Phenology and thermal requirements of the atemoya tree ( Annona cherimola Mill

Submitted on May 27 , 2019 and accepted on June 24 , 2019. 1 Universidade Estadual de Montes Claros, Departamento de Ciências Agrárias, Janaúba 39440-000, Minas Gerais, Brasil. deborasouzamendes@yahoo.com.br; marlon.pereira@unimontes.br; helissonroberth@hotmail.com; matheus_16pinheiro@hotmail.com Universidade Federal de Minas Gerais, Instituto de Ciências Agrárias, Montes Claros, 39404-547 , Minas Gerais, Brasil. silvia.nietsche@gmail.com Universidade Federal de Viçosa, Departamento de Estatística, Viçosa, 36570-977, Minas Gerais, Brasil. pedro.t.m.paixao@gmail.com * Corresponding author: silvia.nietsche@gmail.com Phenology and thermal requirements of the atemoya tree ( Annona cherimola Mill. X Annona squamosa L.)


INTRODUCTION
Atemoya is an interspecific hybrid, resulting from the cross between cherimoya and sugar apple (Annona cherimola Mill x Annona squamosa L.). The most commonly planted hybrids in Brazil are the "Gefner" and "Thompson" (Tokunaga, 2000). "Gefner" is more suited to semiarid conditions with higher temperatures (average annual temperatures around 27 °C and thermal amplitude around 5 °C), whereas "Thompson" is better suited to subtropical climates (average annual temperatures are almost always below 18 ºC, with thermal amplitudes between 9 ºC and 13 ºC) (Pereira et al., 2011).
The hybrid is cultivated on a commercial scale in several Brazilian regions, occupying an area of more than 1,500 hectares. The main national producer is the State of São Paulo, responsible for 43% of the production, followed by Minas Gerais, Paraná and Bahia, each accounting for 18.8% (Lemos, 2014).
The phenological stages of a given species depends on several environmental factors; however, studies indicate that the temperature of the environment is the main meteorological element that affects the development of different cultivars of maize (Stewart et al., 1998). To relate the influence and importance of air temperature in the development of a plant species, studies have indicated the concept of thermal sum or degree days. The concept of degree days is based on an estimate used to define the plant's response regarding its development to temperature (Warrington & Kanemasu, 1983).
Studies on the phenology and thermal requirements for species of the Annonaceae family are limited. Although it is considered an important family, only two species were evaluated for their phenological stages: cherimoya (Cautín & Agustí, 2005) and sugar apple (Liu et al., 2015;Mendes et al., 2017).
In the present study we proposed characterize the principal development stages according to the general BBCH (Biologische Bundesanstalt, Bundessortenamt und Chemische Industrie) scale with a numerical system with two digits and to define the thermal requirement of the atemoya tree in two agronomic seasons in the Brazilian semiarid region.

MATERIAL AND METHODS
The study was conducted in an experimental orchard of "Gefner" atemoya trees. The plants presented seven years old and were grown in 4.0 m x 2.5 m spacing. The commercial orchard is located at the geographic coordinates of 15°47'50" S and 43°18'31" W and is situated at an altitude of 516 m, Janaúba, Minas Gerais, Brazil. The climate is Aw (KÖPPEN). The soil of the site is a clayey Eutrophic Red Latosol. Irrigation was applied with a microsprinkler system. All cultural practices typically recommended for atemoya cultivation were performed (Pereira et al. 2011).
The first and second pruning were performed on August 23, 2013 (winter) and May 16, 2014 (autumn), respectively. Defoliation of the branches was accomplished manually in order to stimulate the vegetative development. Ten plants from central area of the orchard were selected, a spacing of 8 x 5.0 m was used among plants, uniformity, vigor, and health were also observed. Four branches of each plant were labeled, distributed in four quadrants (north, south, east, and west), and an intermediate bud was selected from each branch. The meteorological data were recorded during the whole evaluation period, corresponding to the two production cycles (agronomic seasons) (August 2013 to January 2015) ( Figure 1 and Table 1).
The phenology and the thermal requirement were determined in two sequential agronomic seasons (August 2013 to April 2014 and May 2014 to January 2015), using the equivalent plants of the commercial area described previously. Three visual observations per week for determination of the principal phenological stages of the crop were performed. External phenological principal development stages were photographed and sequentially characterized by using the general BBCH scale (Hack et al., 1992). A two-digit number system was used, where the first digit was used for the main stages, and the second digit was used for the secondary growth. To characterize the thermal requirement of the plants, the sum in degree days (DD) for the two agronomic seasons (production cycles) was used ( Table 2).
The degree days were calculated according to the methodology proposed by Villa Nova et al. (1972), the base temperature of 10 °C was adopted, according to Silva et al. (2006): , for Tm > Tb; , for Tm < Tb and DD = 0, for Tb > TM, where DD = degree day, TM = maximum daily temperature (°C), Tm = minimum daily temperature (°C), and Tb = base temperature (°C).

