Annu. Rev. Entomol. 1999. 44:183206 Copyright c 1999 by Annual Reviews.

All rights reserved

THE ROLE OF STINGLESS BEES IN CROP POLLINATION

Tim A. Heard
CSIRO Entomology, PMB 3 Indooroopilly 4068, Australia; e-mail: tim.heard@brs.ento.csiro.au
KEY WORDS: Apidae, Meliponini, oral biology, alternative pollinators, entomophily

ABSTRACT
Stingless bees (Apidae: Meliponini) are common visitors to owering plants in the tropics, but evidence for their importance and effectiveness as crop pollinators is lacking for most plant species. They are known to visit the owers of 90 crop species. They were conrmed to be effective and important pollinators of 9 species. They may make a contribution to the pollination of 60 other species, but there is insufcient information to determine their overall effectiveness or importance. They have been recorded from another 20 crops, but other evidence suggests that they do not have an important role because these plants are pollinated by other means. The strengths and limitations of stingless bees as crop pollinators are discussed. Aspects of their biology that impact on their potential for crop pollination are reviewed, including generalized ower visiting behavior of colonies, oral constancy of individual bees, ight range, and the importance of natural vegetation for maintaining local populations.

INTRODUCTION
Stingless bees are a group of small- to medium-sized bees, with vestigial stings, found in tropical and many subtropical parts of the world. They are the major visitors of many owering plants in the tropics. They show a level of social organization comparable to that of honey bees (131). Colonies are perennial and usually consist of hundreds or thousands of workers (160). The estimated several hundred species of stingless bees are arranged into 21 genera (79). The rank of the group has varied but recently has been placed at tribe (122). The most important genera are Melipona and Trigona. Melipona 183 0066-4170/99/0101-0183$08.00

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consists of 50 species, is conned to the neotropics, has more complex communication systems (88), and is capable of buzz pollination (i.e. ejecting pollen grains by vibration of the pollen-bearing anthers of owers that dehisce pollen through pores) (24). Trigona is the largest and most widely distributed genus, with 130 species in 10 subgenera, including the neotropical Trigona sensu stricto and most of the Asian Meliponini. It is often stated that stingless bees are important pollinators of crops in tropical and subtropical parts of the world (29, 37, 77, 78, 158). The evidence for these assertions has never been reviewed. Reviews on the role of non-Apis bees in crop pollination mention stingless bees either briey (19, 93, 97) or not at all (121, 147). Books on crop pollination by insects treat the topic in a little more detail (37, 77, 125). This neglect probably reects a lack of knowledge rather than a lack of importance. The use and management of non-Apis bees and other insects for crop pollination is important because of the almost total reliance of world agriculture on honey bees. In many locations and for many crops, the ability of honey bees to pollinate is threatened or limited because of factors such as Africanization, diseases and parasites, low efciency on some crop species, climatic limitations, and economic pressures (93).

STRENGTHS AND LIMITATIONS OF STINGLESS BEES FOR CROP POLLINATION

Many characteristics of stingless bees resemble those of honey bees. Some of the characteristics that inuence their ability as pollinators are (a) polylecty and adaptability, which enable them to pollinate multiple plant species and adapt to new ones (see below for references); (b) oral constancy: A worker on a trip usually visits only one plant species (108); (c) domestication: Colonies can be placed in hives, inspected, propagated, fed, requeened, controlled for enemies, transported, and otherwise managed (91); (d ) perennial colonies, which allow workers to forage continuously within climatic constraints and obviate the need to develop colonies each year; (e) large food reserves are stored in nests: This has the obvious benet of allowing colonies to survive long periods of low food availability. Additionally, it means that workers will collect oral resources beyond immediate needs, resulting in intensive visitation of preferred owers (129); ( f ) possibility of in-hive pollen transfer, decreasing the need for bee movement between plants of self-incompatible species: This has been found for honey bees (30) and is equally likely for stingless bees; (g) forager recruitment: Workers recruit nest mates to rewarding oral resources and provide information on the position of those oral resources, which allows the rapid deployment of large numbers of foragers (88) relative to other bees and insects in which each individual has to nd the resource.

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Unlike honey bees, stingless bees have the following advantages: They are generally less harmful to humans and domesticated animals; they are able to forage effectively in glasshouses (63); propagation of colonies contributes to preservation of biodiversity by conserving populations of species that may otherwise decline owing to human disruption of ecosystems; colonies are rarely able to abscond, as the old queen is ightless (57); and they are resistant to the diseases and parasites of honey bees (31). Thus a honey bee epizootic that disrupted pollination would not effect the stingless bees in that system. Disadvantages of stingless bees for crop pollination include the following: There is a poor level of domestication technology for most species; there is a lack of availability of large numbers of hives; colony growth rates are low compared with honey bees; some species are unable to be domesticated because of specic nesting requirements; some species damage leaves in search of resin (25, 158); and some species are territorial and ght when placed in close proximity.

