European Journal of Plant Pathology

, Volume 145, Issue 2, pp 483–492 | Cite as

Identification of meteorological predictors of Fusarium graminearum ascospore release using correlation and causality analyses

  • Ray F. David
  • Amir E. BozorgMagham
  • David G. SchmaleIII
  • Shane D. Ross
  • Linsey C. Marr
Article

Abstract

Fusarium head blight (FHB), caused by the plant pathogen Fusarium graminearum, is a significant threat to small grains production worldwide. Additional knowledge is required to clarify the influence of meteorological conditions on the release of ascospores of F. graminearum. Here, a new application of causality analysis is used to determine how meteorological conditions cause ascospore release. Two types of causality analyses, convergent cross mapping and multivariate state space forecasting, were applied to field measurements of airborne ascospores of F. graminearum over two years. Convergent cross mapping identified relative humidity, solar radiation, wind speed, and air temperature as predictors of ascospore release. Multivariate state space forecasting identified solar radiation and relative humidity as effective predictors of ascospore release. Increased concentration of ascospores in the atmosphere primarily occurred during periods of high relative humidity, low solar radiation, and low wind speed. Results from this study may assist producers in managing FHB in small grains by narrowing the timing and application of fungicides around major ascospore release intervals predicted by meteorological conditions.

Keywords

Fungus Fusarium head blight Bioaerosol Causality analysis Convergent cross mapping Disease management Fusarium graminearum Multivariate forecasting 

Supplementary material

10658_2015_832_MOESM1_ESM.docx (88 kb)
Online Resource 1(DOCX 88 kb)
10658_2015_832_MOESM2_ESM.docx (785 kb)
Fig. S1(DOCX 785 kb)
10658_2015_832_MOESM3_ESM.docx (61 kb)
Fig. S2(DOCX 76 kb)
10658_2015_832_MOESM4_ESM.docx (167 kb)
Fig. S3(DOCX 182 kb)
10658_2015_832_MOESM5_ESM.docx (81 kb)
Fig. S4(DOCX 95 kb)
10658_2015_832_MOESM6_ESM.docx (59 kb)
Fig. S5(DOCX 73 kb)
10658_2015_832_MOESM7_ESM.docx (219 kb)
Fig. S6(DOCX 233 kb)
10658_2015_832_MOESM8_ESM.docx (152 kb)
Fig. S7(DOCX 166 kb)
10658_2015_832_MOESM9_ESM.docx (15 kb)
Table S1(DOCX 30 kb)
10658_2015_832_MOESM10_ESM.docx (16 kb)
Table S2(DOCX 32 kb)

