Abstracts
The objective of this work was to evaluate the floral biology and pollination requirements of seeded and seedless mini watermelon varieties, and to determine the best varieties to cultivate under protected environment. Three seedless (HA-5106, HA-5158, and HA-5161) and two seeded (Minipol and Polimore) genotypes were tested. Flowers were monitored from the pre-anthesis stage to senescence, and fruit quality was also evaluated. The evaluated treatments were hand-geitonogamous pollination (MG), cross-pollination with pollen from the Polimore variety (MCP), cross-pollination with pollen from the Minipol variety (MCM), and restricted pollination. All varieties had monoecious plants with diclinous flowers, and the stigmas remained receptive throughout anthesis. Fruit set rates of 84.62% (MG), 61.54% (MCP), 48% (MCM), and 0% (restricted) were obtained for seeded varieties, but of 0% (MG), 76.36% (MCP), 82.69% (MCM), and 0% (restricted) for seedless varieties. Fruits did not differ in quality among treatments within each genotype. Therefore, all the studied varieties require a pollination agent and diploid pollen for fruit set to occur, regardless of the donor variety; and Minipol or Polimore with HA-5106 or HA-5158 are the varieties recommended for cultivation in protected environment.
Citrullus lanatus; flowering; fruit quality; fruit set; greenhouse
O objetivo deste trabalho foi avaliar a biologia floral e os requerimentos de polinização de variedades de minimelancia com e sem sementes, e determinar as melhores variedades para cultivo em ambiente protegido. Três genótipos sem semente (HA-5106, HA-5158 e HA-5161) e dois com semente (Minipol e Polimore) foram testados. As flores foram monitoradas da pré-antese à senescência, e a qualidade dos frutos também foi avaliada. Avaliaram-se tratamentos de polinização manual por geitonogamia (MG), de pólen cruzado da variedade Polimore (MCP), de pólen cruzado da variedade Minipol (MCM) e de polinização restrita. Todas as variedades apresentaram plantas monoicas e flores díclinas, e os estigmas permaneceram receptivos durante toda a antese. Foram obtidas taxas de vingamento de 84,62% (MG), 61,54% (MCP), 48% (MCM) e 0% (restrita) para as variedades com semente, mas de 0% (MG), 76,36% (MCP), 82,69% (MCM) e 0% (restrita) para aquelas sem semente. Os frutos não diferiram quanto à qualidade entre os tratamentos dentro de cada genótipo. Portanto, todas as variedades estudadas requerem um agente polinizador e pólen diploide para o vingamento de frutos, independentemente da variedade doadora; e Minipol ou Polimore com HA-5106 ou HA-5158 são as variedades recomendadas para cultivo em ambiente protegido.
Citrullus lanatus; florescimento; qualidade dos frutos; vingamento de frutos; casa de vegetação
Introduction
Traditionally, watermelon [Citrullus lanatus (Thunb.) Matsum. & Nakai] is a plant cultivated in open field and usually produces large-sized fruit with great amount of seeds scattered throughout their flesh. However, motivated by new consumer demands, breeders have developed smaller fruits and seedless varieties (Walters, 2009WALTERS, S.A.; SCHULTHEIS, J.R.Directionality of pollinator movements in watermelon plantings. HortScience, v.44, p.49-52, 2009.; Bomfim et al., 2013BOMFIM, I.G.A.; CRUZ, D. de O.; FREITAS, B.M.; ARAGÃO, F.A.S. de. Polinização em melancia com e sem semente. Fortaleza: Embrapa Agroindústria Tropical, 2013. 54p. (Embrapa Agroindústria Tropical. Documentos, 168).).
The arrival of these new varieties, such as mini watermelons, make feasible the
cultivation of this vegetable in protected environments, which make it possible to
minimize losses in yield, improve fruit quality, and provide early or out-of-season
harvest (Seabra Júnior et al., 2003SEABRA JÚNIOR, S.; PANTANO, S.C.; HIDALGO, A.F.; RANGEL, M.G.; CARDOSO,
A.I.I. Avaliação do número e posição de frutos de melancia produzidos em ambiente
protegido. Horticultura Brasileira v.21, p.708-711, 2003. DOI:
10.1590/S0102-05362003000400028.
https://doi.org/10.1590/S0102-0536200300...
; Cruz & Campos, 2009CRUZ, D. de O.; CAMPOS, L.A. de O. Polinização por abelhas em cultivos
protegidos. Revista Brasileira de Agrociência, v.15, p.5-10, 2009.; Campagnol et al., 2012CAMPAGNOL, R.; MELLO, S. da C.; BARBOSA, J.C. Vertical growth of mini
watermelon according to the training height and plant density. Horticultura
Brasileira, v.30, p.726-732, 2012. DOI:
10.1590/S0102-05362012000400027.
https://doi.org/10.1590/S0102-0536201200...
). However, watermelon plants do not produce
fruits without a pollination agent (Walters,
2005WALTERS, S.A. Honey bee pollination requirements for triploid
watermelon. HortScience, v.40, p.1268-1270, 2005.; Guerra Sanz, 2008GUERRA SANZ, J.M. Crop pollination in greenhouses. In: JAMES, R.R.;
PITTS-SINGER, T.L. (Ed.). Bee pollination in agricultural ecosystems. New York:
Oxford University, 2008. p.27-47. DOI:
10.1093/acprof:oso/9780195316957.003.0003.), and this
artificial environment blocks the entrance of natural pollinators in the system (Cruz & Campos, 2009CRUZ, D. de O.; CAMPOS, L.A. de O. Polinização por abelhas em cultivos
protegidos. Revista Brasileira de Agrociência, v.15, p.5-10, 2009.). Consequently, for highly
pollinator-dependent crops to produce fruits under protected environment, it is
necessary to introduce biotic pollinators (Slaa et al.,
2006SLAA, E.J.; SÁNCHEZ CHAVES, L.A.; MALAGODI-BRAGA, K.S.; HOFSTEDE, F.E.
Stingless bees in applied pollination: practice and perspectives. Apidologie, v.37,
p.293-315, 2006. DOI: 10.1051/apido:2006022.
https://doi.org/10.1051/apido:2006022...
