the great loss of the juice's vitamin C after storage, high wage levels .... Anthesis occurred mainly at dawn, with 98% (nl ... Flowers lasted only one day; they had shed all petals and had .... when other pollen sources were not available during.
Journal of Agricultural Science, Cambridge (1999), 133, 303–311. Printed in the United Kingdom # 1999 Cambridge University Press
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Pollination requirements of West Indian cherry (Malpighia emarginata) and its putative pollinators, Centris bees, in NE Brazil B. M. F R E I T AS*, J. E. A L V ES, G. F. B R A N D A4 O Z. B. A R A U JO Departamento de Zootecnia – CCA, Universidade Federal do CearaT , CP 12168, Campus do Pici, CEP 60355-970, Fortaleza – CE, Brazil (Revised MS received 24 May 1999)
SUMMARY The pollination requirements of West Indian cherry (Malpighia emarginata DC) were investigated in NE Brazil through observations of flower morphology, floral rewards, anthesis, anther dehiscence, stigma receptivity, pollen cross and self-compatibility and proportion of fruit set. Potential insect pollinators and their foraging behaviour were also studied, and the pollination efficiency of the most frequent flower visitor, the bee Centris tarsata Smith (Anthophoridae), was assessed using single visits to flowers. It was shown that the West Indian cherry flower has a short lifespan, thus requiring pollination on the day of anthesis, when both cross- and self-pollen grains set fruit. The flower can potentially be pollinated by an array of insect visitors, but only oil-collecting bees of the genus Centris find it very attractive. Centris tarsata appeared as the main pollinator of West Indian cherry in the area studied, and farmers are advised to encourage its presence in orchards. Despite high levels of natural pollination, only 30 % of flowers set fruits. It is suggested that a high proportion of abnormal ovule development may be responsible for low fruit set where pollination is satisfactory, and that West Indian cherry varieties showing a lower percentage of such abnormalities should be selected for. I N T R O D U C T I ON Uncertainty about the West Indian cherry, Barbados cherry or acerola (Malpighia emarginata DC), a tree originating in tropical America which produces a fruit much like the European cherry (Prunus avium L.), begins with its scientific name. According to Ostendorf (1963), Linnaeus in 1753 identified the West Indian cherry as Malpighia glabra (Malpighiaceae) and later described another species, M. punicifolia, which differed from M. glabra in having only solitary flowers instead of an inflorescence. Such differences have been ignored and both names became synonyms of the West Indian cherry (Ostendorf 1963 ; IBPGR 1986). But because there are other similar species in the Caribbean and Mexico with edible fruits (e.g. Malpighia urens L., M. coccigera L., M. setosa Spreng., M. emarginata DC and M. mexicana A. Juss), much confusion has arisen. Recently, the International Board of Plant Genetic Resources (IBPGR) has stated that Malpighia emarginata is the
* To whom all correspondence should be addressed. Email : freitas!ufc.br
correct name for the West Indian cherry and has rejected the use of M. glabra as a synonym because their gynoecia are different to those of M. emarginata (IBPGR 1986). Despite this, M. glabra is still generally used (Free 1993 ; Carvalho et al. 1995 ; Lorenzon et al. 1995 ; Melo et al. 1997), but in this study we adopted the denomination recommended by the IBPGR. The West Indian cherry attracted worldwide attention when Asenjo & Guzman (1946) found high quantities of natural ascorbic acid in its fruits. The drupaceous fruit weighs from 2 to 10 g and contains between 900 and 3000 mg of ascorbic acid when ripe (Yamane & Nakasone 1961). This discovery awakened interest among scientists, fruit growers and industry and led to many studies between 1946 and 1965 on the fruit’s agricultural production and its nutritional value (Asenjo & Moscoso 1950 ; Moscoso 1956 ; Herna! ndez-Medina & Ve! lez-Santiago 1960 ; Garcia-Monge 1961). But due to a series of factors such as the acid taste of the fruit and its perishable nature that did not allow its commercialization for fresh consumption, the canning process of the fruit’s juice that led to rapid colour and flavour deterioration, the great loss of the juice’s vitamin C after storage, high wage levels and competition by cheap synthetic
