Field susceptibility of almond cultivars to the four most common aerial fungal diseases in southern Spain

Accepted Manuscript Field susceptibility of almond cultivars to the four most common aerial fungal diseases in southern Spain Andrés Ollero-Lara, Carlos Agustí-Brisach, María Lovera, Luis F. Roca, Octavio Arquero, Antonio Trapero PII:

S0261-2194(19)30079-1

DOI:

https://doi.org/10.1016/j.cropro.2019.03.005

Reference:

JCRP 4757

To appear in:

Crop Protection

Received Date: 21 July 2018 Revised Date:

12 March 2019

Accepted Date: 13 March 2019

Please cite this article as: Ollero-Lara, André., Agustí-Brisach, C., Lovera, Marí., Roca, L.F., Arquero, O., Trapero, A., Field susceptibility of almond cultivars to the four most common aerial fungal diseases in southern Spain, Crop Protection (2019), doi: https://doi.org/10.1016/j.cropro.2019.03.005. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

ACCEPTED MANUSCRIPT

Field susceptibility of almond cultivars to the four most common aerial

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fungal diseases in southern Spain

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Andrés Ollero-Laraa,1, Carlos Agustí-Brisacha,1, María Loverab, Luis F. Rocaa,

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Octavio Arquerob, Antonio Traperoa,*

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a

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Rabanales, Building C4, 14071 Córdoba, Spain.

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Formation in Agriculture and Fishery (IFAPA), Av. Menéndez Pidal s/n, 14004,

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Córdoba, Spain

Department of Agronomy, ETSIAM, University of Cordoba (UCO), Campus de

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Department of Mediterranean Fruticulture, Andalusian Institute for Research and

*Corresponding author. E-mail address: [email protected] (A. Trapero).

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These authors contributed equally to this work and are co-first authors.

ABSTRACT

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From 2004 to 2012, the incidence and severity of the four most common almond aerial

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diseases were evaluated in ten experimental fields in the main almond-growing areas of

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Andalusia, southern Spain. The studied experimental fields were representative of the

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different geographic locations, agronomic characteristics and farming systems in

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Andalusia. A total of 14 early-flowering and 26 late-flowering cultivars (cvs.) currently

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grown in the new almond plantings of Andalusia and the Mediterranean basin were

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evaluated. The incidences of red leaf blotch (RLB), shot hole (SH), blossom blight

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(BB), and leaf curl (LC), which were caused by Polystigma amygdalinum, Thyrostroma

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carpophilum, Monilia laxa and Taphrina deformans, respectively, were monitored in

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each field and year. RLB was the most prevalent disease, although its severity varied

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markedly among fields and years. BB caused the higher outbreaks, but this was only the

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ACCEPTED MANUSCRIPT case when rainfall coincided with flowering, and fungicide treatments were not applied.

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The early-flowering cvs. were more affected than the late-flowering cvs. by BB,

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although most of the early-flowering cvs. were less susceptible than the reference cv.

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Marcona to BB. However, ‘Marcona’ was less susceptible than most of the early-

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flowering cvs. to RLB. Among the late-flowering cvs., the reference cv. Guara was

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susceptible to the four monitored diseases. The responses of the cvs. to the diseases

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varied markedly among fields and years, with significant differences among cvs. for all

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diseases. This work represents the first study to evaluate a broad range of almond cvs.

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infected with the main almond foliar diseases in natural field conditions, making an

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important contribution to the understanding of varietal susceptibility of almonds to four

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significant foliar diseases. Moreover, this study highlights the need to consider cultivar

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resistance in the development and selection of plant material for new almond plantings

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and in integrated pest management.

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Keywords Blossom blight, Cultivar susceptibility, Leaf curl, Prunus dulcis, Red leaf

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blotch, Shot hole

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Highlights

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-Understanding of varietal susceptibility of almonds to foliar diseases.

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-Red leaf blotch, caused by Polystigma amygdalinum, was the most prevalent disease.

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-The responses of the cultivars varied markedly among different fields, years, and

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diseases.

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-This work highlights the need to consider cultivar resistance for new almond plantings.

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Abbreviations: RLF: Red leaf blotch; SH: Shot hole; BB: Blossom blight; LC: Leaf

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curl; AA: Almond anthracnose; IFAPA: Instituto de Investigación y Formación Agraria

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y Pesquera de Andalucía (Andalusian Institute for Research and Formation in

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Agriculture and Fishery); RAIF: Red de Alerta e Información Fitosanitaria

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(Phytosanitary Warning and Information Network); DS: Disease severity.

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1. Introduction Almond (Prunus dulcis L.) is a traditional crop in the Mediterranean basin and is

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the fruit crop with the second highest acreage in Spain, after cultivated olive (Olea

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europaea subsp. europaea L.). Based on surface area, Spain currently leads the world in

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almond cultivation, with more than 500,000 ha of cultivated almond; approximately

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28% of this land is in the Andalusia region of southern Spain (Arquero et al., 2013).

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Almond has traditionally been cultivated in marginal areas with unfavorable

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climatic, edaphic, and orographic conditions, and the local early-flowering almond

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cultivars (cvs.) Desmayo Largueta and Marcona are the most common in southern Spain

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(Arquero et al., 2013). However, due to the need to enhance the competitiveness of

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almond production in the global market, there has been a shift in the last few years from

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traditional dry-farming cultivation systems to more intensive almond cropping systems

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based on high-input strategies such as dense planting, summer irrigation,

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mechanization, fertilizers and pesticides in order to increase yields and decrease

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production costs. Indeed, almond kernel production from intensive systems exceeds

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1,000 kg ha-1, while in traditional almond cropping systems it is usually less than 150 kg

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ha-1. Consequently, local cvs. has been replaced with new cvs. that are suitable for

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intensive cultivation systems, such as the late-flowering almond cvs. Guara, Ferragnès

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and Lauranne (Arquero et al., 2013; Ollero-Lara et al., 2016). As a consequence,

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almond-growing areas are experiencing an increase in the incidence and prevalence of

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diseases, as well as the re-emergence of diseases favored by: i) more intensive

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cultivation systems; ii) the introduction and widespread use of new disease-susceptible

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cvs; and iii) the climatic conditions of the new almond growing areas which are

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favorable for the infection and development of fungal diseases. The most common and prevalent fungal aerial diseases affecting almond in the

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Andalusia region are red leaf blotch (RLB) caused by the ascomycete Polystigma

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amygdalinum P.F. Cannon (synonym P. ochraceum (Fr.) Sacc. ), shot hole (SH) caused

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by the ascomycete Thyrostroma carpophilum (Lév.) B. Sutton, blossom blight (BB)

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caused by Monilia spp., and leaf curl (LC) caused by Taphrina deformans (Berk.) Tul.