; Cruz & Campos, 2009CRUZ, D. de O.; CAMPOS, L.A. de O. Polinização por abelhas em cultivos
protegidos. Revista Brasileira de Agrociência, v.15, p.5-10, 2009.) or to
hire manpower to manually pollinate the flowers (Slaa et
al., 2006SLAA, E.J.; SÁNCHEZ CHAVES, L.A.; MALAGODI-BRAGA, K.S.; HOFSTEDE, F.E.
Stingless bees in applied pollination: practice and perspectives. Apidologie, v.37,
p.293-315, 2006. DOI: 10.1051/apido:2006022.
https://doi.org/10.1051/apido:2006022...
).
Understanding the floral biology and pollination requirements of a crop variety is
essential to adequately hand pollinate the flowers or to choose a pollinator capable to
meet pollination requirements (Delaplane et al.,
2013DELAPLANE, K.S.; DAG, A.; DANKA, R.G.; FREITAS, B.M.; GARIBALDI, L.A.;
GOODWIN, R.M.; HORMAZA, J.I. Standard methods for pollination research with Apis
mellifera. Journal of Apicultural Research, v.52, p.1-28, 2013. DOI:
10.3896/IBRA.1.52.4.04.
https://doi.org/10.3896/IBRA.1.52.4.04...
). Even for seedless watermelon varieties (triploid, 3n), adequate
pollination is necessary to release the amount of phytohormones needed to stimulate not
only the fruit set, but also a good fruit development (Walters, 2005WALTERS, S.A. Honey bee pollination requirements for triploid
watermelon. HortScience, v.40, p.1268-1270, 2005.). Walters (2005)WALTERS, S.A. Honey bee pollination requirements for triploid
watermelon. HortScience, v.40, p.1268-1270, 2005. also
stated that, for fruit set to occur in triploid varieties, these must be grown close to
a diploid variety, planted as a pollen donor.
Moreover, although there is some knowledge about pollination of conventional watermelon
varieties (Adlerz, 1966ADLERZ, W.C. Honey bee visit numbers and watermelon pollination. Journal
of Economic Entomology, v.59, p.28-30, 1966. DOI:
10.1093/jee/59.1.28.
https://doi.org/10.1093/jee/59.1.28...
; Stanghellini et al., 1997STANGHELLINI, M.S.; AMBROSE, J.T.; SCHULTHEIS, J.R.The effects of honey
bee and bumble bee pollination on fruit set and abortion of cucumber and watermelon.
American Bee Journal, v.137, p.386-391, 1997., 1998STANGHELLINI, M.S.;; AMBROSE, J.T. SCHULTHEIS, J.R.Using commercial
bumble bee colonies as backup pollinators for honey bees to produce cucumbers and
watermelons. HortTechnology, v.8, p.590-594, 1998., 2002STANGHELLINI, M.S.; SCHULTHEIS, J.R.; AMBROSE, J.T.Pollen mobilization
in selected cucurbitaceae and the putative effects on pollinator abundance on pollen
depletion rates. Journal of the American Society for Horticultural Science, v.127,
p.729-736, 2002.; Araújo et al., 2014BELFORT, C.C.; NERY, E.B.; SILVA FILHO, J.A. de S.; SETÚBAL, J.W.; THÉ,
F. de W.; PARENTE, M.B. Influência da polinização artificial na dinâmica floral de
melancia triplóide em condições de cultivo protegido. Horticultura Brasileira, v.21,
p.349-422, 2003. Suplemento 2.), little has been done to define the floral
biology and pollination requirements of modern genotypes, including mini watermelon
varieties. Sometimes breeders, aiming to improve vegetable traits, also,
unintentionally, alter floral traits, which, to some extent, affect the pollination
process. This probably happens since floral aspects regarding pollination are not
normally targeted by breeders (Guerra Sanz, 2008GUERRA SANZ, J.M. Crop pollination in greenhouses. In: JAMES, R.R.;
PITTS-SINGER, T.L. (Ed.). Bee pollination in agricultural ecosystems. New York:
Oxford University, 2008. p.27-47. DOI:
10.1093/acprof:oso/9780195316957.003.0003.;
Klatt et al., 2013KLATT, B.K.; BURMEISTER, C.; WESTPHAL, C.; TSCHARNTKE, T.; FRAGSTEIN, M.
von. Flower volatiles, crop varieties and bee responses. Plos One, v.8, 2013. DOI:
10.1371/journal.pone.0072724.
https://doi.org/10.1371/journal.pone.007...
).
The objective of this work was to evaluate the floral biology and pollination requirements of seeded and seedless mini watermelon varieties, and to determine the best varieties to cultivate under protected environment.
Materials and Methods
The experiment was carried out from August to October 2011 in a greenhouse covered with transparent plastic film, fitted with automated drip fertigation and temperature control systems, comprising an area of 160 m2 (8 m wide x 20 m long x 3.5 m high), located at Embrapa Agroindústria Tropical, in the municipality of Fortaleza, in the state of Ceará, Brazil (3°45'05"S, 38°34'35"W, at 36 m altitude).
Five different mini watermelon genotypes were tested: three triploid seedless (HA-5106, HA-5158, and HA-5161) and two diploid seeded (Minipol and Polimore) genotypes.
Seeds were sown in 200 cell-plastic trays filled with a commercial substrate prepared
using dried and powdered coconut fiber. Twelve days later, seedlings were transplanted
to 5 L plastic jars, which were previously filled with raw coconut fiber and powdered
coconut fiber (1:1). Jars were spaced at 0.8 m between rows and 0.4 m between plants.
Following recommendations for the cultivation of seedless varieties, a 3:1 ratio between
triploid and diploid varieties was used in dedicated rows (Dittmar et al., 2009DITTMAR, P.J.; MONKS, D.W.; SCHULTHEIS, J.R. Maximum potential
vegetative and floral production and fruit characteristics of watermelon pollenizers.
HortSience, v.44, p.59-63, 2009.). On the seventeenth day after transplanting,
staking was done with a plastic trellis for vertical conduction of plants, a procedure
that facilitates crop management in greenhouse conditions (Campagnol et al., 2012CAMPAGNOL, R.; MELLO, S. da C.; BARBOSA, J.C. Vertical growth of mini
watermelon according to the training height and plant density. Horticultura
Brasileira, v.30, p.726-732, 2012. DOI:
10.1590/S0102-05362012000400027.
https://doi.org/10.1590/S0102-0536201200...
