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