Skip to main content
Log in

Effects of temperature increase on the epidemiology of three major vector-borne viruses

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

The epidemiologies of Maize streak virus (MSV), Maize stripe virus (MSpV), and Maize mosaic virus (MMV) were compared in La Réunion over a three year-period. Disease incidence caused by each virus was assessed, and the leaf and planthopper vector populations (Cicadulina mbila and Peregrinus maidis) were estimated in weekly sowings of the temperate, virus-susceptible maize hybrid INRA 508 and of the composite resistant cv. IRAT 297. MSV caused the most prevalent disease and MMV the least, with lower incidences in cv. IRAT 297 than in INRA 508. For each plant–virus–vector combination, (a) disease incidence was positively correlated to vector abundance, often with 1 month of time lag; (b) annual periodicity of disease incidence and of vector numbers was consistent with highest autocorrelations and a time lag of 12 months, (c) vector numbers and disease incidence were closely associated with temperature fluctuations, both remaining relatively constant below 24°C and increasing rapidly above this threshold temperature. By contrast, relationships with rainfall and relative humidity (RH) were less consistent. Overall, 63 to 80% of the variance of disease incidence was explained through stepwise regression with vector number, temperature, and sometimes also rainfall or RH. The simple epidemiological model proposed underlines the close link between increased temperature and possible (re-) emergence of these three diseases in a maize cropping area.

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

Access this article

Subscribe and save

Springer+
from €37.37 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

Price includes VAT (Norway)

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alto, B. W. & Juliano, S. A. (2001). Precipitation and temperature effects on populations of Aedes albopictus (Diptera: Culicidae): implications for range expansion. Journal of Medical Entomology, 38, 646–656.

    Article  PubMed  CAS  Google Scholar 

  • Asanzi, C. M., Bosque-Perez, N. A., Buddenhagen, I. W., Gordon, D. T. & Nault, L. R. (1994). Interactions among maize streak virus disease, leafhopper vector populations and maize cultivars in forest and savanna zones of Nigeria. Plant Pathology, 43, 145–157. doi:10.1111/j.1365-3059.1994.tb00564.x.

    Article  Google Scholar 

  • Autrey, L. J. C. (1983). Maize mosaic virus and other maize virus diseases in the islands of the Western Indian Ocean, Proceedings International Maize Virus Disease Colloquium and Workshop, Ohio State University, Wooster.

  • Bosque-Perez, N. A. (2000). Eight decades of Maize streak virus research. Virus Research, 71, 107–121. doi:10.1016/S0168-1702(00)00192-1.

    Article  PubMed  CAS  Google Scholar 

  • Brewbaker, J. L. (1979). Disease of maize in the wet lowland tropics and the collapse of the classic Maya civilization. Economic Botany, 33, 101–118.

    Google Scholar 

  • Delpuech, I., Bonfils, J. & Leclant, F. (1986). Contribution à l’étude des virus du maïs transmis par homoptères auchénorrhynques à l’île de la Réunion. Agronomie, 6, 549–554. doi:10.1051/agro:19860607.

    Article  Google Scholar 

  • Dintinger, J., Boissot, N., Chiroleu, F., Hamon, P. & Reynaud, B. (2005a). Evaluation of maize inbreds for Maize stripe virus and Maize mosaic virus resistance: Disease progress in relation to time and the cumulative number of planthoppers. Phytopathology, 95, 600–607. doi:10.1094/PHYTO-95-0600.

    Article  PubMed  CAS  Google Scholar 

  • Dintinger, J., Verger, D., Caiveau, S., Risterucci, A. M., Gilles, J., Chiroleu, F., et al. (2005b). Genetic mapping of maize stripe disease resistance from the Mascarene source. Theoretical and Applied Genetics, 111, 347–359. doi:10.1007/s00122-005-2027-3.

    Article  PubMed  CAS  Google Scholar 

  • Fargette, D., Jeger, M., Fauquet, C., & Fishpool, L. D. C. (1993). Analysis of temporal disease progress of African cassava mosaic virus. Phytopathology, 84, 91–98. doi:10.1094/Phyto-84-91.

