Virgin queens in stingless bee (Apidae, Meliponinae) colonies: a review Vl Imperatriz-Fonseca, R Zucchi

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Vl Imperatriz-Fonseca, R Zucchi. Virgin queens in stingless bee (Apidae, Meliponinae) colonies: a review. Apidologie, Springer Verlag, 1995, 26 (3), pp.231-244. ￿hal-00891261￿

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Virgin queens in stingless bee (Apidae, Meliponinae) colonies: a review

VL Imperatriz-Fonseca R Zucchi

1 Departamento de Ecologia Geral, IBUSP, CP 11461, CEP 05422-970 São Paulo, SP; 2 Setor de Ecologia da Faculdade de Filosofia, Ciências e Letras da USP, CEP 14 300-000 Ribeirâo Preto, SP, Brazil

(Received 9 December 1994; accepted 20 March 1995)

Summary — There are no differences between Trigonini and Meliponini in terms of their treatment of virgin queens. They may stay in the nest, leave during swarm, supersede the dominant queen, or be killed, depending on what happens inside the colony. However, some kinds of behavior and strategies are characteristic of each species and part of its repertoire; examples are the onset of attractiveness, type of isolation, maturity, and the permanence of gynes in the colonies. Behavioral patterns are sim- ilar to all gynes. Attractive gynes have swollen abdomens, and abdominal glands are exposed during periods of attractiveness; they are very active, they run through the colony and search for trophal- laxis. Natural polygyny occurs in Melipona bicolor, but needs additional studies to be well understood. Temporary oligogyny occurs during supersedure process in Plebeia. The control of the number of vir- gin queens during certain periods of time is suggested in Trigona (Trigona), acting on the gynes’ emergence from royal cells or simultaneous metamorphosis of pupae. The presence of gynes in the nests stimulates swarm or supersedure. In these bees, one or more virgin queens depart with a swarm; fertilization occurs in a nuptial flight near the new nest. Swarm is a gradual process, with resource transportation from mother to daughter colonies. Supersedure may or may not be gradual. Attractive gynes, as well as workers, take active part in this process.

Meliponinae / stingless bees / gyne / queen supersedure / swarm

INTRODUCTION perenniality if the dominant queen dies. It is assumed that stingless bee queens have control over worker activities Meliponinae, which are highly eusocial bees, pheromonal and as occurs in other similar constitute a very interesting and diversified physiology, group. Little is known about their reproduc- eusocial species (Engels et al, 1987, 1993). tive strategies (Engels and Imperatriz-Fon- Although the nature of such regulations is seca, 1990). Massive provisioning of the unknown, it probably differs from the closely brood cells entails the need to keep gynes related Apinae. The permanence of attrac- (virgin queens) in the colony to ensure its tive gynes in the nests is a central point in stingless bees sociobiology. As stressed by BEHAVIOUR OF VIRGIN QUEENS Sakagami (1971), the socio-ethological IN MELIPONINI make-up of both societies (Apinae and that their similar Meliponinae) suggests The Meliponinae comprise 2 tribes: eusocial were reached patterns divergently. Meliponini, with a single genus, Melipona, The pattern of queen dominance pre- and Trigonini, with several genera (Moure, sented by Apis mellifera and its effect on 1961). The larger royal cells of the Trigo- workers is normally used for comparative nini distinguish them from the Meliponini, purposes. In this species, the queen con- whose queens, males and workers are bred trols the appearance of royal cells and also in identical cells. the activation of workers’ ovaries (Pain, In Meliponini, castes are determined by 1961; Free, In the 1987). Meliponinae, royal the interaction of genes with the environ- cells are constructed all the and year round, ment (Kerr et al, 1966; Velthuis and Som- whether the has influence on the queen any meijer, 1991). Virgin queens are smaller than construction of such cells is unknown. More- workers, they emerge all the year round, and over, the nurse-workers of most of the stud- are usually killed by workers. In Melipona, ied taxa have activated ovaries and pro- queens have similar characteristics in their duced that are eaten the eggs generally by behavioral repertoire; they have a shorter in such a if is queen. So, taxon, there any ontogeny than workers (data for M marginata control the it involves by queen, probably and M quadrifasciata), and normally emerge different in to pathways comparison Apinae. without attractiveness, ie they do not release This concerns the of work- mainly oviposition specific responses in workers. At the onset ers that will males, after dominant yield of attractivity they move more quickly around and the queen oviposition during opercula- the nest, requesting food from workers by tion of cells (Beig, 1972). making contact with their antennae aided by As regards the emerging virgin queens, their front legs. This is the stage at which they may be killed, supersede the dominant pheromone production probably starts. queen, or