Annu. Rev. Entomol. 1999. 44:183–206 Copyright c 1999 by Annual Reviews.

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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, floral biology, alternative pollinators, entomophily

ABSTRACT
Stingless bees (Apidae: Meliponini) are common visitors to flowering 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 flowers of ∼90 crop species. They were confirmed to be effective and important pollinators of 9 species. They may make a contribution to the pollination of ∼60 other species, but there is insufficient 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 flower visiting behavior of colonies, floral constancy of individual bees, flight 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 flowering 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 confined 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 flowers 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 briefly (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 reflects 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 efficiency 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 influence 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) floral 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 benefit of allowing colonies to survive long periods of low food availability. Additionally, it means that workers will collect floral resources beyond immediate needs, resulting in intensive visitation of preferred flowers (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 floral resources and provide information on the position of those floral resources, which allows the rapid deployment of large numbers of foragers (88) relative to other bees and insects in which each individual has to find the resource.

For example. all examined species show preferences (67. rapidly learning to exploit the resources offered by introduced plants. Despite their generalized flower selection. Hypotrigona pothieri used 54 species in 28 families (69). Aspects of the foraging biology of stingless bees that are pertinent to this topic are reviewed here. 160) but never from the perspective of crop pollination. Few generalizations can be made regarding the plant or flower type preferred by stingless bees. and white or yellow flowers (27). (43. Disadvantages of stingless bees for crop pollination include the following: There is a poor level of domestication technology for most species. Floral . dense inflorescences (128). some species damage leaves in search of resin (25. 97% of the pollen foragers of nine species of stingless bees visited only one floral resource on each trip. there is a lack of availability of large numbers of hives. and diet and seasonal patterns of activity are reviewed by Roubik (124). response to weather. in which a worker visits only one plant species on a single trip. 109. as evidenced by the pure pollen loads in their corbiculae (108). 109. flowers with corolla tubes shorter than the bee’s tongues (50). trees (67. navigation. 128). 67). as the old queen is flightless (57). some species are unable to be domesticated because of specific nesting requirements. 130. flowers with long corolla tubes that are wide enough for the bees to enter (34). ASPECTS OF THE BIOLOGY OF STINGLESS BEES RELEVANT TO POLLINATION The biology of the stingless bees has been reviewed (78. neotropical stingless bees heavily use the introduced Eucalyptus spp. Thus a honey bee epizootic that disrupted pollination would not effect the stingless bees in that system. propagation of colonies contributes to preservation of biodiversity by conserving populations of species that may otherwise decline owing to human disruption of ecosystems. Stingless bees are adaptable. 69. In Brazil. they are able to forage effectively in glasshouses (63). Several other relevant topics including foraging syndromes. All studied species visit a broad range of plant species. 110).CROP POLLINATION BY STINGLESS BEES 185 Unlike honey bees. but it has been suggested they prefer small flowers (161). forager recruitment. 109). stingless bees have the following advantages: They are generally less harmful to humans and domesticated animals. and they are resistant to the diseases and parasites of honey bees (31). For example. Melipona marginata used 173 species in 38 families (67). Floral constancy. 124. floral larceny. colonies are rarely able to abscond. 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. colony growth rates are low compared with honey bees. Stingless bees are generalist flower visitors. 158). is typical of many polyphagous bees (33). and some species are territorial and fight when placed in close proximity.

Stingless bees were common visitors to flowers of cupua¸ u growing near primary forest c in Amazonian Brazil but were absent in disturbed habitats. stingless bees are the confirmed pollinators of many plants on the basis of experimentation or observation. 9 were pollinated by stingless bees (64). (14).186 HEARD constancy is associated with pollinator effectiveness. Illegitimate use of flowers by stingless bees in which they remove resources without pollinating. Examples of these studies were conducted at the community and individual species levels. Trigona bees were shown to be effective pollinators of Spathiphyllum friedrichsthalii (83). In addition to floral species constancy. Flight range is a function of worker bee size (78. the maximum flight range of Cephalotrigona capitata and Melipona panamica in tropical forest was estimated to be 1. pollinates Ondinea purpurea in Australia (133). except for two fields with no surrounding forest for 1 km (161). with or without damaging the flowers. 89) and possibly also colony population size (141). respectively (127). The abundance of Trigona bees on longan flowers in a large orchard was found to decrease with distance from an adjoining forest (20). they have been shown to be important pollinators of noncrop species in natural habitats. Another sapindaceous rainforest understory tree in Costa Rica. The actual foraging distance also depends on the attractiveness of the resource in relation to distance from the nest. Cupania guatemalensis. Using a mark-release technique. as collection and deposition of pollen from two or more species reduces the amount of pollen available and contaminates stigmas with the wrong pollen.1 km. Although many species of stingless bees adapt to artificial nest sites. Trigona spp. all of the 52 species visited by Melipona and 108 of the 128 species visited by other stingless bee species may have benefited directly from pollination services of these bees (123). In the lowland neotropics. Captured . All surveyed chayote fields in Costa Rica had Trigona bees present. 9 are pollinated by stingless bees (3). At the species level. Of the 13 Australian epiphytic orchids whose pollinators are confirmed. Partamona grandipennis pollinates the monoecious herb Begonia involucra in Costa Rica (5). 141). In addition to records of use of many plants by stingless bees. 132). pollen. occurs in both natural habitats (124) and agroecosystems (4. and availability of alternative resources. and Trigona sp.5 and 2. foragers normally show resource constancy to either nectar. is also pollinated by Trigona spp. were the most abundant and effective pollinators of the androdioecious Xerospermum intermedium growing in the understory of Malaysian rainforests (8). Trigona spinipes pollinates Nymphaea ampla in Brazil (103). Abundance of Trigona carbonaria in orchards of macadamia is correlated with extent of surrounding natural eucalyptus vegetation (48). which suggests that bee populations are dependent on the primary forest (153). Of 41 plant species investigated in the forest understory in Sarawak. or resin within a single trip and usually between successive trips (58. needs of the colony. natural vegetation can influence abundance of stingless bees.

