Information Flow and Organization of Stingless Bee Foraging Jacobus Biesmeijer, E

Information flow and organization of stingless bee foraging Jacobus Biesmeijer, E. Judith Slaa

To cite this version:

Jacobus Biesmeijer, E. Judith Slaa. Information flow and organization of stingless bee foraging. Apidologie, Springer Verlag, 2004, 35 (2), pp.143-157. 10.1051/apido:2004003. hal-00891878

HAL Id: hal-00891878 https://hal.archives-ouvertes.fr/hal-00891878 Submitted on 1 Jan 2004

HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Apidologie 35 (2004) 143–157 © INRA/DIB-AGIB/ EDP Sciences, 2004 143 DOI: 10.1051/apido:2004003 Review article

Information flow and organization of stingless bee foraging

Jacobus C. BIESMEIJER*, E. Judith SLAA

Neurobiology and Behavior, Seeley G. Mudd Hall, Cornell University, Ithaca NY 14850, USA

(Received 1st August 2003; revised 16 October 2003; accepted 15 December 2003)

Abstract – Stingless bees (Hymenoptera, Apidae, Meliponini) live in populous permanent colonies and face the same problem as other foraging social insects: how to coordinate the worker’s actions and respond to the spatio-temporal uncertainties of food availability in their habitat. Here we review the (social) information used by individual foragers and how organized collective foraging emerges from the individual actions. We also address intra- and interspecific competition for food and the impact of the African honey bee on stingless bee collective foraging.

Melipona / Trigona / self-organization / communication / foraging / Africanized honeybee / insect society

1. INTRODUCTION mellifera L. The largest (Michener, 2000) group of social bees, the stingless bees (Api- Large social insect colonies lack central- dae, Meliponini) has received much less atten- ized control yet function as coherent wholes tion, probably because they inhabit the tropical and flexibly adjust their activities in response forest, which traditionally has received less to environmental challenges. How such a sys- attention from scientists. Only a small fraction tem is organized has become apparent through of the more than 400 species has been studied painstakingly observing the behavior of indi- in any detail, but already a wide variety of vidually marked individuals (mostly in bees; nesting and foraging habits has been discov- e.g. Seeley, 1995) or largely anonymous ered. In this paper we review information use worker groups (mostly in ants; e.g. various by individual foragers and how this relates to chapters in Detrain et al., 1999a). Observation organized foraging at colony level. First we of marked individuals allows one to assess describe the various sources of information the roles of previous experience and social that foragers may use in individual decision- information on individual decision-making, making, then we address the behavioral forag- whereas observation of worker groups focuses ing strategies that stingless bees display, and on colony-level processes such as allocation of how these lead to single colony and multi spe- workers over tasks and collective defense and cies foraging patterns observed in the field. foraging. Only through connecting these two Finally we analyze the role of different forag- levels, the mechanisms of individual behavior ing strategies in stingless bee coexistence and and the patterns that emerge at colony level, the influence of the recent invasion of the Afri- can a thorough understanding of the social can honey bee in the Americas on stingless bee physiology of insect societies be obtained. collective foraging. Much of our knowledge of social bees Note that although we aim at reviewing stems from studies performed on a single information on all stingless bees, most studies ‘atypical’ species, the western honey bee Apis deal with Neotropical species, some with

* Corresponding author: [email protected]; [email protected] 144 J.C. Biesmeijer, E.J. Slaa

Asian species, and very few with African Memory is another major source of intrinsic species. Much study has been devoted to information and is used to decide when to start recruitment mechanisms of stingless bees, foraging, where to forage, and which flower to which is reviewed by Nieh in this issue. visit. This allows bees to inspect known food sources after an interruption (time-place learning; Freitas and Raw, 2000; Biesmeijer and 2. INFORMATION SOURCES Ermers, 1999; Breed et al., 2002), show flower FOR FORAGERS constancy within patches and over consecutive foraging bouts (Inoue et al., 1985; Biesmeijer An individual bee makes its behavioral and Tóth, 1998; Slaa et al., 1998, 2003a), and decisions based on information from a variety discover new patches of learned food plants of sources. We distinguish five major private (Biesmeijer, unpublished data) without need- and social information sources: the individual ing information from nest mates. As a group itself (spontaneous preferences and memory), experienced foragers probably inspect all prof- the nest environment (colony state and nest itable food sources from the previous day after mates), nest mates in the field, conspecific an overnight interruption. Together they form non-nest mates in the field, and heterospecifics the ‘joint memory’ of the colony (Thierry in the field. These extrinsic information et al., 1996) and provide the up-to-date infor- sources provide a continuous flow of informa- mation that is the basis of efficient and flexible tion to the forager who integrates it with its colony foraging. intrinsic information to make behavioral deci- Other sources of intrinsic information sions. We summarize the evidence for infor- include development and hormones. In bum- mation use from each of these sources and its ble bees larval feeding determines the size effect on the receiver (Tab. I). In this review of the adult bee, which in turn determines we will not address other environmental the bee’s tendency to forage (Spaethe and sources of information used by foragers, Weidenmüller, 2002) and her visual acuity and e.g. climatic conditions (Lutz, 1931; Kleinert- olfactory perception (Spaethe et al., 2001). Giovannini, 1982; Heard and Hendrikz, 1993), Juvenile hormone levels are involved in the features of flowers, flower patches and other switch from nurse bee to forager in honey bees food sources, or the presence of predators (e.g. Robinson, 1987). None of these factors (e.g. Craig et al., 1996). has received much attention in stingless bee research. 2.1. Intrinsic information 2.2. Information from nest environment Influence of genes on stingless bee behavior is virtually unknown. However, it is safe to Stingless bee colonies consist of several assume that stingless bees show spontaneous hundreds to tens of thousands of individuals, preferences for some foraging parameters, e.g. one or few queens, some virgin queens and flower color and odor, and differ in learning males. Virgin queens and males do not partic- capacity (Pessotti and Lé’Sénéchal, 1981; ipate in foraging [but may visit flowers during Biesmeijer and Slaa, unpubl. data) and other their escapades (Kerr, 1994)] and workers col- aspects of foraging (e.g. scouting tendency, lect all food. Therefore, information exchange food type selection), as do honey bees. Ranger among the workers is key to colony foraging and O’Donnell (1999) demonstrated a genetic efficiency and indirectly to colony growth and effect on pollen and nectar collecting among reproductive success. Social organization is Partamona bilineata foragers (= P. orizabaen- probably largely based on self-organization sis according to Pedro and Camargo, 2003). and individuals use rules of thumb based on The acquisition of information must also differ information obtained from the nest structures among the species as a result of species-spe- and nest mates to make decisions. cific differences in their sensory organs (olfac- Although the nest environment is structured tory disk number: Johnson and Howard, 1987; by activities of the colony’s members, it also slight differences in photoreceptors: Menzel, structures individual behavior. This process is 1990), but has rarely been studied. called stigmergy (Grassé, 1959) and plays an Information flow and stingless bee foraging 145