RESULTS AND DISCUSSION
According to the general BBCH scale, the atemoya tree presented eight of the ten main stages of the phenological stages (Figures 2, 3, and 4). The onset was characterized by bud development (stage 0) and ended with the beginning of the rest period (stage 9). The four vegetative stages included the development of buds (stage 0), leaf development (stage 1), shoot (buds) (stage 3), and the beginning of the rest period (stage 9). The reproductive stages corresponded to the emergence of inflorescence (stage 5), flowering (stage 6), fruit growth (stage 7), and fruit maturation (stage 8).
The phenological stages of the atemoya tree are described below according to the general BBCH identification scale (Hack et al., 1992):    Regardless of the agronomic seasons, the atemoya tree presented the same main stages of development as the sugar apple tree. Liu et al. (2015) and Mendes et al. (2017), in their studies on the phenology of A. squamosa, described eight main stages of development, using the general BBCH scale, with a three-and two-digit number system, respectively. In contrast, the phenological studies performed with the other parent, A. cherimola, using the same scale with a two-digit number system, described only seven major stages for the species. For the cherimoya tree, the maturation stage of the fruit was not considered (stage 8). According to the authors, the cherimoya tree did not present alteration of the color of the fruit when physiologically mature (Cautín & Agustí, 2005).
The number of days and the thermal requirements for completing each phenological stage were different between the two agronomic seasons of the atemoya tree ( Figure 1, Table 2). In the first cycle (1), the duration and the thermal requirement for each sub-period were 24 days and 272 DD from the closed leaf buds to the end of the leaf with 5 mm (CLB-EL5); 18 days and 207.2 DD from the first leaves separating until showing completely expanded leaves (FLS-FEL). Around 221 days and 2545 DD from budding with 10% of its length to the maximum length (B10L-BML); 29 days and 357 DD from the closed flower buds covered with light scales until the closed flowers with petals that form a long corolla (CFB-CFPL); 14 days and 163 DD from the beginning of the petal opening in the pre-female stage until the end of flowering (BPO-EF); 168 days and 1911 DD from fruiting at the beginning of the ovary growth to fruits at the ideal maturity size for harvest (FOG-IMH); and 65 days and 760 DD from the appearance of the ripening color for harvest until full maturity (ARC-FMC) ( Figure 1, Table 2).
The number of days and the thermal requirements for completing each sub-period in the appearance of the inflorescence and flowering stages were higher in the second cycle. From pruning to the stage where the flowers are closed and the petals form a long corolla, 46 and 52 days were required, and the total thermal requirements were 542 CDD (cumulative degree days) and 563 CDD in the first and second agronomic seasons, respectively. A period of 52 and 59 days were required for completing the flowering period (pruning until the end of the flowering period), and the total thermal requirements were 600 CDD and 634 CDD in the first and second agronomic seasons, respectively.
According to Kshirsagar et al. (1975), although the atemoya tree possesses in its ancestry a genitor from the Andean valleys, the hybrid species is strongly affected by the temperature, especially at night. Studies show that in places of low nocturnal temperatures, a slower development of the flower buds occurs. According to some studies the chronology of the ûowering is controlled by multiple and complex characters and are influenced by temperature at different periods of the year (Cook et al., 2012;Guo et al., 2013).
The periods from pruning of the plants until complete fruit ripening for consumption a total of 224 and 210 days and 2548.9 and 2349.6 CDD were observed for the first and second agronomic seasons, respectively. The atemoya tree cycle presented close values in the two production cycles, from pruning until budding, with a maximum length of 245 and 250 days and total thermal requirements of 2804.6 and 2823.1 CDD for both agronomic seasons.
The most remarkable difference among the agronomic seasons (cycles) was the extension of the phenological sub-stages of fruit development and fruit ripening (FOG-FMC). Comparing the cycles, a extension of 35 days was detected considering these sub-stages in the first cycle. In this particular case it seems that two climate factors were very important: rainfall and insolation.
During the cycle 1 a total insolation of 2137 hours and a rainfall of 737,5 mm was observed ( Figure 1A), and, a total insolation of 2324 hours and a rainfall of 303,10 mm was detected for the second cycle ( Figure 1B).  The solar radiation that falls on the leaves, is considered a climatic factor fundamental, since the intensity, quality and duration of light act as a source of energy and developmental stimulus (Rizzini, 1997). Besides, in tropical species the water is a very important component and tend to increase the time required to complete the development stages in periods of dry seasons. Popenoe (1952) reports that the atemoya tree is considered as member of Annonaceae family, with the greatest capacity for adaptation to diverse climates and geographic regions. Despite this plasticity, the author notes that the hybrid species has better adaptation in tropical regions with higher rainfall. In regions with low rainfall, irrigation practice has been very efficient in supplying water throughout the year.
Although the hybrid species has a few advantages over its parents, one of the problems noted in several studies is the low efficiency of natural pollination. In addition to the phenomenon of protogynous dichogamy, pollen grains of atemoya tree are heavier and sticky, making dispersion of the genetic material difficult. To increase the yield two important characteristics must be improved: number of fruits per plant and fruit size (length and diameter). In this case the artificial pollination is a fundamental practice, and stages 60 to 65 are the ideal moment for this practice (Pereira et al., 2014).
Phenological observations and estimates of heat requirement measured in degree days should be considered as integrative measures of the physical, chemical, and biological environmental conditions to which a species is submitted. In this way, the knowledge, description, and duration of the stages of development of the atemoya tree will allow an increase in the planning of crop management, especially the practices of pruning, fertilization, irrigation, pollination, harvesting, and commercialization. In the case of the atemoya tree, we emphasize that the studies carried out may contribute significantly to the follow-up and monitoring of phenological responses due to climate change, serving as indicators to warn about the impacts of global warming, as well as indicating new strategies to improve the species.

CONCLUSIONS
The general BBCH scale is efficient in identification of the distinct phenological stages of the atemoya tree, in which the development of two agronomic seasons are divided into eight of the ten main possible stages.
The phenological cycle of the atemoya tree, from the stage of leaf buds closed and covered by brown scales until the complete physiological maturity of the fruits, occurred in the period between 217 and 206 days, with thermal requirements of 2469 and 2302 degree days for the first and second agronomic seasons.