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;
KEY WORDS:Apidae, Meliponini, floral biology, alternative pollinators, entomophily
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.
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
attribe(122). ThemostimportantgeneraareMeliponaandTrigona. Melipona
consists of ∼50 species, is confined to the neotropics, has more complex com-
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
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
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;
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.
CROP POLLINATION BY STINGLESS BEES
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
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:
of availability of large numbers of hives; colony growth rates are low compared
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
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
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
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
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
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 grandipennispollinates 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
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
was found to decrease with distance from an adjoining forest (20). Stingless
bees were common visitors to flowers of cupua¸ cu 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).
population size (141). The actual foraging distance also depends on the attrac-
and availability of alternative resources. Using a mark-release technique, the
maximum flight range of Cephalotrigona capitata and Melipona panamica in
tropicalforestwasestimatedtobe1.5and2.1km, respectively(127). Captured
CROP POLLINATION BY STINGLESS BEES
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
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
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).
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
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.
stingless beekeeping was reviewed recently (29).
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
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
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)
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
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,
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
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
Yields of macadamia
CROP POLLINATION BY STINGLESS BEES
Crops visited and at least occasionally or partially pollinated by stingless bees
Common nameName FamilyReference
Crops for which stingless bees make an important contribution to pollination
Mapati, Uvilla, Amazon Pourouma cecropiaefolia
Crops visited and occasionally or partially pollinated by stingless bees
Peach Palm, Pejibaye
Ice Cream Bean, Sipo,
27, 53, 56
Stylo, Brazilian Lucerne Stylosanthes guianensis
Leg.: Caesalpinioideae 141
1, 69, 141,
27, 34, 53
Panama Hat Plant
Capsicum annuum varieties Solanaceae
Common name NameFamilyReference
CHAYOTE, CHOKO, SECHIUM EDULE (CUCURBITACEAE)
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
The vines that produce
CROP POLLINATION BY STINGLESS BEES
areas with no surrounding trees and hence no stingless bees did not bear fruit
COCONUT, COCOS NUCIFERA (ARECACEAE)
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
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%)
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.
Insect pollination is important for
MANGO, MANGIFERA INDICA (ANACARDIACEAE)
yields of mango (38). The flowers are unspecialized, allowing pollination by
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
large amount of pollen carried on their bodies and the close contact they made
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.
Visits by insects increase
CARAMBOLA, AVERRHOA CARAMBOLA (OXALIDACEAE)
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
The distylous flowers of
had a mean of six pollen grains that did not germinate. T. thoracica made more
because the introduction of hives into two orchards correlated with increased
CAMU-CAMU, MYRCIARIA DUBIA (MYRTACEAE)
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.
Insects are needed to pollinate
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).
UVILLA, AMAZONTREE GRAPE,
Stingless bees and ants were the only visitors to flowers of ma-
ANNATTO, ACHIOTE, BIXA ORELLANA (BIXACEAE)
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
Annatto is efficiently buzz
CUPUAC ¸U, THEOBROMA GRANDIFLORUM (STERCULIACEAE)
ers of the cupua¸ cu 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
Near Belem, flow-
CROP POLLINATION BY STINGLESS BEES
Ptilotrigonalurida). Theformerbeeonlyrobbedpollen, butT.luridaappeared
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
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)
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
actively collected both nectar and pollen, while the Apis spp. actively collected
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).
Seed crops of onion benefit from insect vis-
STRAWBERRY, FRAGARIA CHILOENSIS X ANANASSA (ROSACEAE)
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
more suited to the confined glasshouse space than that of the honey bees (63).
Japan to pollinate strawberries in glasshouses and proved to be efficient, with
flowers that received four visits producing well-formed fruits (72). Although
areas, and other bees and flies are also efficient (37).
COFFEE, COFFEA SPP. (RUBIACEAE)
Coffea arabica flowers in Brazil (92). The larger honey bees and Melipona
spp. were perhaps more efficient pollinators than the smaller species of sting-
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-
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).
