ARTÍCULOS ORIGINALES
Fruit yield and growth parameters of several Carica papaya L. genotypes in a temperate climate
Rendimiento en fruto y parámetros de crecimiento en diferentes genotipos de Carica papaya L. bajo clima templado
Gabriel Céccoli 1, 2, 3, Elisa Soledad Panigo 1, 2, 3, Norberto Gariglio 1, Juan Carlos Favaro 1, Carlos Alberto Bouzo 1
1 Facultad de Ciencias Agrarias. Universidad Nacional del Litoral. Kreder 2805. Esperanza. Santa
Fe, Argentina. (S3080HOF). gabrielcnbj@yahoo.com.ar; gceccoli@conicet.gov.ar
2 Instituto de Agrobiotecnología del Litoral (IAL, UNL-CONICET). Santa Fe, Argentina.
3 Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET).
Originales: Recepción: 15/02/2013 - Aceptación: 02/09/2013
Abstract
The aim of this work was to evaluate changes in growth and productivity parameters of different precocious hybrids and a naturalized variety of papaya under both greenhouse and field cultivation in a temperate climate (the center of the province of Santa Fe, Argentina). In view of the aforesaid, the purpose of our research was to identify further genotypes better suited for the cultivation of this species in temperate climates and demonstrate the need for the use of semi-controlled systems to make possible the cultivation of these promising genotypes in middle latitudes. The average yield was 291% higher in greenhouse than in the field. The average productivity for hybrid genotypes compared with the naturalized variety more than doubled in both environments. Considering behavior in height, leaf area index and yield parameters, hybrids H2 (principally), and H4 showed a great adaptation for use in semi-forced systems. The use of greenhouse and short stature papaya hybrids allows its feasible and surely profitable cultivation in non- tropical climates.
Keywords: Semi-forced systems;Tropical crop; Frosts; Leaf area index
Resumen
El objetivo de este trabajo fue evaluar el crecimiento y los parámetros de productividad en diferentes híbridos precoces de papaya y en una variedad naturalizada bajo dos condiciones ambientales en una zona de clima templado (Centro de la Provincia de Santa Fe, Argentina): al aire libre y en invernadero. A partir de lo anterior, el propósito de la investigación fue identificar, además, los genotipos mejor adaptados al cultivo de esta especie en clima templado y demostrar la necesidad de la utilización de sistemas semicontrolados para hacer factible el cultivo de estos genotipos promisorios en latitudes medias. El rendimiento promedio fue un 291% superior en invernadero que al aire libre. La productividad promedio de los híbridos, comparados con una variedad naturalizada de la zona, aumentó más del doble en ambas condiciones ambientales. Considerando las variables altura, índice de área foliar y rendimiento en fruto, se concluye que los híbridos H2 (principalmente) y H4 presentaron muy buena adaptación para su uso en sistemas semi-forzados. El uso de invernaderos y de genotipos de menor estatura brinda mejores condiciones medioambientales para el crecimiento y la producción. Esto permite que el cultivo de papaya sea factible en zonas no tropicales.
Palabras clave: Sistemas semi-forzados; Cultivo tropical; Heladas; Indice de área foliar
Introduction
Papaya (Carica papaya L.) is a crop grown in tropical and subtropical
regions (4, 27, 28), cultivated for its fruit and for the production of papain, a proteolytic
enzyme of elevated commercial value (13, 18). The stem, fruit, leaves and roots of
papaya are used in a wide range of medical applications (7, 15).
The genetic improvement of this species started with the first domestications carried
out in the early 20th century (20, 31, 32). Between 1900 and 1960, at least 56 open
pollinated varieties of papaya (20, 31, 32) were selected. In the 1990s, hybrid cultivars
began to be commercialized; their main selection features were fruit size, taste, a high
pulp/seed ratio, resistance to pests and diseases, early obtention of crops and dwarf plants for greenhouse use (12, 32, 34). It is precisely this latter feature that makes
these genotypes interesting in the production strategies of semi-forced crops, in annual
production cycles, underutilised crop regions or in areas where the climatic limitations at
certain times of the year do not allow production, e.g., the windy season in Guam (23).
Papaya is a polygamous species exhibiting three sex types: male (staminate),
female (pistillate) and bisexual (hermaphrodite) (9, 14). In most cases, plants with
hermaphrodite flowers are desired for commercial production (10, 29). Fruits from
hermaphrodite flowers are usually heavier than those from female flowers, probably
due to the fact that the self-pollination of the former is more effective than the
cross- pollination of the latter (33). Female papaya trees are not grown commercially
as a result of the reduced seed content resulting in a large air space in the seed
cavity due to an ineffective cross pollination (24). In addition, the round shape of the
female fruits requires greater container volume for shipping than the more slender
pyriform- shaped fruit of the hermaphrodite plants (9, 14).
