Revista Mexicana de Fitopatología ISSN: 0185-3309 [email protected] Sociedad Mexicana de Fitopatología, A.C. México

Ávila Quezada, Graciela Dolores; Téliz Ortiz, Daniel; Mora Aguilera, Gustavo; Vaquera Huerta, Humberto; Tijerina Chávez, Leonardo Spatial and Temporal Dynamic of Scab ( perseae Jenk.) on (Persea americana Mill) Revista Mexicana de Fitopatología, vol. 21, núm. 2, julio-diciembre, 2003, pp. 152-160 Sociedad Mexicana de Fitopatología, A.C. Texcoco, México

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Spatial and Temporal Dynamic of Scab (Sphaceloma perseae Jenk.) on Avocado (Persea americana Mill.) Graciela Dolores Ávila-Quezada, Daniel Téliz-Ortiz, Gustavo Mora-Aguilera, Colegio de Postgraduados (CP), Instituto de Fitosanidad, km 36.5 Carr. México-Texcoco, Montecillo, Edo. de México 56230; Humberto Vaquera-Huerta, CP, Instituto de Socioeconomía, Estadística e Informática; and Leonardo Tijerina-Chávez, CP, Instituto de Recursos Naturales. Correspondence to: [email protected]; [email protected]; (current address of first author: CIAD, A.C., Av. 4 Sur 3820, Fracc. Vencedores del Desierto, Delicias, Chihuahua, México 33089). (Received: October 7, 2002 Accepted: November 19, 2002)

Ávila-Quezada, G.D., Téliz-Ortiz, D., Mora-Aguilera, G., en 60 frutos por árbol. Quince frutos se seleccionaron y Vaquera-Huerta, H., and Tijerina-Chávez, L. 2003. Spatial etiquetaron en cada punto cardinal en la parte baja (1-3 m.) and temporal dynamic of scab (Sphaceloma perseae Jenk.) de cada árbol. Los datos se analizaron mediante índices de on avocado (Persea americana Mill.). Revista Mexicana de dispersión, autocorrelación espacial, y mapas geotopográficos Fitopatología 21:152-160. y de isolíneas. Se encontró agregación de árboles enfermos Abstract. Spatial and temporal dynamics of scab was studied en todas las fechas de muestreo. Al inicio de la epidemia se in a Hass avocado orchard in Michoacan, Mexico in 2000. detectaron patrones de proximidad espacial con correlación Monthly severity assessments were made in 60 trees in 60 significativa. El análisis de autocorrelación espacial mostró fruits per tree, by a logarithmic diagrammatic scale. Fifteen cuadrantes con correlación significativa en el segundo mes fruits were selected and labeled in each cardinal position in de evaluación, no se presentó autocorrelación significativa the lower part (1-3 m.) of each tree. Data were analyzed by en los siguientes meses. La enfermedad progresó en frutos indexes of dispersion, spatial lag autocorrelation, and inmaduros, conforme el fruto fue madurando, se observó una geotopographics and isopaths maps. Aggregation of diseased asíntota en la curva del progreso de la enfermedad. La trees was found for all evaluation dates. Spatial proximity enfermedad se manifestó en marzo, 30 días después de que patterns with significant correlation were detected at the la velocidad del viento incrementó, cuando la temperatura beginning of the epidemic. Spatial lags autocorrelation media mensual estuvo entre 13.7°C (feb) y 14.3°C (mar), y analysis showed quadrats with significant correlation in the la humedad relativa media mensual entre 60% (feb) y 45% second month of the evaluation, there were no significant (mar). La severidad final fue baja 0.82%, con una tasa de autocorrelations in the following months. The disease infección aparente de b-1 = 0.013. La incidencia de la progressed in immature fruits, as the fruit was ripening, an enfermedad estuvo directamente relacionada con la incidencia asymptote in the disease progress curve was observed. The del daño por trips. La incidencia de la roña alcanzó el 97% y disease appeared in March, 30 days after the wind speed la incidencia de daño por trips 90%. Ambas epidemia fueron increased, when the monthly average temperature was estadísticamente similares de acuerdo con el traslape de los between 13.7°C (Feb.) and 14.3°C (Nov.), and the relative intervalos de confianza (95%) de los parámetros c y b. humidity monthly average between 60% (Feb.) and 45% (Mar.). Final severity was low 0.82%, with apparent infection Palabras clave adicionales: Patrón espacial, epidemiología, rate b-1 = 0.013. Disease incidence was directly related with daño por trips, Sphaceloma perseae. damage incidence. Scab incidence reached 97% and thrips damage incidence 90%. Both epidemics were