Accessibility / Report Error

Phenology of hass avocado in the Andean tropics of Caldas, Colombia

Fenologia do abacate hass nos trópicos andinos de Caldas, Colômbia

Juan Sebastián Arias Garcia Danielle Pereira da Silva Alejandro Hurtado Salazar Rodrigo Alejandro Iturrieta Espinoza Nelson Ceballos-Aguirre About the authors

Abstract

The objective of this study was to document and analyze the effect of climate on the phenological development of ‘Hass’ avocado in two contrasting zones of the Andean tropics of Caldas, located at altitudes of 1,950m and 2,400m a.s.l., respectively. A completely randomized experimental design was carried out using a five to seven year-old ‘Hass’ tree as experimental unit and 15 replicates on each area. Observations were conducted on lateral sylleptic shoots and their corresponding apical buds located on the eastern and western sides of each tree. The destination of the apical bud of lateral shoots was quantified, floral phenology was documented, heat units were calculated from reproductive bud stage 1 to anthesis and to harvest and root growth was followed for each study area. Air temperature, soil temperature, precipitation and photosynthetically active radiation (PAR) values were recorded over time. Differences were found in the number of apical buds of lateral shoots with reproductive and vegetative destination, flowering phenology, heat units, root growth, PAR and precipitation. Differences were found among variables evaluated at the two contrasting altitudes. There is a clear need for further ecophysiological studies on this fruit tree in tropical areas in particular.

Index terms
ecophysiology; sylleptic shoots; photosynthetically active radiation; alternate bearing; cumulative heat units

Resumo

Objetivou-se documentar e analisar o efeito do clima no desenvolvimento feno-lógico do abacateiro ‘Hass’ em duas zonas contrastantes dos trópicos andinos de Caldas, localizadas a 1.950m e 2.400m respectivamente. Um delineamento experimental inteiramente casualizado foi implantado usando uma árvore ‘Hass’ de cinco a sete anos como unidade experimental e 15 repetições em cada área. As observações foram realizadas em brotos silépticos laterais e suas gemas apicais correspondentes localizadas no lado leste e oeste de cada árvore. O destino da gema apical das brotações laterais foi quantificado, a fenologia floral foi documentada, as unidades de calor foram calculadas desde o estágio 1 da gema reprodutiva até a antese e até a colheita e o crescimento radicular foi acompanhado para cada área de estudo. Valores de temperatura do ar, temperatura do solo, precipitação e radiação fotossinteticamente ativa (PAR) foram registrados ao longo do tempo. Foram encontradas diferenças no número de gemas apicais de brotações laterais com destino reprodutivo e vegetativo, fenologia de floração, unidades de calor, crescimento radicular, PAR e precipitação. Foram encontradas diferenças entre as variáveis avaliadas nas duas altitudes contrastantes. Há uma clara necessidade de mais estudos ecofisiológicos sobre está frutífera em áreas tropicais em particular.

Termos para indexação
ecofisiologia; brotos silépticos; radiação fotossinteticamente ativa; alternância produtiva; unidades de calor cumulativo

Introduction

Since 2020, world avocado production has shown annual increase of 4.1% (ARIAS et al., 2018 ARIAS, F.; MONTOYA, C.; VELÁSQUEZ, O. Dinámica del mercado mundial de aguacate. Revista Virtual Universidad Católica del Norte, Santa Rosa de Osos, n.55, p.30-48, 2018. ). Current estimates indicate that around 5 million tons of avocado are consumed worldwide each year (SOMMARUGA; ELDRIDGE, 2021 SOMMARUGA, R.; ELDRIDGE, H.M. Avocado production: water footprint and socio-economic implications. EuroChoices, Uckfield, v.20, n.2, p.48-53, 2021. ). In Colombia, the ‘Hass’cultivar corresponds to approximately 25% of the total area cultivated with avocado but it is noteworthy that the increase in the planted area isclose to 73%, from 11,000 hectares in 2014 to 20,182 hectares in 2019.

It is estimated that there are currently more than 30,000 hectares of ‘Hass’ established in the country at different regions; however, about 26% of the cultivated area is at the development stage; therefore, an increase in the annual fruitproduction is expected in the coming years (MADR, 2021 MADR - Ministerio de Agricultura y Desarrollo Rural. Cadena de instrumentos - Cadena del Aguacate. Bogotá, 2021. Disponível em: https://www.sioc.minagricultura.gov.co/DocumentosContexto/A1232Bullets%20aguacate%20Septiembre.pdf. Acesso em: 10 jun. 2021.
https://www.sioc.minagricultura.gov.co/D...
). Despite these figures, in order to meet market demand, it is necessary to have a consolidated knowledge base to adequately support the increase of new areas and safeguard the current ones (DÍAZ et al., 2020 DÍAZ, C.A.; BERNAL, J.; TAMAYO, A. Ecofisiología del aguacate cv. Hass en el trópico andino colombiano. In: BERNAL, J.; DÍAZ, C.A. Actualización tecnológica y buenas prácticas agrícolas (BPA) en el cultivo de aguacate. Mosquera: Agrosavia, 2020. p.331-377. ).

The knowledge about the genotype/environment interaction of the ‘Hass’ cultivar in the conditions of the Andean tropics in which Colombia is located will increase our understanding of how avocado grows and produces in these environments, and isof fundamental to promote sustainable and competitive productionsystems necessary to address problems such as alternate bearing, a phenomenonthat implies a year of very abundant harvests ("on" year) followed by reduced ones ("off" year) and vice versa (ALCARAZ et al., 2013 ALCARAZ, M.L.; THORP, T.G.; HORMAZA, J.I. Phenological growth stages of avocado (Persea americana) according to the BBCH scale. Scientia Horticulturae, Amsterdam, v.164, p.434-439, 2013. ). This behavior results in dramatic variations in fruit volume from year to year and translates into loss of income during low yield years (MICKELBART et al., 2012 MICKELBART, M.V.; ROBINSON, P.W.; WITNEY, G.; ARPAIA, M.L. ‘Hass’ avocado tree growth on four rootstocks in California.II.Shoot and root growth. Scientia Horticulturae, Amsterdam, v.143, p.205-210, 2012. ).

