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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
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184 HEARD
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).
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.
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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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Table 1 Crops visited and at least occasionally or partially pollinated by stingless bees
(Continued)
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Table 1 (Continued)
areas with no surrounding trees and hence no stingless bees did not bear fruit
(161).
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had a mean of six pollen grains that did not germinate. T. thoracica made more
intermorph visits than A. cerana. A. cerana still appeared to be useful, however,
because the introduction of hives into two orchards correlated with increased
yields (100).
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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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).
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.
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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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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.
198 HEARD
personal communication). Honey bees are efficient pollinators but are not
strongly attracted to the crop (59).
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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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
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