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Is manual pollination of yellow passion fruit completely dispensable?
Scientia Horticulturae 146 (2012) 99–103
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Scientia Horticulturae journal homepage: www.elsevier.com/locate/scihorti
Is manual pollination of yellow passion fruit completely dispensable? Murilo V. Silveira a , Alfredo R. Abot b , José N. Nascimento c , Edson T. Rodrigues b , Sérgio R. Rodrigues b , Anderson Puker d,∗ a
Programa de Pós-Graduac¸ão em Agronomia, Universidade Estadual de Mato Grosso do Sul, Aquidauana, MS, Brazil Universidade Estadual de Mato Grosso do Sul, Aquidauana, MS, Brazil Universidade Federal da Grande Dourados, Dourados, MS, Brazil d Programa de Pós-Graduac¸ão em Entomologia, Departamento de Entomologia, Universidade Federal de Vic¸osa, Vic¸osa, MG, Brazil b c
a r t i c l e
i n f o
Article history: Received 26 May 2012 Received in revised form 16 August 2012 Accepted 18 August 2012 Keywords: Carpenter bees Cross-pollination Mass flowering plant Self-incompatible plant Tropical fruit Wild pollinators
a b s t r a c t High dependence on pollination is considered the main cause of low productivity in American yellow passion fruit crops (Passiflora edulis f. flavicarpa). As intensive farming practices require similarly intensive manual pollination, this study sought answer the following questions: (a) is there a difference in the efficiency of fruit production when one or more stigmas are pollinated manually, by natural pollinators (or both)? and (b) does manual or natural pollination (or both) affect the physical and chemical characteristics of the fruits? Flowers were pollinated manually, naturally by native bees or by using both methods. Fruit production was evaluated seven days after anthesis, as well as some selected physico-chemical characteristics of harvested fruits. It was demonstrated that the pollination of yellow passion fruit is satisfactory only with visitation by native bees, especially carpenter bees. There is no difference in fruit production efficiency when one or more stigmas are pollinated manually and then left free for visits by natural pollinators. Manual pollination in one stigma produced less seeds and lower biomass of fruit juice of yellow passion fruits. When there is the presence of natural pollinators (notably carpenter bees), manual services can be reduced but not completely dismissed. Therefore, yellow passion fruit farmers can potentially reduce production costs. © 2012 Elsevier B.V. All rights reserved.
1. Introduction The value of services provided by native pollinators has recently been the focus of much attention (e.g., Allsopp et al., 2008), particularly on foods consumed worldwide and those that require of cross-pollination (Allen-Wardell et al., 1998; Klein et al., 2007; Aizen et al., 2008; Winfree, 2008). For example, a greater abundance and diversity of native bees significantly improved fruit production in coffee (Klein et al., 2003) and rapeseed plantations (Morandin and Winston, 2005). Pollinators, however, are ostensibly subject to anthropogenic landscape changes and the risk of pesticide application (e.g., Watanabe, 1994; Stokstad, 2006; Oldroyd, 2007). Two components of pollination must be evaluated in order to directly compare the effectiveness of pollination: pollen transfer efficiency and frequency of visits (Rader et al., 2009). Pollen transfer efficiency describes the ability of individual pollinators to remove and transport the pollen to the stigmas of conspecifics (Primack and
∗ Corresponding author at: Programa de Pós-Graduac¸ão em Entomologia, Departamento de Entomologia, Universidade Federal de Vic¸osa, 36570-000 Vic¸osa, MG, Brazil. Tel.: +55 31 3899 3785. E-mail address: [email protected] (A. Puker). 0304-4238/$ – see front matter © 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.scienta.2012.08.023
Silander, 1975; Herrera, 1987). Frequency of visitation is the ratio between the abundance of pollinators and the number of flowers visited in a given time interval (Herrera, 1987, 1989; Vazquez et al., 2005). The most effective pollinator is therefore one that is present in large numbers and moves quickly from flower to flower. It would also be frequently in contact with the stigma, and would transfer a high number of pollen grains. On the other hand, the least effective pollinator would show low abundance and move relatively slowly from flower to flower. This type of pollinator would rarely be in contact with the stigma while visiting a flower and transfer few pollen grains (Rader et al., 2009). Passiflora edulis Sims f. flavicarpa Degener (Passifloraceae), known as yellow passion fruit, is a self-incompatible plant that completely depends on cross-pollination for its reproduction (Bruckner et al., 1995). In several countries this function is performed mainly by native bees and especially by the carpenter bees (Sazima and Sazima, 1989; Hoffmann et al., 2000; Camillo, 2003), as the flowers of P. edulis have characteristics adapted to suit pollination by large bees. The distance between the dehiscent side of the anthers and corolla, the shape of the anthers and their versatility (easily moved upon touch) allow a precise coupling in the dorsal region of major pollinators. The stigmas, in turn, resist movement, which facilitates the adhesion of pollen when touched by the dorsal
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region of the bee (Bruckner et al., 1995). In addition, flowers that are large, attractive, have bright colors, strong odors, abundant concentrations of pollen and nectar are characteristics that attract bees (Cobert and Willmer, 1980). Carpenter bees are considered the only effective pollinators of commercial crops of yellow passion fruit due to their morphological and behavioral characteristics (e.g., Keasar, 2010). Because the number of native bees has reduced in commercial crops, manual pollination has been adapted to ensure satisfactory productivity (Calle et al., 2010). The low rates of pollination by native bees are probably related to: the absence and/or reduction of vegetation cover close to cultivated areas (a lack of suitable sites for nesting) and the use of pesticides, which is relatively common in commercial crops. These are probably some of the factors that have justified the use of manual pollination. On the other hand, numerous techniques have been developed and are considered effective for maintaining high populations of native bees in agricultural areas, including artificial nests (e.g., Freitas and Oliveira Filho, 2003; Oliveira Filho and Freitas, 2003), alternative sources of food (Pontin et al., 2006), and the diversification and habitat conservation of areas in the vicinity of the crop (e.g., Freitas et al., 2009). Being a mass flowering plant, the yellow passion fruit and other plants (e.g., Westphal et al., 2003), require pollination when the flower is receptive to receive pollen, usually during hours of high temperature during the day (Cobert and Willmer, 1980; Siqueira et al., 2009); and indeed larger populations of native bees are observed visiting the plant during this period (Benevides et al., 2009; Siqueira et al., 2009). Therefore, the pollination efficiency of this species justifies its conservation in agricultural landscapes (Benevides et al., 2009). Worldwide, surprisingly few studies have directly compared the effectiveness of hand pollination performed by man with the alternative of exclusively using the services of native bees in intensively farmed regions (Siqueira et al., 2009). Even though the main cause of the fall of the flowers from the yellow passion fruit plant and consequently reduced production is the lack of pollination. Therefore, artificial pollination has often been the only alternative in yellow passion fruit plantations, especially in areas with low pollinator population densities. Fear often causes many farmers to use hand pollination, but they recognize the crucial role of native bees, especially the carpenter bees (Calle et al., 2010). As intensive farming practices require similarly intensive manual pollination, this study sought to answer the following questions: (a) is there a difference in the efficiency of fruit production when one or more stigmas are pollinated manually, by natural pollinators (or both)? and (b) does manual or natural pollination (or both) affect the physical and chemical characteristics of the fruits of yellow passion fruit?