ASPECTS OF THE BIOLOGY OF STINGLESS BEES RELEVANT TO POLLINATION

The biology of the stingless bees has been reviewed (78, 124, 130, 160) but never from the perspective of crop pollination. Aspects of the foraging biology of stingless bees that are pertinent to this topic are reviewed here. Several other relevant topics including foraging syndromes, navigation, forager recruitment, response to weather, oral larceny, and diet and seasonal patterns of activity are reviewed by Roubik (124). Stingless bees are generalist ower visitors. All studied species visit a broad range of plant species. For example, Hypotrigona pothieri used 54 species in 28 families (69), Melipona marginata used 173 species in 38 families (67), and Melipona favosa visited 38 species in 26 families (34). The number of plant species visited for nectar may be higher than the number visited for pollen (67, 109). Despite their generalized ower selection, all examined species show preferences (67, 69, 109, 128). Stingless bees are adaptable, rapidly learning to exploit the resources offered by introduced plants. For example, neotropical stingless bees heavily use the introduced Eucalyptus spp. (43, 67). Few generalizations can be made regarding the plant or ower type preferred by stingless bees, but it has been suggested they prefer small owers (161), dense inorescences (128), owers with corolla tubes shorter than the bees tongues (50), owers with long corolla tubes that are wide enough for the bees to enter (34), trees (67, 109, 110), and white or yellow owers (27). Floral constancy, in which a worker visits only one plant species on a single trip, is typical of many polyphagous bees (33). In Brazil, 97% of the pollen foragers of nine species of stingless bees visited only one oral resource on each trip, as evidenced by the pure pollen loads in their corbiculae (108). Floral

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constancy is associated with pollinator effectiveness, as collection and deposition of pollen from two or more species reduces the amount of pollen available and contaminates stigmas with the wrong pollen. In addition to oral species constancy, foragers normally show resource constancy to either nectar, pollen, or resin within a single trip and usually between successive trips (58, 141). In addition to records of use of many plants by stingless bees, they have been shown to be important pollinators of noncrop species in natural habitats. Examples of these studies were conducted at the community and individual species levels. Of 41 plant species investigated in the forest understory in Sarawak, 9 were pollinated by stingless bees (64). In the lowland neotropics, all of the 52 species visited by Melipona and 108 of the 128 species visited by other stingless bee species may have beneted directly from pollination services of these bees (123). At the species level, stingless bees are the conrmed pollinators of many plants on the basis of experimentation or observation. Trigona spp. were the most abundant and effective pollinators of the androdioecious Xerospermum intermedium growing in the understory of Malaysian rainforests (8). Another sapindaceous rainforest understory tree in Costa Rica, Cupania guatemalensis, is also pollinated by Trigona spp. (14). Trigona bees were shown to be effective pollinators of Spathiphyllum friedrichsthalii (83). Of the 13 Australian epiphytic orchids whose pollinators are conrmed, 9 are pollinated by stingless bees (3). Partamona grandipennis pollinates the monoecious herb Begonia involucra in Costa Rica (5). Trigona spinipes pollinates Nymphaea ampla in Brazil (103), and Trigona sp. pollinates Ondinea purpurea in Australia (133). Illegitimate use of owers by stingless bees in which they remove resources without pollinating, with or without damaging the owers, occurs in both natural habitats (124) and agroecosystems (4, 132). Although many species of stingless bees adapt to articial nest sites, natural vegetation can inuence abundance of stingless bees. Abundance of Trigona carbonaria in orchards of macadamia is correlated with extent of surrounding natural eucalyptus vegetation (48). All surveyed chayote elds in Costa Rica had Trigona bees present, except for two elds with no surrounding forest for 1 km (161). The abundance of Trigona bees on longan owers in a large orchard was found to decrease with distance from an adjoining forest (20). Stingless bees were common visitors to owers of cupua u growing near primary forest c in Amazonian Brazil but were absent in disturbed habitats, which suggests that bee populations are dependent on the primary forest (153). Flight range is a function of worker bee size (78, 89) and possibly also colony population size (141). The actual foraging distance also depends on the attractiveness of the resource in relation to distance from the nest, needs of the colony, and availability of alternative resources. Using a mark-release technique, the maximum ight range of Cephalotrigona capitata and Melipona panamica in tropical forest was estimated to be 1.5 and 2.1 km, respectively (127). Captured

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workers of Melipona fuliginosa returned when released from distances of 2 km from their nests (159). By training workers to an articial nectar source and progressively moving the source away from the hive, the maximum ight range of Plebeia mosquito, Trigona rucrus, and Trigona amalthea was 540, 840, and 980 m, respectively (65). Using a similar technique, the maximum ight range of four species of stingless bees was from 120 to 680 m and was closely correlated with head capsule width (151a). Using the calculated ight speed, the actual ight distances (rather than the maximum range) of Trigona minangkabau was estimated to be between 84 and 434 m (58). Most of the nectar and pollen in the reserves of colonies of Plebeia remota came from plants growing within 100 m of their colonies (109). Trigona erythrogaster foraged on oil palms in a plantation 1.1 km from the forest they inhabited (8). The abundance of Trigona sp. in a longan orchard in northern Thailand was high at distances of 50 and 200 m from adjoining forest but decreased greatly at 2.5 and 4 km from the forest (20). The ight activity of colonies of stingless bees depends on species, population of colonies, and availability of resources. The estimated 10,000 workers of a hive of T. carbonaria made about 20,000 ights per day (49). Colonies of Trigona itami, Trigona moorei, and T. minangkabau with populations of 5000, 2000, and 2600 made about 7000, 2400, and 1200 ights per day, respectively (58). A newly established hive of T. minangkabau with only 350 workers made only about 700 ights per day, showing the strong positive relationship between hive population and ight activity (63). The ability of guards at the hive entrance to recognize nestmates and eject non-nestmates is relevant to a situation where hives may be maintained at high densities for crop pollination. T. minangkabau shows a very well-developed ability to do this (144). Workers of Melipona quadrifasciata, Melipona ruventris, and Melipona scutellaris attacked 74, 60, and 14% of non-nestmate conspecics encountered (23). The potential of stingless bees for crop pollination is enhanced by the ability to transfer colonies into articial hives. These hives can be propagated (45, 91, 125) so that growers do not need to rely on natural populations. Hives can also be transported where needed for pollination or for hive strengthening. Hives may be opened for extraction of honey, inspection, feeding, or requeening if necessary and for treatment against natural enemies. The history of traditional stingless beekeeping was reviewed recently (29).

