Apidologie 37 (2006) 124–143 124 c INRA/DIB-AGIB/ EDP Sciences, 2006 DOI: 10.1051/apido:2006026 Review article

Stingless bee nesting biology*

David W. Ra,b

a Smithsonian Tropical Research Institute, Apartado 0843-03092, Balboa, Ancón, Panamá, República de Panamá b Unit 0948, APO AA 34002-0948, USA

Received 2 October 2005 – Revised 29 November 2005 – Accepted 23 December 2005

Abstract – Stingless bees diverged since the Cretaceous, have 50 times more species than Apis,andare both distinctive and diverse. Nesting is capitulated by 30 variables but most do not define clades. Both architectural features and behavior decrease vulnerability, and large genera vary in nest habit, architecture and defense. Natural stingless bee colony density is 15 to 1500 km−2. Symbionts include mycophagic mites, collembolans, leiodid beetles, mutualist coccids, molds, and ricinuleid arachnids. Mutualist bacteria and fungi preserve food and brood provisions. Nest associates include trees, termite, wasp and ant colonies. Ventilation is the means of nest environment regulation, achieved by fanning worker bees. Permanence of stingless bee nests, with annual mortality ca. 13%, implies a colony has 23 years to reproduce. Inability to freely swarm and single mating may all increase nesting specificity, competition, symbiosis and cleptobiosis in communities, while disease is rare.

Meliponini / Apidae / nest architecture / nest microclimate / evolutionary ecology

“Behind this door lives a town. They are 1. OVERVIEW dynamic and hardworking members of a na- tion whose origins go back millions of years 1.1. Nesting and diversity – years of persistent and gradual evolution. If nature be treated with only steel and fire, in a Stingless bees have populated tropical earth short time such actions will destroy the town for over 65 million years – longer than Apis, and its inhabitants. If, however, the heart feels the stinging honey bees (Camargo and Pedro, kinship with the wonders that have been cre- 1992; Michener, 2000). Both groups make ated, this tiny kingdom will be kept, so to bet- honey in perennial nests founded by a swarm ter understand the earth and its residents. The of sterile workers and a queen, and colonies well being of natural resources lies in your occasionally produce male bees.Yet stingless hands.” bees have 50 times more species and, as em- phasized here, differ from Apis in many bio- P. Nogueira-Neto, 1970, interpretation by logically significant ways. present author. Meliponines cannot migrate. Also unlike “As we have stated before, honey bees are honey bees, they produce brood in the manner not domesticated animals. It is possible to keep of solitary bees, with an egg placed on top of a bees in a hive only because we understand food mass in a sealed cell. In general, colonies their biology. Beekeeping is the application of make far less honey, and therefore have less our knowledge of bee behavior.” economic appeal, compared to honey bees (see R.A. Morse, 1994. Fig. A online only). In contrast to Apis, meliponines generally Corresponding author: D.W. Roubik, have no sting, mate only once, do not use wa- [email protected] ter to cool their nest or pure wax to build * Figures A–L are available at it, cannot freely swarm to reproduce (but in- http://www.edpsciences.org stead must first make a new domicile), and Article published by EDP Sciences and available at http://www.edpsciences.org/apido or http://dx.doi.org/10.1051/apido:2006026 Meliponine nesting 125

Figure 1. Distributional map of two distinctive nest entrance tubes constructed by workers of Ptilotrig- ona lurida (Camargo, from Camargo and Pedro, 2004). the males feed at flowers, while the gravid queens cannot fly. The manifold consequences of a single mating in stingless bees, in contrast Figure 2. Nest entrances of Partamona gregaria to multiple mating in Apis, are not explored and P. vicina in a termite nest on the side of a here (see, e.g. Peters et al., 1999). Instead, a hut (Amapá, Brazil) (Camargo, from Camargo and Pedro, 2003). view is given of general ecological and evo- lutionary settings in which stingless bee colo- nial life takes place. The nest is the central 1974). Colonies are active every day and there- place from which stingless bees mate, forage fore have sustained impact among the biota and pass through life stages. Nests are immo- (Roubik, 1989; Hansell, 1993). The individual bile fixtures and potentially long-lived, much species are recognizable from nest entrances like trees in forests where meliponines live. and often their particular site – much obvious Dispersion (spatial arrangement) of colony re- variety exists. Inside the nest, there are dif- sources and ‘stress sources’ have much signif- ferent shapes and arrangements of brood cells icance, thus a primary evolutionary response and food storage containers. Honey and pollen of meliponines to such critical factors de- are stored in separate ‘pots’. Stored nectar or fines their nesting biology (Michener, 1974; ripened honey are in nest cavity extremes (for Roubik, 1989; Nogueira-Neto, 1997; Camargo storage during heavy flowering periods), while and Pedro, 2002a, b; Biesmeijer et al., 2005). pollen and some honey surround the brood Published data on stingless bee nesting span area. However, robber bee genera Lestrimelitta over three centuries (Schwarz, 1948) and re- and Cleptotrigona collect and then store some cent syntheses include Michener (1961, 1974, mixed honey and brood provisions (Sakagami 2000) Wille and Michener (1973), Sakagami et al., 1993). The brood cells are spherical (1982), Wille (1983), Roubik (1989), and to ovoid, while food storage containers are Nogueira-Neto (1997). Research primarily small to large spheres, or are egg-shaped, or considers Neotropical stingless bees, because even conical or cylindrical. Often pots are roughly three-fourths of all species are Amer- pressed together in odd conglomerates, as are ican (Camargo and Pedro, 1992). the brood cells, ranging from individual cells on pillars, to sheets of orderly cells on combs, separated by the pillars (Fig. 3 and Figs. A, C, 1.2. Nest biology I online only). Nests made by stingless bee workers and Because nests are notable points of bee ac- habit (specific location) within forests (Kerr tivity, often spectacular examples of animal et al., 1967; Posey and Camargo, 1985; architecture, nesting biology is a highly visi- Camargo and Pedro, 2003) are foremost ble aspect of stingless bee behavior (Michener, among traits that, along with the workers, 126 D.W. Roubik males and queens, potentially help organize tivity, reproduction, and community ecology biological information with application to of stingless bees are intimately related to nest- research, economics, and conservation of pol- ing biology of each stingless bee species, and linators and honey sources. It is important to await thorough studies. intensify analysis and data collection now, be- Some large genera display considerable cause in many places the original forests occu- species-level variation in nesting habit, likely pied by hundreds of stingless bee species are produced by adaptive radiation. Large varia- degraded, threatened, or gone. tion occurs, for example, within the Neotrop- ical genus Plebeia. The nest sites and archi- tecture include nesting habits on tree trunks, 1.3. Nesting evolution and variability in crevices within rocks, in holes made by other animals, hollow stems (including tree It is a reasonable guess that not half of trunks) and in active termite nests. Some Ple- all meliponine nests are known, and few have beia build the regular pancake-like stack of been studied adequately. Architectural innova- brood cells separated by pillars and arranged tions may occur in a taxon after its divergence in circular combs, like that made by most stin- from ancestors, and at the same time, unrelated gless bees, whereas the smallest species do not species may converge due to the similarity of build combs but instead make loose chains of nesting materials or sites (see Tab. I). There cells or clusters (see Fig. A online only). Aus- is currently no clear picture as to what influ- troplebeia build loose combs, perhaps an in- ence the environment versus pre-programmed termediate comb condition (Michener, 1961). bee behavior supply to nest structures. For the Bee size appears decisive because, among tiny purpose of exploring stingless bee nesting, I Meliponini, clustered cells are the architec- generally refer to clades as genera, of which tural rule among phylogenetically diverse bees several dozen exist (see Camargo and Pedro, (Michener, 2001). In Melipona, Plebeia, Ple- 1992; Michener, 2000; Camargo and Roubik, beina, Nannotrigona, Trigona and Tetragona, 2005). In Table I, without an exhaustive list of stacked combs or a continuous spiral of comb species, it is evident the majority of nest char- are sometimes built by the same colony at acteristics are shared between various genera different times (pers. obs.). Pronounced dif- (see Kerr et al., 1967; Camargo, 1970; Wille ferences may occur geographically, as doc- and Michener, 1973; Roubik, 1979, 1983, umented for nest entrance tubes of Amazo- 1992; Sakagami, 1982; Dollin et al., 1997; nian Ptilotrigona lurida (Camargo and Pedro, Camargo and Pedro, 2003). Because melipo- 2004; Fig. 1). Individual variation in architec- nine nests incorporate a small number of ap- ture, for instance elaboration of the nest en- parently uniform materials, functions, and de- trance (Wille, 1983; Sakagami et al., 1983; signs, there is difficulty assigning phylogenetic Melo, 1996) or thickness of resin enclos- series, such as comb construction, to nesting ing the internal nest, likely relates to (1) attributes (see Wille, 1983; Michener, 2001). nest age, (2) bee genetics, and/or (3) micro- Further attempts must wait until a robust phy- environment, including predators, parasites, logeny for stingless bees is available (Camargo symbionts, rain, wind and sun. One study and Roubik, 2005; Michener, 2000; Franck demonstrates that nest architecture does not di- et al., 2004). At present no fossil nest struc- versify in pace with population divergence, de- tures or ‘ichnofossils’ are known for the group, tected using hypervariable microsatellite DNA while described species and genera are still in an Australian Tetragonula (Franck et al., increasing. This review examines biological 2004). Although there is currently little under- diversity among living stingless bees and in- standing of how micro-architectural variation cludes my unpublished observations. The se- may be adaptive, on some occasions, a nest lected examples of nesting biology help to construction technique can be related to con- identify natural selection elements that shape straints. For example, Melipona forage, and nesting natural history. The nest associates, then employ in their nest construction, small colony maintenance and defense, foraging ac- pebbles and stones. Building material of this Meliponine nesting 127

Table I. Variables for stingless bee nesting biology, and terminology*. Because most species are undocu- mented in the listed traits, and variation is implicit within a genus, the list of genera is not exhaustive and an entry does not represent all species in a genus. Specific references are available from the author.