Recognizing that alternate production is closely related to the presence and location of fruits within the canopy and the subsequent flowering over time (ALCARAZ et al., 2013 ALCARAZ, M.L.; THORP, T.G.; HORMAZA, J.I. Phenological growth stages of avocado (Persea americana) according to the BBCH scale. Scientia Horticulturae, Amsterdam, v.164, p.434-439, 2013. ), the study of the architecture and behavior of avocado buds thatgenerates the units that give rise to reproductive organs, and that defines the growth structure of the avocado tree, is of special importance (ARIAS et al., 2021 ARIAS, J.S.; HURTADO-SALAZAR, A.; CEBALLOS-AGUIRRE, N. Current overview of Hass avocado in Colombia.Challenges and opportunities: a review. Ciência Rural, Santa Maria, v.51, n.8, 2021. ). Thus, the objective of the present study was to follow and evaluate the phenology of ‘Hass’ avocado in two contrasting zones of the Andean tropics of Caldas.

Materials and methods

Plant material

The field stage was carried out between January 2020 and February 2021 in two commercial ‘Hass’ avocado orchards, located at 5˚18' 40" N and 1,950 m a.s.l. (Aranzazu), and Villamaria at 5˚01' 26'' N and 2, 400 m a.s.l., both with loamy texturedsoils. Trees are 5 to 7 years old grafted on "criollo" rootstocks from seedsplanted at 6m x 6m, without irrigation system and with management based on the ICA guidelines (Colombian Agricultural Institute) in resolutions 448 and 30021 for exporting farms (ICA, 2016 ICA – Instituto Colombiano Agropecuario. Normas ICA - Resoluciones. Bogotá, 2016. Disponível em: https://www.ica.gov.co/getattachment/d2dea6cc-b4b0-4e76-85b3614da4761fe4/2016R448.aspx. Acesso em: 24 jun. 2021.
https://www.ica.gov.co/getattachment/d2d...
).

Fifteen trees were selected on each orchard in a completely randomized experimental design (CRD). On each tree, branches of approximately 1.5 m in length were selected and marked from the middle part of the tree canopy with orientation to theeastern and western quadrants. On these selected branches, epicormic shootsand respective lateral shoots were selected and marked (SALAZAR-GARCÍA et al., 2018 SALAZAR-GARCÍA, S.; IBARRA-ESTRADA, M.E.; GONZÁLEZ-VALDIVIA, J. Phenology of ‘Méndez’ avocado in southern Jalisco, México. Agrociencia, Montecillo, v.52, n.7, p.991-1003, 2018. ).

Destination of apical buds of lateral shoots

On each tree and branch with eastern and western orientation, epicormic shoots and their respective lateral shoots were marked, and the destination of their apical buds (vegetative or reproductive) was monitored over time, on each growth flushobserved.

Relative intensity of lateral shoot growth.

The relative intensity of both vegetative and reproductive growth of the apical buds of sylleptic lateral shoots was determined using the following mathematical formula (ROCHA-ARROYO et al., 2011 ROCHA-ARROYO, J.L.; SALAZAR-GARCÍA, S.; BÁRCENAS-ORTEGA, A.E.; GONZÁLEZ-DURÁN, I.J.; COSSIO-VARGAS, L.E. Fenología del aguacate 'Hass' en Michoacán. Revista Mexicana de Ciencias Agrícolas, Morelos, v.2, n.3, p.303-316, 2011. ).

R e l a t i v e i n t e n s i t y : N o . o f r e a d i n g s * N o . o f r e p r o d u c t i v e o r v e g e t a t i v e a p i c a l b u d s 100

Flowering phenology

To document the flowering process, reproductive apical buds at stage ‘510’ according to the phenological scale of Alcaraz et al. (2013) ALCARAZ, M.L.; THORP, T.G.; HORMAZA, J.I. Phenological growth stages of avocado (Persea americana) according to the BBCH scale. Scientia Horticulturae, Amsterdam, v.164, p.434-439, 2013. were marked in four trees and at each cardinal point. This monitoring ended when flower anthesis occurred,determining the time elapsed between development stages.

Accumulated heat units

To quantify the accumulated heat units (AHU), the maximum and minimum temperatures recorded during the time between reproductive bud stage ‘510’ and flowering ‘610’, and from anthesis to harvest, was considered. Temperatures were obtained from automatic weather stations located on each orchard, using the followingequation:

A H U : T m a x + T m i n 2 T b

where Tb= 10

Root growth

To document the presence of new roots, random samples were monthly collected from 2 trees on each orchard, starting on the eastern quadrant. These root samples were collected under the canopy by digging 40x40x40 cm holes. As selection criterion, only light brown roots measuring ≤ 5mm in thickness were used. Oncecollected, root samples were washed, dried in an oven at 70°C for 72 hours and then their dry weight was recorded using analytical scale (ROCHA-ARROYO et al., 2011 ROCHA-ARROYO, J.L.; SALAZAR-GARCÍA, S.; BÁRCENAS-ORTEGA, A.E.; GONZÁLEZ-DURÁN, I.J.; COSSIO-VARGAS, L.E. Fenología del aguacate 'Hass' en Michoacán. Revista Mexicana de Ciencias Agrícolas, Morelos, v.2, n.3, p.303-316, 2011. ).

Climatic variables

Climatic variable data were obtained from automatic weather stations located on each orchard. The variables recorded were air temperature, soil temperature, relative humidity and precipitation. Photosynthetically active radiation was periodicallymeasured at one-hour intervals from 8:00 am to 4:00 pm using PAR MQ-303 full spectrum meter from Apogee Instruments.

Statistical analysis

Completely randomized design (CRD) was used, considering the tree as the experimental unit and replicates and subreplicates corresponding to branches marked at each cardinal point. Results were analyzed by analysis of variance and Tukey's mean comparison (p≤0.05). The SAS statistical software (SAS Inst, Cary N.C. Version 9.4) was used.

Results and Discussion

The variables evaluated, such as destination of apical buds of lateral shoot, flowering phenology and accumulated heat units (AHU), show significant differences between locations, which confirms the fact that environmental conditions have aneffect on tree growth processes. Likewise, the behavior of climatic variablessuch as air temperature, precipitation and solar radiation show significant changes over time in each evaluation zone.

Destination of apical buds of lateral shoots.