). Throughout cultivation, plants were drip
fertigated, and provided with a suitable amount of water and nutrients for each growth
stage.
In order to study the floral characteristics and the period of anthesis of the five
genotypes, 30 buds of each variety were monitored hourly, from the pre-anthesis phase
until petal closure, along the entire flowering phase. Collected data were related to
sexual expression, basic floral morphology, available floral resource, longevity, and
opening and closing time of flowers and petals during anthesis (Andrade et al., 2014ANDRADE, P.B.; FREITAS, B.M.; ROCHA, E.E.M.; LIMA, J.A.; RUFINO, L.L.
Floral biology and pollination requirements of sesame (Sesamum indicum L.). Acta
Scientiarum. Animal Sciences, v.36, p.93-99, 2014. DOI:
10.4025/actascianimsci.v36i1.21838.
https://doi.org/10.4025/actascianimsci.v...
).
In addition, data on luminosity (klux) were collected and determined by a digital lux meter, and data on temperature (°C) and relative humidity (%) of air were measured hourly by a datalogger placed inside the greenhouse.
The pollination requirements of all varieties were studied in a completely randomized
design, with only one hand-pollination treatment performed per plant. For analysis of
pollination requirements, four pollination treatments were carried out in the female
flowers of the five varieties, according to Delaplane et
al. (2013)DELAPLANE, K.S.; DAG, A.; DANKA, R.G.; FREITAS, B.M.; GARIBALDI, L.A.;
GOODWIN, R.M.; HORMAZA, J.I. Standard methods for pollination research with Apis
mellifera. Journal of Apicultural Research, v.52, p.1-28, 2013. DOI:
10.3896/IBRA.1.52.4.04.
https://doi.org/10.3896/IBRA.1.52.4.04...
, with some adaptations, as described below. The number of flowers
per treatment corresponded to the maximum pollination treatments possible for each
variety. Therefore, these numbers varied among varieties.
The cited adaptations included: hand-geitonogamous pollination (MG); manual cross-pollination with pollen from the Minipol variety (2n) (MCM); manual cross-pollination with pollen from the Polimore variety (2n) (MCP); and restricted pollination.
In MG, pre-anthesis pistillate floral buds (female) were protected by tulle bags in the late afternoon. The next morning, the flower buds that opened were unpacked and subjected to manual pollination using pollen from staminate flowers (male) of the same plant. This was accomplished by collecting two staminate flowers (three staminate flowers for triploid varieties) and folding back their petals before manually rubbing the anthers of these flowers against the whole surface of the three stigma lobes of the female flowers. Immediately after pollination, the female flowers were tagged and bagged again, remaining protected until the following morning, in order to avoid any contamination with other pollen grains (Ferreira, 2005FERREIRA, M.A.J. da F. Técnicas de produção de sementes de melancia, via polinizações manuais controladas, em campo e casa-de-vegetação. Brasília: Embrapa Recursos Genéticos e Biotecnologia, 2005. 7p. (Embrapa Recursos Genéticos e Biotecnologia. Circular técnica, 40).).
In MCM, pistillate flower buds were subjected to the same procedure of the previous treatment. However, when the flower was unbagged, pollination was carried out with staminate flowers from the Minipol variety.
MCP was similar to the treatment described before, but the pollen donor variety used to pollinate the flowers was Polimore.
Finally, in restricted pollination, considered as the control treatment, pistillate flowers remained bagged from pre-anthesis until the end of the anthesis period.
All hand pollination treatments were performed in the morning between 6:00 and 10:30
a.m., since this interval corresponds to the period of maximum receptivity, although the
stigmas remain receptive throughout anthesis (Ferreira,
2005FERREIRA, M.A.J. da F. Técnicas de produção de sementes de melancia, via
polinizações manuais controladas, em campo e casa-de-vegetação. Brasília: Embrapa
Recursos Genéticos e Biotecnologia, 2005. 7p. (Embrapa Recursos Genéticos e
Biotecnologia. Circular técnica, 40).; Kwon et al., 2005KWON, S.W.; JASKANI, M.J.; KO, B.R.; CHO, J.L. Collection, germination
and storage of watermelon (Citrullus lanatus Thunb.) pollen for pollination under
temperature conditions. Asian Journal of Plant Science, v.4, p.44-49, 2005. DOI:
10.3923/ajps.2005.44.49.
https://doi.org/10.3923/ajps.2005.44.49...
). Furthermore,
only female flowers from the plant's eighth node onwards were pollinated, as suggested
by Seabra Júnior et al. (2003)SEABRA JÚNIOR, S.; PANTANO, S.C.; HIDALGO, A.F.; RANGEL, M.G.; CARDOSO,
A.I.I. Avaliação do número e posição de frutos de melancia produzidos em ambiente
protegido. Horticultura Brasileira v.21, p.708-711, 2003. DOI:
10.1590/S0102-05362003000400028.
https://doi.org/10.1590/S0102-0536200300...
. The
quantification of the number of fruit sets was conducted three days after the
pollination treatments and then at harvest. Only one fruit per plant was allowed;
therefore, the exceeding fruits were removed during the early days of development, in
order to not affect the development and setting of the first fruit (Walters, 2005WALTERS, S.A. Honey bee pollination requirements for triploid
watermelon. HortScience, v.40, p.1268-1270, 2005.; Campagnol et al., 2012CAMPAGNOL, R.; MELLO, S. da C.; BARBOSA, J.C. Vertical growth of mini
watermelon according to the training height and plant density. Horticultura
Brasileira, v.30, p.726-732, 2012. DOI:
10.1590/S0102-05362012000400027.
https://doi.org/10.1590/S0102-0536201200...
).
All fruits produced as a result of each pollination treatment were harvested 30-35 days
after pollination and taken to the Laboratory of Plant Breeding and Genetic Resources,
of Embrapa Agroindústria Tropical, for analysis of quality traits. The number of fruits
analyzed varied according to the fruit set rate of each pollination treatment for each
variety. The evaluated variables included: fruit weight (g), length (cm), width (cm),
deformation score, rind thickness (cm), flesh firmness (N), soluble solids content
(°Brix), and number of seeds per fruit (Lima Neto et
al., 2010LIMA NETO, I. da S.; GUIMARÃES, I.P.; BATISTA, P.F.; AROUCHA, É.M.M.;
QUEIRÓZ, M.A. de. Qualidade de frutos de diferentes variedades de melancia
provenientes de Mossoró-RN. Revista Caatinga, v.23, p.14-20, 2010.; Delaplane et al., 2013DELAPLANE, K.S.; DAG, A.; DANKA, R.G.; FREITAS, B.M.; GARIBALDI, L.A.;
GOODWIN, R.M.; HORMAZA, J.I. Standard methods for pollination research with Apis
mellifera. Journal of Apicultural Research, v.52, p.1-28, 2013. DOI:
10.3896/IBRA.1.52.4.04.
https://doi.org/10.3896/IBRA.1.52.4.04...