Trigona ruficrus. The flight activity of colonies of stingless bees depends on species. The estimated 10.000 flights per day (49). the maximum flight range of four species of stingless bees was from 120 to 680 m and was closely correlated with head capsule width (151a). The potential of stingless bees for crop pollination is enhanced by the ability to transfer colonies into artificial hives. By training workers to an artificial nectar source and progressively moving the source away from the hive. 125). Workers of Melipona quadrifasciata.CROP POLLINATION BY STINGLESS BEES 187 workers of Melipona fuliginosa returned when released from distances of 2 km from their nests (159). minangkabau with only 350 workers made only about 700 flights per day. and Trigona amalthea was 540. The history of traditional stingless beekeeping was reviewed recently (29). in a longan orchard in northern Thailand was high at distances of 50 and 200 m from adjoining forest but decreased greatly at 2. 105. 118. 840. the maximum flight range of Plebeia mosquito. Trigona erythrogaster foraged on oil palms in a plantation 1. T. feeding. and 2600 made about 7000. showing the strong positive relationship between hive population and flight activity (63). 125) so that growers do not need to rely on natural populations. minangkabau with populations of ∼5000. Melipona rufiventris. fiber. 2000. 2400. respectively (58). carbonaria made about 20.000 workers of a hive of T.1 km from the forest they inhabited (8). and 14% of non-nestmate conspecifics encountered (23). Using a similar technique. the actual flight distances (rather than the maximum range) of Trigona minangkabau was estimated to be between 84 and 434 m (58). minangkabau shows a very well-developed ability to do this (144). and availability of resources. Trigona moorei. beverages. Colonies of Trigona itami. Hives may be opened for extraction of honey. Hives can also be transported where needed for pollination or for hive strengthening. A newly established hive of T. spices. and medicines (104. 125). population of colonies. 91. Nearly half of . and Melipona scutellaris attacked 74. The abundance of Trigona sp. 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. The breeding system and pollinators of many of these crops have been catalogued (37. and 1200 flights per day. or requeening if necessary and for treatment against natural enemies. and 980 m. respectively (65). CROP POLLINATION More than 1000 plant species are cultivated in the tropics for food. 60.5 and 4 km from the forest (20). Using the calculated flight speed. inspection. 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). and T. These hives can be propagated (45.

exploiting the temporary abundance of macadamia pollen by increasing colony activity (155). and low bee populations in many orchards may limit yield and quality (156). This division is preliminary. in Australia (48) and Costa Rica (74). the need for pollination of most mango varieties is unknown. South Pacific. which shows that stingless bees were efficient pollinators (47). MACADAMIA INTEGRIFOLIA (PROTEACEAE) Yields of macadamia benefit from bee visitation (46). compared with 100% of Trigona bees (44). which is outside of their geographic range (13). and Australia. Stingless bees foraged for a mean of 7 h per day.e. All crops recorded as having been visited by stingless bees are reviewed here. Both bee species were present for the entire macadamia flowering season. compared with 10 h for honey bees. but particularly stingless bees. Both bee species. and geographic variability. I include crop species for which stingless bees make a proven and substantial contribution to pollination (Table 1). e.g. Honey bees collected mainly nectar. i. MACADAMIA. Approximately half of these plants are pollinated by bees (125). The major visitors to flowers are honey bees in Hawaii (149) and both honey bees and Trigona spp. were positively correlated to the extent of the absence of surrounding natural eucalyptus vegetation in 5 out of 15 surveyed orchards. No preference was shown by either honey bees or stingless bees for heavily versus lightly flowering trees. 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. Many of these ∼250 species may be adapted to pollination by stingless bees. e. Individuals of both species showed fidelity to the crop (154). where >90% of surrounding vegetation was cleared (48). resulting in fertilization of the flower. Trigona bees were opportunistic foragers. as information is lacking for many crop species. . the neotropics. but not honey bees. stingless bees are visitors to flowers of crop species in many parts of India but not in the Punjab. preferred sunny outer racemes to inner shaded ones. Only 24% of the honey bees returning to hives in a macadamia orchard had been foraging on macadamia.188 HEARD the species of economically significant tropical crops originated in areas where honey bee species do not occur naturally. and stingless bees mainly pollen.g. Populations of Trigona bees. Difficulties in assessment included the lack of information on the need for pollination. bringing the latter into closer contact with the stigma. Close contact with the stigma results in pollen grain deposition. Crops Visited and Pollinated by Stingless Bees In this section. a small surface on top of the style on which the pollen grain germinates. They are divided into sections depending on the importance of the bees.

