Skip to main content
Log in

Spatiotemporal Model of Barley and Cereal Yellow Dwarf Virus Transmission Dynamics with Seasonality and Plant Competition

  • Original Article
  • Published:
Bulletin of Mathematical Biology Aims and scope Submit manuscript

Abstract

Many generalist pathogens are influenced by the spatial distributions and relative abundances of susceptible host species. The spatial structure of host populations can influence patterns of infection incidence (or disease outbreaks), and the effects of a generalist pathogen on host community dynamics in a spatially heterogeneous community may differ from predictions derived via simple models. In this paper, we model the transmission of a generalist pathogen within a patch framework that incorporates the movement of vectors between discrete host patches to investigate the effects of local host community composition and vector movement rates on disease dynamics.

We use barley and cereal yellow dwarf viruses (B/CYDV), a suite of generalist, aphid-vectored pathogens of grasses, and their interactions with a range of host species as our case study. We examine whether B/CYDV can persist locally or in a patch framework across a range of host community configurations. We then determine how pathogen-mediated interactions between perennial and annual competitors are altered at the local and regional scale when the host populations are spatially structured. We find that the spatial configuration of the patch system, host composition within patches, and patch connectivity affect not only the ability of the pathogen to invade a fragmented system, but also determine whether the pathogen facilitates the invasion of a non-native host species. Further, our results suggest that connectivity can interact with arrival time and host infection tolerance to determine the success or failure of establishment for newly arriving species.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Allan, B., Langerhans, R., Ryberg, W., Landesman, W., Griffin, N., Katz, R., Oberle, B., Schutzenhofer, M., Smyth, K., de St. Maurice, A., Clark, L., Crooks, K., Hernandez, D., McLean, R., Ostfeld, R., Chase, J. (2009). Ecological correlates of risk and incidence of west Nile virus in the united states. Oecologia, 158(4), 699–708.

    Article  Google Scholar 

  • Allan, B. F., Keesing, F., & Ostfeld, R. S. (2003). Effect of forest fragmentation on Lyme disease risk. Conserv. Biol., 17(1), 267–272.

    Article  Google Scholar 

  • Arino, J. (2009). Diseases in metapopulations. In: Series in contemporary applied mathematics: Vol. 11, Modeling and dynamics of infectious diseases (pp. 65–123).

    Google Scholar 

  • Arino, J., Davis, J. R., Hartley, D., Jordan, R., Miller, J. M., & van den Driessche, P. (2005). A multi-species epidemic model with spatial dynamics. Math. Med. Biol., 22(2), 129–142.

    Article  MATH  Google Scholar 

  • Arino, J., & van den Driessche, P. (2006). Disease spread in metapopulations. Fields Inst. Commun., 48, 1–12.

    Google Scholar 

  • Begon, M., Bowers, R. G., Kadianakis, N., & Hodgkinson, D. E. (1992). Disease and community structure: the importance of host self-regulation in a host-host-pathogen model. Am. Nat., 139(6), 1131–1150.

    Article  Google Scholar 

  • Borer, E. T., Adams, V. T., Engler, G. A., Adams, A. L., Schumann, C. B., & Seabloom, E. W. (2009). Aphid fecundity and grassland invasion: invader life history is the key. Ecol. Appl., 19(5), 1187–1196.

    Article  Google Scholar 

  • Borer, E. T., Hosseini, P. R., Seabloom, E. W., & Dobson, A. P. (2007). Pathogen-induced reversal of native dominance in a grassland community. Proc. Natl. Acad. Sci. USA, 104(13), 5473.

    Article  Google Scholar 

  • Bowers, R. G., & Turner, J. (1997). Community structure and the interplay between interspecific infection and competition. J. Theor. Biol., 187(1), 95–109.

    Article  Google Scholar 

  • Brownstein, J. S., Skelly, D. K., Holford, T. R., & Fish, D. (2005). Forest fragmentation predicts local scale heterogeneity of Lyme disease risk. Oecologia, 146(3), 469–475.

    Article  Google Scholar 

  • Buskirk, J. V., & Ostfeld, R. S. (1998). Habitat heterogeneity, dispersal, and local risk of exposure to Lyme disease. Ecol. Appl., 8(2), 365–378.

