Statistical model for Plum pox virus prediction in Prunus nursery blocks using vector and virus incidence data in four different European ecological areas

This is the peer reviewed version of the following article: [FULL CITE], which has been published in final form at [Link to final article using the DOI]. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Self-Archiving.[EN] Plum pox virus(PPV) is the causal agent of sharka, the most devastating virus disease ofPrunusspecies. PPV is transmitted by vegetative propagation, particularly by grafting, as well as by aphid species in a nonpersistent manner. The objective of this paper was to evaluate the prevalence and diversity of PPV-vector aphid species in representative European areas of prunus cultivation. Four experimental nursery plots were established in Skierniewice (Poland), Liria (Spain), Plovdiv (Bulgaria) and Bistrita (Romania). Aphid population was weekly monitored using the sticky shoot method in spring and/or autumn in each nursery plot. Furthermore, we estimated the relative efficiency factor for the main PPV-vector aphid species using bibliographic and reference data. Aphid diversity in each nursery plot was assessed using the Shannon index and the number of estimated aphid species was calculated by the rarefaction method. The highest diversity of aphid species population was reported in Plovdiv in spring while the lowest diversity was found in Liria in spring. A cluster analysis based on Morisita-Horn similarity index was performed to study the differences in species composition between the four nursery plots and seasons. Aphid population was clearly grouped by location and season. Results showedAphis spiraecolaandHyalopterus prunicomplex were typically spring aphid species, whileAnoecia corniandRhopalosiphum padidominated autumn catch. Regarding PPV-vector aphid species present in nursery plots,A. spiraecolawas the most prevalent PPV-vector aphid species in Liria and in Bistrita, showing a high relative efficiency factor of PPV transmission (0.91). Consequently,A. spiraecolashould be considered a key actor in the spread of PPV in these regions.Hyalopterus prunicomplex was the most prevalent PPV-vector aphid species in Skierniewice and Plovdiv, showing a very low relative efficiency factor of PPV transmission (0.09). Therefore, the role ofH. prunicomplex in spread of PPV in these regions can be considered negligible. Furthermore, we statistically demonstrated that the presence of specific PPV-vector aphid species is associated with the spread of the disease, whereas the biodiversity of aphid species population does not affect the spread of PPV. Finally, the advantages of the use of vector pressure index in the management of sharka disease are discussed.The research leading to these results were funded by the EU Seventh Framework Programme (FP7/2007-2013), SharCo project grant no. 204429 and by grants from the Spanish Ministry of Science and Education (MEC, AGL2009-07531 and INIA RTA2005-00190). Authors thank I. Baias, S. Sabin (SCDP, Bistrita), B. Tamargo and J. Micó (Cooperativa Vinícola, Líria) for technical assistance in the experimental plots, Viveros Orero and Agromillora Iberia for providing the certified rootstock plants. E. Vidal was recipient of a grant from the Spanish Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA).Vidal, E.; Zagrai, LA.; Malinowski, T.; Soika, G.; Warabieda, W.; Tasheva-Terzieva, E.; Milusheva, S.... (2020). Statistical model for Plum pox virus prediction in Prunus nursery blocks using vector and virus incidence data in four different European ecological areas. Annals of Applied Biology. 