2. Materials and methods 2.1. Location of study, crop and management of the plants The study was conducted at the Universidade Estadual de Mato Grosso do Sul (UEMS), located in Aquidauana, Mato Grosso do Sul, Brazil (20◦ 28 S, 55◦ 48 W). The climate is Tropical Hot–Humid (Aw) according to Köppen classification (Peel et al., 2007), with average annual temperature of 26 ◦ C and annual rainfall from 1200 mm to 1300 mm. The soil is classified as Fluvic Cambisol. Cultivation was initiated in April 2008, with spacing of 3 m between rows and 5 m between plants (density of 667 plants ha−1 ) in a vertical cordon system. Fertilization was performed according to the recommendations of Rodrigues (2008), based on soil analysis. Plants were pruned at biweekly intervals to correct plant architecture.
2.2. Experiments Each treatment of pollination was composed of 60 flowers distributed in 24 plants, with a maximum of three flowers per plant per treatment. Fruit production was recorded seven days after anthesis according to the method proposed by Silva et al. (1997). Treatments of pollination were: (1) spontaneous self-pollination – the marked buds remained covered during the opening of the flower; (2) natural pollination, excluding carpenter bees – buds were marked before anthesis and covered with a screen (6 mm holes diameter) to prevent the entry of carpenter bees, remaining free to visits by other potential pollinators; (3) flowers in pre-anthesis were covered with a screen (mesh 0.5 mm × 0.5 mm), which were removed when the stigmas were capable of being pollinated. At this moment manual pollination was performed, depositing pollen in one stigma and re-covering the flower to prevent the entry of any potential pollinators; (4) idem previous treatment, but to perform the pollination, pollen was deposited in two stigmas, (5) idem treatment 4, but with pollination in three stigmas; (6) natural pollination buds were marked before anthesis and remained free to natural pollination by insects; (7) natural and manual pollination in one stigma – the flower buds were marked, and one hour after anthesis when the stigmas were deflected manually received pollen on one stigma, leaving the flower open for visitation by insects; (8) natural and manual pollination in two stigmas and (9) natural and manual pollination in three stigmas. Manual pollination was always performed between 13:30 and 15:00 (Souza et al., 2004) from April 10 to May 30, 2009, collecting pollen from a recent anther dehiscence and placed on the stigmas of flowers with deflected stigmas, as recommended by Camillo (2003). Ten fruits from each treatment (one fruit per plant) were arbitrarily selected and harvested when they were more than 30% yellow and presented no resistance to abscission (as per the methods of Silva et al., 2008) for analysis of physico-chemical variables. The parameters evaluated were: fresh biomass of the fruit; length; diameter; shell thickness; number of seeds; juice biomass; juice percentage (juice biomass/fruit × 100); total soluble solids (TSS); total titratable acidity (TTA); and finally the ratio between total soluble solids and total titratable acidity (TSS/TTA). TSS were measured directly using a refractometer with results expressed in ◦ Brix. TTA was evaluated by titration of 5 mL of juice diluted in 25 mL of distilled water, using phenolphthalein as an indicator, with a solution of 0.5 N NaOH, until pink color persisted, according to the technique defined by AOAC (1990). 2.3. Data analysis Data referring to the percentage of pollination (n = 60 flowers) were analyzed using Generalized Linear Model (GLM) (Crawley, 2002) with binomial distribution. The results of the time between anthesis and harvest of fruit (n = 10) in the field and of the physicochemical characteristics of fruits (n = 10) also were analyzed using GLM and compared by analysis of the contrast (˛ < 0.05). All GLMs were submitted to residual analysis, so as to evaluate the adequacy of error distribution (Crawley, 2002). These analyzes were conducted with the software program R (R Development Core Team, 2012). 2.4. Sampling, identification and deposit of the voucher specimens Carpenter bees were sampled directly from flowers of the yellow passion fruit plant with an entomological net. The specimens were mounted on entomological pins and identified by Dr. Fernando Cesar Vieira Zanella (Universidade Federal de Campina Grande, UFCG, Patos, Paraíba, Brazil). Voucher specimens were deposited
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Fig. 1. Average number of seeds in the yellow passion fruits in response to different pollination treatments: (1) spontaneous self-pollination; (2) natural pollination, excluding carpenter bees; (3) manual pollination in one stigma; (4) manual pollination in two stigmas; (5) manual pollination in three stigmas; (6) natural pollination; (7) natural pollination + manual pollination in one stigma; (8) natural pollination + manual pollination in two stigmas and (9) natural pollination + manual pollination in three stigmas. Bars on columns represent standard errors. Columns differ significantly when labeled with different letters (p < 0.01).