swarm to start a new nest with Attractive queens generally keep their workers. All 3 possibilities occur in different abdomen swollen and appear larger. They episodes of the colonial cycle. Several fac- actively seek the area where the new comb tors certainly influence these events, of is being built, particularly during the cell pro- which the respective promoters have not visioning and oviposition process, and may yet been identified. possibly ingest alimentary eggs laid by work- This paper presents a review of the virgin ers (Silva et al, 1972; Kleinert-Giovannini, queen’s behavior and permanence in sting- 1989). At the peak of their attractiveness, less bee nests. Most of the reproductive they expose their swollen abdomen to the of the aspects dealt with here are only factual and majority surrounding workers, through derive from unplanned events that took circular movements. Such gynes may then be killed or When the place in the course of several experiments accepted. gyne is and observations. This indicates the char- accepted, she helps workers eliminate the acter of this paper, which mainly intends to other virgin queens. report facts that are not normally delivered In normal colonies, the attractiveness of in formal publications on account of their the virgin queens causes an agonistic atti- incidental occurrence. The generic citations tude among workers who start chasing and throughout the text follow the classificatory killing them by twisting off their heads and system devised by Moure (1951, 1961) and other body parts. Such remains are placed Camargo and Pedro (1992). in the refuse area and removed from the colony. This is the fate of most Melipona M bicolor presents a natural polygyny. queens. M marginata, however, sometimes The term polygyny is used here in the same preserves a larger number of queens inside way as Herbers (1993) did: "to denote the the colony (Kleinert and Imperatriz-Fonseca, peaceful coexistence of 2 or more mated 1994). They take refuge in common areas, egg-layers (queens) in the same nest, ...and such as parts of the exoinvolucrum, remain- the intermixing of their offspring within one ing there for hours. From the body posture socially homogeneous unit". Colonies of M of the virgin queens, and the trophallaxis bicolorwith large populations may have as that occurs, it can be assumed that there is many as 5 physogastric queens simultane- an hierarchy among them. Therefore, in this ously involved in oviposition, apparently case, several queens are protected as a without any agonistic behavior (Bego, 1983, group by a physical barrier. 1988, 1989). There are even situations in Mota studied the development of abdom- which 1 queen remains to attend to the cell where the larval food is while inal glands in Melipona queens (Mota, 1982, being placed, 1988; Cruz-Landim and Mota, 1990). The another approaches and lays. Although presence and development of these glands dominance among queens is likely, conflicts may explain why the virgin queen rubs the are suggested by the male production by tip of her enlarged abdomen on the work- the workers, which is conspicuous than in ers’ head; this has been observed in polygynic nests, and the length of the inter- M quadrifasciata and M marginata at the val between oviposition by the queen and peak of her attractiveness. This might also cell operculation by the workers. Other explain the apparently defensive mecha- behaviors that differ are related to the kind nism used by the virgin queen of M quin- of courtship that workers pay to the queens, quefasciata, who spins around at high with pronounced antennal contact and a speed, hitting workers with her abdomen long duration. them into the distance. While and tossing Unlike those of other known stingless this is the mem- occurring, intersegmental bees, dominant queens of M bicolor rarely branes of the virgin queen’s abdomen are beat their wings, which thus do not wear out exposed, and whenever possible this region as they become older (Bego, 1988). A dom- is pressed against the workers’ heads (Zuc- inant queen may live as long as 7 years chi, 1977). Regarding the natural super- (Drumond, personal communication). Most sedure of queens in Melipona, Silva et al colonies kept in laboratories are mono- described the process for M quadri- (1972) Observations showed increased fasciata and M quinquefasciata. In the phase gynous. queen numbers under laboratory conditions preceding supersedure there are many vir- in colonies with extra food. One gin queens, one of whom occupies an out- provided of these colonies had 2 standing position even before the dominant physogastric 1 of which laid most of the queen is eliminated. If virgin queens con- queens, eggs. A third was selected and tinue to emerge, the possibility of choosing virgin queen mated. When the new a new queen is present. Kleinert-Giovan- queen began laying, nini (1989) observed that the supersedure in her abdomen was very small and similar to Melipona marginata starts taking place when that of an attractive virgin queen. For a few the queen’s productivity is low. Silva et al days only this newly fertilized queen prefer- (1972) made