Shoot growth is generally monopodial and axillary buds can be proleptic (formed after a rest period of their apical meristem) or sylleptic (formed without rest period) (ALCARAZ et al., 2013 ALCARAZ, M.L.; THORP, T.G.; HORMAZA, J.I. Phenological growth stages of avocado (Persea americana) according to the BBCH scale. Scientia Horticulturae, Amsterdam, v.164, p.434-439, 2013. ; WANG et al., 2018 WANG, M.; WHITE, N.; GRIMM, V.; HOFMAN, H.; DOLEY, D.; THORP, G.; HANAN, J. Pattern-oriented modelling as a novel way to verify and validate functional–structural plant models: a demonstration with the annual growth module of avocado. Annals of Botany, London, v.121, n.5, p.941-959, 2018. ). All lateral shoots evaluated on thisresearch were sylleptic (Figure 1 and 2). These shoots are considered highly productive due to their flowering intensity (GARNER; LOVATT, 2016 GARNER, L.; LOVATT, C. Physiological factors affecting flower and fruit abscission of ‘Hass’ avocado. Scientia Horticulturae, Amsterdam, v.199, p.32-40, 2016. ) and are more commonly observed in tropical conditions than in temperate climates (DÍAZ et al., 2020 DÍAZ, C.A.; BERNAL, J.; TAMAYO, A. Ecofisiología del aguacate cv. Hass en el trópico andino colombiano. In: BERNAL, J.; DÍAZ, C.A. Actualización tecnológica y buenas prácticas agrícolas (BPA) en el cultivo de aguacate. Mosquera: Agrosavia, 2020. p.331-377. ).

Figure 1
Proleptic and sylleptic shoot on Hass avocado trees in Caldas, Colombia.

Figure 2
Lateral sylleptic shoot and its apical bud on Hass avocado tree.

Observations made in this study indicate that the Aranzazu area (1,950 m) may be more productive in terms of number of flowers and fruits than the Villamaría area (2,400 m), due to the presence of statistically significant differences in thedestination of reproductive apical buds of sylleptic lateral shoots in both areas under study (Figure 3).

Figure 3
Destination of apical buds of lateral shoots in the first and second semester of 2021 in two contrasting areas of the Andean tropics of Caldas. Bars with asterisk denote significant differences according to the Tukey's test (p=0.05).

Relative shoot growth intensity

The orchard located in Aranzazu (1,950 m) presented relative intensity of 76.84% of lateral shoots with reproductive destination in the first half of the year, while in the second half of the year, the relative intensity of shoots with this destination was 88.1%. The orchard located in Villamaría (2,400 m) had 47.81% of shoots with reproductive fate in the first half of the year, while in the second half of the year, the relative intensity was 43.2%. These differences are comparableto those reported by Reyes-Alemán et al. (2021) REYES-ALEMÁN, J.C.; MEJÍA-CARRANZA, J.; MONTEAGUDO, O.R.; VALDEZ-PÉREZ, M.E.; GONZÁLEZ-DIAZ, J.G.; ESPÍNDOLA-BARQUERA, M.C. Phenology of the ‘Hass’ avocado in the State of Mexico, Mexico. Revista Chapingo, Serie Horticultura, Chapingo, v.27, n.2, p.113-134, 2021. , who found differences in vegetative growth in contrasting zones in different producing areas of Mexico.

These results show tendency to reproductive growth over vegetative growth in the Aranzazu area and more balanced tendency between vegetative and reproductive destination in the Villamaría area.

These results might describe the productive potential of each location and support studies on lateral bud sprouting (sylleptic or proleptic) on the main axes as an important agricultural tool, since the knowledge of the tree architecture (MENZEL et al., 2014 MENZEL, C.; LE, M.D.Increasing the productivity of avocado orchards using high-density plantings: a review. Scientia Horticulturae, Amsterdam, v.77, p.21-36.2014.Available from: https://doi.org/10.1016/j.scienta.2014.07.013.Accessed: 24 Jul 2022.
https://doi.org/10.1016/j.scienta.2014.0...
) and the manipulation of the proportion of sylleptic and proleptic buds can lead to increased productivity (GARNER; LOVATT, 2016 GARNER, L.; LOVATT, C. Physiological factors affecting flower and fruit abscission of ‘Hass’ avocado. Scientia Horticulturae, Amsterdam, v.199, p.32-40, 2016. ). These results might describe the productive potential of each location and support studies onlateral bud sprouting (sylleptic or proleptic) on the main axes as animportant agricultural tool, since the ma-nipulation of the proportion of sylleptic and proleptic shoots can lead to increased productivity (GARNER; LOVATT, 2016 GARNER, L.; LOVATT, C. Physiological factors affecting flower and fruit abscission of ‘Hass’ avocado. Scientia Horticulturae, Amsterdam, v.199, p.32-40, 2016. ). Like-wise, increase in axillary branching could also increase photosynthetic capacity in the “on year” and thus stimulate fruit production in the “off year” (REYES-ALEMÁN et al., 2021 REYES-ALEMÁN, J.C.; MEJÍA-CARRANZA, J.; MONTEAGUDO, O.R.; VALDEZ-PÉREZ, M.E.; GONZÁLEZ-DIAZ, J.G.; ESPÍNDOLA-BARQUERA, M.C. Phenology of the ‘Hass’ avocado in the State of Mexico, Mexico. Revista Chapingo, Serie Horticultura, Chapingo, v.27, n.2, p.113-134, 2021. ). Garner and Lovatt (2016) GARNER, L.; LOVATT, C. Physiological factors affecting flower and fruit abscission of ‘Hass’ avocado. Scientia Horticulturae, Amsterdam, v.199, p.32-40, 2016. , found that only shoots in terminal positions on their respective axes generally became floral, so their number indicated the floral potential of trees.

Flowering phenology

According to the phenological scale of (ALCARAZ et al., 2013 ALCARAZ, M.L.; THORP, T.G.; HORMAZA, J.I. Phenological growth stages of avocado (Persea americana) according to the BBCH scale. Scientia Horticulturae, Amsterdam, v.164, p.434-439, 2013. ) (Figure 4), the time elapsed between stage ‘510’ (dormant reproductive buds), and stage ‘610’ (first open flowers) was different between orchards (location), registering 110 days foranthesis in the municipality of Aranzazu (1,950 m), and 131 days in the municipality of Villamaría (2,400 m). This is in agreement with reports by (SALAZAR-GARCÍA et al., 2018 SALAZAR-GARCÍA, S.; IBARRA-ESTRADA, M.E.; GONZÁLEZ-VALDIVIA, J. Phenology of ‘Méndez’ avocado in southern Jalisco, México. Agrociencia, Montecillo, v.52, n.7, p.991-1003, 2018. ), which indicate that the timing of floral development varies according to the environmental conditions of a specific site. Decreases in temperature play an important role in the transition from the vegetative to the reproductive state (ROCHA-ARROYO et al., 2010 ROCHA-ARROYO, J.L.; SALAZAR-GARCÍA, S.; BÁRCENAS-ORTEGA, A.E. Determinación irreversible a la floración del aguacate 'Hass' en Michoacán. Revista Mexicana de Ciencias Agrícolas, Morelos, v.1, n.4, p.469-478, 2010. ), in addition, the floral development duration increaseswhen temperature is lower (PATTEMORE et al., 2018 PATTEMORE, D.; BUXTON, M.N.; CUTTING, B.T.; MCBRYDIE, H.; GOODWIN, M.; DAG, A. Low overnight temperatures associated with a delay in 'hass' avocado (Persea americana) female flower opening, leading to nocturnal flowering. Journal of Pollination Ecology, v.23, p.127-135, 2018. ).