177(3):308-324. https://doi.org/10.1111/aab.126173083241773Avinent, L., Hermoso de Mendoza, A., & Llácer, G. (1991). Comparison of traps for capture of alate aphids (Homoptera, Aphidinea) in apricot tree orchards. Agronomie, 11(7), 613-618. doi:10.1051/agro:19910709Barba, M., Hadidi, A., Candresse, T., & Cambra, M. (2011). CHAPTER 36: Plum pox virus. Virus and Virus-Like Diseases of Pome and Stone Fruits, 185-197. doi:10.1094/9780890545010.036Blackman, R. L., & Eastop, V. F. (2007). Taxonomic issues. Aphids as crop pests, 1-29. doi:10.1079/9780851998190.0001BROADBENT, L., & TINSLEY, T. W. (1951). EXPERIMENTS ON THE COLONIZATION OF POTATO PLANTS BY APTEROUS AND BY ALATE APHIDS IN RELATION TO THE SPREAD OF VIRUS DISEASES. Annals of Applied Biology, 38(2), 411-424. doi:10.1111/j.1744-7348.1951.tb07816.xCambra, M., Capote, N., Cambra, M. A., Llácer, G., Botella, P., & López-Quílez, A. (2006). Epidemiology of sharka disease in Spain. EPPO Bulletin, 36(2), 271-275. doi:10.1111/j.1365-2338.2006.00986.xCambra, M., Gorris, M. T., Capote, N., Asensio, M., Martínez, M. C., Bertolini, E., … López, A. (2004). EPIDEMIOLOGY OF PLUM POX VIRUS IN JAPANESE PLUMS IN SPAIN. Acta Horticulturae, (657), 195-200. doi:10.17660/actahortic.2004.657.27Cambra, M., & Vidal, E. (2017). Sharka, a vector-borne disease caused by Plum pox virus: vector species, transmission mechanism, epidemiology and mitigation strategies to reduce its natural spread. Acta Horticulturae, (1163), 57-68. doi:10.17660/actahortic.2017.1163.10Capote, N., Gorris, M. T., Martínez, M. C., Asensio, M., Olmos, A., & Cambra, M. (2006). Interference Between D and M Types of Plum pox virus in Japanese Plum Assessed by Specific Monoclonal Antibodies and Quantitative Real-Time Reverse Transcription-Polymerase Chain Reaction. Phytopathology®, 96(3), 320-325. doi:10.1094/phyto-96-0320Capote, N., Pérez-Panadés, J., Monzó, C., Carbonell, E., Urbaneja, A., Scorza, R., … Cambra, M. (2007). Assessment of the diversity and dynamics of Plum pox virus and aphid populations in transgenic European plums under Mediterranean conditions. Transgenic Research, 17(3), 367-377. doi:10.1007/s11248-007-9112-0Chao, A., & Shen, T.-J. (2003). Environmental and Ecological Statistics, 10(4), 429-443. doi:10.1023/a:1026096204727Chirkov, S., Ivanov, P., Sheveleva, A., Zakubanskiy, A., & Osipov, G. (2017). New highly divergent Plum pox virus isolates infecting sour cherry in Russia. Virology, 502, 56-62. doi:10.1016/j.virol.2016.12.016Colwell, R. K. (2009). III.1 Biodiversity: Concepts, Patterns, and Measurement. The Princeton Guide to Ecology, 257-263. doi:10.1515/9781400833023.257Dallot, S., Gottwald, T., Labonne, G., & Quiot, J.-B. (2003). Spatial Pattern Analysis of Sharka Disease (Plum pox virus Strain M) in Peach Orchards of Southern France. Phytopathology®, 93(12), 1543-1552. doi:10.1094/phyto.2003.93.12.1543Dallot, S., Labonne, G., Boeglin, M., Quiot-Douine, L., Quiot, J. B., & Candresse, T. (1998). PECULIAR PLUM POX POTYVIRUS D-POPULATIONS ARE EPIDEMIC IN PEACH TREES. Acta Horticulturae, (472), 355-366. doi:10.17660/actahortic.1998.472.41Bokx, J. A., & Piron, P. G. M. (1990). Relative efficiency of a number of aphid species in the transmission of potato virus YN in the Netherlands. Netherlands Journal of Plant Pathology, 96(4), 237-246. doi:10.1007/bf01974261DIXON, A. F. G. (1971). The life-cycle and host preferences of the bird cherry-oat aphid, Rhopalosiphum padi L., and their bearing on the theories of host alternation in aphids. Annals of Applied Biology, 68(2), 135-147. doi:10.1111/j.1744-7348.1971.tb06450.xDixon, A. F. G. (1973). Metabolic acclimatization to seasonal changes in temperature in the sycamore aphid, Drepanosiphum platanoides (Schr.), and lime aphid, Eucallipterus tiliae L. Oecologia, 13(3), 205-210. doi:10.1007/bf00360511Dixon, A. F. G., & Hopkins, G. W. (2010). Temperature, Seasonal Development and Distribution of Insects with Particular Reference to Aphids. Aphid Biodiversity under Environmental Change, 129-147. doi:10.1007/978-90-481-8601-3_8Garcêz, R. M., Chaves, A. L. R., Eiras, M., Meletti, L. M. M., de Azevedo Filho, J. A., da Silva, L. A., & Colariccio, A. (2015). Survey of aphid population in a yellow passion fruit crop and its relationship on the spread Cowpea aphid-borne mosaic virus in a subtropical region of Brazil. SpringerPlus, 