similar observations regard- ably participated in the arousal phase and ing M quadrifasciata and M quinquefasci- oviposited in cells. Later on the dominant ata and highlighted other disorders on these physogastric queen began ovipositing more occasions, affecting provisioning and lay- frequently, although both occasionally took ing of eggs in brood cells. part in stimulating the oviposition process. The polygyny needs further experimental than workers, and older royal cells can studies to be better understood. therefore be found in the involucrum, sup- bars of since the Kleinert-Giovannini (1989) used an experi- ported by cerumen, origi- comb in which were has been dis- mental technique to promote a polygynic nal they mantled. Some of these cells rise to status, by adding a second physogastric give queen to normal colonies of M marginata. giant males (Nogueira-Neto, 1951; Juliani, For some time, both queens remained alive 1967; Imperatriz, 1970; Imperatriz-Fonseca and ovipositing. It was possible to study the et al, 1975; Silva, 1977; Cortopassi-Lau- conflict of interests of both queens and their rino, 1978; Bego and Camargo, 1984). progenies, taking into account the degree Royal cells may very occasionally produce of relatedness among queens and the health giant workers (Oliveira and Imperatriz-Fon- of their nests (Kleinert-Giovaninni, 1990). seca, 1973). Andrade and Kerr (1990) also changed Royal cells are usually built at the edge of queens among M compressipes colonies, combs. They have the same shape as ordi- adding a second physogastric queen in nary cells, but in Paratrigona subnuda there experimenting with other colonies. are 2 royal cell architectures: 1 is bottle- Melipona queens are fertilized by a single shaped and the other normal. They are male (Kerr et al, 1962; Camargo, 1972, sometimes found side by side. Royal cells 1984; Silva et al, 1972; Page and Kerr, are sometimes built in the center of the 1990). In M quadrifasciata and M quinque- comb. fasciata there is evidence of queens making The number of royal cells built varies from when are 3 to 8 old. nuptial flights they days 1 species to another, and within the same were 33-102 min Nuptial flights long, lasting species it is influenced by many factors. (Silva et al, 1972). There is no evidence of Under favorable conditions, several colonies males close to the entrance of aggregating will often build royal cells at the same time. the colonies when a needs Melipona queen Biotic and abiotic conditions will together act to mate. verified that Sommeijer (1994) to determine the fate of virgin queens. In of M favosa until a non-nest queens fly subtropical environments, an increase of drone area that is formed in congregation construction of royal cell occurs in autumn, the of the neighborhood colony by approx- for instance, in Plebeia remota (Van Ben- 400 drones from differ- imately originated then et al, 1995). Besides the environmental ent nests. factors, the biotic factors that seem to be After the nuptial flight, parts of the male’s important include the physiological state of genitals remain stuck to those of the female. the queen, the population size of the colony This is called the mating sign (Kerr and and the amount of stored food. Krause, 1950; Silva et al, 1972). Occasion- Most stingless bees produce castes ally, when the hive is being handled, the under similar ontogenetic periods. However, physogastric queen may mate again (Cam- in some Trigona, the development period pos and Melo, 1990), but this is an unusual of the is much as a con- situation and reflects abnormal condition. queens longer and, sequence, their nests generally show many such cells scattered around the brood cham- well from the combs. BEHAVIOUR OF VIRGIN QUEENS bers, apart remaining In a nest of 132 IN TRIGONINI given Trigona crassipes, queen cells were found (Camargo and Roubik, 1991). This normally happens In Trigonini, queens are usually larger than because, although queen cells are always workers. They also have a longer ontogeny built at the edge of fully grown fresh combs, their delayed development means that they exactly the same size as the workers or remain long after the emergence of their smaller and can be termed miniature queens synchronously produced sister-workers (fig 1). These categories of queens have (Sakagami, 1982; Camargo and Roubik, different numbers of ovarioles (Camargo, 1991). This is probably the outcome of 2 1974). The combs contain cells with slightly characteristics: post-defecating queen larvae larger pupae which produce medium-sized apparently remain at a quiescent stage for queens, as well as a few large royal cells, long periods (maximum observed time, 11 which produce large queens or giant males. months in T hypogea); and the fully devel- In 2 years of recording the cells being built oped queen remains in the royal cell for by a colony of these bees, only 1 cell being another variable but normally long period constructed was slightly larger than normal. before emergence. Indeed, in some cases, An additional factor that makes this discus- if the cell membrane is torn apart, the fully sion harder is that