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Annu. Rev. Entomol. 1999. 44:183–206

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, 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 pollina-
tors 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 pol-
linated 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
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consists of ∼50 species, is confined to the neotropics, has more complex com-
munication 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 polli-
nation 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, dis-
eases 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.
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CROP POLLINATION BY STINGLESS BEES 185

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 flightless (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 specific
nesting requirements; some species damage leaves in search of resin (25, 158);
and some species are territorial and fight 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, floral larceny, and diet and seasonal patterns of activity
are reviewed by Roubik (124).
Stingless bees are generalist flower 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 flower 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, neotrop-
ical stingless bees heavily use the introduced Eucalyptus spp. (43, 67). Few
generalizations can be made regarding the plant or flower type preferred by
stingless bees, but it has been suggested they prefer small flowers (161), dense
inflorescences (128), flowers with corolla tubes shorter than the bee’s tongues
(50), flowers with long corolla tubes that are wide enough for the bees to enter
(34), trees (67, 109, 110), and white or yellow flowers (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 floral 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 deposi-

tion of pollen from two or more species reduces the amount of pollen available
and contaminates stigmas with the wrong pollen. In addition to floral 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. Exam-
ples 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 sting-
less bee species may have benefited directly from pollination services of these
bees (123). At the species level, stingless bees are the confirmed 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 ef-
fective pollinators of Spathiphyllum friedrichsthalii (83). Of the 13 Australian
epiphytic orchids whose pollinators are confirmed, 9 are pollinated by sting-
less 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 flowers by stingless bees in which they remove resources
without pollinating, with or without damaging the flowers, occurs in both natural
habitats (124) and agroecosystems (4, 132).
Although many species of stingless bees adapt to artificial nest sites, natural
vegetation can influence 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 fields in Costa Rica
had Trigona bees present, except for two fields with no surrounding forest for
1 km (161). The abundance of Trigona bees on longan flowers in a large orchard
was found to decrease with distance from an adjoining forest (20). Stingless
bees were common visitors to flowers of cupuaçu growing near primary forest
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 attrac-
tiveness 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 flight 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 artificial nectar source and
progressively moving the source away from the hive, the maximum flight range
of Plebeia mosquito, Trigona ruficrus, and Trigona amalthea was 540, 840,
and 980 m, respectively (65). Using a similar technique, 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).
Using the calculated flight speed, the actual flight 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 flight 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 flights 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 flights per day, respectively (58).
A newly established hive of T. minangkabau with only 350 workers made only
about 700 flights per day, showing the strong positive relationship between hive
population and flight 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
rufiventris, and Melipona scutellaris attacked 74, 60, and 14% of non-nestmate
conspecifics encountered (23).
The potential of stingless bees for crop pollination is enhanced by the abil-
ity to transfer colonies into artificial 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,
fiber, spices, and medicines (104, 105, 118, 125). The breeding system and pol-
linators of many of these crops have been catalogued (37, 125). Nearly half of
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188 HEARD

the species of economically significant tropical crops originated in areas where

honey bee species do not occur naturally, i.e. the neotropics, South Pacific, 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.
Difficulties 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 flowers 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

benefit from bee visitation (46), and low bee populations in many orchards
may limit yield and quality (156). The major visitors to flowers 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 fidelity to the crop (154).
No preference was shown by either honey bees or stingless bees for heavily
versus lightly flowering 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 flowering 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 flower. 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 efficient
pollinators (47).
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Table 1 Crops visited and at least occasionally or partially pollinated by stingless bees

Common name Name Family Reference

Crops for which stingless bees make an important contribution to pollination

Macadamia Macadamia integrifolia Proteaceae See text
Chayote, Choko Sechium edule Cucurbitaceae See text
Coconut Cocos nucifera Arecaceae See text
Mango Mangifera indica Anacardiaceae See text
Carambola Averrhoa carambola Oxalidaceae See text
Camu-Camu Myrciaria dubia Myrtaceae See text
Mapati, Uvilla, Amazon Pourouma cecropiaefolia Moraceae See text
Tree Grape
Annatto, Achiote Bixa orellana Bixaceae See text
Cupuaçu Theobroma grandiflorum Sterculiaceae See text
Crops visited and occasionally or partially pollinated by stingless bees
Onion Allium cepa Alliaceae See text
Strawberry Fragaria chiloensis Rosaceae See text
X ananassa
Loquat Eriobotrya japonica Rosaceae 109
Peach Prunus persica Rosaceae. 27
Plum Prunus domestica Rosaceae 20
Pear Pyrus communis Rosaceae 20
Coffee Coffea spp. Rubiaceae See text
Guava Psidium guajava Myrtaceae See text
Jaboticaba Myrciaria cauliflora Myrtaceae 43
Jambolan Syzygium cumini Myrtaceae 34
Rose Apple Syzygium jambos Myrtaceae 27, 53, 56
Sunflower Helianthus annuus Asteraceae See text
Niger Guizotia abyssinica Asteraceae 114
Litchi, Lychee Litchi chinensis Sapindaceae See text
Longan Euphoria longan Sapindaceae 20
Rambutan Nephelium lappaceum Sapindaceae See text
Soap-Nut Sapindus emarginatus Sapindaceae See text
Ackee Blighia sapida Sapindaceae 69
Guaraná Paullinia cupana Sapindaceae 102
Squash Cucurbita pepo Cucurbitaceae See text
Bitter Gourd Momordica charantia Cucurbitaceae 34, 141
Watermelon Citrullus lanatus Cucurbitaceae 16, 80
Cucumber Cucumis sativus Cucurbitaceae 16
Luffa Luffa acutangula Cucurbitaceae 16
Indian Jujube Zizyphus mauritiana Rhamnaceae 107
Peach Palm, Pejibaye Bactris gasipaes Arecaceae 84
Sago Palm Metroxylon sagu Arecaceae 150
Rattan Calamus spp. Arecaceae 18, 68
Breadfruit Artocarpus altilis Moraceae See text
Jackfruit Artocarpus heterophyllus Moraceae See text
Ice Cream Bean, Sipo, Inga edulis Leg.: Mimosoideae 1, 2
Guamo

(Continued)
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190 HEARD

Table 1 (Continued)

