ATTEMPTS TO INTRODUCE STINGLESS BEES FOR THE POLLINATION ...

ATTEMPTS TO INTRODUCE STINGLESS BEES FOR THE
POLLINATION OF CROPS UNDER GREENHOUSE
CONDITIONS IN JAPAN

Kazuhiro Amano
Laboratory of Apiculture
National Institute of Livestock and Grassland Science
Tsukuba, Ibaraki 305-0901, Japan

ABSTRACT

In Japan, a growing number of greenhouses for crops are now in use, where no wild pollinators
are available. Although a large number of colonies of honeybees, Apis mellifera, and bumblebees,
Bombus terrestris, are used for pollination, farmers face difficulty because of the absolute shortage
of pollinators. Consequently, many of them are obliged to perform artificial pollination or apply
hormones to their crops. To respond to these situations, the author has been trying to introduce
the use of new efficient pollinators in recent years. Stingless bees, Meliponinae, and honeybees,
Apinae, are the only highly social bees living in permanent colonies, and both share many
biological characteristics. Many advantages could be expected from the use of stingless bees as
pollinators. They are harmless to beekeepers and farmers, are active throughout the year, visit a
wide range of crops (polylecty), and do not pose any environmental risks by escaping into
natural habits because they cannot tolerate cold weather, especially in the winter. Consequently,
among the stingless bees kept in their indigenous habitats, some promising species have been
chosen and introduced from tropical and subtropical habitats overseas. These are Meripona
beecheii, M. quadrifasciata, Trigona carbonaria, Tetragonula fuscobalteata, Scaptotorigona
bipunctata, and Tetragonisca angustula. This paper shows the process of introducing stingless bees
and the facilities involved, together with the pollination results obtained by using these bees.

Keywords: Meliponinae, Apinae, stingless bees, crop pollination under greenhouse conditions, Japan

INTRODUCTION Stingless bees are generally characterized
by their stingers being atrophied and of little
There are two groups of highly eusocial harm to beekeepers as opposed to those of
insects in the world: Apinae bees and honeybees. They are also known as good
Meliponinae bees. Some species of both pollinators of various crops. Since 1997, the
groups have been used in the beekeeping author has been trying to screen promising
industry, apiculture and meliponiculture, owing stingless bees as pollinators out of the species
to the specific characteristics of eusocial being kept in their native areas, and to
insects. The former group (Apinae) consists of introduce them to Japan with the practical aim
less than 10 species including the Western of pollinating crops.
honeybee, Apis mellifera, and the Oriental
honeybee, A. cerana, both of which are well- In Japan, more than 700,000 greenhouses
known as beekeeping species. The other are used to grow crops, where no wind, rain,
group (Meliponinae) constitutes the stingless or wild pollinators are available. Around
bees, and contains more than 400 species in 120,000 colonies of Apis mellifera are used for
tropical and subtropical areas, some of which pollination annually, but farmers would rather
have been used just like honeybees in these not manage the colonies by themselves
areas, especially in the Yucatan. because of the danger that their handling
poses. Professional beekeepers do the job