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ascorbic acid (Ostendorf 1963), this crop was somewhat neglected after 1965, making its future exploitation doubtful. Recent technological and commercial developments that help to overcome these problems have rekindled interest in the West Indian cherry again. Renewed interest in West Indian cherry brought back an old problem : its low percentage of fruit set. Trees introduced to Hawaii in the 1950s showed extremely low fruit set (1n3–11n5 %) despite profuse flowering, and studies demonstrated that absence of pollination was a contributing factor to its poor fruit set (Yamane & Nakasone 1961 ; Miyashita et al. 1964). However, placing honeybee colonies in orchards did not help to increase fruit set (Yamane & Nakasone 1961). Pollination was therefore another puzzling aspect about the West Indian cherry ; little was understood of its pollination requirements (McGregor 1976). Only after Raw (1979) has shown that trees in Jamaica set many fruits after visits of an anthophorid bee, Centris dirrhoda, to its flower, has pollination in West Indian cherry been clarified. Apparently, instead of nectar, flowers of the West Indian cherry produce oils in glands of their calyx which are collected by females of Centris spp. using specialized clumps of spatulate hairs situated in their forelegs (Raw 1979). The availability of Centris bees in orchards is now considered the main factor limiting production of West Indian cherry (IBPGR 1986) and Free (1993) suggested that the importation of Centris bees to Hawaii should be considered. However, the proportion of initial fruit set and the pollination efficiency of floral visitors to West Indian cherry is still unknown. Even in orchards where Centris bees are present in abundance, it was estimated that initial fruit set was rarely 50 % (Raw 1979). Since there is a lack of information on the pollination requirements of West Indian cherry and pollination efficiency of its flower visitors, more investigation in this area could help to explain such a low fruit set. Thus, in this study we covered aspects of the floral and pollination biology of M. emarginata, its flower visitors and their foraging behaviour and the pollination efficiency of C. tarsata in NE Brazil, where the West Indian cherry has become an important crop in recent years (Carvalho et al. 1995).
M A T E R I A L S A N D M E T H O DS The flower and pollination biology and potential pollinators of M. emarginata were studied during 1996 and 1997 in an orchard comprising 24 trees in Fortaleza (3m43hS, 38m32hW, 15n49 m above sea level), Ceara! , Brazil. The climate is dry\subhumid with an average annual precipitation of 1378 mm, relative humidity of 79 % and average minimum and maxi-
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mum temperatures of 24n3 and 30n4 mC, respectively (IPLANCE 1993). Flower biology Flower buds were marked at random and observations made of 64 flowers after they opened. Flower structure, coloration, lifespan, time of anthesis and pollen, nectar and oil presentation were investigated by careful observations of flowers at each hour during their lives. Nectar production was checked on the day of anthesis by sampling flowers with 1 µl micropipettes every 3 h from the time flowers first opened to dusk. In order to investigate changes in stigma receptivity, 192 flowers chosen at random among West Indian cherry trees were covered with fine nylon and muslin bags before they opened and split into six groups of 32 flowers from different trees. Then each group of 32 flowers was hand-pollinated with pollen collected from other trees at 0, 2, 4, 6, 8 or 10 h after anthesis. Pollen was obtained from flowers collected early in the morning and whose anthers were allowed to dehisce in Petri dishes at 28 mC. Some flowers were kept at 20 mC to delay anther dehiscence and produce fresh pollen for hand pollination carried out in the afternoons. After hand pollination, the flowers were rebagged and fruit set checked 7 days later before fruit drop due to physiological stress or pest damage. Pollination biology To determine the importance of the wind in promoting pollination of West Indian cherry flowers, 200 flowers were chosen at random in 24 trees. Of these 100 flowers were marked and bagged with fine nylon and muslin bags (1i1 mm mesh) to prevent access by all but the smallest insects from the day before they opened until 17.00 h of the following day. The remaining 100 flowers were also marked but left unbagged until 17.00 h of the day they opened. At that time, all flowers were carefully collected and the number of West Indian cherry pollen grains found on their stigmas was counted under an optical stereoscopic microscope PZO-Labimex at a magnification ofi40. To assess the compatibility of self- and cross-pollen grains, 120 flowers were chosen at random from the 24 trees. Then 30 of them were hand-pollinated with self-pollen once with a fine paint brush after they opened. Another 30 flowers were also hand-pollinated in the same manner, but using cross-pollen. The cross-pollen was obtained following the same procedure described above to assess changes in stigma receptivity. Self-pollen was transferred directly from dehisced anthers to stigmas. After hand pollination, the flowers were rebagged and observed 7 days later to determine fruit set. The remaining 60 flowers were either bagged to exclude insect visitation and not
