JARQ 34(3), 183- 190 (2000) hltp://ss.jircas.afirc.go.jp

What are Stingless , and Why and How to Use Them as Crop Pollinators? - a Review -

Kazuhiro AMAN01*, Tetsu NEMOTa2 and Tim A. HEARD3

1 Laboratory of Apiculture, National Institute of Industry (Tsukuba, lbaraki, 305-0901 Japan) 2 Laboratory of Neurophysiology, National Institute of Animal Industry (Tsukuba, lbaraki, 305-0901 Japan) 3 Long Pocket Laboratories, CSIRO Entomology (P:M:B 3 Indooroopilly 4068, )

Abstract The efficiency of as crop pollinators depends on their biological characteristics in relation to the crop and the environment in which they are needed. For glasshouse in Japan, stingless bees are potentially promising pollinators for the following reasons: they are harmless to and glasshouse workers, they visit a wide range of crops (polylecly), they are tolerant of high tempera­ tures, they are active throughout the year, they can be transported easily, and they do not pose an envi­ ronmental by escaping and invading natural as they would not survive the Japanese winter. There are still, however, some limitations to using stingless bees in such areas, one of which lies in how to improve methods for propagating and maintaining the colonies throughout the year. To address this prob! em we suggest the development of a new type of hive box.

Discipline: Crop production I Horticulture Additional words: , meliponiculture

111i11a11gkaba11, T. moorei, T. itama, from ; Introduction Na111101rigo11a testaceicomis, dro,ya,,a, T. a11g11s111la, T. barocoloradensis from , with a view Stingless bees are soc ial bees which lack a func­ to testing them as pollinators of strawberries and pub­ tional st ing. They store and , and are some­ lished a note stating that N. lestaceicomis was the most times called stingless honey bees11>. Since they occur in effective one and that economical fruit production could perennial colonies in tropica l and subtropica l climates, it be maintained by the introduction of colonies into is impossible for them to survive naturally th roughout lhe glasshouses 15>. cold season in countries w ith a temperate climate such as In this paper we describe the use of insects as crop Japan. Considering that these people-friendly and eco­ pollinators in Japan, and also the potential of the st ingless system-friendly bees could be used as crop pollinators, , T. carbonaria, from Australia to be kept and utilized we introduced colonies of several species from Australia successfully as pollinators under glasshouse conditions. and other countries, and investigated methods for keep­ ing and multiplying hives. Status of pollinator utilization in Japan The general biology of stingless bees has been 17 23 18 described by various authors • • >, and pollination by Where no pollinators are available, many crops need stinglcss bees in tropical areas has been reviewed hand or mechanical pollination. Multiple use of insecti­ recen tly9>. Most of the research, however, has been con­ cides and expansion of single cropping, both of which ducted in the areas where the bees live. Very little work have been conducive lo the development of modern agri­ on using stingless bees introduced from overseas has cu lture, have also led to the decrease of natural pol lina tor been performed in Japan, much less from the practical populations. In addition, cultivation under structures, pollination point of view. Sakagami introduced the con­ such as glasshouses or , where no rain, w ind, cept of domestication of stinglcss bees first into Japa1122>. or natural pollinators could be expected, has been dis­ Macta ct al. imported 7 species of stingless bees, Trigo11a sem inated in response to the rising demand for fruits and

* Corresponding author: fax +81 - 298- 38- 8606, e-mail [email protected] Received 5 November 1999, accepted 7 December 1999. 184 JARQ 34(3) 2000