• 1, Aggressive worker defense: Duckeola, Heterotrigona, Hypotrigona, Lophotrigona, Melipona, Oxytrigona, Paratrigona, Partamona, Plebeia, Ptilotrigona, Scaptotrigona, Tetragona, Tetragonisca, Tetragonula, Trigona • 2, Exposed nest: Dactylurina, Partamona, Plebeia, Trigona, Tetragonisca • 3, Association with termite, ant or wasp colony: Aparatrigona, Paratrigona, Partamona, Plebeia, Scaura, Schwarzula, Sundatrigona, Trigona • 4, Subterranean nest or non-arboreal, natural cavity; Geotrigona, Lestrimelitta, Melipona, Meliponula, Mourella, Nogueirapis, Paratrigona, Pariotrigona, Partamona, Plebeia, Plebeina, Ptilotrigona, Scaptotrigona, Schwarziana, Tetragonisca, Trigona • 5, Irritant chemical defense: Oxytrigona, Melipona • 6, Flexible entrance tube and/or nocturnal closure: Friesella, Meliponula, Nannotrigona, Pariotrigona, Plebeia, Scaptotrigona, Scaura, Schwarziana, Trigona • 7, Pillars through several combs: Partamona • 8, Ventilated batumen plate; Melipona, Plebeia • 9, Multiple entrances; Lepidotrigona, Plebeia, Scaptotrigona, Tetragona • 10, Aggregation of nests with same or other meliponine species: Hypotrigona, Melipona, Partamona, Plebeia, Tetragonula, Scaura, Schwarzula • 11, Blind tubes by entrance; Lestrimelitta, Partamona • 12, Drainage tube or liquid waste discharge: Geotrigona, Meliponula, Mourella, Schwarzula, Tetragona, Trig- ona • 13, Storage pots large, either cylindrical, spherical, conical, elongate, egg-shaped, and not similar to brood cell size: Cephalotrigona, Duckeola, Frieseomelitta, Geotrigona, Melipona, Meliponula, Tetragona, Tetragonisca • 14, Queen cell: size similar to workers and male, not built on edge of comb: Melipona • 15, Cell construction: synchronous, Frieseomelitta, Lepidotrigona, Lestrimelitta, Nannotrigona, Paratrigona, Plebeia • 16, Brood cell arrangement: not made into a horizontal comb of close cells; Dactylurina, Friesella, Frieseomelitta, Hypotrigona, Leurotrigona, Lisotrigona, Plebeia, Scaura, Tetragonula (Australian-Papuan), Trigonisca • 17, Inquilines: leiodid or other beetles, collembolans, coccids, mites, diverse invertebrates, fungi, microbes (qualitative) all genera? • 18, Trash, resin, resin ball, wax deposit (qualitative, quantitative) all genera • 19, False nest or vestibule: Partamona, Plebeia • 20, Imprisonment chamber: Friesella, Frieseomelitta, Plebeia, Schwarziana, Tetragonisca • 21, Oviposition - Single or multiple advancing fronts; multiple fronts: Geotrigona, Lestrimelitta, Melipona, Meliponula, Nannotrigona, Scaptotrigona, Trigona • 22, Local names and significance (nesting, medicinal, food, fermented beverage, incense, natural enemies, absconding or defense) • 23, Entrance height aboveground and orientation (quantitative and qualitative) • 24, Stored pollen consistency: with mold, or dry; Ptilotrigona • 25, Honey sugar concentration, chemical properties (quantitative and qualitative) • 26, Fecal pollen accumulation or scutellum: Cephalotrigona, Trigona • 27, Sticky resin applied on outside of nest entrance, on substrate or tube: Lepidotrigona, Scaura, Tetragona, Tetragonula, Trigonisca • 28, Wood fiber (paper) nest material: Trigona 128 D.W. Roubik

Table I. Continued.

• 29, Cryptic nest entrances (no tube, small); Austroplebeia, Celetrigona, Dolichotrigona, Friesella, Geotrig- ona, Hypotrigona, Leurotrigona, Liotrigona, Lisotrigona, Melipona, Meliponula, Mourella, Paratrigona, Ple- beia, Schwarziana, Schwarzula, Trigonisca • 30, Hovering nest defenders; Lestrimelitta, Tetragona, Tetragonisca

* Terms coined for stingless bee nests are in Michener (1961), Wille and Michener (1973), Sakagami (1983) or noted below. Cluster nest: brood and food cells arranged in connected chains; cerumen: wax and plant resin mixed for pliable construction material; involucrum: a single or series of sheaths, made of cerumen, surrounding brood; batumen: thick involucrum forming a wall, or resin layer surfacing nest cavity (mud, seeds, wood, vertebrate feces may be added); pillars: cerumen used as anchors of nest elements; entrance tube: passageway connecting colony with outside; storage pots: containers of cerumen, sometimes nearly wax; scutellum: hard, thick outer nest structure (Nogueira-Neto, 1997); imprisonment chamber: cerumen cell attached to the nest wall, with small holes (Drumond et al., 1995); queen cell: generally on comb margin and larger than others, for all but Melipona; advancing front: area (s) of comb where new cells are being constructed; exposed nest: nest not contained in cavity; bottleneck: small tube leading into brood area (Camargo and Pedro, 2003); false nest, vestibule: area near entrance containing empty pots or cells (Camargo and Pedro, 2003); resin deposit: small mound of resin on nest floor or wall; wax deposit: similar to resin deposit; entrance tubercles: hollow finger-like projections; paper nest: outer nest covering made mostly of wood pulp (Roubik, 1989); advancing front: open brood cells, which can be made either synchronously (all at the same stage of completion) or continuously (at all stages at any time). mass could not even be lifted by most sting- 2006). However, common stingless bees with less bees. large colonies, and resources for predators to One highly distinctive trait, vertically ori- consume, also nest in the ground, approxi- ented comb with horizontal cells, has clearly mately from 20 to 200 cm depth (pers. obs., arisen twice. That trait is recorded in one see Tab. I). Neotropical and one Afrotropical genus, Only when nests are opened are the de- Scaura (Nogueira-Neto, 1997) and Dactylu- fensive behavior, such as attack or imme- rina (Darchen, 1972) respectively, and in only diate retreat, and the internal nest architec- one of five species in the former (Tab. I). ture revealed. However, defensive responses to individual small predators, such as insects that catch bees by nests, are rarely studied. 2. PLATFORMS FOR DEFENSE In a study of Panamanian colonies includ- AND FORAGING ing 40 species, half showed no defensive bit- ing behavior toward the observer (Roubik, 2.1. Nest defenses 1983). Bees were timid when approached, and retreated within the entrance. Stingless bee The site and architecture of stingless bee keepers might tend to select gentler species, colonial nests represent compromises between but this is not the case, with half of those nesting material, nest location and a com- well-known in Brazil able to actively defend bative versus cryptic colony profile. Honey nests from large vertebrates (see Nogueira- hunters, both primate and presumably other Neto, 1970). Many species are tremendously vertebrates, use nest entrances, with noises and aggressive and attack while biting, applying the sight of bees in flight or ventilating the sticky resin carried in the mandibles or on nest, to locate stingless bee colonies. In one hind legs. Among ‘fire bees’, Oxytrigona,and study of over 200 nests in Uganda, nest preda- a few others (reportedly Melipona rufiven- tors (primarily tool-using chimpanzees and tris in Bolivia, Stierlin, pers. comm.), caustic humans) most affected colonies in trees at un- secretions, containing formic acid in the for- der seven meters height (Kajobe and Roubik, mer, are applied (Michener, 2000). Bees of this Meliponine nesting 129 nature emit disagreeable odors from mandibu- phonia globulifera (Clusiaceae) provides a lar gland secretions and seem to take spe- steady resin source that is mined daily and de- cial care to fly into the hair, ears, eyes or fended by several nest mates of Trigona ful- mouth, and emit distressing sounds. Accord- viventris (pers. obs.). Resinous material de- ingly, most nests that are exposed and easily posited by female Centris on terminal nest attacked by predators have aggressively defen- cells are used by individuals or small groups sive workers, regardless of bee size or phy- of aggressive Trigona fuscipennis and T. mu- logeny (Sect. 2.3). An exception is the genus zoensis in Panama (pers. obs.). Resin sources Dactylurina in Africa (Eardley, 2004), which are generally wounded trees, and they often have exposed nests but lack aggressive de- have several species visit them, including bee fensive behavior (Darchen, 1972). Moreover, predators, some of which are stingless bee colonies that appear well protected, settled mimics (Roubik, 1989). within several cm of living tree trunk and hav- Nesting cavities with extensive sprays of ing a small nest entrance, can be either aggres- resin droplets, for several cm from an entrance, sive or timid (Sects. 2.3, 2.6). can be found on stems with nesting colonies Defending bees normally come from the of African Meliponula ferruginea (see Fig. I entrance area and nests have suitable architec- online only) Neotropical Trigonisca and Asian tural features to allow their aggregated pres- Geniotrigona thoracica, among others. The ence there (Tab. I; Figs. 1, 2 and Figs. B– use of resin to immobilize large beetles within F, I online only). Defensive strategies in- the nest has been well documented (Nogueira- clude alarm chemicals of mandibular gland Neto, 1997). Resin is usually placed on preda- origin, released in the air within and out- tors’ hair, and it is applied to objects near the side the nest (Smith and Roubik, 1983; sum- nest entrance. mary in Roubik, 1989; Wittmann et al., 1990). Hovering defenders then exit in force, face In Melipona panamica and other Melipona, the nest entrance, and engage in aerial fights hardened balls of resin are loosely cemented with non-nestmates, or directly attack larger by the entrance; when needed, the spheres animals, which retreat with a cloud of de- may be rolled into place, cemented together fending bees surrounding the head. Very few with resin and thus close the entrance to in- species, for example Tetragonisca angustula vaders (pers. obs.); spheres tend to accumu- and Tetragona clavipes, regularly maintain late in older nests at their bases (see Fig. B hovering defenders outside the nest. Hov- online only). Honey has been recorded as a ering ‘guard’ bees may defend against the defense material employed by tiny Hypotrig- robbing bee, Lestrimelitta (Wittmann et al., ona braunsi in Africa (Portugal-Araújo, 1958; 1990), or against raiding individuals from Michener, 1959). other meliponine colonies (Sakagami et al., Few stingless bees make a defensive wall 1993; Sect. 5.2). of enough thickness to permit use of nest cavities that have large openings; these are Melipona, Cephalotrigona and Meliponula 2.2. Defense materials bocandei (Portugal-Araújo, 1955; Roubik, 1983). As mentioned above, Melipona use The primary activity of non-foraging bees small stones. Colony batumen, separating the near their nest entrances is prevention of entry inner nest from the outer environment, may be by small insects, including parasites, and for built to a thickness of 10 cm with the stone, the deposit of fresh resin on external entrance mud and resin mix made by Melipona (see tubes, which may deter ants (see Fig. L online Fig. B online only). Workers of Melipona are, only). The chemistry and choice of nest resins apparently, unique in the behavior of survey- useful as repellants of natural enemies has not ing the outside of both nest and hive for sharp been studied, although the antibacterial prop- edges, openings or other irregularities, then erties of resins are well known (Lokvam and depositing material on them (see Fig. D online Braddock, 1999; Langenheim, 2003). Sym- only). Ramirez (1996, pers. comm.) noted that 130 D.W. Roubik worker Trigona corvina prunes twigs and re- (Sakagami and Zucchi, 1972, in Sakagami, moves leaves in front of the nest entrance. 1982), thus the thin shell may have more than one function. 2.3. Protection of the outer nest There are completely or partly exposed 2.4. Nest entrance platforms nests built on stems or hard substrates by ag- gressive Trigona, Tetragonula, Tetragonisca, The simplest stingless bee nest entrance Partamona, Paratrigona and Plebeia.Many protrudes slightly from the base of the entrance unaggressive species, including those within hole. Nest entrances are not only related to de- most the abovementioned genera, nest in fense and foraging (Biesmeijer et al., 2005), living trees, but those with exposed nests but to physio-chemical regulation, as dis- have an outer nest shell that is delicate, and cussed below. A small or unornamented nest workers immediately flood from the exte- entrance is cryptic (see Fig. F online only), rior of a broken nest envelope, then bite. and is usually the only passage to a relatively Biting behavior in defense against verte- small number of potentially defensive adult brates has no direct relation to bee size. bees. The narrow tube can be closed with resin Tetragonula fuscobalteata is among the most or cerumen, or coated outside with droplets aggressive and also the smallest native stin- of fresh resin where invaders like ants may gless bees in SE Asia. Aggressive colonies be halted (Wittmann, 1989; Camargo, 1984, can be aggregated in a single palm branch see Fig. I online only). Larger species, for ex- (pers. obs., Brunei), whereas stem-nesting ample Melipona, Cephalotrigona and Scap- colonies, ostensibly the same species, are un- totrigona (see Fig. B online only) also build aggressive (Sakagami et al., 1983, Peninsular long and/or wide internal nest entrance tubes, Malaysia). Tiny Plebeia minima builds a nest where foragers, ventilating bees or defenders on spiny palms (Bactris and Astrocaryum), are positioned. In addition, the inside alcove sometimes in small aggregations, and the of the nest entrance of Partamona (Camargo workers have strong biting responses to mo- and Pedro, 2003), often holds decoys of empty lestation (Roubik, 1983). Similarly aggressive storage pots or brood (Fig. 2), which may con- Tetragonisca weyrauchi builds exposed nests fuse and discourage predators who probe, such (Rasmussen, pers. comm.; Cortopassi-Laurino as long-tongued anteaters, Tamandua.Afew and Nogueira-Neto, 2003). Partamona,suchasP. pearsoni and P. p e ck - A noteworthy meliponine defensive struc- olti also have the brood chamber blocked to all ture is the ‘scutellum nest’ of Neotropical entry, save through a secondary entry ‘bottle- Trigona. This hard and thick barrier is made neck’ (Camargo and Pedro, 2003; Fig. C on- by exposed-nesting Trigona (Nogueira-Neto, line only). 1962), by hypogeous T. fulviventris (Roubik, The largest nest entrances are those made 1983), and is an ample protective shield by certain Trigona, Tetragona,andScaptotrig- (Wille, 1983). Nogueira-Neto (1962) noted the ona, in tropical America (see Fig. B on- scutellum is made up largely of bee feces. Af- line only) and Homotrigona and Geniotrig- ter microscopic analysis, Roubik and Moreno ona in Asia. Some are aggressive species, (pers. obs.) find the scutellum of Trigona corv- and they may be mimicked by other, in- ina, up to half a meter thick, is composed of offensive bees in the same forest. For in- pollen exines – feces of pollen consumed by stance, Trigona fuscipennis and T. necrophaga bees. Often surrounded by a few thin batumen have similar large-scooped nest entrance struc- covers, layers outside of the scutellum are eas- tures, but the latter displays no aggressive ily broken by predator attack, thus function to nest defense behavior, and a parallel rela- permit release of many defending bees from tionship may exist between Trigona crassipes throughout the nest surface. In similar nests, T. and T. fulviventris, which build long, wide spinipes opens holes in the outer nest shell in resin entrance tubes (see Roubik, 1979, 1983; response to temperature and ventilation needs Camargo and Roubik, 1991). Meliponine nesting 131

