RSS | Register/註冊 | Log in/登入
Site search:
Home>Attempts to Introduce Stingless Bees for the Pollination of Crops under Greenhouse Conditions in Japan
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, 2004-10-01


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.


There are two groups of highly eusocial insects in the world: Apinae bees and Meliponinae bees. Some species of both groups have been used in the beekeeping industry, apiculture and meliponiculture, owing to the specific characteristics of eusocial insects. The former group (Apinae) consists of less than 10 species including the Western honeybee, Apis mellifera, and the Oriental honeybee, A. cerana, both of which are well-known as beekeeping species. The other group (Meliponinae) constitutes the stingless bees, and contains more than 400 species in tropical and subtropical areas, some of which have been used just like honeybees in these areas, especially in the Yucatan.

Stingless bees are generally characterized by their stingers being atrophied and of little harm to beekeepers as opposed to those of honeybees. They are also known as good pollinators of various crops. Since 1997, the author has been trying to screen promising stingless bees as pollinators out of the species being kept in their native areas, and to introduce them to Japan with the practical aim of pollinating crops.

In Japan, more than 700,000 greenhouses are used to grow crops, where no wind, rain, or wild pollinators are available. Around 120,000 colonies of Apis mellifera are used for pollination annually, but farmers would rather not manage the colonies by themselves because of the danger that their handling poses. Professional beekeepers do the job instead. Since 1991, the bumblebee, Bombus terrestris, has been used, and now up to about 40,000 colonies are consumed annually despite their cost [25,000 yen (=US$200)/colony]. Bumblebees are regarded as easy and safe enough for farmers to manage partly because of their short lifespan, which is far less than one year. However, many more pollinators are needed to match the scale of greenhouses.

Stingless bees are promising pollinators for the following reasons: they are harmless to beekeepers and greenhouse workers, visit a wide range of crops (polylecty), are tolerant of high temperatures, are active throughout the year, can be transported easily, and hardly pose any environmental risks by escaping into and invading natural habitats as they would not survive the Japanese winter. On the other hand, many issues need to be resolved before using stingless bees, one of which is how to improve methods for propagating and maintaining colonies throughout the year. To address this issue, a specific glasshouse with attached laboratories has been completed in the National Institute of Livestock and Grassland Science, Japan solely for stingless bee researches.

Many authors have studied and described various aspects of the biology of stingless bees. Most of these studies have been conducted in the native areas where the species live. This paper hopes to present an outline of the stingless bee researches of the author as well as the facilities where these are conducted.

Status of Pollinator Utilization in Japan

Where no pollinators are available, many crops need hand or mechanical pollination, unless useful pollinators should be released artificially. The multiple use of insecticides and the expansion of single cropping, both of which have been conducive to the development of modern agriculture, have also led to the decrease of natural pollinator populations. In addition, cultivation under structures such as glasshouses and vinyl houses has been increasing in Japan. These agricultural conditions have stimulated the demand for efficient and manageable pollinators for crops. Three species of bees have had a great impact on crop pollination in Japan.

The first one is Osmia cornifrons, a species of solitary bees which is now essential in the pollination of crops, especially apples. Its pollination ability on apples is considered much higher than that of the honeybee. Its life cycle is very simple, and the foraging period coincides with the flowering of apple. Since the bee readily accepts artificial nests just like its native nests such as bamboo or reed, farmers manage it with minimal skills. At present, the bees are used as apple pollinators in more than 18,000 ha of orchards in the northern part of Japan. Furthermore, the bees are expected to be applied to other crops by shifting the adult emerging time through controlling the hibernation temperature.

The second one is the European bumblebee, Bombus terrestris, which is a social insect. Unlike that of the honeybee or the stingless bee, its colony is annual, so the colony could be used for crop pollination for about two months around the climax of its development. The bumblebee is considered an efficient pollinator of some crops such as solanaceous plants, which require the buzz-pollination done by bumblebees. Buzzing bees cling to the ends of the anthers and vibrate their indirect flight muscles, leading to pollen release. These bees are now popular because farmers can manage them by themselves.