CROP POLLINATION
More than 1000 plant species are cultivated in the tropics for food, beverages, ber, spices, and medicines (104, 105, 118, 125). The breeding system and pollinators of many of these crops have been catalogued (37, 125). Nearly half of

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the species of economically signicant tropical crops originated in areas where honey bee species do not occur naturally, i.e. the neotropics, South Pacic, and Australia. Approximately half of these plants are pollinated by bees (125). Many of these 250 species may be adapted to pollination by stingless bees. All crops recorded as having been visited by stingless bees are reviewed here. They are divided into sections depending on the importance of the bees. This division is preliminary, as information is lacking for many crop species. Difculties in assessment included the lack of information on the need for pollination, e.g. the need for pollination of most mango varieties is unknown, and geographic variability, e.g. stingless bees are visitors to owers of crop species in many parts of India but not in the Punjab, which is outside of their geographic range (13).

Crops Visited and Pollinated by Stingless Bees

In this section, I include crop species for which stingless bees make a proven and substantial contribution to pollination (Table 1).
MACADAMIA, MACADAMIA INTEGRIFOLIA (PROTEACEAE) Yields of macadamia benet from bee visitation (46), and low bee populations in many orchards may limit yield and quality (156). The major visitors to owers are honey bees in Hawaii (149) and both honey bees and Trigona spp. in Australia (48) and Costa Rica (74). Individuals of both species showed delity to the crop (154). No preference was shown by either honey bees or stingless bees for heavily versus lightly owering trees. Both bee species, but particularly stingless bees, preferred sunny outer racemes to inner shaded ones. Both bee species were present for the entire macadamia owering season. Stingless bees foraged for a mean of 7 h per day, compared with 10 h for honey bees. Populations of Trigona bees, but not honey bees, were positively correlated to the extent of the absence of surrounding natural eucalyptus vegetation in 5 out of 15 surveyed orchards, where >90% of surrounding vegetation was cleared (48). Honey bees collected mainly nectar, and stingless bees mainly pollen, bringing the latter into closer contact with the stigma, a small surface on top of the style on which the pollen grain germinates, resulting in fertilization of the ower. Close contact with the stigma results in pollen grain deposition. Only 24% of the honey bees returning to hives in a macadamia orchard had been foraging on macadamia, compared with 100% of Trigona bees (44). Trigona bees were opportunistic foragers, exploiting the temporary abundance of macadamia pollen by increasing colony activity (155). Racemes that were enclosed in cages that excluded honey bees but allowed visitation by the smaller stingless bees yielded a nut set equal to that on open pollinated racemes, which shows that stingless bees were efcient pollinators (47).

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Table 1 Crops visited and at least occasionally or partially pollinated by stingless bees Common name Name Family

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Reference

Crops for which stingless bees make an important contribution to pollination Macadamia Macadamia integrifolia Proteaceae Chayote, Choko Sechium edule Cucurbitaceae Coconut Cocos nucifera Arecaceae Mango Mangifera indica Anacardiaceae Carambola Averrhoa carambola Oxalidaceae Camu-Camu Myrciaria dubia Myrtaceae Mapati, Uvilla, Amazon Pourouma cecropiaefolia Moraceae Tree Grape Annatto, Achiote Bixa orellana Bixaceae Cupua u c Theobroma grandiorum Sterculiaceae Crops visited and occasionally or partially pollinated by stingless bees Onion Allium cepa Alliaceae Strawberry Fragaria chiloensis Rosaceae X ananassa Loquat Eriobotrya japonica Rosaceae Peach Prunus persica Rosaceae. Plum Prunus domestica Rosaceae Pear Pyrus communis Rosaceae Coffee Coffea spp. Rubiaceae Guava Psidium guajava Myrtaceae Jaboticaba Myrciaria cauliora Myrtaceae Jambolan Syzygium cumini Myrtaceae Rose Apple Syzygium jambos Myrtaceae Sunower Helianthus annuus Asteraceae Niger Guizotia abyssinica Asteraceae Litchi, Lychee Litchi chinensis Sapindaceae Longan Euphoria longan Sapindaceae Rambutan Nephelium lappaceum Sapindaceae Soap-Nut Sapindus emarginatus Sapindaceae Ackee Blighia sapida Sapindaceae Guaran a Paullinia cupana Sapindaceae Squash Cucurbita pepo Cucurbitaceae Bitter Gourd Momordica charantia Cucurbitaceae Watermelon Citrullus lanatus Cucurbitaceae Cucumber Cucumis sativus Cucurbitaceae Luffa Luffa acutangula Cucurbitaceae Indian Jujube Zizyphus mauritiana Rhamnaceae Peach Palm, Pejibaye Bactris gasipaes Arecaceae Sago Palm Metroxylon sagu Arecaceae Rattan Calamus spp. Arecaceae Breadfruit Artocarpus altilis Moraceae Jackfruit Artocarpus heterophyllus Moraceae Ice Cream Bean, Sipo, Inga edulis Leg.: Mimosoideae Guamo