4(1). doi:10.1186/s40064-015-1263-5García, J. A., Glasa, M., Cambra, M., & Candresse, T. (2014). Plum pox virusand sharka: a model potyvirus and a major disease. Molecular Plant Pathology, 15(3), 226-241. doi:10.1111/mpp.12083Gildow, F., Damsteegt, V., Stone, A., Schneider, W., Luster, D., & Levy, L. (2004). Plum Pox in North America: Identification of Aphid Vectors and a Potential Role for Fruit in Virus Spread. Phytopathology®, 94(8), 868-874. doi:10.1094/phyto.2004.94.8.868Hurlbert, S. H. (1971). The Nonconcept of Species Diversity: A Critique and Alternative Parameters. Ecology, 52(4), 577-586. doi:10.2307/1934145Jevremović, D., Paunović, S. A., & Petrović-Obradović, O. (2016). Flight dynamics and species composition of aphids landing on plum and apricot leaves in the orchards in Western Serbia. Phytoparasitica, 44(4), 501-511. doi:10.1007/s12600-016-0544-zKaya, K., Gazel, M., Serçe, Ç. U., Elçi, E., Cengiz, F. C., Cambra, M., & Çağlayan, K. (2014). Potential vectors of Plum pox virus in the Eastern Mediterranean Region of Turkey. Entomologia Generalis, 35(2), 137-150. doi:10.1127/0171-8177/2014/0019Kimura, K., Usugi, T., Hoshi, H., Kato, A., Ono, T., Koyano, S., … Tsuda, S. (2016). Surveys of Viruliferous Alate Aphid of Plum pox virus in Prunus mume Orchards in Japan. Plant Disease, 100(1), 40-48. doi:10.1094/pdis-05-15-0540-reKindlmann, P., Jarošík, V., & Dixon, A. F. G. (2007). Population dynamics. Aphids as crop pests, 311-329. doi:10.1079/9780851998190.0311Kirchner, S. M., Döring, T. F., Hiltunen, L. H., Virtanen, E., & Valkonen, J. P. T. (2011). Information-theory-based model selection for determining the main vector and period of transmission of Potato virus Y. Annals of Applied Biology, 159(3), 414-427. doi:10.1111/j.1744-7348.2011.00501.xKottek, M., Grieser, J., Beck, C., Rudolf, B., & Rubel, F. (2006). World Map of the Köppen-Geiger climate classification updated. Meteorologische Zeitschrift, 15(3), 259-263. doi:10.1127/0941-2948/2006/0130Labonne, G., Yvon, M., Quiot, J. B., Avinent, L., & Llacer, G. (1995). APHIDS AS POTENTIAL VECTORS OF PLUM POX VIRUS: COMPARISON OF METHODS OF TESTING AND EPIDEMIOLOGICAL CONSEQUENCES. Acta Horticulturae, (386), 207-218. doi:10.17660/actahortic.1995.386.27Leslie, T. W., van der Werf, W., Bianchi, F. J. J. A., & Honěk, A. (2009). Population dynamics of cereal aphids: influence of a shared predator and weather. Agricultural and Forest Entomology, 11(1), 73-82. doi:10.1111/j.1461-9563.2008.00405.xLevy, L., Damsteegt, V., Scorza, R., & Kolber, M. (2000). Plum Pox Potyvirus Disease of Stone Fruits. APSnet Feature Articles. doi:10.1094/apsnetfeature-2000-0300Lowery, D. T., Vickers, P. M., Bittner, L. A., Stobbs, L. W., & Foottit, R. G. (2015). Aphid Transmission of the Ontario Isolate of Plum Pox Virus. Journal of Economic Entomology, 108(5), 2168-2173. doi:10.1093/jee/tov172Manachini, B., Casati, P., Aliverti, I., & Cinanni, L. (2004). Transmission of PPV-M to Prunus persica by Brachycaudus schwartzi and Phorodon humuli (Hem., Aphididae). Journal of Applied Entomology, 128(9-10), 677-680. doi:10.1111/j.1439-0418.2004.00908.xManachini, B., Casati, P., Cinanni, L., & Bianco, P. (2007). Role of Myzus persicae (Hemiptera: Aphididae) and Its Secondary Hosts in Plum Pox Virus Propagation. Journal of Economic Entomology, 100(4), 1047-1052. doi:10.1603/0022-0493(2007)100[1047:rompha]2.0.co;2Marroquı́n, C., Olmos, A., Teresa Gorris, M., Bertolini, E., Carmen Martı́nez, M., Carbonell, E. A., … Cambra, M. (2004). Estimation of the number of aphids carrying Citrus tristeza virus that visit adult citrus trees. Virus Research, 100(1), 101-108. doi:10.1016/j.virusres.2003.12.018Moreno, A., Bertolini, E., Olmos, A., Cambra, M., & Fereres, A. (2007). Estimation of vector propensity for Lettuce mosaic virus based on viral detection in single aphids. Spanish Journal of Agricultural Research, 5(3), 376. doi:10.5424/sjar/2007053-5343Moreno, A., Fereres, A., & Cambra, M. (2009). Quantitative estimation