Fig. 2. Average biomass of fruit juice of yellow passion fruits in response to different pollination treatments: (1) spontaneous self-pollination; (2) natural pollination, excluding carpenter bees; (3) manual pollination in one stigma; (4) manual pollination in two stigmas; (5) manual pollination in three stigmas; (6) natural pollination; (7) natural pollination + manual pollination in one stigma; (8) natural pollination + manual pollination in two stigmas and (9) natural pollination + manual pollination in three stigmas. Bars on columns represent standard errors. Columns differ significantly when labeled with different letters (p < 0.01).
at the Laboratory of Ecology and Biogeography of Insects from the Caatinga (UFCG) and Entomology Laboratory of the UEMS.
whose flowers were exposed to different methods of pollination: the total soluble solids (TSS) (11.83 ◦ Brix; ±0.16) (F6,63 = 0.8839, p > 0.05), total titratable acidity (TTA) (4.73%; ±0.07) (F6,63 = 1.6138, p > 0.05) and the relationship between TSS and TTA (2.53; ±0.05) (F6,63 = 0.7369, p > 0.05) were not affected by the different pollination treatments.
3. Results 3.1. Pollination efficiency and time until harvest There was no fruit production in flowers that did not receive pollen by natural or manual pollinators, confirming the need for cross-pollination by insects or manual methods. In our study, the carpenter bees Xylocopa frontalis (Olivier) and X. grisescens (Lepeletier) (Hymenoptera: Apidae: Xylocopini) were sampled pollinating the yellow passion fruit flowers. For all treatments the pollination rates (average: 34.76%; standard error: ± 2.33) were similar (Chi = 537.44, p > 0.05). The effect of pollination was evaluated on the time between anthesis and harvest of fruit in the field. Fruits were produced in treatments in which the flowers were pollinated manually, naturally or a combination. The time (67.93 days; ± 0.83) required between anthesis and harvest of the fruits was not influenced by the pollination treatments (F6,63 = 1.2373, p > 0.05). 3.2. Physico-chemical profiles of the fruits The biomass (207.40 g; ±7.61) of fresh yellow passion fruits was not affected by pollination (F6,63 = 1.8722, p > 0.05). Different pollination strategies did not alter the length (95.91 mm; ±1.30) (F6,63 = 1.409, p > 0.05), diameter (79.66 mm; ±0.94) (F6,63 = 1.684, p > 0.05) or shell thickness (5.94 mm; ±0.22) (F6,63 = 0.3292, p > 0.05) of fresh fruits harvested from the yellow passion fruit plant. The number of seeds in a particular fruit is closely related to the number of fertilized stigmas, therefore this is an extremely important variable in studies involving different pollination techniques. In our study, different treatments affected the number of seeds in the yellow passion fruit (F6,63 = 2.7108, p < 0.01) (Fig. 1). Juice biomass (F6,63 = 3.2508, p < 0.01) was influenced by the different treatments (Fig. 2) for the yellow passion fruit plant, but not its percentage (37.02%; ±0.87) (F6,63 = 1.6599, p > 0.05). Three of the chemical characteristics of yellow passion fruits were analyzed
4. Discussion 4.1. Pollination efficiency and time until harvest Flowers that only received small potential pollinators (<6.0 mm) were not pollinated (Sazima and Sazima, 1989). The morphology of the body of floral visitors, together with the morphology of flowers of the yellow passion fruit plant are factors that can prevent pollination (Bruckner et al., 1995). This suggests a co-evolution of plant species with large pollinators, especially carpenter bees. Regarding the presence of pollinators, principally carpenter bees, manual pollination can be reduced to ensure satisfactory rates of fruit production. Efficient natural pollination was attributed to the constant presence of carpenter bees (X. frontalis and X. grisescens) throughout the growing season. The presence of both pollinators, X. frontalis and X. grisescens has been fostered in commercial plantations using nest baits and/or traps (Freitas and Oliveira Filho, 2003; Oliveira Filho and Freitas, 2003; Pereira and Garófalo, 2010). These species are considered efficient pollinators of yellow passion fruit in some locations in Brazil (Hoffmann et al., 2000; Benevides et al., 2009; Siqueira et al., 2009). In our study, the constant presence of these pollinators in the field is most likely due to the existence of native vegetation (Brazilian savanna) near the area of research (Puker et al., 2010). Landscapes (when relatively well preserved) can provide a suitable nesting environment for these pollinators, as well as alternative sources of food during the absence of flowers from yellow passion fruit plants (Benevides et al., 2009; Freitas and Oliveira Filho, 2003; Freitas et al., 2009). Because the pollination percentage did not vary with different pollination techniques, it is believed that the stigmas received similar pollen loads. Furthermore, pollination during times when the flower is receptive can encourage successful of fruit production. The
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findings of this study reaffirm the importance of carpenter bees in ensuring high rates of fruit production in commercial crops of yellow passion fruit. However, we believe manual pollination should not be completely ruled out, but instead reduced. For example, assuming the frequent presence and abundance of pollinators in the area, manual pollination may only be performed on a single stigma, ensuring high rates of fruit production, but reducing the costs of manual labor. Therefore, the agricultural producer could use this new available labor to foster shelter and food for pollinators, with the construction of artificial nests, planting of alternative crops and other potential methods. The time required from anthesis to harvest of the fruit was not influenced by the pollination treatments. This information is interesting from a commercial point of view, because it reflects the importance of pollination and/or other factors (e.g., conditions of weather, health and nutrition of the plant) in time for the fruit to be harvested and/or prevent its early fall. 4.2. Physico-chemical profiles of the fruits The biomass of fresh yellow passion fruits was not influenced by pollination. Biomass of fruits from naturally pollinated flowers is similar to commercialized fruits (∼180 g) in the Brazilian state of Acre (Farias et al., 2007) and greater (∼124.7 g) than the 39 progeny of half-sisters of the yellow passion fruit (Negreiros et al., 2008). This study therefore supports the role of carpenter bees for pollination of commercial crops of yellow passion fruit, because only these pollinators ensure that fruit biomass is not reduced. Pollination did not affect the morphology (length, diameter and thickness of the shell) of freshly harvested yellow passion fruits. The shape of fruits obtained in the present study is of interest to consumers of fresh fruit, who generally prefer larger fruits and attractive appearance (Cavichioli et al., 2008). Quantifying the diameter of the yellow passion fruit is interesting