African and Australian meliponine bees have no such large or conspicuous entrances. In contrast, the largest bees in SE Asia, Ge- niotrogona thoracica and Homotrigona fim- briata have enormous, projecting nest en- trances, so large (a few kg and up to 50 cm in length) that their weight makes them periodi- cally fall from trees (Roubik, 1993 and pers. obs.; Roubik et al., 2005). Those large bees have no accessory galleries or lamellate pas- sageways at the entrance, and no aggressive nest defense. The building of a very long but slender nest entrance tube by Neotropical T. cilipes,AsianT. collina, and related species, derives from placing fresh resin on the tube (pers. obs.; see Fig. I online only). In contrast, aggressive (toward humans) Asian Heterotrig- ona canifrons and H. itama (Sakagami et al., 1983) have relatively small, simple entrance tubes.

2.5. Entrance refinements

A defense employed by diverse meliponines is closing the external nest entrance at night, usually accomplished with a ‘curtain’ of a loosely knit (spaces are visible between the mandible-carried bits of resin and cerumen) sheet that covers the entrance. This Figure 3. The nest gallery of Schwarzula cocci- certainly implies that resin or mere barriers dophila and its symbiont coccid (Hemiptera) Cryp- are effective against small parasites (Sect. 4.6) tosternum, scale insects which produce wax used by or ants. the bees for nesting (Camargo and Pedro, 2002b, Camargo (Copyrighted 2002 by the Association for Although large nest entrances are staging Tropical Biology, P.O. Box 1897, Lawrence, KS areas both for foraging and defense, an elab- 66044-8897. Reprinted by permission)). orate entrance or large exit hole are not neces- sary for effective defense against small natural enemies – largely within the nest – or for ag- gressive attacks outside, on marauding verte- the exit of defending bees, but there is only a brates. Given appropriate alarm pheromones, relatively small hole at the base of the ‘fun- bees stream outside the nest, as in Melipona nel’. The entrance of Mexican Lestrimelitta ni- panamica (pers. obs.), and the absolute size itkib designs its entrance for heavy traffic(see of a nest entrance need not be associated with Fig. F online only). The single largest sting- intensive forager traffic (Roubik et al., 1986). less bee nest entrance is of aggressive Trig- Recently, however, an analysis of foraging ac- ona silvestriana (syn. truculenta), in the Pe- tivity and external nest entrance size revealed ruvian Amazon (see Fig. C online only). The a positive correlation (Biesmeijer et al., pers. only other meliponine with such a structure is comm.). Nest entrances of most Partamona Geniotrigona thoracica (pers. obs.) but that of are made like a baseball glove (Camargo and T. silvestriana is a hard resin tube, nearly a Pedro, 2003; Fig. 2), allowing either large in- meter in length and 10 cm in diameter, with flux of incoming foragers to be funneled in, or hard resin lamina along its inside axis, thus a 132 D.W. Roubik large surface area on which many bees assem- tions allow pooled defense against large preda- ble (see Fig. E online only). tors. Direct molestation, rather than the re- Lestrimelitta (see Fig. F online only) and lease of alarm pheromone dispersed in the air, aggressive Partamona make hollow tubes or evokes multicolony attack in Partamona peck- ‘tubercles’ around the exterior nest entrance. olti (Roubik, 1983). Numerous species of this The former are unaggressive toward verte- genus are defensive (see Camargo and Pedro, brate predators at the nest. However, rob- 2003). Group defense occurs among small ber bees routinely engage in battles with ri- meliponines such as Hypotrigona (Kajobe, val colonies (Sakagami et al., 1993), and the pers. comm.; Michener, 1959) and Tetrago- fights may be shortened by decisive battle. nisca weyrauchi, but not Asian Tetragonula or Blind tunnels seem purely defensive in both Heterotrigona (Starr and Sakagami, 1987) or contexts. Their adaptive significance is to in- Scaura tenuis (see Kerr et al., 1967), which crease the available surface area for defend- form aggregations. ing bees, in the same manner as a large- bore entrance, lamellate plates in nest entrance tubes for exiting foragers, ventilators and de- 3. NEST CONDITIONS, MATERIALS, fenders, or multiple platforms and exit holes AND MAINTENANCE on the tube, e.g. those of Tetragona clavipes (Roubik, 1979). Breaking the tubercles of Par- 3.1. Internal nest environment tamona releases a stream of defending bees. Asian Tetragonula pagdeniformis (see Fig. E Within the closed nests of stingless bees, online only) possess rootlet-like resin struc- conditions tend to be relatively stable, but sub- tures on the external entrance, much like those ject to daily cycles. Ventilation has been stud- of Neotropical Tetragona dorsalis (Roubik, ied by Nogueira-Neto (1948) and more re- 1979), whose function is unknown. The many cently by Moritz and Crewe (1988, see Fig. H hanging rootlet-like structures surrounding the online only). Nests ‘breathe’ in the sense that nest entrances of T. corvina, T. spinipes, T. tidal gas exchange occurs frequently, although amazonensis and other aggressive, Neotropi- the entrance tube is the only connection to out- cal Trigona,andPtilotrigona (Camargo and side. Circulation is accomplished by workers Pedro, 2004; Fig. 1) may also provide posi- that fan their wings while facing outward to- tions for defenders. Although the outer nest ward the entrance. Variation in the number of layers and blind tubes have been discussed as nest entrances (some Plebeia and other gen- sites for trash deposit (Rau, in Nogueira-Neto, era have two or three separate, yet very proxi- 1948) and insulation (Drumond et al., 1995), mate, entrance holes) were shown to allow air their primary known function relates to de- to exit from one hole and enter in another, by fense. the use of smoke experiments (Nogueira-Neto, 1948). However, air is drawn into the nest and circulates, depending on physical properties of 2.6. Group protection the nest, the entire living colony, and the cav- ity, to exit at intervals. Such ‘tidal volumes’ Aggregations of colonies occur on natural could be calculated for two African stingless and artificial substrates, including building or bees, one nesting in the ground and one in a hut walls and roofs (Fig. 2). Natural substrates tree cavity. Worker bee ventilation (wing fan- are cliffsides or dense branches. The most ning activity) exchanged the entire nest air in common animal-based substrates are termite 1–7 hours (Moritz and Crewe, 1988). nests – exposed, underground, or within a tree Both carbon dioxide narcosis and critically cavity. Camargo and Pedro (2003) list Synter- high temperatures (> 35.5 ◦C) were prob- mes, Nasutitermes, Amitermes, Constrictoter- lems for the African stingless bees studied by mes, and Termes as Neotropical hosts, and Moritz and Crewe (1988). In the extreme am- also the large mound of nesting debris sur- bient temperatures near the ground nest (see rounding a colony of attine ants. Such aggrega- Fig. H online only), tidal inflow could raise Meliponine nesting 133 the nest temperature to a fatal level, thus ven- area (usually 2 to 5 in number) and a labyrinth tilation was diminished at the highest ambi- of openings and passageways surrounding the ent temperatures, maintaining the cooler air brood (see Fig. K online only). The involu- within the nest cavity. Oxygen level thereby cral sheaths may be significant, therefore, in decreased, and CO2 increased during the day, preventing direct access to the brood, and the thus CO2 was reduced by bee fanning only at open brood cells in particular, by parasites night. Although the change in nest temperature such as phorid (Pseudohypocera), stratiomyid in the shaded tree cavity was minimal, both (Hermetia illucens), and other flies, ants, or the tree cavity and ground nest displayed a robber stingless bees (Lestrimelitta and Clep- temperature gradient. Lethal nest temperatures totrigona), and possibly the lesser wax moth were recorded at 46 ◦CforTetragonula car- Achroia grisella (Cepeda-Aponte et al., 2002). bonaria (Amano, 2005) and 41 ◦CforScap- totrigona postica (Macieiera and Proni, 2004). 3.3. Diverse behavior, 3.2. Brood and involucrum areas materials and hygiene

