Epidemiological and mathematical modeling of vascular and wood‑decay pathogens in almond orchards: a conceptual and theoretical analysis

Ioannis Vagelas

Abstract


Almond decline in Mediterranean and warm temperate areas arises from two distinct but interacting pathosystems: systemic vascular dysfunction caused by Xylella fastidiosa and structural wood degradation caused by fungal species of the Botryosphaeriaceae family. In this research we developed an age-structured multiplicative model for decline that incorporates several interrelated aspects of decline, including infection likelihood, vascular dysfunction, the dynamics of fungal colonization, and the impact of applying chemical control products, to quantify their combined contribution to orchard decline and eventual collapse. Co-infections exhibit a synergistic, accelerating component to their decline, with vascular dysfunction reaching saturation levels early on and therefore strongly limiting orchard life expectancy. Chemical control products such as fungicides, copper and phosphonates significantly lower the effective fungal growth rate and extend the timeline for orchard decline by 1-5 years, but does not eliminate the hydraulic failure in trees infected by Xylella. In fungal‑only systems, application of chemical controls significantly reduces the rate of decline trajectories and enhances orchard longevity. Our model describes the physiological processes that lead to increased decline rates in mixed infections and provides a quantitative framework for evaluating management strategies. Because X. fastidiosa is absent from Greece, the model is developed as a conceptual and theoretical framework grounded in published physiological and epidemiological data.


Keywords


Almond decline, Xylella fastidiosa, Botryosphaeriaceae, Co‑infection, Vascular dysfunction, Canker diseases, Epidemiological modeling, Orchard longevity, Chemical management, Age‑structured decline

Full Text:

PDF

References


Amponsah, N.T., Jones, E.E., Ridgway, H.J., Jaspers, M.V., 2012. Evaluation of fungicides for the management of Botryosphaeria dieback diseases of grapevines. Pest Management Science 68 5, 676-83.

Anguita-Maeso, M., Ares-Yebra, A., Haro, C., Román-Écija, M., Olivares-García, C., Costa, J.C., Marco-Noales, E., Ferrer, A., Navas‐Cortés, J.A., Landa, B.B., 2022. Xylella fastidiosa infection reshapes microbial composition and network associations in the xylem of almond trees. Frontiers in Microbiology 13.

Antón Domínguez, B.I., López‐Moral, A., Raya-Ortega, M.C., Lovera, M., Melgar, S., Roca-Castillo, L.F., Arquero, O., Trapero-Casas, A., Agustí‐Brisach, C., 2023. Fungal pathogens associated with almond decline syndrome, an emerging disease complex in intensive almond crops in southern spain. Plant Disease 107(1)2, 3737-3753.

Antony, S., Steel, C.C., Stodart, B.J., Billones-Baaijens, R., Savocchia, S., 2024. Evaluation of fungicides for management of Botryosphaeriaceae associated with dieback in Australian walnut orchards. Phytopathologia Mediterranea 63(1), 119-134.

Bergamaschi, V., Valente, M.T., Muleo, R., 2025. Pomegranate woody mycobiota associated with wood decay. Journal of Fungi, 11.

Bragard, C., Dehnen‐Schmutz, K., Di Serio, F., Gonthier, P., Jacques, M., Jaques Miret, J.A., Justesen, A.F., MacLeod, A., Magnusson, C.S., Milonas, P.G., Navas‐Cortés, J.A., Potting, R.P., Reignault, P., Thulke, H., van der Werf, W., Vicent Civera, A., Yuen, J.E., Zappalà, L., Boscia, D., Chapman, D.S., Gilioli, G., Krugner, R., Mastin, A.J., Simonetto, A., Spotti Lopes, J.R., White, S.M., Abrahantes, J.C., Delbianco, A., Maiorano, A., Mosbach‐Schulz, O., Stancanelli, G., Guzzo, M., Parnell, S.R., 2019. Update of the Scientific Opinion on the risks to plant health posed by Xylella fastidiosa in the EU territory. EFSA Journal 17.

Brauer, F., 2017. Mathematical epidemiology: Past, present, and future. Infectious Disease Modelling 2(2), 113-127.