Table I. Information sources used by stingless bee foragers. Note that not all bee species use all information sources equally (see text for further explanation). Although most species forage for floral nectar and pollen, the information sources also apply to other resources used by stingless bees, such as fruits, meat, resin, mud and water. Information source Information type Receiver Effect References 1. Intrinsic sources Genes Innate preferences All bees Food type selection 1-4 through gene expression (nectar/pollen, flower color, odor etc.), learning capacity, perception, and possibly scouting tendency Brain Learned information All bees through memory A. Time of foraging Start inspection activity 5-7 B. Place of food source Inspection of known 8-10 food source C. Food type Flower constancy (odor, 11-15 color), quality preference (e.g. nectar concentration) Development and Preference mediated by ?? Not studied hormones larval food experience or hormone levels 2. Nest environment Colony pollen Lack of pollen Pollen foragers Probably intensification 17 reserves availability? of individual foraging Nurse bees? rate Non-foragers Pollen foraging 17 preferred to nectar foraging Successful foragers Behavior (movements, sounds), trophallaxis, odor of returnee A. Location of food Naïve and Recruitment to food 16 source unknown to unemployed foragers source receiver B. Odor of known food Experienced foragers Reactivation to indicated 5,10 source food source C. Food source type Experienced foragers Reactivation to similar 5,10 (nectar/pollen) food sources Waste dumpers Flight activity Experienced foragers Reactivation 5 Nectar collectors ?? Non-foragers Switch to nectar 30 that experience a receiving delay in nectar unloading 3. Field – nest mates Successful foragers A. Location of food Naïve and Recruitment to indicated 16 patch through scent trail unemployed foragers food source and/or scent marks recruited in the nest 146 J.C. Biesmeijer, E.J. Slaa

Table I. Continued. Information source Information type Receiver Effect References B. Presence of nest mate Nest mates foraging Local enhancement 18 on flower in patch (attraction) or local inhibition (rejection) C. Scent marks on Nest mates foraging Selection (or rejection) 16, 19 flowers in patch including the of scented flower actor 4. Field – conspecific non-nest mates Successful foragers A. Presence of Non-nest mates Local enhancement/ 20 conspecific non- foraging in patch local inhibition, nestmate on flower aggressive interactions. Territorial fights may lead to uniform nest distribution B. Scent marks on All foragers in patch Selection (or rejection) 21 flowers of scented flower Nest entrance Visual/olfactory? Bees from other Attack nest and rob food 22 conspecific nests and/or wax 5. Field – heterospecifics Successful foragers A. Presence of Heterospecifics Local enhancement/ 18, 23-26 heterospecific on flower foraging in patch local inhibition, aggressive interactions B. Scent marks on Heterospecifics Selection (or rejection) 2, 27-29 flowers foraging in patch of scented flower Nest entrance Visual/olfactory? Robber bees near Organize raid on nest nest (e.g. Lestrimelitta, Cleptotrigona) References: 1Pessotti and Lé’Senéchal, 1981; 2Johnson, 1987; 3Ranger and O’Donnell, 1999; 4EJS and JCB, unpubl data; 5Biesmeijer et al., 1998; 6Biesmeijer and Ermers, 1999; 7Breed et al., 2002; 8Lindauer and Kerr, 1958; 9Nieh and Roubik, 1995; 10JCB, unpubl. data; 11Roubik et al., 1995; 12Roubik and Buchmann, 1984; 13Biesmeijer et al., 1999b; 14Slaa et al., 1998; 15Slaa et al., 2003a; 16reviewed by Nieh, 2004; 17Biesmeijer et al., 1999a; 18Slaa et al., 2003b; 19Schmidt et al., 2003; 20Hubbell and Johnson, 1977; 21Villa and Weiss, 1990; 22Kerr, 1994; 23Schwarz, 1932; 24Johnson and Hubbell, 1974; 25Howard, 1985; 26Nagamitsu and Inoue, 1997; 27Kerr et al., 1963; 28Johnson, 1974; 29Johnson, 1983; 30Hart, unpubl. data. important role in task coordination and the mates (e.g. nurse bees). Other activities in regulation of building activities in many social which stigmergy probably plays a role is in insects (Theraulaz and Bonabeau, 1995). dead bee removal and waste removal. Stigmergy probably plays an important role in Returning successful foragers are a rich organizing nest and cell building and other source of information to nest mates. They may activities in stingless bees. It is not known provide detailed information on food source whether the increase in pollen foraging in location to naïve foragers (recruitment; Nieh, Melipona beecheii observed after storage 2004) and to experienced foragers (reactiva- pot removal (Biesmeijer et al., 1999a) was tion; Biesmeijer and de Vries, 2001). Moreo- induced through stigmergy (direct observation ver, experienced foragers from other food of pollen shortage by (potential) pollen forag- sources may use odor and food type cues from ers) or through information obtained from nest a returnee to start or continue foraging at their Information flow and stingless bee foraging 147 previous source (Biesmeijer et al., 1998). This away. At closer range the decision whether to is evidenced by the observation that the entry land was made (Slaa et al., 2003b). of a single pollen-carrying forager into the nest of M. costaricensis (all other returnees were 2.4. In the field: information captured) may lead to a dramatic increase in from conspecific non-nest mates outgoing experienced foragers (Biesmeijer et al., 1998). Similarly, injecting scented sugar Although stingless bees lack a functional water into the nest leads to the specific reacti- sting, they are by no means defenseless, and vation of foragers with a previously developed aggression of foragers towards non-nest mates association between that scent and any profit- has been documented repeatedly (Tab. II; able food source (Biesmeijer and Slaa, unpub- e.g. Schwarz, 1932; Johnson and Hubbell, lished data; similar behavior in honey bees: 1974; Nagamitsu et al., 1999; Slaa, 2003). Wenner and Johnson, 1966). Furthermore, Aggressive behavior during foraging is spe- returning nectar foragers of M. beecheii that cies-specific, and seems restricted to species experience a long delay before they unload that possess powerful weapons: multiple man- their nectar can apparently induce nest mates dibular teeth in Trigona, caustic acid from to switch to nectar unloading (A. Hart, pers. mandibular glands in Oxytrigona (Roubik comm.); an effect similar to that of the tremble et al., 1987; Roubik, 1992; Michener et al., dance in Apis mellifera (Seeley et al., 1996). 1994; Tab. II). The movements of waste removal bees near the nest entrance can, in absence of informa- Competition for food is most intense tion from returning foragers, also activate between more similar individuals, i.e. conspe- foragers (Biesmeijer et al., 1998). cifics from different nests (Johnson, 1974). Diets of conspecific nests are more similar than of heterospecific nests (pollen: Ramalho 2.3. In the field: social information et al., 1989; Sommeijer et al., 1983; Biesmeijer from nest mates and van Nieuwstadt, 1997; Nagamitsu et al., The selection of food patches in the field or 1999; Eltz et al., 2001; nectar: Biesmeijer individual flowers within a patch can be et al., 1999c). This renders, if foraging ranges guided by information obtained from nest overlap, a high probability of encountering a mates. Finding unknown food patches is facil- conspecific non-nest mate on a flower. itated by recruitment communication by Intraspecific conflict can only take place if means of scent trails (reviewed by Nieh, bees discriminate nest mates from non-nest 2004). Choosing a flower within a patch may mates. Nest mate discrimination has been be based on scent marks left by nest mates demonstrated in several Melipona (Breed and (Villa and Weiss, 1990; Goulson et al., 2001) Page, 1991; Inoue et al., 1999) and Trigonine or on the physical presence of a nest mate on a species (Suka and Inoue, 1993; Kirchner and flower (Slaa et al., 2003b). In both cases the Friebe, 1999) and seems common in stingless information can be attractive or repellent. Slaa bees. Fights between non-nest mates usually et al. (2003b) observed strong local enhance- end in the death of one or both of the bees ment (Thorpe, 1956), i.e. selection of the (Breed and Page, 1991; Biesmeijer and Slaa, flower occupied by a nest mate, in some pers. obs.) and some fights between conspe- species and local inhibition, i.e. avoidance of cific colonies may result in tens to thousands the flower occupied by a nest mate, in other of dead bees (Johnson and Hubbell, 1974; species. Moreover, in Trigona amalthea the Hubbell and Johnson, 1978). However, in response of arriving bees depended on their some genera, e.g. Scaptotrigona, bees of mul- previous experience at the flower patch. Naïve tiple colonies scramble peacefully together for foragers landed next to their nest mate on their nectar or pollen (Johnson, 1974). In Tetrago- first arrival. This tendency gradually shifted to nisca angustula, a non-aggressive species, for- complete avoidance of the flower occupied by agers do not discriminate among the chemical their nest mate after the fifth visit to the patch. cues left by nest mates and non-nest mates However, to all bees the presence of a nest (Villa and Weiss, 1990), but it is unknown mate is an attractive visual cue from further whether this is similar for aggressive species. 148 J.C. Biesmeijer, E.J. Slaa