The third one is the honeybee, or European honeybee, Apis mellifera. This well-known social insect is an important pollinator of orchards, crop fields, and glasshouses, but the number of colonies used as pollinators in Japan is not as many as expected. Most farmers who need pollinators do not want to keep the honeybees by themselves, and, if necessary, have professional beekeepers manage the colonies. There are less than 5,000 professional or semiprofessional beekeepers in Japan, the small number of which limits the use of honeybees as pollinators. Consequently, farmers in Japan expect easily manageable and efficient pollinators which can be used over the long term.

Materials and Methods

Stingless Bee Colonies Introduced

The important genera for stingless beekeeping, or meliponiculture, are Melipona and Trigona. Crane (1992) listed 14 species of Melipona and 21 of Trigona that have been used in the traditional way. Melipona species are restricted to Central and South America, and are of historical significance because of their long-time culture for the production of honey and wax. Trigona species are present in the entire tropical continental area, and their use in traditional hive beekeeping has been reported in tropical America and occasionally in Asia. The author chose the species to be introduced based on his study of traditional stingless beekeeping. The principal species introduced to Japan were Trigona carbonaria (Australia), T. fuscobalteata (Thailand), Melipona beecheii (Mexico), M. quadrifasciata, Tetragona angustula, Plebeia droryana, and Scaptotrigona bipunctata (Paraguay).

Facilities for Stingless Bee Research

Glasshouses equipped with a thermo-control system were built to keep introduced stingless bee colonies throughout the year, multiply the colonies, and check their foraging activities. The honeybee queen flies whenever swarming occurs, whereas, the stingless bee queen flies only once in its life, that is, for mating. Being different from the honeybee queen, the stingless bee queen usually mates in a low place, at a maximum of 5 m. Thus, the glasshouse was designed to be 10 m high. Two environmentally controlled chambers were attached to the glasshouse, where various aspects of the biology of stingless bees can be observed.

Results and Discussion

Nest Structure

A few species of stingless bees build their nests in underground cavities such as termite mounds, most of them belonging to primitive groups. Some other species build an exposed nest surrounded by hard and sometimes brittle layers hanging on tree branches. Those species do not seem to have ever been considered for beekeeping. The most common type of nest is found in a tree cavity, and the species introduced belongs to this type. The nest is usually made of five parts: brood comb, involucrum, store pots, batumen, and an entrance. The comb consists of brood cells, in each of which a single young is reared, surrounded by a sheath of cerumen, or involucrum. Therefore, the cavity where the brood cells are present is called a brood chamber. Cerumen is made of a mixture of wax secreted from the glands on the abdomen of workers and propolis. The propolis is derived from resins collected from plants. Honey and pollen are stored in pots quite different from the brood cells. These storage pots are usually placed above and below the involucrum, and made of cerumen. The extra space in the tree cavity is sealed by batumen plates, usually made of cerumen and other materials like mud. The entrance of the nest is a simple hole. These observations apply to all of the species included in the study ( Fig. 1).


It is believed that the leading reason why stingless bees have not spread into the temperate zone is because of their lack of tolerance to low temperatures. However, research by the author shows that, for adult workers, the tolerance of T. carbonaria to low temperature is not as poor as that of other Apis honeybees, in addition to the fact that it tolerates much higher temperatures than Apis species ( Fig. 2).

Considering the colonies as a whole, Apis spp. do have a system of thermoregulation. They are able to maintain the temperature around the brood at 34o-36oC year-round. The temperature is raised with their own body heat, generated by shivering the wing muscles, and lowered, if necessary, by fanning their wings at the nest entrance to draw cooler air into the nest or by gathering water into the nest to spread over the comb.

Generally, stingless bees are not as efficient as honeybees in controlling the nest temperature, especially when the temperature is low. When the temperature is too high for them, they have been observed to lower the temperature by fanning their wings at the nest entrance partly for ventilation as honeybees do, but they are inefficient in raising the temperature. This may be a factor that limits stingless bees to tropical and subtropical areas. Studies by the author show that T. carbonaria cannot easily control the temperature in the hive ( Fig. 3).

Hive Boxes for Stingless Bees

Since stingless bees do not tolerate low temperatures, hive boxes should be devised for use in temperate countries like Japan. The author designed the hive box by using the introduced stingless bees. Two points were considered in designing: the first was temperature control, and the second was convenience in splitting or multiplying the colony.