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instead. Since 1991, the bumblebee, Bombus The first one is Osmia cornifrons, a
terrestris, has been used, and now up to species of solitary bees which is now essential
about 40,000 colonies are consumed annually in the pollination of crops, especially apples.
despite their cost [25,000 yen (=US$200)/ Its pollination ability on apples is considered
colony]. Bumblebees are regarded as easy and much higher than that of the honeybee. Its life
safe enough for farmers to manage partly cycle is very simple, and the foraging period
because of their short lifespan, which is far coincides with the flowering of apple. Since the
less than one year. However, many more bee readily accepts artificial nests just like its
pollinators are needed to match the scale of native nests such as bamboo or reed, farmers
greenhouses. manage it with minimal skills. At present, the
bees are used as apple pollinators in more
Stingless bees are promising pollinators than 18,000 ha of orchards in the northern part
for the following reasons: they are harmless to of Japan. Furthermore, the bees are expected to
beekeepers and greenhouse workers, visit a be applied to other crops by shifting the adult
wide range of crops (polylecty), are tolerant of emerging time through controlling the
high temperatures, are active throughout the hibernation temperature.
year, can be transported easily, and hardly
pose any environmental risks by escaping into The second one is the European
and invading natural habitats as they would bumblebee, Bombus terrestris, which is a social
not survive the Japanese winter. On the other insect. Unlike that of the honeybee or the
hand, many issues need to be resolved before stingless bee, its colony is annual, so the
using stingless bees, one of which is how to colony could be used for crop pollination for
improve methods for propagating and about two months around the climax of its
maintaining colonies throughout the year. To development. The bumblebee is considered an
address this issue, a specific glasshouse with efficient pollinator of some crops such as
attached laboratories has been completed in the solanaceous plants, which require the buzz-
National Institute of Livestock and Grassland pollination done by bumblebees. Buzzing bees
Science, Japan solely for stingless bee cling to the ends of the anthers and vibrate
researches. their indirect flight muscles, leading to pollen
release. These bees are now popular because
Many authors have studied and farmers can manage them by themselves.
described various aspects of the biology of
stingless bees. Most of these studies have The third one is the honeybee, or
been conducted in the native areas where the European honeybee, Apis mellifera. This well-
species live. This paper hopes to present an known social insect is an important pollinator
outline of the stingless bee researches of the of orchards, crop fields, and glasshouses, but
author as well as the facilities where these are the number of colonies used as pollinators in
conducted. Japan is not as many as expected. Most
farmers who need pollinators do not want to
Status of pollinator utilization in Japan keep the honeybees by themselves, and, if
necessary, have professional beekeepers
Where no pollinators are available, many crops manage the colonies. There are less than 5,000
need hand or mechanical pollination, unless professional or semiprofessional beekeepers in
useful pollinators should be released artificially. Japan, the small number of which limits the
The multiple use of insecticides and the use of honeybees as pollinators.
expansion of single cropping, both of which Consequently, farmers in Japan expect easily
have been conducive to the development of manageable and efficient pollinators which can
modern agriculture, have also led to the be used over the long term.
decrease of natural pollinator populations. In
addition, cultivation under structures such as MATERIALS AND METHODS
glasshouses and vinyl houses has been
increasing in Japan. These agricultural Stingless bee colonies introduced
conditions have stimulated the demand for
efficient and manageable pollinators for crops. The important genera for stingless beekeeping,
Three species of bees have had a great impact or meliponiculture, are Melipona and Trigona.
on crop pollination in Japan. Crane (1992) listed 14 species of Melipona and

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21 of Trigona that have been used in the RESULTS AND DISCUSSION
traditional way. Melipona species are
restricted to Central and South America, and Nest structure
are of historical significance because of their
long-time culture for the production of honey A few species of stingless bees build their
and wax. Trigona species are present in the nests in underground cavities such as termite
entire tropical continental area, and their use in mounds, most of them belonging to primitive
traditional hive beekeeping has been reported groups. Some other species build an exposed
in tropical America and occasionally in Asia. nest surrounded by hard and sometimes brittle
The author chose the species to be introduced layers hanging on tree branches. Those species
based on his study of traditional stingless do not seem to have ever been considered for
beekeeping. The principal species introduced to beekeeping. The most common type of nest is
Japan were Trigona carbonaria (Australia), T. found in a tree cavity, and the species
fuscobalteata (Thailand), Melipona beecheii introduced belongs to this type. The nest is
(Mexico), M. quadrifasciata, Tetragona usually made of five parts: brood comb,
angustula, Plebeia droryana, and involucrum, store pots, batumen, and an
Scaptotrigona bipunctata (Paraguay). entrance. The comb consists of brood cells, in
each of which a single young is reared,
Facilities for stingless bee research surrounded by a sheath of cerumen, or
involucrum. Therefore, the cavity where the
Glasshouses equipped with a thermo-control brood cells are present is called a brood
system were built to keep introduced stingless chamber. Cerumen is made of a mixture of wax
bee colonies throughout the year, multiply the secreted from the glands on the abdomen of
colonies, and check their foraging activities. workers and propolis. The propolis is derived
The honeybee queen flies whenever swarming from resins collected from plants. Honey and
occurs, whereas, the stingless bee queen flies pollen are stored in pots quite different from
only once in its life, that is, for mating. Being the brood cells. These storage pots are usually
different from the honeybee queen, the placed above and below the involucrum, and
stingless bee queen usually mates in a low made of cerumen. The extra space in the tree
place, at a maximum of 5 m. Thus, the cavity is sealed by batumen plates, usually
glasshouse was designed to be 10 m high. made of cerumen and other materials like mud.
Two environmentally controlled chambers were The entrance of the nest is a simple hole.
attached to the glasshouse, where various These observations apply to all of the species
aspects of the biology of stingless bees can included in the study (Fig. 1).
be observed.

Fig. 1. Nest of Melipona beecheii Brood comb of Melipona beecheii.
in an observation box. The arrow shows a queen.