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(Ollero-Lara et al., 2016). Although these four fungal diseases are the most common

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aerial almond diseases, since 2014, serious symptoms of almond anthracnose (AA) have

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been observed in commercial almond orchards in the provinces of Huelva and Sevilla

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from the Andalusia region, southern Spain (López-Moral et al., 2016; 2017). Although

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anthracnose is a major almond disease worldwide, the incidence of AA in Andalusia is

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still low due to its recent re-emergence as a consequence of the new establishment of

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almond plantings in non-traditional almond growing areas (López-Moral et al., 2016;

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2017).

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Of the four most common fungal aerial diseases of almond in southern Spain,

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RLB is considered the most prevalent disease in all growing regions of the

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Mediterranean countries. RLB symptoms are restricted to the foliage. Lesions begin as

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minute circular, elliptical, or irregularly shaped spots 30-35 days after infection.

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Incipient lesions develop into larger blotches (10-22 mm in diameter) composed of the

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pathogen stromata intermixed with host tissue. The blotches are initially yellow and

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then successively turn orange, red, brown, and finally black, acquiring a crusty texture

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with the changes in color. Infection causes foliage hypertrophy, and infected leaves roll

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inward, culminating in a premature defoliation when severe epidemics occur

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(Teviotdale et al., 2002; Ollero-Lara et al., 2016; Palacio-Bielsa et al., 2017). SH has

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ACCEPTED MANUSCRIPT been reported in all of the almond-growing regions of the world, and it has also been

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described affecting other Prunus spp., mainly P. armeniaca L. and P. persica (L.)

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Stokes. In Spain, the disease is very common in all Prunus fruit trees, but its importance

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depends on the climatic conditions specific to areas and years. The most characteristic

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symptoms of SH are observed on leaves and consist of localized circular lesions that

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begin as small, purple areas and expand to chlorotic and then necrotic tannish spots (3-

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10 cm in diameter). Subsequently, in infected leaves remaining on the tree, the lesions

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coalesce and cause numerous circular holes. Although stem and bud infections are

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common in other Prunus such as peach or nectarine, they are not frequent in almond.

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On fruit, circular lesions are also observed, usually on the upper side of the fruit, and the

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infection is associated with gumming when the fruit lesions abscise (Teviotdale et al.,

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2002; Ollero-Lara et al., 2016; Palacio-Bielsa et al., 2017). BB, a flower and fruit

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disease, is one of the major diseases of almond and other stone fruit crops worldwide.

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The disease is caused by Monilia fructigena (Pers.) Pers., M. fructicola (L.R. Batra) and

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M. laxa (Ehrenb.) Sacc. & Voglino, and M. laxa being the most common pathogen

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species in almond (Teviotdale et al., 2002-; Palacio-Bielsa et al., 2017). Symptoms of

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BB in almond are associated with two different syndromes: i) blossom, bud and shoot

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blight and ii) cankers on infected twigs and branches. BB begins in the anthers and

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progress across the stigma or anther filaments, and the plant tissues become brown and

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necrotic as the infection extends into the peduncle. The blossom collapses and turns

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brown, and gum develops at the base of the blighted flowers which then remain on the

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shoots. When the infection progresses into the twigs, elliptical and fusoid cankers

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develop, with gum forming at the advancing margin. The affected twigs that finally die

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retain their leaves, which turn tan to brown (Teviotdale et al., 2002; Ollero-Lara et al.,

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2016; Palacio-Bielsa et al., 2017). Finally, although LC is considered the most serious

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ACCEPTED MANUSCRIPT disease of P. persica, it is rare in almond (Teviotdale et al., 2002; Palacio-Bielsa et al.,

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2017). In the spring, the LC infection causes foliage hypertrophy, and young leaves

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develop thick and punctured areas. As the infection progresses, the color of these areas

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changes from bright red to light green, turning white when the pathogen sporulates.

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Frequently, the infection affects all the shoot, causing shoot deformation. However, fruit

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infection is rare (Teviotdale et al., 2002; Ollero-Lara et al., 2016; Palacio-Bielsa et al.,

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2017).

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Although these four diseases cause serious damage to almond crops and

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associated economic loses, to date, there have been no conclusive reports about the

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susceptibility of the main almond cvs. to RLB, SH, BB and LC in the Andalusia region.

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Even though there are some publications referencing this topic in the main Spanish

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almond-growing areas, including southern Spain (Egea et al., 1984; Navarro, 1996,

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2002; Salazar and Melgarejo, 2002; Egea et al., 2003; Malagón, 2007; Dicenta et al.,

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2010), this information comes from field observations that are not based on an

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experimental design, resulting in contradictory and unclear conclusions. Therefore, the

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aim of this study was to elucidate the susceptibility and resistance of almond cvs. to the

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four most common foliar diseases of the almond crop. To this end, we compared the

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susceptibilities of a broad range of almond cvs. to RLB, SH, BB and LC in naturally

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infected almond orchards via experimental field networks established in the main

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almond-growing regions of Andalusia.

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2. Material and Methods

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2.1. Experimental fields

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The susceptibility of almond to RLB, SH, BB and LC was evaluated from 2004

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to 2012 in ten different almond orchards within the experimental fields network 6

ACCEPTED MANUSCRIPT established in Andalusia (southern Spain) by the Andalusian Institute for Research and

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Formation in Agriculture and Fishery (IFAPA in Spanish) in collaboration with

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Andalusian almond growers. The experimental fields were planted in two periods, the

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first between 2000 and 2002 and the second between 2010 and 2012, and are distributed

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in the main almond-producing areas of Andalusia (the provinces of Almería, Córdoba,

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Granada, Huelva and Málaga) (Fig. 1; Table 1). The fields are representative of the

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different geographic locations, edapho-climatic characteristics and farming systems in

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Andalusia (Table 2). During the study, the experimental fields were managed according

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to the principles of each type of farming system (conventional, dry or irrigated; or

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organic) used in Andalusia. The experimental field networks comprise a broad range of

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traditional and novel commercial almond cvs. (40 in total) including early-flowering (14

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out of 40) and late-/extra-late-flowering (26 out of 40) cvs. The distribution of the early-

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and late-flowering almond cvs. in the experimental fields network is described in Table

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1. For comparative purposes, ‘Marcona’ and ‘Guara’ were selected as the reference cvs.

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(control) of the early- and late-flowering cvs., respectively. These two cvs. were

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selected because their susceptibility to almond diseases and their high importance and

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frequency in the main almond-growing areas in Andalusia (Arquero et al., 2013).

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Moreover, the climatic conditions were monitored over time in the five Andalusian

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provinces involved in this work via the Andalusian weather station network, which

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belongs to the IFAPA and to the Phytosanitary Warning and Information Network

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(known as RAIF in Spanish). The data of the different weather stations reported for

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each experimental field of this study are shown in Table 3.