Pejibaye Bactris gasipaes Arecaceae Sago Palm Metroxylon sagu Arecaceae Rattan Calamus spp. Achiote Bixa orellana Bixaceae Cupua¸ u c Theobroma grandiflorum 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. Choko Sechium edule Cucurbitaceae Coconut Cocos nucifera Arecaceae Mango Mangifera indica Anacardiaceae Carambola Averrhoa carambola Oxalidaceae Camu-Camu Myrciaria dubia Myrtaceae Mapati. 53. 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. Plum Prunus domestica Rosaceae Pear Pyrus communis Rosaceae Coffee Coffea spp.: 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. 68 See text See text 1. Sipo. 56 See text 114 See text 20 See text See text 69 102 See text 34.CROP POLLINATION BY STINGLESS BEES Table 1 Crops visited and at least occasionally or partially pollinated by stingless bees Common name Name Family 189 Reference Crops for which stingless bees make an important contribution to pollination Macadamia Macadamia integrifolia Proteaceae Chayote. Inga edulis Leg. Arecaceae Breadfruit Artocarpus altilis Moraceae Jackfruit Artocarpus heterophyllus Moraceae Ice Cream Bean. Amazon Pourouma cecropiaefolia Moraceae Tree Grape Annatto. Uvilla. 2 (Continued) . Rubiaceae Guava Psidium guajava Myrtaceae Jaboticaba Myrciaria cauliflora Myrtaceae Jambolan Syzygium cumini Myrtaceae Rose Apple Syzygium jambos Myrtaceae Sunflower Helianthus annuus Asteraceae Niger Guizotia abyssinica Asteraceae Litchi. 80 16 16 107 84 150 18. 141 16.

two fields of chayote in . 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. Capsicum. on the basis of abundance and efficiency. many species of bees and wasps visited chayote flowers. Brazilian Lucerne Indigofera Pigeon Pea Tamarind Hogplum Citrus Fennel Coriander Field Mustard Castor Oil Bellyache Bush Rubber Sweet Pepper. Furthermore. were 28 species of stingless bees. producing both male and female flowers on all plants. 69. Those open and visited by other bees and wasps produced fruit but in reduced quantities. In Costa Rica. CHOKO.: 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. Of these species.: Papilionoideae Leg. Murici Acerola. Flowers covered with bags produced no fruits. 34. 141. 142 See text 56 See text 60 27. Trigona corvina and Partamona cupira were particularly important. The plant is considered a good source of nectar for honey bees in the United States (77).: Papilionoideae Leg. SECHIUM EDULE (CUCURBITACEAE) The vines that produce the subtropical vegetable chayote are monoecious.: Papilionoideae Leg. Chili Eggplant Sesame Indian Shot Membrillo Kapok Avocado Monsterio Cardamom Saren Nanche. Those open and visited by stingless bees produced fruit. 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.190 HEARD Table 1 (Continued) Common name Leucaena Stylo.: Mimosoideae Leg. but the only important ones. Barbados Cherry Sisal White Jute Panama Hat Plant Name Leucaena leucocephala Stylosanthes guianensis Indigofera endocaphylla Cajanus cajan Tamarindus indica Spondias mombin Citrus spp.