the size of workers may pigmented queen moves around quickly and also vary, mainly according to colonial con- can even fly. These adaptations increase ditions. When virgin queens are emerging, there be as as considerably the number of gynes available may many 30-40 queens and can make an eventual supersedure pro- simultaneously. cess less hazardous than usual. Moreover, Except in the case of S quadripunctata, Trigona bees usually make very large nests normal colonies do not usually contain and their queens normally have an miniature queens, ie queens of Trigonini increased number of ovarioles (10-15) per reared in cells normally built for males and ovary. workers. There are references to these miniature in the literature In some Trigonini, royal cells are rarely queens femorata, seen in the nest. Among these, Leurotrig- (Cephalotrigona Nogueira-Neto, ona mülleri and Frieseomelitta varia are of 1951; P juliani, Juliani, 1962; P remota, et al, 1975; P emerina, special interest since they are capable of Imperatriz-Fonseca Kleinert P dro- breeding queens in 2 different ways. One (personal communication); P remota and testa- is the classic method, ie by building royal ryana, Nannotrigona cells. However, Terada (1974) found that ceicornis, Imperatriz-Fonseca et al, unpub- lished data). In the case of N testaceicornis, in these bees royal cells may originate by 7 miniature queens were found in a comb superfeeding some of the larvae. They then perforate the wall of a neighboring cell and consume the food it contains. The prepupa can then enlarge its cell to the size of a royal cell. This system evidences a different method for producing queens compared with the other stingless bees studied to date. Other stingless bees regularly produce queens of different sizes, eg, Schwarziana quadripunctata. One characteristic distin- guishing this Trigonini species from others is the regular emergence of queens of vary- ing sizes throughout the year. Camargo (1974) remarked that combs with pupae point to the presence of larger cells in an irregular spatial arrangement, which give rise to queens. Some of these queens are also containing a normal royal cell; the selves can open or close the royal cham- colony was swarming. In this case it was bers, allowing some workers to enter or possible to observe the behavior of these leave them. The name prison could give queens, which did not differ from that of nor- the idea of an area under complete worker mal queens (Imperatriz-Fonseca et al, control, which is a misunderstanding of the unpublished data). Lucio de Oliveira Cam- phenomenon of a protected individual terri- pos also found 5 of these queens simulta- tory. neously in N testaceicornis. These facts A different strategy has been observed in constitute a challenge to the theories of C longicornis and L mülleri (Terada, 1974). caste determination in Trigonini. In these bees, the virgin queen is constantly There are differences among species surrounded by a court of workers, who form (and also variations are found intraspecifi- a kind of barrier by preventing her from mov- cally) in terms of the activities of virgin ing outside the center of the ring in which queens from the moment of emergence. In she is confined. Workers forming this living some species, most of queens are born barrier prevent any aggressions to the unattractive and non-pigmented (eg, Scap- queen. Sometimes the territorial limits are totrigona, Paratrigona, Schwarziana and crossed. The virgin queen breaks out, fol- Nannotrigona), while in others they are born lowed by many workers and creating gen- attractive (Plebeia, Frieseomelitta, eral havoc. She may then be killed or once Tetragonula, Meliponula and Friesella). more ’trapped’ in a circle of workers. In this Emerging attractive means causing changes case, a mobile territory for gyne is created. in the intranidal behavior, which even may When protected by a royal chamber, the alter the of brood cell construction, process virgin queen can generally communicate worker mov- triggering specific responses, with the outside through an orifice. She can the entire hive with abun- ing quickly through be fed by workers, who may enter and leave dant abdominal movements, and seeking through the cell hole, probably transmitting for trophallaxis with workers. In exceptional information about pheromones eliminated the be so attractive at cases, queen may in the neighborhood. The gyne controls this this time that she the dom- may supersede opening, as well as the presence of workers inant queen in the nest (P remota). Being inside it (Imperatriz-Fonseca et al, 1975). born unattractive means not causing any The duration of closure varies considerably, worker at response all. from days to months. More than 1 royal Queens that emerge attractive alter the chamber in 1 colony has been observed at behavior of the colony. According to Van the same time in Plebeia and Schwarziana Benthem et al (1995), P remota queens are (Juliani, 1962; Imperatriz-Fonseca, 1990). always attractive at emergence, and most Cortopassi-Laurino (1978) observed the were killed in a few hours after emergence behavior of virgin queens