Table II. Aggression during foraging in the different stingless bee genera. Note that some species that do not forage aggressively may show aggressive behavior in other contexts, such as nest defense (e.g. Scaptotrigona and Partamona).

(sub)Genus Aggressive foraging Non-aggressive foraging Reference Melipona costaricensis(±) (prev. fasciata), 1, 2 fulva 12 Cephalotrigona capitata 1 Homotrigona fimbriata 3 Hypotrigona spp. 4 Lepidotrigona ventralis 3 Liotrigona spp. 4 Nannotrigona testaceicornis(±) 1, 5 Noguerapis mirandula 2 Oxytrigona mellicolor, 1 obscura 12 Partamona aff. cupira(±), 1, 2 testacea 12 Plebeia frontalis, 1, 5 jatiformis 2 Scaptotrigona pectoralis, 1, 6 mexicana 7 Scaura latitarsus 7 Tetragona dorsalis 1 clavipes 12 Tetragonisca angustula 1 Tetragonula melina(±) melanocephala, 3 leaviceps 3 Tetrigona apicalis 3 Trigona corvina, 1, 6, 7 cilipes, 12 fuscipennis, 5, 6, 8 hyalinata, 6, 9 pallens, 6 amalthea, 1, 2, 5-7 fulviventris(±), 1, 2, 5, 8 canifrons 2 iridipennis 10 williana 5, 11-13 spinipes 9 Trigonisca buyssoni 5 References: 1Slaa, 2003; 2Howard, 1985; 3Nagamitsu and Inoue, 1997; 4Darchen, 1972, cited in Hubbell and Johnson, 1977; 5Hubbell and Johnson, 1978; 6Johnson, 1983; 7Johnson and Hubbell, 1974; 8Johnson and Hubbell, 1975; 9Kerr et al., 1981; 10Koeniger and Vorwohl, 1979; 11Schwarz, 1932; 12Roubik, 1980; 13Johnson, 1981. Information flow and stingless bee foraging 149