). In
particular, for deformation parameters (qualitative variable), fruits were scored from 1
to 4, with score 1 for perfect fruit, score 2 for slightly deformed fruits, score 3 for
fruits with moderate deformation, and score 4 for fruits with severe deformation (Delaplane et al., 2013DELAPLANE, K.S.; DAG, A.; DANKA, R.G.; FREITAS, B.M.; GARIBALDI, L.A.;
GOODWIN, R.M.; HORMAZA, J.I. Standard methods for pollination research with Apis
mellifera. Journal of Apicultural Research, v.52, p.1-28, 2013. DOI:
10.3896/IBRA.1.52.4.04.
https://doi.org/10.3896/IBRA.1.52.4.04...
).
Due to the binomial character (in which 1 is developed; and 0 is not developed) of fruit setting, data for this parameter were subjected directly to the nonparametric Kruskal-Wallis test, at 5% probability. The R statistical software, version 2.9.1 (R Development Core Team, 2012R DEVELOPMENT CORE TEAM. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing, 2012.) was used to perform this analysis. All data of variables related to fruit quality parameters were subjected to normality tests. Those variables with normal distribution were subjected to analysis of variance using the SAS software, version 9.1 (SAS Institute, 2003SAS INSTITUTE. SAS/STAT user's guide. Version 9.1. Cary: SAS Institute, 2003.), through the procedure of generalized linear models (PROC GLM), and means were compared by the Tukey test, at 5% probability. However, when there was no normal distribution, even after data transformation, nonparametric statistical analysis and mean comparisons were performed. Therefore, data regarding flesh firmness were analyzed using the SAS software, version 9.1 (SAS Institute, 2003SAS INSTITUTE. SAS/STAT user's guide. Version 9.1. Cary: SAS Institute, 2003.), through the routine PROC NPAR1WAY, and the obtained results were compared, depending on the number of treatments compared within each variety, by the Wilcoxon (two treatments compared) or the Kruskal-Wallis (three treatments compared) tests, at 5% probability.
Results and Discussion
The five evaluated varieties presented monoecy as a sexual expression. Therefore, both
types of flowers were located within the same plant, but separated into distinct flowers
(diclinous): staminate (male) and pistillate (female). In all studied varieties, the
corolla was slightly tubular, shallow, with five petals fused only at their bases, and a
slightly greenish-yellow color that faded throughout the day, probably due to sun
exposure. The observed characteristics corroborate the studies of Delaplane & Mayer (2000)DELAPLANE, K.S.; MAYER, D.F. Crop pollination by bees. Cambridge: CABI,
2000. 344p. DOI: 10.1079/9780851994482.0000.
https://doi.org/10.1079/9780851994482.00...
and Guerra Sanz (2008)GUERRA SANZ, J.M. Crop pollination in greenhouses. In: JAMES, R.R.;
PITTS-SINGER, T.L. (Ed.). Bee pollination in agricultural ecosystems. New York:
Oxford University, 2008. p.27-47. DOI:
10.1093/acprof:oso/9780195316957.003.0003..
For all five varieties, the staminate flowers had three stamens separated from each other and inserted into the center of the flower, surrounding a shallow floral nectary located at the inner base of the corolla. Each stamen was formed by a filament that held an anther with longitudinal dehiscence. When flowers opened, anther dehiscence and the consequent exposure of pollen grains had already occurred, but pollen grains remained firmly adhered to each other and to the anthers, forming a pollen mass. However, during anthesis, as temperature increased and humidity decreased, the pollen grains became loose, although still forming a pollen mass adhered to the anther. From this moment on, pollen grains could fall onto the petals of the same flower by any movement suffered by the flower or the plant. Staminate flowers of triploid varieties (HA-5106, HA-5158, and HA-5161) visually presented less pollen than the diploid ones (Figure 1 A and B); however, some presented anthers with a dehydrated appearance, brown in color, and visually with little or no pollen grains, even at the beginning of anthesis (Figure 1 C). Conversely, Stanghellini et al. (2002)STANGHELLINI, M.S.; SCHULTHEIS, J.R.; AMBROSE, J.T.Pollen mobilization in selected cucurbitaceae and the putative effects on pollinator abundance on pollen depletion rates. Journal of the American Society for Horticultural Science, v.127, p.729-736, 2002. found no differences in the amount of pollen between diploid and triploid genotypes.
Pollen grains on anthers: A, staminate flower (2n) of the Minipol variety with typical amount of pollen; B, HA-5161 staminate flower (3n) with typical amount of pollen; C, HA-5161 staminate flower (3n) with anthers with a dehydrated appearance.
The pistillate flower was easily distinguished from the staminate flower, because the former had a prominent ovary at its base that resembled the ripened fruit, though still much reduced in size. Its ovary was also attached to a thick and very short style, whose base was surrounded by a shallow nectary and whose top presented an adhesive stigma divided into three or, less frequently, four large lobes. The surface of these lobes remained moist, sticky, and shiny during the time the pistillate flower remained open. According to Njoroge et al. (2010)NJOROGE, G.N.; GEMMILL, B.; BUSSMANN, R.; NEWTON, L.E.; NGUMI, V.M. Diversity and efficiency of wild pollinators of watermelon (Citrullus lanatus (Thunb.) Mansf.) at Yatta (Kenya). Journal of Applied Horticulture, v.12, p.35-41, 2010., a stigma with glossy secretion may be considered receptive, that is, ready for pollination. This information is important to define when these varieties can be pollinated, either in watermelon breeding programs or in commercial production in greenhouses. This result is also an indicative that, based on stigma receptivity, these varieties can benefit from pollinator visits along the entire time the flowers remain open. It is important to highlight that, in systems in which pollinators are present, pollen grains, unlike nectar, are quickly reduced during the first hours after anthesis due to pollinator activity and are no longer replenished (Araújo et al., 2014BELFORT, C.C.; NERY, E.B.; SILVA FILHO, J.A. de S.; SETÚBAL, J.W.; THÉ, F. de W.; PARENTE, M.B. Influência da polinização artificial na dinâmica floral de melancia triplóide em condições de cultivo protegido. Horticultura Brasileira, v.21, p.349-422, 2003. Suplemento 2.).