because there is a close correlation with the fruit biomass and pulp, indicated as the variable with the most direct effect on biomass pulp production (Santos et al., 2009). Normally consumers prefer fruits with thinner skin, but fruits with thicker skins can be a desirable feature, because it confers greater resistance to transportation and storage. Our findings show that there is no effect of pollination on some morphological characteristics of commercial interest of the fruits of yellow passion fruit. Therefore, it is imperative to declare the importance of carpenter bees for fruit production of commercial interest, without adversely affecting its quality. The number of seeds per fruit was influenced by the different pollination methods. Because there is a positive correlation between the number of seeds per fruit and the amount of juice, this parameter is interesting from a commercial standpoint. Moreover, this is an interesting aspect with regards to seed production, seeking to select varieties and/or mechanisms that can produce more seeds per fruit. The average number of seeds found in this study was higher than in many other studies conducted in Brazil (Nascimento et al., 1999, 2003; Meletti et al., 1992) although under different conditions of cultivation. However, it is important to state that pollination performed solely by carpenter bees affects seed production. Average juice biomass was influenced by the pollination treatments. The juice itself is encountered in the aril surrounding the seed. Because the seeds are dependent on pollination it is expected that juice biomass will increase with the increased number of stigmas pollinated. It is therefore highlighted that the number of pollinated stigmas was similar in the different methods, except for manual pollination of a stigma. Regarding juice percentage the treatments were quite similar. For industry, the juice percentage is used in an evaluation of raw material (Cavichioli et al., 2008), with Brazilian industry requiring
at least 33% juice (Costa et al., 2001). Therefore, the fruits analyzed in the present study meet these requirements. The juice percentage is not only dependent on pollination, but is also related to the fruit production period (Sáenz et al., 1998; Nascimento et al., 2003). Total soluble solids (TSS), total titratable acidity (TTA) and the relationship between TSS and TTA of yellow passion fruits were not altered by pollination treatments. In this study the average TSS was 11.83 ◦ Brix, higher than the minimum content (11 ◦ Brix) required by Brazilian legislation for fresh juice (Brasil, 2000). The average TTA obtained herein (4.73%) is higher than the standards required by industry (3.2–4.5%). Acidity tends to decrease with the advance of fruit ripening. The accumulation of organic acids is determinant of the acidity and these are partially consumed during maturation, with optimum levels when the fruits are 65% yellow (Silva et al., 2005). Citric acid is most abundant, quickly reaching its maximum level after maturation, and later decreasing due to increased fruit size and respiratory rate, depending on temperature (which provokes dilution of the acid). Nutritional conditions, radiation, and particularly low temperatures are the factors that most influence the accumulation of this acid (Cavichioli et al., 2008). The relationship between TSS/TTA is considered one of the most practical ways to evaluate the flavor of the fruit (Nascimento et al., 1999). Although no minimum has been established by national legislation and it is a little-studied variable, it is known that the higher this ratio is, the better the taste of the juice. It is therefore emphasized that different pollination strategies do not negatively influence the chemical parameters of yellow passion fruits. 5. Conclusions In conclusion, we demonstrated that pollination of yellow passion fruit plants is satisfactory when performed only by the visitation of native bees, especially the carpenter bees. There is no difference in the efficiency of fruit production when one or more stigmas are pollinated manually, and combining manual and natural pollination. Manual pollination in one stigma produced less seeds and lower biomass of yellow passion fruits. When natural pollinators are present, especially carpenter bees, manual service can be reduced. Farmers can thus potentially reduce their costs of production. Acknowledgements This paper is part of the Senior project (Undergraduate in Agronomy) of MVS who received a scholarship from the Institutional Program of Scientific Initiation Scholarships of the Universidade Estadual de Mato Grosso do Sul. We thank Laura Pereira de Oliveira, Daniel Makoto Kusano, Elisa Pereira de Oliveira, Lais Luque de Lima, Jefferson Bittencourt Venancio and Ricardo Fernando Da Rui for their help during the execution of this research. Special thanks to Dr. Fernando Cesar Vieira Zanella (UFCG, Brazil) who performed the taxonomic identification of the carpenter bees. We thank Patty Ramirez (University of Lancaster, Lancaster, UK) for reviewing the English of this article. We also thank the Cassiano Sousa Rosa (Universidade Federal de Vic¸osa, Vic¸osa, Minas Gerais, Brazil) for the corrections and suggestions made to the previous version of this manuscript. References AOAC, 1990. Official Methods of Analysis of the Association of Official Analytical Chemists, 15th ed. AOAC, Washington, USA. Aizen, M.A., Garibaldi, L.A., Cunningham, S.A., Klein, A.M., 2008. Long-term global trends in crop yield and production reveal no current pollination shortage but increasing pollinator dependency. Curr. Biol. 18, 1572–1575. Allen-Wardell, G., Bernhardt, P., Bitner, R., Burquez, A., Buchmann, S., Cane, J., Cox, P.A., Dalton, V., Feinsinger, P., Ingram, M., Inouye, D., Jones, C.E., Kennedy, K.,
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Scientia Horticulturae journal homepage: www.elsevier.com/locate/scihorti
Is manual pollination of yellow passion fruit completely dispensable? Murilo V. Silveira a , Alfredo R. Abot b , José N. Nascimento c , Edson T. Rodrigues b , Sérgio R. Rodrigues b , Anderson Puker d,∗ a
Programa de Pós-Graduac¸ão em Agronomia, Universidade Estadual de Mato Grosso do Sul, Aquidauana, MS, Brazil Universidade Estadual de Mato Grosso do Sul, Aquidauana, MS, Brazil Universidade Federal da Grande Dourados, Dourados, MS, Brazil d Programa de Pós-Graduac¸ão em Entomologia, Departamento de Entomologia, Universidade Federal de Vic¸osa, Vic¸osa, MG, Brazil b c
a r t i c l e
i n f o
Article history: Received 26 May 2012 Received in revised form 16 August 2012 Accepted 18 August 2012 Keywords: Carpenter bees Cross-pollination Mass flowering plant Self-incompatible plant Tropical fruit Wild pollinators