ants. Stingless bees are the most common insects visiting mango flowers in studies in Brazil (27. favosa have been recorded visiting the flowers of carambola in Surinam (34). Stingless bees visit both male and female flowers (51). Stingless bees. and others. Honey bees. Honey bees are not strongly attracted to mango flowers and are only occasionally observed (37.CROP POLLINATION BY STINGLESS BEES 191 areas with no surrounding trees and hence no stingless bees did not bear fruit (161). This efficiency is due to the large amount of pollen carried on their bodies and the close contact they made with the stigma. are the dominant visitors in Costa Rica (51) and Surinam (34). Control flowers left bagged . Many of these (33%) then visited staminate flowers on the same inflorescence. flies (37). In Trinidad. T. Large numbers of two bee species. MANGIFERA INDICA (ANACARDIACEAE) Visits by insects increase yields of mango (38). 139). have been recorded on coconut flowers in Hawaii. the Philippines. In Australia. and beetles (51) have also been recorded but are not considered effective pollinators. India (140). Ecuador (37). India. there is evidence that both honey bees and stingless bees contribute to the pollination this crop. coconut pollen was occasionally collected by four species of stingless bees but was much more heavily collected by honey bees (141). Furthermore. Pollen of mango was found in pollen stores of hives of Trigona angustula in Chiapas (142). Malaysia. thoracica was an efficient pollinator. Yields are higher where hives of honey bees are kept in plantations (77). with hundreds of successfully germinated pollen grains deposited on flowers that were bagged and then exposed to one bee visit. Both bee species carried large numbers of pollen grains on their bodies. M.. both Melipona spp. Trinidad. Most (83%) individuals visiting pistillate flowers in search of nectar carried loads of coconut pollen from previously visited staminate flowers. and Fiji (77). This behavior is conducive to efficient pollen grain transfer. butterflies. COCOS NUCIFERA (ARECACEAE) Insect pollination is important for high yield of coconut (54). Apis spp. Trigona bees were the most efficient pollinators on the basis of the proportions of flowers pollinated after a visit. Thus. Thus. allowing pollination by most visiting insects. Trigona thoracica and Apis cerana visited flowers of carambola in orchards in Malaysia. earwigs. Wasps. Trigona bees moved more frequently from tree to tree and thus were probably the most effective cross pollinators (7). MANGO. 60. The flowers are unspecialized. Flies are the most common visitors to mango flowers in many parts of the tropics (37) and are probably also efficient pollinators. stingless bees and flies are the most important pollinators of this crop. AVERRHOA CARAMBOLA (OXALIDACEAE) The distylous flowers of carambola require cross pollination to achieve fruit yield (37). 77). CARAMBOLA. and Australia (7). COCONUT.

and the behavior of the bee was more conducive to out-crossing than that of the weevil. CAMU-CAMU. collected pollen in a manner that achieved little pollination (75). bees are the most important pollinators and are attracted by the fragrance and nectar of the flowers. MYRCIARIA DUBIA (MYRTACEAE) Insects are needed to pollinate the protogynous flowers camu-camu. This plant is stated to be almost exclusively pollinated by M. pothieri in the Ivory Coast (69). cerana. The most common visitors to camu-camu in Amazonian Peru were Melipona sp. because the introduction of hives into two orchards correlated with increased yields (100). and hence. the importance of stingless bees in the pollination of Myrtaceae may be greater than current records indicate. Bagged flowers did not set fruit. Activity was greatest in the morning. ANNATTO. when bees first visited the male flowers collecting pollen and then rapidly visited the female flowers. but not the bees. fuliginosa in many regions (159). suggesting that the bees depend on primary forest (153). Pollination by bees.192 HEARD had a mean of six pollen grains that did not germinate. CUPUACU. 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). Visitors to flowers 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 . T. The bees visited the flowers frequently and carried many pollen grains on their legs and bodies. but pollination was not limiting because of the many bees attracted to the flowers and their effective pollinator behavior (35). AMAZON TREE GRAPE. Pollen of this species was also found in a hive of M. UVILLA. cerana still appeared to be useful. is the dominant pollination system in the Myrtoideae (71). Most plants were self incompatible. thoracica made more intermorph visits than A. The pollen of annatto was found in the honey stores of hives of H. BIXA ORELLANA (BIXACEAE) Annatto is efficiently buzz pollinated by large bees including the stingless bee Melipona melanoventer. and small weevils. ACHIOTE. Although wind may effect some pollination. particularly Meliponini. MAPATI. flow¸ ers of the cupua¸ u fruit tree are visited by stingless bees. The weevils. especially Plebeia c minima. were present in a plantation in a disturbed habitat. THEOBROMA GRANDIFLORUM (STERCULIACEAE) Near Belem. A. The ants did not carry pollen on their bodies nor move frequently between trees. and Scaptotrigona postica (99). however. POUROUMA CECROPIAEFOLIA (MORACEAE) Stingless bees and ants were the only visitors to flowers of ma- pati in the Manaus region of Brazil (35). The non–buzz pollinating species Apis mellifera and Trigona spp. rufiventris in Amazonas (1).