Regarding the flower opening and closing time, the five varieties showed the same period
of anthesis. In general, flowers of both sexes began corolla expansion in the first few
hours of sunshine, approximately at 5:20 a.m. (at 24.2°C, 97.1% humidity, and 0.430
klux), and remained open throughout the morning until they finally closed in the early
afternoon, around 2:20 p.m. (at 33.2°C, 65.6% humidity, and 36.9 klux), with a total
anthesis period of 9 hours. These results are similar to those reported by Stanghellini et al. (2002)STANGHELLINI, M.S.; SCHULTHEIS, J.R.; AMBROSE, J.T.Pollen mobilization
in selected cucurbitaceae and the putative effects on pollinator abundance on pollen
depletion rates. Journal of the American Society for Horticultural Science, v.127,
p.729-736, 2002. and Azo'o Ela et al. (2010)AZO'O ELA, M.; MESSI, J.; TCHUENGUEM FOHOUO, F.N.; TAMESSE, J.L.;
KEKEUNOU, S.; PANDO, J.B. Foraging behaviour of Apis mellifera adansonii and its
impact on pollination, fruit and seed yields of Citrullus lanatus at Nkolbisson
(Yaoundé, Cameroon). Cameroon Journal of Experimental Biology, v.6, p.41-48, 2010.
DOI: 10.4314/cajeb.v6i1.56879.
https://doi.org/10.4314/cajeb.v6i1.56879...
. Regarding the movement of petals, corolla
expansion and retraction for both pistillate (Figure 2 A
to K) and staminate flowers (Figure 3 A to
K) behaved as follows: soon after opening, the corolla exhibited a cup-shape
structure and continued its expansion, transitioning to the plate format, and, finally,
fully expanding to an inverted umbrella. After this period, which lasted about 4 hours,
the corolla started to retract, returning through all stages until finally closing and
not opening again, even if not pollinated. This petal movement throughout the day was
also observed by Emuh & Ojeifo (2011)EMUH, F.N.; OJEIFO, I.M. The phenology of flowering in Citrullus lanatus
(Thumb.) Mansf. in southwestern Nigeria. International Journal of Biological and
Chemical Sciences, v.5, p.2031-2034, 2011..
Corolla movements during the anthesis of pistillate flowers (♀) in mini watermelon (Citrullus lanatus) varieties under protected cultivation: A, floral bud in pre-anthesis; B, beginning of anthesis at 5:25 a.m.; C, flower at 6:00 a.m.; D, flower at 7:00 a.m.; E, flower at 8:00 a.m.; F, flower at 9:00 a.m.; G, flower at 10:00 a.m.; H, flower at 11:00 a.m.; I, flower at 1:00 p.m.; J, flower at 2:00 p.m.; K, flower one day after anthesis.
Corolla movements during the anthesis of staminate flowers (♂) in mini watermelon (Citrullus lanatus) varieties under protected cultivation: A, floral bud in pre-anthesis; B, beginning of anthesis at 5:20 a.m.; C, flower at 6:00 a.m.; D, flower at 7:00 a.m.; E, flower at 8:00 a.m.; F, flower at 9:00 a.m.; G, flower at 10:00 a.m.; H, flower at 11:00 a.m.; I, flower at 1:00 p.m.; J, flower at 2:00 p.m.; K, flower one day after anthesis.
The evaluated set of characteristics, including type of sexual expression, corolla shape and color, anthesis, and the presence of nectar and pollen, reveals that the flowers of all five varieties still have traits that are important in attracting bees to promote pollination. This indicates that bees are a suitable pollinator to be introduced in areas cultivated with these varieties.
Pistillate flowers of both diploid varieties (Minipol and Polimore), when subjected to
the treatment of restricted pollination with tulle bag, differed significantly from the
other treatments, setting no fruits (Table 1).
These results are not surprising, since the watermelon plant, independently of being
diploid or triploid, is not capable to produce fruit through asexual reproduction (Walters, 2005WALTERS, S.A. Honey bee pollination requirements for triploid
watermelon. HortScience, v.40, p.1268-1270, 2005.; Taha
& Bayoumi, 2009TAHA, E.A.; BAYOUMI, Y.A. The value of honey bees (Apis mellifera, L.)
as pollinators of summer seed watermelon (Citrullus lanatus colothynthoides L.) in
Egypt. Acta Biologica Szegediensis, v.53, p.33-37, 2009.), unlike other cucurbits, as some cucumber
(Cucumis sativus L.) varieties (Nicodemo et al., 2013NICODEMO, D.; MALHEIROS, E.B.; DE JONG, D.; NOGUEIRA COUTO, R.H.
Enhanced production of parthenocarpic cucumbers pollinated with stingless bees and
Africanized honey bees in greenhouses. Semina: Ciências Agrárias, v.34, p.3625-3634,
2013. DOI: 10.5433/1679-0359.2013v34n6Supl1p3625.
https://doi.org/10.5433/1679-0359.2013v3...
), except when chemicals, such as growth regulators, are
applied to the flower ovaries (Huitrón et al.,
2007HUITRÓN, M.V.; DIAZ, M.; DIÁNEZ, F.; CAMACHO, F. Effect of 2,4-D and
CPPU on triploid watermelon production and quality. HortScience, v.42, p.559-564,
2007.). For the Polimore variety, the other pollination treatments did not
differ significantly from each other with respect to the percentage of fruit set (Table 1). Therefore, the Polimore variety accepted
well pollen grains from the same plant, from another individual of the same variety, and
from the Minipol variety. According to Souza
(2003)SOUZA, F. de F. Técnicas de propagação para plantas de melancia:
ferramentas úteis no melhoramento genético da cultura. Porto Velho: Embrapa Rondônia,
2003. 54p. (Embrapa Rondônia. Documentos, 80)., although the conventional watermelon (2n) is a xenogamous species
(cross-pollination), it is also a self-compatible plant. In other words, it accepts
autogamy (pollination within the same flower) in the case of andromonoecious varieties,
and geitonogamy (pollination between different flowers of the same plant). Therefore,
this variety presents a mixed pollination breeding system.