2.5. In the field: information ety of solitary and social foraging behaviors. from heterospecifics Whereas stingless bees, like honey bees, are highly social concerning nest activities, forag- Because the stingless bees of a community ing is not necessarily a group activity. This is overlap highly in foraging range (e.g. Hubbell in fact also similar to the honey bee, where the and Johnson, 1977; Roubik, 1983b; Eltz et al., waggle dance is used only for excellent food 2002; Slaa, 2003), encounters between heter- sources (rare and unpredictable in nature) and ospecifics are common. Reactions to a heter- where in dearth periods many foragers search ospecific vary widely from avoidance to independently for food (Seeley, 1983; Seeley attack, depending on the species combination and Visscher, 1988; Biesmeijer, unpublished (Slaa et al., 2003b). Aggressive species are data). sometimes attracted towards a heterospecific, Some species are always solitary foragers, generally leading to the departure of the resi- i.e. they never recruit nest mates to food dent bee. However, avoidance of a heterospe- sources, others are obligate group foragers, cific seems much more common, and avoid- and yet others are facultative group foragers ance behaviour is accurately predicted by (Johnson, 1983). The solitary foragers use relative body size and aggressiveness of the mainly intrinsic information to exploit food two species: non-aggressive species avoid sources, but may use odors from foragers aggressive species and smaller species gener- returning to the nest (Lindauer and Kerr, ally avoid larger species (Slaa et al., 2003b). 1958), scent marks left by others on flowers Besides the physical presence of a bee, for- and the presence of nest mates on resources as agers may also pick up scent cues from heter- cues. The group foragers may use any ospecifics. Evidence exists for both attraction information source mentioned above and in to and avoidance of heterospecific scent Table I to make foraging decisions. marks. Johnson (1974) found that pheromones of an aggressive species on a food source repel The social physiology of stingless bee colonies is probably as advanced as that of honey a less aggressive species. Experiments by Kerr et al. (1963) suggest that Scaptotrigona xan- bees (Seeley, 1995). So far they have been thotricha can follow the scent trails left by shown to have coordinated nest defense (e.g. Lindauer, 1957) and nest building, division of S. postica, although this hetero-specific trail following was non-reciprocal. In addition, the labor (e.g. Sommeijer et al., 1982; Sommeijer, dominant T. amalthea seems to exploit the 1984), task partitioning of nectar foraging (Sommeijer et al., 1985; Hart and Ratnieks, capacity of the less aggressive T. fulviventris to quickly find new food sources by attraction 2002), adjustment of worker behavior and to its scent marks (Johnson, 1983, 1987). worker allocation in response to the removal of nectar reserves (Kolmes and Sommeijer, Although most species collect their food 1992a, b), the ability to counter deficits in pol- from sources in the field (i.e. flowers, car- len reserves (Biesmeijer et al., 1999a) and to casses, fruits, etc.), some species are special- select the best of a series of food sources ized in attacking other stingless bee nests for (Biesmeijer and Ermers, 1999). the collection of food. Such obligate robbers (belonging to the genera Lestrimelitta and The collective foraging patterns emerge Cleptotrigona) probably use visual and/or from the multitude of activities of individual olfactory cues to find nest entrances of poten- foragers that make foraging decisions based tial victim colonies. Such raids may also occa- on intrinsic and other information they have sionally occur in species that normally collect acquired. The life of a stingless bee (or other food from sources in the field (Roubik, 1989; social insect) forager looks more or less like H. de Jong, pers. comm.). this (Biesmeijer and de Vries, 2001; Seeley, 1995): each bee starts as a naïve forager, and can then either become a scout (if only 3. FORAGING ORGANIZATION intrinsic information is used) or a recruit (if OF A SINGLE COLONY information from nest mates stimulates the start of foraging). After having found a food The use of information from the various source she is an employed forager and tends to sources described above leads to a wide vari- revisit the food source. At the end of the day or 150 J.C. Biesmeijer, E.J. Slaa foraging period she becomes temporarily renewing sources and as a response to bigger, unemployed. Next she can either revisit her more aggressive residents. 2. Displacement, previous food source as an inspector (based on an arriving bee causes the departure of a (gen- intrinsic information from previous foraging) erally smaller) resident with or without or as a reactivated forager (if nest mates aggressive behavioral interaction. 3. Glean- provide information about her previous food ing, a (generally small) bee collects the lefto- source) or search for a new food source as a vers after the peak of attractiveness or other scout or recruit. After finding a rich food visitors have passed. 4. Insinuation, a (small) source she can (in most species) provide nest bee nervously but persistently collects from a mates with information on the location of that source occupied by aggressive bees. food source and initiate recruitment. The group foraging strategies distinguished Recruitment communication directs the by Johnson (1983) are: 1. Scramble group for- allocation of naïve and temporarily unem- aging, also referred to as exploitation compe- ployed foragers over food sources. However, tition, where each bee collects food (and the majority of the foragers at any time have recruits) as quickly as possible without physi- some previous experience and much of the cal interference with other bees. 2. Bustling, colony’s efficiency in exploiting food sources the hyperactive foraging movements of bees is a result of individual foragers responding to discourages other bees to forage at the same the changes in their direct environment. For flowers. 3. Extirpation, where after rapid example, new food sources may be found by recruitment of nest mates to a rich food source special scouts, but also by experienced bees the residents are chased off aggressively. that start searching after their food sources 4. Opportunism, bees usually forage solitary dried up and by errand recruits (Biesmeijer, but may rapidly recruit nest mates if an excep- unpublished data). Also, the choice of a colony tionally good food source is found. They con- for the richest food source is simply a result of tinue till stronger rivals extirpate them from bees that decide to start, continue or stop for- the flowers. aging based on previous experience at their Johnson’s eight foraging strategies are nei- food source and not of any cross-referencing ther species-specific nor complementary. Fur- procedure (Biesmeijer and Ermers, 1999). thermore, although scramble is defined as a This again is similar in honey bees where the group foraging strategy, a single forager that nectar receiving bees are the only link between does not show avoidance or displacement but the various nectar sources exploited by differ- peacefully feeds with other bees is also a ent groups of bees (Seeley, 1995). The spe- scrambler (and cannot be put in any other cat- cies-specific spatial pattern of food source egory). Another way of approaching stingless exploitation is also a result of individual bees bee foraging strategies in relation to heter- showing either local enhancement, which ospecifics would be to describe them in terms leads to clumped group foraging, or local inhi- of three foraging parameters: recruitment abil- bition, which leads to dispersed group forag- ity (solitary or group foraging), degree of local ing (Slaa et al., 2003b). enhancement towards heterospecifics (attraction or avoidance), and competitive ability (aggressive or not). Table III shows that most 4. FORAGING STRATEGIES of Johnson’s strategies correspond to a spe- IN HETEROSPECIFIC cific combination of these three parameters. INTERACTIONS Only avoidance and gleaning correspond to the same combination of bees that do not Based on years of behavioral observation of recruit, show local inhibition towards heter- interactions among Costa Rican Trigona bees, ospecifics and are competitively weak. The Johnson (1983) recognized four solitary and only difference is that gleaners stick around till four group foraging strategies. the stronger rivals have gone and then start The solitary foraging strategies are: 1. food collecting, whereas avoiders leave with- Avoidance, a bee chooses not to forage near out collecting food. In addition, opportunists another bee or bees (i.e. local inhibition). form a difficult category. When not recruiting Avoidance occurs on small, scattered, slow- they may show avoidance, displacement or Information flow and stingless bee foraging 151

Table III. Social foraging strategies of stingless bees defined by Johnson (1983) and their relation with three major foraging parameters: recruitment ability, local enhancement in heterospecific encounters, and individual aggressiveness.