The brood area forms the thermal core Fanning during night or day should be influ- of a stingless bee nest, where heat may be enced by colony honey production (Nogueira- kept in (or out) by concentric involucra. It Neto, 1948). The fact that stingless bees use has long been speculated that the involu- nectars that average about 65% water, then crum layers surrounding the brood permit heat convert this to honey of 30% water (Roubik, to be retained there (reviews by Nogueira- 1989; Roubik et al., 1995) means that mois- Neto, 1948; Kerr et al., 1967). Circumstantial ture must be removed from the nest cavity. The evidence indicates that Melipona may build large batumen plates having many air chan- more involucrum (see Fig. G online only) nels, made by Melipona and some Plebeia in cooler climates than in equatorial forests (Nogueira-Neto, 1948; Roubik, 1979, pers. (Engels et al., 1995); however, a colony that obs.) seem ideal for the purpose of water loss. is starved will build less involucrum (Kolmes However, as mentioned above, CO2 loss may and Sommeijer, 1992). Work with hives of also be significant, and other nest entrance fea- Melipona (Roubik and Peralta, 1983) showed tures involving surface area and openings de- that two species, each with an involucrum, termine available fanning positions for bees. actively and/or passively (via nest architec- Water is often carried by worker bees (im- ture) controlled the nest temperature within bibed) and dumped from the nest entrance the brood area. Recent study with Tetragonisca area, sometimes leaving wet marks near the weyrauchi (Cortopassi-Laurino and Nogueira- nesting cavities (see Fig. H online only). Apart Neto, 2003) showed similar dynamics, with from this, latrines are maintained within nests, the addition of an architectural innovation, a where several symbionts live (Sect. 4.5). ‘respiracle’ or facultative opening on top of Drainage outlets are maintained in the the nest cavity. Because brood remained over nests of subterranean stingless bees, such 31 ◦C, well above ambient temperature in the as Meliponula and Plebeina, and in tree- shade, heat from the bodies of the bees, es- nesting species including Trigona and Tetrag- pecially adults between the brood combs, is ona, plus exclusively ground-nesting Geotrig- likely responsible for heating the brood area. ona (Portugal-Araújo, 1955; Sakagami, 1982; ‘Social thermoregulation’ may or may not be Camargo and Wittmann, 1989; Camargo and required, in general, because nest temperatures Roubik, 1991; summary in Camargo and are not precisely controlled and bees are seem- Moure, 1996). The nesting cavities are not ingly more tolerant to brief chilling, at least constructed by the bees, are often left by in some genera (Engels et al., 1995; Drumond failed Atta colonies in the Neotropics or ter- et al., 1995). mites in Africa, and are modified so that water The involucrum is also a barrier, with drier can be ejected. Nesting by some subterranean cerumen leaves or sheaths outside of the brood colonies takes place just above a soil horizon 134 D.W. Roubik of very well drained material (see Fig. F on- Sakagami, 1982; Koedam et al., 2002). Differ- line only) thus nest drainage from rain or water ent stingless bee waxes have different chemi- from ripening of honey should pose no special cal properties, and are much simpler than wax problem (Camargo and Wittmann, 1989). of Apis (Blomquist et al., 1985). Cerumen, The insulation provided by wood and resin, the product of plant resin mixed with wax earth, stone, or other nest substrates, make and employed exclusively by meliponines, re- it unlikely that colonies overheat, provided mains soft for an extended time and is more nests are not in full sunlight and not too pliable than beeswax – that of Apis mellifera many bees engage in fanning during extremely (Hepburn and Kurstjens, 1984). In addition to high ambient temperatures. As demonstrated being used for constructing nest forms, ceru- by Moritz and Crewe (1988) tidal air flow may menmaybetakentomakeanemergencyre- cause hot external air to enter the nest. Com- pair of natural enemy damage. pared to resin, wax is much more rigid and Cerumen is normally made freshly to con- four times stronger, especially at temperatures struct brood cells, involucrum, nest entrance higher than 35 ◦C (Hepburn and Kurstjens, tubes, or storage pots. The wax is taken 1984), yet stingless bee cerumen has a higher from a pure wax deposit and combined with melting temperature (Buchwald et al., 2005). resin taken from a pure resin deposit (see No comparative study has been made on Fig. K online only). These may be in sev- relative amounts of resin and wax used in eral positions near the nest entrance and brood cerumen of different stingless bees. Small Hy- cells; workers mix the materials with their potrigona, Trigonisca, Schwarzula and Ple- mandibles (Michener, 1974; Sakagami, 1982). beia use very little resin, using almost pure In response to drastic nest alteration, such as wax (Sakagami, 1982; Blomquist et al., 1985; opening of the nest, bees respond by seek- Drumond et al., 1995; Camargo and Pedro, ing and collecting more resin and, in genera 2002a). Such an adaptive response by small such as Plebeia, Melipona, Cephalotrigona, stingless bees nesting in slender stems and and Partamona, mud is deposited directly on exposed to high temperatures would be ex- the edges of the opening (always interspersed pected from the thermal conditions, as would with resin), which is then gradually closed, a loose nest element architecture and large by working toward the middle. I briefly ex- cavities, which allow adult movement as heat perimented with a nest of Trigona nigerrima, sources, or migration. Daily dynamics of air which is one of the three Trigona that, like cer- temperature have not been measured among tain wasps, construct paper nests from chewed the outer nest batumen layers in the large, ex- wood pulp (Roubik, 1989). A 5 cm square posed nests, although temperature measure- of the nest surface was removed during the ments (Zucchi and Sakagami, 1972; Wille and evening. The following morning the nest had Orozco, 1975; Roubik and Peralta, 1983) and been repaired, without incoming material. direct observation of incoming foragers re- When a nest is severely damaged, colonies veal no use of water droplets to cool nests cannot fly with their queen to a new nest- (Moritz and Crewe, 1988; Engels et al., 1995; ing site, but a queen deprived of food did Nogueira-Neto, 1997). When water is col- fly to an empty hive box in T. laeviceps lected by workers, it is likely to be used for in Sumatra (Inoue et al., 1984). Abandoned honey dilution. intact brood comb with males of Melipona Nest repairs incorporate available nesting fulva present was an indication of abscond- material. Workers do essentially all the work, ing (Roubik, 1979). Melipona and presumably even though males occasionally perform su- other stingless bees aggregate on nearby tree perficially similar (i.e. irregular) maintenance trunks when their nest is destroyed. Whether activity (Velthuis et al., 2005). Workers make they can survive to establish a new nest, using wax that is secreted from dorsal glands, but a flying virgin queen, or merge with another some queens or males also make a small quan- colony after such occurrences, is unknown. tity; the wax is first placed on a wax deposit in However, a mixed colony nesting association the nest (Cruz-Landim, 1967; Michener, 1974; has been documented for Melipona panamica Meliponine nesting 135 and M. fuliginosa (Roubik, 1981) and has been tic fungi or bacteria seem normal, and some encountered in the field a second time since nest associates seem to have become semi- that report. The largest stingless bee, the latter domesticated. Considering the nest site, nest- species, makes a nest that is occupied secon- ing in an active termite or ant nest is obligate, darily by the smaller species, whose workers yet rare, among stingless bees, although the feed it nectar outside the nest entrance when use of cavities left by termite or ant colonies is returning from the field. Ultimately, as in para- also known (Tab. I). Nest construction in aban- sitic Bombus (Goulson, 2003) the nest may be doned bird nests is documented for Partamona usurped by the newcomer species. Melipona musarum and P. helleri (Camargo and Pedro, are keenly interested in returning to a damaged 2003). nest and collect resin from resin deposits, and Although no exchange of material oc- also cerumen and honey, as do many stingless curs, the ‘host’ ant or termite colonies of- bee genera. ten do not obtain or share protection from Bees eject water, as explained above, but stingless bee colonies. Aparatrigona, Scaura, are far more regularly seen ejecting a bolus Nannotrigona mellaria and some Trigona of trash, carried in the mandibles. This ac- (mazucatoi, cilipes), Paratrigona pannosa tivity may occur daylong, or primarily in the (Dejean and Roubik, pers. obs.) and Sun- afternoon. A few genera, like Lestrimelitta, datrigona moorei (Sakagami et al., 1989) Hypotrigona and Trigonisca (pers. obs.) drop are parasites in terms of lodging and de- the bolus from the nest entrance, while most, fense. The bees have no aggressive de- like Melipona, fly to drop trash meters from fense but use the nests of pugnacious Nasu- the nest (Kerr and Kerr, 1999). Trash balls titermes, Dolichoderus, Azteca (Kerr et al., are mainly meconia (larva defecations) on cell 1967), Epipona (Rasmussen, 2004), Pachy- bases. Adult defecations in the nest are gath- condyla goeldii (Dejean and Roubik, pers. ered at small latrines; most are consumed by obs.), and Crematogaster, respectively (further mutualist organisms (Sect. 4.6). The cerumen references in Roubik, 1989). In contrast, Par- coat is immediately removed from a newly tamona and most Trigona are aggressive and spun pupal cocoon (Michener, 1974). associate with a variety of hosts. Even birds may derive benefits from aggressive Trigona 4. NESTING ASSOCIATES colonies near their nests (Smith, 1968). In- deed, Stierlin and I observed Sarcoramphus 4.1. Biological nest requirements papa in lowland northern Bolivia, nesting in Stingless bees carefully select where to the crown of a tree, near a nest of highly ag- build nests, often within a living woody plant. gressive Trigona amazonensis. In each case, There are thus always associated organisms, parasitic flies are possibly kept out of the bird which occur there or in the immediate environ- nests by aggressive bees. ment. In addition, no thorough review of or- ganisms associated with a stingless bee nest is 4.3. Microbes possible, because taxonomic names are often lacking and studies are far from complete in Bacillus of several species, most the same natural habitats (Kistner, 1982; Roubik, 1989; as those found in nests of honey bees, Eickwort, 1990; Nogueira-Neto, 1997). An ex- Apis mellifera, occur in the stored pollen ception is in the extraordinary series of nest- or brood provisions. These include Bacillis ing associations reported in Brazil by Camargo megaterium, B. circulans and B. alvei, which and Pedro (see 2002, 2003, 2004). produce enzymes that may facilitate stor- age and / or digestion, plus secrete antibiotics 4.2. Collaborators, parasites and fatty acids (Gilliam et al., 1990). The or commensals? yeasts Candida (Camargo and Pedro, 2004) and Starmerella meliponinorum also are mu- Living within stingless bee nests, the tualists in bee nests (Teixeira et al., 2003). mites, collembolans, leiodid beetles, mutualis- Camargo and Pedro found yeast covering 136 D.W. Roubik stored pollen of Ptilotrigona lurida, which de- (Roubik, Stierlin, Harrison, Kondo, pers. obs.) hydrated and preserved the pollen, also po- receive wax bugs Cryptostigma (Coccidae: tentially supplying carbohydrates to bees, and Hemiptera) as coinhabitants of their nests, likely making the nest less attractive to the which presumably exist only because they are main natural enemies, phorid flies. protected by the stingless bees, and provide valuable wax and sugar in return (see Fig. 3). 4.4. Non-floral plant mutualisms? Such coccids, which feed on plant sap, also Many stingless bee associates are trees, live with ants, to which they give sugar secre- which of course provide both food and nest tions in exchange for protection. Intricacies of sites. At present, we do not know whether cohabitation may ultimately involve cavity uti- ff there are plants which attract stingless bees lization by di erent organisms, which evolve for nesting due to pollination benefits. The complex interdependencies. gathering of floral resins for nest material The leiodid beetles, or scotocryptines has been used at least by two tropical plant Scotocryptus, Scotocryptodes, Synaristus, genera as a basis for pollinator attraction Parabystus (Roubik and Wheeler, 1982; Peck, (Armbruster, 1984). However, whereas studies 2003; Fig. K online only) live in nests of in relatively species-poor dry tropical forests Neotropical genera, primarily Melipona, and show that only a few tree species are used also Cephalotrigona and Partamona. Beetle by the stingless bee fauna (Moritz and Crewe, adults are blind and flightless; the males and 1988; Camargo and Pedro, 2002a; Antonini females, often a few dozen, live among the and Martins, 2004; Martins et al., 2004), most pollen fecal debris and consume that resource studies document use of many families and (Peruquetti and Dias Bezerra, 2003), fungi or genera (Hubbell and Johnson, 1977; Johnson slime molds (which also consume fungi) in and Hubbell, l986; Oliveira et al., 1995; Eltz wet parts of the nest (Roubik and Wheeler, et al., 2002, 2003; Kajobe and Roubik, un- 1982). Dispersal of beetles occurs on hindlegs published data), with apparent exception in a of Melipona (Nogueira-Neto, 1949). Adult hyperdiverse Asian forest (Samehima et al., beetles have a special mandibular notch that 2004). Among strangler figs and their host secures their ‘ride’ holding on the worker trees, a disproportionate abundance of sting- bee corbicular hairs, and transfer between less bee nests occur (Cameron et al., 2004; nests occurs at muddy flats where bees collect Roubik and Harrison, pers. obs.). Potential nesting material (Roubik and Wheeler, 1982). pollination benefit to the figs is not possible, Documented residents in stingless bee nests and for the other trees would be fortuitous. also include ricinuleids, very slow-moving Some resins used by meliponines carry arachnids, Cryptocellus gamboa (Platnick, small seeds from fruit of Coussapoa asperi- pers. comm.; see Platnick and Shadab, 1981) folia (Cecropiaceae, see Garcia et al., 1992), in the hypogeous nests of Trigona fulviven- such as those embedded in the mud and resin tris in Panamanian rain forest (pers. obs.). batumen block of Melipona. Such seeds were Pseudoscorpions, Dasychernes, were abun- previously confused (Roubik, 1989) with Vis- dant in the nest of another Melipona in mia (Clusiaceae). Trigona carbonaria collects Colombia (Salt, in Kistner, 1982). Cyphoderid resin with the seeds of Eucalyptus torelliana collembolans Paracyphoderus, Cyphorderus (Wallace and Trueman, 1995). The importance and Pseudocyphoderus are common in nests of of seeds in nest construction is unclear, but Melipona and Partamona. These fungus feed- the seeds of both plants (Coussapoa is a hemi- ers, like leiodid beetles, have morphology sug- epiphyte) germinate on the outside of the bee gesting persistent associations with the bees nests (pers. obs.). (Kistner, 1982). They are tough and can hide or tuck away their appendages. 4.5. Mutualist inquilines Many mite genera occur in stingless bee nests and eat fungi – Neotydeolus, Schwarzula coccidophila (Camargo and Macrocheles, Tyrophagus, Trigonholaspis and Pedro, 2002a, b) and Schwarzula timida Hemileius, while others, apparently less Meliponine nesting 137 numerous, feed on pollen, such as Pye- 5. COLONIAL COMMUNITIES motes, Lasioseius, Glycyphagus, Neocypho- laelaps and Tyroglyphus (Delfinado-Baket 5.1. Reproduction and nesting et al., 1984; Baker and Delfinado-Baker, 1985; summaries in Eickwort, 1990; Nogueira-Neto, The relative numbers and positions of 1997). The predaceous laelapid mite Neohy- colonies within an area have perforce shaped poaspis ampliseta feeds on astigmatid mites the evolution of stingless bees. Virgin queens in stingless bee nests (Delfinado-Baker et al., accompany swarms of workers to new nest 1983). Michiliid flies (Melo, 1996) also con- sites, and males wait there in anticipation (re- sume fecal debris in nests of at least one views in Nogueira-Neto, 1997; Velthuis et al., Melipona. 2005) – clearly indicating the queen odors are dispersed from the nest. Afterwards, the new 4.6. True parasites and predators queen flies out for a single mating, pursued by Considering Diptera, the internal and nest hundreds of males (Peters et al., 1999; Palmer parasites of meliponines include three gen- et al., 2002). The queen may be killed, or in- era of Phoridae, Pseudohypocera, and internal deed, several queens are killed by predators adult bee parasites, Apocephalus and Melalon- (Michener, 1961; Paxton et al., 2003) on such cha (Brown, 1997). Those flies, the first in mating attempts. Therefore, reproductive bi- particular among the worst enemies of the ology of stingless bees includes the connec- Neotropical fauna, are completely absent (as tion for food, and potentially for new vir- bee natural enemies) in the Old World. They gin queens, between the mother and daughter mate hovering in copula near the nest en- colony. The relationship has been documented trance, then invade the nest and lay their eggs to last up to six months (Wille and Orozco, in all crevices or small spaces (Sect. 3.2). 1975; Sakagami et al., 1983; Drumond et al., Evidently parasitic mites can infest larvae of 1995). Melipona, Meliponula and Trigona, and in- The mean ‘nearest neighbor’ distance be- clude Meliponaspis, Hypoaspis and Trigonho- tween conspecific colonies nesting in nature laspis (review by Kistner, 1982). may be on the order of 50 to a few hundred me- The largest predators of stingless bee ters (Hubbell and Johnson, 1977; Breed et al., nests are the mustelids, bears and primates, 1999; Samejima et al., 2004). Cameron et al. with anteaters Tamandua, Myrmecophaga,and (2004) estimated that 132 colonies with males armidillos (and other, less fearsome omni- participated in a mating, by analysis of mi- crosatellite DNA markers. At a nest density vores, such as procyonids or coatimundis Na- −1 sua, civets Civerridae, and opossums Didel- of 3 ha (the species studied, T. collina,has phidae), all of which are opportunistic preda- aggregated nests) colony reproductive ecology tors of stingless bee colonies. Mustelids are potentially included all colonies in 50 ha. major colony enemies in the Neotropics (Eira barbara)andConepatus hog-nosed skunks, 5.2. The cost of stability while in savanna-dominated Africa, honey badgers (Mellivora capensis) and their mutu- Bee diseases are more frequent and well- alist birds, Indicator, are deft colony preda- known in honey bees than in stingless bees tors. Bears – Tremarctos, Helarctos, Ursus,are (Nogueira-Neto, 1997; Morse, 1994), which significant predators in Andean South Amer- implies that meliponines, in contrast to trop- ica and SE Asia (Roubik, 1989). African rain ical Apis (Akratanakul, 1986), do not expe- forests have primates as principal bee colony rience strong selection to regularly change predators - chimps, gorillas and baboons (Pan, nesting sites, in order to shed their par- Gorilla, Langur) but the honey badger is al- asite load. Further, a sustained connection most absent in dense forest. Australia lacks between mother and daughter colony pro- any significant stingless bee nest predator, as vides evolutionary pathways for parasitism do Madagascar and some large islands with and, ultimately, cleptoparasitism. Cleptopara- stingless bees, such as Taiwan and Philippines. sitism evolved independently in Neotropical 138 D.W. Roubik