a b s t r a c t High dependence on pollination is considered the main cause of low productivity in American yellow passion fruit crops (Passiflora edulis f. flavicarpa). As intensive farming practices require similarly intensive manual pollination, this study sought answer the following questions: (a) is there a difference in the efficiency of fruit production when one or more stigmas are pollinated manually, by natural pollinators (or both)? and (b) does manual or natural pollination (or both) affect the physical and chemical characteristics of the fruits? Flowers were pollinated manually, naturally by native bees or by using both methods. Fruit production was evaluated seven days after anthesis, as well as some selected physico-chemical characteristics of harvested fruits. It was demonstrated that the pollination of yellow passion fruit is satisfactory only with visitation by native bees, especially carpenter bees. There is no difference in fruit production efficiency when one or more stigmas are pollinated manually and then left free for visits by natural pollinators. Manual pollination in one stigma produced less seeds and lower biomass of fruit juice of yellow passion fruits. When there is the presence of natural pollinators (notably carpenter bees), manual services can be reduced but not completely dismissed. Therefore, yellow passion fruit farmers can potentially reduce production costs. © 2012 Elsevier B.V. All rights reserved.
1. Introduction The value of services provided by native pollinators has recently been the focus of much attention (e.g., Allsopp et al., 2008), particularly on foods consumed worldwide and those that require of cross-pollination (Allen-Wardell et al., 1998; Klein et al., 2007; Aizen et al., 2008; Winfree, 2008). For example, a greater abundance and diversity of native bees significantly improved fruit production in coffee (Klein et al., 2003) and rapeseed plantations (Morandin and Winston, 2005). Pollinators, however, are ostensibly subject to anthropogenic landscape changes and the risk of pesticide application (e.g., Watanabe, 1994; Stokstad, 2006; Oldroyd, 2007). Two components of pollination must be evaluated in order to directly compare the effectiveness of pollination: pollen transfer efficiency and frequency of visits (Rader et al., 2009). Pollen transfer efficiency describes the ability of individual pollinators to remove and transport the pollen to the stigmas of conspecifics (Primack and
∗ Corresponding author at: Programa de Pós-Graduac¸ão em Entomologia, Departamento de Entomologia, Universidade Federal de Vic¸osa, 36570-000 Vic¸osa, MG, Brazil. Tel.: +55 31 3899 3785. E-mail address: [email protected] (A. Puker). 0304-4238/$ – see front matter © 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.scienta.2012.08.023
Silander, 1975; Herrera, 1987). Frequency of visitation is the ratio between the abundance of pollinators and the number of flowers visited in a given time interval (Herrera, 1987, 1989; Vazquez et al., 2005). The most effective pollinator is therefore one that is present in large numbers and moves quickly from flower to flower. It would also be frequently in contact with the stigma, and would transfer a high number of pollen grains. On the other hand, the least effective pollinator would show low abundance and move relatively slowly from flower to flower. This type of pollinator would rarely be in contact with the stigma while visiting a flower and transfer few pollen grains (Rader et al., 2009). Passiflora edulis Sims f. flavicarpa Degener (Passifloraceae), known as yellow passion fruit, is a self-incompatible plant that completely depends on cross-pollination for its reproduction (Bruckner et al., 1995). In several countries this function is performed mainly by native bees and especially by the carpenter bees (Sazima and Sazima, 1989; Hoffmann et al., 2000; Camillo, 2003), as the flowers of P. edulis have characteristics adapted to suit pollination by large bees. The distance between the dehiscent side of the anthers and corolla, the shape of the anthers and their versatility (easily moved upon touch) allow a precise coupling in the dorsal region of major pollinators. The stigmas, in turn, resist movement, which facilitates the adhesion of pollen when touched by the dorsal
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region of the bee (Bruckner et al., 1995). In addition, flowers that are large, attractive, have bright colors, strong odors, abundant concentrations of pollen and nectar are characteristics that attract bees (Cobert and Willmer, 1980). Carpenter bees are considered the only effective pollinators of commercial crops of yellow passion fruit due to their morphological and behavioral characteristics (e.g., Keasar, 2010). Because the number of native bees has reduced in commercial crops, manual pollination has been adapted to ensure satisfactory productivity (Calle et al., 2010). The low rates of pollination by native bees are probably related to: the absence and/or reduction of vegetation cover close to cultivated areas (a lack of suitable sites for nesting) and the use of pesticides, which is relatively common in commercial crops. These are probably some of the factors that have justified the use of manual pollination. On the other hand, numerous techniques have been developed and are considered effective for maintaining high populations of native bees in agricultural areas, including artificial nests (e.g., Freitas and Oliveira Filho, 2003; Oliveira Filho and Freitas, 2003), alternative sources of food (Pontin et al., 2006), and the diversification and habitat conservation of areas in the vicinity of the crop (e.g., Freitas et al., 2009). Being a mass flowering plant, the yellow passion fruit and other plants (e.g., Westphal et al., 2003), require pollination when the flower is receptive to receive pollen, usually during hours of high temperature during the day (Cobert and Willmer, 1980; Siqueira et al., 2009); and indeed larger populations of native bees are observed visiting the plant during this period (Benevides et al., 2009; Siqueira et al., 2009). Therefore, the pollination efficiency of this species justifies its conservation in agricultural landscapes (Benevides et al., 2009). Worldwide, surprisingly few studies have directly compared the effectiveness of hand pollination performed by man with the alternative of exclusively using the services of native bees in intensively farmed regions (Siqueira et al., 2009). Even though the main cause of the fall of the flowers from the yellow passion fruit plant and consequently reduced production is the lack of pollination. Therefore, artificial pollination has often been the only alternative in yellow passion fruit plantations, especially in areas with low pollinator population densities. Fear often causes many farmers to use hand pollination, but they recognize the crucial role of native bees, especially the carpenter bees (Calle et al., 2010). As intensive farming practices require similarly intensive manual pollination, this study sought to answer the following questions: (a) is there a difference in the efficiency of fruit production when one or more stigmas are pollinated manually, by natural pollinators (or both)? and (b) does manual or natural pollination (or both) affect the physical and chemical characteristics of the fruits of yellow passion fruit?