Figure 4
Reproductive phenological scale of ‘Hass’ avocado in the Andean tropics of Caldas. Based on (Alcaraz et al., 2013).

Thus, the difference of 21 days to reach anthesis between orchards (location) can be explained considering the average temperature values during the observation period, since the Aranzazu area had average temperature of 21.4ºC, while inVillamaría, the average temperature was 17.8ºC.

Accumulated heat units (AHU)

AHU showed differences between orchards (locations). In Aranzazu (1,950 m), the amount of AHU to achieve anthesis was 1,096.55 and only 862.7 AHU (Table 1) were observed in Villamaría (2,400 m). This some-what differs from values reported by Chávez-Bárcenas et al. (2008), who determined that trees located in semiwarm humidclimate orchards require less AHU to reach anthesis than orchards located in temperate humid climate. AHU calculated for the period from flowering to harvest in both locations showed the same trend, 2,530.9 AHU for Aranzazu and 279 days untilharvest while Villamaria had 2,092.72 AHU and 355 days until harvest (Table 2). Anguiano et al; (2007) ANGUIANO, C.J.; ALCÁNTAR, J.J.; TOLEDO, B.R.; TAPIA, L.M.; VIDALES-FERNÁNDEZ, J.A. Caracterización edafoclimática del área productora de aguacate de Michoacán, México. In: WORLD AVOCADO CONGRESS, 6., 2007, Viña Del Mar. Proceedings […] . Woolloongabba: International Avocado Society. Disponível em: http://www.avocadosource.com/wac6/es/Extenso/3c-112.pdf. Acesso em: 16 mar. 2022. , reported accumulation of 2,200 AHU per year for ‘Hass’ avocado, while Vargas et al., (2012) VARGAS, L.M.; GUZMÁN, A.; MIRANDA, V.; BARRADAS, L. Respuesta fenológica del aguacate (Persea americana Mill) al gradiente climático en Michoacán. In: GRANADOS, R; REYNA, T. (ed.). Centro-Occidente de México variación climática e impactos en la producción agrícola. Ciudad de México: Instituto de Geografía, Universidad Autónoma de México, 2012. p.77-94. reported AHU values between 1,800 and 2,000 depending on the timeof flower-ing, which indicates that in the Aranzazuarea, the energy needs of the tree are fully satisfied, while in Villamaría, values would be below ideal optimum.

Table 1
Accumulated Heat Units (AHU) in flowering phenology in two contrasting zones of the Andean tropics of Caldas, Colombia.
Table 2
Accumulated Heat Units (AHU) from flowering to harvest in two contrasting zones of the Andean tropics of Caldas, Colombia.

These results are probably related to the difference in average temperature between locations, with Aranzazu having higher average temperature (21.4 ºC), compared to Villamaría (17.8 ºC).

Root growth

Root growth can occur throughout the year but be reduced at times of vegetative flush or flowering (ROCHA-ARROYO et al., 2011 ROCHA-ARROYO, J.L.; SALAZAR-GARCÍA, S.; BÁRCENAS-ORTEGA, A.E.; GONZÁLEZ-DURÁN, I.J.; COSSIO-VARGAS, L.E. Fenología del aguacate 'Hass' en Michoacán. Revista Mexicana de Ciencias Agrícolas, Morelos, v.2, n.3, p.303-316, 2011. ; MICKELBART et al., 2012 MICKELBART, M.V.; ROBINSON, P.W.; WITNEY, G.; ARPAIA, M.L. ‘Hass’ avocado tree growth on four rootstocks in California.II.Shoot and root growth. Scientia Horticulturae, Amsterdam, v.143, p.205-210, 2012. ), or even growth dormancy can occur (GARNER; LOVATT, 2016 GARNER, L.; LOVATT, C. Physiological factors affecting flower and fruit abscission of ‘Hass’ avocado. Scientia Horticulturae, Amsterdam, v.199, p.32-40, 2016. ). The results of this research showcontinuous roots growth over time in both loca-tions (Figure 5); however, higher growth is evident in the Villamaría area (2,400 m). Like-wise, it is observed that for the Aranzazu area (1,950 m), the most significant growth was observed on thesecond semester of the year (20.7 gr), while in the Villamaría area, the highest growth was registered in the first semester (23 gr).

Figure 5
Root growth of ‘Hass’ avocado in two contrasting areas of the Andean tropics of Caldas. FA: Flowering Aranzazu FV: Flowering Villamaría IB: Initial budbreak. Initials above bars indicate the month where flowering or budbreak occurred in the different areas evaluated.

Regarding the relationships between root growth, vegetative flush and flowering, it is important to mention that flowering events occurred in February and August in the Aranzazu area, and in March and September in the Villamaría area. For bothareas, root growth was reduced after flowering in the first half of the year; however, in the second half of the year in the Villamaría area, root growth increased after flowering, while in Aranzazu, root growth was reduced. As for the initialvegetative flush, the apical growth of lateral shoots began in December 2020 in both areas, and in the second semester of 2021, vegetative flush occurred near the month of June.

