling the effect of landscape heterogeneity on the efficacy of vaccination for wildlife infectious disease control. J Appl Ecol 50:881–891CrossRefGoogle Scholar
  75. Reisen WK (2010) Landscape epidemiology of vector-borne diseases. Annu Rev Entomol 55:461–483CrossRefPubMedGoogle Scholar
  76. Rhodes CJ, Atkinson RPD, Anderson RM, Macdonald DW (1998) Rabies in Zimbabwe: reservoir dogs and the implications for disease control. Philos Trans Soc Lond B Biol Sci 353:999–1010CrossRefGoogle Scholar
  77. Richter MH, Hanson JD, Cajimat MN, Milazzo ML, Fulhorst CF (2010) Geographical range of Rio Mamoré virus (family Bunyaviridae, genus Hantavirus) in association with the small-eared pygmy rice rat (Oligoryzomys microtis). Vector Borne Zoonotic Dis 10:613CrossRefPubMedPubMedCentralGoogle Scholar
  78. Riley S, Eames K, Isham V, Mollison D, Trapman P (2015) Five challenges for spatial epidemic models. Epidemics 10:68–71CrossRefPubMedPubMedCentralGoogle Scholar
  79. Russell CA, Real LA, Smith DL (2006) Spatial control of rabies on heterogeneous landscapes. PLoS One 1:e27CrossRefPubMedPubMedCentralGoogle Scholar
  80. Schnell GD, De Lourdes Romero-almaraz M, Martínez-chapital ST, Sánchez-hernández C, Kennedy ML, Best TL, Wooten MC, Owen RD (2010) Habitat use and demographic characteristics of the west Mexican cotton rat (Sigmodon mascotensis). Mammalia 74:379–393CrossRefGoogle Scholar
  81. Simone I, Cagnacci F, Provensal C, Polop J (2010) Environmental determinants of the small mammal assemblage in an agroecosystem of central Argentina: the role of Calomys musculinus. Mammal Biol 75:496–509CrossRefGoogle Scholar
  82. Smith DL, Lucey B, Waller LA, Childs JE, Real LA (2002) Predicting the spatial dynamics of rabies epidemics on heterogeneous landscapes. Proc Natl Acad Sci U S A 99:3668–3672CrossRefPubMedPubMedCentralGoogle Scholar
  83. Smith KF, Goldberg M, Rosenthal S, Carlson L, Chen J, Chen C, Ramachandran S (2014) Global rise in human infectious disease outbreaks. J Royal Soc 11:20140950Google Scholar
  84. Suggitt AJ, Gillingham PK, Hill JK, Huntley B, Kunin WE, Roy DB, Thomas CD (2011) Habitat microclimates drive fine-scale variation in extreme temperatures. Oikos 120:1–8CrossRefGoogle Scholar
  85. Suzuki A, Bisordi I, Levis S, Garcia J, Pereira LE, Souza RP, Sugahara TK, Pini N, Enria D, Souza LT (2004) Identifying rodent hantavirus reservoirs, Brazil. Emerg Infect Dis 10:2127–2134CrossRefPubMedPubMedCentralGoogle Scholar
  86. Torres-Perez F, Navarrete-Droguett J, Aldunate R, Yates TL, Mertz GJ, Vial PA, Ferres M, Marquet PA, Palma RE (2004) Peridomestic small mammals associated with confirmed cases of human hantavirus disease in southcentral Chile. Am J Trop Med Hyg 70:305–309PubMedCrossRefGoogle Scholar
  87. Tucker CJ, Wilson JM, Mahoney R, Anyamba A, Linthicum KJ, Myers M (2002) Climatic and ecological context of the 1994-1996 ebola outbreaks. Photogr Eng Rem Sens 68:147–152Google Scholar
  88. Vaheri A, Strandin T, Hepojoki J, Sironen T, Henttonen H, Makela S, Mustonen J (2013) Uncovering the mysteries of hantavirus infections (Disease/Disorder overview). Nat Rev Microbiol 11:539CrossRefPubMedGoogle Scholar
  89. Watts DJ, Muhamad R, Medina DC, Dodds PS (2005) Multiscale, resurgent epidemics in a hierarchical metapopulation model. Proc Natl Acad Sci U S A 102:11157CrossRefPubMedPubMedCentralGoogle Scholar
  90. Woolhouse MEJ, Gowtage-Sequeria S (2005) Host range and emerging and reemerging pathogens. Emerg Infect Dis 11:1842CrossRefPubMedPubMedCentralGoogle Scholar
  91. Wu J (1999) Hierarchy and scaling: extrapolating information along a scaling ladder. Can J Rem Sens 25:367–380CrossRefGoogle Scholar
  92. Wu J, Loucks OL (1995) From balance of nature to hierarchical patch dynamics: a paradigm shift in ecology. Q Rev Biol 70:439–466CrossRefGoogle Scholar
  93. Yahnke CJ, Meserve PL, Ksiazek TG, Mills JN (2001) Patterns of infection with Laguna Negra virus in wild populations of Calomys laucha in the central Paraguayan chaco. Am J Trop Med Hyg 65:768CrossRefPubMedGoogle Scholar
  94. Yates TL, Mills JN, Parmenter CA, Ksiazek TG, Parmenter RR, Vande Castle JR, Calisher CH, Nichol ST, Abbott KD, Young JC, Morrison ML, Beaty BJ, Dunnum JL, Baker RJ, Salazar-Bravo J, Peters CJ (2002) The ecology and evolutionary history of an emergent disease: hantavirus pulmonary syndrome. BioScience 52:989–998CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Douglas G. Goodin
    • 1
  • Colleen B. Jonsson
    • 2
  • Linda J. S. Allen
    • 3
  • Robert D. Owen
    • 4
  1. 1.Department of GeographyKansas State UniversityManhattanUSA
  2. 2.Department of Microbiology, Immunology and BiochemistryUniversity of Tennessee Health Science CenterMemphisUSA
  3. 3.Department of Mathematics and StatisticsTexas Tech UniversityLubbockUSA
  4. 4.Department of Biological SciencesTexas Tech UniversityLubbockUSA

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