Pollination requirements of West Indian cherry hand-pollinated (n l 30 flowers) or simply tagged and left unbagged (n l 30 flowers) to evaluate the natural open-pollination in the orchard. Flower visitors and their foraging behaviour Observations of floral visitors to West Indian cherry flowers were taken from 6.00 to 17.30 h from 24 different trees, for five consecutive days when the trees were in bloom. The frequency of the floral visitors to the flowers was determined by walking between all trees of the orchard at every hour and sampling flowers at random to check for the presence of visitors. The ‘ peak of abundance ’ within a day was defined as the time between which the majority ( 75 %) of observations of a floral visitor species was recorded (Freitas & Paxton 1996). The presence and identity of floral visitors was recorded, as was their behaviour on the flowers, whether they collected pollen or oil, and whether they touched the reproductive organs of the flowers. Specimens of all common flower visitors present in the orchard were collected for identification. Pollination efficiency of C. tarsata The pollination efficiency of C. tarsata, the most common potential pollinator of West Indian cherry, was evaluated by enclosing 90 flowers selected at random and yet to open in fine nylon and muslin bags. Thirty of these 90 flowers were kept bagged throughout their lives to prevent insect visitation. The other 60 flowers were released from their bags soon after anthesis and carefully observed until a C. tarsata bee visited them. Immediately after the first bee visit to a virgin flower, the flower was labelled and rebagged to prevent further visitation. This procedure was repeated until 30 flowers had been visited once by a C. tarsata bee. The remaining 30 flowers were simply labelled and left unbagged, exposed to unrestricted insect visitation.
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R E S U L TS Flower biology West Indian cherry flowers are 2n0–2n5 cm in diameter and produced in clusters of two to six in the axils of the leaves on lateral spurs. The flower is hermaphrodite and has five green sepals, five pink petals, 6–10 large sessile oil-producing glands (epithelial elaiophores) in the calyx, ten erect stamens united below, three styles reaching the same height as the stamens and a three-carpel superior ovary bearing one single ovule per locule (Fig. 1). No nectar was obtained from the flowers and, despite the lack of free-flowing oils in the flowers, the presence of epithelial elaiophores and the foraging behaviour of flower visitors (see flower visitors and their foraging behaviour) suggests M. emarginata produced oil as a reward for flower visitors, as proposed by Raw (1979). Anthesis occurred mainly at dawn, with 98 % (n l 63) of flowers starting to open between 4.00 and 5.00 h and only 1 % of them opening between 5.00 and 8.00 h (n l 1). Anther dehiscence started at 6.00 h and continued throughout the day, with most (72 %) occurring between 7.00 and 10.00 h (Table 1). Some flowers (12n5 %) never released pollen (Table 1). Flowers lasted only one day ; they had shed all petals and had shrivelled stamens by next morning. Stigmas were already receptive at 6.00 h when anthers started to dehisce to release fresh pollen. There were significant differences in the number of flowers that set fruits after hand-pollination of different-aged stigmas (G# l 76n143, .. l 5, P 0n001). Fruit set achieved a maximum value of ten fruits (31 %) set from 32 flowers when handpollination was carried out between 6.00 and 7.00 h, and differed significantly to hand-pollination made Petals
Statistical analysis Means and standard errors were calculated for data assessing the time spent by C. tarsata and Centris aenea in West Indian cherry flowers and means were tested by ANOVA. Due to the binomial character of data obtained for stigma receptivity, pollen compatibility and pollination efficiency of C. tarsata experiments (fruit set or not set), data were analysed using G-tests (Sokal & Rohlf 1981) and means were compared by a Simultaneous Test Procedure (STP), as suggested by Sokal & Rohlf (1981). Data on the number of pollen grains found on stigmas of bagged and unbagged West Indian cherry flowers also did not conform to ANOVA assumptions and were analysed using a Mann–Whitney U test.
Anthers Oil glands
Stigmas
Fig. 1. Schematic drawing of a West Indian cherry flower.
