Journal of Agriculture Food and Development, 2020, 6, 1-9 1 Floral Behaviour, Flowering Phenology and Fruit Production of Passion Fruit ( Species) in East Malaysia

Shiamala Devi Ramaiya1,*, Japar Sidik Bujang2, Muta Harah Zakaria3 and Nur Shahirah Shahbani1

1Department of Crop Science, Faculty of Agriculture and Food Sciences, Universiti Putra Malaysia Bintulu Campus, 97008 Bintulu, Sarawak, Malaysia 2Department of Biology, Faculty of Science, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor Darul Ehsan, Malaysia 3Department of Aquaculture, Faculty of Agriculture, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor Darul Ehsan, Malaysia Abstract: Passiflora species generally known as passion fruit may well be the most fascinating plant of the tropics. This plant is known to be self-incompatible in its native environment and it affects the fruit production. Extend of passion fruit set is highly dependent on effective such as carpenter bees and honey bees. However, in East Malaysia, there was good fruit sets, although lesser number of pollinators visiting the farm or sometimes absence. It is important therefore, to study the reproduction mechanisms of Passiflora plants, because this factor reflect the quantity of the fruit produced. The present studies aim therefore to evaluate the floral behaviours, reproductive mechanism and fruit production of locally grown Passiflora species. Based on the observations, Passiflora species was classified as “steady- state species” that exhibit constant production of few flowers, each day lasting only one day. All species have the ability to adapt to the local condition where plants continuously grew and produced flowers and fruits all the year around. The flowering and fruiting were not synchronized and showed a marked phenological pattern with species. Good fruit yields were observed throughout the year which was attributed to Passiflora species ability for self-pollination, involving the movement of styles to lead the stigma faced the anthers during flower blooming. This is an important phenomenon in order to reduce the distance between the stigma and anther, aid for pollination and provided reproductive assurance to the species. As P. edulis growing in its native environment is reported to be self-incompatible and have become self- compatible in the present study; showed that evolution of these features is an important factor for its adaptability and survivability, thus crucial to P. edulis propagation optimally in local conditions. Keywords: Self-pollination, fruit sets, herkogamy, homogamous, passion fruit.

1. INTRODUCTION 1960s [5]. Thereafter, the passion fruit production in these regions has been affected by a passion fruit Passiflora plants generally known as passion fruit woodiness diseases (PWD) which discouraged further may well be the most fascinating plant of the tropics. expansion in commercial planting [5]. However, this Their unique, almost lavishly beautiful flowers have a fruit is started to cultivated in commercial scale due to mysterious look and convey an exotic ambiance [1]. the prevalence of suitable growing conditions [6]. There Passion fruit plants belong to the family Passifloraceae is an immense potentiality of boosting passion fruit consists of 18 genera including genus Passiflora [2]. industry in Malaysia. The region has good climate with Passion fruits are one of the widely grown fruit crops sufficient rainfall and warm temperature with little around the world. The main dispersal area extends variation in the photoperiod for growing a variety of over Central America and [2,3]. horticultural crops very successfully [7]. Although 50 species bear edible fruits, only two forms of P. edulis; i.e., P. edulis (Purple passion fruit) and P. Pollination is essential for fruit production on edulis f. flavicarpa (Yellow passion fruit) are widely Passiflora plant. Flowers of the P. edulis vine normally cultivated in commercial scale for fresh fruit and juice set fruit when the flowers are cross pollinated [8]. The market [4]. amount of deposited on the stigma determines the number of seeds set and size of the fruit. The most In Peninsular Malaysia, Passiflora plants were effective pollinating of Passiflora species are grown in Ayer Hitam (Johor) and Cameron Highlands (Xylocopa sonorina) and the honeybee (Pahang) which were extended to be a commercial in (Apis millifera) [9]. It has been reported, in its native country and other parts of the world, most of the

Passiflora speciesare observed to be self- *Address correspondence to this author at the Department of Crop Science, Faculty of Agriculture and Food Sciences, Universiti Putra Malaysia Bintulu incompatible[10-13]. Extend of passion fruit set is Campus, 97008 Bintulu, Sarawak, Malaysia; highly dependent on effective pollinators such as E-mail: [email protected]