2. Materials and methods 2.1. Location of study, crop and management of the plants The study was conducted at the Universidade Estadual de Mato Grosso do Sul (UEMS), located in Aquidauana, Mato Grosso do Sul, Brazil (20◦ 28 S, 55◦ 48 W). The climate is Tropical Hot–Humid (Aw) according to Köppen classification (Peel et al., 2007), with average annual temperature of 26 ◦ C and annual rainfall from 1200 mm to 1300 mm. The soil is classified as Fluvic Cambisol. Cultivation was initiated in April 2008, with spacing of 3 m between rows and 5 m between plants (density of 667 plants ha−1 ) in a vertical cordon system. Fertilization was performed according to the recommendations of Rodrigues (2008), based on soil analysis. Plants were pruned at biweekly intervals to correct plant architecture.
2.2. Experiments Each treatment of pollination was composed of 60 flowers distributed in 24 plants, with a maximum of three flowers per plant per treatment. Fruit production was recorded seven days after anthesis according to the method proposed by Silva et al. (1997). Treatments of pollination were: (1) spontaneous self-pollination – the marked buds remained covered during the opening of the flower; (2) natural pollination, excluding carpenter bees – buds were marked before anthesis and covered with a screen (6 mm holes diameter) to prevent the entry of carpenter bees, remaining free to visits by other potential pollinators; (3) flowers in pre-anthesis were covered with a screen (mesh 0.5 mm × 0.5 mm), which were removed when the stigmas were capable of being pollinated. At this moment manual pollination was performed, depositing pollen in one stigma and re-covering the flower to prevent the entry of any potential pollinators; (4) idem previous treatment, but to perform the pollination, pollen was deposited in two stigmas, (5) idem treatment 4, but with pollination in three stigmas; (6) natural pollination buds were marked before anthesis and remained free to natural pollination by insects; (7) natural and manual pollination in one stigma – the flower buds were marked, and one hour after anthesis when the stigmas were deflected manually received pollen on one stigma, leaving the flower open for visitation by insects; (8) natural and manual pollination in two stigmas and (9) natural and manual pollination in three stigmas. Manual pollination was always performed between 13:30 and 15:00 (Souza et al., 2004) from April 10 to May 30, 2009, collecting pollen from a recent anther dehiscence and placed on the stigmas of flowers with deflected stigmas, as recommended by Camillo (2003). Ten fruits from each treatment (one fruit per plant) were arbitrarily selected and harvested when they were more than 30% yellow and presented no resistance to abscission (as per the methods of Silva et al., 2008) for analysis of physico-chemical variables. The parameters evaluated were: fresh biomass of the fruit; length; diameter; shell thickness; number of seeds; juice biomass; juice percentage (juice biomass/fruit × 100); total soluble solids (TSS); total titratable acidity (TTA); and finally the ratio between total soluble solids and total titratable acidity (TSS/TTA). TSS were measured directly using a refractometer with results expressed in ◦ Brix. TTA was evaluated by titration of 5 mL of juice diluted in 25 mL of distilled water, using phenolphthalein as an indicator, with a solution of 0.5 N NaOH, until pink color persisted, according to the technique defined by AOAC (1990). 2.3. Data analysis Data referring to the percentage of pollination (n = 60 flowers) were analyzed using Generalized Linear Model (GLM) (Crawley, 2002) with binomial distribution. The results of the time between anthesis and harvest of fruit (n = 10) in the field and of the physicochemical characteristics of fruits (n = 10) also were analyzed using GLM and compared by analysis of the contrast (˛ < 0.05). All GLMs were submitted to residual analysis, so as to evaluate the adequacy of error distribution (Crawley, 2002). These analyzes were conducted with the software program R (R Development Core Team, 2012). 2.4. Sampling, identification and deposit of the voucher specimens Carpenter bees were sampled directly from flowers of the yellow passion fruit plant with an entomological net. The specimens were mounted on entomological pins and identified by Dr. Fernando Cesar Vieira Zanella (Universidade Federal de Campina Grande, UFCG, Patos, Paraíba, Brazil). Voucher specimens were deposited
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Fig. 1. Average number of seeds in the yellow passion fruits in response to different pollination treatments: (1) spontaneous self-pollination; (2) natural pollination, excluding carpenter bees; (3) manual pollination in one stigma; (4) manual pollination in two stigmas; (5) manual pollination in three stigmas; (6) natural pollination; (7) natural pollination + manual pollination in one stigma; (8) natural pollination + manual pollination in two stigmas and (9) natural pollination + manual pollination in three stigmas. Bars on columns represent standard errors. Columns differ significantly when labeled with different letters (p < 0.01).