Papaya displays considerable phenotypic variation for many morphological and
horticultural traits (28, 29). However, there are few precise data on morphological diversity
in papaya in the literature (28, 29). Moreover, since this species yields high-quality
products under high radiation and temperatures between 16°C and 25°C (3, 7), in
Argentina it grows mainly in the Northern part of the country (1). At higher latitudes, this
species encounters certain difficulties for its growth and production mainly related to
the incidence of frosts, which may reduce production and cause total loss of plants (4).
Even temperatures lower than 11°C adversely affect papaya growth (4, 5).
In the East central region of the province of Santa Fe, the expansion of this
crop is principally limited by the occurrence of frost, but it is possible to find large
samples of naturalized varieties in urban plantations with a lower incidence of frosts.
The generation and subsequent use of precocious hybrids with smaller plants would
facilitate the inclusion of this species both in semi-forced greenhouse systems (15) and frost-free fields (4).
The aim of this work was to evaluate changes in growth and productivity
parameters of different precocious hybrids and a naturalized variety of papaya under
both greenhouse and field cultivation in a temperate climate (the center of the province
of Santa Fe, Argentina), as well as to identify materials best adapted to semi-forced
systems in non tropical climates.
Materials and methods
Plant materials and cultivation conditions
The study was performed at the Experimental Field of Intensive and Forest Farming
(Campo Experimental de Cultivos Intensivos y Forestales, Facultad de Ciencias
Agrarias, Universidad Nacional del Litoral) (32°30' S, 62°15' W), Esperanza, Santa Fe,
Argentina. Mean annual precipitation total is about 1,000 mm. Eight experimental
precocious hybrids of papaya (Carica papaya L.) were used, supplied by Western
Seed Co. Spain S. A. (Las Palmas, Islas de Gran Canaria, Spain) here described by
an alpha-numeric code: H1, H2, H3, H4, H5, H7, H8, and H9. A naturalized variety (T)
of the region was also included. Two environmental conditions were established:
field (F) and greenhouse cultivation (GC). Multi-span greenhouses were used with
vertical walls of 3.5 m and total height of 5.5 m, 30 m length and 9 m width. Each
greenhouse had a floor surface covered of 270 m2. They were heated to maintain a
minimum temperature above 0°C and ventilation was natural and automatic; windows
opened when the air temperature was higher than 23°C. In F, average maximum and
minimum temperatures were lower than in GC, with absolute minimum temperatures
of -5°C during the first year and- 3°C in the second year (figure 1a) and absolute
maximum temperature of 40°C. In GC, absolute minimum temperatures were always
above 1°C (figure 1b), and absolute maximum temperature of 47°C in the first year
and 49°C in the second one.
Figure 1. Maximum and minimum temperature values (°C) in field (a) and in the
greenhouse experiments (b).
Figura 1. Valores de temperaturas máximas y mínimas (°C) en el experimento al aire
libre (a) y en invernadero (b).
Seeds were sown at warm temperatures (30°C) as described by Yahiro (38),
without removing the sarcotesta (36), in pots of 1,500 cm3. Transplantation was
performed after 5 months of sowing. At this time, plants had an average height of 0.50 m
and 550°Cd of thermal time accumulation (37). Plants density was 2,380.95 plants ha-1 obtained by a planting distance of 1.4 m between rows and 3.0 m between plants in
F and 2,222.22 plants ha-1 obtained by a planting distance of 1.5 m between rows
and 3.0 m between plants in GC. As shown, differences in plant densities between
field and greenhouse conditions were due to the distance of the drip lines installed.
Silt loam Molisolls (Aquic Argiudoll in both conditions) were used as growing medium.
In order to prevent the possible accumulation of water and the risk of plant loss, the
soil was prepared by building 0.20 m high and 0.60 m wide domes to avoid water
logging (16). The drip irrigation system was accomplished by means of surface
pipelines. A fertirrigation with N, P2O4 and K2O was also performed according to what
was recommended by Crane (9, 14).
Air temperature was measured hourly during 650 days after transplant (DAT) by means
of two Davis Weather Wizard III® automatic meteorological stations, one in F and the other
in GC. Mean annual radiation values were 18.1 MJ m-2 d-1 for F and 14.2 MJ m-2 d-1 for GC.
Growth and productivity variables
The experiment ended at 650 DAT. The following variables were measured: leaf
area (LA) (cm2), plant total height (cm), number of flowers at anthesis, fruits per plant
(N° plant-1), fruit weight (g fruit-1) and variety total yield (kg plant-1).