See text See text See text See text See text See text See text See text See text See text See text 109 27 20 20 See text See text 43 34 27, 53, 56 See text 114 See text 20 See text See text 69 102 See text 34, 141 16, 80 16 16 107 84 150 18, 68 See text See text 1, 2

(Continued)

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Table 1 (Continued) Common name Leucaena Stylo, Brazilian Lucerne Indigofera Pigeon Pea Tamarind Hogplum Citrus Fennel Coriander Field Mustard Castor Oil Bellyache Bush Rubber Sweet Pepper, Capsicum, Chili Eggplant Sesame Indian Shot Membrillo Kapok Avocado Monsterio Cardamom Saren Nanche, Murici Acerola, Barbados Cherry Sisal White Jute Panama Hat Plant Name Leucaena leucocephala Stylosanthes guianensis Indigofera endocaphylla Cajanus cajan Tamarindus indica Spondias mombin Citrus spp. Foeniculum vulgare Coriander sativum Brassica campestris Ricinus communis Jatropha gossypifolia Hevea brasiliensis Capsicum annuum varieties Solanum melongena Sesamum indicum Canna indica Gustavia superba Ceiba pentandra Persea americana Monstera deliciosa Elettaria cardamomum Amomum villosum Byrsonima crassifolia Malpighia punicifolia Agave sisalana Corchorus capsularis Carludovica palmata Family Leg.: Mimosoideae Leg.: Papilionoideae Leg.: Papilionoideae Leg.: Papilionoideae Leg.: Caesalpinioideae Anacardiaceae Rutaceae Apiaceae Apiaceae Brassicaceae Euphorbiaceae Euphorbiaceae Euphorbiaceae Solanaceae Solanaceae Pedaliaceae Cannaceae Lecythidaeae Bombacaceae Lauraceae Araceae Zingiberaceae Zingiberaceae Malpighiaceae Malpighiaceae Agavaceae Tiliaceae Cyclanthaceae Reference 56 98 See text See text 141 1, 69, 141, 142 See text 56 See text 60 27, 34, 53 See text See text See text See text See text See text See text 69 See text 111 See text See text See text See text See text 53 See text

CHAYOTE, CHOKO, SECHIUM EDULE (CUCURBITACEAE) The vines that produce the subtropical vegetable chayote are monoecious, producing both male and female owers on all plants. The plant is considered a good source of nectar for honey bees in the United States (77). In Costa Rica, many species of bees and wasps visited chayote owers, but the only important ones, on the basis of abundance and efciency, were 28 species of stingless bees. Of these species, Trigona corvina and Partamona cupira were particularly important. Flowers covered with bags produced no fruits. Those open and visited by stingless bees produced fruit. Those open and visited by other bees and wasps produced fruit but in reduced quantities. Furthermore, two elds of chayote in

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areas with no surrounding trees and hence no stingless bees did not bear fruit (161).
COCONUT, COCOS NUCIFERA (ARECACEAE) Insect pollination is important for high yield of coconut (54). Honey bees, Apis spp., have been recorded on coconut owers in Hawaii, India, Malaysia, the Philippines, Trinidad, Ecuador (37), and Fiji (77). Stingless bees, both Melipona spp. and others, are the dominant visitors in Costa Rica (51) and Surinam (34). In Trinidad, coconut pollen was occasionally collected by four species of stingless bees but was much more heavily collected by honey bees (141). Wasps, ants, earwigs, ies (37), butteries, and beetles (51) have also been recorded but are not considered effective pollinators. Stingless bees visit both male and female owers (51). Most (83%) individuals visiting pistillate owers in search of nectar carried loads of coconut pollen from previously visited staminate owers. Many of these (33%) then visited staminate owers on the same inorescence. This behavior is conducive to efcient pollen grain transfer. Yields are higher where hives of honey bees are kept in plantations (77). Thus, there is evidence that both honey bees and stingless bees contribute to the pollination this crop. MANGO, MANGIFERA INDICA (ANACARDIACEAE) Visits by insects increase yields of mango (38). The owers are unspecialized, allowing pollination by most visiting insects. Stingless bees are the most common insects visiting mango owers in studies in Brazil (27, 60, 139), India (140), and Australia (7). Pollen of mango was found in pollen stores of hives of Trigona angustula in Chiapas (142). In Australia, Trigona bees were the most efcient pollinators on the basis of the proportions of owers pollinated after a visit. This efciency is due to the large amount of pollen carried on their bodies and the close contact they made with the stigma. Furthermore, Trigona bees moved more frequently from tree to tree and thus were probably the most effective cross pollinators (7). Honey bees are not strongly attracted to mango owers and are only occasionally observed (37, 77). Flies are the most common visitors to mango owers in many parts of the tropics (37) and are probably also efcient pollinators. Thus, stingless bees and ies are the most important pollinators of this crop. CARAMBOLA, AVERRHOA CARAMBOLA (OXALIDACEAE) The distylous owers of carambola require cross pollination to achieve fruit yield (37). M. favosa have been recorded visiting the owers of carambola in Surinam (34). Large numbers of two bee species, Trigona thoracica and Apis cerana visited owers of carambola in orchards in Malaysia. Both bee species carried large numbers of pollen grains on their bodies. T. thoracica was an efcient pollinator, with hundreds of successfully germinated pollen grains deposited on owers that were bagged and then exposed to one bee visit. Control owers left bagged