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Table 1. Number and proportion of West Indian cherry (Malpighia emarginata) flowers with anthers dehisced or not dehisced at different times of the day (n l 64) Time of day (h)
Number of flowers with anthers dehisced
Flowers (%) with anthers dehisced
Number of flowers with anthers not dehisced
Flowers (%) with anthers not dehisced
04.00–05.00 05.00–06.00 06.00–07.00 07.00–08.00 08.00–09.00 09.00–10.00 10.00–11.00 11.00–12.00 12.00–13.00 13.00–14.00 14.00–15.00 15.00–16.00 Total
0 0 9 11 14 12 6 1 1 1 1 0 56
0 0 14n2 17n2 21n9 18n8 9n4 1n5 1n5 1n5 1n5 0 87n5
64 64 55 44 30 18 12 11 10 9 8 8 8
100n0 100n0 85n9 68n7 46n8 28n1 18n7 17n1 15n6 14n0 12n5 12n5 12n5
Table 2. Stigma receptivity of West Indian cherry (Malpighia emarginata) flowers to hand-pollinated cross-pollen at different times after flower anthesis
Time of day (h)
Number of flowers hand pollinated
Number of flowers set
Flowers set (%)
06.00–07.00 08.00–09.00 10.00–11.00 12.00–13.00 14.00–15.00 16.00–17.00
32 28 29 30 30 29
10 4 6 8 8 1
31n2 14n3 20n7 26n7 26n7 3n4
between 16.00 and 17.00 h when only one fruit (3 %) was set from 29 flowers (Table 2). The other treatment means did not differ significantly from each other (Table 2), suggesting that stigmas were equally receptive from anthesis to 15.00 h, but receptivity decreased thereafter. Pollination biology There was a significant difference between the number of M. emarginata pollen grains found on stigmas of bagged and unbagged flowers (U l 156n6, P 0n001). Unbagged flowers (n l 100) had 18n9p1n32 (range 1–54) pollen grains in all three stigmas per flower, while only 0n8p0n18 (range 0–15) pollen grains were found on the stigmas of bagged flowers (n l 100). All unbagged flowers examined bore pollen grains on their stigmas while only 31 % of bagged flowers bore any pollen grains. It seems that flowers auto-pollinate poorly, and the wind plays little or no role in the pollination of West Indian cherry flowers. There were significant differences in the number of
fruits set between treatments when flowers were bagged to exclude insects, open-pollinated, bagged but self-pollinated by hand and bagged but crosspollinated by hand (G# l 66n081, .. l 3, P 0n001 ; Table 3). The number of fruits set after openpollination or cross-pollination was significantly greater than the number of fruits set when flowers were bagged to exclude insects, but they did not differ from the number of fruits set by flowers bagged and self-pollinated. The latter also did not differ from flowers from which floral visitors were excluded (Table 3). The results suggest that pollination in West Indian cherry is carried out by floral visitors, and probably more than one visit is needed to achieve optimal fruit set. Both hand cross and self-pollination can lead to fruit set of West Indian cherry flowers. Flower visitors and their foraging behaviour Only few insect species were observed visiting West Indian cherry flowers. Centris tarsata was the most common potential pollinator (33 % of all visits), being
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Pollination requirements of West Indian cherry
Table 3. Fruit set of West Indian cherry (Malpighia emarginata) flowers that were bagged to exclude insect visits, left unbagged and open-pollinated or pollinated by hand (self- or cross-) and then bagged. Sample sizes are 30 in some cases due to loss of flowers following experimental manipulation
Treatment of flower Insects excluded Open-pollinated Self-pollinated Cross-pollinated
Number of flowers tagged
Number of fruits set
Flowers that set fruits (%)
30 30 29 21
0 9 5 5
0 30n0 17n3 23n8
Anthers Petals
Oil glands
Stigmas
Fig. 2. Schematic drawing of a female Centris tarsata collecting oils from a West Indian cherry flower. Note that the ventral parts of the bee touch the flower’s reproductive organs.