Avocado scab injures the pericarp of young fruits of statistically similar according to the splice of the confidence susceptible avocado (Persea americana Mill.) varieties intervals (95%) of the c and b parameters. affecting their commercial value. This disease has been reported to be caused by the Sphaceloma perseae Additional keywords: Spatial pattern, epidemiology, damage Jenk. (Jenkins, 1934a, 1934b; Morales, 2000), and its by thrips, Sphaceloma perseae. association with the damage by thrips, is probable (Marroquín-Pimentel, 2000). Scab appears on the first stages Resumen. La dinámica espacial y temporal de la roña se of fruit development (Vidales, 1996; Marroquín-Pimentel, estudió en un huerto de aguacate Hass en Michoacán, México 1999), causing crop losses up to 53% (Vidales, 1996). The en el 2000. Con una escala logarítmica diagramática se disease is widely spread in many countries, and its constant realizaron evaluaciones mensuales de severidad en 60 árboles presence and chemical control increase production costs Revista Mexicana de FITOPATOLOGIA/ 153

(Marroquín-Pimentel, 2000). Disease control in Michoacan, Table 1. Phenological stages of avocado (Persea americana) the number one avocado producing state in Mexico (Téliz, fruit cv. Hass based on fruit size and corresponding heat units, 2000), is carried out by continuous fungicide sprays in an orchard in Zirosto, Los Reyes, Michoacan, Mexico, in (Marroquín-Pimentel, 1999) without previous knowledge of 2000. the disease epidemiology. Some epidemiological studies in Phenological Size (mm) Size (mm) Approx. heat Michoacan have described the temporary progress of this stage wide long unitsy disease as graphical explorations and prediction models 1 3-7 4-10 316 (Vidales, 1996; Marroquín-Pimentel, 1999; Morales, 2000); 2 8-19 11-23 609 however, studies on disease spatial distribution, which are 3 20-29 24-39 870 important for management, have not been conducted. Spatial 4 30-49 40-66 1134 pattern analysis has been proposed to understand the dynamics 5 50-70 WGz 67-82 1418 of diseases (Madden, 1989), to develop more precise 6 > 70 DGz > 82 1648 sampling plans (Madden et al., 1996), for better evaluation ySince fruit set; 10ºC as base temperature. of harvest losses related to incidence and severity (Hughes, zWG = whitish green; DG = dark green. 1988), and to design and analyze experiments in more efficient ways (Hughes and Madden, 1995). There are several methods that examine the space relations of diseased plants; among trees), and disease severity (average percent of symptomatic all, indices of dispersion are solid for their strength and fruits in each tree). Severity was assessed on 60 fruits, 15 per biological basis (Campbell and Madden, 1990), but these each of the four cardinal points in the lower part of each tree methods have the disadvantage of providing little spatial (1-3 m height). Severity was measured by a logarithmic information, because they neither indicate the location of the diagrammatic scale of eight classes (Ávila-Quezada et al., sampling sites nor its relation with neighboring sites (Larkin 2001). Both fruit sides were assessed, from fruit set to et al., 1995). However, the spatial autocorrelation analysis physiological maturity. allows the determination of the intensity and direction of Damage by thrips assessment. Incidence of damage by aggregates of diseased plants, or the direction of pathogen thrips was assessed on the same fruits evaluated for scab and propagules between rows and throughout rows (Gottwald et on the same dates. al., 1989b). Isopath contour maps or lines of equal values of Temporal analysis. The monthly average of scab and damage disease severity, is another method that describes the spatial by thrips incidence and scab severity was adjusted by the Weibull model (Y = 1-exp[-(t/b)c]), where t = time, b = change of the disease over time (Minogue and Fry, 1983a, estimator of the rate parameter in the inverse form and, c = 1983b; Van der Bosch et al., 1988a, 1988b). In this study the form of the curve. This model was chose to obtain the average spatial and temporal progress of avocado scab in a commercial monthly rates of disease intensity (b-1). grove was characterized in Michoacan, Mexico, with the Spatial pattern analysis. The spatial pattern of the disease purpose of obtaining