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had a mean of six pollen grains that did not germinate. T. thoracica made more intermorph visits than A. cerana. A. cerana still appeared to be useful, however, because the introduction of hives into two orchards correlated with increased yields (100).
CAMU-CAMU, MYRCIARIA DUBIA (MYRTACEAE) Insects are needed to pollinate the protogynous owers camu-camu. Although wind may effect some pollination, bees are the most important pollinators and are attracted by the fragrance and nectar of the owers. The most common visitors to camu-camu in Amazonian Peru were Melipona sp. and Scaptotrigona postica (99). Pollination by bees, particularly Meliponini, is the dominant pollination system in the Myrtoideae (71), and hence, the importance of stingless bees in the pollination of Myrtaceae may be greater than current records indicate. MAPATI, UVILLA, AMAZON TREE GRAPE, POUROUMA CECROPIAEFOLIA (MORACEAE) Stingless bees and ants were the only visitors to owers of ma-

pati in the Manaus region of Brazil (35). The ants did not carry pollen on their bodies nor move frequently between trees. The bees visited the owers frequently and carried many pollen grains on their legs and bodies. Activity was greatest in the morning, when bees rst visited the male owers collecting pollen and then rapidly visited the female owers. Bagged owers did not set fruit, but pollination was not limiting because of the many bees attracted to the owers and their effective pollinator behavior (35).
ANNATTO, ACHIOTE, BIXA ORELLANA (BIXACEAE) Annatto is efciently buzz pollinated by large bees including the stingless bee Melipona melanoventer. The nonbuzz pollinating species Apis mellifera and Trigona spp. collected pollen in a manner that achieved little pollination (75). This plant is stated to be almost exclusively pollinated by M. fuliginosa in many regions (159). The pollen of annatto was found in the honey stores of hives of H. pothieri in the Ivory Coast (69). The pollen of annatto was one of the most common found on the legs of workers of Melipona seminigra merrillae entering their hive in Amazonas (2). Pollen of this species was also found in a hive of M. ruventris in Amazonas (1). CUPUACU, THEOBROMA GRANDIFLORUM (STERCULIACEAE) Near Belem, ow ers of the cupua u fruit tree are visited by stingless bees, especially Plebeia c minima, and small weevils. Most plants were self incompatible, and the behavior of the bee was more conducive to out-crossing than that of the weevil. The weevils, but not the bees, were present in a plantation in a disturbed habitat, suggesting that the bees depend on primary forest (153). Visitors to owers of this plant in a forest area near Manaus included the stingless bees Trigona clavipes (referred to as Tetragona clavipes) and Trigona lurida (referred to as

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Ptilotrigona lurida). The former bee only robbed pollen, but T. lurida appeared to be an effective pollinator (138).

Crops Visited and Occasionally or Partially Pollinated by Stingless Bees

Included in this section are crops that are recorded as having been visited or pollinated by stingless bees but where pollinator effectiveness is not determined. Also included are crops that are usually pollinated by other means but at some times or in some locations are pollinated by stingless bees. Table 1 includes all crop species for which records exist. Where the record is a simple observation of use of a crop species, they are listed in Table 1 but not discussed in the text.
ONION, ALLIUM CEPA (ALLIACEAE) Seed crops of onion benet from insect visitation. A review of world studies shows that various species of bees and ies are the most common ower visitors (37). Honey bees and Trigona iridipennis were shown to be the most important pollinators in India (113, 137). In a study in Maharastra State in India, hives of T. iridipennis and Apis spp. were introduced to an experimental farm. T. iridipennis accounted for almost half of all visits to onion owers, with A. cerana and Apis orea accounting for most of the remainder. All species foraged throughout the day. The Apis spp. visited approximately twice as many owers per minute than T. iridipennis. T. iridipennis actively collected both nectar and pollen, while the Apis spp. actively collected only nectar and incidentally collected pollen as a result. Although bee visitation was shown to increase seed set, the relative pollinator efciency of the three bee species was not determined (81). Honey bees and stingless bees were the most common insects visiting onion owers in Brazil (6, 70). The stingless bees did not pollinate as efciently as Apis spp., but they were still important (70). STRAWBERRY, FRAGARIA CHILOENSIS X ANANASSA (ROSACEAE) Imported stingless bees have been evaluated in Japan for pollination of strawberries in glasshouses. Colonies of T. minangkabau from Sumatra and honey bees both efciently pollinated owers. The number of owers visited per 10 min was estimated to be 7.7 for honey bees and 3.1 for T. minangkabau. A single honey bee visit to a ower pollinated 11% of achenes, while a T. minangkabau visit pollinated 4.7%. To produce high quality fruits, 11 honey bee visits or 30 T. minangkabau visits are required per ower. Foraging by T. minangkabau was more suited to the conned glasshouse space than that of the honey bees (63). The Brazilian stingless bee Nannotrigona testaceicornis was also introduced in Japan to pollinate strawberries in glasshouses and proved to be efcient, with owers that received four visits producing well-formed fruits (72). Although strawberries can be pollinated by stingless bees, most production is in temperate areas, and other bees and ies are also efcient (37).