Common name Name Family Reference

Leucaena Leucaena leucocephala Leg.: Mimosoideae 56

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

CHAYOTE, CHOKO, SECHIUM EDULE (CUCURBITACEAE) The vines that produce

the subtropical vegetable chayote are monoecious, producing both male and
female flowers on all plants. The plant is considered a good source of nec-
tar for honey bees in the United States (77). In Costa Rica, many species of
bees and wasps visited chayote flowers, but the only important ones, on the
basis of abundance and efficiency, 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 stin-
gless bees produced fruit. Those open and visited by other bees and wasps
produced fruit but in reduced quantities. Furthermore, two fields 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 co-
conut flowers in Hawaii, India, Malaysia, the Philippines, Trinidad, Ecuador
(37), and Fiji (77). Stingless bees, both Melipona spp. and others, are the dom-
inant 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, flies (37), butter-
flies, and beetles (51) have also been recorded but are not considered effective
pollinators. Stingless bees visit both male and female flowers (51). Most (83%)
individuals visiting pistillate flowers in search of nectar carried loads of coconut
pollen from previously visited staminate flowers. Many of these (33%) then vis-
ited staminate flowers on the same inflorescence. This behavior is conducive
to efficient 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 flowers are unspecialized, allowing pollination by
most visiting insects. Stingless bees are the most common insects visiting mango
flowers 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 efficient pollinators on the basis
of the proportions of flowers pollinated after a visit. This efficiency 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 flowers and are only occasionally observed
(37, 77). Flies are the most common visitors to mango flowers in many parts of
the tropics (37) and are probably also efficient pollinators. Thus, stingless bees
and flies are the most important pollinators of this crop.
CARAMBOLA, AVERRHOA CARAMBOLA (OXALIDACEAE) The distylous flowers of
carambola require cross pollination to achieve fruit yield (37). M. favosa have
been recorded visiting the flowers of carambola in Surinam (34). Large num-
bers of two bee species, Trigona thoracica and Apis cerana visited flowers of
carambola in orchards in Malaysia. Both bee species carried large numbers
of pollen grains on their bodies. T. thoracica was an efficient pollinator, with
hundreds of successfully germinated pollen grains deposited on flowers that
were bagged and then exposed to one bee visit. Control flowers left bagged
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192 HEARD

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 flowers camu-camu. Although wind may effect some pollina-
tion, bees are the most important pollinators and are attracted by the fragrance
and nectar of the flowers. The most common visitors to camu-camu in Ama-
zonian 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 flowers 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 flowers
frequently and carried many pollen grains on their legs and bodies. Activity
was greatest in the morning, when bees first visited the male flowers collecting
pollen and then rapidly visited the female flowers. Bagged flowers did not set
fruit, but pollination was not limiting because of the many bees attracted to the
flowers and their effective pollinator behavior (35).

ANNATTO, ACHIOTE, BIXA ORELLANA (BIXACEAE) Annatto is efficiently buzz

pollinated by large bees including the stingless bee Melipona melanoventer.
The non–buzz 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. rufiventris in Amazonas (1).

CUPUAÇU, THEOBROMA GRANDIFLORUM (STERCULIACEAE) Near Belem, flow-

ers of the cupuaçu fruit tree are visited by stingless bees, especially Plebeia
minima, and small weevils. Most plants were self incompatible, and the behav-
ior 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 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
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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 benefit from insect vis-
itation. A review of world studies shows that various species of bees and flies
are the most common flower 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 intro-
duced to an experimental farm. T. iridipennis accounted for almost half of all
visits to onion flowers, with A. cerana and Apis florea accounting for most of
the remainder. All species foraged throughout the day. The Apis spp. visited ap-
proximately twice as many flowers 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 efficiency of the three bee
species was not determined (81). Honey bees and stingless bees were the most
common insects visiting onion flowers in Brazil (6, 70). The stingless bees did
not pollinate as efficiently as Apis spp., but they were still important (70).
STRAWBERRY, FRAGARIA CHILOENSIS X ANANASSA (ROSACEAE) Imported stin-
gless bees have been evaluated in Japan for pollination of strawberries in
glasshouses. Colonies of T. minangkabau from Sumatra and honey bees both
efficiently pollinated flowers. The number of flowers 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 flower 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 flower. Foraging by T. minangkabau was
more suited to the confined 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 efficient, with
flowers 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 flies are also efficient (37).
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194 HEARD

COFFEE, COFFEA SPP. (RUBIACEAE) Honey bees and stingless bees visited
Coffea arabica flowers in Brazil (92). The larger honey bees and Melipona
spp. were perhaps more efficient pollinators than the smaller species of sting-
less bees. In highland central America, Trigona nigerrima, Trigona fulviventris,
and T. angustula were the most common stingless bee visitors of the flowers
(126). In Chiapas, Mexico, T. angustula are common visitors (142). In Papua
New Guinea, Trigona spp. were the most abundant visitors on heavily flower-
ing Coffea canephora plants but were absent from isolated flowering 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 flowers 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 flowers. 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 polli-
nation 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 efficacy as pollinators are unknown.

SUNFLOWER, HELIANTHUS ANNUUS (ASTERACEAE) Near São Paulo in Brazil,

sunflowers were visited by F. schrottkyi (27) and T. spinipes, Trigona hyalinata,
and Geotrigona sp. (85). In India, sunflower 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 sunflower 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 sunflower
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CROP POLLINATION BY STINGLESS BEES 195

crops in Australia, 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). Honey bees are usually the most abundant insects visiting sunflowers;
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 sunflowers
but are probably rarely important.

LITCHI, LYCHEE, LITCHI CHINENSIS (SAPINDACEAE) Stingless bees (identified as

Melipona but probably Trigona sp.) and honey bees were the most common
visitors to flowers of litchi in India in both Uttar Pradesh (96) and West Bengal
(21). Trigona sp. (probably T. carbonaria) was the most common species visit-
ing flowers of litchi at one site in Australia but was absent at another site (66).
Trigona bees collected pollen and nectar from litchi flowers but did not often
touch the stigma. The larger honey bees usually touched the stigmas while vis-
iting the flowers (66). More behavioral observations at other sites are required
to determine if this is a common pattern on litchi flowers.

RAMBUTAN, NEPHELIUM LAPPACAUM (SAPINDACEAE) Bagged flowers 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 flowers in Peninsula Malaysia. None of the insects, including the
stingless bees, foraging on hermaphrodite flowers carried rambutan pollen on
their bodies, which suggests that they were not the pollinators (101).