Brent, K.J., Hollomon, D.W., 2007. Fungicide resistance: The assessment of risk. FRAC Monograph No. 2. https://www.frac.info/media/23rp130k/monograph-2.pdf

Camposeo, S., Vivaldi, G.A., Saponari, M., 2022. Attempts to reduce the systemic spread of Xylella fastidiosa in olive trees by pruning. Agronomy 12(1)2, 2917.

Cardinale, M., Luvisi, A., Meyer, J.B., Sabella, E., De Bellis, L., Cruz, A.C., Ampatzidis, Y., Cherubini, P., 2018. Specific fluorescence in situ hybridization (FISH) test to highlight colonization of xylem vessels by Xylella fastidiosa in naturally infected olive trees (Olea europaea L.). Frontiers in Plant Science, 9.

Cendoya, M., Navarro-Quiles, A., López-Quílez, A., Vicent, A., Conesa, D., 2024. An individual-based spatial epidemiological model for the spread of plant diseases. Journal of Agricultural, Biological and Environmental Statistics 30, 618 - 637.

Chatterjee, S., Almeida, R.P., Lindow, S.E., 2008. Living in two worlds: the plant and insect lifestyles of Xylella fastidiosa. Annual Review of Phytopathology 46, 243-71.

Cunniffe, N.J., Stutt, R.O., DeSimone, R.E., Gottwald, T.R., Gilligan, C.A., Tanaka, M.M., 2015. Optimising and communicating options for the control of invasive plant disease when there is epidemiological uncertainty. Plos Computational Biology, 11.

Distefano, G., Kodad, O., Inzirillo, I., Allach, K., Catalano, C., Luca, L.P., Ruiz Artiga, V., Espiau Ramírez, M.T., Grimplet, J., Bielsa, B., Erami, M., Uzun, A., El Yaacoubi, A., Rubio-Cabetas, M.J., 2026. Almond: domestication, germplasm, drought stress tolerance and genetic improvement perspectives. Horticulturae 12(4), 493.

Gaire, A., KC, A.N., 2025. Evaluation of copper-based fungicides for Botryosphaeria dieback management of grapevines in central point, OR, 2024. Plant Health Progress 26(4), 740.

Garcia, J.F., Lawrence, D.P., Morales-Cruz, A., Travadon, R., Minio, A., Hernández-Martínez, R., Rolshausen, P.E., Baumgartner, K., Cantu, D., 2021. Phylogenomics of plant-associated Botryosphaeriaceae species. Frontiers in Microbiology 12.

Giampetruzzi, A., Velasco-Amo, M.P., Marco-Noales, E., Montes-Borrego, M., Román-Écija, M., Navarro, I., Monterde, A., Barbé, S., Almeida, R.P., Saldarelli, P., Saponari, M., Montilon, V., Savino, V.N., Boscia, D., Landa, B.B., 2019. Draft genome resources of two strains (“ESVL” and “IVIA5901”) of Xylella fastidiosa associated with almond leaf scorch disease in Alicante, Spain. Phytopathology 109(2), 219-221.

Gilligan, C.A., 2008. Sustainable agriculture and plant diseases: an epidemiological perspective. Philosophical Transactions of the Royal Society B: Biological Sciences 363, 741-759.

González-Domínguez, E., Fedele, G., Salinari, F., Rossi, V., 2020. A general model for the effect of crop management on plant disease epidemics at different scales of complexity. Agronomy 10(4), 462.

Gramaje, D., Agustí-Brisach, C., Pérez-Sierra, A., Moralejo, E., Olmo, D., Mostert, L., Damm, U., Armengol, J., 2012. Fungal trunk pathogens associated with wood decay of almond trees on Mallorca (Spain). Persoonia : Molecular Phylogeny and Evolution of Fungi 28, 1-13.

Guest, D. I., Grant, B. R., 1991. The complex action of phosphonates as antifungal agents. Biological Reviews 66(2), 159-187.

Holland, L.A., Trouillas, F.P., Nouri, M.T., Lawrence, D.P., Crespo, M., Doll, D., Duncan, R., Holtz, B.A., Culumber, C.M., Yaghmour, M.A., Niederholzer, F.J., Lightle, D.M., Jarvis-Shean, K.S., Gordon, P.E., Fichtner, E.J., 2020. Fungal pathogens associated with canker diseases of almond in California. Plant disease.

Krugner, R., Ledbetter, C.A., 2016. Rootstock effects on almond leaf scorch disease incidence and severity. Plant disease 100(8), 1617-1621.