with flowers that received four visits producing well-formed fruits (72). ONION. STRAWBERRY. but they were still important (70). but T. minangkabau from Sumatra and honey bees both efficiently pollinated flowers. minangkabau was more suited to the confined glasshouse space than that of the honey bees (63). FRAGARIA CHILOENSIS X ANANASSA (ROSACEAE) Imported stingless bees have been evaluated in Japan for pollination of strawberries in glasshouses. Colonies of T. . 70). The Apis spp. Honey bees and Trigona iridipennis were shown to be the most important pollinators in India (113.7 for honey bees and 3. they are listed in Table 1 but not discussed in the text. the relative pollinator efficiency of the three bee species was not determined (81). most production is in temperate areas. with A. Table 1 includes all crop species for which records exist. Also included are crops that are usually pollinated by other means but at some times or in some locations are pollinated by stingless bees. Foraging by T. The number of flowers visited per 10 min was estimated to be 7. hives of T. iridipennis. while the Apis spp. minangkabau.. cerana and Apis florea accounting for most of the remainder. iridipennis actively collected both nectar and pollen. 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.7%. A review of world studies shows that various species of bees and flies are the most common flower visitors (37). The stingless bees did not pollinate as efficiently as Apis spp. To produce high quality fruits. were introduced to an experimental farm. visited approximately twice as many flowers per minute than T. T. Although bee visitation was shown to increase seed set. minangkabau visit pollinated 4. Although strawberries can be pollinated by stingless bees. T. and other bees and flies are also efficient (37). ALLIUM CEPA (ALLIACEAE) Seed crops of onion benefit from insect visitation. actively collected only nectar and incidentally collected pollen as a result.CROP POLLINATION BY STINGLESS BEES 193 Ptilotrigona lurida). All species foraged throughout the day.1 for T. A single honey bee visit to a flower pollinated 11% of achenes. The former bee only robbed pollen. iridipennis accounted for almost half of all visits to onion flowers. In a study in Maharastra State in India. 11 honey bee visits or 30 T. Where the record is a simple observation of use of a crop species. 137). lurida appeared to be an effective pollinator (138). minangkabau visits are required per flower. iridipennis and Apis spp. while a T. Honey bees and stingless bees were the most common insects visiting onion flowers in Brazil (6. The Brazilian stingless bee Nannotrigona testaceicornis was also introduced in Japan to pollinate strawberries in glasshouses and proved to be efficient.

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). In highland central America. and growers are recommended to keep hives in their plantations (37). quadrifasciata (43) and T. and Geotrigona sp. HELIANTHUS ANNUUS (ASTERACEAE) Near S˜ o Paulo in Brazil. angustula are common visitors (142). it was only occasionally collected by honey bees (141). GUAVA.194 HEARD COFFEE. jambolan. In Java. In Papua New Guinea. schrottkyi (27) and T. Honey bees are the most common visitors to coffee flowers in East Africa and Jamaica. Creightonella frontalis. >10% of the total. The larger honey bees and Melipona spp. spinipes (28). Stingless bees were recorded visiting sunflower . AND OTHER MYRTACEOUS CROPS (MYRTACEAE) Stingless bees were observed to collect pollen of guava in Guatemala. Trigona hyalinata. Lassioglossum. were the most abundant visitors on heavily flowering Coffea canephora plants but were absent from isolated flowering plants and did not move as regularly as a leaf cutter bee. the pollen of guava was collected by all species and was the most commonly collected pollen by all but one species. angustula were the most common stingless bee visitors of the flowers (126). pothieri in the Ivory Coast (69). Trigona nigerrima.) and other insects including Xylocopa bees (53). C. The importance of insects in pollination of guava and the role of the various visitors requires study. COFFEA SPP. spinipes. of guava were found in both the honey and pollen pots of hives of Melipona marginata marginata in Brazil (67). and T. the potential of T. sunflower is also attractive to all the Apis spp. and T. The yields in those cages was higher than plants caged without bees but was not as high as open pollinated plants (17). Guava pollen was found in the pollen stores of hives of H. Also in India. pollen of guava was found in the honey and pollen stores of M. Costa Rica. but their importance and efficacy as pollinators are unknown. and Equador but not the Dominican Republic (52). In a study of the pollen returned to the hive by four species of stingless bees in Trinidad. (RUBIACEAE) Honey bees and stingless bees visited Coffea arabica flowers in Brazil (92). SUNFLOWER. were perhaps more efficient pollinators than the smaller species of stingless bees. iridipennis as a pollinator was tested by enclosing sunflower plants in cages. In Chiapas. Also in Brazil. canephora is visited by many Trigona sp. T. Large quantities of pollen. A. iridipennis (40). which was considered to be the best candidate for pollen grain transfer (162). and Xylocopa also collected pollen from guava flowers. PSIDIUM GUAJAVA. (referred to as Melipona sp. where stingless bees do not occur. mellifera and bees of the genera Bombus. Trigona fulviventris. Trigona spp. Jaboticaba. Mexico. a sunflowers were visited by F. and rose apple are also visited by stingless bees (Table 1). (85). In India.