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COFFEE, COFFEA SPP. (RUBIACEAE) Honey bees and stingless bees visited Coffea arabica owers in Brazil (92). The larger honey bees and Melipona spp. were perhaps more efcient pollinators than the smaller species of stingless bees. In highland central America, Trigona nigerrima, Trigona fulviventris, and T. angustula were the most common stingless bee visitors of the owers (126). In Chiapas, Mexico, T. angustula are common visitors (142). In Papua New Guinea, Trigona spp. were the most abundant visitors on heavily owering Coffea canephora plants but were absent from isolated owering plants and did not move as regularly as a leaf cutter bee, Creightonella frontalis, which was considered to be the best candidate for pollen grain transfer (162). In Java, C. canephora is visited by many Trigona sp. (referred to as Melipona sp.) and other insects including Xylocopa bees (53). Honey bees are the most common visitors to coffee owers in East Africa and Jamaica, and growers are recommended to keep hives in their plantations (37). GUAVA, PSIDIUM GUAJAVA, AND OTHER MYRTACEOUS CROPS (MYRTACEAE)

Stingless bees were observed to collect pollen of guava in Guatemala, Costa Rica, and Equador but not the Dominican Republic (52), where stingless bees do not occur. A. mellifera and bees of the genera Bombus, Lassioglossum, and Xylocopa also collected pollen from guava owers. In a study of the pollen returned to the hive by four species of stingless bees in Trinidad, the pollen of guava was collected by all species and was the most commonly collected pollen by all but one species; it was only occasionally collected by honey bees (141). Guava pollen was found in the pollen stores of hives of H. pothieri in the Ivory Coast (69). Guava pollen was found in the hives of honey bees and of 4 of the 10 species of stingless bees included in a study in a garden in Brazil (56). Large quantities of pollen, >10% of the total, of guava were found in both the honey and pollen pots of hives of Melipona marginata marginata in Brazil (67). Also in Brazil, pollen of guava was found in the honey and pollen stores of M. quadrifasciata (43) and T. spinipes (28). The importance of insects in pollination of guava and the role of the various visitors requires study. Jaboticaba, jambolan, and rose apple are also visited by stingless bees (Table 1), but their importance and efcacy as pollinators are unknown.
SUNFLOWER, HELIANTHUS ANNUUS (ASTERACEAE) Near S o Paulo in Brazil, a sunowers were visited by F. schrottkyi (27) and T. spinipes, Trigona hyalinata, and Geotrigona sp. (85). In India, sunower is also attractive to all the Apis spp. and T. iridipennis (40). Also in India, the potential of T. iridipennis as a pollinator was tested by enclosing sunower plants in cages. The yields in those cages was higher than plants caged without bees but was not as high as open pollinated plants (17). Stingless bees were recorded visiting sunower

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crops in Australia, but their low populations relative to those of honey bees led Radford et al to conclude that they have an insignicant role in pollination (106). Honey bees are usually the most abundant insects visiting sunowers; however, locally abundant insects, particularly large solitary bees and bumble bees, may be important owing to their greater interest in collecting pollen (37). In tropical regions, stingless bees are sometimes common visitors to sunowers but are probably rarely important.
LITCHI, LYCHEE, LITCHI CHINENSIS (SAPINDACEAE) Stingless bees (identied as Melipona but probably Trigona sp.) and honey bees were the most common visitors to owers of litchi in India in both Uttar Pradesh (96) and West Bengal (21). Trigona sp. (probably T. carbonaria) was the most common species visiting owers of litchi at one site in Australia but was absent at another site (66). Trigona bees collected pollen and nectar from litchi owers but did not often touch the stigma. The larger honey bees usually touched the stigmas while visiting the owers (66). More behavioral observations at other sites are required to determine if this is a common pattern on litchi owers. RAMBUTAN, NEPHELIUM LAPPACAUM (SAPINDACEAE) Bagged owers of this androdioecious species set no fruit. Five species of Trigona and A. cerana are potential pollinators in East Kalimantan, Indonesia (148). T. thoracica and two other species of Trigona were among the most common insects visiting rambutan owers in Peninsula Malaysia. None of the insects, including the stingless bees, foraging on hermaphrodite owers carried rambutan pollen on their bodies, which suggests that they were not the pollinators (101). SOAP-NUT, SAPINDUS EMARGINATUS (SAPINDACEAE) In Southern India, the owers of the soap-nut tree were visited by a broad spectrum of insects, including Apis spp., Trigona sp., and other bees, wasps, ies, and butteries. The wasps and butteries were considered to deliver more cross pollen, but both cross and self pollination result in fruit set (115). SQUASH, CUCURBITA PEPO AND OTHER CUCURBIT CROPS (CUCURBITACEAE)

Honey bees and T. spinipes were the most common insects visiting owers in Brazil (10). Squash bees of the genera Peponapis and Xenoglossa (Anthophorini) rely solely on species of Cucurbita for their pollen and most of their nectar. They coevolved with their hosts in Mexico, but it is often suggested they be introduced to other parts of the world for Cucurbita pollination (146). However, honey bees, carpenter bees, bumble bees, halictid bees, and stingless bees are occasionally important pollinators of squash (55). Bitter gourd, watermelon, cucumber, and luffa are visited by stingless bees (Table 1), but they are usually only a small proportion of the complex of visitors (37).