vcgc1ab les. These agricu ltural conditions have stimu­ age them by themselves. lated 1he demand fol' efficient manageable pollinators for The third is the , or the European crops. honey bee, Apis mel/ifera. This well-known social insec t Three species or insects have had a great impact on is an important pollinator of orchards, fields, and large­ crop pollination recent ly in Japan. scale glasshouses partly because of its large co lony popu­ The lirst is Osmia cvm((rv11s, a solitary bee used lation (over 10,000 individuals), long distance nights since 1945 and now essential for the pollination of crops, (more than 2 km), wide range or plants on which it for­ especially of apples. The po llina1ing ability of Osmia ages (more than 80% of cultivated crops), and availabil­ com(fi,)1/s on apple is considered to be much higher than ity of estab lished beekeeping techniques. In fact, honey 1hat of the honey bee. Osmia com((rons is so efficient at bees are used widely as pollinators overseas but 1101 in pollinating crops tha1 ii was introduced into the USA in Japan. Most of the Japanese farmers who need poll ina­ 1977 for sma ll orchards on the East coast, and into Den ­ tors do not keep the honey bees by themse lves, but, if mark for crops. Its li fe cycle is very simple: necessary, have professiona l beekeepers manage the col­ the mated female makes a series or cells in the tubes it onies. There are only 5,000 professional or semiprofes­ se lects for nesting in spring; when foraging trips occur, sional beekeepers in Japan, the smal I number of which each cell is Ii lied with a honey pollen mixture on wh ich it limits the use or honey bees as pollinators. lays an egg; a new adult emerges within the nest in early Both and Osmih comifro11s bees have autumn and overwinters therein; she appears out of the been commonly used mainly because the farmers can nest anti mates and then makes foraging trips for a new manage the bees by 1hemselves unlike the case of honey nest in the following spring. The foraging period co in­ bees. A study aimed at breeding a mu rant strain of honey cides with the nowering of apple. Since Osmia comi­ bees with non-stinging characteristics by using gamma fi'o11s bees nest in bamboo or recd and readily accept radiation has been initiated so that the farmers can man­ art i licial nests, beekeeping is simple for the farmer to age the colonies for pollination with easc11. manage with minimal skill. Presently the bees arc being Only honey bees and slinglcss bees are highly euso­ used as apple pollinators in more than 18,000 ha of­ cial spec ies living in perennial colonies which are easy to orchards in the northern part of Japan, and furthermore keep in hives and to be moved to any place, when neces­ the bees will be applied 10 other crops by shilling 1he sa ry. As a highly eusoeial bee group. st ingless bees also adult emerging time through the control of the hiberna­ share various useful characterist ics, and could be tion tempera ture. expected to be effective crop pollinators. T he second useful insect pollinator is the European , /30111b11s terrestris, which is a social inscc1. Stinglcss bees and honey bees Unlike honey bees or stinglcss bees, the colonies are annual and only queens fertilized the previous autumn Social insects show some of the following character­ survive the winter in hibernation alone and appear in istics: cooperation among adults in brood care and nest spring to start up new co lonies by themselves. The first construction; overlapping of at least 2 generations; and adults produced by the queen arc all workers. With the reproductive division of laborm. Those which display all progression of the season, the co lony becomes more pop­ 3 of the above characteris1ics are ca lled eusocial insects. ulous. Males and new queens arc produced at the climax Of over I 0,000 dilTerent species of social insects cxisiing of colony development around summer. The males of the today, honey bees of the subfamily and st ingless colony. whether they mated or not. die before the onset of bees of the subfamily Meliponinae, have attained the the winter season. So do the workers. fn the case of arti­ most advanced social levels and they are called highly ficial nests, the co lony around the climax of i1s develop­ eusocial insects. The colonies of other social insects die ment can be used for crop pollination for about 2 months. when the fertile individual dies. But honey bees and The bumble bee is cons idered to be an efficient pol I inaior stinglcss bees live in perennial colonies by replacement of some crops because buzz-pollination of crops that or the queen when needed. European honey bees and require it such as Solanaccac can be achieved. Buzzing Oriental honey bees (A. cernna) have been kept for a long bees cling to the ends of the anthers and vibrate their indi­ time in Europe and Asia (beekeeping or apiculture), and rect night muscles, leading to pollen release. stingless bees have been kept in Central and South Amer­ The colonies have been imported from Europe since ica (stingless beekeeping or 1neliponiculturc) due to their 1991 for pollination of tomatoes alone in glasshouses, perennial colonies. and now more than 30,000 co lonies arc imported per yea r. These bees arc popular because farmers can man- K. A111a110, T. Ne111010 & 1: A. Heard: Slingless Bees as Crop Po//im11or.1· 185