SQUASH. NEPHELIUM LAPPACAUM (SAPINDACEAE) Bagged flowers of this androdioecious species set no fruit. foraging on hermaphrodite flowers carried rambutan pollen on their bodies. which suggests that they were not the pollinators (101). may be important owing to their greater interest in collecting pollen (37). halictid bees. spinipes were the most common insects visiting flowers in Brazil (10). honey bees. (probably T.. None of the insects. however. Trigona bees collected pollen and nectar from litchi flowers but did not often touch the stigma. and butterflies. The larger honey bees usually touched the stigmas while visiting the flowers (66). including the stingless bees. CUCURBITA PEPO AND OTHER CUCURBIT CROPS (CUCURBITACEAE) Honey bees and T. and luffa are visited by stingless bees (Table 1).) and honey bees were the most common visitors to flowers of litchi in India in both Uttar Pradesh (96) and West Bengal (21). In tropical regions.CROP POLLINATION BY STINGLESS BEES 195 crops in Australia. particularly large solitary bees and bumble bees. More behavioral observations at other sites are required to determine if this is a common pattern on litchi flowers. Bitter gourd. They coevolved with their hosts in Mexico. but both cross and self pollination result in fruit set (115). SOAP-NUT. Indonesia (148). LYCHEE. wasps. carpenter bees. LITCHI CHINENSIS (SAPINDACEAE) Stingless bees (identified as Melipona but probably Trigona sp. cerana are potential pollinators in East Kalimantan. T. cucumber. RAMBUTAN. stingless bees are sometimes common visitors to sunflowers but are probably rarely important. thoracica and two other species of Trigona were among the most common insects visiting rambutan flowers in Peninsula Malaysia. SAPINDUS EMARGINATUS (SAPINDACEAE) In Southern India. Trigona sp. . Squash bees of the genera Peponapis and Xenoglossa (Anthophorini) rely solely on species of Cucurbita for their pollen and most of their nectar. Five species of Trigona and A. Trigona sp. LITCHI. watermelon. but their low populations relative to those of honey bees led Radford et al to conclude that they have an insignificant role in pollination (106). and stingless bees are occasionally important pollinators of squash (55). locally abundant insects. flies. The wasps and butterflies were considered to deliver more cross pollen. and other bees. Honey bees are usually the most abundant insects visiting sunflowers.. the flowers of the soap-nut tree were visited by a broad spectrum of insects. bumble bees. but they are usually only a small proportion of the complex of visitors (37). including Apis spp. carbonaria) was the most common species visiting flowers of litchi at one site in Australia but was absent at another site (66). but it is often suggested they be introduced to other parts of the world for Cucurbita pollination (146). However.

were the most common insect. A. was rarely collected by two species of Melipona and honey bees but not by N. In Malaysia. cerana and a Trigona sp. as they are odorless and have powdery pollen. CALAMUS SPP. so no self pollination can occur. clavipes were collected while visiting the flowers of Citrus sp. known as tripping. T. Trigona bees as well as drosophilid and phorid flies are attracted to the male and female flowers in Java (151). no visitors were observed to female flowers. can only be performed by a bee of adequate weight. Cajanus cajan. in Surinam (34). were visited by pollen-collecting Trigona (referred to as Melipona sp. but nocturnal visitors were considered more important because pollen release occurs at night (68). 151). Citrus grandis and another Citrus sp. Scaura latitarsus and T. JACKFRUIT. the stingless bee was not common whereas the halictid bee Nomia quadridentata was a frequent and effective pollinator (9). BREADFRUIT. . ARTOCARPUS HETEROPHYLLUS (MORACEAE) Jackfruit has male and female inflorescences (37) and is considered to be insect pollinated on the basis of its scent and sticky pollen (105. and insect-assisted wind pollination is suggested (82). Indigofera endocaphylla. In Brazil. Flowers are said to be wind pollinated. However. This mode of insect-assisted wind pollination may explain why the plants produce nectar (22). mellaria and T. including Trigona itama. 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. hand pollination is practiced to increase fruit set (37. 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). (ARECACEAE) The most important pollinating agents of four species of Calamus in Thailand were Trigona spp. 118). mainly bees. ARTOCARPUS ALTILIS (MORACEAE) A breadfruit tree produces male and female inflorescences alternately. nigra in Trinidad (141). (18). They may have contributed to wind pollination by dislodging pollen grains from the male flowers.196 HEARD RATTAN. are not effective pollinators. fulviventris collected nectar in the morning and pollen in the afternoon from male inflorescences. such as many stingless bees. were the most common visitors to flowers of pigeon pea. In another study. CITRUS SPP. They did not visit female inflorescences and therefore did not effect pollination. is visited in Indonesia by a range of insects. This process.) bees in Java (53). but the former was considered the more effective pollinator (95). as many citrus cultivars are parthenocarpic (135). LEGUMES (LEGUMINOSAE) Indigofera. and hence smaller bees. CITRUS. Evaluation of the importance of bees needs to account for the breeding system. (RUTACEAE) Pollen of Citrus spp. 105. Trigona spp.