To address the problem of temperature, the hive was constructed of two boxes, an inner hive box and an outer box. The outer box was equipped with a heater system to keep the hive at a fixed temperature even in winter ( Fig. 4). The hive boxes made it possible for T. carbonaria and S. bipunctata colonies to survive for years in the outdoor field.

The inner hive box was designed to split the colony. Researchers in Australia have developed various types of hives for T. carbonaria. The design of the inner hive box, which consists of three-storied spaces to contain a brood space, a food storage space, and a feeding space, was inspired by their ideas. The brood space can be divided for propagating the colony when it matures.

Splitting the Colony

To multiply the colony, the nest, especially the brood, should be split. The layers of T. carbonaria's brood cells form a single spiral, that is, a single comb. The summit and the advancing edges of the spiral comb are a growing portion where new cells are constructed and added along them. When the summit reaches the ceiling of the brood chamber, the growing portion appears again at the bottom to repeat its rise. To split a mature nest, the inner box is prised open, while the brood in a brood space is cut in half. The top part and mid-part of the inner box are kept together, and a new bottom part is added. The bottom part is given a new top part and a new mid-part. Then, two new nests are formed. There is no problem with the new nest containing the original queen, but the other one does not contain any mature queens. However, in this species, there are usually several large cells containing developing queen bees scattered throughout the brood comb. One of these cells will grow to be a new queen. It is going to fly for mating return to its new colony, which subsequently becomes independent. For success in multiplying the colony, plural colonies of the same species should be kept in the same place for mating. When provided with the thermo-equipped hive boxes, colonies of the two species, T. carbonaria and S. bipunctata, can survive for years even in the winter season. Mature colonies of the bees can also be multiplied in a glasshouse along with other colonies of the species.

Pollination Efficiency

Although there are limited data on the influence of pollination by stingless bees on crop yield, many species are considered useful for the pollination of crops. Pollination tests comparing stingless bees with honeybees and/or bumblebees were performed.

Pollination of white clover. Two species each of stingless bees, honeybees, and bumblebees were placed in greenhouses of white clover, Trifolium repens. White clover must be pollinated to produce seed. The results of tests comparing bumblebees, honeybees, and stingless bees showed somewhat poor results, contrary to what was expected ( Fig. 5). As the control, bagged flower heads produced almost no seed. The average weights of flower heads produced by T. carbonaria, S. bipunctata, B. terrestris, and A. mellifera were 4.7 g, 7.1 g, 16.6 g, and

14.2 g, respectively, while the weights of yield per 0.75 m2 were 4.0 g, 7.9 g, 19.4 g, and

17.0 g. Several reasons were advanced for the poor performance of stingless bees. Perhaps the main one was that 0.2 ha of one greenhouse compartment was too spacious for one colony of the stingless bees to pollinate, and the second was that the colonies were tested too soon after introduction from overseas, and they had not adjusted to their new habitat yet. Actually, many individuals of both species gathered around the ceiling facing the sun and stayed there, causing wear and tear to the colonies.

Pollination of tomato plants. The flowers of tomatoes, Lycopersicon esculentum, do not produce nectar, and the specific shape of their anthers favors the bumblebee, which does buzzing-pollination. The effect of bumblebees, B. terrestris, and stingless bees, T. carbonaria, on producing fruit were compared. One compartment of a greenhouse contained a colony of B. terrestris and another of T. carbonaria. It is well known that when B. terrestris visits tomato flowers, it leaves a bite-mark on the flower. T. carbonaria was found to visit the flowers very often and leave a similar bite-mark. Based on calculations of the number of bite-marked flowers, B. terrestris visited the flowers at 82% of the time, T. carbonaria more than 95%. However, T. carbonaria yielded about 8% fruits from visited flowers, whereas B. terrestris had over 90% from visited flowers, corresponding to about 80% from all flowers ( Fig. 5).