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For the experimental design, there were at least twelve replicate trees per cv. in a

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completely randomized block design. The number of blocks ranged from two to six and

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the number of replicate trees per elemental plot ranged from two to ten, depending on 7

ACCEPTED MANUSCRIPT the availability of almond trees per cv. The experimental design and the number of cvs.

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evaluated in each experimental field are specified in Table 2. In addition, at least six

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almond plants of cvs. different to the main ones evaluated in each experimental field

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(Table 4) were planted between blocks as well as along the border of the main plots as

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guard line in a completely randomized design. Susceptibility of almond cvs. from the

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line guard to the four foliar diseases was also evaluated as described below.

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2.2. Disease severity assessment

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All the experimental fields in the three networks established for this study (Fig.

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1; Table 1) were monitored for natural infections of RLB, SH, BB and LC between

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2004 and 2012. During this period, the susceptibility of almond to each foliar disease

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was assessed only in the fields and years in which the diseases showed high enough

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incidence levels (more than 0.25%) to be evaluated. The disease severity (DS) was

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assessed by two different methods according to the disease to be evaluated. For RLB

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and SH diseases, which had a higher incidence, about 40-100 leaves per tree were

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sampled, depending on the experimental design, to reach a total of 800 leaves per

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cultivar. These leaves were taken to the laboratory where the percentage of leaf surface

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with disease symptoms was directly estimated in each leaf. For BB and LC diseases,

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which had a lower incidence, the percentage of affected shoots per tree was determined

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using a 0-9 rating scale, based on the 0-10 scale for olive anthracnose (Moral and

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Trapero, 2009), although with a slight modification that consisted in joining the values

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of 9 and 10 of the olive scale in a single value of 9 for these almond diseases. The

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values of this scale have a logistic relationship with the percentage of affected tissues

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(leaves, fruits, shoots). Thus, data delivered from the scale results in better homogeneity

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of variances and normality, so that they are more suitable for statistical analysis (Moral

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and Trapero, 2009). Some of the equivalences between the values of the scale and the

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ACCEPTED MANUSCRIPT percentage of affected shoots are: 0 = 0%, 1 = <0.24%, 2 = 0.4%, 3 = 1.2%, 4 = 3.6%, 5

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= 10%, 6 = 25%, 7 = 50%, 8 = 75% and 9 = ≥84%. Finally, DS of SH on naturally

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infected almond fruit was evaluated in the epidemic year 2006. For this purpose, a total

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of 160 fruit per cultivar were randomly sampled from the whole perimeter of the tree

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canopy, and the percentage of the fruit surface with SH lesions was estimated in each

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fruit. The DS of RLB and SH were assessed at the beginning of August since RLB and

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SH infections rarely occur after August. The DSs of LC and BB were assessed in April

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and May, respectively, when the symptoms were clear and more disease progress was

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unexpected, according to the weather conditions.

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2.3. Data analysis

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To compare the DS of the four foliar almond diseases among the experimental

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fields and years, data of the four foliar diseases obtained from early- and late-flowering

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cvs. were related to the DS score (DSs) obtained for ‘Marcona’ and ‘Guara’,

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respectively. To this end, DSs=100 was assumed for these two reference cvs.

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Subsequently, for each foliar disease, the DSs for each cv. evaluated were transformed

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according to this assumption and expressed as percentages relative to control. In each

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group of cvs. (early- and late-flowering), the DSs of cvs. for each foliar disease were

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compared with the Dunnett’s multiple comparison test at P=0.05.

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Pearson correlation coefficients (r) between the four diseases were calculated

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using the average DSs of the cvs. for each disease, but performing separate analyzes for

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the two groups of early- and late-flowering cvs. Likewise, for the SH disease, Pearson’s

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correlation coefficients between the average DSs of leaves and fruit were also calculated

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separating the two groups of early- and late-flowering cvs. All the data were analyzed

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using Statistix 10 (Analytical Software, 2013).

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3. Results 9

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3.1. Variability of the four almond aerial diseases among fields and years The variability of the four almond aerial diseases among the experimental fields

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and years was evaluated with the two reference cvs. Marcona and Guara. For each

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disease, only DS data from the experimental fields and years in which the disease

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showed a high enough incidence level for the evaluation are shown. In general, RLB

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was the most prevalent disease, although its severity varied markedly among fields and

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years. SH was the second most prevalent disease. Although BB was markedly less

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frequent than RLB and SH, it caused the most severe outbreaks, but only when the rain

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coincided with flowering and when fungicide treatments were not applied to the crop. .

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Finally, LC was rare, showing a very low incidence over time. Comparing the two

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reference cvs. for their response to the four diseases, 'Guara' was more susceptible than

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'Marcona' to RLB and LC; the two cvs. presented similar susceptibility to SH; and

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'Marcona' was more susceptible than 'Guara' to BB (Fig. 2).

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3.1.1. Red leaf blotch

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A total of seven RLB evaluations were conducted from 2004 to 2012 on

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‘Marcona’ (early-flowering). The leaf surface area affected by the disease was <12% for

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all evaluations. Main differences among years were observed in the five evaluations

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conducted in Córdoba (Fig. 2a).

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Twelve evaluations were conducted on ‘Guara’ (late-flowering) from 2004 to

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2012. The leaf surface area affected never exceeded 35%. The highest RLB DSs

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(31.7%) was assessed in Chirivel field, while the lowest DSs (4.5%) was assessed in

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Córdoba. Differences in the DSs among different years were also observed in Córdoba,

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where RLB was observed in five years from 2004 to 2012 (Fig. 2a).

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ACCEPTED MANUSCRIPT The variation in the DS of ‘Marcona’ and ‘Guara’ with time followed the same

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pattern when both cvs. were compared in Cordoba field, with ‘Guara’ being more

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susceptible than ‘Marcona’ (Fig. 2a).

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3.1.2. Shot hole

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A total of seven SH evaluations were conducted from 2004 to 2012 on

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‘Marcona’. Most of the evaluations were done in the Córdoba field, where the DS

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values ranged from 1.5 to 4.0% in 2012 and 2011, respectively. SH also affected leaves

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in Chirivel in 2004 (1.5%) and in Venta Quemada in 2012 (1.3%) (Fig. 2b).

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Twelve evaluations were conducted from 2004 to 2012 on ‘Guara’. The lowest

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and highest DS values were 0.17% and 7.5%, respectively, and both values were

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observed in the Córdoba field in 2012 and 2004, respectively. In 2008, SH was

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evaluated in four different fields, Antequera, Chirivel, Córdoba, and Huéneja. The

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highest DSs (2.7%) of SH was assessed in Córdoba field, whereas the lowest DSs

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(0.7%) was assessed in Huéneja. DSs varied depending on the evaluated years in

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Antequera, Córdoba and Chirivel fields. (Fig. 2b).

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The DS of SH on almond fruit was also evaluated in Córdoba in 2006. That year,

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the DS of SH was higher (2.4%) on the fruit than on the leaves (1.7%) of the cv.