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RATTAN, CALAMUS SPP. (ARECACEAE) The most important pollinating agents of four species of Calamus in Thailand were Trigona spp. (18). In Malaysia, Trigona spp. were the most common insect, but nocturnal visitors were considered more important because pollen release occurs at night (68). BREADFRUIT, ARTOCARPUS ALTILIS (MORACEAE) A breadfruit tree produces male and female inorescences alternately, so no self pollination can occur. Flowers are said to be wind pollinated, as they are odorless and have powdery pollen; hand pollination is practiced to increase fruit set (37, 105, 118). In Brazil, T. fulviventris collected nectar in the morning and pollen in the afternoon from male inorescences. They did not visit female inorescences and therefore did not effect pollination. They may have contributed to wind pollination by dislodging pollen grains from the male owers. This mode of insect-assisted wind pollination may explain why the plants produce nectar (22). JACKFRUIT, ARTOCARPUS HETEROPHYLLUS (MORACEAE) Jackfruit has male and female inorescences (37) and is considered to be insect pollinated on the basis of its scent and sticky pollen (105, 151). Trigona bees as well as drosophilid and phorid ies are attracted to the male and female owers in Java (151). In another study, no visitors were observed to female owers, and insect-assisted wind pollination is suggested (82). LEGUMES (LEGUMINOSAE) Indigofera, Indigofera endocaphylla, is visited in Indonesia by a range of insects, mainly bees, including Trigona itama. However, the stingless bee was not common whereas the halictid bee Nomia quadridentata was a frequent and effective pollinator (9). A. cerana and a Trigona sp. were the most common visitors to owers of pigeon pea, Cajanus cajan, but the former was considered the more effective pollinator (95). Records exist of stingless bees visiting other legumes (Table 1). For many papilionoid legumes, the sexual column must be released from its concealed position within the petals for pollination to occur. This process, known as tripping, can only be performed by a bee of adequate weight, and hence smaller bees, such as many stingless bees, are not effective pollinators. CITRUS, CITRUS SPP. (RUTACEAE) Pollen of Citrus spp. was rarely collected by two species of Melipona and honey bees but not by N. mellaria and T. nigra in Trinidad (141). Citrus pollen was found in the hives of honey bees and of 2 of the 10 species of stingless bees included in a study in a garden in Brazil (56). Scaura latitarsus and T. clavipes were collected while visiting the owers of Citrus sp. in Surinam (34). Citrus grandis and another Citrus sp. were visited by pollen-collecting Trigona (referred to as Melipona sp.) bees in Java (53). Evaluation of the importance of bees needs to account for the breeding system, as many citrus cultivars are parthenocarpic (135).

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CORIANDER, CORIANDER SATIVUM (APIACEAE) Apis spp. and T. iridipennis were the main pollinating insects of coriander near Pune, India. A. cerana, A. orea, and T. iridipennis visited 14, 13, and 10 umbels (ower heads) per minute and 4, 3, and 2 plants per minute, respectively (136). BELLYACHE BUSH, JATROPHA GOSSYPIFOLIA (EUPHORBIACEAE) Three species of stingless bees, particularly P. mosquito, were considered the main pollinators of J. gossypifolia, a medicinal plant in Brazil (94). Trigona sp. was an important pollinator in India (116). SWEET PEPPER, CAPSICUM, CHILI, CAPSICUM ANNUUM VARIETIES (SOLANACEAE)

Wild bees and honey bees visit C. annuum owers. The most common visitors to these owers in Brazil were the stingless bees T. angustula and honey bees (37). In Java, Trigona sp. (referred to as Melipona sp.) collect pollen from stamens and often climb to the top of stigmas, potentially transferring pollen (53). Roubik, however, stated that the smaller bees, including stingless bees, are probably not effective pollinators (125).
EGGPLANT, SOLANUM MELONGENA (SOLANACEAE) Trigona fulviventris guianae have been recorded visiting the owers of eggplant (34). However, this species is buzz pollinated, and therefore, Trigona spp. are unlikely to effectively pollinate these plants (24). SESAME, SESAMUM INDICUM (PEDALIACEAE) The stingless bees Melipona fulva, Trigona mazucatoi, T. lurida, T. williana, and C. capitata were collected from the owers of sesame in Surinam (34). These authors noted that these species were all larger stingless bees and could not explain the absence of smaller species. T. iridipennis visited plots of sesame in India but were observed only on extraoral nectaries (112). INDIAN SHOT, CANNA INDICA (CANNACEAE) This crop is visited by Trigona sp. (referred to as Melipona sp.) in Java (53). The stingless bees forage deep in the owers collecting nectar and, in doing so, effect pollination. MEMBRILLO, GUSTAVIA SUPERBA (LECYTHIDAEAE) Flowers of species of membrillo are pollinated by small- to medium-sized pollen-gathering bees such as Trigona, Melipona, and Bombus (102). Melipona fasciata heavily utilized pollen of G. superba in Panama (129). AVOCADO, PERSEA AMERICANA (LAURACEAE) Small stingless bees are claimed to be good pollinators of avocado trees, though data are lacking (29, 152). In Mexico and Guatemala, Geotrigona acapulconis, T. nigerrima, Partamona sp., and Scaptotrigona sp. are common visitors (DW Roubik, S Gazit & G Ish-Am,

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personal communication). Honey bees are efcient pollinators but are not strongly attracted to the crop (59).
CARDAMOM, ELETTARIA CARDAMOMUM (ZINGIBERACEAE) In India, the honey bee, A. cerana, was the most common insect visiting cardamom collecting pollen in the morning and nectar in the afternoon. The stingless bee, T. iridipennis, was commonly observed collecting pollen. The pollen foragers made good contact with the anthers and stigma, which suggests they effectively pollinated (25a). In Papua New Guinea, stingless bees were not observed; instead the solitary bee Amegilla sapiens efciently pollinated the owers (143). SAREN, AMOMUM VILLOSUM (ZINGIBERACEAE) Saren, a valuable medicinal crop, was visited by Trigona sp. (referred to as Melipona sp.) in Yunnan, giving a fruit set 4% higher than articially pollinated plants and 29% higher than open-pollinated controls (157). NANCHE, BYRSONIMA CRASSIFOLIA, AND ACEROLA, MALPIGHIA PUNICIFOLIA (MALPIGHIACEAE) Both nanche and acerola crops are visited and occasionally