Solitary foraging Recruitment Local enhancement Aggressive behavior Avoidance No No No Displacement No Yes Yes Gleaning No No No Insinuation No Yes No Social foraging Scrambling Yes Yes No Bustling Yes No No Extirpation Yes Yes Yes Opportunism Yes/No Yes/No No individual scrambling, but when recruiting pollen diet. Their generalist foraging strategy they may show local enhancement or inhibi- and the overlap in resource use has led to the tion towards nest mates and local inhibition hypothesis that coexistence of stingless bees towards stronger rivals. largely stems from subtle partitioning of food Honey bees can be categorized as scram- sources based on diversity in timing, persist- blers both when foraging solitary among other ence, renewal rate, and spatial dispersion bees and when foraging in groups. Because of of their limited food sources (Hubbell and their large size, however, they may cause dis- Johnson, 1978). placement and avoidance of smaller stingless The foraging strategies observed at present bees including aggressive species (Roubik, have evolved from a basic plan. Each is geared 1980; Slaa, 2003). towards exploitation of specific food sources by putting differential weight on the major information sources and foraging parameters, 5. COEXISTENCE OF SPECIES e.g. recruitment precision and intensity, WITH DIFFERENT FORAGING aggressiveness, independent search, and local STRATEGIES enhancement. The mass-recruiting aggressive bees, e.g. several Trigona and Oxytrigona, are Stingless bees are very successful in most high-density specialists. They form dense for- tropical habitats where about 1 of every 2 bees ager groups through local enhancement, pos- seen on flowers is a stingless bee (Heithaus, sess powerful weapons (teeth or burning acid; 1979; Roubik, 1989) and up to several dozen Slaa, 2003) to attack everything at and near the species may occur sympatrically (Roubik, food and so monopolize clumped food 1989; Slaa, 2003). Stingless bee abundance sources. They are, however, not very good at seems more dependent on food sources than finding new food sources (Nagamitsu et al., on nest site availability (Hubbell and Johnson, 1999; Slaa, 2003). This is the trade-off for low 1977; Eltz et al., 2002), and diet overlap, in independent scouting ability (all bees are terms of food plant species used, is generally needed as recruits) and strong local enhance- considerable (Roubik et al., 1986; Ramalho ment (no neighboring food patches are found). et al., 1990; Eltz et al., 2001). However, The mass-recruiting non-aggressive bees, e.g. Roubik and Moreno (2000) found that three Scaptotrigona, Partamona and Apis, are also species of stingless bees were both generalists high-density specialists. They do not show (using the same key species) and specialists strong local enhancement and quickly find (using minor and major species little used by food patches near the one discovered by the others) and Nieuwstadt et al. (1997) found that scout bee (Nagamitsu et al., 1999; Slaa, 2003). a few plant species make up the bulk of the In this way they can keep one step ahead of the 152 J.C. Biesmeijer, E.J. Slaa aggressive group foragers and display short- Melipona, Partamona, Scaptotrigona, and term use of rich and clumped food sources. smaller stingless bees, may share the food The poorly recruiting species probably pro- source with African honey bees (Roubik, vide nest mates with some general indication 1980). In this way African honey bees can of food odor or location that can guide their make rich food sources accessible to stingless largely independent search (Lindauer and bee scramblers that would otherwise be dis- Kerr, 1958, 1960; similar in bumble bees: placed by aggressive group foragers. Other Dornhaus and Chittka, 2001). They may show aggressive stingless bees, e.g. Trigona pallens local enhancement (e.g. Tetragonisca angus- and Tetragona clavipes, may share a rich food tula; Slaa et al., 2003b) or indifference to the source with African honey bees by monopoliz- presence of nest mates (e.g. Tetragona dorsa- ing part of it (Roubik, 1980). The impact of lis; Slaa et al., 2003b). Occasionally they per- African honey bees on stingless bee foraging sist as scramblers at high-density food sources, thus depends on the foraging strategy used by but generally use low-density food sources the stingless bee species. (Hubbell and Johnson, 1978). Yet another group of species, e.g. Trigona fulviventris and T. amalthea, uses recruitment occasionally, 7. CONCLUDING THOUGHTS but commonly forage solitarily at low-density food sources (facultative group foragers; Stingless bee foraging is, as is foraging in Hubbell and Johnson, 1978; Slaa, 2003). They most social insects, largely self-organized. are strong individual competitors that show There is no omniscient manager that integrates local inhibition towards nest mates (Slaa et al., all information and issues orders to the subu- 2003b), but carefully single out weaker rivals nits. This does not mean, however, that indi- for attack. In this way they spread out over vidual foragers lack sophisticated cognitive food sources and may monopolize high-den- abilities. They can learn and memorize many sity food patches till the arrival of extirpators things and may share some advanced cogni- or dominate low-density patches for longer tive features, e.g. concept abstraction (Giurfa periods (Johnson, 1975). et al., 1996, 1999), with honey bees. For foraging, some species (solitary foragers) rely largely on individual decision making in the 6. COEXISTENCE WITH field. This is similar to bumble bee foraging THE AFRICAN HONEY BEE (Dornhaus and Chittka, 2004). On the other extreme are the obligate group foragers that Since its introduction into Brazil in 1956 largely rely on collective decision-making. the African honey bee, Apis mellifera scutel- However, here it is not ‘blind’ trail following lata Lepeletier has invaded every corner of as in some ants (e.g. Detrain et al., 1999b), tropical and subtropical America including since individuals that loose track can rely on stingless bee territory. Many studies show that intrinsic and field information to locate other the presence of the African honey bee leads to food sources (Slaa, 2003) or return home. The a decrease in stingless bee foraging at flower facultative group foragers are intermediate. patches (e.g. Roubik, 1978, 1989) and dimin- They normally rely on individual decision- ished colony foraging peaks in various species making, but in ‘recruitment mode’ rely heavily (Roubik et al., 1986), but not to lower colony on collective decision-making. food storage or brood production (Roubik, The species-specific balance between indi- 1983a). In Panama, stingless bee populations vidual and collective decision-making deter- do not seem affected by African honey bees mines the foraging niche of each species. The even 10 years after their arrival (Roubik and coexistence of multiple species with different Wolda, 2001). foraging strategies indicates that the various Honey bees are scramble competitors and strategies are complementary in the way they larger than stingless bees. This prevents extract food from their ever-changing habitat. aggressive Trigona from taking over a food It seems therefore not justified to refer to source occupied by multiple African honey some strategies as primitive and others bees, but other scramble foragers, e.g. (e.g. mass-recruiting strategies) as advanced. Information flow and stingless bee foraging 153