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Marcona. However, the DS of SH on the fruit and leaves of cv. Guara were identical

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(2.8%) (Fig. 2b and Fig. 3).

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3.1.3. Blossom blight

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The DS of BB on ‘Marcona’ was evaluated only in the Puebla de Guzmán field

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in 2009. In this case, the DSs was 7.3 which is equivalent to 58.2% of affected leaf

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surface (Fig. 2c). 11

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The DS was evaluated two times in Antequera and one time in Puebla de Guzmán

on ‘Guara’. In all cases, the DSs was lower than 5, equivalent to

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approximately 10% of the affected shoots. In 2011, the DS was evaluated in the

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Chirivel field by counting the number of affected shoots per tree due the low incidence

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of the disease. An average of 18 affected shoots per tree was obtained (0.8% of affected

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shoots) (Fig. 2c)

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Although BB was more prevalent on ‘Guara’ that on ‘Marcona’, the latter was

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more susceptible to BB than ‘Guara’ (Fig. 2c). BB was the disease that caused the

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highest outbreaks, but this was only the case when the rain coincided with flowering

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and fungicide treatments were not applied to the crop.

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3.1.4. Leaf curl

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The DS of LC on ‘Marcona’ was evaluated only in Venta Quemada in 2011 and

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in Puebla de Guzmán in 2006. In Puebla de Guzmán, the DSs was 0.2, according to the

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established rating scale from 0 to 9, whereas in Venta Quemada, the DSs showed the

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highest value (6.6=39.2% of affected leaf surface) (Fig. 2d).

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The DS on ‘Guara’ was evaluated in the same fields and years that ‘Marcona’.

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In both cases, ‘Guara’ was more susceptible than ‘Marcona’ to LC. The DSs was 3.2

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(1.5% affected leaf surface) in Puebla de Guzmán field; while it reached a DSs of 7.2

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(55.5% affected leaf surface) in Venta Quemada field (Fig. 2d).

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3.2. Comparing the susceptibility of the almond cultivars to the four aerial diseases

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The mean DS values of each foliar disease were expressed relative to those of

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the reference cvs. Marcona and Guara (DS=100%), respectively, for both the early- and

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late-flowering cv. groups. In general, statistical analysis using the relative DS values of

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each disease and cv. group (early- and late-flowering) allowed the establishment of 12

ACCEPTED MANUSCRIPT three major groups of susceptibility: i) cvs. more susceptible than ‘Marcona’ or ‘Guara’;

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ii) cvs. with a similar susceptibility to that of ‘Marcona’ or ‘Guara’; and iii) cvs. less

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susceptible than ‘Marcona’ or ‘Guara’. The results of the comparison of the

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susceptibility of the early- and late-flowering cvs. to RLB, SH, BB and LC are shown in

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Table 4.

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3.2.1. Susceptibility of the early-flowering almond cultivars

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In general, most of the early-flowering cvs. evaluated showed similar

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susceptibility to RLB, SH and LC to the refence cv. Marcona. For these three diseases,

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cvs. less susceptible than ‘Marcona’ were not found. However, ten out of 12 early-

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flowering cvs. evaluated against BB were less susceptible than ‘Marcona’. The linear

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correlation analyses of the four aerial diseases for the susceptibility of early-flowering

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cvs. showed no significant correlation between diseases (P > 0.05).

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Red Leaf Blotch. Two groups of susceptibility to RLB were observed for early-

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flowering cvs. The first group showed similar susceptibility to the disease than the

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reference cv. Marcona, and it was composed by nine cvs. including ‘Marcona’. The

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second group comprises a total of five cvs. that were more susceptible to RLB than

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‘Marcona’(Table 4).

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Shot Hole. Early-flowering cvs. showed a broad variation of relative DS to SH, ranging

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from 63.9 to 615.8% for ‘Blanquerna’ and ‘Pizzuta de Avola’, respectively. Only this

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last cv. was separated in a different susceptibility group classified as more susceptible

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than ‘Marcona’ (Table 4).

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‘Marcona’ resulted in the least susceptible cv. to SH (DS=2.8%) on fruit,

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followed by ‘Rumbeta’ (DSs=4.9%) and ‘Pajarera’ (DSs=6.8%) . The remaining early-

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flowering cvs. were grouped together in a different group classified as more susceptible 13

ACCEPTED MANUSCRIPT than ‘Marcona’ (Fig. 3a). Fruit susceptibility to SH in early-flowering cvs. showed more

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variation among cvs. than that observed in affected leaves, and disease severity in fruit

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and in leaves was not significantly correlated (r = 0.3408, P = 0.0704).

318

Blossom Blight. All early-flowering almond cvs. evaluated were less susceptible to BB

319

than ‘Marcona’, with the exception of ‘Rumbeta’ (DS=91.5%), which did not differ

320

from ‘Marcona’ (Table 4).

321

Leaf Curl. Two groups of susceptibility to LC were observed for early-flowering cvs.

322

The first group showed similar susceptibility to the disease than the reference cv.

323

Marcona, and it was composed by eleven cvs. including ‘Marcona’. A second group

324

classified as more susceptible than ‘Marcona’ was formed by ‘Asperilla’ (DS=422.3%)

325

and ‘Pajarera’ (DS=754.5%) (Table 4).

326

3.2.2. Susceptibility of the late-flowering almond cultivars

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In general, 21 out of the 26 late-flowering cvs. evaluated were less susceptible

328

than the reference cv. Guara to at least one of the four diseases. However, there were no

329

cultivars less susceptible than ‘Guara’ for SH (Table 4). Significant differences in

330

cultivar susceptibility with respect to ‘Guara’ were observed among cvs. for the four

331

almond foliar diseases. The only cultivar that showed a similar susceptibility to ‘Guara’

332

for the four diseases was ‘Tuono’. Pearson’s correlations between the four foliar

333

diseases for the susceptibility of the late-flowering cvs. only showed a positive

334

correlation between BB and LC (r = 0.8123; P = 0.0013).

335

Red leaf blotch. Two groups of susceptibility to RLB were observed for the late-

336

flowering cvs. The first group comprised 18 almond cvs. showing a lower susceptibility

337

than that of the reference cv. Guara. Eighteen cvs. were less susceptible than ‘Guara’ to

338

RLB, with ‘Francolí’, ‘Mardía’ and ‘Tardona’ were the least affected cvs. A second

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ACCEPTED MANUSCRIPT group showing a similar susceptibility to RLB as that of ‘Guara’ was observed. No late-

340

flowering cv. was more susceptible than ‘Guara’ to RLB (Table 4).

341

Shot hole. The late-flowering cvs. showed a broad variation in relative DS to SH,

342

ranging from 63.7% (‘Francolí’) to 327.7% (‘Nopareil’). Five cvs. were classified as

343

more susceptible than ‘Guara’. The remaining late-flowering cvs. showed a similar

344

susceptibility to SH as that of ‘Guara’, and none of the cvs. was less susceptible than

345

‘Guara’ (Table 4).