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Thermoregulation stingless bees to tropical and subtropical areas.
Studies by the author show that T. carbonaria
It is believed that the leading reason why cannot easily control the temperature in the
stingless bees have not spread into the hive (Fig. 3).
temperate zone is because of their lack of
tolerance to low temperatures. However, Hive boxes for stingless bees
research by the author shows that, for adult
workers, the tolerance of T. carbonaria to low Since stingless bees do not tolerate low
temperature is not as poor as that of other temperatures, hive boxes should be devised for
Apis honeybees, in addition to the fact that it use in temperate countries like Japan. The
tolerates much higher temperatures than Apis author designed the hive box by using the
species (Fig. 2). introduced stingless bees. Two points were
considered in designing: the first was
Considering the colonies as a whole, Apis temperature control, and the second was
spp. do have a system of thermoregulation. convenience in splitting or multiplying the
They are able to maintain the temperature colony.
around the brood at 34o-36oC year-round. The
temperature is raised with their own body heat, To address the problem of temperature,
generated by shivering the wing muscles, and the hive was constructed of two boxes, an
lowered, if necessary, by fanning their wings at inner hive box and an outer box. The outer
the nest entrance to draw cooler air into the box was equipped with a heater system to
nest or by gathering water into the nest to keep the hive at a fixed temperature even in
spread over the comb. winter (Fig. 4). The hive boxes made it
possible for T. carbonaria and S. bipunctata
Generally, stingless bees are not as colonies to survive for years in the outdoor
efficient as honeybees in controlling the nest field.
temperature, especially when the temperature is
low. When the temperature is too high for The inner hive box was designed to split
them, they have been observed to lower the the colony. Researchers in Australia have
temperature by fanning their wings at the nest developed various types of hives for T.
entrance partly for ventilation as honeybees carbonaria. The design of the inner hive box,
do, but they are inefficient in raising the which consists of three-storied spaces to
temperature. This may be a factor that limits contain a brood space, a food storage space,

A BC D
A Effective
temperature A. mellifera
A. cerana japonica
BC D
Effective
temperature

AB Effective CD

temperature T. carbonaria

5 15 35 45 55
0 10 20 40 50 (oC)
Fig. 2. Thermo-responses of adult workers in three species
A: Lethal low temperature, B: Effective low temperature,
C: Effective high temperature, D: Lethal high temperature

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(oC) Brood area
40 Food storage area
30
20 Inner space near
entrance
10 Ambient
temperature

40

30

20 0:00 0:00 Brood area

10 Food storage area
0:00 Innheirvespeadcege of

Ambient
temperature

(Time)

Fig. 3. Temperature in and out of the nest of honey bee,
Apis mellifera (above), and the stingless bee, Trigona
carbonaria (below)

30

25
Inside of inner box

20
15 Inside of outer box

10
Ambient temperature

5

0 0:00 0:00 0:00 0:00 0:00 0:00

Fig. 4. Temperature in and out of the hive box

and a feeding space, was inspired by their advancing edges of the spiral comb are a
ideas. The brood space can be divided for growing portion where new cells are
propagating the colony when it matures. constructed and added along them. When the
summit reaches the ceiling of the brood
Splitting the colony chamber, the growing portion appears again at
the bottom to repeat its rise. To split a mature
To multiply the colony, the nest, especially the nest, the inner box is prised open, while the
brood, should be split. The layers of T. brood in a brood space is cut in half. The top
carbonaria's brood cells form a single spiral, part and mid-part of the inner box are kept
that is, a single comb. The summit and the together, and a new bottom part is added. The

5

bottom part is given a new top part and a somewhat poor results, contrary to what was
new mid-part. Then, two new nests are expected (Fig. 5). As the control, bagged
formed. There is no problem with the new nest flower heads produced almost no seed. The
containing the original queen, but the other average weights of flower heads produced by
one does not contain any mature queens. T. carbonaria, S. bipunctata, B. terrestris, and
However, in this species, there are usually A. mellifera were 4.7 g, 7.1 g, 16.6 g, and
several large cells containing developing queen 14.2 g, respectively, while the weights of yield
bees scattered throughout the brood comb. per 0.75 m2 were 4.0 g, 7.9 g, 19.4 g, and
One of these cells will grow to be a new 17.0 g. Several reasons were advanced for the
queen. It is going to fly for mating return to poor performance of stingless bees. Perhaps
its new colony, which subsequently becomes the main one was that 0.2 ha of one
independent. For success in multiplying the greenhouse compartment was too spacious for
colony, plural colonies of the same species one colony of the stingless bees to pollinate,
should be kept in the same place for mating. and the second was that the colonies were
When provided with the thermo-equipped hive tested too soon after introduction from
boxes, colonies of the two species, T. overseas, and they had not adjusted to their
carbonaria and S. bipunctata, can survive for new habitat yet. Actually, many individuals of
years even in the winter season. Mature both species gathered around the ceiling facing
colonies of the bees can also be multiplied in the sun and stayed there, causing wear and
a glasshouse along with other colonies of the tear to the colonies.
species.
Pollination of tomato plants. The flowers
Pollination efficiency of tomatoes, Lycopersicon esculentum, do not
produce nectar, and the specific shape of their
Although there are limited data on the anthers favors the bumblebee, which does
influence of pollination by stingless bees on buzzing-pollination. The effect of bumblebees,
crop yield, many species are considered useful B. terrestris, and stingless bees, T. carbonaria,
for the pollination of crops. Pollination tests on producing fruit were compared. One
comparing stingless bees with honeybees and/ compartment of a greenhouse contained a
or bumblebees were performed. colony of B. terrestris and another of T.
carbonaria. It is well known that when B.
Pollination of white clover. Two species terrestris visits tomato flowers, it leaves a
each of stingless bees, honeybees, and bite-mark on the flower. T. carbonaria was
bumblebees were placed in greenhouses of found to visit the flowers very often and leave
white clover, Trifolium repens. White clover a similar bite-mark. Based on calculations of
must be pollinated to produce seed. The the number of bite-marked flowers, B. terrestris
results of tests comparing bumblebees, visited the flowers at 82% of the time, T.
honeybees, and stingless bees showed carbonaria more than 95%. However, T.