Lalancette, N., Robison, D.M., 2002. Effect of fungicides, application timing, and canker removal on incidence and severity of constriction canker of peach. Plant disease 86(7), 721-728.

Linaldeddu, B.T., Rossetto, G., Maddau, L., Vatrano, T.P., Bregant, C., 2023. Diversity and pathogenicity of Botryosphaeriaceae and Phytophthora species associated with emerging olive diseases in Italy. Agriculture 13(8), 1575.

Loureiro, T., Mesquita, M.M., Dapkevicius, M.D., Serra, L., Martins, Â., Cortez, I., Poeta, P., 2023. Xylella fastidiosa: A glimpse of the Portuguese situation. Microbiology Research 14(4), 1568-1588.

Luque‐Cruz, C., Capote, N., Marco‐Noales, E., Palomares‐Rius, J.E., Romero-Cuadrado, L., Morán, F., Armengol, J., Agustí‐Brisach, C., 2026. Insights into the aetiology of almond canker diseases and decline syndromes: an emerging and complex phytopathological challenge. Plant Pathology 75(1). https://doi.org/10.1111/ppa.70126

Madden, L.V., Hughes, G., van den Bosch, F., 2017. The Study of Plant Disease Epidemics.

Manetti, G., Brunetti, A., Lumia, V., Sciarroni, L., Marangi, P., Cristella, N., Faggioli, F., Reverberi, M., Scortichini, M., Pilotti, M., 2023. Identification and characterization of Neofusicoccum stellenboschiana in branch and twig dieback-affected olive trees in Italy and comparative pathogenicity with N. Mediterranean. Journal of Fungi, 9(3), 292.

Mansfield, J., Genin, S., Magori, S., Citovsky, V., Sriariyanum, M., Ronald, P.C., Dow, M., Verdier, V., Beer, S.V., Machado, M.A., Toth, I.K., Salmond, G.P., Foster, G.D., 2012. Top 10 plant pathogenic bacteria in molecular plant pathology. Molecular Plant Pathology 13(6), 614-29.

Marco-Noales, E., Barbé, S., Monterde, A., Navarro, I., Ferrer, A., Dalmau, V., Aure, C.M., Domingo-Calap, M.L., Landa, B.B., Roselló, M., 2021. Evidence that Xylella fastidiosa is the causal agent of almond leaf scorch disease in Alicante, mainland Spain (Iberian Peninsula). Plant disease 105(1)1, 3349-3352.

Moral, J., Muñoz-Díez, C., González, N., Trapero, A., Michailides, T.J., 2010. Characterization and pathogenicity of Botryosphaeriaceae species collected from olive and other hosts in Spain and California. Phytopathology, 100(12), 1340-1351.

Moralejo, E., Gomila, M., Montesinos, M., Borras, D., Pascual, A., Nieto, A., Adrover, F., Gost, P.A., Seguí, G., Busquets, A., Jurado-Rivera, J.A., Quetglas, B., García, J.D., Beidas, O.E., Juan, A., Velasco-Amo, M.P., Landa, B.B., Olmo, D., 2020. Phylogenetic inference enables reconstruction of a long-overlooked outbreak of almond leaf scorch disease (Xylella fastidiosa) in Europe. Communications Biology, 3(1). https://doi.org/10.1038/s42003-020-01284-7

Olmo, D., Armengol, J., León, M., Gramaje, D., 2016. Characterization and pathogenicity of Botryosphaeriaceae species isolated from almond trees on the island of Mallorca (Spain). Plant Disease 100(12), 2483-2491.

Petit, G., Bleve, G., Gallo, A., Mita, G., Montanaro, G., Nuzzo, V., Zambonini, D., Pitacco, A., 2021. Susceptibility to Xylella fastidiosa and functional xylem anatomy in Olea europaea: revisiting a tale of plant–pathogen interaction. AoB Plants, 13(4). https://doi.org/10.1093/aobpla/plab027

Rapicavoli, J.N., Ingel, B., Blanco‐Ulate, B., Cantu, D., Roper, C., 2018. Xylella fastidiosa: an examination of a re-emerging plant pathogen. Molecular Plant Pathology 19(4), 786-800.