References

  1. Abarbanel, H. (1996). Analysis of observed chaotic data. Berlin: Springer-Verlag.CrossRefGoogle Scholar
  2. Ayers, J., Pennypacker, S., Nelson, P., & Pennypacker, B. (1975). Environmental factors associated with airborne ascospores of Gibberella zeae in corn and wheat fields. Phytopathology, 65:835.Google Scholar
  3. Bolton, D. (1980). The computation of equivalent potential temperature. Monthly Weather Review, 108(7), 1046–1053.CrossRefGoogle Scholar
  4. BozorgMagham, A. E., Motesharrei, S., Penny, S. G., & Kalnay, E. (2015). Causality analysis: Identifying the leading element in a coupled dynamical system. PLoS One, 10(6), e0131226. doi:10.1371/journal.pone.0131226.
  5. Burt, P., Rutter, J., & Gonzales, H. (1997). Short-distance wind dispersal of the fungal pathogens causing Sigatoka diseases in banana and plantain. Plant Pathology, 46(4), 451–458.CrossRefGoogle Scholar
  6. Burt, P., Rosenberg, L., Rutter, J., Ramirez, F., & Gonzales, O. H. (1999). Forecasting the airborne spread of Mycosphaerella fijiensis, a cause of black Sigatoka disease on banana: estimations of numbers of perithecia and ascospores. Annals of Applied Biology, 135(1), 369–377.CrossRefGoogle Scholar
  7. Buttner, M. P., & Stetzenbach, L. D. (1993). Monitoring airborne fungal spores in an experimental indoor environment to evaluate sampling methods and the effects of human activity on air sampling. Applied and Environmental Microbiology, 59(1), 219–226.PubMedPubMedCentralGoogle Scholar
  8. Chen, X., & Yuan, C. (1984). Application of microcomputer in studying wheat scab epidemiology and forecasting. Zhejiang Agricultural Science, 2, 55–60.Google Scholar
  9. Clark, A. T., Ye, H., Isbell, F., Deyle, E. R., Cowles, J. M., Tilman, D., et al. (2015). Spatial 'convergent cross mapping' to detect causal relationships from short time-series. Ecology, 96(5), 1174–1181.CrossRefPubMedGoogle Scholar
  10. Clarkson, J. P., Staveley, J., Phelps, K., Young, C. S., & Whipps, J. M. (2003). Ascospore release and survival in Sclerotinia sclerotiorum. Mycological Research, 107(02), 213–222.CrossRefPubMedGoogle Scholar
  11. Del Ponte, E. M., Fernandes, J. M. C., Pavan, W., & Baethgen, W. E. (2009). A model-based assessment of the impacts of climate variability on fusarium head blight seasonal risk in southern Brazil. Journal of Phytopathology, 157(11–12), 675–681. Google Scholar
  12. Deyle, E. R., Fogarty, M., Hsieh, C.-H., Kaufman, L., MacCall, A. D., Munch, S. B., et al. (2013). Predicting climate effects on Pacific sardine. Proceedings of the National Academy of Sciences, 110(16), 6430–6435.CrossRefGoogle Scholar
  13. Farmer, J. D., & Sidorowich, J. J. (1987). Predicting chaotic time series. Physical Review Letters, 59(8), 845.CrossRefPubMedGoogle Scholar
  14. Fernando, W. G., Miller, J., Seaman, W., Seifert, K., & Paulitz, T. (2000). Daily and seasonal dynamics of airborne spores of Fusarium graminearum and other Fusarium species sampled over wheat plots. Canadian Journal of Botany, 78(4), 497–505.CrossRefGoogle Scholar
  15. Gadoury, D. M., Stensvand, A., & Seem, R. C. (1998). Influence of light, relative humidity, and maturity of populations on discharge of ascospores of Venturia inaequalis. Phytopathology, 88(9), 902–909.CrossRefPubMedGoogle Scholar
  16. Gilbert, J., & Fernando, W. (2004). Epidemiology and biological control of Gibberella zeae/Fusarium graminearum. Canadian Journal of Plant Pathology, 26(4), 464–472.CrossRefGoogle Scholar
  17. Gilbert, J., & Tekauz, A. (2000). Review: Recent developments in research on fusarium head blight of wheat in Canada. Canadian Journal of Plant Pathology-Revue Canadienne De Phytopathologie, 22(1), 1–8.Google Scholar
  18. Gilbert, J., Woods, S., & Kromer, U. (2008). Germination of ascospores of Gibberella zeae after exposure to various levels of relative humidity and temperature. Phytopathology, 98(5), 504–508.CrossRefPubMedGoogle Scholar
  19. Granger, C. W. (1969). Investigating causal relations by econometric models and cross-spectral methods. Econometrica: Journal of the Econometric Society, 424–438.Google Scholar