The results of this research are similar to those reported in California by Mickelbart et al. (2012) MICKELBART, M.V.; ROBINSON, P.W.; WITNEY, G.; ARPAIA, M.L. ‘Hass’ avocado tree growth on four rootstocks in California.II.Shoot and root growth. Scientia Horticulturae, Amsterdam, v.143, p.205-210, 2012. , who determined that root growth flushes occurred about 30 to 60 days after shoot growth flushes; likewise, root growth was greater when shootswere not actively growing (GARNER; LOVATT, 2016 GARNER, L.; LOVATT, C. Physiological factors affecting flower and fruit abscission of ‘Hass’ avocado. Scientia Horticulturae, Amsterdam, v.199, p.32-40, 2016. ). On the other hand, Rocha-Arroyo et al., (2011) ROCHA-ARROYO, J.L.; SALAZAR-GARCÍA, S.; BÁRCENAS-ORTEGA, A.E.; GONZÁLEZ-DURÁN, I.J.; COSSIO-VARGAS, L.E. Fenología del aguacate 'Hass' en Michoacán. Revista Mexicana de Ciencias Agrícolas, Morelos, v.2, n.3, p.303-316, 2011. concluded that in the Michoacán area (Mexico), root production occurred throughout the year, although the presence of two main root flushes thatvaried with climate was evident. Despite these results, Silva et al. (2017) SILVA, S.; CANTUARIAS-AVILÉS, T.; CHIAVELLI, B.; MARTINS, M.; OLIVEIRA, M. Phenological models for implementing management practices in rain-fed avocado orchards. Pesquisa Agropecuária Tropical, Goiânia, v.47, n.3, p.321-327, 2017. determined that under Brazilian conditions, maximum root growth coincided with flowering and with spring and summer vegeta-tive flushes.

The information obtained in this study allows inferring that in tropical conditions, it is usual to have distinct variations in the root growth patterns. There may be growth after flowering at some periods of the year, as well as simultaneous growth during flowering, or root growth before or after a vegetative growth flush (DÍAZ et al., 2020 DÍAZ, C.A.; BERNAL, J.; TAMAYO, A. Ecofisiología del aguacate cv. Hass en el trópico andino colombiano. In: BERNAL, J.; DÍAZ, C.A. Actualización tecnológica y buenas prácticas agrícolas (BPA) en el cultivo de aguacate. Mosquera: Agrosavia, 2020. p.331-377. ). This variability in growth patterns seems to be linked to changes in climate, as temperatures, precipitation and luminosity are not stable overtime as they may be in Mediterranean climates. For example, in the first half of the year, when there was high precipitation, increase in root growth was observed for both areas under study; however, this behavior pattern was not repeated in thesecond half of the year, despite the observation of new precipitations.

Climate conditions in both areas under study

The results obtained in this study show climatic differences between areas, which confirm the fact that climate has high influence on the vegetative and reproductive growth of avocado trees (CHUNG et al., 2022 CHUNG, S.W.; RHO, H.; LIM, C.K.; JEON, M.; KIM, S.; JANG, Y.; An, H. Photosynthetic response and antioxidative activity of ‘Hass’ avocado cultivar treated with short-term low temperature. Scientific Reports, v.12, n.11593, 2022. ), since at level of these variables, the two areas under study also show important differences.

Air temperature

According to the Caldas-Lang climate classification, the Aranzazu area is classified as semi-humid temperate climate, while the higher elevation area of Villamaría is classified as humid cold climate (IDEAM, 2015 IDEAM - Instituto de Hidrología, Meteorología y Estudios Ambientales. Clasificación de los climas. Atlas climatológico de Colombia. Bogotá, 2015. Disponível em: http://www.atlas.ideam.gov.co/basefiles/clima-text.pdf. Acesso em: 29 nov 2021.
http://www.atlas.ideam.gov.co/basefiles/...
). In this regard, differences inminimum, mean and maximum air temperatures recorded in both areas over time are evident (Figure 6).

Figure 6
Maximum, mean and minimum air temperatures in the two contrasting areas of the Andean tropics of Caldas.

While the three ecological avocado cultivars offer a wide range of adaptation to air temperature (WEIL et al., 2022 WEIL, A.; RUBINOVICH, L.; TCHERNOV, D.; LIRAN, O. Comparative study between the photosynthetic parameters of two avocado (Persea americana) cultivars reveals natural variation in light reactions in response to frost stress. Agronomy, Madison, v.12, n.5, p.1129, 2022. ), for the ‘Hass’ cultivar in particular, Garner and Lovatt (2016) found that under the southern Australia conditions, only thecoldest (17/10°C) and hottest (37/30°C) treatments restricted growth and dry matter accumulation, while Rocha-Arroyo et al. (2010) ROCHA-ARROYO, J.L.; SALAZAR-GARCÍA, S.; BÁRCENAS-ORTEGA, A.E. Determinación irreversible a la floración del aguacate 'Hass' en Michoacán. Revista Mexicana de Ciencias Agrícolas, Morelos, v.1, n.4, p.469-478, 2010. found that in Cal-ifornia, the ‘Hass’ cultivar did not flower when maintained at temperatures of 30/25, 25/20 or20/5°C (day/night), but flowered when exposed to 3-4 months of 15/10, 18/15, 20/15 and 23/18°C (day/night) respectively.

Air temperature data during this research do not seem to restrict tree growth in either of the two areas under study. Research carried out in Brazil determined that constant night temperatures below 10ºC can alter avocado flowering development(SOARES et al., 2002 SOARES, N.; JUNIOR, M.; TEIXEIRA, L.; CASTRO, J. Tolerância a baixas temperaturas de cultivares de abacate (Persea americana Mill.). Revista Brasileira de Fruticultura, Jaboticabal, v.24, n.3, p.721-723, 2002. ) and in California (USA), evaluations carried out on 'Hass' avocado cultivar showed that maximum air temperatures below 15 ºC reduce bee movement in the orchard (GARNER; LOVATT, 2016 GARNER, L.; LOVATT, C. Physiological factors affecting flower and fruit abscission of ‘Hass’ avocado. Scientia Horticulturae, Amsterdam, v.199, p.32-40, 2016. ); however, in this area, inflorescence development is correlated with night temperature ≤15 ºC (SALAZAR-GARCÍA et al., 2018 SALAZAR-GARCÍA, S.; IBARRA-ESTRADA, M.E.; GONZÁLEZ-VALDIVIA, J. Phenology of ‘Méndez’ avocado in southern Jalisco, México. Agrociencia, Montecillo, v.52, n.7, p.991-1003, 2018. ). In the case of Aranzazuand Villamaría, night temperatures were rarely above 15ºC or below 10ºC, which indicates that floral development should not be affected; however, differences between one location and the other can accelerate or reduce the time of the differentphenological phases, specifically the flowering time and the flower-to-fruit period.