    Article  Google Scholar 

  • Fargette, D., Konate, G., Fauquet, C., Muller, E., Peterschmitt, M. & Thresh, J. M. (2006). Molecular ecology and emergence of tropical plant viruses. Annual Review of Phytopathology, 44, 235–260. doi:10.1146/annurev.phyto.44.120705.104644.

    Article  PubMed  CAS  Google Scholar 

  • Fauquet, C. & Thouvenel, J. C. (1980). Maladies virales des plantes cultivées en Côte d’Ivoire ORSTOM-Documentations techniques, n°46, 128p.

  • Gagnon, A. S., Bush, A. B. G., & Smoyer-Tomic, K. E. (2001). Dengue epidemics and the El Niño Southern Oscillation. Climate Research, 19, 35–43. doi:10.3354/cr019035.

    Article  Google Scholar 

  • Greber, R. S. (1981). Maize stripe disease in Australia. Australian Journal of Agricultural Research, 32, 27–36. doi:10.1071/AR9810027.

    Article  Google Scholar 

  • Hainzelin, E. & Marchand, J. L. (1986). Registration of IRAT 297 maize germplasm. Crop Science, 26, 1090–1091.

    Google Scholar 

  • Kulkarni, H. Y. (1973). Comparison and characterization of maize stripe and maize line viruses (MSV etMLV). The Annals of Applied Biology, 75, 205–216. doi:10.1111/j.1744-7348.1973.tb07300.x.

    Article  Google Scholar 

  • Lett, J. M., Granier, M., Grondin, M., Turpin, P., Molinaro, F., Chiroleu, F., et al. (2001). Electrical penetration graphs from Cicadulina mbila on maize, the fine structure of its stylet pathways and consequences for virus transmission efficiency. Entomologia Experimentalis et Applicata, 101, 93–109. doi:10.1023/A:1019216431435.

    Article  Google Scholar 

  • Madden, L. V. & Hughes, G. (1995). Plant disease incidence: distributions, heterogeneity, and temporal analysis. Annual Review of Phytopathology, 33, 529–564. doi:10.1146/annurev.py.33.090195.002525.

    Article  PubMed  CAS  Google Scholar 

  • Madden, L. V., Louie, R. & Knoke, J. K. (1987). Temporal and spatial analysis of maize dwarf mosaic epidemics. Phytopathology, 77, 148–156. doi:10.1094/Phyto-77-148.

    Article  Google Scholar 

  • Mora-Aguilera, G., Teliz, D., Campbell, C. L. & Avila, C. (1992). Temporal and spatial development of papaya ring spot in Veracruz, Mexico. Journal of Phytopathology, 136, 27–36. doi:10.1111/j.1439-0434.1992.tb01278.x.

    Article  Google Scholar 

  • Mouchet, J., Manguin, S., Sircoulon, J., Laventure, S., Faye, O., Onapa, A. W., et al. (1998). Evolution of malaria in Africa for the past 40 years: impact of climatic and human factors. Journal of the American Mosquito Control Association, 14, 121–130.

    PubMed  CAS  Google Scholar 

  • Okoth, V. A. O. & Dabrowski, Z. T. (1987). Population density, species composition and infectivity with Maize streak virus (MSV) of Cicadulina spp. Leafhopper in rame ecological zones in Nigeria. Acta Oecologica Applicata, 8, 191–200.

    Google Scholar 

  • Patz, J. A., Campbell-Lendrum, D., Holloway, T. & Foley, J. A. (2005). Impact of regional climate change on human health. Nature, 438, 310–317. doi:10.1038/nature04188.

    Article  PubMed  CAS  Google Scholar 

  • Pernet, A., Hoisington, D., Dintinger, J., Jewell, D., Jiang, C., Khairallah, M., et al. (1999a). Genetic mapping of Maize streak virus resistance from the Mascarene source. II. Resistance in line CIRAD390 and stability across germplasm. Theoretical and Applied Genetics, 99, 540–553. doi:10.1007/s001220051267.