SOAP-NUT, SAPINDUS EMARGINATUS (SAPINDACEAE) In Southern India, the

flowers of the soap-nut tree were visited by a broad spectrum of insects, in-
cluding Apis spp., Trigona sp., and other bees, wasps, flies, and butterflies. The
wasps and butterflies 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 flowers 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 intro-
duced 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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196 HEARD

RATTAN, CALAMUS SPP. (ARECACEAE) The most important pollinating agents of

four species of Calamus in Thailand were Trigona spp. (18). In Malaysia, Trig-
ona 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 inflorescences alternately, so no self pollination can occur.
Flowers are said to be wind pollinated, as they are odorless and have pow-
dery 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 inflorescences. They did not visit female inflorescences and there-
fore did not effect pollination. They may have contributed to wind pollination
by dislodging pollen grains from the male flowers. This mode of insect-assisted
wind pollination may explain why the plants produce nectar (22).

JACKFRUIT, 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, 151). Trigona bees as well as drosophilid
and phorid flies are attracted to the male and female flowers in Java (151). In
another study, no visitors were observed to female flowers, 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. How-
ever, the stingless bee was not common whereas the halictid bee Nomia quadri-
dentata was a frequent and effective pollinator (9). A. cerana and a Trigona sp.
were the most common visitors to flowers 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 flowers 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. florea, and T. iridipennis visited 14, 13, and 10 umbels (flower 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 flowers. The most common visitors
to these flowers 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 flowers of eggplant (34). However,
this species is buzz pollinated, and therefore, Trigona spp. are unlikely to ef-
fectively 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 flowers 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 ob-
served only on extrafloral 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 flowers collecting nectar and, in doing so, effect pollination.

MEMBRILLO, GUSTAVIA SUPERBA (LECYTHIDAEAE) Flowers of species of mem-

brillo 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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198 HEARD

personal communication). Honey bees are efficient 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. iridipen-
nis, 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 efficiently pollinated the flowers (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 artificially 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 ex-
trafloral nectaries (61). In the New World, Ceratopogonidae flies 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 flowers (41).
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
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
Common name Name Family of fertilization Referencea

Papaya, papaw Carica papaya Caricaceae Sphingidae and other 11, 36, 53
crepuscular moths
and butterflies
Custard apple, Annona spp. Annonaceae Nitidulidae beetles 86
cherimoya,
atemoya,
Oil palm Elaeis guineensis Arecaceae Elaeidobius spp. 42, 145
(weevils)
Vanilla Vanilla spp. Orchidaceae Eulaema spp. (bees) 32
Cocoa, cacao Theobroma cacao Sterculiaceae Ceratopogonidae 163
midges
Brazil nut Bertholletia excelsa Lecythidaceae Large euglossine and 87, 102
carpenter bees
Mangosteen Garcinia spp. Clusiaceae Parthenocarpic 119, 120
and relatives
Bacuri Platonia insignis Clusiaceae Birds 76
Benoil Moringa oleifera Moringaceae Xylocopa spp. (bees) 62
Cashew Anacardium Anacardiaceae Bees and flies 39, 50
occidentale
Lucerne, Medicago sativa Leguminosae: Large bees, e.g. 37
Alfalfa Papilionoideae megachilids,
bumble bees
Sunn hemp Crotalaria juncea Leguminosae: Large bees e.g. 53, 90
Papilionoideae Xylocopa spp.
Black pepper Piper nigrum Piperaceae Wind or rain 37
Bananas Musa spp. Musaceae Parthenocarpic 105
Passionfruit Passiflora edulis Passifloraceae Carpenter bees 26, 132
Rape Brassica napus Brassicaceae Honey bees 4
var. oleifera
a
References that demonstrate or review efficacy of pollinator.

pollen, making the flowers less attractive to the effective pollinator. In extreme
cases, stingless bees have a more obvious negative impact, such as damaging
the flowers 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. Character-
istics of their social life (perenniality, polylecty, floral constancy, recruitment,
harmlessness) suit them for pollination. Challenges to their widespread use
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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.
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 flight 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 benefit from pollination by these insects. Stin-
gless bees are confirmed and important pollinators of annatto, camu-camu,
chayote, coconut, cupuaçu, carambola, macadamia, mango, and mapati. They
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 benefits, by their crop
pollination services, that are substantial but not presently quantifiable. Sting-
less 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 stim-
ulates 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.
Visit the Annual Reviews home page at
http://www.AnnualReviews.org