nigerrima. T. Melipona fasciata heavily utilized pollen of G. Geotrigona acapulconis. Trigona sp. and Scaptotrigona sp. SESAMUM INDICUM (PEDALIACEAE) The stingless bees Melipona fulva. however. in doing so. superba in Panama (129). and 2 plants per minute. Trigona mazucatoi. though data are lacking (29. The most common visitors to these flowers in Brazil were the stingless bees T. respectively (136). CORIANDER SATIVUM (APIACEAE) Apis spp.) collect pollen from stamens and often climb to the top of stigmas. CANNA INDICA (CANNACEAE) This crop is visited by Trigona sp.CROP POLLINATION BY STINGLESS BEES 197 CORIANDER. iridipennis were the main pollinating insects of coriander near Pune. CHILI. and Bombus (102). 3. are common visitors (DW Roubik. CAPSICUM ANNUUM VARIETIES (SOLANACEAE) Wild bees and honey bees visit C. and 10 umbels (flower heads) per minute and 4.. and C. BELLYACHE BUSH. gossypifolia.) in Java (53). . including stingless bees.to medium-sized pollen-gathering bees such as Trigona. williana. annuum flowers. Trigona spp. were considered the main pollinators of J. EGGPLANT. lurida. SOLANUM MELONGENA (SOLANACEAE) Trigona fulviventris guianae have been recorded visiting the flowers of eggplant (34). are unlikely to effectively pollinate these plants (24). particularly P. S Gazit & G Ish-Am. In Mexico and Guatemala. a medicinal plant in Brazil (94). and T. (referred to as Melipona sp. SWEET PEPPER. iridipennis visited 14. MEMBRILLO. and T. A. effect pollination. SESAME. INDIAN SHOT. mosquito. T. Roubik. (referred to as Melipona sp. cerana. iridipennis visited plots of sesame in India but were observed only on extrafloral nectaries (112). In Java. GUSTAVIA SUPERBA (LECYTHIDAEAE) Flowers of species of membrillo are pollinated by small. was an important pollinator in India (116). are probably not effective pollinators (125). T. CAPSICUM. JATROPHA GOSSYPIFOLIA (EUPHORBIACEAE) Three species of stingless bees. India. 152). Trigona sp. These authors noted that these species were all larger stingless bees and could not explain the absence of smaller species. stated that the smaller bees. Partamona sp. this species is buzz pollinated. The stingless bees forage deep in the flowers collecting nectar and. Melipona. angustula and honey bees (37). AVOCADO. florea. PERSEA AMERICANA (LAURACEAE) Small stingless bees are claimed to be good pollinators of avocado trees. capitata were collected from the flowers of sesame in Surinam (34). and therefore. 13. However. T. potentially transferring pollen (53). A.

crassifolia (12. T. CARLUDOVICA PALMATA (CYCLANTHACEAE) Flowers of C. Honey bees are efficient pollinators but are not strongly attracted to the crop (59). giving a fruit set 4% higher than artificially pollinated plants and 29% higher than open-pollinated controls (157). SAREN. indica in Java (53). In some cases. AGAVE SISALANA (AGAVACEAE) F. RUBBER. NANCHE. In the natural habitats of C. AND ACEROLA. palmata. specialist oil-collecting anthophorine bees are the main pollinators for both B. four species of stingless bees (all Trigona) pollinated C. stingless bees were not observed. was visited by Trigona sp. a crop plant. SISAL. However. cerana. Ceratopogonidae flies are probably the main pollinators (105). However in Amazonian Peru. schrottkyi was observed to visit sisal growing in a garden near Sao Paulo in Brazil (27). small weevils pollinated the flowers (41). HEVEA BRASILIENSIS (EUPHORBIACEAE) Some stingless bees of the genus Trigona collected pollen in India. The stingless bee. was the most common insect visiting cardamom collecting pollen in the morning and nectar in the afternoon. was commonly observed collecting pollen. In Papua New Guinea. In Panama. punicifolia (73). are visited and pollinated by Trigona sp. CARDAMOM. where honey bees only visited extrafloral nectaries (61).198 HEARD personal communication). PANAMA HAT PLANT. iridipennis. This species is mainly pollinated by bats at night and during the day by larger bees (125). a valuable medicinal crop.) and by A. (referred to as Melipona sp. instead the solitary bee Amegilla sapiens efficiently pollinated the flowers (143). personal communication). palmata (134). AMOMUM VILLOSUM (ZINGIBERACEAE) Saren. MALPIGHIA PUNICIFOLIA (MALPIGHIACEAE) Both nanche and acerola crops are visited and occasionally pollinated by stingless bees. A. BYRSONIMA CRASSIFOLIA. T. stingless bees may have a negative impact by removing nectar or . (referred to as Melipona sp. In the New World. fuscipennis are the common visitors (DW Roubik. corvina and T. 117) and M. palmata in Colombia. the honey bee. which suggests they effectively pollinated (25a). ELETTARIA CARDAMOMUM (ZINGIBERACEAE) In India. The pollen foragers made good contact with the anthers and stigma. Crops Visited by Stingless Bees But Pollinated by Other Means Records exist of visitation by stingless bees to the flowers of some crop species that are known to be effectively pollinated only by other means (Table 2).) in Yunnan.