Fig. 2. Average biomass of fruit juice of yellow passion fruits in response to different pollination treatments: (1) spontaneous self-pollination; (2) natural pollination, excluding carpenter bees; (3) manual pollination in one stigma; (4) manual pollination in two stigmas; (5) manual pollination in three stigmas; (6) natural pollination; (7) natural pollination + manual pollination in one stigma; (8) natural pollination + manual pollination in two stigmas and (9) natural pollination + manual pollination in three stigmas. Bars on columns represent standard errors. Columns differ significantly when labeled with different letters (p < 0.01).
at the Laboratory of Ecology and Biogeography of Insects from the Caatinga (UFCG) and Entomology Laboratory of the UEMS.
whose flowers were exposed to different methods of pollination: the total soluble solids (TSS) (11.83 ◦ Brix; ±0.16) (F6,63 = 0.8839, p > 0.05), total titratable acidity (TTA) (4.73%; ±0.07) (F6,63 = 1.6138, p > 0.05) and the relationship between TSS and TTA (2.53; ±0.05) (F6,63 = 0.7369, p > 0.05) were not affected by the different pollination treatments.
3. Results 3.1. Pollination efficiency and time until harvest There was no fruit production in flowers that did not receive pollen by natural or manual pollinators, confirming the need for cross-pollination by insects or manual methods. In our study, the carpenter bees Xylocopa frontalis (Olivier) and X. grisescens (Lepeletier) (Hymenoptera: Apidae: Xylocopini) were sampled pollinating the yellow passion fruit flowers. For all treatments the pollination rates (average: 34.76%; standard error: ± 2.33) were similar (Chi = 537.44, p > 0.05). The effect of pollination was evaluated on the time between anthesis and harvest of fruit in the field. Fruits were produced in treatments in which the flowers were pollinated manually, naturally or a combination. The time (67.93 days; ± 0.83) required between anthesis and harvest of the fruits was not influenced by the pollination treatments (F6,63 = 1.2373, p > 0.05). 3.2. Physico-chemical profiles of the fruits The biomass (207.40 g; ±7.61) of fresh yellow passion fruits was not affected by pollination (F6,63 = 1.8722, p > 0.05). Different pollination strategies did not alter the length (95.91 mm; ±1.30) (F6,63 = 1.409, p > 0.05), diameter (79.66 mm; ±0.94) (F6,63 = 1.684, p > 0.05) or shell thickness (5.94 mm; ±0.22) (F6,63 = 0.3292, p > 0.05) of fresh fruits harvested from the yellow passion fruit plant. The number of seeds in a particular fruit is closely related to the number of fertilized stigmas, therefore this is an extremely important variable in studies involving different pollination techniques. In our study, different treatments affected the number of seeds in the yellow passion fruit (F6,63 = 2.7108, p < 0.01) (Fig. 1). Juice biomass (F6,63 = 3.2508, p < 0.01) was influenced by the different treatments (Fig. 2) for the yellow passion fruit plant, but not its percentage (37.02%; ±0.87) (F6,63 = 1.6599, p > 0.05). Three of the chemical characteristics of yellow passion fruits were analyzed
4. Discussion 4.1. Pollination efficiency and time until harvest Flowers that only received small potential pollinators (<6.0 mm) were not pollinated (Sazima and Sazima, 1989). The morphology of the body of floral visitors, together with the morphology of flowers of the yellow passion fruit plant are factors that can prevent pollination (Bruckner et al., 1995). This suggests a co-evolution of plant species with large pollinators, especially carpenter bees. Regarding the presence of pollinators, principally carpenter bees, manual pollination can be reduced to ensure satisfactory rates of fruit production. Efficient natural pollination was attributed to the constant presence of carpenter bees (X. frontalis and X. grisescens) throughout the growing season. The presence of both pollinators, X. frontalis and X. grisescens has been fostered in commercial plantations using nest baits and/or traps (Freitas and Oliveira Filho, 2003; Oliveira Filho and Freitas, 2003; Pereira and Garófalo, 2010). These species are considered efficient pollinators of yellow passion fruit in some locations in Brazil (Hoffmann et al., 2000; Benevides et al., 2009; Siqueira et al., 2009). In our study, the constant presence of these pollinators in the field is most likely due to the existence of native vegetation (Brazilian savanna) near the area of research (Puker et al., 2010). Landscapes (when relatively well preserved) can provide a suitable nesting environment for these pollinators, as well as alternative sources of food during the absence of flowers from yellow passion fruit plants (Benevides et al., 2009; Freitas and Oliveira Filho, 2003; Freitas et al., 2009). Because the pollination percentage did not vary with different pollination techniques, it is believed that the stigmas received similar pollen loads. Furthermore, pollination during times when the flower is receptive can encourage successful of fruit production. The
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findings of this study reaffirm the importance of carpenter bees in ensuring high rates of fruit production in commercial crops of yellow passion fruit. However, we believe manual pollination should not be completely ruled out, but instead reduced. For example, assuming the frequent presence and abundance of pollinators in the area, manual pollination may only be performed on a single stigma, ensuring high rates of fruit production, but reducing the costs of manual labor. Therefore, the agricultural producer could use this new available labor to foster shelter and food for pollinators, with the construction of artificial nests, planting of alternative crops and other potential methods. The time required from anthesis to harvest of the fruit was not influenced by the pollination treatments. This information is interesting from a commercial point of view, because it reflects the importance of pollination and/or other factors (e.g., conditions of weather, health and nutrition of the plant) in time for the fruit to be harvested and/or prevent its early fall. 4.2. Physico-chemical profiles of the fruits The biomass of fresh yellow passion fruits was not influenced by pollination. Biomass of fruits from naturally pollinated flowers is similar to commercialized fruits (∼180 g) in the Brazilian state of Acre (Farias et al., 2007) and greater (∼124.7 g) than the 39 progeny of half-sisters of the yellow passion