For the Minipol variety, although MG differed significantly from MCM (p≤0.05), it did
not differ from the MCP treatment, which in turn was similar to MCM (Table 1). In the present study, the percentage of
fruit set of the seeded varieties subjected to the three hand pollination treatments
(MG, MCP, and MCM) was much higher than that observed by Adlerz (1966)ADLERZ, W.C. Honey bee visit numbers and watermelon pollination. Journal
of Economic Entomology, v.59, p.28-30, 1966. DOI:
10.1093/jee/59.1.28.
https://doi.org/10.1093/jee/59.1.28...
for fruit sets obtained by hand pollination in open fields,
which varied from 33.3 to 40.6% between consecutive years for the diploid variety. Ferreira (2005)FERREIRA, M.A.J. da F. Técnicas de produção de sementes de melancia, via
polinizações manuais controladas, em campo e casa-de-vegetação. Brasília: Embrapa
Recursos Genéticos e Biotecnologia, 2005. 7p. (Embrapa Recursos Genéticos e
Biotecnologia. Circular técnica, 40). states that, in general, rates of
fruit setting in open field are much lower when compared to pollinations performed in
greenhouses, where it is possible to control better the weather conditions and the
number of fruits per plant. This is explained by the pre-existence of a developing fruit
in the plant, which interferes in the setting of another fruit for at least seven days
(Walters, 2005WALTERS, S.A. Honey bee pollination requirements for triploid
watermelon. HortScience, v.40, p.1268-1270, 2005.). The fact that seeded mini
watermelon varieties set well under MG may indicate that these varieties may be
naturally benefited by bee visits, which tend to explore various flowers on the same
plant before moving to the next one (Walters &
Schultheis, 2009WALTERS, S.A.; SCHULTHEIS, J.R.Directionality of pollinator movements in
watermelon plantings. HortScience, v.44, p.49-52, 2009.; Delaplane et al.,
2013DELAPLANE, K.S.; DAG, A.; DANKA, R.G.; FREITAS, B.M.; GARIBALDI, L.A.;
GOODWIN, R.M.; HORMAZA, J.I. Standard methods for pollination research with Apis
mellifera. Journal of Apicultural Research, v.52, p.1-28, 2013. DOI:
10.3896/IBRA.1.52.4.04.
https://doi.org/10.3896/IBRA.1.52.4.04...
).
Despite geitonogamous pollination having been successful for seeded varieties (2n), it was not suitable for seedless ones (3n): HA-5158, HA-5161, and HA-5106 (Table 2). The pistillate flowers of triploid varieties subjected to the MG treatment showed 0% of fruit set, identical to the results obtained in the treatment of restricted pollination, and both differed from the other treatments, MCP and MCM. Among the three varieties of seedless mini watermelon (3n), the one with worst fruit set for all treatments was HA-5161, which set fruits in only 60 and 58.82% of the flowers pollinated with pollen from the Minipol (MCM) and Polimore (MCP) varieties, respectively; these did not differ from each other.
The other triploid varieties showed high rates of fruit set, and no differences were found among MCM and MCP pollination treatments within each of these varieties. These results agree with the findings of Belfort et al. (2003)BELFORT, C.C.; NERY, E.B.; SILVA FILHO, J.A. de S.; SETÚBAL, J.W.; THÉ, F. de W.; PARENTE, M.B. Influência da polinização artificial na dinâmica floral de melancia triplóide em condições de cultivo protegido. Horticultura Brasileira, v.21, p.349-422, 2003. Suplemento 2., who, in protected cultivation, obtained an overall rate of fruit set in seedless watermelon (3n) exceeding 75% when flowers were pollinated with pollen from diploid genotypes. The results of the present study are similar to those of Walters (2005)WALTERS, S.A. Honey bee pollination requirements for triploid watermelon. HortScience, v.40, p.1268-1270, 2005., except for HA-5161, who also observed a fruit set rate of 80% while working with a triploid variety in open field subjected to open pollination (about 24 visits of Apis mellifera). The high fruit set rate reported by this author was attributed to the removal of early or subsequent fruits on the same vine. In the present work, for all triploid varieties studied, only manual cross-pollination treatments using pollen derived from diploid varieties were capable to produce fruits (Table 2). This can be explained by the fact that only the diploid varieties have viable pollen grains able to germinate on the stigma of triploid female flowers and, consequently, able to promote the release of plant hormones, which directly influence fruit setting and growth (Walters, 2005WALTERS, S.A. Honey bee pollination requirements for triploid watermelon. HortScience, v.40, p.1268-1270, 2005.; Guerra Sanz, 2008GUERRA SANZ, J.M. Crop pollination in greenhouses. In: JAMES, R.R.; PITTS-SINGER, T.L. (Ed.). Bee pollination in agricultural ecosystems. New York: Oxford University, 2008. p.27-47. DOI: 10.1093/acprof:oso/9780195316957.003.0003.).
Due to the absence of fruit set when flowers were subjected to the restricted pollination treatment, in both types of mini watermelons (2n and 3n), and to the MG treatment for seedless varieties (3n), fruit quality characters were compared only among the other pollination treatments. There were no significant differences (p>0.05) between pollination treatments for any of the variables investigated. Therefore, regarding weight, length, width, deformation, rind thickness, flesh firmness, soluble solids content, and number of seeds per fruit, all treatments showed similar results for each of these variables analyzed within each variety (Table 3).
These results indicate that once the fruit has set, regardless of the type of
pollination treatment performed on the flower, it is able to develop well and present
similar qualitative traits to those of the fruits produced by treatments that resulted
in a higher percentage of fruit setting. According to Serrano & Guerra Sanz (2006)SERRANO, A.R.; GUERRA SANZ, J.M.Quality fruit improvement in sweet
pepper culture by bumblebee pollination. Scientia Horticulturae, n.110, p.160-166,
2006. DOI: 10.1016/j.scienta.2006.06.024.
https://doi.org/10.1016/j.scienta.2006.0...