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Two groups of fruit susceptibility to SH were observed for late-flowering cvs.

347

The first group comprised eight cvs., including ‘Guara’, which showed a similar

348

susceptibility to that of reference cv. Guara (DS=2.8%). Fruit of ‘Genco’, ‘Mandaline’,

349

‘Nonpareil’ and ‘Texas’ were more susceptible than those ‘Guara’ to SH. As with the

350

leaf evaluation, none of the cultivars evaluated was less susceptible than ‘Guara’ (Fig.

351

3b). Pearson’s correlation between disease severity in the fruit and in the leaves was

352

significant (r = 0.5655, P = 0.0224).

353

Blossom blight. Three groups of susceptibility to BB were observed for the late-

354

flowering cvs. The cvs. Antoñeta, Glorieta and Tuono showed a similar susceptibility to

355

BB as that of ‘Guara’. ‘Cristomorto’, ‘Ferraduel’, ‘Ferragnès’, ‘Lauranne’, ‘Marta’ and

356

‘Masbovera’ were classified as less susceptible than ‘Guara’, with ‘Cristomorto’

357

showing the lowest DS value (36.9%). On the other hand, ‘Cambra’ (DS=133.1%) and

358

‘Supernova’ (DS=138.6%) were more susceptible than ‘Guara’. The remaining 14 cvs.

359

could not be evaluated for their susceptibility to BB (Table 4).

360

Leaf curl. Two groups of susceptibility to LC were observed for the late-flowering cvs.

361

The first group comprised 16 cvs., which were less susceptible than ‘Guara’. A second

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ACCEPTED MANUSCRIPT 362

group comprised by seven cvs., including ‘Guara’, showed a similar susceptibility as

363

that of ‘Guara’ (Table 4).

364

4. Discussion In this study, the susceptibility of 40 cvs., including early- and late-/extra-late-

366

flowering cvs., was evaluated against the four most common almond foliar diseases in

367

Spain. To avoid the possible effects of flowering time on disease susceptibility, the

368

early- and late-flowering cv. groups were evaluated separately. This work is the first

369

study evaluating a broad range of almond cvs. against foliar diseases in natural field

370

conditions in the Andalusia region of southern Spain.

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RLB and SH were the most prevalent diseases among fields and years, whereas

372

significant outbreaks of BB and LC were observed in only a few fields and years.

373

Notably, the BB outbreaks were the most severe, causing shoot defoliation and dieback.

374

Marked differences in DS were observed among experimental fields, years and cvs.

375

Indeed, the incidence and severity of the four foliar diseases on the reference cvs.

376

Marcona and Guara varied among the experimental fields in the same year and among

377

years in the same field. These variations were probably because of the genetic

378

differences of the cvs., the agronomical characteristics of the experimental fields, the

379

cultural practices, the annual rainfall, and the farming systems. In particular, the shift

380

occurred in Andalusia region from traditional dry-farming cultivation systems to more

381

intensive almond cropping systems based on high-input strategies has favored the

382

epidemics in the new almond growing regions across this land where almond was a

383

non-traditional crop.

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384

For the reference cv. Marcona and Guara, the variation in the DS of RLB over

385

the years followed the same pattern, but it was as much as 50% lower for ‘Marcona’ 16

ACCEPTED MANUSCRIPT than that observed for ‘Guara’. This similar pattern over time could be due to the

387

climatic conditions that occurred in each year. On the other hand, the differences in

388

susceptibility may be because ‘Marcona’ is genetically less susceptible than ‘Guara’ to

389

RLB, or it may be due to the premature flowering period of ‘Marcona’, which flowered

390

at least 7 days before ‘Guara’. However, the latter hypothesis contradicts the general

391

idea that the early-flowering cvs. are more exposed to infection by P. amygdalinum than

392

the late-flowering cvs. because the first cvs. to flourish are subjected to a broader

393

infection period when ascospores of P. amygdalinum are spread (Almacellas, 2014).

394

Regarding the DS of SH in the two reference cvs., different patterns of susceptibility

395

were observed in the five evaluations in the Córdoba field. The differences in

396

susceptibility between ‘Marcona’ and ‘Guara’ could be related to the different cycles of

397

rainfall and temperature observed in each year during the flowering period. Differences

398

in susceptibility to BB were also observed between ‘Marcona’ and ‘Guara’, as

399

‘Marcona’ was markedly more susceptible than ‘Guara’. Our results are in concordance

400

with those obtained by several authors who reported that ‘Marcona’ is more susceptible

401

than ‘Guara’ to BB. This difference in susceptibility between these early- and late-

402

flowering cvs. could be attributed to their different flowering times. Finally, differences

403

in susceptibility to LC were also observed between ‘Marcona’ and ‘Guara’, with

404

‘Guara’ being more susceptible than ‘Marcona’. The main reason for this difference

405

could be the different flowering times of the cvs. because the tender leaves developed

406

by the late-flowering cv. Guara are exposed to more favorable climatic conditions than

407

the tender leaves of ‘Marcona’ for the infection by T. deformans.

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408

Most of the 14 early-flowering cvs. showed a similar susceptibility to

409

RLB, SH and LF as that of ‘Marcona’. For ‘Cartayera’, our results agree with those

410

obtained by several authors who have described this cv. as tolerant against the most 17

ACCEPTED MANUSCRIPT fungal diseases (Navarro, 1996; Salazar and Melgarejo, 2002; Arquero et al., 2008). For

412

RLB disease, the early-flowering cvs. were grouped as having a similar susceptibility as

413

that of ‘Marcona’ or as more susceptible than ‘Marcona’. Among the cvs. clustered in

414

these two groups, our results demonstrated that ‘Blanquerna’ was moderately

415

susceptible, which agrees with the results obtained by Malagón (2007). However, based

416

on the literature, several contradictory results were obtained for the susceptibility of the

417

cvs. to RLB. ‘Desmayo Largueta’ and ‘Garrigues’ showed a similar susceptibility to

418

RLB as that of ‘Marcona’ in this work, whereas several previous studies have suggested

419

that they are tolerant to RLB, showing less susceptibility than ‘Marcona’ (Egea et al.,

420

1984; Navarro, 1996; Miarnau and Vargas, 2013). Malagón (2007) classified ‘Pajarera’

421

as moderately susceptible, while our results demonstrated that it was significantly more

422

susceptible than ‘Marcona’ to RLB. ‘Ramillete’ and ‘Rumbeta’ were previously

423

classified as tolerant or less susceptible than ‘Marcona’ to RLB by Egea et al. (1984)

424

and Arquero and Oukabli (2007), respectively. Nevertheless, our results demonstrated

425

that these two cvs. were more susceptible than ‘Marcona’. ‘Cavaliera’ also showed a

426

higher susceptibility than ‘Marcona’ to RLB, whereas it has been classified as resistant

427

in previous studies (Egea et al., 1984; Miarnau and Vargas, 2013). For SH affecting

428

leaves, the early-flowering cvs. showed a similar susceptibility to that of ‘Marcona’,

429

with the exception of ‘Pizzuta de Avola’, which was significantly more susceptible than

430

‘Marcona’. Previous studies conducted by Egea et al. (1984) have classified ‘Desmayo

431

Largueta’, ‘Garrigues’ and ‘Peraleja’ as very susceptible to SH and have classified

432

‘Marcona’ and ‘Ramillete’ as moderately susceptible to SH. This information is in

433

concordance with our results. However, no information about the leaf susceptibility to

434

SH of the rest of early-flowering cvs. that were evaluated is available in the literature.