Leaf area was estimated, by the authors, from the following allometric equation,
previously obtained for the naturalized variety:
LA (cm2) = 0.89 x (length x width) - 49.41 (R2 = 0.97)
Then, the LA expression in m2 plant-1 and considering plant density (plants m-2)
allowed estimating the Leaf Area Index (LAI) (m2 m2). Plant height was taken with a
graduated tape measure.
Time to flowering was recorded once plants presented first flowers at anthesis. The
number of flowers at anthesis was counted, every 40 days, on 13 samplings from 19 DAT
up to 544 DAT. Following Parés et al. (30), measurements were performed during daytime.
At the end of the experiment, productivity was quantified as the individual
weight and fruit number per plant and variety total yield (in fruits with an equatorial
diameter above 100 mm) as described by Pomper et al. (32). Five plants were randomly
selected from each hybrid and repeated, the selected fruit having a diameter above
50 mm at the time of the first extraction.
Statistical design and analysis
The experimental design used was randomized blocks with three blocks per
treatment and 5 plants per block. In this way, 18 treatments were obtained, from a
combination of 9 genotypes and 2 environments (F and GC). The statistical analysis was performed through ANOVA; the means between treatments were compared by
Duncan's test, with a significance level of 5% and 1% in certain cases. The Statgraphics
Plus 5.0® computer statistical program was used to perform the statistical analyses
and graphs (21). ANOVA assumptions were met in all analyses.
Results and discussion
Leaf area index (LAI)
LAI was greater in GC than in F (figures 2a-2b). In F, the lower values of LAI
(figure 2b) resulted in a slower growth of the plants after winter. In GC, since there
were no frosts and day temperatures were higher than in F, ambient conditions in GC
resembled those of tropical regions, where higher growth rates are reached. With
temperatures below 15°C, this crop grows more slowly, which finally occurs at the
end of autumn and beginnings of spring (22, 26, 27).
Figure 2. Evolution of the leaf area index of the cultivars in field (a) and greenhouse
cultivation (b) as a function of the days after transplant (DAT).
Figura 2. Evolución del índice de área foliar de los genotipos utilizados al aire
libre (F) (a) y en invernadero (GC) (b) en función de los días luego del
trasplante (DAT).
Even temperatures lower than 11°C adversely affect papaya growth (3, 4, 5, 7, 26).
Given the fact that in GC temperatures were similar to those of tropical regions, but
not equal, even in winter, genotypes also decreased their LAI. These low values of
LAI could not only be the result of low temperatures (as in F) but also a consequence
of the lower radiation received in this season of the year (winter) (figure 2a).
When the older leaves are in a low light-intensity environment, the photosynthesis
rate is reduced as the stomatic conductance dramatically decreases (3, 8). If this
situation persists, with light intensities below the light compensation point, leaf
abscission occurs (6).
Damage or death caused by frost starts at temperatures below -0.6°C (9, 14, 26, 27).
In F, frost severity during the first year resulted in total defoliation (figure 2b, page 303)
and in some cultivars, such as H3, H4 and H9, even in plant death or null yield, such
as in H3, H4, H8 and H9 (table 1).
Table 1. Effect of two environmental conditions, greenhouse cultivation (GC) and
field (F), upon the final accumulated yield values (kg plant-1), number of fruits
(N° plant-1), individual weight (g fruit-1) and latex production (cm3 fruit-1).
Tabla 1. Efecto de dos condiciones ambientales, cultivo en invernadero (GC) y al aire
libre (FC), sobre el rendimiento en fruto por planta (kg planta-1), el número
de frutos (N° planta-1), el peso individual de los mismos (g fruto-1) y sobre
la producción de látex (cm3 fruto-1).
The plants in GC never presented total defoliation, different from those in F, in
which the LAI was zero in winter (figure 2b, page 303). Hybrid H2 had the highest
LAI both in F (in Summer) and in GC (Autumn-Winter), possibly being a genotype
with good adaptation to cool conditions given its tolerance to frost and rapid regrowth
with increasing temperatures, these variables being well correlated with high fruit
yields (table 1).
The source/sink balance in papaya is critical for the establishment and development
of fruit (6). In general, each mature leaf is able to provide photoassimilates for about
three fruits (19, 35, 39). This ratio would mostly explain the yield difference obtained
in GC compared to the production in F (table 1, page 304).
Height
In GC, the naturalized cultivar (T) was the tallest one, reaching 4.30 m (figure 3a) at the end of the experiment. This meant a difference above 2.00 m with respect to
hybrid cultivars, among which the tallest one was H9 (2.31 m) and the smallest one,
H5 (1.76 m) (figure 3a).