    Article  Google Scholar 

  • Case, T. J. (1990). Invasion resistance arises in strongly interacting species-rich model competition communities. Proc. Natl. Acad. Sci. USA, 87(24), 9610.

    Article  MATH  Google Scholar 

  • Chase, J. M., Abrams, P. A., Grover, J. P., Diehl, S., Chesson, P., Holt, R. D., Richards, S. A., Nisbet, R. M., & Case, T. J. (2002). The interaction between predation and competition: a review and synthesis. Ecol. Lett., 5(2), 302–315.

    Article  Google Scholar 

  • Chitnis, N., Hyman, J. M., & Cushing, J. M. (2008). Determining important parameters in the spread of malaria through the sensitivity analysis of a mathematical model. Bull. Math. Biol., 70(5), 1272–1296.

    Article  MathSciNet  MATH  Google Scholar 

  • Condeso, T. E., & Meentemeyer, R. K. (2007). Effects of landscape heterogeneity on the emerging forest disease sudden oak death. Ecology, 95, 364–375.

    Article  Google Scholar 

  • Cronin, J. P., Welsh, M. E., Dekkers, M. G., Abercrombie, S. T., & Mitchell, C. E. (2010). Host physiological phenotype explains pathogen reservoir potential. Ecol. Lett., 13(10), 1221–1232.

    Article  Google Scholar 

  • de Castro, F., & Bolker, B. (2005). Mechanisms of disease-induced extinction. Ecol. Lett., 8(1), 117–126.

    Article  Google Scholar 

  • Dobson, A. (2004). Population dynamics of pathogens with multiple host species. Am. Nat., 164, S65–S78 (supplement).

    Article  Google Scholar 

  • Fabre, F., Pierre, J. S., Dedryver, C. A., & Plantegenest, M. (2006). Barley yellow dwarf disease risk assessment based on Bayesian modelling of aphid population dynamics. Ecol. Model., 193(3–4), 457–466.

    Article  Google Scholar 

  • Grenfell, B., & Harwood, J. (1997). (Meta) population dynamics of infectious diseases. Trends Ecol. Evol., 12(10), 395–399.

    Article  Google Scholar 

  • Hanski, I. (1998). Metapopulation dynamics. Nature, 396(6706), 41–49.

    Article  Google Scholar 

  • Hatcher, M. J., Dick, J. T. A., & Dunn, A. M. (2006). How parasites affect interactions between competitors and predators. Ecol. Lett., 9(11), 1253–1271.

    Article  Google Scholar 

  • Hess, G. (1996). Disease in metapopulation models: implications for conservation. Ecology, 77(5), 1617–1632.

    Article  Google Scholar 

  • Hess, G. R. (1994). Conservation corridors and contagious disease: a cautionary note. Conserv. Biol., 8(1), 256–262.

    Article  Google Scholar 

  • Hess, G. R., Randolph, S. E., Arneberg, P., Chemini, C., Furlanello, C., Harwood, J., Roberts, M. G., & Swinton, J. (2002). Spatial aspects of disease dynamics. In The ecology of wildlife diseases (pp. 102–118). Oxford: Oxford University Press.

    Google Scholar 

  • Holmes, E. E. (1997). Basic epidemiological concepts in a spatial context. In Spatial ecology: the role of space in population dynamics and interspecific interactions (pp. 111–136).

    Google Scholar 

  • Holt, R. D., Dobson, A. P., Begon, M., Bowers, R. G., & Schauber, E. (2003). Parasite establishment and persistence in multi-host-species systems. Ecol. Lett., 6, 837–842.

    Article  Google Scholar 

  • Holt, R. D., & Dobson, A. P. (2006). Disease ecology: community structure and pathogen dynamics. In Extending the principles of community ecology to address the epidemiology of host-pathogen systems.

    Google Scholar 

  • Holt, R. D., & Pickering, J. (1985). Infectious disease and species coexistence: a model of Lotka-Volterra form. Am. Nat., 126(2), 196–211.