Lestrimelitta and African Cleptotrigona cubi- adult bees (Batista et al., 2003; Eltz et al., ceps. Phylogenetic origins of these taxa are 2003; Kajobe and Roubik, 2006). Individual now being clarified. Some Oxytrigona attack species may have several hundred nests in a other colonies and use their nests (Nogueira- few hectares, but those are very small colonies. Neto, 1997), as does Tetragonisca angustula An estimate of 2 to 6 colonies ha−1 seems to (Sakagami et al., 1993; pers. obs.). apply to most larger or detectable colonies. Nest dispersion, within a species, may Such resources for honey exploitation should be due to competition and anticipates uni- be comparable to roughly one colony of Apis form distribution among aggressive foraging mellifera per hectare, 10 times the nesting den- species (Hubbell and Johnson, 1977; Breed sity estimated for A. mellifera in tropical habi- et al., 1999) – provided suitable nesting sites tats (Kajobe and Roubik, 2006). are available. Colonies may battle over po- How often might stingless bee colonies tential nesting sites (Hubbell and Johnson, reproduce, either by swarming or by hav- 1977; Sakagami et al, 1993). Lestrimelitta reg- ing males fertilize queens? Remarkably, three ulate their colony densities by periodic con- studies done in Africa, America and Asia show tests (Sakagami et al., 1993), including pyrric annual mortality is 12 to 15% (Eltz et al., battles, in which the raid costs many robbers’ 2002; Kajobe and Roubik, 2006; Roubik and lives (Johnson, 1987, pers. obs.), or colony Harrison, pers. obs.). If and only if nests are takeover of host nests, in which the entire continuously occupied, a stable local colony host population is exterminated, but the rob- population with mortality of 13% means that bers sustain little loss (Sakagami et al., 1993, about 5% (.8722) of the original colonies are pers. obs.). These and other authors observed still living after 23 years. Thus, on average, a that raiding Lestrimelitta also draw Pseudo- stingless bee colony can pass on its genes by hypocera (phorid flies) to raided nests, which reproducing in approximately a dozen years. is against their interest – host nests are nor- mally raided as sustainable resources. ACKNOWLEDGEMENTS The stasis of stingless bee nesting commu- nities thus implies natural selection to reduce I thank J.M.F. Camargo, T. Eltz and C. Ras- vulnerability to other stingless bee colonies, mussen for helpful criticism, J.M.F. Camargo, S. as outlined above, and also to avoid conse- Pedro and R. Kajobe for illustrative material or data, quences of intense competition for food and J. Biesmeijer, C. Rasmussen and E. Stierlin for data, nests that can lead to usurpation of nest sites, and Wildlife Conservation Society for support in or cleptoparasitism. Bolivia, Liu Fanglin and the Chinese Academy of Sciences for support in Yunnan, and Biotropica for 6. COMMUNITY DYNAMICS permission to reprint Figure 3.