Figure 3. Changes in the average height of plants (cm) of the field (a) and greenhouse
cultivation (b) conditions as a function of the days after transplant (DAT).
Figura 3. Cambios en la altura promedio de las plantas (cm) al aire libre (F) (a) en
invernadero (GC) (b) en función de los días luego del trasplante (DAT).
On the contrary, in F there were no statistically significant differences between
T and hybrid cultivars (figure 3b). The behavior observed in T, which occurred in the
GC microclimate explained above, also resembled the heights that plants can reach in
tropical regions (9 m) (9, 11, 19, 23). The difference in height between environments
could be caused by the low temperatures in F. Besides, the action of the wind could
be another determining factor of this variable, since it is known that it decreases the
production of leaf and stem dry matter (6, 23, 25). Therefore, the use of greenhouse
would encourage vegetative growth.
In this trial, sensitivity differences between hybrids could be not observed.
Considering that low temperatures are one of the main limitations for the expansion
of papaya-cultivated areas to higher latitudes (11, 26), all hybrids genotypes could be
taken into account in improvement programs, being suitable for greenhouse cultivation
due to their smaller height or dwarf habitus (figure 3b). In contrast, the use of the
naturalized cultivar T in GC is not recommended because of its high stature.
Floral parameters
Flowering time
During 100 DAT, there was only vegetative growth in GC (figure 4b), in agreement
with what was reported by Khan et al. (17) for varieties of papaya in Hawaiian fields,
where flowering occurs approximately at 120 DAT. In F, precocity was observed in
cultivars H1, H2 and H5, with flowering starting at 45 DAT (figure 4a).
Figure 4. Number of flowers per plant in field (a) and greenhouse cultivation (b)
cultivars.
Figura 4. Número de flores totales por planta al aire libre (a) y en invernadero (b) en
los genotipos estudiados.
Genotypes T and H7 did not present this behavior (figure 4b). The differences between these two groups of genotypes (H1, H2 and H5 vs. T and H7) may have been caused by the maximum temperature during this period (Autumn, figure 1a, page 301), since minimum temperatures were similar under both conditions (figures 1a-1b, page 301).
Number of flowers
In this species, the available information on phenology is relatively
scarce (6, 10, 17, 19). Temperatures above 32°C and below 10°C would severely
affect the production of pollen and its viability (3, 4). After 200 DAT, flower production
increased in GC, with no substantial modification in maximum temperatures,
even though an increase in minimum temperatures was certainly observed
(figure 1, page 301; figure 4b). In this period there was an increase in solar radiation
coinciding with a higher LAI (figure 2a, page 303). These factors are directly involved in
both an increase in the photosynthesis rate of the crop (3, 7, 8) and a greater amount
of the photoassimilates available for flowering (3, 4). Only two genotypes showed
differences in total number of flowers, having a high number of flowers compared with
all the genotypes under study (hybrid H4 in GC between 100 and 375 DAT, figure 4b;
and T in F between 300 DAT and the end of trial, figure 4a).
Fruit yield
Differences between environmental conditions
Average yields were 15.48 kg pl-1in F and 60.48 kg pl-1 in GC (291% > in GC). Average
productivity for hybrid genotypes (without taking into account T) under greenhouse
conditions was 71.3 kg pl-1 while in F it was 17.5 kg pl-1. The difference in yield was
higher if the hybrid average was compared to T (307% in the hybrids and 201% in T).
The yields in GC were 134 Mg ha-1 (expressed in Mg ha-1). These values show first
the production potential represented by the greenhouse production of this crop, and
second, that better benefits are achieved if hybrids are used instead of naturalized
materials (T). The same conclusions were arrived at with greenhouse production
in the Canary Islands, where better yields and quality were obtained than in field
conditions (15). Another reason for the yield in GC being higher than in F was
probably due to the fact that during the winter months, the plants kept their leaves
(figure 2a, page 303) whereas in F defoliation was complete (figure 2b, page 303).
Although LAI in GC decreased during winter, the few leaves produced allowed the
rapid growth of previously established fruits. Likewise, the growth rate of these fruits
was lower than that obtained under optimal conditions (3).
Difference between genotypes
The production of fruit presented statistically significant differences between
genotypes for both environmental conditions (table 1, page 304).The maximum
production in GC was obtained with hybrid H2 (91.8 kg pl-1) whereas in F, this genotype
produced 24.3 kg pl-1 (table 1, page 304). The greatest production of this hybrid in
both experiments was well correlated with the highest value of LAI reached at the
end of the experiment mainly (450-550 DAT; figure 2, page 303). On the contrary, the
naturalized material presented lower yield values. Different from hybrid cultivars, the
height of this genotype in GC (figure 3a, page 305) caused that parts of the flowers
were subject to temperatures above the optimal level (threshold).This could bring
about flower abortion and abscission and, consequently, a lower production of fruit.