Biology of stingless bees bees have various and efficient means of defense fo r col­ onies. Some species adopt aggressive ways of defense, The characteristics of stingless bees including r. like biting (7: cupia. T. ji1scipe1111is), emi1ting a caustic carbonaria are reviewed here. liquid from the mouth (all species of 0).y/rigona), releas­ ing unpleasant odors (T. capita/a, J'vl. 111argi11aw) and irri­ I) Distrib111io11 tating by crawling into eyes ears, etc. I lowever, the most Stingless bees arc considered to have their center or common strategy of defense is to make their nests and the origin in and have dispersed 10 other tropical and entrance invisible 10 intruders. T herefore, most species subtropical parts of the world, based on pa leontological do 1101 harm people or . and biogeographic data. This hypothesis is also sup­ T carbonaria is a gentle species and can be manipu­ ported by the fact that their primitive species with a well­ lated w ith case. T he insects defend Lhe nest by sea ling up developed sting system live in Africa exclusivcly27>. all unnecessary nest openings, and sometimes crawl over Stingless bees belong to the subfamily Meliponinae persons, and give tiny nips with their mandibles when in the family . In general, stingless bees are easily their nest is disturbed6l. distinguished from other bees by the fo llowing 3 charac­ ters: reduction and weakness of' the wing venation; pres­ 4) Nest s11·11ct11re 281 ence of the pcnicillum; and reduction of the sting • In A few species of stingless bees build their nests in contrast to Apinae which consist of only 4 main species underground cavities such as mounds, most of and less than IO species in total in the one genus Apis, them belonging to primitive groups, e.g. genera of Meli­ Mcliponinae are a fairly large group with diverse mor­ pfebeia, Plebeia, and Nogueirapfs. Some other species phology and biology. The group contains more than 400 build an exposed nest which is surrounded by lrnrd and species. At least 250 species have been described in sometimes brillle layers hanging 0 11 tree branches in the South and where research has been most air. Those species do not seem 10 have ever been consid­ advanced. About 50 spec ies live in South Asia and ered for beekeeping. Malaysia, and 20 in Australia, Papua New Guinea, and The most common type of nest is found in a tree the Philippines and as many as 40 arc native to Africa. cavity. The nest is usually made or 5 pa rts; brood comb. Since the forests in the tropical areas mostly consist of involucrum, store pots, batumen, and an entrance. T he en tomophilous plants, stingless bees arc of great impor­ comb consists of brood cells, in each of which a single tance for the pollination of many wild plants in addition young is reared, and su rrounded by a sheath of cennncn, to tropical crops211• or involuenun (Fig. I). Therefore, the cavity where the brood cells are present is called a brood chambeL Ceru­ 2) Species used.for sti11gles.1· beekeeping mcn is made ofa mixture of wax secreted from the glands The important genera for st inglcss beekeeping are on the abdomen of workers and , which is lvlelipo11a and 'frigona. Crane listed I 4 species of Meli­ derived from collected from plants. Honey and /JOiia and 21 of Trigon{I that have been used in traditional pollen are stored in pots quite different from the brood beekeeping•>. species arc restricted 10 Central cells. These storage pots are usually placed above and and , and are of historical significance below the involucrum, and made of cerumen. The extra because of their long-lime culture for the production of space in the irce cavity is sealed by batumen plates, usu­ honey and wax. 1i-igona species are present in all the ally made of cerumen and mud. The en trance of the nest tropical continental areas, and traditional hive beekeep­ is a simple hole. It often extends from the nest as a tube, ing with them has occurred in tropical America and occa­ and also continues inside the nest cavity. There are pil­ sionally in Asin. Most 1i'igo11a species are relatively lars and connectives inside the nest 10 support all the small, and long-winged. Melipona species are short­ other structures within the batumen plates. The brood winged and tend 10 be larger, some being as large as cells of the combs are in contact with one another. and the 41 honey bees • combs are usually horizontal, but in some species like 7: carbo11aria is very common in coastal Queens­ 'frigo11a c{lrbonaria. the combs form a spirnl. In subgen­ land in Australia and extends as far south as Sydney, era, such as Ph:beia. Hypo1rigo11a, Trigo11isca, 1i·igo11a, being the southernmost species of all slingless bees in the and , some species construct cluster-type nests. 11 world ''· This type of nest contains a cluster of brood cells irregu­ larly arranged instead of combs. Unlike the nests with 3) Defense 111echa11is111s combs, cluster-type nests can take advantage of small and The are vestigial and non-functional bui the irregular spaces17>. 186 JARQ 34(3) 2000

Fig. I. Brood comb or the siinglcss brc. 1h1:011a carbouaria showing a spiral type