20 T. carbonaria
15 S. bipunctata
10 B. terrestris
A. mellifera
5
0

Wweieghigt hoft o f N Noo.ooff fflloowweer r WWeeigighthotf osefeds
flfolowweerrhehaedsa(dgs) hheeaaddss(x(2x02) 0 ) speere0d.7s5 pme2 r

(g) 0 .7 5 m 2

Fig. 5. Pollination efficiency for white clovers by four species

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100 T. carbonaria
90 B. terrestris
80
70 frFuruiitts sperpfelorwer frvFuirsuiitiettds sperpfelorwer
60 flowers flowers

50
40
30
20
10

0 Flfowleorswveisritsed

visted

visited

Fig. 6. Differences between T. carbonaria and B. terrestris in
visited and fruiting tomatoes

1.5 red stingless
1 pepper honeybees

0.5 honey
0 bees
cucumber egg plant paprika

Fig. 7. Relative incidence in fruiting crops by two
kinds of pollinators

carbonaria yielded about 8% fruits from grown crops need to be pollinated to produce
visited flowers, whereas B. terrestris had over satisfactory fruits with commercially high value.
90% from visited flowers, corresponding to The presence of both bees, honeybees and
about 80% from all flowers (Fig. 5). stingless bees, was frequent enough during the
entire flowering season of the crops, during
Pollination of other crops. Using his which time they were observed to visit the
glasshouse and apiary area, the author flowers. Stingless bees foraged mainly in the
conducted a pollination efficiency test of morning, compared with all day for honeybees,
stingless bees, T. carbonaria and C. which may be due to the difference in their
bipunctata, and of honeybees, A. mellifera field situations.
(Fig. 6). During the experiment period, 10
colonies of each stingless bee were kept inside Generally, the results show that stingless
the glasshouse with some fluctuation in the bees pollinate as well as honeybees, factoring
colony number, while about 30 colonies of in the difference among the crops (Fig. 7). The
honeybees were kept in the apiary. Four kinds stingless bees in the glasshouse had settled
of crops, namely, cucumbers, eggplants, long enough to adjust themselves to field
paprikas, and red peppers, were settled in the conditions, implying that once stingless bees
glasshouse as well as in the apiary for are accustomed to conditions in the field, they
comparison. In Japan, these four commercially show their efficiency in pollination.

7

From the three experiments on pollination Crane, E. 1992. The past and present status
efficiency above and other surveys on of beekeeping with stingless bees. Bee
stingless beekeeping techniques, T. carbonaria World 73: 29-42.
and S. bipunctata can be expected to show
good potential as effective pollinators of crops Cruz-Landim, C. et al. 1968. Mandibular gland
in glasshouse conditions in temperate development and communication in field
countries. bees of Trigona (Scaptotrigona) postica. J.
Kans. Entomol. Soc. 41: 474-481.
CONCLUSION
Dollin, A. and T. Heard. 1998. Keeping
The efficiency of insects as crop pollinators Australian stingless bees in a log or box.
would depend on their biological characteristics In Native Bees of Australia Series Booklet
in relation to the crop and the environment in 5. By Australian Native Bee Research
which they are needed. Each insect species Center: 1-14.
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would have its specific characteristics, which Esch, H. et al. 1965. Sound: an element
might be favorable or unfavorable from the common to communication of stingless
standpoint of the user. The value of stingless bees and to dances of the honeybee.
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desirable, as in greenhouses. However, very bee Trigona carbonaria (Hymenoptera:
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