Fruit size would be a function not only of efficient pollination but also of
LAI and photosynthetic activity (6, 25).Hybrid H2 had the longest production
time of hermaphrodite flowers (data not shown) and presented the highest yield
(table 1, page 304; figure 4, page 306) but not the highest fruit number and fruit
weight. These two parameters overall led hybrid H2 to have the highest yield per
plant. Moreover, it is known that both variables are not independent from one another
because the fruit average weight partly depends on the number of fruit present (6, 25).
Cultivar T in GC obtained the highest number of fruit per plant and, accordingly,
the lowest weight per fruit (table 1, page 304). Although LAI in T was high
(figure 2a, page 303), when the average foliar area was related to the number of
fruit per plant during the whole experiment, the latter was one of the lowest (1107
cm2 of leaf per established fruit), thus showing the high efficiency of this genotype
for the establishment of fruit per foliar area unit (data not shown). On the contrary,
hybrids H2 and H8 presented the highest individual weight per fruit (1.531 and
1.718 kg fruit-1, respectively) (table 1, page 304) but the ratio average leaf surface to fruit was 1764 cm2 and 2318 cm2 of leaf per fruit. Beyond the commercial need of
obtaining bigger fruit, genotype T would have a better efficiency in the source/sink
ratio, e.g. a higher capacity of producing fruit per foliar surface area. As observed for
other species, obtaining a better efficiency in the source/ sink ratio is detrimental to
fruit weight (2, 6, 25).
Hybrid H2 could be a good candidate for use in semi-forced systems just as it
is good for greenhouse utilization. This claim is sustained by the fact that it had the
best performance with the parameters measured, high weight of fruits per plant and
intermediate number of fruits per plant compared with the other genotypes.
The decrease in fruit number per plant was the main component explaining the
lesser yield in F. In the genotypes which tolerated low temperatures in F and then regrew
(H1, H2, H5, H7 and T), this variable was 79% lower in F than in GC. Considering
survivor genotypes in F, fruit weight did not explain the decrease in yields between
F and GC. On the contrary, there was an increase in the average weight fruit in F of
about 19% compared with GC. (table 1, page 304). This increase in fruit weight in F
compared with GC was not enough to compensate the greater decrease in fruit number,
leading to a steep decline in fruit number per plant (table 1, page 304).
Conclusions
Environmental factors profoundly affect growth and productivity parameters in
papaya. Therefore, an accurate understanding of the interaction between environmental
conditions and the different genotypes is extremely important for the profitable,
sustainable production of this plant.
Considering the LAI parameter, hybrid H2 had the highest values in F (in Summer)
and in GC (Autumn-Winter), possibly being a genotype with good adaptation to cool
conditions given its tolerance to frost and rapid regrowth with increasing temperatures.
Considering the height parameter, all hybrid genotypes could be taken into account
in improvement programs, being suitable for greenhouse cultivation due to their smaller
height or dwarf behavior.
Considering the number of flowers, hybrid H4 had the highest value, correlating
well with a high yield.
The higher temperatures and the non-existence of temperatures that might
cause frost in GC allowed all genotypes to obtain higher yields than in F. The average
productivity of hybrid genotypes compared to that of the naturalized variety was more
than double in both environments. In the same way, average productivity for hybrid
genotypes under greenhouse conditions was 71.3 kg pl-1 while in F it was 17.5 kg pl-1.
The average yields obtained with greenhouse hybrids indicate their productive potential
when they are placed under optimal environmental conditions.
Considering behavior in height, LAI and yield, hybrids H2 and H4 presented a high
level of adaptation. These genotypes were the most promising ones in the greenhouse
production of papaya in temperate climates.
Finally, we would like to emphasize the need for carrying out this crop under
semi-forced systems in temperate climate latitudes (as the area studied in this work)
where outdoor growing is not feasible. The use of greenhouse and short stature papaya
hybrids allows its feasible and surely profitable cultivation in non-tropical climates.
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Acknowledgments
To Universidad Nacional del Litoral for the support in supplying the infrastructure and equipment needed to
carry out this research study.
To CONICET (Consejo Nacional de Investigaciones Científicas y Técnicas) for allowing
G. Céccoli and E. S. Panigo devote time to the processing and realization of this work.
To Dr. Abelardo Vegetti for his useful comments and advice.