Honey bees and stingless bees visited
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).Largequantitiesofpollen, >10%ofthetotal, ofguavawerefoundinboth
the honey and pollen pots of hives of Melipona marginata marginata in Brazil
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)
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
Near S˜ ao Paulo in Brazil,
CROP POLLINATION BY STINGLESS BEES
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).
but are probably rarely important.
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)
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).
Bagged flowers of this
SOAP-NUT, SAPINDUS EMARGINATUS (SAPINDACEAE)
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).
In Southern India, the
SQUASH, CUCURBITA PEPO AND OTHER CUCURBIT CROPS (CUCURBITACEAE)
Honey bees and T. spinipes were the most common insects visiting flowers in
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).
fourspeciesofCalamusinThailandwereTrigonaspp. (18). InMalaysia,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)
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
from male inflorescences. They did not visit female inflorescences and there-
fore did not effect pollination. They may have contributed to wind pollination
wind pollination may explain why the plants produce nectar (22).
A breadfruit tree produces
JACKFRUIT, ARTOCARPUS HETEROPHYLLUS (MORACEAE)
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).
Jackfruit has male and
Indonesia by a range of insects, mainly bees, including Trigona itama. How-
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,
by a bee of adequate weight, and hence smaller bees, such as many stingless
bees, are not effective pollinators.
Indigofera, Indigofera endocaphylla, is visited in
CITRUS, CITRUS SPP. (RUTACEAE)
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).
Pollen of Citrus spp. was rarely collected by
CROP POLLINATION BY STINGLESS BEES
CORIANDER, CORIANDER SATIVUM (APIACEAE)
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).
Apis spp. and T. iridipennis
BELLYACHE BUSH, JATROPHA GOSSYPIFOLIA (EUPHORBIACEAE)
ofJ.gossypifolia,amedicinalplantinBrazil(94). Trigonasp. wasanimportant
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).
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)
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).
The stingless bees Melipona
INDIAN SHOT, CANNA INDICA (CANNACEAE)
(referred to as Melipona sp.) in Java (53). The stingless bees forage deep in
the flowers collecting nectar and, in doing so, effect pollination.
This crop is visited by Trigona sp.
MEMBRILLO, GUSTAVIA SUPERBA (LECYTHIDAEAE)
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).
Flowers of species of mem-
AVOCADO, PERSEA AMERICANA (LAURACEAE)
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,
Small stingless bees are claimed
personal communication). Honey bees are efficient pollinators but are not
strongly attracted to the crop (59).
CARDAMOM, ELETTARIA CARDAMOMUM (ZINGIBERACEAE)
bee, A. cerana, was the most common insect visiting cardamom collecting
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).
In India, the honey
SAREN, AMOMUM VILLOSUM (ZINGIBERACEAE)
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).
Saren, a valuable medicinal
NANCHE, BYRSONIMA CRASSIFOLIA, AND ACEROLA, MALPIGHIA PUNICIFOLIA
pollinated by stingless bees. However, specialist oil-collecting anthophorine
RUBBER, HEVEA BRASILIENSIS (EUPHORBIACEAE)
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).
Some stingless bees of the
SISAL, AGAVE SISALANA (AGAVACEAE)
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).
F. schrottkyi was observed to visit sisal
PANAMA HAT PLANT, CARLUDOVICA PALMATA (CYCLANTHACEAE)
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
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
CROP POLLINATION BY STINGLESS BEES
Crop species with records of visitation by stingless bees but known to be pollinated by
Pollinator or means
of fertilization Common nameName FamilyReferencea
CaricaceaeSphingidae and other
11, 36, 53
Annona spp. Annonaceae86
Eulaema spp. (bees)
Large euglossine and
Garcinia spp. Clusiaceae119, 120
Xylocopa spp. (bees)
Bees and flies
Large bees, e.g.
Large bees e.g.
Wind or rain
aReferences 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
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
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
pollination. The foraging flight range often is between 100 and 400 m. Hence
remnant forests within this distance from orchards can provide adequate bee
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, cupua¸ cu, 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-
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.
and Tad Bartareau for many helpful comments on the manuscript.
Visit the Annual Reviews home page at
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