Occurrence of Puccinia spp. spores in Madeira Island and their phytopathological importance

Abstract

The genus Puccinia represents rust infections, which are responsible for great productivity losses in crops of commercial and ornamental plants worldwide. This work is aimed at determining the occurrence of Puccinia spp. spores in Madeira Island in order to infer the exposure risks from a phytopathological point of view. A phytopathological analysis was performed in 203 local plant samples between January 2003 and December 2012. During the same period the airborne concentrations of rust spores were monitored following well-established guidelines. Aerobiological data was compared with meteorological records. Based on macro and microscopic analyses, five species of rusts were identified: P. horiana, P. buxi, P. porri, P. pelargonii-zonalis, and P. sorghi, and they were found mostly in spring and summer. A total of 20 samples out of 203 analysed plants (9.8%), were infected with Puccinia spores, i.e., P. horiana (5.9%), P. buxi (1.47%), P. porri and P. pelargonii-zonalis (0.98%), and P. sorghi (0.5%). During the studied period Puccinia spores attained an annual average concentration of 126 spores m−3 and most of them were recorded between March and October. Meteorological factors were determinant in fluctuations in spore concentration. Relative humidity was the parameter that favoured the biggest release and dispersal of the rust spores, whereas rainfall revealed a significant negative effect. Rusts do not represent an important plant pathogen in Madeira Island, as shown by the low infection frequencies and levels of airborne spore concentrations.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

References

  1. Agrios, G. N. (1997). Plant pathology. San Diego: Academic press.

    Google Scholar 

  2. Babadoost, M. (1991). Common rust and southern rust of sweet corn. Report on plant disease. University of Illinois Extension, RPD, (Serial No. 965).

  3. Bonde, M. R., Palmer, C. L., Luster, D. G., Nester, S. E., Revell, J. M., & Berner, D. K. (2014). Viability of Puccinia horiana teliospores under various environmental conditions. Plant Health Progress, 15, 25–28. https://doi.org/10.1094/PHP-RS-13-0117.

    Google Scholar 

  4. Borges, P. A. V., Abreu, C., Aguiar, A. M. F., Carvalho, P., Jardim, R., Melo, I., et al. (2008). A list of the terrestrial fungi, flora and fauna of Madeira and Selvagens archipelagos. Direcção Regional do Ambiente da Madeira and Universidade dos Açores, Funchal and Angra do Heroísmo.

  5. Calderon, C., Lacey, J., McCartney, H. A., & Rosas, I. (1995). Seasonal and diurnal variation of airborne basidiomycete spore concentrations in Mexico City. Grana, 34, 260–268.

    Article  Google Scholar 

  6. Calheta (Madeira) (2017). https://www.infopedia.pt/$calheta-(madeira). Accessed 5 Jan 2017.

  7. D’Amato, G., & Spieksma, F. Th. M. (1995). Aerobiologic and clinical aspects of mould allergy in Europe. European Academy of Allergology and Clinical Immunology Position Paper. Allergy, 50, 870–877.

  8. De Backer, M., Alaei, H., Van Bockstaele, E., Roldan-Ruiz, I., van der Lee, T., Maes, M., et al. (2011). Identification and characterization of pathotypes in Puccinia horiana, a rust pathogen of Chrysanthemum x morifolium. European Journal of Plant Pathology, 130, 325–338.

    Article  Google Scholar 

  9. De Wolf, E., Murray, T., Paul, P., Osborne, L., & Tenuta, A. (2011). Identification and Management of Stem Rust on Wheat and Barley. USDA-CREES Extension IPM 2009-41533-05331. http://plantpath.wsu.edu/wp-content/uploads/2012/10/Stem-Rust-Man-WA1.pdf. Accessed 15 Nov 2016.

  10. Dennis, R. W. G. (1986). Fungi of the Hebrides. Kew: Royal Botanic Garden.

    Google Scholar 

  11. Dunhin, B. J., Pretorius, Z. A., Bender, C. M., Kloppers, F. J., & Flett, B. C. (2004). Description of spore stages of Puccinia sorghi in South Africa, south African. Journal of Plant Soil, 21, 48–52.

