1. Introduction
Papaya (
Carica papaya L.) is a tropical fruit crop with a short juvenile phase that exhibits continuous flowering after reaching adult phase [
1,
2]. This juvenile phase lasts between three and eight months, depending on genotype, management, and climate. Harvest often starts 9–15 months after planting [
3]. Under favorable conditions, papaya grows nonstop and lives for up to 20 years [
4]. However, most commercial plantations are removed after two or three years mainly because its enormous plant height and plant damages due to pests and diseases [
3].
The benign climate in tropical areas permits papaya planting all throughout the year, allowing continuous fruit production [
5]. In Europe, only a few areas present the climate required to produce papaya, and, where possible, protected cultivation is almost mandatory [
6,
7]. In these areas, performing plantation in the best season determines when the plants enter into production and selects the most favorable dates for initial growth, flowering, and fruit setting. In this regard, climate during flowering strongly affects productivity, since papaya flowers are highly sensitive to extreme environmental conditions of temperature and humidity, resulting in flower malformations that lead to non-commercial fruit [
8]. However, under favorable conditions, papaya cultivation under greenhouses has proven to be very interesting, with yields reaching 200 t ha
−1 in 2 years after planting.
In subtropical papaya-producing areas of Europe, seasonal climate occurs and temperatures above optimum are reached in summer, and below in winter [
6,
9,
10]. Seasonality affects crop performance, resulting in fruit setting failures in different sectors of the trunk. Besides, unstable fruit quality is common in the subtropics. Thus, for these regions, it is necessary to select the season that provides the best yields and fruit quality, and check if we can obtain a more stable supply by combining transplanting seasons. In the Canary Islands, papaya plantations are usually carried out under mesh and are initiated in spring or summer (April or July). These greenhouses up to 7 m high allow plantations lasting for over three years and more. On the contrary, greenhouses of lower height and the more continental climate impede the extrapolation of this model to mainland Europe. It is important to consider that fast growth due to high summer temperatures generates taller plants, even more so if first flowers do not set. This work aims to select the best planting season for papaya grown in plastic greenhouses in subtropical regions of Europe, seeking rapid and stable fruit production and quality throughout the year.
2. Materials and Methods
2.1. Site and Plant Material
The research was performed at the Cajamar Experimental Station ‘Las Palmerillas’, situated in El Ejido, Almería (South East Spain) (2°43′ W, 36°48′ N, 15 km from the Mediterranean Sea and 151 m above sea level). Papaya plants under study grew in a multi-tunnel type greenhouse with five chapels, each 7.5 m wide each, covered with low density polyethylene, and E–W-orientated. The structure was 3.4 m high in the eaves and 5.4 m up to the ridge.
Hermaphrodite plants of the cultivar ‘Intenzza’, provided by the company Semillas del Caribe (Mexico), were selected for the experiment. This hybrid is characterized by red pulp, fruit weight around 1.5 kg (in Spain often less), total soluble solid content between 10 and 13 °Brix in the best seasons, and high and regular production under plastic greenhouses. Hermaphrodite ‘Intenzza’ seedlings were selected at the nursery using molecular markers base on SNPs (Single-Nucleotide Polymorphism), following the procedure described by Parasnis et al. [
11]. The feasibility and profitability of this sexing procedure is compared to the traditional morphological sexing of papaya in the work of Salinas et al. [
12]. Accurate molecular sexing of papaya seedlings, although still expensive, allows planting only one plant per hole, instead of using three–four seedlings per hole and selecting later one hermaphrodite, as it is mandatory when sexing is based on flower appearance weeks after planting. Molecular sexing is also convenient because it avoids the intense initial competition for light among papaya seedlings, unavoidable when 3–4 seedlings are planted together, which provokes taller and thinner plants.
Plant growth, flowering, yield, and fruit quality of plantations implemented in spring versus autumn were compared. The spring plantation, with seedlings spaced 2.5 m × 2 m, was carried out on 6 April 2016, and the autumn plantation, with seedlings spaced 2.5 m × 1.5 m, was carried out on 20 September 2016 (
Figure 1). At the of the experiment, all plants were pulled out at the same date, on 6 July 2018, 27 months and 21 months after transplanting, respectively, once harvesting all commercial fruit took place and when the plants, above 3 m height, were reaching the greenhouse ceiling.
After transplanting, seedlings were given copious irrigation and maintained free of weeds by white plastic mulching (
Figure 1) to assure establishment and good initial growth. Afterward, irrigation and fertilization of these papayas were carried out, taking into consideration plant size and following recommendations for our climate conditions. Misshapen flowers and non-commercial deformed fruits were removed as soon as they were detected, as it was the blade of senescent leaves. Pests and diseases were controlled following IPM guidelines. Powdery mildew (oidium) and red mite are the two most common threats in the protected cultivation of papaya in our experimental conditions.