    Article  Google Scholar 

  • Irwin, M. E., & Thresh, J. M. (1990). Epidemiology of barley yellow dwarf: a study in ecological complexity. Annu. Rev. Phytopathol., 28(1), 393–424.

    Article  Google Scholar 

  • Irwin, M. E., Thresh, J. M., & Harrison, B. D. (1988). Long-range aerial dispersal of cereal aphids as virus vectors in North America (and Discussion). Philos. Trans. R. Soc. Lond. B, Biol. Sci., 321(1207), 421–446.

    Article  Google Scholar 

  • Jeger, M. J., Pautasso, M., Holdenrieder, O., & Shaw, M. W. (2007). Modelling disease spread and control in networks: implications for plant sciences. New Phytol., 174(2), 279–297.

    Article  Google Scholar 

  • Keeling, M. J., Bjornstad, O. N., & Grenfell, B. T. (2004). Metapopulation dynamics of infectious diseases. In Ecology, evolution and genetics of metapopulations (pp. 415–446). Amsterdam: Elsevier.

    Chapter  Google Scholar 

  • Keeling, M. J., Woolhouse, M. E. J., Shaw, D. J., Matthews, L., Chase-Topping, M., Haydon, D. T., Cornell, S. J., Kappey, J., Wilesmith, J., & Grenfell, B. T. (2001). Dynamics of the 2001 UK foot and mouth epidemic: stochastic dispersal in a heterogeneous landscape. Science, 294(5543), 813.

    Article  Google Scholar 

  • Keesing, F., Holt, R. D., & Ostfeld, R. S. (2006). Effects of species diversity on disease risk. Ecol. Lett., 9(4), 485–498.

    Article  Google Scholar 

  • Kendall, D. A., Brain, P., & Chinn, N. E. (1992). A simulation model of the epidemiology of barley yellow dwarf virus in winter sown cereals and its application to forecasting. J. Appl. Ecol., 29(2), 414–426.

    Article  Google Scholar 

  • Knops, J. M. H., Tilman, D., Haddad, N. M., Naeem, S., Mitchell, C. E., Haarstad, J., Ritchie, M. E., Howe, K. M., Reich, P. B., Siemann, E., et al. (1999). Effects of plant species richness on invasion dynamics, disease outbreaks, insect abundances and diversity. Ecol. Lett., 2(5), 286–293.

    Article  Google Scholar 

  • Langlois, J. P., Fahrig, L., Merriam, G., & Artsob, H. (2001). Landscape structure influences continental distribution of hantavirus in deer mice. Landsc. Ecol., 16(3), 255–266.

    Article  Google Scholar 

  • Leclercq-Le Quillec, F., Plantegenest, M., Riault, G., & Dedryver, C. A. (2000). Analyzing and modeling temporal disease progress of barley yellow dwarf virus serotypes in barley fields. Phytopathology, 90(8), 860–866.

    Article  Google Scholar 

  • Lowry, E. (2007). The role of aphid host preference in barley yellow dwarf virus epidemiology.

  • Malmstrom, C. M. (1998). Barley yellow dwarf virus in native California grasses. Grasslands, 8(1), 6–10.

    Google Scholar 

  • Malmstrom, C. M., Hughes, C. C., Newton, L. A., & Stoner, C. J. (2005a). Virus infection in remnant native bunchgrasses from invaded California grasslands. New Phytol., 168(1), 217–230.

    Article  Google Scholar 

  • Malmstrom, C. M., McCullough, A. J., Johnson, H. A., Newton, L. A., & Borer, E. T. (2005b). Invasive annual grasses indirectly increase virus incidence in California native perennial bunchgrasses. Oecologia, 145(1), 153–164.

    Article  Google Scholar 

  • McCallum, H., & Dobson, A. (2002). Disease, habitat fragmentation and conservation. Proc., Biol. Sci., 269(1504), 2041–2049.

    Article  Google Scholar 

  • McCormack, R. K. (2006). Multi-host multi-patch mathematical epidemic models for disease emergence with applications to hantavirus in wild rodents. PhD thesis, Texas Tech University.

  • McCormack, R. K., & Allen, L. J. S. (2007). Disease emergence in multi-host epidemic models. Math. Med. Biol., 24(1), 17.