Soil temperature

The 3 avocado cultivars, Mexican, Guatemalan and Antillean, were cultivated in different climatic regions and may show different responses to soil temperature (SILVA et al 2017 SILVA, S.; CANTUARIAS-AVILÉS, T.; CHIAVELLI, B.; MARTINS, M.; OLIVEIRA, M. Phenological models for implementing management practices in rain-fed avocado orchards. Pesquisa Agropecuária Tropical, Goiânia, v.47, n.3, p.321-327, 2017. ). Furthermore, it has been shown that there is root growthrestriction at soil tem-perature below 13.5ºC (WEIL et al., 2022 WEIL, A.; RUBINOVICH, L.; TCHERNOV, D.; LIRAN, O. Comparative study between the photosynthetic parameters of two avocado (Persea americana) cultivars reveals natural variation in light reactions in response to frost stress. Agronomy, Madison, v.12, n.5, p.1129, 2022. ). Likewise, soil temperature ranging from 21º to 27° was better for avocado seedling growth, but temperatures above 27° reduce growth (SILVA et al 2017 SILVA, S.; CANTUARIAS-AVILÉS, T.; CHIAVELLI, B.; MARTINS, M.; OLIVEIRA, M. Phenological models for implementing management practices in rain-fed avocado orchards. Pesquisa Agropecuária Tropical, Goiânia, v.47, n.3, p.321-327, 2017. ).

Soil temperature levels in this study did not show strong variations in any of the areas under study (Figure 7), which results are not in agreement with those found by Rocha-Ar-royo et al., (2011) ROCHA-ARROYO, J.L.; SALAZAR-GARCÍA, S.; BÁRCENAS-ORTEGA, A.E.; GONZÁLEZ-DURÁN, I.J.; COSSIO-VARGAS, L.E. Fenología del aguacate 'Hass' en Michoacán. Revista Mexicana de Ciencias Agrícolas, Morelos, v.2, n.3, p.303-316, 2011. , where in different growing areas of Michoacán,Mexico, soil temperature variation was from 13 ºC to 21 ºC. The minimum temperature recorded in Villamaría was 16.4ºC in November, while the highest temperature was 18.1ºC in July. In Aranzazu, the minimum temperature recorded was 17ºC in January, while the maximum temperature was 18.4ºC in April. This information allows inferring that the soil temperature in these two areas was never below the critical minimum reported and also did not reach levels relevant to stimulate rootgrowth. Furthermore, the maximum root growth in Villamaría occurred in April, while in Aranzazu, it occurred in July, and considering this information, there seems to be no relationship between maximum root growth and maximum soil temperature.

Figure 7
Soil temperature in two contrasting areas of the Andean tropics of Caldas.

Precipitation

Precipitation registered in both areas under study shows significant variations over time, although the bimodal behavior characteristic of the Andean region is preserved (RAMÍREZ; JARAMILLO, 2009 RAMÍREZ, V.H.; JARAMILLO, A. Relación entre el índice oceánico de El Niño y la lluvia, en la región andina central de Colombia. Cenicafe, Caldas, v.60, n.2, p.161-172, 2009. ). Nonetheless, precipitation of 316 mm in March forthe Villamaría area is an atypical annual value in terms of precipitation (Figure 8). This demonstrates not only the intense climatic variability of the area but also the important water supply in this central part of the country. These data contrast with what was found in a study conducted in Brazil, where in the area of the municipality of Assis Chateaubriand, state of Paraná, 1.2mm of precipitation was recorded for themonth of March (CALDANA et al., 2019 CALDANA, N.F.D.S.; NITSCHE, P.R.; MARTELÓCIO, A.C.; RUDKE, A.P.; ZARO, G.C.; BATISTA, L.G.; CONTADOR, Z.P.B.; COLUCCHI, S.L.; MARTINS, J.A. Agroclimatic risk zoning of avocado (Persea americana) in the hydrographic basin of Paraná River III, Brazil. Agriculture, Basel, v.9, n.12, p. 263, 2019. ), which required the implementation ofirrigation systems for the proper develop-ment of the avocado crop.

Figure 8
Precipitation in two contrasting areas of the Andean tropics of Caldas.

The two peak flowering periods recorded during the year in the two locations correspond to February-March and August-Sep-tember, contrasting with high rainfall in the first semester of the year in the Villamaría area, and high precipitation in thethird semester of the year in the Aranzazu area.

Silber et al. (2012) SILBER, A.; ISRAELI, Y.; LEVI, M.; KEINAN, A.; SHAPIRA, O.; CHUDI, G.; ASSOULINE, S. Response of ‘Hass’ avocado trees to irrigation management and root constraint. Agricultural Water Management, Amsterdam, v.104, p.95-103, 2012. have explained which is the environmental factor that can induce flowering in avocado and reported that flower initiation can be induced by water stress. Salazar-García et al., (2018) SALAZAR-GARCÍA, S.; IBARRA-ESTRADA, M.E.; GONZÁLEZ-VALDIVIA, J. Phenology of ‘Méndez’ avocado in southern Jalisco, México. Agrociencia, Montecillo, v.52, n.7, p.991-1003, 2018. concluded that the environmental stimulusfor flowering induction was photoperiod and/or air temperature. In contrast to the above, research carried out in the Andean tropics of Colombia showed that flowering induction occurred in some areas only at times when precipitation was reduced,while in others, flowering occurred after high precipitation (DÍAZ et al., 2020 DÍAZ, C.A.; BERNAL, J.; TAMAYO, A. Ecofisiología del aguacate cv. Hass en el trópico andino colombiano. In: BERNAL, J.; DÍAZ, C.A. Actualización tecnológica y buenas prácticas agrícolas (BPA) en el cultivo de aguacate. Mosquera: Agrosavia, 2020. p.331-377. ).

The results of this study have shown that several environmental factors may be associated with the floral induction of avocado under the conditions of the Andean tropics. Cloud cover may play an important role since the presence of high precipitation increases cloud cover and therefore there is a drop in photosynthetically active radiation (PAR). In this scenario, a hypothesis that may be viable is that the avocado tree could stop vegetative growth if radiation decreased constantly, and switch to a reproductive phase that would begin with flowering induction.