Literature Cited

1. Absy ML, Camargo JMF, Kerr WE,
de A Miranda IP. 1984. Espécies de
plantas visitadas por Meliponinae (Hy-
menoptera; Apoidea), para coleta de
pólen na região do médio Amazonas.
Rev. Brasil. Biol. 44:227–37
2. Absy ML, Kerr WE. 1977. Algumas
plantas visitadas para obtenção de pólen
por operárias de Melipona seminigra
merrillae em Manaus. Acta Amazon.
7:309–15
3. Adams PB, Lawson SD. 1993. Pollina-
tion in Australian orchids: a critical as-
sessment of the literature 1882–1992.
Aust. J. Bot. 41:553–75
4. Adegas JEB, Nogueira Couto RH.
P1: KKK/plb P2: ARS/KKK/plb QC: ARS/anil T1: KKK
November 4, 1998 11:18 Annual Reviews
CROP POLLINATION BY STINGLESS BEES
1992. Entomophilous pollination in rape
(Brassica napus L. var. oleifera) in
Brazil. Apidologie 23:203–9
5. Ågren J, Schemske DW. 1991. Polli-
nation by deceit in a neotropical mo-
noecious herb, Begonia involucrata.
Biotropica 23:235–41
6. Alves SB, Vendramim JD, Silveira Neto
S, Nakano O. 1982. Polinização ento-
mofila da cebola Allium cepa L. Solo
74:18–22
7. Anderson DL, Sedgley M, Short JRT,
Allwood AJ. 1982. Insect pollination of
mango in Northern Australia. Aust. J.
Agric. Res. 33:541–48
8. Appanah S. 1982. Pollination of andro-
dioecious Xerospermum intermedium
Radlk. (Sapindaceae) in a rain forest.
Biol. J. Linn. Soc. 18:11–34
9. Atmowidjojo A-H, Adisoemarto S.
1986. Potential pollen-transferring in-
sects of Indigofera spp. Treubia 29:225–
35
10. Avila CJ, Martinho MR, de Campos
JP. 1989. Polinização e polinizadores
na produção de frutos e sementes
hı́bridas de abobora (Cucurbita pepo var.
melopepo). Anais Soc. Entomol. Bras.
18:13–19
11. Baker HG. 1976. “Mistake” pollination
as a reproductive system with special
reference to the Caricaceae. In Tropical
Trees: Variation, Breeding and Conser-
vation, ed. J Burley, BT Styles, pp. 161–
69. London: Academic
12. Barros MAGe. 1992. Fenologia da
floração, estrategias reprodutivas e
polinização de especies simpatricas do
genero Byrsonima Rich. (Malpighi-
aceae). Rev. Brasil. Biol. 52:343–53
13. Batra SW. 1967. Crop pollination and
the flower relationships of the wild bees
of Ludhiana, India. J. Kans. Entomol.
Soc. 40:164–77
14. Bawa KS. 1977. The reproductive bi-
ology of Cupania guatemalensis Radlk.
(Sapindaceae). Evolution 31:52–63
15. Deleted in proof
16. Bhambure CS. 1958. Further studies on
the importance of honey bees in the pol-
lination of Cucurbetacea. Indian Bee J.
20:10–12
17. Bichee SL, Sharma M. 1988. Effect of
different modes of pollination in sun-
flower Helianthus annuus L. (Composi-
tae) sown on different dates by Trigona
iridipennis Smith. Apiacta 23:65–68
18. Bogh A. 1996. The reproductive phe-
nology and pollination biology of four
Calamus (Arecaceae) species in Thai-
land. Principes 40:5–15
AR074-08
201
19. Bohart GE. 1972. Management of wild
bees for the pollination of crops. Annu.
Rev. Entomol. 17:287–312
20. Boonithee A, Juntawong N, Pechhacker
H, Hüttinger E. 1991. Floral visits to se-
lect crops by four Apis species and Trig-
ona sp. in Thailand. Int. Symp. Pollin.,
6th, Tilburg, Acta Hort. 288:74–80
21. Brahmachary RL, Saha L, Mondal AK,
Dasgupta P, Paul P. 1980. Apis florea
and dammar bees (Trigonidae): as the
pollinating agents of certain fruit trees
in Bengal. Proc. State-Level Sem. Bee-
keep., West Bengal, pp. 63–66. West
Bengal: Gobardanga Renaiss. Inst.
22. Brantjes NBM. 1981. Nectar and the pol-
lination of bread fruit, Artocarpus altilis
(Moraceae). Acta Bot. Néerl. 30:345–52
23. Breed MD, Page RE J. 1991. Intra-
and interspecific nestmate recognition
in Melipona workers (Hymenoptera:
Apidae). J. Insect Behav. 4:463–69
24. Buchmann SL. 1995. Pollen, anthers and
dehiscence. In Pollination of Cultivated
Plants in the Tropics, ed. DW Roubik,
pp. 121–23. Rome: Food Agric. Org.
25. Camacho E. 1966. Daño que las abe-
jas jicotes del género Trigona causan
a los árboles de Macadamia. Turrialba
16:193–94
25a. Chandran K, Rajan P, Joseph D, Surya-
narayana MC. 1983. Studies on the role
of honeybees in the pollination of car-
damom. Proc. Internatl Conf. Apicul-
ture Tropical Climates, 2nd, New Delhi,
1980, pp 497–504. New Delhi: Indian
Agricultural Research Institute
26. Corbet SA, Willmer PG. 1980. Pollina-
tion of the yellow passionfruit: nectar,
pollen and carpenter bees. J. Agric. Sci.
95:655–66
27. Cortopassi-Laurino M, Knoll FRN,
Ribeiro MF, Heemert Cvan, Ruijter Ade.
1991. Food plant preferences of Frie-
sella schrottkyi. Acta Hort. 288:382–85
28. Cortopassi-Laurino M, Ramalho M.
1988. Pollen harvest by Africanized Apis
mellifera and Trigona spinipes in Sao
Paulo botanical and ecological views.
Apidologie 19:1–23
29. Crane E. 1992. The past and present sta-
tus of beekeeping with stingless bees.
Bee World 73:29–42
29a. da Silva MF. 1976. Insetos que visi-
tam o ‘cupuaçu’, Theobroma grandiflo-
rum (Willd. ex Spring.) Schum. (Stercu-
liaceae), e ı́ndice de ataque nas folhas.
Acta Amazon. 6:49–54
30. DeGrandi-Hoffman G, Hoopingarner R,
Klomparens K. 1986. Influence of honey
bee (Hymenoptera: Apidae) in-hive
P1: KKK/plb P2: ARS/KKK/plb QC: ARS/anil T1: KKK
November 4, 1998 11:18 Annual Reviews
202 HEARD