    Article  Google Scholar 

  12. Elvira-Rendueles, B., Moreno, J., Garcia-Sanchez, A., Vergara, N., Martinez-Garcia, M. J., & Moreno-Grau, S. (2013). Air-spore in Cartagena, Spain: Viable and non-viable sampling methods. Annals of Agricultural and Environmental Medicine, 20, 664–671.

    PubMed  Google Scholar 

  13. EPPO/CABI. (1997). Puccinia horiana. In I. M. Smith, D. G. McNamara, P. R. Scott, & M. Holderness (Eds.), Quarantine pests for Europe. Wallingford: CABI.

    Google Scholar 

  14. Farr, D. F., Bills, G. F., Chamuris, G. P., & Rossman, A. Y. (1989). Fungi on plants and plant products in the United States. St. Paul: American Phytopathological Society Press.

    Google Scholar 

  15. Fried, G., Chauvel, B., Reynaud, P., & Sache, I. (2017). Decreases in crop production by non-native weeds, pests, and pathogens. In M. Vilá & P. E. Hulme (Eds.), Impact of biological invasions on ecosystem services (pp. 83–102). Switzerland: Springer International Publishing.

    Google Scholar 

  16. Gage, S. H., Isard, S. A., & Colunga-Garcia, M. (1999). Ecological scaling of aerobiological dispersal processes. Agricultural and Forest Meteorology, 97, 249–261.

    Article  Google Scholar 

  17. Galán, C., Cariñanos, P., Alcázar, P., & Dominguez-Vilches, E. (2007). Spanish aerobiology network (REA) management and quality manual. Córdoba: Servicio de Publicaciones Universidad de Córdoba, Argos Impresores SL.

    Google Scholar 

  18. Galán, C., Smith, M., Thibaudon, M., Frenguelli, G., Oteros, J., Gehrig, R., et al. (2014). Pollen monitoring: Minimum requirements and reproducibility of analysis. Aerobiologia, 30, 385–395.

    Article  Google Scholar 

  19. Geagea, L., Hubera, L., & Sache, I. (1999). Dry-dispersal and rain-splash of brown (Puccinia recondite f.sp. tritici) and yellow (P. striiformis) rust spores from infected wheat leaves exposed to simulated raindrops. Plant Pathology, 48, 472–482.

    Article  Google Scholar 

  20. Ghatge, M. M., Salunkhe, V. S., & Jadhav, R. R. (2013). Diversity of airborne fungi in Kadegaon Tahsil, district Sangli, MS, India. International Research Journal of Environmental Sciences, 2, 26–29.

    Google Scholar 

  21. Gjaerum, H. B. (1982). Rust fungi from Madeira. Boletim do Museu Municipal do Funchal, 34, 1–22.

    Google Scholar 

  22. Glen, M., Alfenas, A. C., Zauza, E. A. V., Wingfield, M. J., & Mohammed, C. (2007). Puccinia psidii: A threat to the Australian environment and economy–a review. Australasian Plant Pathology, 36, 1–16.

    Article  Google Scholar 

  23. Göre, M. E. (2008). Geranium rust disease caused by Puccinia pelargonii-zonalis: First report in Turkey. Plant Pathology, 57, 786.

    Google Scholar 

  24. Goudie, A. S., & Middleton, N. J. (2001). Saharan dust storms: Nature and consequences. Earth-Science Reviews, 56, 179–204.

    CAS  Article  Google Scholar 

  25. Gregorio-Cipriano, M. R., Fernández-Pavía, S. P., Rodríguez-Alvarado, G., & Gómez-Dorantes, N. (2013). First report of geranium rust (Puccinia pelargonii-zonalis) in the state of Michoacán, México. Plant Disease, 97(12), 1660 http://apsjournals.apsnet.org/doi/abs/10.1094/PDIS-05-13-0570-PDN. Accessed 14 Nov 2016.

    Article  Google Scholar 

  26. Guarín, F. A., Abril, M. A. Q., Alvarez, A., & Fonnegra, R. (2015). Atmospheric pollen and spore content in the urban area of the city of Medellin, Colombia. Hoehnea, 42, 9–19.