E-ISSN: 2415-0142/20 © 2020 Journal of Agriculture Food and Development 2 Journal of Agriculture Food and Development, 2020, Vol. 6 Ramaiya et al. carpenter bees in its nativewhile in India, Apis cerana is Monograph, [15]). The observations taking into account the primary [14]. of occurrence, duration and frequency of the vegetative growth, flowering and fruiting. Flowering was defined However, in East Malaysia, there was good fruit as open flowers since Passiflora species produce sets, although lesser number of effective pollinators flowers all year around. Data on flowering phenology visiting the farm or sometimes absence. It is important were obtained to verify the blooming pattern. The major to study the reproduction mechanisms of Passiflora bloom and minor bloom was worked out on the basis of plants because this factor reflect the quantity of the fruit number of flowers opened every day. In case of major produced and it was claimed that plant from different bloom, more than half of the vines produced five or geographical locations can produce plants more number of flowers per day for 10 days in a month phenotypically different from their native environment. was considered, in accordance with the methodology of Therefore, the present study are aim to evaluate the Kishore et al. [16]. In addition, detail observation made floral behaviours, reproductive mechanism and fruit on blooming time, continuous observations were made production of locally grown passion fruit species; from time of anthesis until closing flowers, recording (Purple), Passiflora edulis (Frederick), changes in position of pistil and stamen were also Passiflora maliformisand Passiflora incarnata with the recorded. Flower visitors have been observed time to condition of lesser or absence of effective pollinators. time. Fruiting was also defined as the presence of young and ripe fruits. Detail observations were also 2. MATERIALS AND METHODS made on fruit development and fruit productivity. 2.1. Study Locationand Plant Cultivation 3. RESULTS AND DISCUSSION

The present study was conducted at the small scale 3.1. Flower Development of Passiflora Species passion fruit farm initiated in Universiti Putra Malaysia Bintulu (N 03° 12.45' and E 113° 4.68'), Sarawak. Flower bud differentiation occurs during the growth Planting materials used in this study were seeds ofshoots and the stages of bud development varied acquired from the commercial supplier Trade Winds among vines [17]. Five main stages have been Fruit, Windsor, California. There were four Passiflora recognized in Passiflora flowers development. The species; Passiflora edulis (Purple), Passiflora edulis flower stages were; Stage 1-bracts formation, Stage 2- (Frederick), Passiflora maliformisand Passiflora bud initiation, Stage 3-bud development, Stage 4- incarnatawhich were cultivated and examined in the complete bud formation, Stage 5-flower blooming. present study. For planting of Passiflora species, a Flowering behaviors varied significantly between the vertical trellis system with ten rows, each with 25 m studied species. Among the Passiflora species studied, was constructed. The trellis system consisted of 2.4 m the earliest flower initiation was recorded in P. tall post set at 5 m intervals along the rows. Three incarnata. The plant displayed expressive bloom after gauge galvanized wires (2.5 mm) were strung along 14 weeks of transplanting. The maximum bud size was the posts. Four months old seedling with similar height 5.04±0.09 cm and days required for flower opening (about 20-25 cm) and number of leaves (approximately from bud stage were 13.4±0.55 days. For P. edulis 9-13) were chosen for transplanting with planting (Purple) and P. edulis (Frederick), the first flower distance of 3.0 m between rows and 2.5 m within rows. initiation was recorded on 5th month after transplanting Plant management including pruning, fertilizing and and the bloom appeared approximately 6 months (160 weeding were performed accordingly. days) after transplanting. The results were in accordance with study by Banu et al. [18], who stated 2.2. Observation on Phenological Study and Fruits Productivity first flowering was on 152 days after transplanting in Bangladesh but little varied with Montero et al. [19] th Vegetative shoots were tagged and observed for where first flower bud initiated after 14 weeks (4 their developmental changes up to fruiting stage.The month) and first bloom was recorded on 34 weeks (~8 phenological records were correlated with metrological months) after transplanting. A flower bud took 14.6 data (i.e., monthly rainfall, temperature, relative days to developed with maximum size of bud was humidity and sunshine hours). The plant development 5.15±0.10 cm. Time required for bud initiation to flower phase recorded in the present study, based on opening ranged from 10-15 days in the study reported extended BBCH scale (Growth stage of plants, BBCH by Das et al. [20] in P. edulis (Purple). However, among the examined species, the last species to Floral Behaviour, Flowering Phenology and Fruit Production Journal of Agriculture Food and Development, 2020, Vol. 6 3 produce flower was P. maliformis. The first blooms flowers opened about 0400-0500 hour and closed at began later at 195 days, at 7th month after 1800-2000 hour [20]. This shows the variation may be transplanting. Flower bud development took 14.0±1.00 due to the phenological differences, environment, days with the larger flower bud size of 6.79±0.10 cm. adaptability and genetics [22].