435

For fruit, ‘Marcona’ was the most tolerant cv. to SH disease, while ‘Abizanda’ was the

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18

ACCEPTED MANUSCRIPT most susceptible cv. However, to date, no information about the fruit susceptibility of

437

almond cvs. to SH is available. Concerning the susceptibility of the early-flowering cvs.

438

to BB, ‘Marcona’ was the most susceptible cv., followed by ‘Rumbeta’. The rest of the

439

cvs. were significantly less susceptible than ‘Marcona’. Our results confirm the high

440

susceptibility of ‘Marcona’ to BB that has previously been described by several authors

441

(Muncharaz, 2004; Arquero and Oukabli, 2007). Finally, for LC, most the early-

442

flowering cvs. were grouped as having a similar susceptibility as ‘Marcona’ or as more

443

susceptible than ‘Marcona’. Among the cvs. clustered in the group with a similar

444

susceptibility as that of ‘Marcona’, a broad range of variation in susceptibility was

445

recorded. Although our results cannot consistently confirm that ‘Desmayo Largueta’

446

was very susceptible to LC, these results are close with those observed by Arquero et al.

447

(2013), who described ‘Desmayo Largueta’ as very susceptible to LC. No information

448

about the susceptibility to LC of the rest of early-flowering cvs. is available in the

449

literature, so comparisons cannot be made with our results.

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Concerning the response of the late-flowering cvs., 21 out of the 26 cvs.

451

evaluated were less susceptible than ‘Guara’ to at least one of the four monitored foliar

452

diseases It is interesting to note that ‘Tuono’ and ‘Guara’ showed very similar levels of

453

susceptibility for the four diseases evaluated. This result is in agreement with the

454

identical genetic profiles for these two cultivars that have been recently characterized

455

(Dicenta et al., 2015). With regards to RLB disease, the late-flowering cvs. either had a

456

similar susceptibility as ‘Guara’ or were less susceptible than ‘Guara’, and ‘Guara’ was

457

among the most susceptible cvs. Our results confirm that ‘Guara’ is highly susceptible

458

to RLB, as previously described by Navarro (1996). Among the cvs. with a similar

459

susceptibility to RLB as that of ‘Guara’, our results agreed with those obtained by

460

several authors (Egea et al., 1984; Bonaccorsi et al., 2010; Arquero et al., 2013) for

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19

ACCEPTED MANUSCRIPT ‘Nonpareil’, ‘Supernova’ and ‘Tuono’. Although no significant differences in

462

susceptibility to RLB were observed between ‘Genco’ and ‘Guara’, ‘Genco’ showed a

463

lower DS value than ‘Guara’, which is in agreement with the results described by

464

Malagón (2007). ‘Texas’ and ‘Soleta’ were previously classified as resistant (Egea et

465

al., 1984) or moderately susceptible (Malagón, 2007; Arquero and Oukabli, 2007) to

466

RLB, but in this study, the two cvs. and ‘Guara’ had a similar susceptibility. The

467

information provided here for ‘Mandaline’, which indicates that it has a similar

468

susceptibility to RLB as that of ‘Guara’, represents the first report for this cv. Regarding

469

the cvs. grouped as less susceptible than ‘Guara’ to RLB, in general, our results were

470

similar to those obtained in previous studies (Egea et al., 1984, 2003; Navarro, 1996;

471

Salazar and Melgarejo, 2002; Heydarian and Moradi, 2005; Malagón, 2007; CITA,

472

2009; Bonaccorsi et al., 2010; Dicenta et al., 2010; IRTA, 2010; Miarnau and Vargas,

473

2013), with some discrepancies in the susceptibility among cvs. Regarding the cvs. with

474

the lowest susceptibilities to RLB, ‘Cristomorto’, Mardía’ and ‘Tardona’ were classified

475

as resistant or tolerant cvs., a result that was in concordance with the observations of

476

several authors (Egea et al., 1984; Monastra et al., 1984; Miarnau and Vargas, 2013).

477

Nevertheless, we described ‘Francolí’ as tolerant to RLB, while Malagón (2007) and

478

Miarmau and Vargas (2013) considered this cv. as slightly or moderately susceptible to

479

the disease. Our results suggest that most of the late-flowering cvs. have a susceptibility

480

to SH that is similar to that of ‘Guara’. Egea et al. (1984) categorized ‘Cristomorto’,

481

Ferragnès’ and ‘Genco’ as tolerant cvs. to SH, whereas we demonstrated that ‘Genco’ is

482

significantly more susceptible than ‘Guara’ to SH and that the susceptibility of

483

‘Cristomorto’ and ‘Ferragnès’ is similar to that of ‘Guara’. In this study, the

484

susceptibility of ‘Ferraduel’ was also similar to that of ‘Guara’, while Salazar and

485

Melgarejo (2002) described ‘Ferraduel’ as very susceptible. The 12 late-flowering

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20

ACCEPTED MANUSCRIPT almond cvs. evaluated against BB were clustered into three groups of susceptibility. Our

487

results are in agreement with those obtained by several authors for ‘Ferraduel’, ‘Marta’,

488

which were described as resistant to BB (Navarro, 1996; Salazar and Melgarejo, 2002),

489

and ‘Supernova’, which was described as very susceptible to BB (Arquero et al., 2013).

490

However, although we showed that ‘Lauranne’ was less susceptible than ‘Guara’ to BB,

491

Arquero et al. (2013) considered this cv. highly susceptible to the disease. Finally, for

492

LC, most of the late-flowering cvs. resulted in a similar susceptibility to LC as that of

493

‘Guara’. Our results agree with those of previous studies conducted by Arquero et al.

494

(2013) for ‘Francolí’, ‘Guara’, ‘Supernova’ and ‘Tuono’, which were classified as

495

susceptible to LC. On the other hand, among the cvs. classified as less susceptible than

496

‘Guara’, only the observed response of ‘Ferragnès’ was comparable to the results of

497

previous studies. In this case, our results were in agreement with those obtained by

498

Salazar and Melgarejo (2002), who considered ‘Ferraduel’ highly susceptible to LC.