fruit (Negreiros et al., 2008). This study therefore supports the role of carpenter bees for pollination of commercial crops of yellow passion fruit, because only these pollinators ensure that fruit biomass is not reduced. Pollination did not affect the morphology (length, diameter and thickness of the shell) of freshly harvested yellow passion fruits. The shape of fruits obtained in the present study is of interest to consumers of fresh fruit, who generally prefer larger fruits and attractive appearance (Cavichioli et al., 2008). Quantifying the diameter of the yellow passion fruit is interesting because there is a close correlation with the fruit biomass and pulp, indicated as the variable with the most direct effect on biomass pulp production (Santos et al., 2009). Normally consumers prefer fruits with thinner skin, but fruits with thicker skins can be a desirable feature, because it confers greater resistance to transportation and storage. Our findings show that there is no effect of pollination on some morphological characteristics of commercial interest of the fruits of yellow passion fruit. Therefore, it is imperative to declare the importance of carpenter bees for fruit production of commercial interest, without adversely affecting its quality. The number of seeds per fruit was influenced by the different pollination methods. Because there is a positive correlation between the number of seeds per fruit and the amount of juice, this parameter is interesting from a commercial standpoint. Moreover, this is an interesting aspect with regards to seed production, seeking to select varieties and/or mechanisms that can produce more seeds per fruit. The average number of seeds found in this study was higher than in many other studies conducted in Brazil (Nascimento et al., 1999, 2003; Meletti et al., 1992) although under different conditions of cultivation. However, it is important to state that pollination performed solely by carpenter bees affects seed production. Average juice biomass was influenced by the pollination treatments. The juice itself is encountered in the aril surrounding the seed. Because the seeds are dependent on pollination it is expected that juice biomass will increase with the increased number of stigmas pollinated. It is therefore highlighted that the number of pollinated stigmas was similar in the different methods, except for manual pollination of a stigma. Regarding juice percentage the treatments were quite similar. For industry, the juice percentage is used in an evaluation of raw material (Cavichioli et al., 2008), with Brazilian industry requiring
at least 33% juice (Costa et al., 2001). Therefore, the fruits analyzed in the present study meet these requirements. The juice percentage is not only dependent on pollination, but is also related to the fruit production period (Sáenz et al., 1998; Nascimento et al., 2003). Total soluble solids (TSS), total titratable acidity (TTA) and the relationship between TSS and TTA of yellow passion fruits were not altered by pollination treatments. In this study the average TSS was 11.83 ◦ Brix, higher than the minimum content (11 ◦ Brix) required by Brazilian legislation for fresh juice (Brasil, 2000). The average TTA obtained herein (4.73%) is higher than the standards required by industry (3.2–4.5%). Acidity tends to decrease with the advance of fruit ripening. The accumulation of organic acids is determinant of the acidity and these are partially consumed during maturation, with optimum levels when the fruits are 65% yellow (Silva et al., 2005). Citric acid is most abundant, quickly reaching its maximum level after maturation, and later decreasing due to increased fruit size and respiratory rate, depending on temperature (which provokes dilution of the acid). Nutritional conditions, radiation, and particularly low temperatures are the factors that most influence the accumulation of this acid (Cavichioli et al., 2008). The relationship between TSS/TTA is considered one of the most practical ways to evaluate the flavor of the fruit (Nascimento et al., 1999). Although no minimum has been established by national legislation and it is a little-studied variable, it is known that the higher this ratio is, the better the taste of the juice. It is therefore emphasized that different pollination strategies do not negatively influence the chemical parameters of yellow passion fruits. 5. Conclusions In conclusion, we demonstrated that pollination of yellow passion fruit plants is satisfactory when performed only by the visitation of native bees, especially the carpenter bees. There is no difference in the efficiency of fruit production when one or more stigmas are pollinated manually, and combining manual and natural pollination. Manual pollination in one stigma produced less seeds and lower biomass of yellow passion fruits. When natural pollinators are present, especially carpenter bees, manual service can be reduced. Farmers can thus potentially reduce their costs of production. Acknowledgements This paper is part of the Senior project (Undergraduate in Agronomy) of MVS who received a scholarship from the Institutional Program of Scientific Initiation Scholarships of the Universidade Estadual de Mato Grosso do Sul. We thank Laura Pereira de Oliveira, Daniel Makoto Kusano, Elisa Pereira de Oliveira, Lais Luque de Lima, Jefferson Bittencourt Venancio and Ricardo Fernando Da Rui for their help during the execution of this research. Special thanks to Dr. Fernando Cesar Vieira Zanella (UFCG, Brazil) who performed the taxonomic identification of the carpenter bees. We thank Patty Ramirez (University of Lancaster, Lancaster, UK) for reviewing the English of this article. We also thank the Cassiano Sousa Rosa (Universidade Federal de Vic¸osa, Vic¸osa, Minas Gerais, Brazil) for the corrections and suggestions made to the previous version of this manuscript. References AOAC, 1990. Official Methods of Analysis of the Association of Official Analytical Chemists, 15th ed. AOAC, Washington, USA. Aizen, M.A., Garibaldi, L.A., Cunningham, S.A., Klein, A.M., 2008. Long-term global trends in crop yield and production reveal no current pollination shortage but increasing pollinator dependency. Curr. Biol. 18, 1572–1575. Allen-Wardell, G., Bernhardt, P., Bitner, R., Burquez, A., Buchmann, S., Cane, J., Cox, P.A., Dalton, V., Feinsinger, P., Ingram, M., Inouye, D., Jones, C.E., Kennedy, K.,
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