present in the orchard between 7.00 and 15.00 h, with a peak between 9.00 and 12.00 h. This fast-flying bee species visited a few flowers per tree, and preferred to visit exposed flowers on the outside of the tree’s canopy, though it was also seen visiting flowers inside the tree’s canopy. The bee grasped a flower with its midlegs, kept a foothold with the rear pair of legs, and quickly collected oils from the flower’s elaiophores with fast movements of the forelegs (Fig. 2). Pollencollecting visits were also observed by C. tarsata, with bees performing characteristic anther-scrambling movements. Centris tarsata’s visits to West Indian cherry flowers were timed as lasting 3n0p0n1 seconds (n l 95 visits), with no distinction being made between oil- and pollen-collecting visits. The bee’s body positioning during flower visits, either to collect pollen or oils, led to it contacting anthers and stigmas and to pollen adhering to its ventral side. Regular
movements of bees between trees may have favoured cross pollination. Centris aenea Lepeletier was the second most common flower visitor to M. emarginata flowers (11 %), but much less abundant than C. tarsata. Centris aenea was observed in the orchard collecting oils and pollen, mainly between 6.00 and 12.00 h, with a peak of abundance from 6.00 to 9.00 h. Its visits were concentrated in flowers found inside the tree’s canopy, and were quick (0n7p0n1 s, n l 15 visits). Centris aenea spent significantly (F , l 72n136, .. " "!* l 1, P 0n001) less time per flower visit than C. tarsata. Few flowers were visited per tree by C. aenea and its foraging behaviour seemed to be conducive to cross pollination since the bee contacted both anthers and stigmas of the flowers, though their low frequency at flowers did not allow assessment of their pollination efficiency. Apis mellifera were seen only occasionally (8 % of all visitors) visiting West Indian cherry flowers. Visits were mainly during the morning and always for pollen, since M. emarginata flowers do not produce nectar. We observed that honeybees preferred to visit flowers of other plant species, even for pollen collection, and only visited West Indian cherry flowers when other pollen sources were not available during that period of the year or time of the day. In this case, honeybees showed their characteristic scrabble movements of pollen collection at M. emarginata flowers and may have touched the reproductive organs of the flowers in doing so. No pollination efficiency trial was carried out for A. mellifera due to the scarcity of foragers visiting West Indian cherry flowers. Carpenter bees (Xylocopa frontalis) also visited West Indian cherry flowers. However, this bee species was observed only sporadically (2 % of all visitors), and on many days no visits were recorded. All visits of X. frontalis to M. emarginata flowers happened in the morning, and only for pollen. The bee hung heavily on the flower and actively buzzed, removing most of the flower’s pollen. Despite its pollen removal success, X. frontalis usually visited only a few flowers situated at the top of the tree’s canopy before leaving the orchard.
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E T A L.
Table 4. Number and proportion of fruits set per West Indian cherry (Malpighia emarginata) flower allowed no insect visits, a single visit by Centris tarsata or unrestricted visits
Treatment of flower
Number of flowers tagged
Number of fruits set
Flowers that set fruits (%)
30 30 30
0 2 9
0 6n7 30n0
No visit One visit by C. tarsata Unrestricted visits
The most common visitor of West Indian cherry flowers was the stingless bee Trigona spinipes (53 % of all visitors). However, this bee restricted its floral visits to resin and oil collection from the receptacle of old flowers whose petals had already fallen. It never contacted the flower’s stamens or stigmas. Thus, despite being the most common flower visitor, it cannot be considered to be a potential pollinator of West Indian cherry flowers. Other common flower visiting insects such as butterflies and flies were also observed in the orchard, but they rarely visited West Indian cherry flowers and then did not show a behaviour that would favour contact with stamens and stigmas. Besides, their numbers were very small. Pollination efficiency of C. tarsata The number of fruits set following no insect visits, unrestricted visitation and single visits by C. tarsata to West Indian cherry flowers differed significantly (G# l 63n911, .. l 2, P 0n001). The number of fruits set after open-pollination was significantly greater than the number of fruits set by flowers that received no visits, but fruit set by single visits of C. tarsata did not differ from both fruit set of openpollinated and flowers bagged to exclude insects (Table 4). Apparently C. tarsata can pollinate West Indian cherry flowers, but more than one visit per flower is necessary for a high fruit set to be achieved. D I S C U S S I ON Pollination biology The West Indian cherry showed a well-defined pollination process. Its flowers lasted only one day, with anthesis and pollen dehiscence occurring early in the morning, the stigmas being receptive at anthesis and for most of the day but losing receptivity towards the evening. Wind played no role in the pollination process and insect floral visitors were necessary to set fruits, agreeing with Yamane & Nakasone (1961) and Raw (1979). No nectar was secreted and fatty oils produced in the epithelial elaiophores seemed to be the primary floral rewards since pollen collecting was mainly performed by bees that also collected oils from