    Article  Google Scholar 

  27. Harrison, J. M. (1987). Observations on the occurrence of telia of Puccinia porri on leeks in the UK. Plant Pathology, 36, 114–115.

    Article  Google Scholar 

  28. Hermansen, J. E., Torp, U., & Prahm, L. P. (1978). Studies of transport of live spores of cereal mildew and rust fungi across the North Sea. Grana, 17, 41–46.

    Article  Google Scholar 

  29. Herut, B., Collier, R., & Krom, M. D. (2002). The role of dust in supplying nitrogen and phosphorus to the Southeast Mediterranean. Limnology and Oceanography, 47(3), 870–878.

    CAS  Article  Google Scholar 

  30. Hiratsuka, Y., & Sato, S. (1982). Morphology and taxonomy of rust fungi. In K. Scott & A. K. Chakravorty (Eds.), The rust fungi (pp. 1–36). New York: Academic press.

    Google Scholar 

  31. Hirst, J. M. (1952). An automatic volumetric spore trap. Annals of Applied Biology, 39, 257–265.

    Article  Google Scholar 

  32. Ho, T. M., Tan, B. H., Ismail, S., & Bujang, M. K. (1995). Seasonal prevalence of air-borne pollen and spores in Kuala Lumpur, Malaysia. Asian Pacific Journal of Allergy and Immunology, 13, 17–22.

    CAS  PubMed  Google Scholar 

  33. Holl, F. (1830). Verzeichniss der auf der Insel Madeira beobachteten Pflazen, nebst Beschreibung einiger neuen Arten. Flora, 13, 369–392.

    Google Scholar 

  34. Huerta-Espino, J., Singh, R. P., & Roelfs, A. P. (2014). Rust fungi of wheat. In J. K. Misra, J. P. Tewari, S. K. Deshmukh, & C. Vágvölgyi (Eds.), Fungi from different substrates (pp. 217–259). Boca Raton: CRC press.

    Google Scholar 

  35. Hutchidon, L. J. (1996). Puccinia pelargonii-zonalis (Uredinales: Pucciniaceae), an addition to the rust flora of Canada. Mycoscience, 37, 467–469.

    Article  Google Scholar 

  36. Isard, S. A., & Russo, J. M. (2011). Risk assessment of aerial transport of rust pathogens to the western hemisphere and within North America. In McIntosh, R. (Ed.) Proc BGRI 2011Technical Workshop (pp. 25–34). St. Paul. http://www.globalrust.org/sites/default/files/2011%20BGRI%20plenary%20presentations-ALL.pdf. Accessed 18 May 2017.

  37. Isard, S. A., Gage, S. H., Comtois, P., & Russo, J. M. (2005). Principles of the atmospheric pathway for invasive species applied to soybean rust. Bioscience, 55, 851–861.

    Article  Google Scholar 

  38. Jędryczka, M., Brachaczek, A., Kaczmarek, J., Dawidziuk, A., Kasprzyk, J., Mączyńska, A., et al. (2012). System for forecasting disease epidemics (SPEC) – Decision support system in polish agriculture, based on aerobiology. Alergologia Immunologia, 9, 89–91.

    Google Scholar 

  39. Kadam, R. M., Reddy, N. J. M., & Biradar, R. P. (2010). Air-borne spore population of Puccinia penniseti in relation to rust disease of bajra at Ahmedpur. International Journal of Plant Protection, 3, 160–162.

    Google Scholar 

  40. Kolmer, J. A. (2001). Early research on the genetics of Puccinia Graminis and stem rust resistance in wheat in Canada and the United States. In P. D. Peterson (Ed.), Stem rust of wheat: From ancient enemy to modern foe (pp. 51–82). St Paul: APS press.

    Google Scholar 

  41. Levetin, E., & Horner, W. E. (2002). Fungal aerobiology: Exposure and measurement. Chemical Immunology, 81, 10–27.

    Article  PubMed  Google Scholar 

  42. Luck, J., Spackman, M., Freeman, A., Trebicki, P., Griffiths, W., Finlay, K., et al. (2011). Climate change and diseases of food crops. Plant Pathology, 60, 113–121.