pollinated by stingless bees. However, specialist oil-collecting anthophorine bees are the main pollinators for both B. crassifolia (12, 117) and M. punicifolia (73).
RUBBER, HEVEA BRASILIENSIS (EUPHORBIACEAE) Some stingless bees of the genus Trigona collected pollen in India, where honey bees only visited extraoral nectaries (61). In the New World, Ceratopogonidae ies are probably the main pollinators (105). SISAL, AGAVE SISALANA (AGAVACEAE) F. schrottkyi was observed to visit sisal growing in a garden near Sao Paulo in Brazil (27). This species is mainly pollinated by bats at night and during the day by larger bees (125). PANAMA HAT PLANT, CARLUDOVICA PALMATA (CYCLANTHACEAE) Flowers of C. palmata, a crop plant, are visited and pollinated by Trigona sp. (referred to as Melipona sp.) and by A. indica in Java (53). In Panama, T. corvina and T. fuscipennis are the common visitors (DW Roubik, personal communication). In the natural habitats of C. palmata in Colombia, four species of stingless bees (all Trigona) pollinated C. palmata (134). However in Amazonian Peru, small weevils pollinated the owers (41).

Crops Visited by Stingless Bees But Pollinated by Other Means

Records exist of visitation by stingless bees to the owers of some crop species that are known to be effectively pollinated only by other means (Table 2). In some cases, stingless bees may have a negative impact by removing nectar or

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Table 2 Crop species with records of visitation by stingless bees but known to be pollinated by other means Pollinator or means of fertilization Sphingidae and other crepuscular moths and butteries Nitidulidae beetles Referencea 11, 36, 53

Common name Papaya, papaw

Name Carica papaya

Family Caricaceae

Custard apple, cherimoya, atemoya, Oil palm Vanilla Cocoa, cacao Brazil nut Mangosteen and relatives Bacuri Benoil Cashew Lucerne, Alfalfa Sunn hemp Black pepper Bananas Passionfruit Rape
a

Annona spp.

Annonaceae

86

Elaeis guineensis Vanilla spp. Theobroma cacao Bertholletia excelsa Garcinia spp. Platonia insignis Moringa oleifera Anacardium occidentale Medicago sativa

Arecaceae Orchidaceae Sterculiaceae Lecythidaceae Clusiaceae Clusiaceae Moringaceae Anacardiaceae Leguminosae: Papilionoideae Leguminosae: Papilionoideae Piperaceae Musaceae Passioraceae Brassicaceae

Elaeidobius spp. (weevils) Eulaema spp. (bees) Ceratopogonidae midges Large euglossine and carpenter bees Parthenocarpic Birds Xylocopa spp. (bees) Bees and ies Large bees, e.g. megachilids, bumble bees Large bees e.g. Xylocopa spp. Wind or rain Parthenocarpic Carpenter bees Honey bees

42, 145 32 163 87, 102 119, 120 76 62 39, 50 37

Crotalaria juncea Piper nigrum Musa spp. Passiora edulis Brassica napus var. oleifera

53, 90 37 105 26, 132 4

References that demonstrate or review efcacy of pollinator.

pollen, making the owers less attractive to the effective pollinator. In extreme cases, stingless bees have a more obvious negative impact, such as damaging the owers of rape (4) or aggressively deterring the effective pollinators of passionfruit (132).

CONCLUSIONS
Stingless bees possess many characteristics that enhance their importance as crop pollinators both as wild populations and managed pollinators. Characteristics of their social life (perenniality, polylecty, oral constancy, recruitment, harmlessness) suit them for pollination. Challenges to their widespread use

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include the lack of availability of large numbers of hives and the dearth of knowledge of the pollination needs and major pollinators of tropical crops. The absence of natural vegetation is associated with low local populations of stingless bees, and hence forest clearing threatens the role of these insects in crop pollination. The foraging ight range often is between 100 and 400 m. Hence remnant forests within this distance from orchards can provide adequate bee populations. Improved domestication practices would increase hive availability, thereby reducing reliance on natural populations. There are no crops known to be exclusively pollinated by stingless bees. Few generalizations can be drawn about the types of plants that they visit and pollinate. There are many crops in many families that, on the basis of often scanty knowledge, appear to benet from pollination by these insects. Stingless bees are conrmed and important pollinators of annatto, camu-camu, chayote, coconut, cupua u, carambola, macadamia, mango, and mapati. They c make a contribution to the pollination of 60 other crop species. They have been reported visiting 20 crop species which are effectively pollinated by other means; these have been listed to refute the occasional false claims made of the pollinator potential of stingless bees. Probably many other crops in the tropics are pollinated by stingless bees but have never been recorded in the literature. It is clear that these bees provide economic benets, by their crop pollination services, that are substantial but not presently quantiable. Stingless bees display greater diet breadth and range of foraging behavior than honey bees, making them likely to be important to future development of pollinators best suited to the needs of particular crops and habitats. I hope this review stimulates the necessary observation, experimentation, and publication to clarify the importance of this abundant group of insects in world agriculture. ACKNOWLEDGMENTS I am grateful to David Roubik, Margaret Sedgley, Ben Oldroyd, Helen Wallace, and Tad Bartareau for many helpful comments on the manuscript.
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