, the number of pollen grains deposited on
the stigma of a flower is the variable that can affect fruit quality. In the present
work, because all pollination treatments tested were carried out by hand pollination,
depositing a large amount of pollen grains on the stigmas, there was no pollen
limitation. Therefore, it is reasonable to believe that this is the reason for the
uniformity in the quality traits observed in the fruits among treatments. Under
conditions of natural pollination, however, care should be taken to ensure that
pollinators deposit at least the minimum amount of pollen needed in order for the fruits
to develop well and fully express desirable traits (Delaplane et al., 2013DELAPLANE, K.S.; DAG, A.; DANKA, R.G.; FREITAS, B.M.; GARIBALDI, L.A.;
GOODWIN, R.M.; HORMAZA, J.I. Standard methods for pollination research with Apis
mellifera. Journal of Apicultural Research, v.52, p.1-28, 2013. DOI:
10.3896/IBRA.1.52.4.04.
https://doi.org/10.3896/IBRA.1.52.4.04...
). Indeed, Guerra Sanz
& Serrano (2008)GUERRA SANZ, J.M.; SERRANO, A.R. Influence of honey bees brood pheromone
on the production of triploid melon. In: EUCARPIA MEETING ON GENETICS AND BREEDING OF
CUCURBITACEAE, 9., 2008, Avignon. Proceedings. Avignon: Institut National de la
Recherche Agronomique, 2008. p.385-390. found that the increase in flower visitation by bees
resulted in a higher number of fruits per plant, besides heavier and sweeter fruits for
triploid varieties, and heavier and sweeter fruits, with more seeds, for diploid
varieties.
Conclusions
-
All seeded and seedless mini watermelon (Citrullus lanatus) varieties have monoecious plants and diclinous flowers with similar pattern of anthesis, preserve traits for attracting bees, and cannot autopollinate.
-
For fruit set, all mini watermelon varieties need a pollination agent and diploid pollen, regardless of the donor variety, which does not interfere in the quality of the produced fruit.
-
The Minipol or Polimore varieties with HA-5106 or HA-5158 are recommended for cultivation in greenhouses.
Acknowledgements
To Hazera Genetics, for providing the seeds of the tested varieties; to Top Plant, for cultivating the seedlings; and to Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico (Funcap) and to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), for a PhD scholarship to Isac Gabriel Abrahão Bomfim, an undergrad scholarship to Antonio Diego de Melo Bezerra, and a research fellowship to Breno Magalhães Freitas (Process no. 302934/2010-3).
- ADLERZ, W.C. Honey bee visit numbers and watermelon pollination. Journal of Economic Entomology, v.59, p.28-30, 1966. DOI: 10.1093/jee/59.1.28.
» https://doi.org/10.1093/jee/59.1.28 - ANDRADE, P.B.; FREITAS, B.M.; ROCHA, E.E.M.; LIMA, J.A.; RUFINO, L.L. Floral biology and pollination requirements of sesame (Sesamum indicum L.). Acta Scientiarum. Animal Sciences, v.36, p.93-99, 2014. DOI: 10.4025/actascianimsci.v36i1.21838.
» https://doi.org/10.4025/actascianimsci.v36i1.21838 - ARAÚJO, D.; SIQUEIRA, K.; DUARTE, P.; SILVA, N. Comportamento de forrageamento de Apis mellifera na melancieira (Citrullus lanatus) no município de Juazeiro, BA. Revista Verde de Agroecologia e Desenvolvimento Sustentável, v.9, p.59-67, 2014.
- AZO'O ELA, M.; MESSI, J.; TCHUENGUEM FOHOUO, F.N.; TAMESSE, J.L.; KEKEUNOU, S.; PANDO, J.B. Foraging behaviour of Apis mellifera adansonii and its impact on pollination, fruit and seed yields of Citrullus lanatus at Nkolbisson (Yaoundé, Cameroon). Cameroon Journal of Experimental Biology, v.6, p.41-48, 2010. DOI: 10.4314/cajeb.v6i1.56879.
» https://doi.org/10.4314/cajeb.v6i1.56879 - BELFORT, C.C.; NERY, E.B.; SILVA FILHO, J.A. de S.; SETÚBAL, J.W.; THÉ, F. de W.; PARENTE, M.B. Influência da polinização artificial na dinâmica floral de melancia triplóide em condições de cultivo protegido. Horticultura Brasileira, v.21, p.349-422, 2003. Suplemento 2.
- BOMFIM, I.G.A.; CRUZ, D. de O.; FREITAS, B.M.; ARAGÃO, F.A.S. de. Polinização em melancia com e sem semente. Fortaleza: Embrapa Agroindústria Tropical, 2013. 54p. (Embrapa Agroindústria Tropical. Documentos, 168).
- CAMPAGNOL, R.; MELLO, S. da C.; BARBOSA, J.C. Vertical growth of mini watermelon according to the training height and plant density. Horticultura Brasileira, v.30, p.726-732, 2012. DOI: 10.1590/S0102-05362012000400027.
» https://doi.org/10.1590/S0102-05362012000400027 - CRUZ, D. de O.; CAMPOS, L.A. de O. Polinização por abelhas em cultivos protegidos. Revista Brasileira de Agrociência, v.15, p.5-10, 2009.
- DELAPLANE, K.S.; DAG, A.; DANKA, R.G.; FREITAS, B.M.; GARIBALDI, L.A.; GOODWIN, R.M.; HORMAZA, J.I. Standard methods for pollination research with Apis mellifera. Journal of Apicultural Research, v.52, p.1-28, 2013. DOI: 10.3896/IBRA.1.52.4.04.
» https://doi.org/10.3896/IBRA.1.52.4.04 - DELAPLANE, K.S.; MAYER, D.F. Crop pollination by bees. Cambridge: CABI, 2000. 344p. DOI: 10.1079/9780851994482.0000.
» https://doi.org/10.1079/9780851994482.0000 - DITTMAR, P.J.; MONKS, D.W.; SCHULTHEIS, J.R. Maximum potential vegetative and floral production and fruit characteristics of watermelon pollenizers. HortSience, v.44, p.59-63, 2009.
- EMUH, F.N.; OJEIFO, I.M. The phenology of flowering in Citrullus lanatus (Thumb.) Mansf. in southwestern Nigeria. International Journal of Biological and Chemical Sciences, v.5, p.2031-2034, 2011.