    Article  MathSciNet  MATH  Google Scholar 

  • McElhany, P., Real, L. A., & Power, A. G. (1995). Vector preference and disease dynamics: a study of barley yellow dwarf virus. Ecology, 76(2), 444–457.

    Article  Google Scholar 

  • Meentemeyer, R. K., Rank, N. E., Anacker, B. L., Rizzo, D. M., & Cushman, J. H. (2008). Influence of land-cover change on the spread of an invasive forest pathogen. Ecol. Appl., 18(1), 159–171.

    Article  Google Scholar 

  • Mitchell, C. E., Tilman, D., & Groth, J. V. (2002). Effects of grassland plant species diversity, abundance, and composition on foliar fungal disease. Ecology, 83(6), 1713–1726.

    Article  Google Scholar 

  • Ostfeld, R., Keesing, F., & Eviner, V. T. (2008). Infectious disease ecology: the effects of ecosystems on disease and of disease on ecosystems. Princeton: Princeton University Press.

    Google Scholar 

  • Ostfeld, R. S., Glass, G. E., & Keesing, F. (2005). Spatial epidemiology: an emerging (or re-emerging) discipline. Trends Ecol. Evol., 20(6), 328–336.

    Article  Google Scholar 

  • Plantegenest, M., Le May, C., & Fabre, F. (2007). Landscape epidemiology of plant diseases. J. R. Soc. Interface, 4(16), 963.

    Article  Google Scholar 

  • Power, A. G., & Mitchell, C. E. (2004). Pathogen spillover in disease epidemics. Am. Nat., 164, S79–S89 (supplement).

    Article  Google Scholar 

  • Rushton, S. P., Lurz, P. W. W., Gurnell, J., & Fuller, R. (2000). Modelling the spatial dynamics of parapoxvirus disease in red and grey squirrels: a possible cause of the decline in the red squirrel in the UK? J. Appl. Ecol. (pp. 997–1012).

  • Saltelli, A., Chan, K., Scott, E. M. et al. (2004). Sensitivity analysis. New York: Wiley.

    MATH  Google Scholar 

  • Saramäki, J., & Kaski, K. (2005). Modelling development of epidemics with dynamic small-world networks. J. Theor. Biol., 234(3), 413–421.

    Article  Google Scholar 

  • Seabloom, E. W., Harpole, W. S., Reichman, O. J., & Tilman, D. (2003). Invasion, competitive dominance, and resource use by exotic and native California grassland species. Proc. Natl. Acad. Sci. USA, 100(23), 13384.

    Article  Google Scholar 

  • Seabloom, E. W., Hosseini, P. R., Power, A. G., & Borer, E. T. (2009). Diversity and composition of viral communities: coinfection of barley and cereal yellow dwarf viruses in California Grasslands. Am. Nat., 173, E79–E98.

    Article  Google Scholar 

  • Smith, D. L., Lucey, B., Waller, L. A., Childs, J. E., & Real, L. A. (2002). Predicting the spatial dynamics of rabies epidemics on heterogeneous landscapes. Proc. Natl. Acad. Sci. USA, 99(6), 3668–3672.

    Article  Google Scholar 

  • Tompkins, D. M., White, A. R., & Boots, M. (2003). Ecological replacement of native red squirrels by invasive greys driven by disease. Ecol. Lett., 6(3), 189–196.

    Article  Google Scholar 

  • van den Driessche, P., & Watmough, J. (2002). Reproduction numbers and sub-threshold endemic equilibria for compartmental models of disease transmission. Math. Biosci., 180(1), 29–48.

    Article  MathSciNet  MATH  Google Scholar 

  • Zhang, X. S., & Holt, J. (2001). Mathematical models of cross protection in the epidemiology of plant-virus diseases. Phytopathology, 91(10), 924–934.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to C. A. Manore.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Moore, S.M., Manore, C.A., Bokil, V.A. et al. Spatiotemporal Model of Barley and Cereal Yellow Dwarf Virus Transmission Dynamics with Seasonality and Plant Competition. Bull Math Biol 73, 2707–2730 (2011). https://doi.org/10.1007/s11538-011-9654-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11538-011-9654-4

Keywords

Navigation