the flowers. Honeybees and other non-oil-collecting bees only sporadically collected pollen from M. emarginata. In our study we observed that anthers of 12n5 % of the flowers failed to dehisce. Yamane & Nakasone (1961) and Miyashita et al. (1964) also found similar results in some clones which only released pollen in the afternoon or failed to dehisce. Failure in anther dehiscence of West Indian cherry seems to be a genetic characteristic which may have important implications for pollen dispersal and a flower’s male reproductive success (see Harder & Thomson 1989 ; Thomson & Thomson 1989 ; Young & Stanton 1990). Furthermore, pollen grains germinate very well on the day of anthesis but were almost entirely non-viable on the following day (Yamane & Nakasone 1961 ; Miyashita et al. 1964). Therefore, successful pollination of West Indian cherry flowers must take place within the day of a flower’s anthesis, pollinators must be able to transfer pollen between flowers if pollination of flowers with non-dehiscent anthers is to be accomplished, and pollinators must be present in the orchard in sufficient numbers to ensure that most flowers are effectively pollinated. In NE Brazil, pollination of the West Indian cherry was mediated by insects, particularly bees of the genus Centris. This has been suggested already by other authors who observed various Centris species visiting West Indian cherry flowers in the region (Carvalho et al. 1995 ; Lorenzon et al. 1995 ; Melo et al. 1997). According to Simpson et al. (1990), pollination of oil-secreting plants of all families of the New World, except the Primulaceae, is related to pollination by exomalopsine (Hymenoptera, Anthophoridae) and centridine bees. Besides, Raw (1979) explains that both the Malpighiaceae and oilcollecting anthophorid bees are almost entirely confined to the neotropics. Centridini bees in general are restricted to the tropical and subtropical Americas (Kerr & Maule 1964). This could help to explain the poor fruit set of West Indian cherry flowers observed in Hawaii by Yamane & Nakasone (1961). But even with a large number of insect visits to flowers, only 30 % of West Indian cherry flowers set fruits in our experiment, while Raw (1979) estimated that 50 % of open-pollinated flowers in Jamaica set fruits. Hand pollination with cross-pollen did not
Pollination requirements of West Indian cherry improve fruit set in Brazil (31 %) but increased it (to 52 %) significantly in Hawaii where flower-visiting insects were rare (Yamane & Nakasone 1961). The IBPGR (1986) reports self-incompatibility in cultivars of West Indian cherry, but the trees studied by us and in Hawaii set fruits when self-pollinated, though in smaller numbers than when open or cross-pollinated. Since the low fruit set of 50 % or less cannot be explained solely by self-incompatibility, other causes must be sought. Miyashita et al. (1964) observed abnormal development in a large proportion of ovules of West Indian cherry flowers. In 33 % of ovules, the nucellar beak began disintegrating on the day of anthesis, before fertilization, and 3 days later the nucellar cells were almost completely disintegrated, leading to abortion of the embryo sac (Miyashita et al. 1964). Another abnormality reported by Miyashita et al. (1964) was the differentiation of two ovules in some locules (up to 50 % of locules, depending on the clone studied) early in floral development, with subsequent ovule abortion and collapse. Both factors can contribute to low seed and fruit set in West Indian cherry and may explain why only 30 % of flowers open to unrestricted insect visits set fruits. West Indian cherry varieties with a lower proportion of abnormal ovule development should be selected in order to improve fruit set. In contrast, Miyashita et al. (1964) have also described occasional cases of parthenocarpy in West Indian cherry. They also noticed germination and pollen tube growth within an undehisced anther at flower anthesis. According to Anderson (1980), four genera of Malpighiaceae (Aspicarpa, Camarea, Janusia and Gaudichaudia) have cleistogamous flowers (i.e. small flowers that never open) with cryptic selffertilization. In such a situation, pollen grains germinate inside the undehiscent anther and pollen tubes grow down through the anther’s filament to fertilize the ovules in the ovary, producing normal viable seeds. Although the West Indian cherry does not produce cleistogamous flowers, it may be possible that fruit set in chasmogamous (normal) flowers not receiving pollination are due to cryptic selffertilization instead of parthenocarpy. This is yet to be shown, but previous observations of failure in anther dehiscence and pollen germination within undehisced anthers (Yamane & Nakasone 1961 ; Miyashita et al. 1964) warrant further studies of parthenocarpy and cryptic self-fertilization in West Indian cherry. Flower visitors and their foraging behaviour Few insect species visited West Indian cherry flowers. Despite the fact that all flower-visiting species, except Trigona spinipes, showed foraging behaviour conducive to successful pollination of flowers, only bees