499

Unfortunately, information about the susceptibility of late-flowering almond cvs. to SH,

500

BB and LC is very limited in the literature, and we were not able to compare all of our

501

results with those of previous studies.

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In general, there was no significant correlation between the four diseases for the

503

susceptibility of the cultivars, both for those of early-flowering and for those of late-

504

flowering. However, there was an exception since the diseases BB and LC were

505

positively correlated for the late-flowering cultivars. In the absence of information in

506

this regard, this correlation could be of interest to develop joint management strategies

507

for both diseases. For SH disease, a significant positive correlation was also obtained

508

between leaf and fruit severities for late-flowering cvs. This correlation, however, was

509

not significant for early-flowering cvs. These results suggest a different susceptibility of

510

fruits and leaves to SH, but only in early-flowering cvs.

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ACCEPTED MANUSCRIPT Our work is relevant because it generates novel information about almond cv.

512

susceptibility to the most common foliar diseases of this crop. The main conclusions of

513

this study indicate that differences in the disease susceptibility of cvs. within early- and

514

late-flowering groups, as well as variations in the disease susceptibility of the cvs. over

515

multiple years and experimental fields, are related to agro-climatic conditions. These

516

conclusions will be truly useful to growers and farm advisors for preventing almond

517

diseases. Moreover, cultivar resistance is among the most important management

518

strategy for preventing diseases in context of sustainable agriculture. Likewise, this

519

study highlights the need to consider cultivar resistance in the development and

520

selection of plant material for new almond plantings as well as in integrated pest

521

management. It provides relevant information about the control of RLB, SH, BB and LF

522

in almond crops in an economically and environmentally sustainable way.

523

Acknowledgments

524

This research was funded by the IFAPA, Junta de Andalucía and the Instituto Nacional

525

de Investigación y Tecnología Agraria y Alimentaria, INIA (projects PPTRATRA-

526

2016.00.6 and RTA2017-00009-C04-03, respectively). C. Agustí-Brisach is the holder

527

of a Juan de la Cierva-Incorporación fellowship from MINECO. The authors thank

528

‘Crisol/Arboreto’ and ‘Mañán’ OPFHs, and the private companies ‘Almendras

529

Francisco Morales’ and Bain (Borges Group) for their collaboration.

530

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531

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J.L., Gallego, J.C., García, A., Lorite, I., Lovera, M., Parra, M.A., Ramírez, A.,

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Roca, L., Romancho, F.J., Romero, J., Salguero, A., Santos, C., Serrano, N.,

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Bonaccorsi, A., Bella, P., Catara, A., 2010. Gravi infezioni di Polystigma amygdalinum

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Salazar, D.M., Melgarejo, P. 2002. El cultivo del almendro. Ed. Mundi Prensa, Madrid, Spain. Teviotdale, B.L., Michailides, T.J., Pscheidt, J.W., 2002. Compendium of Nut Crop Diseases in Temperate Zones. APS Press, Saint Paul, MN, USA. 25

ACCEPTED MANUSCRIPT Table 1 Geographical location of the experimental fields network and cultivars evaluated in this study. Year of plantation

Locality/Province

Almond cultivars Flowering period Cultivarb

Antequera/Málaga Chirivel/Almería Córdoba/Córdoba Huéneja/Granada Puebla de Guzmán/Huelva

Late

2001 2002

Córdoba/Córdoba Puebla de Guzmán/Huelva

Early

2012 2010 2010

Antequera/Málaga Córdoba/Córdoba Venta Quemada/Granada

Late, Extra-late

See reference color and geographical location in Figure 1.

b

Reference cultivars (control) in bold type.

SC

AC C

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a

Antoñeta, Cambra, Cristomorfo, Ferraduel, Ferragnès, Francolí, Glorieta, Guara, Genco, Glorieta, Lauranne, Mandaline, Marta, Masbovera, Nonpareil, Supernova, Texas, Tuono Abizanda, Asperilla, Blanquerna, Cartayera, Cavaliera, Desmayo Largueta, Garrigues, Marcona, Pajarera, Peraleja, Pizzuta Avola, Ramillete, Rumbeta, Verd Antoñeta, Belona, Constantí, Ferraduel, Ferragnès, Francolí, Guara, Genco, Lauranne, Mandaline, Mardía, Marinada, Nonpareil, Penta, Soleta, Tardona, Tarraco, Texas, Tuono, Vairo

RI PT

2000 2001 2000 2001 2002

M AN U

Experimental field networka

26

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Table 2

RI PT

Geographic location, agronomic characteristics and experimental design of the ten almond experimental fields evaluated in this study. Experimental design

Altitude (m) 595

UTM (X; Y) 366,276; 4,111,469

Soil Loamy; deep

Field 1

Organic; dry land

340,908; 4,190,774

Sandy-loam, calcareous; shallow Loamy-silty; very deep

Córdoba

92

Huéneja

1,113

506,183; 4,117,380 654,219; 4,158,215

Clay-loam; shallow Clay-loam; shallow

Conventional; very deficit irrigation Conventional; normal irrigation

Puebla de Guzmán

214

Venta Quemada

1,035

548,347; 4,160,626

Sandy-loam, calcareous; shallow

Organic; dry land

Conventional; deficit irrigation

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563,230; 4,159,123

Nº of experimental blocks 2

Nº of trees per elemental plot 10

12

4

4

3

Late/2001

12

2

10

4 5 6 7

Late/2000 Early/2001 Late, Extra-late/2010 Late/2001

12 10 12 12

6 3 4 2

2 5 4 10

8

Late/2002

12

2

10

9 10

Early/2002 Late, Extra-late/2010

10 12

3 3

5 5

EP

1,105

Nº of cultivars 12

AC C

Chirivel

Late, Extra-late/2012

M AN U

2

Flowering period/Year of plantation Late/2000

SC

Locality Antequera

Farming system/irrigation Conventional; deficit irrigation

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ACCEPTED MANUSCRIPT Table 3 Location and characteristics of Andalusian weather stations analyzed for each experimental field.

AC C

EP

TE D

M AN U

SC

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Weather Station Experimental field Monitoring (Locality/Province) Name (Location) Propertya Altitude (m) years UTM (X; Y) Antequera, Málaga Villanueva de Algaida RAIF 480 2001-2012 369,214; 4,116,067 Chirivel, Almería Chirivel RAIF 1,080 2003-2012 656,136; 4,160,498 Córdoba, Córdoba Córdoba IFAPA 117 2001-2012 341,339; 4,191,480 Huéneja, Granada Jerez del Marquesado IFAPA 1,212 2001-2012 486,699; 4,116,020 Puebla de Guzmán, Huelva Puebla de Guzmán IFAPA 288 2001-2012 124,659; 4,164,620 Venta Quemada, Granada Chirivel RAIF 1,080 2003-2012 656,136; 4,160,498 a IFAPA: Instituto de Investigación y Formación Agraria y Pesquera de Andalucía (Andalusian Institute for Research and Formation in Agriculture and Fishery); RAIF: Red de Alerta e Información Fitosanitaria (Phytosanitary Warning and Information Network).