of plum pox virus targets acquired and transmitted by a single Myzus persicae. Archives of Virology, 154(9), 1391-1399. doi:10.1007/s00705-009-0450-5Ng, J. C. K., & Falk, B. W. (2006). Virus-Vector Interactions Mediating Nonpersistent and Semipersistent Transmission of Plant Viruses. Annual Review of Phytopathology, 44(1), 183-212. doi:10.1146/annurev.phyto.44.070505.143325Olmos, A., Cambra, M., Dasi, M. A., Candresse, T., Esteban, O., Gorris, M. T., & Asensio, M. (1997). Simultaneous detection and typing of plum pox potyvirus (PPV) isolates by heminested-PCR and PCR-ELISA. Journal of Virological Methods, 68(2), 127-137. doi:10.1016/s0166-0934(97)00120-1Perez, P., Collar, J. L., Avilla, C., Duque, M., & Fereres, A. (1995). Estimation of Vector Propensity of Potato Virus Y in Open-Field Pepper Crops of Central Spain. Journal of Economic Entomology, 88(4), 986-991. doi:10.1093/jee/88.4.986RACCAH, B., GAL-ON, A., & EASTOP, V. F. (1985). The role of flying aphid vectors in the transmission of cucumber mosaic virus and potato virus Y to peppers in Israel. Annals of Applied Biology, 106(3), 451-460. doi:10.1111/j.1744-7348.1985.tb03135.xRimbaud, L., Dallot, S., Gottwald, T., Decroocq, V., Jacquot, E., Soubeyrand, S., & Thébaud, G. (2015). Sharka Epidemiology and Worldwide Management Strategies: Learning Lessons to Optimize Disease Control in Perennial Plants. Annual Review of Phytopathology, 53(1), 357-378. doi:10.1146/annurev-phyto-080614-120140SCHOLTHOF, K.-B. G., ADKINS, S., CZOSNEK, H., PALUKAITIS, P., JACQUOT, E., HOHN, T., … FOSTER, G. D. (2011). Top 10 plant viruses in molecular plant pathology. Molecular Plant Pathology, 12(9), 938-954. doi:10.1111/j.1364-3703.2011.00752.xSequeira, R., & Dixon, A. F. G. (1997). POPULATION DYNAMICS OF TREE-DWELLING APHIDS:THE IMPORTANCE OF SEASONALITY AND TIME SCALE. Ecology, 78(8), 2603-2610. doi:10.1890/0012-9658(1997)078[2603:pdotda]2.0.co;2Smith, W., & Grassle, J. F. (1977). Sampling Properties of a Family of Diversity Measures. Biometrics, 33(2), 283. doi:10.2307/2529778Strażyński, P., & Ruszkowska, M. (2015). The life cycle functional response of Rhopalosiphum padi (L.) to higher temperature: territorial expansion of permanent parthenogenetic development as a result of warmer weather conditions. Journal of Plant Protection Research, 55(2), 162-165. doi:10.1515/jppr-2015-0021Van Dyke, F. (2008). Conservation Biology. doi:10.1007/978-1-4020-6891-1Van Harten, A. (1983). The relation between aphid flights and the spread of potato virus YN (PVYN) in the Netherlands. Potato Research, 26(1), 1-15. doi:10.1007/bf02357369Verbeek, M., Piron, P. G. M., Dullemans, A. M., Cuperus, C., & Van Der Vlugt, R. A. A. (2010). Determination of aphid transmission efficiencies for N, NTN and Wilga strains of Potato virus Y. Annals of Applied Biology, 156(1), 39-49. doi:10.1111/j.1744-7348.2009.00359.xVidal, E., Moreno, A., Bertolini, E., Pérez-Panadés, J., Carbonell, E. A., & Cambra, M. (2010). Susceptibility of Prunus rootstocks to natural infection of Plum pox virus and effect of mineral oil treatments. Annals of Applied Biology, 157(3), 447-457. doi:10.1111/j.1744-7348.2010.00436.xVidal, E., Zagrai, L., Milusheva, S., Bozhkova, V., Tasheva-Terzieva, E., Kamenova, I., … Cambra, M. (2013). Horticultural mineral oil treatments in nurseries during aphid flights reducePlum pox virusincidence under different ecological conditions. Annals of Applied Biology, 162(3), 299-308. doi:10.1111/aab.12022Wallis, C. M., Fleischer, S. J., Luster, D., & Gildow, F. E. (2005). Aphid (Hemiptera: Aphididae) Species Composition and Potential Aphid Vectors of Plum Pox Virus in Pennsylvania Peach Orchards. Journal of Economic Entomology, 98(5), 1441-1450. doi:10.1093/jee/98.5.1441Whittaker, R. H. (1960). Vegetation of the Siskiyou Mountains, Oregon and California. Ecological Monographs, 30(3), 279-338. doi:10.2307/1943563Wolda, H. (1981). Similarity indices, sample size and diversity. Oecologia, 50(3), 296-302. doi:10.1007/bf0034496