3.2. Different Flower Blooming Time and Duration 3.3. Flower Blooming Stages and The Stigma and Anther Positions Based on the detail observation, the time of flowering varied between Passiflora species. The Position of stigma and anther are very important in details of flower blooming time are presented in Table Passiflora flower due to its natural pollination factor. 1. Among the four species, the earlier flower opening The example of complete Passiflora flower (P. was recorded in P. maliformis. Flowers of this species incarnata) blooming stages is showed in Figure 1. started to open early in the morning at 0820±0.10 hour Basically, there were three phenological stages have and flowers remained opened until sunset about 1600- been recognized in all the studied Pasiflora species. No 1730 hour. The flower full blooming was recorded significant changes in colour and odour were observed around 0831±0.20 hour and it took around 40 min for in flower from opened to closed. Phase 1- Pre- the styles to be completely curved and in contact with anthesis: Bud stage prior to anthesis was known as the anthers where anthesis started at 0913±0.20 hour. phase 1 and corresponds to the immediately preceding anthesis floral stage. At this stage the gynoecium, Among the Passiflora species, the longer duration androecium and the corona were fully covered by the of flower blooming was observed in P. incarnata, period sepals. The sepals converged from when the flower opened until the styles fully curved and stigma touched the anther about 100 toward the center of the flower. The reproductive minutes. Passiflora edulis (Purple) flower opened and structures were not visible. The styles were erected showed full bloom around noon 1223±0.25 hour and (Figure 1a) while the anthers dehiscenced facing up the anthesis started at 1316±0.29 hour. The flowers (Figure 1b). were open until night fall. Banu et al. [18] stated, P. edulis (Purple) flowers were in full bloom within 1052- Phase 2- Anthesis (Flower homogamous with 1240 hour in Bangladesh. In this present study, P. herkogamy). In this phase, the flower started to open, edulis (Purple) flower bloomed later than from the sepals, and corona spread out rapidly and Bangladesh. Similarly, observation made on P. edulis the reproductive structures fully exposed to the external in Queensland by Souza et al. [8], revealed the flowers environment when the flower reached its maximum were opened around mid-day and the stigma staying opening (Figure 1c). The upright facing anthers during receptive for approximately 90 min. In contrast, Cox flower opening, were tumbled down and turned around, [21] stated, in New South Wales, Australia, the P. thus bringing the dehisced side of the anther was edulis (Purple) flower bloomed in the night or early facing downward (Figure 1d) at this phase. Styles in morning and closed at mid-day, with the stigma fully the upright position began to tilt to reach the anthers receptive only on the morning of first day. Similarly, (Figure 1e-g). Simultaneously, the stigma remained , USA, Florida the flowers of the P. edulis receptive and anthers were indehiscent. The style (Purple) opened early in the morning usually around continuous tilted until the receptive stigma came into dawn, and closed before noon. In Brazil, P. edulis contact with the receptive anthers, donating pollen

Table 1: Flowering Time of Passiflora Species Observed in n=50 Flowers

Blooming events P. edulis P. edulis P. maliformis P. (Purple) (Frederick) incarnata

Flower started toopen (hr) 1153±0.20 1100±0.25 0820±0.10 1214±0.19 (1130-1221) (1028-1120) (0802-0849) (1130-1212) Full bloom(hr) 1223±0.25 1123±0.07 0831±0.20 1229±0.36 (1134-1240) (1102-1140) (0820-0853) (1148-1315) Style facedanther (hr) 1316±0.29 1219±0.28 0913±0.20 1351±0.20 (1215-1340) (1138-1258) (0834-0912) (1300-1400)

Values are given as means (hr) ± SD and values in parenthesis are the range. 4 Journal of Agriculture Food and Development, 2020, Vol. 6 Ramaiya et al.