    Article  CAS  Google Scholar 

  • Pernet, A., Hoisington, D., Franco, J., Isnard, M., Jewell, D., Jiang, C., et al. (1999b). Genetic mapping of Maize streak virus resistance from the Mascarene source. I. Resistance in line D211 and stability against different virus clones. Theoretical and Applied Genetics, 99, 524–539. doi:10.1007/s001220051266.

    Article  CAS  Google Scholar 

  • Peterschmitt, M., Quiot, J. B., Reynaud, B. & Baudin, P. (1992). Detection of Maize streak virus antigens over time in different parts of maize plants of a sensitive and a so-called tolerant cultivar by ELISA. The Annals of Applied Biology, 121, 641–653. doi:10.1111/j.1744-7348.1992.tb03473.x.

    Article  Google Scholar 

  • Reynaud, B. (1988). Transmission des virus de la striure, du stripe et de la mosaïque du maïs par leurs vecteurs, Cicadulina mbila (Naude, 1924) et Peregrinus maïdis (Ashmead, 1890) (Homoptera). Approches biologique, génétique et épidémiologique de la relation vecteur–virus–plante PhD. Thesis, Université des Sciences et Techniques du Languedoc, 173.

  • Rocha-Pena, M. A., Monreal, C. T., Becerra, E. N. & Ruiz, P. (1984). Presencia del virus del mosaico del maiz en el estado de tabasco, Mexico. Turrailba, 34, 233–235.

    Google Scholar 

  • Rose, D. J. W. (1972). Times and sizes of dispersal flights by Cicadulina species (Homoptera : Cicadellidae), vectors of maize streak disease. Journal of Animal Ecology, 4, 495–506. doi:10.2307/3483.

    Google Scholar 

  • Rose, D. J. W. (1973). Field studies in Rhodesia on Cicadulina spp. (herm, Cicaddellidae), vectors of maize streak disease. Bulletin of Entomological Research, 62, 477–495.

    Article  Google Scholar 

  • Rose, D. J. W. (1974). The epidemiology of maize streak disease in relation to population densities of Cicadulina spp. The Annals of Applied Biology, 76, 199–207. doi:10.1111/j.1744-7348.1974.tb07973.x.

    Article  Google Scholar 

  • Rose, D. J. W. (1983). The distribution of various species of Cicadulina in different African countries, frequency of their altade and impact on crop production, Proceedings of the International Workshop on Biotaxonomy, classification and biology of leafhoppers and planthoppers (Auchenorryncha) of economic Importance.

  • Traore, S. N. & Ouédraogo, I. (1995). Etude de la bioécologie des cicadelles vectrices de la striure du maïs. Sahel-IPM, 5, 2–12.

    Google Scholar 

  • Van Rensburg, G. D. (1982). Laboratory observations on the biology of Cicadulina mbila Naude (Homoptera: Cicadellinae), a vector of maize streak disease. 1. Effect of temperature. Phytolactica, 14, 99–107.

    Google Scholar 

  • Wilkinson, L. (1989). SYSTAT: The system for statistics. Evanston, IL. SYSTAT.

  • Zell, R. (2004). Global climate change and the emergence/re-emergence of infectious diseases. International Journal of Medical Microbiology, 293, 16–26.

    PubMed  Google Scholar 

Download references

Acknowledgements

We thank M. Grondin and R. P. Hoareau for their technical assistance, P. Letourmy and N. Boissot for help with statistical analysis, J. C. Combres and R. Nativel for meteorological data, and J.L. Marchand and J.M. Thresh for helpful discussions. The research was conducted during a PhD scholarship programme supported by the French Ministry of Research and partially financed by an EU project (TSD-A-085).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to H. Delatte.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Reynaud, B., Delatte, H., Peterschmitt, M. et al. Effects of temperature increase on the epidemiology of three major vector-borne viruses. Eur J Plant Pathol 123, 269–280 (2009). https://doi.org/10.1007/s10658-008-9363-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue date:

  • DOI: https://doi.org/10.1007/s10658-008-9363-5

Keywords