in P droryana. In by workers. Those left alive can be this case, the prison, which was initially built ’enclosed’ and kept alive in cerumen cham- with thin walls, was almost always sur- bers, protected by a physical barrier of wax, rounded by workers, who deposited pure or a royal chamber, originally termed a wax outside the chamber, which gradually ’prison’ (Moure et al, 1958; Nogueira-Neto, took on quite a different shape. Initially, the 1958). ’Prisons’ have been observed in P chamber was often closed. After some time, remota, P juliani, P emerina, P droryana, F it remained opened most of the time so as to varia, F silvestrii, F languida, Tetragonisca enable the virgin queen to leave it, move angustula, Friesella schrottkyi and Scaura around the colony and return, until maturity latitarsis. Nevertheless, the gynes them- was reached. This kind of behavior was not observed in a long study of colonies of lar glands develop (Cruz-Landim et al, 1980) P remota, for example. Isolation of the gynes and they maintain trophallactic and antennal occurred shortly after emergence of attrac- contacts with workers. As soon as these tive queens in P remota, P droryana, P eme- glandular products run out, they take refuge rina, P juliani, F varia, F languida, P in empty food pots, which they seal up using (Friesella) schrottkyi and S latitarsis, and their mandibles. The period of isolation in as soon as attractiveness is manifest in these pots varies considerably. It can be a S quadripunctata. Several chambers built few minutes or several hours, during which side by side on the same day, with partially they remain alone or may be accompanied common walls, were observed in S by workers. Before leaving the refuge they quadripunctata, for queens of intermediate thrust their antennae outside the pot, prob- size (Imperatriz-Fonseca, 1990). They were ably to obtain information about the external destroyed one by one on the same day, situation. Presumably, when they have leaving one intact. The internal conditions replenished their glands with new sub- of the colony which favor construction of stances, they voluntarily leave the pot and royal chambers in Schwarziana have not circulate through the colony, seeking trophal- been clarified. On some occasions, we have laxis, and returning to the refuge whenever observed chambers being built by medium- necessary. The refuge is not fixed for the size pigmented queens, without causing use of 1 particular gyne, but can be used any worker response. Queens may remain by more than 1 queen consecutively. This in these chambers for a few days, leave and process leads to a peak of attractiveness, build other chambers in the involucrum. probably when the virgin queen completes Some form of homeostasis causes these glandular development to the secretion of queens to be tolerated, without provoking pheromone. She then tries to supersede worker any specific responses. the queen of the colony (Imperatriz-Fon- Depending on the state of the colony at seca, 1977). Thus the virgin queen usually the time when the virgin queen becomes continues her development in the colony attractive, the royal chamber may be built until she reaches maturity, passing through by the workers or by the queen herself (F specific glandular changes and being recog- schrottkyi, F varia, F languida, S quadripunc- nized by a certain number of workers tata, P droryana and P remota). Construc- through physical contacts. Workers may be tion by the queen involves the same gyrat- progressively recruited and several virgin ing abdominal movements mentioned above queens may be simultaneously active in the for M quinquefasciata, with small pieces of same colony. In the case of imprisoned cerumen being torn away from nearby walls queens (Plebeia, Friesella and Tetrago- so as to delimit a circle or ring. Workers may nisca), pheromones are probably concen- provide assistance later on. trated in the surrounding structure, which is Virgin queens who emerge unattractive, manipulated regularly by the gyne. In the usually with little pigmentation (Nannotrig- case of gynes who move around, they pre- ona, Schwarziana, Paratrigona and Scap- sumably concentrate these substances in totrigona), initially remain close to the comb, their own glands and spread them in trophal- as do newly emerged workers, and are not laxis and droppings. molested by older workers. They move Hebling et al (1964) observed a virgin freely about in the colony until they begin queen of Scaptotrigona xanthotricha who to be attractive. was kept in the colony for 32 d and then When virgin queens of P subnuda killed in 17 min, after a sudden attack by become attractive, their tergal and mandibu- workers. Although Scaptotrigona is one of the most intensely studied genera of sting- quadripunctata, but only 1 of them less bees, there are few data about the biol- oviposited. Camargo and Moure (1994) also ogy of its virgin queens (Engels and Imper- found 2 physogastric queens in Apotrigona atriz-Fonseca, 1990). impunctata, but did not mention their behav- Regardless of the strategy pursued, the ioral conditions. virgin queen must be duly recognized by In P remota, the