information as a support to propose was examined with Morisita´s index of dispersion (Ig) and sampling plans and efficient methods for prevention and Lloyd´s index of patchiness (LIP), as well as geotopographics controling the disease. and isopath contour maps of diseased tress and spatial lag autocorrelation analysis. In this analysis, each tree was MATERIALS AND METHODS consider as a spatial unit, and severity the analyzed variable Orchard description. An orchard with mild scab infection (Gottwald et al., 1992a). Proximity patterns of spatial lags on fruits was selected in an important avocado producing with significant autocorrelation were calculated among region in the state of Michoacan, Mexico, to study the spatial diseased trees within a row and through rows, and the direction and temporal dynamics of the disease. The orchard was in that the new diseased trees followed in time, using the software Zirosto, Los Reyes, at 2,100 masl. An experimental block of LCOR2 (Gottwald et al., 1992c). To determine indices of 60 Hass avocado trees was chosen at the center of the dispersion, each section was divided into contiguous quadrats plantation. Trees were 18 to 20 years old. Climate Cw is base on a modification of the Greig-Smith method (Campbell predominant in the area. Development of avocado fruits was and Madden, 1990), dividing the block into quadrats of 3, 6, classified in the phenological stages shown in Table 1, which 12, 30, and 60 trees. The isopath contour maps of diseased are proposed as a reference for future studies. Heat units were trees were generated for each matrix of data and date of calculated on 10ºC as a base temperature for avocado evaluation of disease severity with Surfer ver. 6.04, using development (Lahav and Trochoulias, 1982), with the kriging to smooth the contours and geostatistically interpolate software SICA (Medina-García, 1989), using the residual the whole space studied (Ripley, 1981). Additionally, three- method with the highest and lowest daily temperature, from dimensional maps were generated to observe the increase of fruit set. severity and to have a comparison reference. Disease assessment. Monthly disease measurements were Weather data. The wind direction and speed, temperature made throughout 2000, recording the incidence (number of (°C) and relative humidity (%) were recorded in a trees with scab symptoms on fruits related to the total of 60

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during the most susceptible fruit period to scab, whereas the insect may be responsible for allowing pathogen penetration. The disease severity increased with wind speed; these results March showed that wind and other environmental factors are important for spreading the disease and establishment of infection. Wind probably disperses the spores of the fungus and predisposes organs to pathogen invasion when these are laid on the fruit surface or on wounds. Rosenberg (1974) and April Coombs et al. (1985) mentioned that the greater the wind speed (greater turbulence) the thinner the boundary layer which facilitates the entrance or presence of microorganisms. Timmer and Duncan (1999) and Whiteside (1975) mentioned the importance of wind on the dispersal of fungal spores. May The disease symptoms appeared at temperatures around 14°C. In this work, relative humidity and temperature had some influence on symptom appearance, but young tissue and thrip damage are more important in this region. Marroquín- Pimentel (1999, 2000), and Vidales et al. (1999) concluded that the disease infection occurred from 10 to 26°C. June Apparently, scab appeared in small fruits from fruit set to phenological stage 3. The disease did not relate to high relative humidity (> 80%), since the rate of disease progress increased at relative humidity as low as 30%. Marroquin-Pimentel (1998) based on graphical explorations, showed that disease symptoms started with relative humidity lower than 80%. July Vidales et al. (1999) have proposed a scab simulation model based on number of hours of relative humidity higher than 80%. According to Whiteside (1975) Sphaceloma conidia require free water for at least 1.5 to 2.5 h to germinate and infect. Probably, spores only require dew deposit over the August fruit, which occurs during the morning. Marroquín-Pimentel 5 3 1 0 1 3 5 (2000) and