Pollination of other crops. Using his glasshouse and apiary area, the author conducted a pollination efficiency test of stingless bees, T. carbonaria and C. bipunctata, and of honeybees, A. mellifera ( Fig. 6). During the experiment period, 10 colonies of each stingless bee were kept inside the glasshouse with some fluctuation in the colony number, while about 30 colonies of honeybees were kept in the apiary. Four kinds of crops, namely, cucumbers, eggplants, paprikas, and red peppers, were settled in the glasshouse as well as in the apiary for comparison. In Japan, these four commercially grown crops need to be pollinated to produce satisfactory fruits with commercially high value. The presence of both bees, honeybees and stingless bees, was frequent enough during the entire flowering season of the crops, during which time they were observed to visit the flowers. Stingless bees foraged mainly in the morning, compared with all day for honeybees, which may be due to the difference in their field situations.

Generally, the results show that stingless bees pollinate as well as honeybees, factoring in the difference among the crops ( Fig. 7). The stingless bees in the glasshouse had settled long enough to adjust themselves to field conditions, implying that once stingless bees are accustomed to conditions in the field, they show their efficiency in pollination.

From the three experiments on pollination efficiency above and other surveys on stingless beekeeping techniques, T. carbonaria and S. bipunctata can be expected to show good potential as effective pollinators of crops in glasshouse conditions in temperate countries.


The efficiency of insects as crop pollinators would depend on their biological characteristics in relation to the crop and the environment in which they are needed. Each insect species which has been used as a pollinator so far would have its specific characteristics, which might be favorable or unfavorable from the standpoint of the user. The value of stingless pollinators is obvious from the farmer's point of view. Due to their compact colonies and safety for farmers and visitors, they can be used in areas where stinging insects are not desirable, as in greenhouses. However, very few surveys concerning pollination by stingless bees have been conducted in the temperate countries. The work of the author is still limited, and experiments to assess crop pollination efficiency by stingless bees and to improve colony management techniques are needed before they can be confidently used for the pollination of crops in greenhouses.