In natural vegetation, the stingless bee com- munity, in terms of active nests, may number Résumé – Biologie de la nidification des abeilles sans aiguillon. Par rapport au genre Apis,les approximately 150 colonies in a square kilo- abeilles sans aiguillon (Hymenoptera, Apidae, Me- meter (100 ha), and the known range is from liponini) sont des sources variées et uniques de 15 to 1500 colonies, but varies considerably in miel, avec 50 fois plus d’espèces et une origine qui biomass of colonies and bee size (Kajobe and remonte au Crétacé. Les reines s’accouplent une Roubik, 2006; Samehima et al., 2004; Breed fois, les ouvrières n’ont pas d’aiguillon, les mâles butinent, la cire n’est pas le matériau primaire pour et al., 1999; Nogueira-Neto, 1997). Slight la construction et l’eau n’est pas utilisée pour re- disturbance can change species composition froidir les nids. Bien qu’on ignore pour la plupart (Brown and Albrecht, 2001). Unnatural hu- la biologie de leur nidification, nous donnons ici man habitats have also yielded information on une vue générale sur l’architecture, la défense et la bee nest density (e.g. Michener, 1946; Morse, maintenance des nids, la reproduction de la colonie, les symbiotes, les ennemis naturels et les associa- 1994). There are often many more nests in tions animales dans le nid. La densité moyenne de sites that are not extensive, intact old for- colonies est de 150/km2 dans les habitats naturels est, but far fewer species, and possibly fewer mais la biomasse des colonies et la taille des abeilles Meliponine nesting 139

varie énormément. Il y a souvent plus de colonies Meliponini / abeille sans aiguillon / nidifica- dans les sites perturbés, par contre la richesse en es- tion / architecture nid / micro-climat / écologie pèces est bien moindre. de l’évolution Les prédateurs comprennent des invertébrés, prin- cipalement des fourmis, et des vertébrés dont les chimpanzés qui utilisent des outils et les humains, Zusammenfassung – Nistbiologie bei Stachello- ainsi que les ours, les mustélidés, les fourmiliers et sen Bienen. Im Vergleich zu den Honigbienen sind de nombreux opportunistes. Parmi les parasites on Stachellose Bienen sehr facettenreich und nutzen trouve des mouches de la famille des phoridés néo- einzigartige Honigquellen, sie stellen 50 mal mehr tropicales, quelques acariens mais peu de microbes Arten und entstanden bereits in der Kreidezeit. Die connus. Les symbiotes des nids incluent des aca- Königinnen paaren sich nur einmal, die Arbeite- riens fongivores, des coléoptères, des moisissures, rinnen haben keinen Stachel, die Männchen su- des collemboles dans les latrines de la colonie, des chen Futter, Wachs ist nicht das hauptsächliche coccidies qui fournissent de la cire et des acariens Baumaterial und Wasser wird nicht zur Kühlung nécrophages. Les champignons et les bactéries mu- des Nestes benutzt. Obwohl die Nistbiologie meist tualistes conservent la nourriture, fournissent des unbekannt ist, wird hier eine allgemeine Sicht nutriments et écartent les parasites. über Nestarchitektur, Verteidigung, Erhalt, Volks- Contrairement à Apis, les abeilles sans aiguillon vermehrung, Symbionten, natürliche Feinde und n’essaiment pas franchement (un nouveau site de Verhaltensmuster der Volksgemeinschaft gegeben. nidification doit d’abord être préparé) et elles Unter natürlichen Umweltbedingungen beträgt die n’abandonnent pas leur nid. La reine n’effectue plus durchschnittliche Nestdichte 150/km2,aberesle- de vol une fois fécondée et les colonies ont appa- ben dort verglichen mit veränderten Lebensräumen remment une longue vie. L’adaptation est très vi- nur 1 % der Völker. In diesen gestörten Regionen sible dans les tubes d’entrée des nids, dans les plate- gibt es zwar eine geringere Artenzahl, die aber un- formes propres aux espèces pour la défense du nid, terschiedliche Biomasse aufweisen. dans le butinage et la ventilation. Les ouvrières ven- Feinde setzen sich aus Wirbellosen, vor al- tilent avec leurs ailes et créent un courant d’air avec lem Ameisen, und Wirbeltieren zusammen, ein- « des marées » qui renouvellent l’air du nid. Aux schließlich werkzeugbenutzenden Schimpansen, températures élevées, une moindre ventilation aide Menschen, Bären, Mardern, Ameisenbären und à maintenir une température fraîche dans le nid, vielen Opportunisten. Als Parasiten kommen neo- mais le CO2 augmente et est évacué la nuit. L’ar- tropische Buckelfliegen, einige Milben, aber nur chitecture est variable, en fonction de l’âge, du gé- wenige bekannte Mikroben vor. Als Symbion- notype et du microenvironnement, y compris les en- ten kommen pilzverzehrende Milben und Käfer nemis naturels. Les grands genres comme Trigona, vor; in den Volkslatrinen gibt es Schimmelpilze Melipona et Plebleia ont une variabilité interspéci- und Springschwänze, im Nest Wachs erzeugende fique considérable en ce qui concerne les sites de ni- Schildläuse und Unrat vertilgende Milben. Mutuel- dification, l’architecture et le comportement de dé- le Pilze und Bakterien konservieren Futter, stellen fense, souvent lié à la vulnérabilité du nid. Le genre Nährstoffe bereit und schalten Parasiten aus. Trigona fabrique avec ses excréments une plaque, Im Gegensatz zu Honigbienen bilden Stachellose sorte de bouclier, qui lui procure défense et isola- Bienen keine freien Schwärme und verlassen ihre tion, comme c’est le cas avec la terre, le bois, la Nester nicht. Die Königin fliegt nach Beginn der résine ou les pierres pour les espèces qui nidifient Eiablage nicht mehr. Ein neuer Nistplatz muss erst dans le sol ou dans des cavités d’arbres. Une fine vorbereitet werden und Völker sind anscheinend couche de surface sur les nids exposés permet en langlebig. Besondere Anpassungen sind in den cas de rupture la sortie des abeilles qui défendent Röhren am Nesteingang zu erkennen, die artspezi- le nid et se mettent à mordre. On ne comprend pas fische Plattformen für die Nestverteidigung, Sam- actuellement le niveau d’évolution ni la phyloge- melflüge und Ventilation darstellen. Arbeiterinnen nèse du comportement de nidification. La disposi- schlagen die Flügel und erzeugen einen “Gezeiten” tion des cellules de couvain en chaînes reliées ou en – Luftstrom, der die Luft im Nest erneuert. Bei ho- amas ne semble pas liée particulièrement à la pe- hen Temperaturen hilft vermindertes Fächeln eine tite taille des abeilles. Les abeilles choisissent soi- kühlere Temperatur beizubehalten, aber der Gehalt gneusement leur mode de nidification et font preuve an CO2 steigt dann an und kann erst nachts entfernt ainsi d’une adaptation particulière pour minimiser werden. Die Architektur ist unterschiedlich, abhän- la vulnérabilité de la colonie aux ennemis naturels, gig möglicherweise vom Alter, Genotyp und der à la compétition intraspécifique et à la cleptobiose. die natürlichen Feinde einschliessenden Mikroum- Elles conservent des liens durables entre la colo- welt. Große Arten wie Trigona, Melipona und Ple- nie mère et les colonies filles pour ce qui est de la beia zeigen beachtliche innerartliche Varianzen in nourriture et des reines vierges. Les reines ne s’ac- Lage und Architektur des Nestes und im Vertei- couplent qu’une fois et la mortalité de la colonie est digungsverhalten, das mit der Verletzlichkeit des de 13 % par an ; on peut donc prévoir une longévité Nestes zusammenhängt. Trigona formt mit ihren de la colonie de 24 ans. Exkrementen eine Deckplatte, die für Schutz und 140 D.W. Roubik