Vidales (1996) also mentioned that fruits are susceptible to scab from fruit set to half or three quarters of Lags SE-NW Lags SW-NE its final size, and that thrip damage was associated with the 7 5 3 1 0 1 3 5 7 disease. There was a direct relation between scab symptoms Fig. 3. Proximity patterns of scab (Sphaceloma perseae) in and thrip damage; probably, weather conditions influenced avocado (Persea americana) fruits, calculated by spatial the insect populations more than to the disease. Disease autocorrelation in a Hass avocado orchard in Zirosto, Los dispersal direction apparently was not influenced by wind Reyes, Michoacan, Mexico, 2000. Black squares in the direction, since the movement from the primary foci took a autocorrelograms indicate significant autocorrelations (p = random direction. The aggregation at the beginning of the 0.05). epidemic lost intensity through time, according to the indices of dispersion. The initially autocorrelation corresponded to that disease incidence reached 98% in the first fruit growth high values for indices of dispersion (Reynolds and Madden, stages (1-3) in the state of Michoacan. Disease incidence was 1988). Spatial lag with significant autocorrelations (p = 0.01 directly related with thrips damage incidence; as the disease and 0.05) appeared at the beginning of the epidemics. The increase, damage by thrips also increase. Marroquín-Pimentel presence of noncontiguous elements of proximity patterns (2000) and Gallegos (1983) found a relation between avocado happened at the same time as the development of new foci scab incidence and thrip damage; they indicated the possibility (Gottwald et al., 1992b). Because conidia are transferred by that feeding damages the fruit epidermis, facilitating entrance wind, significant autocorrelations with noncontiguous trees of the fungus. These insects feed preferably in small fruits to distances up to 70 m, could be due to infections from fallen (from fruit set to half of its final size), before the pericarp rotten fruit, which might represent the most important source hardens (Ascención-Betanzos et al., 1999; Bailey et al., 1987; of inoculum in the grove. The isopath contour maps of the Fisher and Davenport, 1989; Gonzalez-Hernandez et al., disease showed the sprouting and expansion of foci in relation 1999). Marroquín-Pimentel (1999) found that the highest thrip to the primary foci, indicated by the movement of the isopaths, populations appeared from March to June in Michoacan, which allowed a better understanding of disease direction of

Revista Mexicana de FITOPATOLOGIA/ 159 dispersion within and through row (Gottwald et al., 1989a, Gottwald, T.R., Timmer, L.W., and McGuire, R.G. 1989b. 1992b). Secondary foci coalesced due to the progress of the Analysis of disease progress of citrus canker in nurseries disease (Gottwald et al., 1992b). The analytical study allowed in Argentina. Phytopathology 79:1276-1283. a better understanding of scab dynamics in space and time. Gottwald, T.R., Graham, J.H., and Egel, D.S. 1992a. Analysis Results of this study confirmed that avocado fruits are most of foci of asiatic citrus canker in Florida citrus orchard. susceptible at phenological stages 1 to 3. We suggest thrip Plant Disease 76:389-396. control programs from the beginning of flowering to fruit Gottwald, T.R., Reynolds, K.M., Campbell, C.L., and Timmer, stage 3. Protective control programs could include Bordeaux L.W. 1992b. Spatial and spatiotemporal autocorrelation mixture (copper sulfate and lime) applications, from the analysis of citrus canker epidemics in citrus nurseries and beginning of flowering to fruit stage 3 in the whole grove. It groves in Argentina. Phytopathology 82:843-851. is necessary to sample and monitor native avocado trees and Gottwald, T.R., Richie, S.M., and Campbell, C.L. 1992c. trees around them, starting at fruit set. Fallen fruit should be LCOR2-Spatial autocorrelation analysis software for eliminated from the soil to avoid new inoculum sources. personal computer. Plant Disease 76:213-215. Hughes, G. 1988. Spatial heterogeneity in crop loss Acknowledgements. The authors would like to thank Mr. assessment models. Phytopathology 78:883-884. Alejandro Guerrero for the economical support for this Hughes, G., and Madden, L.V. 1995. 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