  20. Hart, M., Wentworth, J., & Bailey, J. (1994). The effects of trap height and weather variables on recorded pollen concentration at Leicester. Grana, 33(2), 100–103.CrossRefGoogle Scholar
  21. Holling, C. S. (2001). Understanding the complexity of economic, ecological, and social systems. Ecosystems, 4(5), 390–405.CrossRefGoogle Scholar
  22. Inch, S., Fernando, W., & Gilbert, J. (2005). Seasonal and daily variation in the airborne concentration of Gibberella zeae (Schw.) Petch spores in Manitoba. Canadian Journal of Plant Pathology, 27(3), 357–363.CrossRefGoogle Scholar
  23. Jennings, P., & Turner, J. (1996) Towards the prediction of Fusarium ear blight epidemics in the UK-the role of humidity in disease development. In Brighton Crop Protection Conference: Pests & Diseases-1996. Volume 1. Proceedings of an International Conference, Brighton, UK, 18–21 November, 1996 (pp. 233–238): British Crop Protection Council.Google Scholar
  24. Maldonado-Ramirez, S. L., Schmale III, D. G., Shields, E. J., & Bergstrom, G. C. (2005). The relative abundance of viable spores of Gibberella zeae in the planetary boundary layer suggests the role of long-distance transport in regional epidemics of fusarium head blight. Agricultural and Forest Meteorology, 132(1–2), 20–27.Google Scholar
  25. McMullen, M. P., & Stack, R. W. (1983). Head blight (scab) of small grains. North Dakota Cooperative Extension Service Circular(NPP-8), 1–2.Google Scholar
  26. Meredith, D., Lawrence, J., & Firman, I. (1973). Ascospore release and dispersal in black leaf streak disease of bananas (Mycosphaerella fijiensis). Transactions of the British Mycological Society, 60(3), 547–554.CrossRefGoogle Scholar
  27. Oke, T. R. (1987). Boundary layer climates, 2nd edn. London: Methuen.Google Scholar
  28. Parnell, M., Burt, P. J. A., & Wilson, K. (1998). The influence of exposure to ultraviolet radiation in simulated sunlight on ascospores causing Black Sigatoka disease of banana and plantain. International Journal of Biometeorology, 42(1), 22–27.CrossRefGoogle Scholar
  29. Paulitz, T. (1996). Diurnal release of ascospores by Gibberella zeae in inoculated wheat plots. Plant Disease, 80(6), 674–678.CrossRefGoogle Scholar
  30. Paulitz, T. (1999). Fusarium head blight: a re-emerging disease. Phytoprotection, 80(2), 127–133.CrossRefGoogle Scholar
  31. Prussin II, A. J., Li, Q., Malla, R., Ross, S. D., & Schmale III, D. G. (2014a). Monitoring the long distance transport of Fusarium graminearum from field-scale sources of inoculum. Plant Disease, 98(4), 504–511.Google Scholar
  32. Prussin II, A. J., Szanyi, N. A., Welling, P. I., Ross, S. D., & Schmale III, D. G. (2014b). Estimating the production and release of ascospores from a field-scale source of Fusarium graminearum inoculum. Plant Disease, 98(4), 497–503.Google Scholar
  33. Prussin II, A. J., Marr, L. C., Schmale III, D. G., Stoll, R., & Ross, S. D. (2015). Experimental validation of a long-distance transport model for plant pathogens: Application to Fusarium graminearum. Agricultural and Forest Meteorology, 203(0), 118–130.Google Scholar
  34. Reis, E. (1990). Effects of rain and relative humidity on the release of ascospores and on the infection of wheat heads by Gibberella zeae. Fitopatologia Brasileira, 15, 339–343.Google Scholar
  35. Rotem, J., & Aust, H. (1991). The effect of ultraviolet and solar radiation and temperature on survival of fungal propagules. Journal of Phytopathology, 133(1), 76–84.CrossRefGoogle Scholar
  36. Rutter, J., Burt, P. J., & Ramirez, F. (1998). Movement of Mycosphaerella fijiensis spores and sigatoka disease development on plantain close to an inoculum source. Aerobiologia, 14(2–3), 201–208.Google Scholar
  37. Sauer, T., Yorke, J. A., & Casdagli, M. (1991). Embedology. Journal of Statistical Physics, 65(3–4), 579–616.Google Scholar
  38. Schmale III, D. G., & Bergstrom, G. C. (2004). Spore deposition of the ear rot pathogen, Gibberella zeae, inside corn canopies. Canadian Journal of Plant Pathology-Revue Canadienne De Phytopathologie, 26(4), 591–595.Google Scholar
  39. Schmale III, D. G., & Ross, S. D. (2015). Highways in the sky: Scales of atmospheric transport of plant pathogens. Annual Review of Phytopathology, 53(1), 591–611.Google Scholar