- FERREIRA, M.A.J. da F. Técnicas de produção de sementes de melancia, via polinizações manuais controladas, em campo e casa-de-vegetação. Brasília: Embrapa Recursos Genéticos e Biotecnologia, 2005. 7p. (Embrapa Recursos Genéticos e Biotecnologia. Circular técnica, 40).
- GUERRA SANZ, J.M. Crop pollination in greenhouses. In: JAMES, R.R.; PITTS-SINGER, T.L. (Ed.). Bee pollination in agricultural ecosystems. New York: Oxford University, 2008. p.27-47. DOI: 10.1093/acprof:oso/9780195316957.003.0003.
- GUERRA SANZ, J.M.; SERRANO, A.R. Influence of honey bees brood pheromone on the production of triploid melon. In: EUCARPIA MEETING ON GENETICS AND BREEDING OF CUCURBITACEAE, 9., 2008, Avignon. Proceedings. Avignon: Institut National de la Recherche Agronomique, 2008. p.385-390.
- HUITRÓN, M.V.; DIAZ, M.; DIÁNEZ, F.; CAMACHO, F. Effect of 2,4-D and CPPU on triploid watermelon production and quality. HortScience, v.42, p.559-564, 2007.
- KLATT, B.K.; BURMEISTER, C.; WESTPHAL, C.; TSCHARNTKE, T.; FRAGSTEIN, M. von. Flower volatiles, crop varieties and bee responses. Plos One, v.8, 2013. DOI: 10.1371/journal.pone.0072724.
» https://doi.org/10.1371/journal.pone.0072724 - KWON, S.W.; JASKANI, M.J.; KO, B.R.; CHO, J.L. Collection, germination and storage of watermelon (Citrullus lanatus Thunb.) pollen for pollination under temperature conditions. Asian Journal of Plant Science, v.4, p.44-49, 2005. DOI: 10.3923/ajps.2005.44.49.
» https://doi.org/10.3923/ajps.2005.44.49 - LIMA NETO, I. da S.; GUIMARÃES, I.P.; BATISTA, P.F.; AROUCHA, É.M.M.; QUEIRÓZ, M.A. de. Qualidade de frutos de diferentes variedades de melancia provenientes de Mossoró-RN. Revista Caatinga, v.23, p.14-20, 2010.
- NICODEMO, D.; MALHEIROS, E.B.; DE JONG, D.; NOGUEIRA COUTO, R.H. Enhanced production of parthenocarpic cucumbers pollinated with stingless bees and Africanized honey bees in greenhouses. Semina: Ciências Agrárias, v.34, p.3625-3634, 2013. DOI: 10.5433/1679-0359.2013v34n6Supl1p3625.
» https://doi.org/10.5433/1679-0359.2013v34n6Supl1p3625 - NJOROGE, G.N.; GEMMILL, B.; BUSSMANN, R.; NEWTON, L.E.; NGUMI, V.M. Diversity and efficiency of wild pollinators of watermelon (Citrullus lanatus (Thunb.) Mansf.) at Yatta (Kenya). Journal of Applied Horticulture, v.12, p.35-41, 2010.
- R DEVELOPMENT CORE TEAM. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing, 2012.
- SAS INSTITUTE. SAS/STAT user's guide. Version 9.1. Cary: SAS Institute, 2003.
- SEABRA JÚNIOR, S.; PANTANO, S.C.; HIDALGO, A.F.; RANGEL, M.G.; CARDOSO, A.I.I. Avaliação do número e posição de frutos de melancia produzidos em ambiente protegido. Horticultura Brasileira v.21, p.708-711, 2003. DOI: 10.1590/S0102-05362003000400028.
» https://doi.org/10.1590/S0102-05362003000400028 - SERRANO, A.R.; GUERRA SANZ, J.M.Quality fruit improvement in sweet pepper culture by bumblebee pollination. Scientia Horticulturae, n.110, p.160-166, 2006. DOI: 10.1016/j.scienta.2006.06.024.
» https://doi.org/10.1016/j.scienta.2006.06.024 - SLAA, E.J.; SÁNCHEZ CHAVES, L.A.; MALAGODI-BRAGA, K.S.; HOFSTEDE, F.E. Stingless bees in applied pollination: practice and perspectives. Apidologie, v.37, p.293-315, 2006. DOI: 10.1051/apido:2006022.
» https://doi.org/10.1051/apido:2006022 - SOUZA, F. de F. Técnicas de propagação para plantas de melancia: ferramentas úteis no melhoramento genético da cultura. Porto Velho: Embrapa Rondônia, 2003. 54p. (Embrapa Rondônia. Documentos, 80).
- STANGHELLINI, M.S.; AMBROSE, J.T.; SCHULTHEIS, J.R.The effects of honey bee and bumble bee pollination on fruit set and abortion of cucumber and watermelon. American Bee Journal, v.137, p.386-391, 1997.
- STANGHELLINI, M.S.;; AMBROSE, J.T. SCHULTHEIS, J.R.Using commercial bumble bee colonies as backup pollinators for honey bees to produce cucumbers and watermelons. HortTechnology, v.8, p.590-594, 1998.
- STANGHELLINI, M.S.; SCHULTHEIS, J.R.; AMBROSE, J.T.Pollen mobilization in selected cucurbitaceae and the putative effects on pollinator abundance on pollen depletion rates. Journal of the American Society for Horticultural Science, v.127, p.729-736, 2002.
- TAHA, E.A.; BAYOUMI, Y.A. The value of honey bees (Apis mellifera, L.) as pollinators of summer seed watermelon (Citrullus lanatus colothynthoides L.) in Egypt. Acta Biologica Szegediensis, v.53, p.33-37, 2009.
- WALTERS, S.A. Honey bee pollination requirements for triploid watermelon. HortScience, v.40, p.1268-1270, 2005.
- WALTERS, S.A. Influence of plant density and cultivar on mini triploid watermelon yield and fruit quality. HortTechnology, v.19, n.3, p.553-557, 2009.
- WALTERS, S.A.; SCHULTHEIS, J.R.Directionality of pollinator movements in watermelon plantings. HortScience, v.44, p.49-52, 2009.
Publication Dates
-
Publication in this collection
Jan 2015
History
-
Received
18 Apr 2014 -
Accepted
03 Dec 2014