pollen transfer on cross-pollination and
fruit set in apple. Environ. Entomol.
15:723–25
31. Delfinado-Baker M, Baker EW, Phoon
ACG. 1989. Mites (Acari) associated
with bees (Apidae) in Asia, with de-
scription of a new species. Am. Bee J.
129:609–13
32. Dressler RL. 1981. The Orchids. Cam-
bridge: Harvard Univ. Press
33. Eickwort GC, Ginsberg HS. 1980. For-
aging and mating behavior in Apoidea.
Annu. Rev. Entomol. 25:421–46
34. Engel MS, Dingemans-Bakels F. 1980.
Nectar and pollen resources for sting-
less bees (Meliponinae, Hymenoptera)
in Surinam (South America). Apidolo-
gie 11:341–50
35. Falcão M A, Lleras E. 1980. Aspectos
fenológicos, ecológicos e de produtivi-
dade do mapati (Pourouma cecropiifolia
Mart.). Acta Amazon. 10:711–24
36. Free JB. 1975. Observations on the pol-
lination of papaya (Carica papaya L.) in
Jamaica. Trop. Agric. 52:275–79
37. Free JB. 1993. Insect Pollination of
Crops. London: Academic
38. Free JB, Williams IH. 1976. Insect
pollination of Anacardium occidentale
L., Mangifera indica L., Blighia sap-
ida Koenig and Persea americana Mill.
Trop. Agric. 53:125–39
39. Freitas BM, Paxton RJ. 1996. The role of
wind and insects in cashew (Anacardium
occidentale) pollination in NE Brazil. J.
Agric. Sci. 126:319–26
40. Goel SC, Kumar A. 1981. Population ag-
gregate of Melipona iridipennis Smith
(Apidae) on sunflower. Indian J. Hort.
38:125–28
41. Gottsberger G. 1991. Pollination of
some species of the Carludovicoideae,
and remarks on the origin and evolution
of the Cyclanthaceae. Bot. Jahrb. Syst.
Pflanzengesch. Pflanzengeogr. 113:221–
35
42. Greathead DJ. 1983. The multi-million
dollar weevil that pollinates oil palms.
Antenna 7:105–7
43. Guibu LS, Ramalho M, Kleinert-
Giovannini A, Imperatriz-Fonseca VL.
1988. Exploração dos recursos florais
por colônias de Melipona quadrifasci-
ata (Apidae, Meliponinae). Rev. Brasil.
Biol. 48:299–305
44. Heard TA. 1987. Preliminary studies on
the role of Trigona bees in the pollination
of macadamia. Proc. Aust. Macadamia
Res. Workshop, 2nd, Bangalow, ed. T
Trochoulias, I Skinner, pp. 192-97. New
South Wales: Government Print.
AR074-08
45. Heard TA. 1988. Propagation of hives
of Trigona carbonaria Smith (Hy-
menoptera: Apidae). J. Aust. Entomol.
Soc. 27:303–4
46. Heard TA. 1993. Pollinator require-
ments and flowering patterns of Maca-
damia integrifolia. Aust. J. Bot. 41:491–
97
47. Heard TA. 1994. Behaviour and pollina-
tor efficiency of stingless bees and honey
bees on macadamia flowers. J. Apic. Res.
33:191–98
48. Heard TA, Exley EM. 1994. Diversity,
abundance, and distribution of insect
visitors to macadamia flowers. Environ.
Entomol. 23:91–100
49. Heard TA, Hendrikz JK. 1993. Factors
influencing flight activity of colonies
of the stingless bee Trigona carbonaria
(Hymenoptera: Apidae). Aust. J. Zool.
41:343–53
50. Heard TA, Vithanage V, Chacko EK.
1990. Pollination biology of cashew in
the Northern Territory of Australia. Aust.
J. Agric. Res. 41:1101–14
51. Hedström I. 1986. Pollen carriers of Co-
cos nucifera L. (Palmae) in Costa Rica
and Ecuador (Neotropical region). Rev.
Biol. Trop. 34:297–301
52. Hedström I. 1988. Pollen carriers and
fruit development of Psidium guajava L.
(Myrtaceae) in the Neotropical region.
Rev. Biol. Trop. 36:551–53
53. Heide F. 1923. Bloembestuiving in
West-Java. Meded. Alg. Proefstn. Land-
bou 14:20–37
54. Henderson A. 1988. Pollination biol-
ogy of economically important palms.
In The Palm-Tree of Life: Biology, Uti-
lization and Conservation. Proc. Symp.
Soc. Econ. Bot., New York, pp. 36–41.
New York: NY Bot. Gard.
55. Hurd P. 1966. The pollination of pump-
kins, gourds and squashes (genus Cucur-
bita). Proc. Int. Symp. Pollin. 2nd, Lon-
don, Bee World Suppl. 47:97–98
56. Imperatriz-Fonseca VL, Kleinert-Gio-
vannini A, Ramalho M. 1989. Pollen
harvest by eusocial bees in a non-natural
community in Brazil. J. Trop. Ecol. 5:
239–42
57. Inoue T, Sakagami SF, Salmah S, Nuk-
mal N. 1984. Discovery of successful
absconding in the stingless bee Trigona
(Tetragonula) laeviceps. J. Apic. Res. 23:
136–42
58. Inoue T, Salmah S, Abbas I, Yusuf
E. 1985. Foraging behavior of indi-
vidual workers and foraging dynamics
of colonies of three Sumatran stingless
bees. Res. Popul. Ecol. 27:373–92
P1: KKK/plb P2: ARS/KKK/plb QC: ARS/anil T1: KKK
November 4, 1998 11:18 Annual Reviews
CROP POLLINATION BY STINGLESS BEES
59. Ish-Am G, Eisikowitch D. 1993. The
behaviour of honey bees (Apis mellif-
era) visiting avocado (Persea ameri-
cana) flowers and their contribution to
its pollination. J. Apic. Res. 32:175–
86
60. Iwama S, Melhem TS. 1979. The pollen
spectrum of the honey of Tetragonisca
angustula angustula Latreille (Apidae,
Meliponinae). Apidologie 10:275–95
61. Jayarathnam K. 1970. Hevea brasilensis
as a source of honey. J. Palynol. 6:101–
3 Proc. Int. Symp. Poll., 7th, Lethbridge,
62. Jyothi PV, Atluri JB, Reddi CS. 1990.
Pollination ecology of Moringa oleifera
(Moringaceae). Proc. Indian Acad. Scis.
Plant Sci. 100:32–42
63. Kakutani T, Inoue T, Tezuka T, Maeta
Y. 1993. Pollination of strawberry by
the stingless bee, Trigona minangkabau,
and the honey bee, Apis mellifera: an
experimental study of fertilization effi-