17 Only the African species Dttcty/uri,w sta11di11geri nest is occupied by adult bees including lhe new qucen '. has vertical, double combs, each consisting of2 layers or It has been reported lhat r. j11/ia11ii and T. varia carry out horizontal cells opening in opposite direclions, as in the some construction work in lhe new nesl before the young 281 13 case of honey bees • queen arrivcs 1, and thal slingless bees do noi necessarily 11 need to fly during mating- • Variations in the swarming 5) l?eproductio11 process have been reported 1n. There arc 2 ways or rcproduclion in social insects as follows: (I) development of a co lony, or increase in the 6) Pop11/atio11

(the pollen-carryi ng structures on the hindlegs) and wax and the caste is determined lrophically. In contrast. glands. queens and wo rkers are reared in cells with the same size As workers age, their tasks change. Their sequence and caste is determined geneticall y in Melipona. Kerr 281 of activit ies ca n be divided into stages as fo llows : self:. suggests that the caste genes regulate j uvenile hormone grooming (just after emergence from the pupae); incuba­ production' )>. tion and repairs in the brood chamber; construction and provisioning or cells, and feeding of young ad ults and the I OJ Foragi11g queen; rcconstrnction or the involucrum and guard duty The last stage of the workers' activity is foraging. at the entrance; and collection or pollen, , and prop­ Like honey bees, stingless bees collec t po ll en, nectar, and oli s. Basically the sequence or the workers' activities is propolis. Most of the species are polylectic, similar to that in honey bees. foraging a wide range of crops for pollen. In contrast lo honey bees, since stinglcss bees ca n ,9) Thermoregulation forage without the help of near ultraviolet light, they can Honeybees are ab le to maintain the temperature easily forage in a greenhouse with a roof made of ultravi­ 241 around the brood at 34-36°C. The Lemperall!re is ra ised olet-absorbing fi lm • The colonies of 7: ji1scobalteata with their own body heat, generated by shivering the were be ing kept without any problems in foraging in an 2 wing muscles, and lowered, if necessary, by fan ning their environmentall y controlled chamber (IO m , 26°C, wings at the nest entrance 10 draw cooler ai r into the nest 13 L: 11D wi th nuorescenl lamps) provided properly with or gathering water into the nest Lo spread over the comb. plant flowers21• T. a11g11swla, T. bip1mctata, aud T. car­ Genera ll y, sLingless bees are not as efficient as honey bo11aria can also be successfully kept in the same condi­ bees in controlling the nest temperature, especially when lioncd chamber. the temperature is low, they are inetlicicnt in raising it. This may be a factor that limits stingless bees to tropical I I) Flight range and subtropical areas. When the temperanire is high, St ingless bees show a compact flight range com­ they lower the temperature by fanning their wings at the pared wi th honey bees. The workers of honey bees can nest entrance partly for ventilation as honey bees do. forage over 2- 3 km, wh ile those of the st ingless bee ca n Only a few species, spi11ipes and T. duckei. how­ forage over I km at most. There are some correlations ever, are known to have the ability to regu late the nest between the flight range and the body si7.c of the 171 121 121 temperature within certain limits • Ou r stud ies show workers • According to Kcrr • small bees like those or that 7: carbo11aria can not easily control the temperature the subgenus Plebeia (3-4 mm) have a ni ght range of in the hive (Fig. 2). about 300 m, medium-sized bees, as in the case or the subgenu s 7hgona (5 111111), have a night range of about 9) Queen belwvior a11d ovipositio11 600 111 , large bees ( IO 111111) have a flight range of about The honey bee queen tlies when swanning occurs, 800 m, and very large bees (13- 15 111111) , i.e. 1\1/e/ipona 28 while the stingless bee queen nies only once in her life. jirliginosa, have a night range of about 2,000 111 >. Flight Once she has mated and begun to lay eggs, her abdomen activity of slingless bees is constantly influenced by the enlarges and she loses the ability to fly. As a result, she wea ther conditions81• In M. 11l(lrgi11a1a, the tlight activity remains in the old nest. In cont rast to honey bees, sting­ is correlated positively with the temperature and nega­ Jess bee queens are reared continuously, and tolerated in tively with RH, but the behavior indicates a llcxible 141 the nest for a Lime. Some of them establish new coloni es response to prevailing weather conditions • In T. through swarming or take over th e old queen. but most carbonaria. foraging bees tly over a maximum distance 11 are kill ed by workers 1. of 500 111 and usually prefer to fly over a distance of abou t St ingless bees provide the brood cells with the food I00 111 from the 11es1'°1• all al once. and then close the cell just after the queen lays an egg. In the genus Trigona, the rearing method of 12) Co1111 111111ica1iou queens and workers is similar to that of honey bees. Like the honey bees, many species of sti ngless bees Queens are reared in special large ce lls at the margi ns of are able to communicate the location of a food source. the comb and filled wi th more larval food than workers' They use a chemical secreted from the mandibular gla nd cells. The production of a queen depends on the amount and sunlight for orienteering. Foraging workers stop at of food during the larval stages, and any ferti lized egg intervals or a certain distance and leave scented spots on ca n become a queen or a worker, that is , growing imo a the way from a good source or food 10 the colony. Other queen is purely the resu lt or a greater larval rood supply, bees leave the nest and begin to follow the odor trail 188 J/\RQ 34(3) 2000 outward28>. In 'frigo11a pos£ica, the foraging workers disaster does 1101 occur. Generally, the longevity of the seem to be able to act as guide bees by leading the others queens seems lo be longer than that of the honey bees 5 2 in a group back and forth for several trips '. Some spe­ which is 3- 5 years ~'. We obtained a colony of 7: cies of stingless bees such as T. a11guswla communieate ji,scov(1r1iata from Thailand in 1995, when the colony with sounds and zigzag running. In M. quadr(f'asciala was 12 yea rs old. We have kept it under environmentally and M. merillae, returning foragers produce sou nd closed conditions for more than 3 yea rs since then. [t is impulses varying proportionally to the distance or the st ill in good condition and there has not been any 7 food sourcc ' . In T. carbonaria, a foraging bee that has exchange of queen. The workers of stinglcss bees also located a good food sou rce marks it with a chemical scent seem to live considerably longer than those of honey to help other workers find it. bees. For instance, T. xa11tl,otriclw workers spend about 6 weeks in the nest and then about the same length of 13) lo11gevity ofc olonies time in the field. a lifespan about double of that of a The colony of stingless bees could last permanently honey beeio>. by replacing the queen success ively as long as a lethal 14) Polli11atio11 efficiency Although Cew quantitative data arc available on the ('Cl influence of pollination by stingless bees on crop yield, 40 many species are considered to be useful for pollination Brood ;irc:1 1:ocxl ,toie. rucl1 of plants91, although some species can not be used. 7: 30 silvestria11a. 1: jiilvive11/rid and T. texwcea the Inner :,p;1cc nc:1r 01 20 corolla of T/11111bergia grnnd/flonr' • 1\mh1c111 T. carbo11aria is polylectic and an efTectivc potential 10 1c1111 •cr:111u~ pollinator of crops such as the nut-bearing tree, Macada­ mia integr(lolia, and also quickly adapts to new plants 10 5 ,10 previously unknown .2 i, In fact the foraging bees thrive