Photosynthetically Active Radiation (PAR)

For both locations, the light intensity observed at different times of the year showed tendency to concentrate the highest PAR values between 11:00 am and 02:00 pm (Fig-ure 9 A-B); however, the Villamaría area shows significant reduction inradiation after 02:00 pm, which might be due to greater presence of cloud cover if we consider that at that altitude, the presence of cloud cover in the afternoon hours is frequent. According to these results, it is important to consider thatincident PAR varies according to latitude, season, planting date and plant phenology (CRUZ et al., 2021 CRUZ DÍAZ, I.; CHAPARRO, H.N.; DÍAZ, L.I.; ROMERO, G.A. Effect of sowing density on the agronomic performance of Quinoa Nariño cultivar and the transmissivity of photosynthetically active radiation in the high tropics of Colombia. Revista Facultad Nacional de Agronomía, Medellín, v.74, n.2, p.9491-9497, 2021. ). In areas close to the equator, the length of the day does not seem to change significantly (YEANG, 2007), and as for solar radiation, Renner(2007) RENNER, S.S. Synchronous flowering linked to changes in solar radiation intensity. New Phytologist, London, v.175, n.2, p.195-197, 2007. reported that when the sun passes directly over the equator twice a year, a bimodal cyclic change in the incoming solar radiation (insolation) is observed on these regions.

The PAR values obtained in this study are high in relation to the light saturation point reported for avocado. For California, Israel and Australia, values of 300, 500, 660 and up to 1,100 μmol/m-2/s-1 respectively are re-ported as sufficient toreach light saturation point (WEIL et al., 2022 WEIL, A.; RUBINOVICH, L.; TCHERNOV, D.; LIRAN, O. Comparative study between the photosynthetic parameters of two avocado (Persea americana) cultivars reveals natural variation in light reactions in response to frost stress. Agronomy, Madison, v.12, n.5, p.1129, 2022. ). In this research, maximum PAR values above 2,000 μmol/m-2/s-1 were recorded and the average values observed were slightly less than 1,400 μmol/m-2/s-1 (Figure 9 A-B). This indicates very good PAR supply in areas understudy and shows the opportunity to study the effect of this high solar radiation on tree physiology and productivity.

Figure 9
Photosynthetically active radiation in (A) Villamaría and (B) Aranzazu, Caldas.

Conclusion

The Aranzazu area showed higher values of shoots with reproductive destination in their apical buds on both semesters of the year. Also, in Aranzazu (AHU 1,096.55), anthesis occurred 21 days earlier than in Villamaría (AHU 862.7), and in Aranzazu(AHU 2,530.9), harvest occurred 76 days earlier than in Villamaría (AHU2,092.72). For both locations, there were two important root growth peaks, and soil temperature remained within maximum and minimum ranges reported. There were differences in precipitation and air temperature in the different areas.

This study reveals the need for further research on the ecophysiology of ‘Hass’ avocado under the conditions of the Andean tropics, since the results obtained show dif-ferential behavior of trees compared to other latitudes where this fruit isalso grown.