The aggressive group foraging strategy has compétitive individuelle (agressivité ou non ; received most attention simply because it is Tab. II). Chacune de ces stratégies de butinage pro- spectacular and easily observed at an artificial pre à chaque espèce semble conçue pour exploiter un sous-ensemble spécifique (dans l’espace, le nectar feeder. However, it is only one aspect of temps ou l’identité floristique) des sources poten- the rich variety of foraging behaviors that tielles de nourriture et les diverses stratégies sont stingless bees perform. grandement complémentaires. Le monde des abeilles sans aiguillon néotropicales a récemment été occupé par des milliers de colonies Résumé – Flux d’information et organisation du d’abeilles africanisées avec lesquelles elles parta- butinage chez les abeilles sans aiguillon. Les gent désormais de nombreuses sources de nourri- abeilles sans aiguillon (Hymenoptera, Apidae, ture. Les pics de butinage ont diminué et le déplace- Meliponini) vivent en colonies pérennes populeuses ment a régulièrement lieu, mais l’impact des et sont confrontées aux mêmes problèmes que les abeilles africanisées sur la population d’abeilles autres insectes sociaux qui butinent : comment sans aiguillon n’est pas encore entièrement com- coordonner l’action des ouvrières et répondre aux prise. incertitudes spatio-temporelles de la disponibilité en nourriture dans leur habitat. Nous passons en Melipona / Trigona / autoorganisation / commu- revue les informations sociales utilisées individuel- nication / butinage /abeille africanisée /société lement par les butineuses et examinons comment un d’insectes butinage collectif organisé émerge des actions individuelles. Nous traitons aussi de la compétition intra- et interspécifique pour la nourriture et de l’impact de l’Abeille africanisée sur le butinage Zusammenfassung – Informationsübertragung collectif des abeilles sans aiguillon. und Organisation des Sammelverhaltens bei Sta- chellosen Bienen. Stachellose Bienen (Hymenop- Le tableau I résume les principales sources d’infor- tera, Apidae, Meliponini) leben in mitgliederstar- mations que peuvent utiliser les butineuses des ken dauerhaften Völkern und haben das gleiche abeilles sans aiguillon. Elles se répartissent en Problem wie alle sozialen Insekten beim Futter informations intrinsèques (par ex., les préférences sammeln: Koordination der Aktionen der Arbeite- innées dues à l’expression des gènes, à la mémoire, rinnen und Reaktion auf räumlich – zeitliche Unsi- aux taux d’hormones) et les informations extrinsè- cherheiten im Futterangebot ihres Umfelds. Wir ques. Celles-ci incluent les informations en prove- geben hier einen Überblick über die (soziale) Infor- nance du nid (membres de la colonie, structure du mation, die von individuellen Sammelbienen nid) et celles provenant de l’extérieur par l’intermé- benutzt werden und wie ein kollektives Sammeln diaire des membres de la colonie, des individus de aus den Aktionen von Einzeltieren hervorgeht. Wir la même espèce et des autres espèces. Les membres sprechen auch über die intra- und interspezifische de la colonie prennent à titre individuel leurs déci- Konkurrenz für Nahrung und die Auswirkung von sions en se basant sur l’intégration des informations Afrikanisierten Honigbienen auf das kollektive intrinsèques et extrinsèques et la multitude des acti- Sammeln bei Stachellose Bienen. vités individuelles aboutit à un comportement col- Die wichtigsten Informationsquellen, die von Samm- lectif efficace. La physiologie sociale des colonies lerinnen der Stachellose Bienen genutzt werden d’abeilles sans aiguillon est aussi avancée que celle können, sind in Tabelle I zusammengefasst und des abeilles mellifères et comprend la construction basieren auf in der Biene liegender Information et la défense du nid par coopération, le butinage (z.B. angeborene Vorzüge auf Grund genetischer collectif et le choix de la meilleur source de Expression, Gedächtnis, Hormonspiegel) und von nourriture. außen wirkender Information. Letzteres umfasst Dans la plupart des habitats tropicaux plusieurs Informationen innerhalb des Nestes (Nestgenossin- espèces d’abeilles sans aiguillon sont présentes de nen und Neststruktur) und aus dem Umfeld des façon sympatrique et entrent en compétition pour Nestes durch Nestgenossinnen, durch artgleiche la nourriture. La coexistence est rendue possible Nicht – Nestgenossinnen und Bienen anderer Arten. par le développement d’une diversification des Einzelne Volksmitglieder entscheiden sich im stratégies individuelles et sociales de butinage. Verhalten auf Grund einer Integration von inneren On dénombre quatre stratégies individuelles : les und äußeren Informationen, und die Vielzahl von butineuses s’évitent, se déplacent, glanent et se individuellen Aktivitäten führt zu einem effektiv- faufilent, et quatre stratégies sociales : elles se kollektiven Verhalten. Die soziale Physiologie der bousculent, s’agitent, s’extirpent et font preuve Völker der Stachellosen Bienen ist genauso weit d’opportunisme. Ces huit stratégies reposent sur fortgeschritten wie das der Honigbienen und des différences dans les paramètres de butinage schließt gemeinsamen Nestbau und Verteidigung, (Tab. III) : capacité de recrutement (butinage soli- kollektives Sammeln von Nahrung und Auswahl taire ou recrutement jusqu’à un certain degré), der besten Nahrungsquelle