2.2. Plant Growth Conditions
Climate conditions inside the greenhouse were regulated through natural ventilation provided by one zenithal window per chapel and a lateral side panel. The temperature set point to activate the opening of the windows was established at 24 °C. Throughout the study period, a ventilated aspyropsychrometer with a PT-100 probe recorded the temperature in the greenhouse, while a Priva climate controller stored the data and managed the window activity. Roof whitening was also performed on 1 June 2017, as it is common in the greenhouses of Almería, and consisted of 25 kg of Whitefix® (Royal Brinkman’s, Gravenzande, The Netherlands) diluted in 300 L of water.
2.3. Plant and Fruit Measurements
Plant growth was evaluated every three months. Plant height, considered as the distance from the ground to the top of the canopy, was measured with a grader bar, while trunk perimeter, recorded at 15 cm above the ground, was measured using a seamstress tape ruler. This seamstress tape ruler was also used to measure the distance from the ground to the first flower and later to the first fruit formed. The time, expressed in days, from planting to flowering, and from flowering to harvest, was counted too. The frequency of elongata-type, pentandric and carpelloid hermaphrodite flowers, and that of female and functionally male flowers [
13], was seasonally recorded in selected days of spring (16 May 2017), summer (16 August 2017), autumn (17 November 2017), and winter (14 February 2018). The percentage of flowers with regard to the number of total open flowers at the measurement day was therefore expressed.
Total and commercial yield, the discards (the percentage of non-commercial misshapen fruits not removed and fruits lighter than 200 g), the number of fruits per plant, and their average weight were compared between spring and autumn planting seasons. Harvest was performed several times per week, seasonally dependent, when fruits had 50% of their skin becoming yellow.
Fruit quality was evaluated by its size, firmness, color, and sweetness in papayas harvested from both treatments on 8 May 2018. Fruit size was characterized by its weight, length, and equatorial diameter. Fruits were weighed in a precision balance (d = 0.1 g) (model SB12001, Mettler Toledo, Barcelona, Spain). Fruit length, maximum equatorial diameter, and the width of internal cavity were measured with a digital caliper (model Z22855, Powerfix Profi, Heidelberg, Germany). Pulp firmness was assessed after peel removal, in two opposite equatorial spots of each fruit, through a firmness texter (model Pénéfel DFT 14, Agro-Technology, Forges Les Eaux, France), and expressed in newtons. The juice of each fruit was used to quantify its total soluble solid content (TSS) and its titratable acidity. TSS, measured in °Brix, was determined with a digital-type refractometer (model PR-101, Atago Co., Tokyo, Japan). Titratable acidity (TA) was assessed by titration using 0.1 N NaOH and phenolphthalein as an indicator, expressing the results in g of citric acid per L. TSS changes along the year were compared between planting seasons. Finally, for skin and pulp color determination, three different positions of each fruit were measured with a colorimeter (model CR-400, Konica Minolta Co., Tokyo, Japan). To express the results, we used hue angle (hue°), which indicates the fruit color tone as follows: red at 0°, orange at 45°, yellow-orange at 60°, yellow at 90°, yellowish-green at 120°, green at 180°.
2.4. Statistical Assessment
A randomized complete block experiment was designed with two treatments (spring versus autumn planting season) and four replicates constituted by three experimental plants each (12 plants per treatment in total). Analyses of variance (ANOVA) and mean separation by Tukey’s test were performed, when needed, using Statistix 8.0 software (Analytical Software, Tallahassee, FL, USA).
4. Discussion
Plant growth results indicate that winter is a critical period for papaya growth in our experimental conditions. This happens regardless of the planting season. However, low winter temperatures affect more negatively younger plants transplanted in autumn, especially because the cold conditions that occur shortly after planting delay their entry into production. These young plantlets are besides more exposed to diseases common in humid periods such as powdery mildew and root and trunk rot, which have a serious negative impact on yield.
Spring and early summer in our climate favored growth, flowering, and fruit ripening for the spring cycle plants, explaining thus the better results in the plants of the spring cycle. In contrast, winter slowed down these processes in the plants of the autumn cycle. In this regard, temperatures below 15 °C affect internode elongation in papaya [
15]. Thus, this slower plant growth explains the statistically lower distance from the ground to the first flower formed and to the first fruit set in plants of the autumn cycle.