30 Outer hive box Brood :1rc:t 20 ~-+,~::,.c.....->,.-:::..+~=-.....=r~~r"-' Foo,I :ltUIC ;1rc:1 Thcnnn·cOntfOllcr Inner si,:u.sc of hivct•dgc 10 --+-=-----+------.+-= Amhic,11 1cmr,c1;.11111c 0: 00 0:00 0:00 (Time)

Fig. 2. Tcmpci-atu,·cs in nncl out of the nest of the honeybee, Apis mellifera (above), and the stinglcss bee, Trigo1111 c11rbtn1tll'i11 (below)

A O C 0 ~,;,,;-r--..,; A. mcllifcrn ~,.. ~

8 C A Eftecti,•c ~ O (tl'npc:rnlu~ A. cct:11,:; jnponica

B C o Hea1- ern:ccivc: T. c,ubomui. ., ~~ccmpcrnlurc rcflcctor Heater p l 11 1111 11111 111 11 11 11111111 11 1111 11 11r 1111 11 11 5 IS 36 ,15 55 0 1 0 2 0 40 so ('Cl

Fig. 3. Tht.'rmo-rcsponscs of adult workers in 3 species )# Outer hive stand A : Lethal low temperature. B: EOcctivc low temperature. C: Effective high temperature. Fig. 4. Thermo-controlled hiv!' box for the stinglcss bee, D: Letha l high 1cmpem1urc. Trigo11a cfll·bo11fll·ia K. Amr111<1. T Nemoto & 7: A. Ilea!'(/; Sti11gless Bees r,s Crop Polli11ators 189 on a wide variety of Japanese nowering plants they have queen. Consequently the other one does not contain never seen before, whi ch we provided in our experiment. queens. However, in this species, usuall y several large Two hives per IO a of crop fields would be recommended cells contain developing queen bees, scattered throughout for suffi cie111 poll ination 10>. the brood comb. One of these cells wi ll grow to become a queen6>. Stinglcss beekeeping By using Uiis type of hi ve boxes, we have succeeded in keeping the colonies of T. carbo11aria in Japan with a Before honey bees were imported to South and Cen­ view to using them as polli nalors of crops in glasshouses. tral America, stingless bees were the only honey produc­ ers in these areas. Even presently hives of stingless bees References are kept for honey harvest, and some researchers have out li ned in detail the managemenl and domestication of I) A ma110, K. (1997): Successful breeding of non-stinging several stingless bee species. Various kinds of hives have honeybees. l~an11i11g Jpn., 3 1 (5). 36-42. 2) i\mano, K & Boongird, S. (1997): Kecpi11g of the sting­ been designed according to the species 10 faci litate honey Jess bee, Trigona fuscobalteata (Hyme11op1era: Apidae) harvesting and avoid the destruction of the nest 19>. in an environmentally enclosed chamber. J/111111 . Rcpt. />rot. Nortlt .Jp11. , 48, 210- 212 [In Japanese with Gngl ish I) Hives/or T. carbonaria summary]. Researchers in Australia have developed various 3) Camargo, C. A. (1972): Mating of the social bee Meli­ types of hives for T. carbo11aria61. As shown in Fig. 2, T. po 11a quadrifasciaw under controlled conditions. J. Kans. t::11101110 /. Soc., 45, 520-523. carbo11aria are not able to control the temperature in the 4) Crane, E. ( 1992): The past and present status of beekeep­ hive, compared wiLh honey bees. The to lerance of low ing with stinglcss bees. Bee World, 73, 29-42. temperature in 1: carbo11aria adult bees is not appreciably 5) Cruz-Land im , C. et al. (I 968): Mandibular gland devel­ different from th at in the honey bees (Fig. 3). The honey opment and comrnun icatio11 in field bees of 1i·igona bees form a cluster when the ambient temperature is (Srnptotrigona) posiica. J. Kans. L;;11101110/. Soc .. 