ein. augmentation locale des membres de la colonie In vielen tropischen Lebensräumen kommen (attraction, indifférence ou évitement) et capacité mehrere Arten der Stachellose Bienen sympatrisch 154 J.C. Biesmeijer, E.J. Slaa vor und konkurrieren um die Nahrung. Die Coexis- Biesmeijer J.C., Born M., Lukács S., Sommeijer M.J. tenz ist durch die Entwicklung einer Mannigfaltig- (1999a) The response of M. beecheii experimen- keit der individuellen und der sozialen Sammelstra- tal pollen stress, worker loss and different levels tegie möglich. Diese bestehen aus 4 individuellen of information input, J. Apic. Res. 38, 29–37. Strategien: Vermeidung, Verlagerung, Nachlese Biesmeijer J.C., Richter J.A.P., Smeets M., und sich Einschleichen; und 4 Gruppenstrategien: Sommeijer M.J. (1999b) Niche differentiation in Drängeln, Vorpreschen, Vernichtung und Opportu- nectar-collecting stingless bees: the influence of nismus. Diese 8 Strategien beruhen auf Unterschie- morphology, floral choice and interference den von 3 Parametern (Tab. III): Fähigkeit zur competition, Ecol. Entomol. 24, 380–388. Rekrutierung, (solitäres Sammeln oder Rekrutie- Biesmeijer J.C., Smeets M., Richter J.A.P., rung bis zu einem gewissen Grad), lokale Ver- Sommeijer M.J. (1999c) Nectar foraging by stärkung von Nestgenossinnen (Attraktion, Nicht- stingless bees in Costa Rica: botanical and beachtung oder Vermeidung) und individuelle climatological influences on sugar concentration Fähigkeiten bei der Konkurrenz (aggressiv oder of nectar collected by Melipona, Apidologie 30, nicht; Tab. II). Jede dieser artspezifischen Sam- 43–55. melstrategien scheint an die Nutzung von spezifi- Breed M.D., Page R.E. Jr. (1991) Intra- and schen Teileigenschaften (in Raum, Zeit oder interspecific nestmate recognition in Melipona Blütenidentität) von möglichen Nahrungsquellen workers (Hymenoptera: Apidae), J. Insect Behav. angepasst zu sein und die verschiedenen Strategien 4, 463–469. ergänzen sich großenteils. Breed M.D., Stocker E.M., Baumgartner L.K., Vargas Der Lebensraum der neotropen Stachellosen Bie- S.A. (2002) Time-place learning and the ecology nen ist in der letzten Zeit von tausenden Völkern der of recruitment in a stingless bee, Trigona Afrikanisierten Honigbienen bewohnt, mit denen amalthea (Hymenoptera, Apidae), Apidologie sie jetzt viele ihrer Nahrungsquellen teilen müssen. 33, 1–8. Spitzenernten beim Sammeln sind seltener gewor- den und Verdrängungen kommen regelmäßig vor, Craig C.L., Weber R.S., Bernard G.D. (1996) aber die Auswirkung der Afrikanisierten Honigbie- Evolution of predator-prey systems: Spider foraging plasticity in response to the visual nen auf die Population der Stachellosen Bienen ist ecology of prey, Am. Nat. 147, 205–229. immer noch nicht vollständig klar. Darchen R. (1972) Écologie de quelques trigones Melipona / Trigona / Selbstorganisation / (Trigona sp.) de la savane de Lamto (Côte Kommunikation / Sammeln / Afrikanisierte d’Ivoire), Apidologie 3, 341–367. Honigbiene / Insektenvolk Detrain C., Deneubourg J.L., Pasteels J.M. (1999a) Information processing in social insects, Birkhäuser, Basel. Detrain C., Deneubourg J.L., Pasteels J.M. (1999b) REFERENCES Decision-making in foraging by social insects, in: Detrain C., Deneubourg J.L., Pasteels J.M. (Eds.), Biesmeijer J.C., van Nieuwstadt M.G.L. (1997) Information processing in social insects, Birkhäu- Colony foraging patterns of stingless bees in ser, Basel, pp. 331–354. Costa Rica, with special reference to pollen, in: The Organisation of Foraging in Stingless Bees of Dornhaus A., Chittka L. (2001) Food alert in bumble- the Genus Melipona, dissertation Utrecht bees (Bombus terrestris): possible mechanisms University, The Netherlands, pp. 35–57. and evolutionary implications, Behav. Ecol. Sociobiol. 50, 570–576. Biesmeijer J.C., Tóth E. (1998) Individual foraging, activity level and longevity in the stingless bee Dornhaus A., Chittka L. (2004) Information flow and Melipona beecheii in Costa Rica (Hymenoptera, regulation of foraging activity in bumble bees Apidae, Meliponinae), Insectes Soc. 45, 427– (Bombus spp.), Apidologie 35, 183–192. 443. Eltz T., Brühl C.A., van der Kaars S., Chey V.K., Biesmeijer J.C., de Vries H. (2001) Exploration and Linsenmair K.E. (2001) Pollen foraging and exploitation of food sources by social insect resource partitioning of stingless bees in relation colonies: a revision of the scout-recruit concept, to flowering dynamics in a Southeast Asian Behav. Ecol. Sociobiol. 49, 89–99. tropical rainforest, Insectes Soc. 48, 273–279. Biesmeijer J.C., Ermers M.C.W. (1999) Social Eltz T., Brühl C.A., van der Kaars S., Linsenmair foraging in stingless bees: how a M. fasciata K.E. (2002) Determinants of stingless bee nest colony chooses between nectar sources, Behav. density in lowland dipterocarp forests of Sabah, Ecol. Sociobiol. 46, 129–140. Malaysia, Oecologia 131, 27–34. Biesmeijer J.C., van Nieuwstadt M.G.L., Lukács S., Freitas R.I.P., Raw A. (2000) The perception of time Sommeijer M.J. (1998) The role of internal and by foraging workers of stingless bees (Hymenop- external information on foraging decisions of tera: Apidae, Meliponini), in: Proc. 6th Int. Conf. Melipona workers (Hym.; Meliponinae), Behav. on Apiculture in Tropical Climates, Costa Rica, Ecol. Sociobiol. 42, 107–116. IBRA, Cardiff, pp. 101–105. Information flow and stingless bee foraging 155