The first harvest took place much earlier in plants transplanted spring than in those transplanted in autumn, and six months was saved for the entry into production. In this regard, the fruit that were harvested in August, in the plants of the autumn cycle, came from flowers set in February–March, while in the spring cycle, the first flowers setting at the end of the first summer (August–September) allowed harvesting of the first fruits in early winter.
According to previous experimentation, transplanting ‘Intenzza’ seedlings in June is worse, since flowering occurs at a higher height (83.8 cm) than in spring and autumn plants, and the setting of the first fruits takes place at 85.1 cm from the ground [
16], higher than in seedlings transplanted either in spring or autumn. Besides, seedlings transplanted in summer started to ripen fruit 307 days after planting, requiring only 76 days to reach flowering but 231 days from flowering to harvest [
16]. In this context, our results emphasize the importance of maintaining suitable environmental conditions during the first summer following a plantation in a greenhouse, in order to encourage the formation of fertile flowers in the first nodes of the trunk and thus preventing the loss of the first flowers due to fruit set failures. In the work above cited [
16], ‘Intenzza’ seedlings transplanted in June showed an important frequency of functionally male useless flowers during the following months, thus evidencing that harsh conditions of summer affect negatively flower differentiation weeks later. These results also confirm the different performance of a given cultivar (in this case, ‘Intenzza’) depending on the planting season and especially according to the prevalent environmental conditions, as stated by Cabrera et al. [
10]. Nonetheless, in comparison with the yields here measured, that 20-month-long summer cycle was more productive. The commercial yield in that case was 18.7 kg m
−2, with production peaks in spring and autumn and lighter fruits formed (938 g). However, harvest started 10 months after planting, much later than the time measured in our spring cycle.
Gunes and Gübbük [
6] compared three papaya genotypes under protected cultivation in Antalya (Turkey), transplanting them also in spring, but harvesting first fruit in all of them almost 8 months after, 2 months later than in our experiment, in part, because flowering started also 40 days later. This occurred despite the environmental conditions of Antalya seem very similar to those of Almería (Spain). In warmer and more humid conditions, such as those of Bangladesh, sheltering date considers especially cyclone and rain seasons. Nonetheless, plantations carried out in February under different types of nets also shorten the period to flowering and harvesting and allow more and heavier fruit [
17], than in the open field making protected cultivation more profitable.
Cultivation costs of papaya in greenhouses of SE Spain for a 26-month growing cycle are estimated around 0.60 EUR kg
−1, which, although still high, is lower than that for vegetable production considering the higher water consumption for papaya but a much lower expenditure on phytosanitary products than in other horticultural crops [
18]. These calculations of the production costs in protected cultivation include labor force (mostly for cultivation and harvest); inputs for irrigation, fertilization, pest and disease control, and the indirect costs associated with the depreciation of the infrastructure (greenhouse and equipment) [
18]. Considering that the average selling price of papaya paid to farmers is around 1.1 EUR kg
−1 in the main Spanish cooperative (M Casas, pers. comm.), this lower production cost and its high productivity make papaya an attractive and profitable alternative to vegetable production in Almería greenhouses.
On the other hand, our work suggests that combining different planting dates in the same area is not a solution to the seasonality of papaya production, a challenge in the Mediterranean areas. This approach does not fill the production gaps that occur throughout the year, because the plants respond similarly to the climate regardless of their age. Therefore, seasonality cannot be reduced in our climate unless adverse environmental conditions inside the greenhouse are efficiently avoided. Considering our results, an option to maximize early production in the spring plants is to carry out earlier transplanting (at the end of February or early March), which will lead to flowering under the milder temperatures of May–June, with better initial fruit set. A different option is to rely on active greenhouse climate control, as successfully demonstrated by Salinas et al. [
18], or to transplant more developed (and expensive) plantlets raised longer by the nursery, because larger plants with greater leaf area tolerate better the high temperatures of summer. In this context, Honoré et al. [
19] support short cycle papaya cultivation in this region (maximum 18 months), and proposes grafting onto female ‘Intenzza’ rootstock to increase the yield in this cultivar.
Finally, fruit quality was mainly determined by the environmental conditions, so our evaluations support the view that favorable and unfavorable periods affect equally fruit ripening and quality regardless of plant age. Similar total soluble solid changes along the year were also observed in plantations starting in June [
16]. Nevertheless, Nascimento et al. [
20] indicate, on the contrary, that differences in sugar content are related to fluctuations in source–sink relationships throughout the cycle, so higher sugar content might coincide with a larger canopy and/or with a lower number of fruits per plant, and vice versa.