    Article  Google Scholar 

  43. Ma, L., Hu, X., & Xu, X. (2017). Effect of controlled fluctuating low temperatures on survival of Puccinia striiformis f. sp. Tritici. European Journal of Plant Pathology, 147, 713–716.

    CAS  Article  Google Scholar 

  44. Magyar, D., & Manninger, K. (2004). Effects of meteorological conditions on uredo- and teliospores of rusts. In Proceedings of the International Cereal Rusts and Powdery Mildews Conference. Norwich: John Innes Centre, 22-27 August 2004.

  45. Mallaiah, K. V., & Rao, A. S. (1982). Aerial dissemination of urediniospores of groundnut rust. Transactions of the British Mycological Society, 78, 21–28.

    Article  Google Scholar 

  46. Marasas, C. N., Smale, M., & Singh, R. P. (2004). The economic impact in developing countries of leaf rust resistance breeding in CIMMYT-related spring bread wheat. Economics program paper 04–01. Mexico: D. F, CIMMYT.

  47. Morin, L., Aveyard, R., Lidbetter, J. R., & Wilson, P. G. (2012). Investigating the host-range of the rust fungus Puccinia psidii sensu lato across tribes of the family Myrtaceae present in Australia. PloS One, 7, e35434.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  48. Morris, C. E., Sands, D. C., Glaux, C., Samsatly, J., Asaad, S., Moukahel, A. R., et al. (2013). Urediospores of rust fungi are ice nucleation active at >−10 °C and harbor ice nucleation active bacteria. Atmospheric Chemistry and Physics, 13, 4223–4233.

  49. Nagarajan, S., & Singh, D. V. (1990). Long-distance dispersion of rust pathogens. Annual Review of Phytopathology, 28, 139–153.

    CAS  Article  PubMed  Google Scholar 

  50. Pegg, G. S., Giblin, F. R., McTaggart, A. R., Guymer, G. P., Taylor, H., Ireland, K. B., et al. (2014). Puccinia psidii in Queensland, Australia: Disease symptoms, distribution and impact. Plant Pathology, 63, 1005–1021.

    Article  Google Scholar 

  51. Peixoto-Junior, R. F., Creste, S., Landell, M. G. A., Nunes, D. S., Sanguino, A., Campos, M. F., et al. (2014). Genetic diversity among Puccinia Melanocephala isolates from Brazil assessed using simple sequence repeat markers. Genetics and Molecular Research, 13, 7852–7863.

    CAS  Article  PubMed  Google Scholar 

  52. Preece, T. F. (2000). The strange story of the box rust, Puccinia buxi, in Britain. Mycologist, 14(part 3), 104–106.

    Article  Google Scholar 

  53. Pria, M. D., Zagonel, J., & Fernandes, E. C. (2008). Controle de ferrugem na cultura do alho com uma nova mistura de fungicidas. Horticultura Brasileira, 26, 268–270.

    Article  Google Scholar 

  54. Purdy, L. H., Krupa, S. V., & Dean, J. L. (1985). Introduction of sugarcane rust into the Americas and its spread to Florida. Plant Disease, 69, 689–693.

    Article  Google Scholar 

  55. Quintal, R. (2007). Quintas, Parques e Jardins do Funchal - Estudo fitogeográfico. Lisboa: Esfera do Caos Editores.

  56. RHS. (2016). Box problems, Diseases of box. https://www.rhs.org.uk/advice/profile?PID=851. Accessed 2 Nov 2016.

  57. Rivas-Martínez, S. (2001). Bioclimatic map of Europe – Thermotypes. Léon: University of Léon, Cartographic Service.

    Google Scholar 

  58. Rivera-Mariani, F. E., & Bolanños-Rosero, B. (2012). Allergenicity of airborne basidiospores and ascospores: Need for further studies. Aerobiologia, 28, 83–97.

    Article  Google Scholar 

  59. Roelfs, A. P. (1985). Epidemiology in North America. In A. P. Roelfs & W. R. Bushnell (Eds.), The cereal rusts, diseases, distribution epidemiology and control (pp. 403–434). Orlando: Academic Press.