41 . 474-48 I. fairly low, as the temperat11Fc in Lhc hive remai ns within 6) Dollin, A. & Heard, T. (1998): Keeping Austral ian sting­ the opiirmnn range, unlike T. carbo11aria. Therefore, the less bees in a log or box. /11 Native Bees of Australia major problem for keeping them in Japan is how lo main­ Series Booklet 5. Austral ian Native Bee Research Cen­ tain them safely under warm conditions. We have tried to ter, 1- 14. design a hive in reference to Heard's works, so as to 7) Esch, H. ct al. ( 1965): Sound; an element co111111011 10 make the bees survive throughout the year and even comm11nicatio11 of stingless bees and to dances of the honeybee. Science. 149, 320-321. enable them to multiply lhe colony in Japan. The hive 8) Heard, T. A. ct al. ( 1993) Factors innuencing flight activ­ consists of two boxes, an inner hi ve box and an outer box ity or colonies of the sti11gless bee 'll'igo 11a carbonaria (Fig. 4). The inner box is designed with three stories 10 (1-l ymenoptera: Apidae). Aust. J. Zoo/., 41 , 343- 353. co111ai 11 a brood space, food storage space, and feed ing 9) I Icard, T. i\. (1999): The role of'stingJcss bees (Mclipon i­ space. The brood space can be divided for propagating nac) in crop pollination. A111111. Rev. £11101110/., 44, I83 - the colony. The outer box is equi()ped with a heater sys­ 206. I 0) Heard, T. i\. & Doll in, i\. ( J998): Crop pollination with tem which keeps the hive at a fixed temperaLu re even in i\11s1ralian s1inglcss bees. /11 Native Bees of Australia the winter season. Series Booklet 6. i\ustrnlian Nat ive Bee Research Cen­ tre, 2- 17. 2) Splitli11g the co/011y 11) lmpcratriz-Fonseea, V. L. (1975): On swarming activity To multiply the colony, the nest, especially brood. in Mcliponinac. /11 Proc. 25 th 1111. Apic. Congr., 298. 12) Kerr. W. E. ( 1959): Bionomy of Mcl iponicls. VI. Aspects should be spli t. The layers of carbonaria's brood cells 7: of food gathering a11<1 processing in some stingless bees. form a single spiral, that is, a single comb. The summit /11 food ga thering in llymenoplera. Symp. Entomol. Soc. and the advancing edges of th e spiral comb are a growing Am . Dc1ro ii , 24- 3 I. portion where new cells are constructed and added along 13) Kerr, W. E. (1974): Sex determination in bees. JII. Caste them. When th e summit reaches the ceiling of the brood determi na1lon and genetic control i11 Melipo11a. !11sec1es chamber, the growing portion appears again at the bottom Soc., 21 . 357- 367. 16 14) Kleinert-Giovanni ni, A. et al. (1987): Aspects of the to repeat its rise >. To split a nest, the inner box is prized trophic niche of Melipona 11111rgi11111r1 margi11m1, Lepcle­ open while the brood in a brood space is cut in half. New ticr (Apidac, Mcliponinac). Apidologie, 18. 69- 100. empty inner boxes are then added to each half of the orig­ 15) Maeta, Y. e1 al. {I 992): Uti lization of the Brazilin n sting­ inal inner box. Then 2 new nests arc fanned. There is no Jess bee. Nm11wtrigo11a testaceicomis as a pollinator of t>roblcm wi th the new nests which contain the original strawberries. HmwybeeSci .. 13, 71 - 78 lln Japa nese wi th 190 JARQ 34(3) 2000