Figure 1: Flower blooming stages of P. incarnata; a) flower bud-ready to be opened, b) flower opening, c) anthers started to tumble down, d) all the anthers facing, e) styles were in horizontal position, f) styles taking curve, g) styles were tilt and stigma started to in contact with the anthers, h)- i) stigma touched the anthers and were transferred. grains ontothe stigmatic surface (Figure 1h-i). This is showed rapid enlargement of the ovary and developing an important phenomenon in Passiflora flowers inorder fruit can be recognized in 3 days. to reduce the distance between the stigma and anther, which is necessary for pollination. As the pollen grains In addition, based on the detail observation during were large and bright yellow to white in colour the the phase 2 of flower blooming, the Passiflora flowers presence of pollen grains on the stigma surface could exhibited 3 types of style morphology; a) styles without be clearly seen. This phase has been identified that all curvature (WC), where the style stand erect, b) partially the Passiflora flowers as homogamous floral where curved (PC) style, where the style curved partially, and anther and stigma mature simultaneously and present the stigmas does not touch the anther and c) herkogamy, with supplying a spatial separation of completely curved (CC) style, where style is curved anthers and stigma. Phase 3- Flower senescence. This and the stigmas in contact with the anther. Percentage phase is the closure of the flower. It was observed that (%) of different types of styles in Passiflora flower is the petals and corona wilted and the surfaces lose presented in Figure 2. Among four Passiflora species, turgidity and started closing. The sepal returned to an the CC flowers were commonly found (≥80% except in upright position while stigmas were erected backward, P. maliformis, 38.33%) and produced more fruits. The while the bracts remained fresh. Pollinated flowers WC flowers were relatively less common where such Floral Behaviour, Flowering Phenology and Fruit Production Journal of Agriculture Food and Development, 2020, Vol. 6 5

Figure 2: Percentage (%) of different types of styles in Passiflora flowers (n=60 flowers). CC- completely curved, PC- partially curved and WC-without curvature (stand erect). flowers did not get pollinated and did not produce fruits. and observed that the P. edulis produced good fruit The maximum WC flowers was recorded in P. edulis sets continuously even in the absence of pollinators. As (6.67%) while 0% was observed in P. incarnata. P. edulis growing in its native habitat and other parts of Flowers of P. maliformis possessed mostly the PC the world is reported to be self-incompatible and have styles (60.00%) and P. incarnata had minimum, 5.00% become self-compatible in the present study and also of PC flowers. in India [23] showed that evolution of these features in Passiflora flower is important factor for its adaptability As discussed above, the unique movement of styles and survivability. and position of stigma and anthers are important for self-pollination besides the presence of effective 3.4. Passiflora Phenology pollinators. In its native habitat and most of other places of the world, the Passiflora species were self- Passiflora plant continuously grew and produced incompatible and carpenter bees were the effective flowers and fruits all year around. Throughout the year, pollinators’ that help in pollination. In the present study the vegetative growths were very vigorous during the site, there was good fruit sets, although there was rainy season. This showed the vines preferred moist lesser number of pollinators visiting the farm or soil to grow well. The flowering and fruiting were not sometimes absence. The pollinators observed were synchronized and showed a marked phenological few numbers of butterfly, wasps and bees and pattern with species (Figure 3). Different flowering carpenter bees. As the visitors landed on the flat peaks (major bloom) were observed in per year cycle, corona and feeding on , the upper part of the e.g., four peaks in P. edulis (Purple) observed in approaching pollinators came into contact with the January, April-May, July-September and November- lower exposed pollen bearing surface of the anther and December and followed by fruiting with two months some pollen grains deposited on their wings and after anthesis. In P. edulis (Purple) and P. edulis thorax, thus touched the stigma and transferred the (Frederick), high number of fruits was harvested prior pollen grains. The most common visitors were the ants to the rainy season with good quality during February- but they are nectar feeders and not the pollinators. March, June-July and September-October. The P. edulis species flowers bloom and fruiting all year round, In this sense, the studied species mostly exhibited a therefore it was common to find fruits in different unique autonomous self-pollination, involving the development stages in a vine in a year. The flowering movement of styles to lead the stigma faced the was continuous due to very little variation in the anthers during flower blooming which provided photoperiod and moderate temperatures. According to reproductive assurance to the species. The plants were Koehler-Santos et al. (2006), in such way, the self-compatible and able to produce constant fruit sets absorption of nutrients should be constant and this during the study period when biotic pollination is a makes the vines continuously bear fruits. limitation. This finding was supported by Shivanna [23], where the author carried out the detail study in India The phenological patterns of Passiflora species especially P. edulis (Purple) and P. edulis f. flavicarpa 6 Journal of Agriculture Food and Development, 2020, Vol. 6 Ramaiya et al.