Retamal, V., San Martín, J.G., Ruíz, B., Bastías, R.M., Sanfuentes, E., Lisperguer, M.J., De Gregorio, T., Maspero, M., Moya-Elizondo, E.A., 2024. Assessment of chemical and biological fungicides for the control of Diplodia mutila causing wood necrosis in hazelnut. Plants, 13(9), 2753.

Sabella, E., Aprile, A., Genga, A., Siciliano, T., Nutricati, E., Nicolì, F., Vergine, M., Negro, C., De Bellis, L., Luvisi, A., 2019. Xylem cavitation susceptibility and refilling mechanisms in olive trees infected by Xylella fastidiosa. Scientific Reports, 9(1). https://doi.org/10.1038/s41598-019-46092-0

Scortichini, M., Loreti, S., Scala, V., Pucci, N., Pilotti, M., Tatulli, G., Cesari, E., L'Aurora, A., Reverberi, M., Cristella, N., Marangi, P., Blonda, P.N., Tarantino, C., Adamo, P., Maggi, S., Cesari, G., Girelli, C.R., Angilè, F., Hussain, M., Migoni, D., Fanizzi, F.P., 2024. Management of the olive decline disease complex caused by Xylella fastidiosa subsp. pauca and Neofusicoccum spp. in Apulia, Italy. Crop Protection 184, 106782.

Scortichini, M., Manetti, G., Brunetti, A., Lumia, V., Sciarroni, L., Pilotti, M., 2023. Xylella fastidiosa subsp. pauca, Neofusicoccum spp. and the decline of olive trees in Salento (Apulia, Italy): comparison of symptoms, possible interactions, certainties and doubts. Plants, 12(20), 3593.

Serio, F.D., Imbriani, G., Girelli, C.R., Miglietta, P.P., Scortichini, M., Fanizzi, F.P., 2024. A Decade after the Outbreak of Xylella fastidiosa subsp. pauca in Apulia (Southern Italy): Methodical Literature Analysis of Research Strategies. Plants, 13(11), 1433.

Slippers, B., Wingfield, M.J. (2007). Botryosphaeriaceae as endophytes and latent pathogens of woody plants: diversity, ecology and impact. Fungal Biology Reviews, 21, 90-106.

Torguet, L., Zazurca, L., Martínez, G., Pons-Solé, G., Luque, J., Miarnau, X., 2022. Evaluation of fungicides and application strategies for the management of the red leaf blotch disease of almond. Horticulturae 8(6), 501.

Trkulja, V., Tomić, A., Iličić, R., Nožinić, M., Milovanović, T.P., 2022. Xylella fastidiosa in Europe: From the Introduction to the Current Status. The Plant Pathology Journal 38, 551-571.

Úrbez Torres, J.R., Leavitt, G.M., Guerrero, J.C., Guevara, J., Gubler, W.D., 2008. Identification and pathogenicity of Lasiodiplodia theobromae and Diplodia seriata, the causal agents of bot canker disease of grapevines in Mexico. Plant Disease 92(4), 519-529.

Vagelas, I., 2026. A Dynamic SEIR Approach to foliar disease management in wheat: Linking fungicide timing to epidemic growth rate suppression. Molecular Sciences and Applications, 6, 35-53.

Valdez-Tenezaca, A., Lolas, M.A., Núñez, F.B., Latorre, B., Mostert, L., Halleen, F., Ferrada, E., Díaz, G.A., 2025. Efficacy of pruning-wound protectant fungicides for the management of Botryosphaeria canker and dieback of apple trees in Maule region, Chile. Plant Disease 109(10), 2190-2196.

White, S.M., Bullock, J.M., Hooftman, D.A., Chapman, D.S., 2017. Modelling the spread and control of Xylella fastidiosa in the early stages of invasion in Apulia, Italy. Biological Invasions 19, 1825-1837.

White, S.M., Bullock, J.M., Hooftman, D.A., Chapman, D.S., 2017. Modelling the spread and control of Xylella fastidiosa in the early stages of invasion in Apulia, Italy. Biological Invasions 19(6), 1825-1837.

Wu, H., Dahlsjö, C.A., Malhi, Y.S., 2024. Evaluating the impact of an invasive pathogen on tree population decline: An evidence based modelling approach. Forest Ecology and Management, 566, 122098.




DOI: https://doi.org/10.33804/pp.010.05.6245

Refbacks

  • There are currently no refbacks.