English summmy]. USA, 362- 376. 16) Michener, C. D. (1961): Observations on the nests and 24) Tczuka, T. & Macta. Y. ( 1993): Effect of UVA film on behavior of 1i'igona in Australia and New Guinea. Am. cxlranidal acti vities of three species ofbecs. .Jpn . ./. Appl. Mus. Novil. 2026, 1- 46. £11101110/. :Cool. , 37, 175- 180. 17) Michener, C. D. ( 1974): The social behavior of the bees; 25) Wal lace. 11. M., Vithanngc, V. & Exley E. M. ( 1996): The A comparative study. Cambridge, Mass, Marvard Univ. cffec1 o f supplementary pollination on nul SCI of Press, pp. 404. (Protcaccac). A111111. Bot., 78, 765- 773. 18) Moritz. R. l'. A. ( 1986): Genetics of bees other than Api.f 26) Wi lle, A. & Michener, C. D. ( 1973): The nest architecture me/Ii/era. /11 Bee genetics and breeding. Academic press of' the stinglcss bees wit h special reference to those o f Inc., 121- 154. Costa Rica. Re1t Biol. 7l'op., 21, Suppl. I, pp. 278. 19) Nogueira-Neto, J). ( 195 1) : Stinglcss bees and their study. 27) Wille, A. (1979): Phylogeny and rclmionships among the Bee Wnrld, 30 (10), 73- 76. genera and subgenera of the sting lcss bees (Mcliponinae) 20) o· Toole, C. & Raw. A. ( 1991): Bees of the world. of the worlcl . Revi.,u, de Biologia Tivpical, 27 (2). 24 1- Blandford (a Cassell imprint), London, pp. 192. 277. 21) Roubik, D. W. (1990): Biogcographical ecology of Meli­ 28) Wille, A. (1983): Biology of the stingless bees. A1111. RcH pona (Apidae: Meliponinac). /11 Proc. I Ith Int. Congr. £ 11/omol., 28, 41 - 64. IUSSI, 379- 380. 29) Wilson, E. O. (1971): The insect societies. Belknap Press 22) Sakagami. S. F. ( 1957. 58): Biology of the stingless bee of Harvard University Press. Cambridge, Mass., pp. 548. and its domestication ( 1), (2). Seitfli-komyu, 6 (15), 101 - 30) Young. A. M. (1983): Nectar and pollen robbing of 116, 7( I), 28-46 [In Japanese). 1'l11111bergit1 gra111/ijlom by 7i-igo11a bees in Costa Rica. 23) Sakagami, S. F. ( 1982): Stingless bees. /11 Social insects. Biotropica, IS ( I), 78- 80. Vol 3. ed. 11.cnnann. 11. R .. Academic Press. New York,