natural supersedure workers, as is the case in other eusocial observed by Van Benthem et al (1995) bees. Supersedure of the dominant queen at occurred in a strong colony immediately varying intervals ensures the perenniality after emergence of the virgin queen and by of the colony. This process was observed the latter’s initiative, when she successively in P subnuda (Imperatriz-Fonseca, 1977), attacked the dominant queen until death. P droryana (Silva, 1972), P remota (Van After this process, however, she roamed Benthem and Imperatriz-Fonseca, unpub- freely through the colony, passing through lished data), P wittmannii (Freitas, 1994) the stages of contact with workers, and only and F languida (Ribeiro, 1989). Attempts a few days later making the nuptial flight to supersede the queen in Paratrigona, mark and resuming egg laying. the end of the process by which the virgin In F languida, Ribeiro (1989) verified queen reaches maturity, with fully devel- that when the gyne superseded the queen, oped mandibular glands. After reaching a she also attacked and was helped by work- peak of attractiveness, the virgin queen ers that kept the physogastric queen immo- deposits drops of mandibular, and some- bile. After having been chosen by the colony, times fecal, substances on the body of the the gynes help to eliminate the queen. Dur- dominant queen, which is then intensely ing the supersedure process, which is not licked by workers, and is courted by an always successful for the gyne, yellowish unusually large number of individuals. After mandibular or fecal substances are often depositing her substances, the virgin queen liberated on the comb, or elsewhere in the continues to seek trophallaxis and contacts colony (Simões, 1974; Imperatriz-Fonseca, with workers, and deposits drops on the 1977; Simões and Bego, 1979; Bego, 1989; other queen’s body from time to time. The Ribeiro, 1989). laying queen does not defend herself. Lick- ing the physogastric queen’s body, work- ers can evaluate which of the 2 queens has VIRGIN QUEENS AND SWARMS the greater power of attraction. One of them will then be killed. To depart with a swarm is another possibil- In the case of P droryana (Silva, 1972) ity for the gynes that are kept alive in the and P wittmanni (Freitas, 1994), a new nest. This unpredictable occurrence was queen may be chosen and mated so as to not generally observed within the few sting- supersede while the old queen is still active less bees species that have been studied in egg laying. Both will coexist for a time, up to now. Hockings (1884) was the first to and both oviposit over a few days. Freitas notice the participation of virgin queens in (1994) observed the change of queen attrac- the stingless bee swarm, instead of the dom- tiveness by comparing the number of cells inant queen, as in Apis. Peckolt (1894) oviposited by each queen in a batch of cells, thought that virgin queens should guide and until the new queen eliminated the other by find new nests with workers. Nogueira-Neto attacking her bodily. Workers then killed the (1954) later pointed out that colony repro- old queen. Imperatriz-Fonseca (1973) found duction in Meliponinae is a gradual phe- 2 physogastric queens in a colony of S nomenon, reporting to the long link between the mother and daughter colony in this pro- attractiveness of gynes changes after mat- cess. He also mentioned the gynes’ arrival ing. According to Engels and Engels (1988) at the new nest. Kerr et al (1962) revealed and Engels et al (1993), virgin queens of that the S postica virgin queen arrived at S postica present different patterns of age- the new nest 5 d after the beginning of the dependent pheromone composition; this process of nest construction. Sometimes, can be a rule for stingless bees. more than one gyne moves to the new nest Imperatriz-Fonseca (1975) observed where fertilization occurs. Michener (1946) swarming departure in P subnuda. In this mentioned the of a new nest of beginning case, it occurred on the same day of the a the male swarm at its jaty, including beginning of cerumen transportation from entrance. Ferreira studied (1994) T angust- mother to daughter nests. The gynes were ula and verified that those males arrived to very active. The most active searched for the daughter nest entrance earlier than the trophallaxis with the workers who carried swarm this a volatile attrac- did; suggests loads of cerumen to the new nest and left tive substance produced by the workers in accompanied by them and by males; 2 other the new nest. gynes also left the nest. This departure was Terada (1974) observed the mother and very fast, and there was no cloud of males the daughter nest of F varia and gave a in front of the mother nest. The daughter wider view of swarm activity. In the mother nest was not found. nest, an imprisoned virgin queen was Finally, it is interesting to mention another the workers; the mother nest accepted by swarm departure observed in S tubiba. A entrance was and cerumen trans- enlarged swarm left the nest and stopped near the between colonies This portation began. gyne mother nest for 2 d, similar to what occurs in left the