  40. Schmale III, D. G., Arntsen, Q. A., & Bergstrom, G. C. (2005a). The forcible discharge distance of ascospores of Gibberelia zeae. Canadian Journal of Plant Pathology-Revue Canadienne De Phytopathologie, 27(3), 376–382.CrossRefGoogle Scholar
  41. Schmale III, D. G., Shah, D. A., & Bergstrom, G. C. (2005b). Spatial patterns of viable spore deposition of Gibberella zeae in wheat fields. Phytopathology, 95(5), 472–479. doi:10.1094/phyto-95-0472.CrossRefPubMedGoogle Scholar
  42. Schmale III, D. G., Shields, E. J., & Bergstrom, G. C. (2006). Night-time spore deposition of the fusarium head blight pathogen, Gibberella zeae, in rotational wheat fields. Canadian Journal of Plant Pathology-Revue Canadienne De Phytopathologie, 28(1), 100–108.CrossRefGoogle Scholar
  43. Schmale III, D. G., Ross, S. D., Fetters, T. L., Tallapragada, P., Wood-Jones, A. K., & Dingus, B. (2012). Isolates of Fusarium graminearum collected 40–320 meters above ground level cause fusarium head blight in wheat and produce trichothecene mycotoxins. Aerobiologia, 28(1), 1–11.Google Scholar
  44. Schollenberger, M., Jara, H. T., Suchy, S., Drochner, W., & Müller, H.-M. (2002). Fusarium toxins in wheat flour collected in an area in southwest Germany. International Journal of Food Microbiology, 72(1), 85–89.CrossRefPubMedGoogle Scholar
  45. Spotts, R., & Cervantes, L. (1994). Factors affecting maturation and release of ascospores of Venturia pirina in Oregon. Phytopathology, 84(3), 260–263.CrossRefGoogle Scholar
  46. Stern, D. I., & Enflo, K. (2013). Causality between energy and output in the long-run. Energy Economics, 39(0), 135–146, doi:10.1016/j.eneco.2013.05.007.
  47. Su, H., Van Bruggen, A., & Subbarao, K. (2000). Spore release of Bremia lactucae on lettuce is affected by timing of light initiation and decrease in relative humidity. Phytopathology, 90(1), 67–71.Google Scholar
  48. Sugihara, G., May, R., Ye, H., Hsieh, C.-h., Deyle, E., Fogarty, M., et al. (2012). Detecting causality in complex ecosystems. Science, 338(6106), 496–500.Google Scholar
  49. Sung, J.-M., & Cook, R. (1981). Effect of water potential on reproduction and spore germination by Fusarium roseum 'Graminearum,' 'Culmorum,' and 'Avenaceum'. Phytopathology, 71(5), 499–504.Google Scholar
  50. Sutton, J. (1982). Epidemiology of wheat head blight and maize ear rot caused by Fusarium graminearum. Canadian Journal of Plant Pathology, 4(2), 195–209.CrossRefGoogle Scholar
  51. Takens, F. (1981). Detecting strange attractors in turbulence. Berlin Heidelberg: Springer.CrossRefGoogle Scholar
  52. Trail, F. (2007). Fungal cannons: explosive spore discharge in the Ascomycota. FEMS Microbiology Letters, 276(1), 12–18.CrossRefPubMedGoogle Scholar
  53. Trail, F., Xu, H., Loranger, R., & Gadoury, D. (2002). Physiological and environmental aspects of ascospore discharge in Gibberella zeae (anamorph Fusarium graminearum). Mycologia, 94(2), 181–189.CrossRefPubMedGoogle Scholar
  54. Trail, F., Gaffoor, I., & Vogel, S. (2005). Ejection mechanics and trajectory of the ascospores of Gibberella zeae (anamorph Fusarium graminearum). Fungal Genetics and Biology, 42(6), 528–533.CrossRefPubMedGoogle Scholar
  55. Tschanz, A. T., Horst, R. K., & Nelson, P. E. (1975). Ecological aspects of ascospore discharge in Gibberella zeae. Phytopathology, 65, 597.CrossRefGoogle Scholar
  56. Windels, C. E. (2000). Economic and social impacts of fusarium head blight: changing farms and rural communities in the Northern Great Plains. Phytopathology, 90(1), 17–21.CrossRefPubMedGoogle Scholar

Copyright information

© Koninklijke Nederlandse Planteziektenkundige Vereniging 2015

Authors and Affiliations

  • Ray F. David
    • 1
  • Amir E. BozorgMagham
    • 2
  • David G. SchmaleIII
    • 3
  • Shane D. Ross
    • 4
  • Linsey C. Marr
    • 1
  1. 1.Department of Civil and Environmental EngineeringVirginia TechBlacksburgUSA
  2. 2.Department of Atmospheric and Oceanic ScienceUniversity of MarylandCollege ParkUSA
  3. 3.Department of Plant Pathology, Physiology, and Weed ScienceVirginia TechBlacksburgUSA
  4. 4.Department of Biomedical Engineering and MechanicsVirginia TechBlacksburgUSA

Personalised recommendations