  • Amano, K., T. Nemoto and T. Heard. 2000. Amano, K., Nemoto T. and Heard T. 2000. What are stingless bees, and why and how to use them as crop pollinators? A review . JARQ 34,3: 183-190.
  • Amano, K. 1997. Successful breeding of non-stinging honey bees farming Japan 31,5: 36-42.
  • Amano, K. and S. Boongird. 1997. Keeping of the stingless bee, Trigona fuscobalteata (Hymenoptera: Apidae) in an environmentally enclosed chamber. Ann. Rept. Prot. North Japan 48: 210-212 (In Japanese with English summary).
  • Camargo, C. A. 1972. Mating of the social bee Melipona quadrifasciata under controlled conditions. J. Kansas Entomol. Soc. 45: 520-523.
  • Crane, E. 1992. The past and present status of beekeeping with stingless bees. Bee World 73: 29-42.
  • Cruz-Landim, C. et al. 1968. Mandibular gland development and communication in field bees of Trigona (Scaptotrigona) postica. J. Kans. Entomol. Soc. 41: 474-481.
  • Dollin, A. and T. Heard. 1998. Keeping Australian stingless bees in a log or box. In Native Bees of Australia Series Booklet 5. By Australian Native Bee Research Center: 1-14.
  • Esch, H. et al. 1965. Sound: an element common to communication of stingless bees and to dances of the honeybee. Science 149: 320-321.
  • Heard, T.A. et al. 1993. Factors influencing flight activity of colonies of the stingless bee Trigona carbonaria (Hymenoptera: Apidae). Aust. J. Zool. 41: 343-353.
  • Heard, T.A. 1999. The role of stingless bees (Meliponinae) in crop pollination. Annual Review of Entomology, 44: 183-206.
  • Heard, T.A. and A. Dollin. 1998. Crop pollination with Australian stingless bees. In Native Bees of Australia Series Booklet 6. By Australian Native Bee Research Centre: 2-17.
  • Imperatriz-Fonseca, V.L. 1975. On swarming activity in Meliponinae. Proc. of the 25th International Apicultural Congress: 298.
  • Kerr, W.E. 1959. Bionomy of Meliponids - VI. Aspects of food gathering and processing in some stingless bees. In Food Gathering in Hymenoptera. Symp. Entomol. Soc. Am. Detroit: 24-31.
  • Kerr, W.E. 1974. Sex determination in bees. III. Caste determination and genetic control in Melipona. Insectes Soc. 21: 357-367.
  • Kleinert-Giovannini, A. et al. 1987. Aspects of the trophic niche of Melipona marginata marginata Lepeletier (Apidae, Meliponinae). Apidologie 18: 69-100.
  • Maeta, Y. et al. 1992. Utilization of the Brazilian stingless bee, Nannotrigona testaceicornis as a pollinator of strawberries. Honey bee Science 13: 71-78 (In Japanese with English summary).
  • Michener, C.D. 1961. Observations on the nests and behavior of Trigona in Australia and New Guinea. American Museum Novitates 20261-46.
  • Michener, C.D. 1974. The social behavior of the bees: A comparative study. Cambridge, Mass, Harvard Univ. Press. 404 pp.
  • Moritz, R.F.A. 1986. Genetics of bees other than Apis mellifera. In Bee genetics and breeding, Academic Press, Inc.: 121-154.
  • Nogueira-Neto, P. 1951. Stingless bees and their study. Bee World, 30,10: 73-76.
  • O'toole, C. and Raw, A. 1991. Bees of the world. Blandford (a Cassell imprint), London. 192 pp.
  • Roubik, D.W. 1990. Biogeographical ecology of Melipona (Apidae: Meliponinae). Proc. of the 11th International Congress IUSSI: 379-380.
  • Sakagami, S.F. 1957, 1958. Biology of the stingless bee and its domestication (1), (2). Seitai-kontyu, 6,15: 101-116, 7,1: 28-46 (in Japanese).
  • Sakagami, S.F. 1982. Stingless bees. In Social Insects. Vol 3. Hermann, H. R. (ed) Academic Press, New York. USA: 362-376.
  • Tezuka, T. and Maeta, Y. 1993. Effect of UVA film on extranidal activities of three species of bees. Jpn. J. Appl. Entomol. Zool. 37: 175-180.
  • Wallace, H.M., Vithanage, V. and Exley, E.M. 1996. The effect of supplementary pollination on nut set of Macadamia (Proteaceae). Ann. Bot., 78: 765-773.
  • Wille, A. and Michener, C.D. 1973. The nest architecture of the stingless bees with special reference to those of Costa Rica. Rev. Biol. Trop. 21,1: 278.
  • Wille, A. 1979. Phylogeny and relationships among the genera and subgenera of the stingless bees (Meliponinae) of the world. Revista de Biologia Tropical 27,2: 241-277.
  • Wille, A. 1983. Biology of the stingless bees. Ann. Rev. Entomol. 28: 41-64.
  • Wilson, E.O. 1971. The insect societies. Belknap Press of Harvard University Press, Cambridge, Mass, 548 pp.
  • Young, A.M. 1983. Nectar and pollen robbing of Thunbergia grandiflora by Trigona bees in Costa Rica. Biotropica, 15,1: 78-80.

Index of Images

  • Figure 1 (L) Nest of Melipona Beecheii in an Observation Box. (R) Brood Comb of Melipona Beecheii. the Arrow Shows a Queen.

    Figure 1 (L) Nest of Melipona Beecheii in an Observation Box. (R) Brood Comb of Melipona Beecheii. the Arrow Shows a Queen.

  • Figure 2 Thermo-Responses of Adult Workers in Three Species

    Figure 2 Thermo-Responses of Adult Workers in Three Species

  • Figure 3 Temperature in and Out of the Nest of Honey Bee, Apis Mellifera (Above), and the Stingless Bee, Trigona Carbonaria (below)

    Figure 3 Temperature in and Out of the Nest of Honey Bee, Apis Mellifera (Above), and the Stingless Bee, Trigona Carbonaria (below)

  • Figure 4 Temperature in and Out of the Hive Box

    Figure 4 Temperature in and Out of the Hive Box

  • Figure 5 Pollination Efficiency for White Clovers by Four Species

    Figure 5 Pollination Efficiency for White Clovers by Four Species

  • Figure 6 Differences between T. Carbonaria and B. Terrestris in Visited and Fruiting Tomatoes

    Figure 6 Differences between T. Carbonaria and B. Terrestris in Visited and Fruiting Tomatoes

  • Figure 7 Relative Incidence in Fruiting Crops by Two Kinds of Pollinators

    Figure 7 Relative Incidence in Fruiting Crops by Two Kinds of Pollinators

Download the PDF. of this document, 312,239 bytes (305 KB).