Figure 3: Phenological pattern per year cycle in a) P. edulis (Purple), b) P. edulis (Frederick), c) P. maliformis and d) P. incarnata. and their climatic seasonality have been discussed by January). A shorter photoperiod and lower temperature other researchers from various geographical locations. during winter caused weak nutrient absorption and lead In the origin center and main producer (Brazil), e.g., in to low fruit sets. Jaboticabal and Botucatu (Southeast regions) the Passiflora flowers for 12 months a year with 2 flowering Other than Brazil, cultivated Passiflora species also peaks; first in January-February and the second is in grew and adapted well in a wide range of climatic September-October [24]. The preset observation was condition around the world. The authors Kishore et al. similar to their findings with additional peak observed in [16] from India (mean temperature of 28.5ºC, relative November-December. Besides, in State Sao Paulo, the humidity of 71.2% and annual rainfall of 2650 mm), blossom peaks were started at the middle of March revealed that P. edulis (Purple) had three major period continued until July [19]. Furthermore, Koehler-Santos of bloom in March-April, July-August and September- et al. [25] also reported similar pattern in North-East of October. The finding of Das et al. [20] from Bangladesh Brazil (Bahia), flower consistently seen in all the was similar with the present study where the effective months because of the less variability in the climate blooming occurred during April to August when the whereas in the Southeast (Rio Grande do Sul), the only temperature and humidity were relatively high. In the vegetative state was observed in 4 months, 2 in Indonesia Passiflora fruit is available all year round and winter (July-August) and 2 in summer (December- varied between each district; West Java- February to Floral Behaviour, Flowering Phenology and Fruit Production Journal of Agriculture Food and Development, 2020, Vol. 6 7