chamber 1 h before swarm royal Apis. This possibility of another kind of departure and arrived in the new nest, 50 m swarm, as well as absconding (Inoue et al, after 30 workers of away, s, accompanied by 1984b ) within stingless bees, should be different some ages, including newly considered. emerged. In this case, males arrived at the Behavioral is in new nest entrance 5 d later. variability expected large bee families such as Meliponinae. This sur- Darchen (1977) observed the swarm in vey indicates some trends. Fluctuations in 22 nests of Hypotrigona. He also verified population size and ecological pressures will the arrival of virgin queen encircled by work- entail a plasticity of solutions for the same ers of several Clouds of males were ages. problem: the increase in the production of observed in front of the new nests. The sexuals to assure the colony perenniality. gynes fertilization occurred after 48 h. The entrance, in this case a kind of excluder for was after the fertiliza- queens, completed ACKNOWLEDGMENT tion of the gyne. Inoue et al (1984a) studied a swarm in The authors thank to W Engels for his comments T (Tetragonula) laeviceps. This is a very and helpful suggestions. rapid process, where daughter colony is independent of mother colony 1 week after the arrival of the virgin queen. Most of the Résumé — Les reines vierges dans les males remained at the nest entrance for 2 d colonies d’abeilles sans dard (Apidae, after arrival of the gyne. The behavior of Meliponinae) : mise au point. Il existe plu- gynes in the daughter nest is mentioned sieurs stratégies pour maintenir les reines before the beginning of egg laying. The chez les espèces d’abeilles sans dard. Elles incluent toutes une protection des reines essaim. La colonie peut contrôler l’apparition vierges, au moins durant certaines périodes simultanée de nombreuses reines même du cycle de la colonie. Chez les Meliponini, chez les espèces qui construisent conti- où les reines émergent et sont tuées en nuellement des cellules royales. Par grand nombre tout au long de l’année, il exemple, chez Trigona hypogea, les reines existe des possibilités pour survivre plus peuvent rester jusqu’à 11 mois dans leur longtemps dans le nid : les reines se réfu- cellule royale au stade de nymphe et ter- gient dans des endroits déterminés utilisés miner ensemble leur cycle de développe- en commun. Chez ces reines, on peut déce- ment quand un signal spécial est donné par ler des niveaux de hiérarchie. Schwarziana la colonie. Chez Trigona recursa, les reines quadripunctata présente une autre forme prêtes n’émergent pas de leur cellule royale de coexistence des reines, grâce à une plas- élargie, mais y restent pendant une longue ticité du répertoire comportemental qui va période au cours de laquelle elles consom- de la protection des reines dans des ment les réserves de leur corps pour sur- chambres royales individuelles à une totale vivre. Quant au changement de la reine indifférence à leur présence dans le nid. dominante (supersédure), les tentatives des Chez Nannotrigona et Scaptotrigona on reines vierges pour éliminer la reine en place trouve des reines en nombre réduit circu- sont fréquentes mais souvent infructueuses. lant librement dans le nid. L’étape suivante La supersédure est généralement réalisée est représentée par Paratrigona subnuda, par les reines matures, mais elle peut être chez qui les reines utilisent des pots à miel tentée par une reine fraîchement éclose, vides comme refuges temporaires. Ces pots particulièrement attractive. Un remplace- peuvent être visités par plus d’une reine ment graduel semble commun chez les dans la même journée, ce qui prouve que la espèces de Plebeia. Dans ce cas la reine protection de la reine n’est due qu’à une est choisie ; après s’être accouplée, elle barrière physique ; dans ce cas les reines commence à pondre tandis que la vieille circulent librement dans le nid pendant cer- reine physogastre est toujours en vie et taines périodes à la recherche d’échanges continue de pondre. Les comportements trophallactiques. Un caractère commun à qui dénotent une très forte attraction des toutes les reines dont il a été question jus- reines vierges sont les mêmes chez les qu’à présent est leur mobilité dans le nid. espèces étudiées : elles offrent aux Celetrigona longicornis et Leurotrigona mul- ouvrières qui entourent la reine attractive leri présentent l’étape suivante, où les reines un abdomen gonflé, recherchent les sont constamment entourées par une cour échanges trophallactiques avec les d’ouvrières. Elles se déplacent ensemble ouvrières et parfois délivrent une goutte dans le nid mais restent généralement à d’une substance jaunâtre au cours de la tro- distance de la reine fécondée et des rayons phallaxie. Le comportement le plus frappant à couvain. Chez de nombreuses espèces pendant la supersédure a été observé chez (Plebeia, Friesomellita) les reines sont main- Paratrigona subnuda, chez qui la jeune reine tenues dans des zones déterminées, les attractive répand sur le corps de la vieille chambres royales, pendant une période de reine des substances dont les caractéris- temps variable. Dans ce