  • ALCARAZ, M.L.; THORP, T.G.; HORMAZA, J.I. Phenological growth stages of avocado (Persea americana) according to the BBCH scale. Scientia Horticulturae, Amsterdam, v.164, p.434-439, 2013.
  • ANGUIANO, C.J.; ALCÁNTAR, J.J.; TOLEDO, B.R.; TAPIA, L.M.; VIDALES-FERNÁNDEZ, J.A. Caracterización edafoclimática del área productora de aguacate de Michoacán, México. In: WORLD AVOCADO CONGRESS, 6., 2007, Viña Del Mar. Proceedings […] . Woolloongabba: International Avocado Society. Disponível em: http://www.avocadosource.com/wac6/es/Extenso/3c-112.pdf. Acesso em: 16 mar. 2022.
  • ARIAS, F.; MONTOYA, C.; VELÁSQUEZ, O. Dinámica del mercado mundial de aguacate. Revista Virtual Universidad Católica del Norte, Santa Rosa de Osos, n.55, p.30-48, 2018.
  • ARIAS, J.S.; HURTADO-SALAZAR, A.; CEBALLOS-AGUIRRE, N. Current overview of Hass avocado in Colombia.Challenges and opportunities: a review. Ciência Rural, Santa Maria, v.51, n.8, 2021.
  • CALDANA, N.F.D.S.; NITSCHE, P.R.; MARTELÓCIO, A.C.; RUDKE, A.P.; ZARO, G.C.; BATISTA, L.G.; CONTADOR, Z.P.B.; COLUCCHI, S.L.; MARTINS, J.A. Agroclimatic risk zoning of avocado (Persea americana) in the hydrographic basin of Paraná River III, Brazil. Agriculture, Basel, v.9, n.12, p. 263, 2019.
  • CHUNG, S.W.; RHO, H.; LIM, C.K.; JEON, M.; KIM, S.; JANG, Y.; An, H. Photosynthetic response and antioxidative activity of ‘Hass’ avocado cultivar treated with short-term low temperature. Scientific Reports, v.12, n.11593, 2022.
  • CRUZ DÍAZ, I.; CHAPARRO, H.N.; DÍAZ, L.I.; ROMERO, G.A. Effect of sowing density on the agronomic performance of Quinoa Nariño cultivar and the transmissivity of photosynthetically active radiation in the high tropics of Colombia. Revista Facultad Nacional de Agronomía, Medellín, v.74, n.2, p.9491-9497, 2021.
  • DÍAZ, C.A.; BERNAL, J.; TAMAYO, A. Ecofisiología del aguacate cv. Hass en el trópico andino colombiano. In: BERNAL, J.; DÍAZ, C.A. Actualización tecnológica y buenas prácticas agrícolas (BPA) en el cultivo de aguacate. Mosquera: Agrosavia, 2020. p.331-377.
  • GARNER, L.; LOVATT, C. Physiological factors affecting flower and fruit abscission of ‘Hass’ avocado. Scientia Horticulturae, Amsterdam, v.199, p.32-40, 2016.
  • ICA – Instituto Colombiano Agropecuario. Normas ICA - Resoluciones. Bogotá, 2016. Disponível em: https://www.ica.gov.co/getattachment/d2dea6cc-b4b0-4e76-85b3614da4761fe4/2016R448.aspx. Acesso em: 24 jun. 2021.
    » https://www.ica.gov.co/getattachment/d2dea6cc-b4b0-4e76-85b3614da4761fe4/2016R448.aspx.
  • IDEAM - Instituto de Hidrología, Meteorología y Estudios Ambientales. Clasificación de los climas. Atlas climatológico de Colombia. Bogotá, 2015. Disponível em: http://www.atlas.ideam.gov.co/basefiles/clima-text.pdf. Acesso em: 29 nov 2021.
    » http://www.atlas.ideam.gov.co/basefiles/clima-text.pdf.
  • MADR - Ministerio de Agricultura y Desarrollo Rural. Cadena de instrumentos - Cadena del Aguacate. Bogotá, 2021. Disponível em: https://www.sioc.minagricultura.gov.co/DocumentosContexto/A1232Bullets%20aguacate%20Septiembre.pdf. Acesso em: 10 jun. 2021.
    » https://www.sioc.minagricultura.gov.co/DocumentosContexto/A1232Bullets%20aguacate%20Septiembre.pdf.
  • MENZEL, C.; LE, M.D.Increasing the productivity of avocado orchards using high-density plantings: a review. Scientia Horticulturae, Amsterdam, v.77, p.21-36.2014.Available from: https://doi.org/10.1016/j.scienta.2014.07.013.Accessed: 24 Jul 2022.
    » https://doi.org/10.1016/j.scienta.2014.07.013.
  • MICKELBART, M.V.; ROBINSON, P.W.; WITNEY, G.; ARPAIA, M.L. ‘Hass’ avocado tree growth on four rootstocks in California.II.Shoot and root growth. Scientia Horticulturae, Amsterdam, v.143, p.205-210, 2012.
  • PATTEMORE, D.; BUXTON, M.N.; CUTTING, B.T.; MCBRYDIE, H.; GOODWIN, M.; DAG, A. Low overnight temperatures associated with a delay in 'hass' avocado (Persea americana) female flower opening, leading to nocturnal flowering. Journal of Pollination Ecology, v.23, p.127-135, 2018.
  • RAMÍREZ, V.H.; JARAMILLO, A. Relación entre el índice oceánico de El Niño y la lluvia, en la región andina central de Colombia. Cenicafe, Caldas, v.60, n.2, p.161-172, 2009.
  • RENNER, S.S. Synchronous flowering linked to changes in solar radiation intensity. New Phytologist, London, v.175, n.2, p.195-197, 2007.
  • REYES-ALEMÁN, J.C.; MEJÍA-CARRANZA, J.; MONTEAGUDO, O.R.; VALDEZ-PÉREZ, M.E.; GONZÁLEZ-DIAZ, J.G.; ESPÍNDOLA-BARQUERA, M.C. Phenology of the ‘Hass’ avocado in the State of Mexico, Mexico. Revista Chapingo, Serie Horticultura, Chapingo, v.27, n.2, p.113-134, 2021.
  • ROCHA-ARROYO, J.L.; SALAZAR-GARCÍA, S.; BÁRCENAS-ORTEGA, A.E. Determinación irreversible a la floración del aguacate 'Hass' en Michoacán. Revista Mexicana de Ciencias Agrícolas, Morelos, v.1, n.4, p.469-478, 2010.
  • ROCHA-ARROYO, J.L.; SALAZAR-GARCÍA, S.; BÁRCENAS-ORTEGA, A.E.; GONZÁLEZ-DURÁN, I.J.; COSSIO-VARGAS, L.E. Fenología del aguacate 'Hass' en Michoacán. Revista Mexicana de Ciencias Agrícolas, Morelos, v.2, n.3, p.303-316, 2011.
  • SALAZAR-GARCÍA, S.; IBARRA-ESTRADA, M.E.; GONZÁLEZ-VALDIVIA, J. Phenology of ‘Méndez’ avocado in southern Jalisco, México. Agrociencia, Montecillo, v.52, n.7, p.991-1003, 2018.
  • SILBER, A.; ISRAELI, Y.; LEVI, M.; KEINAN, A.; SHAPIRA, O.; CHUDI, G.; ASSOULINE, S. Response of ‘Hass’ avocado trees to irrigation management and root constraint. Agricultural Water Management, Amsterdam, v.104, p.95-103, 2012.
  • SILVA, S.; CANTUARIAS-AVILÉS, T.; CHIAVELLI, B.; MARTINS, M.; OLIVEIRA, M. Phenological models for implementing management practices in rain-fed avocado orchards. Pesquisa Agropecuária Tropical, Goiânia, v.47, n.3, p.321-327, 2017.
  • SOARES, N.; JUNIOR, M.; TEIXEIRA, L.; CASTRO, J. Tolerância a baixas temperaturas de cultivares de abacate (Persea americana Mill.). Revista Brasileira de Fruticultura, Jaboticabal, v.24, n.3, p.721-723, 2002.
  • SOMMARUGA, R.; ELDRIDGE, H.M. Avocado production: water footprint and socio-economic implications. EuroChoices, Uckfield, v.20, n.2, p.48-53, 2021.
  • VARGAS, L.M.; GUZMÁN, A.; MIRANDA, V.; BARRADAS, L. Respuesta fenológica del aguacate (Persea americana Mill) al gradiente climático en Michoacán. In: GRANADOS, R; REYNA, T. (ed.). Centro-Occidente de México variación climática e impactos en la producción agrícola. Ciudad de México: Instituto de Geografía, Universidad Autónoma de México, 2012. p.77-94.
  • WANG, M.; WHITE, N.; GRIMM, V.; HOFMAN, H.; DOLEY, D.; THORP, G.; HANAN, J. Pattern-oriented modelling as a novel way to verify and validate functional–structural plant models: a demonstration with the annual growth module of avocado. Annals of Botany, London, v.121, n.5, p.941-959, 2018.
  • WEIL, A.; RUBINOVICH, L.; TCHERNOV, D.; LIRAN, O. Comparative study between the photosynthetic parameters of two avocado (Persea americana) cultivars reveals natural variation in light reactions in response to frost stress. Agronomy, Madison, v.12, n.5, p.1129, 2022.
  • YEANG, H.Y. Synchronous flowering of the rubber tree (Hevea brasiliensis) induced by high solar radiation intensity. New Phytologist, London, v.175, n.2, p.283-289, 2007.

Publication Dates

  • Publication in this collection
    25 Nov 2022
  • Date of issue
    2022

History

  • Received
    14 June 2022
  • Accepted
    23 Aug 2022
Sociedade Brasileira de Fruticultura Via de acesso Prof. Paulo Donato Castellane, s/n , 14884-900 Jaboticabal SP Brazil, Tel.: +55 16 3209-7188/3209-7609 - Jaboticabal - SP - Brazil
E-mail: rbf@fcav.unesp.br