Isolation sorgt, ähnlich wie Erde, Holz oder Steine Trigonisca group (Apidae: Meliponinae), Comp. bei anderen Arten, die in Erd- oder Baumhöhlen ni- Biochem. Physiol. 82, 137–142. sten. Eine schwache Oberflächenschicht bei freilie- Breed M.D., McGlynn T.P., Sanctuary M.D., Stocker genden Nestern ermöglicht den Austritt von vertei- E.M., Cruz E. (1999) Distribution and abundance digenden, beißenden Bienen sowie diese zerbricht. of selected stingless bee colonies in a Costa Rican Zur Zeit ist das Niveau der Evolution und die Phy- tropical wet forest, J. Trop. Ecol. 16, 765–777. logenie des Nistverhaltens noch nicht verstanden. Brown B.V. (1997) Parasitic phorid flies: a previously Die Anordnung der Brutzellen in Ketten oder Grup- unrecognized cost to aggregation behavior of male pen scheint vor allem mit den kleinen Köpergrö- stingless bees, Biotropica 29, 370–372. ßen der Bienen zusammenzuhängen. Bienen suchen ff sich sorgfältig die Lage ihres Nestes aus und sind Brown J.C., Albrecht C. (2001) The e ect of besonders angepasst, die Verletzlichkeit des Volkes tropical deforestation on stingless bees of the gegen natürliche Feinde, innerartliche Konkurrenz genus Melipona (Insecta: Hymenoptera: Apidae: und Räuberei zu minimieren. Sie halten in Bezug Meliponini) in central Rondonia, Brazil, J. auf Nahrung und unbegattete Königinnen dauerhaft Biogeogr. 28, 623–634. Verbindungen zwischen Mutter- und Tochterkolo- Buchwald R., Greenberg A.R., Breed M.D. (2005) nien. Königinnen paaren sich nur einmal und die A biomechanical perspective on beeswax, Am. Volkssterblichkeit beträgt 13 % y−1. Demnach be- Entomol. 51, 39–41. rechnet sich die Überlebensdauer einer Kolonie auf Camargo J.M.F. (1970) Ninhos e biologia de algumas 12 Jahre. especies de meliponideos (Hymenoptera: Apidae) da região de Porto Velho, Territorio de Rondônia, Meliponini / Apidae / Nestarchitektur / Nestmi- Brasil, Rev. Biol. Trop. 16, 207–239. kroklima / evolutionäre Ökologie Camargo J.M.F. (1984) Notas sobre habitos de ni- dificação de Scaura (Scaura) latitarsis (Friese) (Hymenoptera, Apidae, Meliponinae), Bol. Mus. Paraense E. Goeldi. 1, 89–95. REFERENCES Camargo J.M.F., Wittmann D. (1989) Nest architec- ture and distribution of the primitive stingless Akratanakul P. (1986) Beekeeping in Asia, F.A.O. bee, Mourella caerulea (Hymenoptera, Apidae, Agric. Serv. Bull 68/4, Rome. Meliponinae): evidence of the origin of Plebeia (s. Amano K. (2005) Attempts to introduce stingless bees lat.) on the Gondwana continent, Stud. Neotropic. for the pollination of crops in green-house con- Fauna Environ. 4, 213–229. ditions in Japan, Food and Fertilizer Technology Camargo J.M.F., Roubik D.W. (1991) Systematics and Center, Taipei, available at: http://www.fftc.agnet. / / / bionomics of the apoid obligate necrophages: the org library article tb167.html (accessed on 23 Trigona hypogea group (Hymenoptera: Apidae; January 2006). Meliponinae), Biol. J. Linn. Soc. 44, 13–39. Antonini J., Martins R.P. (2004) The value of a tree Camargo J.M.F., Pedro S.R.M. (l992) Systematics, species (Caryocar brasiliense) for a stingless bee phylogeny and biogeography of the Meliponinae Melipona quadrifasciata quadrifasciata, J. Insect (Hymenoptera, Apidae): a mini-review, Conserv. 7, 1671–1674. Apidologie 23, 509–522. Armbruster W.S. (1984) The role of resin in an- Camargo J.M.F., Moure J.S. (1996) Meliponini giosperm pollination: ecological and chemical neotropicais: o gênero Geotrigona Moure, 1943 considerations, Am. J. Bot. 71, 1149–1160. (Apinae, Apidae, Hymenoptera), com especial Baker E.W., Delfinado-Baker M. (1985) An un- referência à filogenia e biogeografia, Arq. Zool. usual new species of Neocypholaelaps (Acari: São Paulo 33, 71–161. Ameroseiidae) from the nests of stingless bees Camargo J.M.F., Pedro S.R.M. (2002a) Mutualistic as- (Apidae: Meliponinae), Int. J. Acarol. 11, 227– sociation between a tiny Amazonian stingless bee 232. and a wax-producing scale insect, Biotropica 34, Batista M.A., Ramalho M., Soares A.E.E. (2003) 446–451. Nesting sites and abundance of Meliponini Camargo J.M.F., Pedro S.R.M. (2002b) Uma especie (Hymenoptera: Apidae) in heterogeneous habitats nova de Schwarzula da Amazonia, Iheringia, Ser. of the Atlantic rain forest, Bahia, Brazil. Lundiana Zool. 92, 101–112. 4, 19–23. Camargo J.M.F., Pedro S.R.M. (2003) Meliponini Biesmeijer J.C., Giurfa M., Koedam D., Potts S.G., neotropicais: o genero Partamona Schwarz, 1939 Joel D.M., Dafni A. (2005) Convergent evolu- (Hymenoptera, Apidae, Apinae) – bionomia e bio- tion: floral guides, stingless bee nest entrances, geografia, Rev. Bras. Entomol. 47, 311–372. and insectivorous pitchers, Naturwissenschaften, Camargo J.M.F., Pedro S.R.M. (2004) Meliponini 92, 444–450. neotropicais: o genero Ptilotrigona Moure Blomquist G.J., Roubik D.W., Buchmann S.L. (1985) (Hymenoptera, Apidae, Apinae), Rev. Bras. Wax chemistry of two stingless bees of the Entomol. 48, 353–377. Meliponine nesting 141

Camargo J.M.F., Roubik D.W. (2005) Neotropical Engels W., Rosenkranz P., Engels E. (1995) Meliponini: Paratrigonoides mayri,new Thermoregulation in the nest of the Neotropical genus and species from western Colombia stingless bee Scaptotrigona postica and a hypoth- (Hymenoptera, Apidae, Apinae) and phylogeny esis on the evolution of temperature homeostasis of related groups, Zootaxa 1081, 33–45. in highly eusocial bees, Stud. Neotrop. Fauna Cameron E.C., Franck P., Oldroyd B.P. (2004) Genetic Environ. 30, 193–205. structure of nest aggregations and drone congrega- Franck P., Cameron E., Good G., Rasplus J.-Y., tions of the southeast Asian stingless bee Trigona Oldroyd B.P. (2004) Nest architecture and genetic collina, Mol. Ecol. 13, 2357–2364. differentiation in a species complex of Australian Cepeda-Aponte O.I., Imperatriz-Fonseca V.L., stingless bees, Mol. Ecol. 13, 2317–2331. Velthuis H.H.W. (2002) Lesser wax moth Achroia Garcia M.V.B., Oliveira M.L., Campos L.A.O. (1992) grisella: first report for stingless bees and new Use of seeds of Coussapoa asperifolia mag- capture method, J. Apic. Res. 41, 107–108. nifolia (Cecropiaceae) by stingless bees in the Cortopassi-Laurino M., Nogueira-Neto P. (2003) central Amazonian forest (Hymenoptera: Apidae: Notas sobre a bionomia de Tetragonisca Meliponinae), Entomol. Gen. 17, 255–258. weyrauchi Schwarz, 1943 (Apidae, Meliponini), Gilliam M., Roubik D.W., Lorenz B.J. (1990) Acta Amaz. 33, 643–650. Microorganisms associated with pollen, honey, Cruz-Landim C. da C. (1967) Estudo comparativo and brood provisions in the nest of a stingless bee, de algumas glândulas das abelhas (Hymenoptera, Melipona fasciata, Apidologie 21, 89–97. Apoidea) e respectivas implicações evolutivas, Goulson D. (2003). Bumblebees: behavior and ecol- Arq. Zool. São Paulo, 15, 177–290. ogy, Oxford, UK. Darchen R. (1972) Éthologie comparative de Hansell M.H. (1993) The ecological impact of animal l’économie des matériaux de construction chez nests and burrows, Funct. Ecol. 7, 5–12. divers apids sociaux, Apis, Trigona et Melipona Hepburn H.R., Kurstjens S.P. (1984) On the strength of (Apidés), Rev. Comp. Anim. 6, 201–215. propolis (bee glue), Naturwissenschaften 71, 591– Delfinado-Baker M., Baker E.W., Roubik D.W. (1983) 592. New genus and species of Hypoaspidinae (Acari: Hubbell S.P., Johnson L.K. (1977) Competition and Laelapidae) from nests of stingless bees, Int. J. nest spacing in a tropical stingless bee community, Acarol. 9, 195–203. Ecology 58, 949–963. Delfinado-Baker M., Baker E.W., Flechtmann Inoue T., Sakagami S.F., Salmah S., Nukmal N. (1984) C.H.W. (1984) Acari Domum Meliponinarum Discovery of successful absconding in the sting- Brasiliensium Halitontes. 5. Two new genera and less bee Trigona (Tetragonula) laeviceps,J.Apic. species of Laelapidae (Mesostigmata: Acari) from Res. 23, 136–142. stingless bee nests, Int. J. Acarol. 10, 3–10. Johnson L.K. (1987) The pyrric victory of nest- Dollin A.E., Dollin L.J., Sakagami S.F. (1997) robbing bees: did they use the wrong pheromone? Australian stingless bees of the genus Trigona Biotropica 19, 188–189. (Hymenoptera: Apidae), Invertebr. Taxon. 11, 861–896. Johnson L.K., Hubbell S.P. (1986) Nest tree se- lectivity and density of stingless bee colonies Drumond P.M., Bego L.R., Melo G.A.R. (1995) in a Panamanian forest, in: Chadwick A.C., Nest architecture of the stingless bee Plebeia Sutton S.L. (Eds.), Tropical Rain-Forest: The poecilochroa Moure and Camargo, 1993 and Leeds Symposium, Leeds Phil. Soc., Leeds, UK, related considerations (Hymenoptera, Apidae, pp. 147–154. Meliponinae), Iheringia, Ser. Zool., Porto Alegre 79, 39–49. Kajobe R., Roubik D.W. (2006) Honey-making bee colony abundance and predation by apes and hu- Eardley C.D. (2004) Taxonomic revision of the mans in a Uganda forest reserve, Biotropica 38, African stingless bees (Apoidea: Apidae: Apinae: 210–218. Meliponini), African Plant Protection 10, 63–96. Kerr A.S., Kerr W.E. (1999) Melipona garbage bees Eickwort G.C. (1990) Associations of mites with so- release their cargo according to a Gaussian distri- cial insects, Annu. Rev. Entomol. 35, 469–488. bution, Rev. Bras. Biol. 59, 119–123. Eltz T., Bruhl C.A., Kaars S. van der, Linsenmair K.E. Kerr W.E., Sakagami S.F., Zucchi R., Portugal Araújo (2002) Determinants of stingless bee nest density V., Camargo J.M.F. (1967) Observações sobre a in lowland dipterocarp forests of Sabah, Malaysia, arquitetura dos ninhos e comportamento de al- Oecologia 131, 27–34. gumas especies de abelhas sem ferrão das viz- Eltz T., Bruhl C.A., Imiyabir Z., Linsenmair K.E. inhanças de Manaus, Amazonas (Hymenoptera, (2003) Nesting and nest trees of stingless bees Apoidea), Atlas do simpôsio sobre a biota (Apidae: Meliponini) in lowland dipterocarp Amazônica 5, 255–309. forests of Sabah, Malaysia, with implications for Kistner D.H. (1982) The social insects’ bestiary, in: forest management, For. Ecol. Manage. 172, 301– Hermann H.R. (Ed.), Social Insects, Vol. III, 313. Academic Press, New York, pp. 2–244. 142 D.W. Roubik