    Google Scholar 

  60. Russi, L., Romani, M., & Pecetti, L. (2009). Susceptibility to rust (Puccinia sp.) in cultivars of Italian and perennial ryegrass grown in two locations of Italy. Italian Journal of Agronomy, 1, 69–77.

    Article  Google Scholar 

  61. Sadyś, M., Adams-Groom, B., Herbert, R. J., & Kennedy, R. (2016). Comparisons of fungal spore distributions using air sampling at Worcester, England (2006–2010). Aerobiologia. https://doi.org/10.1007/s10453-016-9436-4.

  62. Sansford, C., Beal, E. J., Denton, G., & Denton, J. O. (2015). First report of the rust Puccinia porri on cultivated Allium vineale ‘Hair’. New Disease Reports, 31, 4. https://doi.org/10.5197/j.2044-0588.2015.031.004.

    Article  Google Scholar 

  63. Scocco, E. A., Walcott, R. R., Jeffers, S. N., & Buck, J. W. (2013). Detection of Puccinia pelargonii-zonalis-infected geranium tissues and Urediniospores. Journal of Phytopathology, 161, 341–347.

    CAS  Article  Google Scholar 

  64. Silva, E., Carvalho, R., Nunes, N., Ramos, A. P., & Talhinhas, P. (2016). First report of Puccinia hemerocallidis causing daylily rust in Europe. Plant Disease, 100, 2163. https://doi.org/10.1094/PDIS-02-16-0242-PDN.

    Article  Google Scholar 

  65. Smith, R. S. (1966). The liberation of cereal stem rust uredospores under various environmental conditions in a wind tunnel. Transactions of the British Mycological Society, 49, 33–41.

    Article  Google Scholar 

  66. Talhinhas, P., Silva, E., Nunes, N., & Ramos, A. P. (2016). First report of Puccinia thaliae causing rust on canna spp. in Europe. Plant Disease, 100(6), 1242. https://doi.org/10.1094/PDIS-12-15-1404-PDN.

    Article  Google Scholar 

  67. Tessmanna, D. J., Dianeseb, J. C., Miranda, A. C., & Castro, L. H. R. (2001). Epidemiology of a Neotropical rust (Puccinia psidii): Periodical analysis of the temporal progress in a perennial host (Syzygium Jambos). Plant Patholology, 50, 725–731.

    Article  Google Scholar 

  68. Trejo, F. H., Rodríguez, A. F. M., Molina, F. T., & Palacios, I. S. (2013). Airborne spores of basidiomycetes in Mérida (SW Spain). Annals of Agriculture Environment Medicine, 20, 657–663.

    Google Scholar 

  69. Vodonos, A., Friger, M., Katra, I., Avnon, L., Krasnov, H., Koutrakis, P., et al. (2014). The impact of desert dust exposures on hospitalizations due to exacerbation of chronic obstructive pulmonary disease. Air Quality, Atmosphere and Health. https://doi.org/10.1007/s11869-014-0253-z.

  70. Zadoks, J. C. (1967). International dispersal of fungi. Netherlands Journal of Plant Pathology, Supp. 1, 61–80.

  71. Zanatta, P. (2013). Controle preventivo de doenças foliares em híbridos comerciais de milho com fungicidas em espaçamento reduzido. Master's thesis, Brazil: Universidade Estadual do Centro-Oeste, Unicentro.

Download references

Acknowledgements

The authors are grateful to the Portuguese Society of Allergology and Clinical Immunology (SPAIC) for the help and support in the aerobiological study and the Institute of Ocean and Atmosphere (IPMA) - Regional Station in Funchal for providing the meteorological data. Special thanks go to the Center for Invasive Species and Ecosystem Health, USA, for providing selected images of rust species.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Irene Camacho.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Camacho, I., Leça, R., Sardinha, D. et al. Occurrence of Puccinia spp. spores in Madeira Island and their phytopathological importance. Eur J Plant Pathol 150, 955–969 (2018). https://doi.org/10.1007/s10658-017-1335-1

Download citation

Keywords

  • Rust
  • Inoculum detection
  • Infection conditions
  • Aerobiology
  • Portugal