Alfalfa Sunn hemp Black pepper Bananas Passionfruit Rape a Annona spp. 102 119. cacao Brazil nut Mangosteen and relatives Bacuri Benoil Cashew Lucerne. cherimoya. (bees) Bees and flies Large bees. pollen. Xylocopa spp. Oil palm Vanilla Cocoa.g. Annonaceae 86 Elaeis guineensis Vanilla spp. CONCLUSIONS Stingless bees possess many characteristics that enhance their importance as crop pollinators both as wild populations and managed pollinators. making the flowers less attractive to the effective pollinator. (weevils) Eulaema spp. Challenges to their widespread use . Platonia insignis Moringa oleifera Anacardium occidentale Medicago sativa Arecaceae Orchidaceae Sterculiaceae Lecythidaceae Clusiaceae Clusiaceae Moringaceae Anacardiaceae Leguminosae: Papilionoideae Leguminosae: Papilionoideae Piperaceae Musaceae Passifloraceae Brassicaceae Elaeidobius spp. 53 Common name Papaya. Theobroma cacao Bertholletia excelsa Garcinia spp. 132 4 References that demonstrate or review efficacy of pollinator. Passiflora edulis Brassica napus var. Wind or rain Parthenocarpic Carpenter bees Honey bees 42. megachilids. harmlessness) suit them for pollination. atemoya.CROP POLLINATION BY STINGLESS BEES 199 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 butterflies Nitidulidae beetles Referencea 11. 145 32 163 87. papaw Name Carica papaya Family Caricaceae Custard apple. (bees) Ceratopogonidae midges Large euglossine and carpenter bees Parthenocarpic Birds Xylocopa spp. In extreme cases. recruitment. stingless bees have a more obvious negative impact. e. oleifera 53. 120 76 62 39. floral constancy. polylecty. bumble bees Large bees e. such as damaging the flowers of rape (4) or aggressively deterring the effective pollinators of passionfruit (132). 36.g. 50 37 Crotalaria juncea Piper nigrum Musa spp. Characteristics of their social life (perenniality. 90 37 105 26.

thereby reducing reliance on natural populations. Lawson SD. Camargo JMF. 41:553–75 4. Bot. Hence remnant forests within this distance from orchards can provide adequate bee populations. these have been listed to refute the occasional false claims made of the pollinator potential of stingless bees. Algumas plantas visitadas para obten¸ ao de p´ len c˜ o por oper´ rias de Melipona seminigra a merrillae em Manaus.AnnualReviews. macadamia. chayote. and mapati.org Literature Cited 1. Visit the Annual Reviews home page at http://www. Brasil. o a e Rev. Helen Wallace. 7:309–15 3. There are no crops known to be exclusively pollinated by stingless bees. Esp´ cies de e plantas visitadas por Meliponinae (Hymenoptera. I hope this review stimulates the necessary observation. para coleta de p´ len na regi˜ o do m´ dio Amazonas. experimentation. mango. Pollination in Australian orchids: a critical assessment of the literature 1882–1992. J. cupua¸ u. and publication to clarify the importance of this abundant group of insects in world agriculture. Absy ML. Stingless bees display greater diet breadth and range of foraging behavior than honey bees. 1993. 44:227–37 2. ACKNOWLEDGMENTS I am grateful to David Roubik. Ben Oldroyd. 1984. camu-camu. It is clear that these bees provide economic benefits. . Margaret Sedgley. Improved domestication practices would increase hive availability. by their crop pollination services. Kerr WE. carambola. making them likely to be important to future development of pollinators best suited to the needs of particular crops and habitats. Acta Amazon. Apoidea). The foraging flight range often is between 100 and 400 m. Absy ML. and Tad Bartareau for many helpful comments on the manuscript. on the basis of often scanty knowledge. Biol. Adegas JEB. They c make a contribution to the pollination of ∼60 other crop species. Aust. appear to benefit from pollination by these insects. coconut. Stingless bees are confirmed and important pollinators of annatto. There are many crops in many families that. They have been reported visiting ∼20 crop species which are effectively pollinated by other means. Probably many other crops in the tropics are pollinated by stingless bees but have never been recorded in the literature. Kerr WE. and hence forest clearing threatens the role of these insects in crop pollination. Nogueira Couto RH.200 HEARD 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. de A Miranda IP. The absence of natural vegetation is associated with low local populations of stingless bees. that are substantial but not presently quantifiable. 1977. Few generalizations can be drawn about the types of plants that they visit and pollinate. Adams PB.

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