ciency. Res. Popul. Ecol. 35:95–111
64. Kato M. 1996. Plant-pollinator interac-
tions in the understory of a lowland
mixed dipterocarp forest in Sarawak.
Am. J. Bot. 83:732–43
65. Kerr WE. 1959. Biology of meliponids
VI Aspects of food gathering and pro-
cessing in some stingless bees. In Food
Gathering Behavior of Hymenoptera.
Symp. Entomol. Soc. Am., pp. 24–31.
Detroit: Entomol. Soc. Am.
66. King J, Exley EM, Vithanage V. 1988.
Insect pollination for yield increases in
lychee. Proc. Aust. Conf. Tree Nut Crops,
4th, Lismore, ed. D Batten, pp. 142–45.
Lismore: Exotic Fruit Grow. Assoc.
67. Kleinert-Giovannini A, Imperatriz-
Fonseca VL. 1987. Aspects of the
trophic niche of Melipona marginata
marginata Lepeletier (Apidae, Melipon-
inae). Apidologie 18:69–100
68. Lee YF, Jong K, Swaine MD, Chey VK,
Chung AYC. 1995. Pollination in the rat-
tans Calamus subinermis and C. cae-
sius (Palmae: Calamoideae). Sandaka-
nia 6:15–39
69. Lobreau-Callen D, Thomas Ale,
Darchen B, Darchen R. 1990. Quelques
facteurs déterminant le comportement
de butinage d’Hypotrigona pothieri
(Trigonini) dans la végétation de
Côte-d’Ivoire. Apidologie 21:69–83
70. Lorenzon MCA, Rodrigues AG, Des-
ouza JRGC. 1993. Comportamento
polinizador de Trigona spinipes (Hy-
menoptera, Apidae) na florada da ce-
bola (Allium cepa L.) hı́brida. Pesq.
Agropecu. Brasil. 28:217–21
71. Lughadha EN, Proença C. 1996. A
AR074-08
203
survey of the reproductive biology of the
Myrtoideae (Myrtaceae). Ann. Mo. Bot.
Gard. 83:480–503
72. Maeta Y, Tezuka T, Nadano H, Suzuki
K. 1992. Utilization of the Brazilian stin-
gless bee, Nannotrigona testaceicornis,
as a pollinator of strawberries. Honeybee
Sci. 13:71–78
73. Magalhaes LMF, Oliveira Dde, Ohashi
OS. 1997. Pollination and pollen vec-
tors in acerola, Malpighia punicifolia L.
In Pollination: from theory to practise,
Acta Hort. 437:419–23
74. Ması́s CE, Lezama HJ. 1991. Estudio
preliminar sobre insectos polinizadores
de macadamia en Costa Rica. Turrialba
41:520–23
75. Maues MM, Venturieri GC. 1995. Pol-
lination biology of anatto and its polli-
nators in Amazon area. Honeybee Sci.
16:27–30
76. Maués MM, Venturieri GC. 1997. Pol-
lination ecology of Platonia insignis
Mart. (Clusiaceae), a fruit tree from
eastern Amazon region. In Pollination:
From Theory to Practise, Proc. Int.
Symp. Pollin., 7th, Lethbridge, Alberta,
Canada, ed. KW Richards, pp. 255–
59. Lethbridge, Alberta, Can.: Agric. &
Agri-Food Can.
77. McGregor SE. 1976. Insect Pollination
of Cultivated Crop Plants, Agriculture
Handbook No. 496. Washington, DC:
US Dep. Agric.
78. Michener CD. 1974. The Social Behav-
ior of the Bees. Cambridge, MA: Belk-
nap, Harvard Univ. Press
79. Michener CD. 1990. Classification of
the Apidae (Hymenoptera). Univ. Kans.
Sci. Bull. 54:75–164
80. Mohana Rao G, Suryanarayana MC.
1988. Studies on pollination of wa-
termelon [Citrullus lanatus (Thunb.)
Mansf.]. Indian Bee J. 50:5–8
81. Mohanrao G, Lazar M. 1980. Studies on
bee behaviour and pollination in onion.
Khadigramodyog 26:378–83
82. Moncur MW. 1985. Floral ontogeny of
the jackfruit, Artocarpus heterophyllus.
Aust. J. Bot. 33:585–93
83. Montalvo AM, Ackerman JD. 1986.
Relative pollinator effectiveness and
evolution of floral traits in Spathiphyl-
lum friedrichsthalii (Araceae). Am. J.
Bot. 73:1665–76
84. Mora Urpı́ J, Solı́s EM. 1980. Po-
linización en Bactris gasipaes H.B.K.
(Palmae). Rev. Biol. Trop. 28:153–74
85. Moreti AC CC, Marchini LC. 1992.
Observacoes sobre as abelhas visitantes
P1: KKK/plb P2: ARS/KKK/plb QC: ARS/anil T1: KKK
November 4, 1998 11:18 Annual Reviews
204 HEARD
da cultura do girassol (Helianthus an-
nuus L.) em Piracicaba, SP. Zootecnia
30:21–27
86. Nadel H, Peña JE. 1994. Identity, be-
havior, and efficacy of nitidulid beetles
(Coleoptera: Nitidulidae) pollinating
commercial Annona species in Florida.
Environ. Entomol. 23:878–86
87. Nelson BW, Absy ML, Barbosa EM,
Prance GT. 1985. Observations on
flower visitors to Bertholletia excelsa
H.B.K. and Couratari tenuicarpa A.C.
Sm. (Lecythidaceae). Acta Amazon.
15:225–34
88. Nieh JC, Roubik DW. 1995. A stingless
bee (Melipona panamica) indicates food
location without using a scent trail. Be-
hav. Ecol. Sociobiol. 37:63–70
89. Deleted in proof
90. Nogueira-Couto RH, Costa JA, Silveira
RCM, Couto LA. 1992. Polinização de
Crotalaria juncea por abelhas nativas.
Ecossistema 17:12–16
91. Nogueira-Neto P. 1997. Vida e Criação
de Abelhas Indı́genas sem Ferrão. São
Paulo: Ed. Nogueirapis
92. Nogueira-Neto P, Carvalho A, Antunes
H. 1959. Efeito da exclusão dos inse-
tos pollinizadores na produção do café
bourbon. Bragantia 18:441–68
93. Ormond WT, Pinheiro MCB, de Castells
ARC. 1984. Contribuição ao estudo da
reprodução e biologia floral de Jatropha
gossypifolia L. (Euphorbiaceae). Rev.
Brasil Biol. 44:159–67
94. O’Toole C. 1993. Diversity of native
bees and agroecosystems. In Hymenop-
tera and Biodiversity, ed. J LaSalle, ID
Gauld, pp. 169–96. Wallingford, UK:
CAB Int.
95. Pande YD, Bandyopadhyay S. 1985.
The foraging behaviour of honey bees
on flowers of pigeon pea (Cajanus ca-
jan) in Agartala, Tripura. Indian Bee J.
47:13–15
96. Pandey RS, Yadava RPS. 1970. Polli-