June; North Sumatra- August to December and South variable with species. Fruit maturity of a crop is Sulawesi- September and January to February. In influenced by genetic make-up, physiological condition Kenya, there were only two major peaks observed in of the specific crop as well as environmental factors July-August and December-January. In Florida such as rainfall, humidity, temperature, and day length (subtropical area), the P. edulis bear higher yield in late [20]. Results revealed that plants required 61.0±2.23 spring and early summer, then ceased flowering and days with minimum days of 58 from the flower anthesis bore no fruit in mid-summer and subsequently lower to full maturity in P. edulis (Purple). Similarly, about two yields in autumn [26]. The vine of P. maliformis bore months (63.6±2.40) required for P. edulis (Frederick) fruits almost throughout the year with no flowering ripening. The fruits of P. edulis (Purple) and P. edulis observed in January and October subsequent with (Frederick) matured and harvested after 228-234 and pruning. The main flowering period of this species 236-242 days whichwas about 8 months after occurred during the months of low precipitation and the transplanting. The fruits of P. maliformis took about percentage of individuals fruiting was high and the 65.2±2.68 days to ripen and harvesting period was fruits harvested mainly from June-July and October. 273-281 days after transplanting (9-10 months after Passiflora incarnata also flowering all year around with transplant). absence of flowering observed in June concurrent with pruning and initiation of new buds took longer period. Good fruit yields were observed throughout the year, attributed by Passiflora species being 3.5. Passiflora Fruit Development and Production successfully pollinated by pollinators and their ability for self-pollination. For the annual production per The data recorded on the fruit developing stages hectarethe higher numbers of fruits were harvested in and their behaviors are presented in Table 2. Fruiting P. edulis (Purple) of 119,174 fruits, followed by P. behaviors varied significantly between the studied edulis (Frederick) of 101,921 fruits, P. incarnata of species. The fruit developed from ovary was round to 85,108 fruits and the least was in P. maliformis of oblong in shape and showed marked variation in their 49,736 fruits. According to Kishore et al. [16] the size, weight and number of seeds per fruit. After the largest flower and fruit number were produced by P. anthesis, the ovary enlarged and the fruits developed. edulis as expected since this species had a more Simultaneously, seeds and pulp were developed. The intense selective breeding than any other of the studied days required for fruit ripening also varied between species. This study finding was also in agreement with species which approximately took 2 months after the total production recorded from various regions. In anthesis. Upon maturity the fruit rind colour changed Fiji, with hand pollination, 1 hectare yielded 433.52 kg and softened. The matured fruit varies in colour; P. of fruits monthly. On the average, P. edulis (Purple) in edulis (Purple) produced purple fruits, P. edulis Kenya yielded 9071.85-13,607.80 kg ha-1 year-1. A (Frederick) produced dark purple fruits, P. maliformis much higher yield is possible of 45,359.20 kg year-1 for produced yellow fruits, and P. incarnata produced P. edulis (Purple) has been reported in Kenya [14]. The green fruits.Fruit maturity of Passiflora was noticeable

Table 2: Fruiting Duration and Behaviors of Passiflora Species

Fruiting events P. edulis P. edulis P. maliformis P. (Purple) (Frederick) incarnata

Anthesis to ripening 61.0±2.23 63.6±2.40 65.2±2.68 44.2±4.55 (Days) (58-64) (61-67) (63-71) (42-48)

Fruiting after transplant (Days) 230.55±0.40 239.10±0.46 276.70±0.70 165.60±0.87 (228-234) (236-242) (273-284) (159-171)

Fruit length (cm) 7.48±0.96 5.44±0.51 4.28±0.52 2.79±0.32 (5.89-8.76) (4.56-6.14) (3.33-4.85) (1.85-3.14)

Fruit width (cm) 6.61±0.49 4.66±0.30 3.62±0.14 2.32±0.20 (5.56-7.53) (4.23-5.02) (3.43-3.94) (1.88-2.54)

Fruit weight (g) 98.53±28.91 44.72±8.45 33.58±5.29 2.12±0.49 (56.45-156.57) (27.57-63.05) (24.87-37.78) (1.43-2.95)

Values are given as means (hr) ± SD and values in parenthesis are the range. 8 Journal of Agriculture Food and Development, 2020, Vol. 6 Ramaiya et al. least yield was attained in P. maliformis in two characteristic associated to time of pollination in the yellow passion fruit Passiflora edulis Sims Degener (Passifloracea). subsequent years with fruits were half of the production Scientia Horticulturae 2004; 101: 373-385. of P. edulis (Purple). Lower fruit sets in P. maliformis https://doi.org/10.1016/j.scienta.2003.11.020 (1505.24 kg ha-1), due to the partially curved style with [9] Lim TK. 2012. Passiflora edulis. Edible Medicinal and Non- Medicinal Plants, pp 47-163. Springer Science, Germany. stigmas unable to completely touch by the anthers. https://doi.org/10.1007/978-94-007-4053-2 [10] Bruckner CH, CasaliVWD, MoraesCF, Regazzi AJand CONCLUSION SilvaEAM.Self-incompatibility in passion fruit (P. edulis Sims). Acta Horticulturae 1995; 370: 45-57. 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Received on 28-11-2019 Accepted on 05-01-2020 Published on 17-01-2020

DOI: https://doi.org/10.30635/2415-0142.2020.06.01

© 2020 Ramaiya et al.; Journal of Agriculture Food and Development. This is an open access article licensed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted, non-commercial use, distribution and reproduction in any medium, provided the work is properly cited.