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of the genus Centris, especially C. tarsata, were attracted to the orchard in sufficient number to ensure satisfactory pollination. Centris bees are common visitors of West Indian cherry flowers, and reports of visits by C. dirrhoda, C. fuscata, C. aenea, C. spousa, C. spilopoda and C. bicolor to M. emarginata can be found in the literature (Raw 1979 ; Carvalho et al. 1995 ; Melo et al. 1997). This is the first report of C. tarsata visiting West Indian cherry flowers. Other M. emarginata flower visitors in this study, such as A. mellifera and X. frontalis, only visited a few flowers and their contribution to pollination of the West Indian cherry seems to be small and unreliable. Apis mellifera has been cited as an occasional flower visitor of West Indian cherry in other studies (Yamane & Nakasone 1961 ; Melo et al. 1997), but we found no such reports for Xylocopa bees. The most common flower visitor in the orchard, T. spinipes, collected resins and oils from the receptacles of old West Indian cherry flowers, probably for nest construction, and so this species cannot be considered a pollinator. Some meliponin (Apidae) bee species, including T. spinipes, have been implicated as pollinators of M. emarginata (Lorenzon et al. 1995 ; Melo et al. 1997). But according to Simpson et al. (1990), stingless bees rarely serve as pollinators to the oil flowers they visit. Other insect species mentioned as visiting West Indian cherry flowers, such as halictidine bees and syrphid flies (Yamane & Nakasone 1961 ; Carvalho et al. 1995 ; Melo et al. 1997), were not observed in the present study. Pollination efficiency of C. tarsata The efficiency of C. tarsata in pollinating cashew (Anacardium occidentale L.) has already been demonstrated (Freitas 1997 a, b ; Freitas & Paxton, 1998), and there is evidence that it may be the main pollinator of Byrsonima verbascifolia Rich, a bush of the Malpighiaceae family indigenous to the coastal areas of NE Brazil which has oil-secreting flowers and produces edible fruits (Freitas et al., unpublished data). In West Indian cherry, however, the pollination efficiency of flower visitors had not been investigated before, and C. tarsata had never been suggested as its pollinator. The foraging behaviour of C. tarsata seems to be appropriate for it to pollinate West Indian cherry flowers due to its body positioning on the flower and timing of its visits with anther dehiscence and stigma receptivity. It also seems to promote cross-pollination due to its constant movement between trees, which may increase fruit set, and fast visits (3n0 s per visit) that allows many flowers to be visited per minute (19n7 visits\min). Raw (1979) observed that Centris dirrhoda females were even faster, visiting between 26n0 and 41n8 flowers per minute, depending on
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whether the bee was collecting pollen or oils, respectively. Measurements of pollination efficiency using single visits by C. tarsata showed that it can set West Indian cherry fruits, but the low number of fruits set following single visits suggests that more than one visit per flower is necessary to maximize fruit set. The need for many visits per flower to achieve high seed and fruit set has been observed in other plant-pollinator systems (see Herrera 1987 ; Freitas & Paxton 1998). The number of bees in the orchard studied implicates this bee species as the main pollinator of West Indian cherry. But their numbers varied considerably in 1996 and 1997 and this may have affected the number of visits each flower received and, consequently, total fruit set. Besides, possibilities of seasonal changes in the size of natural populations of C. tarsata in the vicinity of the orchard and competition by other plant species for pollinator attention should be considered
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since C. tarsata was also observed foraging on other plant species. West Indian cherry growers in NE Brazil should provide nesting facilities, remove pollination-competing plant species and control insecticide applications to stimulate intensive foraging by C. tarsata on their orchards, because flowers need to be visited more than once to ensure good fruit set and a great proportion of flowers have abortive ovules that will never develop into mature seeds even after the flower has been pollinated. The authors thank D. G. F. Freitas for the drawings, J. E. Pinheiro Jr. for helping with data collection, F. Silveira for the identification of C. aenea, R. J. Paxton for valuable discussion and commenting on the manuscript and CNPq-Brasilia\ Brazil for a research grant to B. M. Freitas, sponsorships to J. E. Alves and G. F. Branda4 o, and financial support to the project (T521946\96-4 SU).
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