nation of litchi (Litchi chinensis) by in-
sects with special reference to honeybees
(Apis spp.) in India. J. Apic. Res. 9:103–
5 preferences. Apidologie 20:185–95
97. Parker FD, Batra SWT, Tepedino VJ.
1987. New pollinators for our crops.
Agric. Zool. Rev. 2:279–304
98. Pereira-Noronha MR, Gottsberger I,
Gottsberger G. 1982. Biologia floral de
Stylosanthes (Fabaceae) no serrado de
Botacatu, estado de São Paulo. Rev.
Brasil. Biol. 42:595–605
99. Peters C, Vasquez A. 1986. Estudios
ecológicos de camu-camu (Myrciaria
dubia) I. Producción de frutas en pobla-
AR074-08
ciones naturales. Acta Amazon. 16–17:
161–74
100. Phoon A, Suhaimi A, Marshall A. 1984.
The pollination of some Malaysian
fruit trees. Simp. Biol. Kebangsaan,
1st, Kebangsaan, pp. 87–111. Selangor
Malaysia: Bangi
101. Phoon ACG. 1985. Pollination and
fruit production of carambola, Aver-
rhoa carambola, in Malaysia. Proc. Int.
Conf. Apic. Trop. Climat., 3rd , Nairobi,
Kenya, London: Int. Bee Res. Inst.
102. Prance GT. 1985. The pollination of
Amazonian plants. In Key Environ-
ments: Amazonia, ed. GT Prance, TE
Lovejoy, pp. 166–91. Cambridge: Perg-
amon
103. Prance GT, Anderson AB. 1976. Stud-
ies on the floral biology of neotropical
Nymphaeaceae. 3. Acta Amazon. 6:163–
70
104. Purseglove J. 1968. Tropical Crops: Di-
cotyledons. London: Longman
105. Purseglove J. 1972. Tropical Crops Mo-
nocotyledons. London: Longman
106. Radford B, Nielsen R, Rhodes J. 1979.
Agents of pollination in sunflower crops
on the central Darling Downs, Queens-
land. Aust. J. Exp. Agric. Anim. Husb.
19:565–69
107. Rama Devi K, Atluri JB, Subba Reddi
C. 1989. Pollination ecology of Zizyphus
mauritiana (Rhamnaceae). Proc. Indian
Acad. Sci. Plant Sci. 99:223–39
108. Ramalho M, Giannini TC, Malagodi-
braga KS, Imperatriz-Fonseca VL. 1994.
Pollen harvest by stingless bee foragers
(Hymenoptera, Apidae, Meliponinae).
Grana 33:239–44
109. Ramalho M, Imperatriz-Fonseca VL,
Kleinert-Giovannini A, Cortopassi-Lau-
rino M. 1985. Exploitation of floral re-
sources by Plebeia remota Holmberg
(Apidae, Meliponinae). Apidologie 16:
307–29
110. Ramalho M, Kleinert-Giovannini A,
Imperatriz-Fonseca VL. 1989. Utiliza-
tion of floral resources by species of
Melipona (Apidae, Meliponinae): floral
111. Ramı́rez BW, Gómez PL. 1978. Pro-
duction of nectar and gums by flowers
of Monstera deliciosa (Araceae) and of
some species of Clusia (Guttiferae) col-
lected by New World Trigona bees. Bre-
nesia 14–15:407–12
112. Rao GM, Lazar M, Suryanarayana MC.
1981. Foraging behaviour of honeybees
in sesame (Sesamum indicum L.). Indian
Bee J. 43:97–100
113. Rao GM, Suryanarayana MC. 1989.
P1: KKK/plb P2: ARS/KKK/plb QC: ARS/anil T1: KKK
November 4, 1998 11:18 Annual Reviews
CROP POLLINATION BY STINGLESS BEES
Effect of honey bee pollination on seed
yield in onion (Allium cepa L.). Indian
Bee J. 51:9–11
114. Rao GM, Suryanarayana MC. 1990.
Studies on the foraging behaviour of
honey bees and its effect on the seed
yield in Niger. Indian Bee J. 52:31–33
115. Reddi CS, Reddi EUB, Reddi NS,
Reddi PS. 1983. Reproductive ecology
of Sapindus emarginatus Vahl (Sapin-
daceae). Proc. Indian Natl. Sci. Acad. B
49:57–72
116. Reddi EUB, Reddi CS. 1983. Pollination
ecology of Jatropha gossypiifolia (Eu-
phorbiaceae). Proc. Indian Acad. Sci.
Plant Sci. 92:215–31
117. Rego MMC, de Albuquerque PMC.
1989. Comportamento das abelhas vis-
itantes de murici, Byrsonima crassifo-
lia (L.) Kunth, Malpighiaceae. Bol. Mus.
Para. Emilio Goeldi. Nova Ser. Zool.
5:179–93
118. Rehm S, Espig G. 1991. The Cultivated
Plants of the Tropics and Subtropics:
Cultivation, Economic Value, Utiliza-
tion. Weikersheim, Germany: Joseph
Margraf
119. Richards AJ. 1990. Studies in Garcinia,
dioecious tropical forest trees: agamo-
spermy. Bot. J. Linn. Soc. 103:233–50
120. Richards AJ. 1990. Studies in Garcinia,
dioecious tropical forest trees: the phe-
nology, pollination biology and fertiliza-
tion of G. hombroniana Pierre. Bot. J.
Linn. Soc. 103:251–61
121. Richards KW. 1993. Non-Apis bees
as crop pollinators. Rev. Suisse Zool.
100:807–22
122. Roig-Alsina A, Michener CD. 1993.
Studies of the phylogeny and classifi-
cation of long-tongued bees (Hymenop-
tera: Apoidea). Univ. Kans. Sci. Bull.
55:124–62
123. Roubik DW. 1979. Africanized honey
bees, stingless bees, and the structure
of tropical plant-pollinator communi-
ties. Proc. Int. Symp. Pollin. 4th, Mary-
land, Md. Agric. Exp. Stn. Spec. Misc.
Publ. 1:403–17
124. Roubik DW. 1989. Ecology and Natu-
ral History of Tropical Bees. Cambridge,
UK: Cambridge Univ. Press
125. Roubik DW. 1995. Pollination of Culti-
vated Plants in the Tropics. FAO Agric.
Serv. Bull. No. 118. Rome, Italy: Food
Agric. Org.
126. Roubik DW. 1998. Coffee pollination
in Central American highlands: African
bees and the reproduction of an autoga-
mous shrub. Ecol. Lett. In Press
127. Roubik DW, Aluja M. 1983. Flight
AR074-08
205
ranges of Melipona and Trigona in
tropical forest. J. Kans. Entomol. Soc.
56:217–22
128. Roubik DW, Moreno JE. 1990. Social
bees and palm trees: what do pollen di-
ets tell us? In Social Insects and the En-
vironment: Proc. 11th Int. Congr. IUSSI,
Bangalore India, ed. GK Veeresh, B