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ACCEPTED MANUSCRIPT Table 4 Relative disease severity (%) of Red leaf blotch, Shot hole, Blossom blight and Leaf curl in almond cultivars evaluated from 2004 to 2012 in Andalusia region (southern Spain).

AC C

EP

TE D

M AN U

SC

RI PT

Early-flowering cultivars Relative disease severity (%) Cultivar Groupa Red leaf blotchb Shot holeb Blossom blightb Leaf curlb Abizanda MC 164.6 105.9 34.8* 356.3 Asperilla MC 235.5* 100.1 38.2* 422.3* Blanquerna MC 169.0 63.9 39.2 0 Cartayera GL 60.0 107.7 54.9* 0 Cavaliera GL 310.0* 145.8 n/d n/d Desmayo Largueta MC 130.0 133.7 15.6* 262.8 Garrigues MC 146.0 123.6 32.4* 18.3 Marcona MC 100.0 100.0 100.0 100.0 Pajarera MC 274.4* 96.0 74.4* 754.5* Peraleja MC 136.0 107.0 33.9* 166.3 Pizzuta de Avola GL 139.3 615.8* n/d 0 Ramillete MC 209.1* 76.9 43.9* 67.9 Rumbeta MC 257.7* 78.4 91.5 95.0 Verd GL 118.3 135.8 24.0* 0 Late-flowering cultivars Relative disease severity (%) Cultivar Groupa Red leaf Blotchb Shot holeb Blossom blightb Leaf curlb Antoñeta MC 42.4* 101.3 86.7 66.1* Belona NLC 37.6* 63.9 n/d 0.0* Cambra MC 50.8* 124.5 133.1* 92.3 Constantí NLC 36.6* 104.0 n/d 101.9 Cristomorto MC 20.8* 90.7 36.9* 35.2* Ferraduel MC 34.0* 135.1 39.0* 12.3* Ferragnès MC 34.0* 118.0 47.1* 28.0* Francolí GL 4.0* 63.7 n/d 117.9 Genco GL 64.5 223.9* n/d 0.0* Glorieta MC 39.9* 146.3 91.4 7.8* Guara MC 100.0 100.0 100.0 100.0 Lauranne MC 58.3* 110.1 38.0* 37.1* Mandaline GL 86.3 186.7 n/d n/d Mardía NLC 0.5* 77.0 n/d 19.4* Marinada NLC 21.0* 153.0 n/d 60.2* Marta MC 31.0* 163.1* 59.7* 12.3* Masbovera MC 38.2* 109.7 54.3* 12.4* Nonpareil GL 68.7 327.7* n/d n/d Penta NLC 13.0* 61.4 n/d 0.9* Soleta MC 112.8 72.2 n/d 0.9* Supernova MC 84.0 110.7 138.6* 120.7 Tardona MC 5.0* 177.2* n/d 99.2 Tarraco NLC 18.0* 130.9 n/d 11.1* Texas GL 108.8 281.7* n/d n/d Tuono MC 100.0 105.4 109.6 88.2 Vairo NLC 10.4* 96.3 n/d 29.6* a Situation of each cultivar in the experimental fields: MC: Main cultivar; GL: Guard line; NLC: New plantations of late-flowering cultivars. b

Means represent the average of 100 leaves evaluated per tree, cultivar, year and experimental field combination. In each group (early- or late-flowering cvs.), means in a column followed by an asterisk (*)

29

ACCEPTED MANUSCRIPT differ significantly from the reference cvs. Marcona and Guara, both used as control cvs. for early- and lateflowering cvs. group, respectively, according to Dunnett’s multiple comparison test at P = 0.05. Difference in susceptibility are highlighted in colors: blue (no differences in susceptibility between cultivars and controls); green (cultivars significantly less susceptible than controls); red (cultivars significantly more susceptible than controls).

EP

TE D

M AN U

SC

RI PT

n/d: Non-determined.

AC C

c

30

ACCEPTED MANUSCRIPT Fig. 1. The geographical location of Andalusia, southern Spain [Provinces of Almería (AL), Cádiz (CA), Córdoba (CO), Granada (GR), Huelva (HU), Jaén (JA), Málaga (MA) and Sevilla (SE)] and the location of the three experimental field networks (red, yellow and blue circles) established in this study.

RI PT

Fig. 2. Disease severity [(a,b), (%); (c,d), (0-9)] of (a), red leaf blotch, (b), shot hole, (c), blossom blight, and (d) leaf curl on the naturally infected almond leaves of the Guara and Marcona cvs. in the experimental fields evaluated from 2004 to 2012 in

SC

Andalusia (southern Spain). For each foliar disease, only results from fields and years in

M AN U

which disease incidence levels were high enough to be evaluated are shown. Columns represent the means of 100 leaves per tree, cultivar, year and experimental field combination. The vertical bars are the standard errors of the means. Fig. 3. Disease severity (%) of shot hole on naturally infected almond fruit of (a) early-

TE D

and (b) late-flowering almond cvs. in the Córdoba field in 2006. ‘Marcona’ and ‘Guara’ were used as the reference cvs. for the early- and late-flowering groups, respectively. Columns represent the means of 40 fruit per tree, cultivar and experimental field

EP

combination. The vertical bars are the standard errors of the means. In each group (early- or late-flowering cvs.), columns with the same color do not differ significantly

AC C

according to Dunnett’s multiple comparison test at P=0.05.

31

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ACCEPTED MANUSCRIPT

Late flowering cultivars Year of plantation: 2000-2002

CO HU

SE

JA GR

AL

MA

Late/Extra-late flowering cultivars Year of plantation: 2010-2012

Andalusia region (southern Spain)

AC C

EP

TE D

M AN U

CA

SC

Early flowering cultivars Year of plantation: 2001-2002

32

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25

25

20

20

15

15

10

10

5

5

0

0

7

(d)

8 7

6

6

5

5

4

4

3

3

2

TE D

2

EP

Antequera Antequera Puebla de Puebla de Chirivel 09 10 Guzmán Guzmán 11 09 09

1 0 Puebla Puebla Venta Venta Guzmán 06 Guzmán 06 Quemada 11 Quemada 11

Field/Year

AC C

0

9

M AN U

(c)

8

1

(b)

30

9

0-9) Disease severity ((0

35

RI PT

30

(a)

'Guara' 'Marcona'

SC

Disease severity ((% %)

35

33

ACCEPTED MANUSCRIPT 45

(a)

40 35 30 25 20

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15 5

SC

0

45 40 35 30 25 20 15 10

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5 0

(b)

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Disease severity (%)

10

AC C

EP

Almond cultivar

34