Koedam D., Jungnickel H., Tentschert J., Jones G.R., Nogueira-Neto P. (1949) Notas bionomicas sobre Morgan E.D. (2002) Production of wax by vir- meliponineos. II. Sobre a pilhagem. Papeis gin queens of the stingless bee Melipona bicolor Avulsos do depto. De Zoologia da Secr. Agr. Do (Apidae, Meliponinae), Insectes Soc. 49, 229– Est. De São Paulo, pp. 13–32. 233. Nogueira-Neto P. (1962) The scutellum nest structure Kolmes S.A., Sommeijer M.J. (1992) Ergonomics of Trigona (Trigona) spinipes Fab. (Hymenoptera: in stingles bees changes in intranidal behav- Apidae), J. N.Y. Entomol. Soc. 70, 239–264. ior after partial removal of storage pots and Nogueira-Neto P. (1970) A criaçao de abelhas sem honey in Melipona favosa (Hymenoptera: Apidae; ferrao (1st ed., 1953), Chacaras e Quintais, Sao Meliponinae), Insectes Soc. 39, 215–232. Paulo. Langenheim J. (2003) Plant resins. Chemistry, evolu- Nogueira-Neto P. (1997) Vida e criaçao de abelhas tion, ecology, ethnobotany, Timber Press, Portland indigenas sem ferrao, Editora Nogueirapis, Sao Oregon. Paulo. Lokvam J., Braddock J.F. (1999) Anti-bacterial func- Oliveira M.L., Morato E.F., Garcia M.V.B. (1995) tion in the sexually dimorphic pollinator rewards Diversidade de espécies e densidade de nin- of Clusia grandiflora (Clusiaceae), Oecologia hos de abelhas socias sem ferrão (Hymenoptera, 119, 534–540. Apidae, Meliponinae) em floresta de terra firma na Macieiera O.J.D., Proni E.D. (2004) Capacidade de Amazônia central, Rev. Bras. Biol. 12, 13–24. resistência a altas e baixas temperaturas em Palmer K.A., Oldroyd B.P., Quezada-Euan J.G., operárias de Scaptotrigona postica (Latreille) Paxton R., May-Itza W. de. J. (2002) Paternity fre- (Hymenoptera, Apidae) durante os períodos de quency and maternity of males in some stingless verão e inverno, Rev. Bras. Zool. 21, 293–296. bee species, Mol. Ecol. 11, 2107–2113. Martins C.F., Cortopassi-Laurino M., Koedam Paxton R.J., Bego L.R., Shah M.M., Mateus S. (2003) D., Imperatriz-Fonseca V.L. (2004) Tree Low mating frequency of queens in the stingless species used for nidification by stingless bee Scaptotrigona postica and worker paternity of bees in Brazilian Caatinga, Biota Neotropica males, Behav. Ecol. Sociobiol. 53, 174–181. / / v4n2 en BN00104022004. Peck S.B. (2003) The eyeless inquiline genera Melo G.A.R. (1996) Notes on the nesting biology Parabystus and Scotocryptus ofCostaRicaand of Melipona capixaba (Hymenoptera, Apidae), J. Panama; inhabitants of nests of stingless bees Kans. Entomol. Soc. 69, 207–210. (Coleoptera: Leiodidae), Sociobiology 42, 65–80. Michener C.D. (1946) Notes on the habits of Peruquetti R.C., Dias Bezerra J.M. (2003) Inquilinos some Panamanian stingless bees (Hymenoptera, de abelhas-sem-ferrão (Hymenoptera: Apidae): Apidae), J. N.Y. Entomol. Soc. 54, 179–197. aspectos da biologia de Scotocryptus meli- Michener C.D. (1959) Sibling species of Trigona from tophilus Reitter, 1881 (Coleoptera: Leiodidae), Angola (Hymenoptera, Apidae), Am. Mus. Novit. Entomotropica 18, 215–218. 1956, 1–5. Peters J., Queller D.C., Imperatriz-Fonseca V.L., Michener C.D. (1961) Observations on the nests and Roubik D.W., Strassmann J.E. (1999) Mate num- behavior of Trigona in Australia and New Guinea ber, kin selection and social conflicts in stingless (Hymenoptera, Apidae), Am. Mus. Novit. 2026, bees and honeybees, Proc. R. Soc. London B 266, 1–46. 379–384. Michener C.D. (1974) The social behavior of the bees: Platnick N.I., Shadab M.U. (1981) On Central a comparative study, Belknap, Harvard University American Cryptocellus (Arachnida, Ricinulei), Press, Cambridge. Am. Mus. Novit. 2711, 1–21. Michener C.D. (2000) Bees of the world, Johns Portugal-Araújo V. (1955) A contribution to the bio- Hopkins Press, Baltimore. nomics of Lestrimelitta cubiceps (Hymenoptera, Apidae), J. Kans. Entomol. Soc. 31, 203–211. Michener C.D. (2001) Comments on minute Meliponini and the male of the genus Pariotrigona Portugal-Araújo V. (1958) Notas sobre coloinas de (Hymenoptera: Apidae), J. Kans. Entomol. Soc. meliponineos de Angola, Dusenia 6, 97–114. 74, 231–236. Posey D.A., Camargo J.M.F. de (1985) Additional Moritz R.F.A., Crewe R.M. (1988) Air ventilation in notes on the classification and knowledge of sting- nests of two African stingless bees Trigona denoiti less bees (Meliponinae, Apidae, Hymenoptera) by and Trigona gribodoi, Experientia 44, 1024–1027. the Kayapó Indians of Gorotire, Pará, Brazil, Ann. Carnegie Mus. 54, 247–274. Morse R.A. (1994) The new complete guide to beekeeping, The Countryman Press, Woodstock, Rasmussen C. (2004) A stingless bee nesting with a Vermont. paper wasp (Hymenoptera: Apidae, Vespidae), J. Nogueira-Neto P. (1948) Notas bionomicas sobre Kans. Entomol. Soc. 77, 593–601. meliponineos. I. Sobre ventilação dos ninhos e as Roubik D.W. (1979) Nest and colony characteristics of constucões com ela relationadas, Rev. Bras. Biol. stingless bees from French Guiana (Hymenoptera: 8, 465–488. Apidae), J. Kans. Entomol. Soc. 52, 443–470. Meliponine nesting 143

Roubik D.W. (1981) A natural mixed colony limao (Hymenoptera: Apidae), Sociobiology 21, of Melipona (Hymenoptera: Apidae), J. Kans. 237–277. Entomol. Soc. 54, 263–268. Samejima H., Marzuki M., Nagamitsu T., Nakashizuka Roubik D.W. (1983) Nest and colony characteristics T. (2004) The effects of human disturbance on a of stingless bees from Panama, J. Kans. Entomol. stingless bee community in a tropical rainforest, J. Soc. 56, 327–355. Biol. Conserv. 120, 577–587. Roubik D.W. (1989) Ecology and natural history of Schwarz H.F. (1948) Stingless bees (Meliponidae) of tropical bees, Cambridge University Press, New the Western Hemisphere, Bull. Am. Mus. Nat. York. Hist. 90, 1–546. Roubik D.W. (1992) Stingless bees (Apidae: Smith B.H., Roubik D.W. (1983) Mandibular glands Meliponinae): a guide to Panamanian and of stingless bees (Hymenoptera: Apidae): chemi- Mesoamerican species and their nests, in: cal analysis of their contents and biological func- Quintero D., Aiello A. (Eds.), Insects of Panama tion in two species of Melipona,J.Chem.Ecol.9, and Mesoamerica, Oxford University Press, 1465–1472. Oxford, UK, pp. 495–524. Smith NG. (1968) The advantage of being parasitized, Roubik D.W. (1993) Direct costs of forest reproduc- Nature 219, 690–694. ffi tion, bee-cycling and the e ciency of pollination Starr C.K., Sakagami S.F. (1987) An extraordi- modes, J. Biosci. 18, 537–552. nary concentration of stingless bee colonies in Roubik D.W., Wheeler Q. (1982) Flightless beetles and the Philippines, with notes on nest architecture stingles bees: phoresy of scotocryptine beetles on (Hymenoptera: Apidae: Trigona spp.), Insectes their meliponine hosts, J. Kans. Entomol. Soc. 55, Soc. 34, 96–107. 125–135. Teixeira C.P., et al. (2003) Starmerella meliponino- Roubik D.W., Peralta F.A.P. (1983) Thermodynamics rum sp. nov., a novel ascomycetous yeast species in nests of two Melipona species in Brasil, Acta associated with stingless bees, Int. J. Syst. Ecol. Amaz. 13, 453–466. Microbiol. 53, 339–343. Roubik D.W. Moreno J.E., Vergara C., Wittmann Velthuis H.W., Koedam K., Imperatriz-Fonseca V. D. (1986) Sporadic food competition with the (2005) The males of Melipona and other stingless African honey bee: projected impact on neotrop- bees, and their mothers, Apidologie 36, 169–185. ical social bees, J. Trop. Ecol. 2, 97–111. Wallace H.M., Trueman S.J. (1995) Dispersal of Roubik D.W., Yanega D., Aluja-S. M., Buchmann S.L., Eucalyptus torelliana seeds by the resin-collecting Inouye D.W. (1995) On optimal nectar foraging stingless bee, Trigona carbonaria, Oecologia 104, by some tropical bees (Hymenoptera: Apidae), 12–16. Apidologie 26, 197–211. Wille A. (1983) Biology of the stingless bees, Annu. Roubik D.W., Sakai S., Hamid Karim A.A. (Eds.) Rev. Entomol. 28, 41–64. (2005) Pollination ecology and the rain forest: Wille A., Michener C.D. (1973) The nest architecture Sarawak Studies, Springer Ecological Studies No. of stingless bees with special reference to those 174, Springer Sciences + Business Media Inc., of Costa Rica (Hymenoptera: Apidae), Rev. Biol. New York. Trop. Suppl. 21, 9–278. Sakagami S.F. (1982) Stingless bees, in: Herman H.H. Wille A., Orozco E. (1975) Observations on the (Ed.), Social insects, Vol. III, Academic Press, founding of a new colony by Trigona cupira New York, pp. 361–423. (Hymenoptera: Apidae) in Costa Rica, Rev. Biol. Trop. 22, 253–287. Sakagami S.F., Yamane S., Hambali H.G. (1983a) Nests of some southeast Asian stingless bees, Wittmann D. (1989) Nest architecture, nest site pref- Bull. Fac Education, Ibaraki Univ. (Nat. Sci.) 32, erences and distribution of Plebeia wittmanni 1–21. (Moure and Camargo, 1989) in Rio Grande do Sul, Brazil (Apidae: Meliponinae), Stud. Neotrop. Sakagami S.F., Inoue T., Yamane S., Salmah S. Fauna Environ. 24, 17–23. (1983b) Nest architecture and colony compo- sition of the Sumatran stingless bee Trigona Wittmann D., Radtke R., Zeil J., Lubke G., Francke (Tetragonula) laeviceps, Kontyû 51, 100–111. W. (1990) Robber bees (Lestrimelitta limao)and their host chemical and visual cues in nest defense Sakagami S.F., Inoue T., Yamane S., Salmah S. by Trigona (Tetragonisca) angustula (Apidae: (1989) Nests of the myrmecophilous stingless bee, Meliponinae), J. Chem. Ecol. 16, 631–641. Trigona moorei: how do bees initiate their nests within an arboreal ant nest? Biotropica 21, 265– Zucchi R., Sakagami S.F. (1972) Capacidade termo- 274. reguladora em Trigona spinipes e em algu- mas outras aspecies de abelhas sem ferrão, in: Sakagami S.F., Roubik D.W., Zucchi R. (1993) Homenagem a W.E. Kerr, Rio Claro, Brasil, Ethology of the robber stingless bee, Lestrimelitta pp. 301–309.