Mallik, CA Viraktamath, pp. 427–28.
Leiden: EJ Brill
129. Roubik DW, Moreno JE, Vergara C,
Wittmann D. 1986. Sporadic food com-
petition with the African honey bee: pro-
jected impact on neotropical social bees.
J. Trop. Ecol. 2:97–111
130. Sakagami SF. 1982. Stingless bees. In
Social Insects, ed. HR Hermann, 3:361–
423. New York: Academic
131. Sakagami SF. 1971. Ethosoziologischer
vergleich zwischen honigbienen und
stachellosen bienen. Zeit. Tierpsychol.
28:337–50
132. Sazima I, Sazima M. 1989. Maman-
gavas e irapuás (Hymenoptera, Apoi-
dea): visitas, interaçães e conseqüências
para polinização do maracujá (Passiflo-
raceae). Rev. Brasil. Entomol. 33:109–
18
133. Schneider E. 1983. Gross morphology
and floral biology of Ondinea purpurea
den Hartog. Aust. J. Bot. 31:371–82
134. Schremmer F. 1982. Blühverhalten
und bestäubungsbiologie von Carlu-
dovica palmata (Cyclanthaceae)—ein
ökologisches paradoxon. Plant Syst.
Evol. 140:95–107
135. Sedgley M, Griffin AR. 1989. Sexual
Reproduction of Tree Crops. London:
Academic
136. Shelar DG, Suryanarayana MC. 1981.
Preliminary studies on pollination of co-
riander (Coriandrum sativum L.). Indian
Bee J. 43:110–11
137. Sihag RC. 1985. Floral biology, melit-
tophily and pollination ecology of onion
crop. In Recent Advances in Pollen Re-
search, ed. TM Varghese, pp. 277–84.
New Delhi, India: Allied
138. Deleted in proof
139. Simão S, Maranhão ZC. 1959. Os in-
setos como agentes polinizadores da
mangeira. An. Esc. Super. Agric. “Luis
De Queiroz” 16:299–304
140. Singh G. 1989. Insect pollinators of
mango and their role in fruit setting. Acta
Hort. 231:629–32
141. Sommeijer MJ, de Rooy GA, Punt W,
de Bruijn LLM. 1983. A comparative
study of foraging behavior and pollen re-
sources of various stingless bees (Hym.,
Meliponinae) and honeybees (Hym.,
P1: KKK/plb P2: ARS/KKK/plb QC: ARS/anil T1: KKK
November 4, 1998 11:18 Annual Reviews
206 HEARD
Apinae) in Trinidad, West-Indies. Api-
dologie 14:205–24
142. Sosa-Nájera MS, Martı́nez-Hernández
E, Lozano-Garcı́a MS, Cuadriello-
Aguilar JI. 1994. Nectaropolliniferous
sources used by Trigona (Tetragonisca)
angustula in Chiapas, southern Mexico.
Grana 33:225–30
143. Stone GN, Willmer PG. 1989. Pollina-
tion of cardamon in Papua New Guinea.
J. Apic. Res. 28:228–37
144. Suka T, Inoue T. 1993. Nestmate Recog-
nition of the Stingless Bee Trigona
(Tetragonula) minangkabau (Apidae,
Meliponinae). J. Ethol. 11:141–47
145. Syed RA. 1979. Studies on oil palm pol-
lination by insects. Bull. Entomol. Res.
69:213–24
146. Tepedino VJ. 1981. The pollination effi-
ciency of the squash bee (Peponapis pru-
inosa) and the honey bee (Apis mellifera)
on summer squash (Cucurbita pepo). J.
Kans. Entomol. Soc. 54:359–77
147. Torchio PF. 1987. Use of non-honey bee
species as pollinators of crops. Proc. En-
tomol. Soc. Ont. 118:111–24
148. Uji T. 1987. Penyerbukan pada rambutan
(Nephelium lappaceum var. lappaceum).
Berita Biol. 3:31–34
149. Urata U. 1954. Pollination requirements
of macadamia. Hawaii Agric. Exp. Stn.
Tech. Bull. 22:1–40
150. Utami N. 1986. Pollination in sago
(Metroxylon sagu). Berita Biol. 3:229–
31
151. van der Pijl L. 1953. On the flower biol-
ogy of some plants from Java. Ann. Bo-
gor. 1:77–99
151a. van Nieuwstadt MGL, Iraheta CER.
1996. Relation between size and for-
aging range in stingless bees (Apidae,
Meliponinae). Apidologie 27:219–28
152. Velthuis H. 1990. The biology and the
economic value of the stingless bees,
compared to the honey bees. Apiacta
25:68–74
AR074-08
153. Venturieri GA, Pickersgill B, Overal
WL. 1993. Floral biology of the Ama-
zonian fruit tree “cupuassu” (Theo-
broma grandiflorum). In Biodiversity
and Environment—Brazilian Themes for
the Future, London, p. 23. London:
Linn. Soc. London, R. Bot. Gard.
154. Vithanage V, Ironside DA. 1986. The in-
sect pollinators of macadamia and their
relative importance. J. Aust. Inst. Agric.
Sci. 52:155–60
155. Wallace H. 1994. Bees and the pollina-
tion of macadamia. PhD thesis. Univ.
Queensland
156. Wallace HM, Vithanage V, Exley EM.
1996. The effect of supplementary pol-
lination on nut set of Macadamia (Pro-
teaceae). Ann. Bot. 78:765–73
157. Wang XZ, Chen YP, Gao XO, Xie JM.
1981. The discovery of Melipona sp.
pollinating Amomum villosum Lour. in
Yunnan Province. Yunnan Agric. Sci.
Tech. 5:49
158. Wille A. 1965. Las abejas atarrá de
la región mesoamericana del género
y subgénero Trigona (Apidae-Melipo-
nini). Rev. Biol. Trop. 13:271–91
159. Wille A. 1976. Las abejas jicotes del
genero Melipona (Apidae: Meliponini)
de Costa Rica. Rev. Biol. Trop. 24:123–
47
160. Wille A. 1983. Biology of the stingless
bees. Annu. Rev. Entomol. 28:41–64
161. Wille A, Orozco E, Raabe C. 1983.
Polinización del chayote Sechium edule
(Jacq.) Swartz en Costa Rica. Rev. Biol.
Trop. 31:145–54
162. Willmer PG, Stone GN. 1989. Incidence
of entomophilous pollination of lowland
coffee (Coffea canephora); the role of
leafcutter bees in Papua New Guinea.
Entomol. Exp. Appl. 50:113–24
163. Young AM. 1983. Nectar and pollen
robbing of Thunbergia grandiflora by
Trigona bees in Costa Rica. Biotropica
15:78–80
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