cas, ce n’est tiques déterminent le déroulement du pro- qu’après un signal spécial issu du milieu, cessus de remplacement. Les ouvrières par- apporté par les ouvrières ou par l’intermé- ticipent aussi aux tentatives de supersédure diaire des phéromones de la colonie, que en protégeant ou en attaquant la reine. Dans la reine quitte la chambre royale et circule le nid et dans les conditions de milieu parti- librement dans la colonie pour tenter de culières les reines vierges attractives peu- remplacer la reine ou de partir avec un vent favoriser la division de la colonie par un essaimage graduel : l’emplacement du frei im Volk. Der nächste Schritt kann am nouveau nid est choisi, préparé et reçoit Beispiel von Paratrigona subnuda gezeigt une ou plusieurs reines vierges accompa- werden: Königinnen benutzen leere Honig- gnées d’ouvrières d’âge varié. Le cérumen, töpfe als zeitweises Versteck. Diese Töpfe la cire et la propolis proviennent de la colo- können von mehreren Königinnen an dem- nie mère. La reine sera fécondée lors de selben Tag benutzt werden, was darauf hin- son vol vers le nouveau nid où, chez les weist, daß der Schutz nur eine physikali- Trigonini, l’attend généralement un nuage sche Barriere ist. Außerdem laufen die de mâles. Chez les Meliponini, les données Königinnen bei dieser Art für bestimmte Zeit- concernant Melipona favosa montrent que spannen frei im Volk auf der Suche nach les reines vierges sélectionnées volent jus- Futteraustausch (Trophallaxis). Die gemein- qu’à un lieu de rassemblement de mâles same Eigenschaft aller bisher besproche- situé près du nid. Les 2 colonies, mère et nen Fälle ist, daß sich die Königinnen im fille, communiquent pendant une certaine Nest frei bewegen können. Ein nächster période par l’intermédiaire de l’activité des Schritt ist bei den Arten verwirklicht, bei ouvrières. denen die Königinnen ständig von einem Hofstaat von Arbeiterinnen umgeben sind Meliponinae / reine / supersédure / essai- (Celetrigona longicornis and Leurotrigona mage / régulation sociale mulleri). Sie laufen gemeinsam im Nest, hal- ten aber im allgemeinen Abstand von der begatteten Königin und den Brutwaben. Bei Zusammenfassung — Unbegattete Köni- vielen Arten (Plebeia, Frieseomellita) werden ginnen in Völkern der stachellosen Bie- junge Königinnen in bestimmten Territorien, nen (Apidae, Meliponinae): Ein Überblick. den ’Königinnenkammern’, über unter- Es gibt mehrere Strategien innerhalb der schiedlich lange Zeiten gehalten. In diesen stachellosen Bienenarten, wie weibliche Fällen verlassen die Königinnen erst nach Geschlechtstiere im Volk behandelt wer- bestimmten Umweltreizen, die durch die den. Bei allen Arten gibt es zumindest Arbeiterinnen oder Pheromone übertragen während einer begrenzten Zeitspanne inner- werden, ihre Zellen. Dann zirkulieren sie halb des Volkszyklus einen Schutz für unbe- durch das Volk und versuchen, die alte Köni- gattete Königinnen. Bei Meliponinen schlüp- gin abzulösen oder mit einem Schwarm das fen Geschlechtstiere während des ganzen Nest zu verlassen. Eine Kontrolle über das Jahres. Eine große Zahl wird getötet, aber simultane Auftreten mehrerer Königinnen es besteht auch die Möglichkeit, für eine durch das Volk kommt auch bei Arten vor, längere Zeit im Nest zu überleben. Dazu die fortwährend Königinnenzellen bauen. ziehen sich die Königinnen auf bestimmte, Bei Trigona hypogea zB können Königin- gemeinsam genutzte Plätze zurück. In die- nen bis zu 11 Monaten als Puppen in den sen Fällen läßt sich eine hierarchische Zellen verharren, um dann auf einen spe- Rangordnung zwischen den Königinnen ziellen Reiz hin simultan zu schlüpfen. Bei beobachten. Eine andere Form der Koexi- Trigona recursa schlüpfen die fertigen Köni- stenz ist bei Schwarziana quadripunctata ginnen nicht aus ihren großen Königinnen- verwirklicht. Dort gibt es vielfältige Verhal- zellen, sondern verbleiben dort für lange tensmuster, die vom Königinnenschutz in Zeit, wobei sie von ihren körpereigenen individuellen ’Königinnenkammern’ bis zu Reservesubstanzen leben. Die unbegatteten einer vollständigen Gleichgültigkeit gegenü- Königinnen versuchen zwar häufig, die ber ihrer Anwesenheit im Volk reichen. Bei dominante Königin im Volk abzulösen, dies Nannotrigona und Scaptotrigona bewegen ist aber meist vergeblich. Der Königinnen- sich die Königinnen in verringerter Anzahl wechsel erfolgt überwiegend durch reife Königinnen, jedoch manchmal versucht es Meliponinae / Königinnentausch / auch eine besonders attraktive frisch Schwärmen / soziale Regulation geschlüpfte Königin. Ein gradueller Ersatz der alten Königin ist bei Plebeia Arten ver- breitet. In diesen Fällen wird eine neue Köni- REFERENCES gin ausgewählt. Nach ihrer Begattung beginnt sie mit der Eiablage, während die Andrade CM, Kerr WE (1990) Experimental exchange of alte physogastrische Königin noch lebt und queens between colonies of Melipona compressipes (Apidae, Meliponinae). Rev Bras Biol 50, 975-981 Eier legt. Die Verhaltensweisen von unbe- gatteten besonders attraktiven Beig D (1972) The production of males in queenright Königinnen colonies of Trigona postica. 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