Giurfa M., Eichmann B., Menzel R. (1996) Symmetry Biology of Social Insects, Verlag J. Peperny, perception in an insect, Nature 382, 458–461. München, pp. 698–699. Giurfa M., Zhang S., Jennet A., Menzel R., Srinivasan Johnson L.K., Howard J.J. (1987) Olfactory disc M.V. (1999) The concepts of ‘sameness’ and number in bees of different sizes and ways of life ‘difference’ in an insect, Nature 410, 930–933. (Apidae: Meliponinae), J. Kans. Entomol. Soc. Goulson D., Chapman J.W., Hughes W.O.H. (2001) 60, 380–388. Discrimination of unrewarded flowers by bees; Johnson L.K., Hubbell S.P. (1974) Aggression and direct detection of rewards and use of repellent competition among stingless bees: Field studies, scent marks, J. Insect Behav. 14, 669–678. Ecology 55, 120–127. Grassé P.P. (1959) La reconstruction du nid et les Johnson L.K., Hubbell S.P. (1975) Contrasting coordinations interindividuelles chez Bellicosi- foraging strategies and coexistence of two bee termes natalensis et Cubitermes sp. La théorie species on a single resource, Ecology 56, 1398– de la stigmergie. Essais d’interprétation du com- 1406. portement des termites constructeurs, Insectes Soc. 6, 41–84. Kerr W.E. (1994) Communication among Melipona workers (Hymenoptera: Apidae), J. Insect Behav. Hart A.G., Ratnieks F.L.W. (2002) Task-partitioned nectar transfer in stingless bees: work organiza- 7, 123–128. tion in a phylogenetic context, Ecol. Entomol. 27, Kerr W.E., Ferreira A., Simões de Mattos N. (1963) 163–168. Communication among stingless bees – Addi- Heard and Hendrikz (1993) Factors influencing flight tional data (Hymenoptera: Apidae), J. N.Y. Ento- activity of colonies of the stingless bee Trigona mol. Soc. 71, 80–90. carbonaria, Aust. J. Zool. 41, 343–353. Kerr W.E., Blum M., Fales H.M. (1981) Communica- Heithaus E.R. (1979) Community structure of tion of food source between workers of Trigona neotropical flower visiting bees and wasps: (Trigona) spinipes, Rev. Bras. Biol. 41, 619–623. diversity and phenology, Ecology 60, 190–202. Kirchner W.H., Friebe R. (1999) Nestmate recogni- Howard J.J. (1985) Observations on resin collecting tion in the African stingless bee Hypotrigona gri- by six interacting species of stingless bees bodoi Magretti (Hymenoptera: Apidae), Apidolo- (Apidae: Meliponinae), J. Kans. Entomol. Soc. gie 30, 293–298. 58, 337–345. Kleinert-Giovannini A. (1982) The influence of cli- Hubbell S.P., Johnson L.K. (1977) Competition and matic factors on flight activity of Plebeia emerina nest spacing in a tropical stingless bee commu- Friese (Hymenoptera, Apidae, Meliponinae) in nity, Ecology 58, 949–963. winter, Rev. Bras. Entomol. 26, 1–13. Hubbell S.P., Johnson L.K. (1978) Comparative Koeniger N., Vorwohl G. (1979) Competition for foraging behavior of six stingless bee species food among four sympatric species of Apini in Sri exploiting a standardized resource, Ecology 59, Lanka (Apis dorsata, Apis cerana, Apis florea and 1123–1136. Trigona iridipennis), J. Apic. Res. 18, 95–109. Inoue T., Salmah S., Abbas I., Yusuf E. (1985) Kolmes S.A., Sommeijer M.J. (1992a) Ergonomics in Foraging behaviour of individual workers and stingless bees: changes in intranidal behaviour foraging dynamics of colonies of three Sumatran after partial removal of storage pots and honey in stingless bees, Res. Popul. Ecol. 27, 373–392. Melipona favosa (Hym. Apidae, Meliponinae), Inoue T., Roubik D.W., Suka T. (1999) Nestmate Insectes Soc. 39, 215–232. recognition in the stingless bee Melipona Kolmes S.A., Sommeijer M.J. (1992b) A quantitative panamica (Apidae, Meliponini), Insectes Soc. 46, analysis of behavioral specialization among 208–218. worker stingless bees (Melipona favosa F.) Johnson L.K. (1974) The Role of Agonistic Behavior performing hive duties (Hymenoptera, Apidae), in the Foraging Strategies of Trigona Bees, J. Kans. Entomol. Soc. 65, 421–430. Doctoral thesis, University of California, Berkeley, California. Lindauer M. (1957) Zur Biologie der stachellosen Bienen: ihre Abwehrmethoden. Ber. Wanderver- Johnson L.K. (1975) Contrasting foraging strategies samml., Dtsch. Entomol. 8, 71–78. and coexistence of two bee species on a single resource, Ecology 56, 1398–1406. Lindauer M., Kerr W.E. (1958) Die gegenseitige Verständigung bei den stachellosen Bienen, Z. Johnson L.K. (1981) Effect of flower clumping on Vergl. Physiol. 41, 405–434. defense of artificial flowers by aggressive stingless bees, Biotropica 13, 151–157. Lindauer M., Kerr W.E. (1960) Communication between the workers of stingless bees, Bee World Johnson L.K. (1983) Foraging strategies and the 41, 29–41; 65–71. structure of stingless bee communities in Costa Rica, in: Jaisson P. (Ed.), Social Insects in the Lutz F.E. (1931) Light as a factor in controlling the Tropics 2, Université Paris-Nord, Paris, pp. 31–58. start of daily activity of a wren and stingless bees, Am. Mus. Novit. 468, 1–9. Johnson L.K. (1987) Communication of food source location by the stingless bee Trigona fulviventris, Menzel R. (1990) Colour vision in flower visiting in: Eder J., Rembold H. (Eds.), Chemistry and insects, Jülich, Berlin. 156 J.C. Biesmeijer, E.J. Slaa

Michener C.D. (2000) The bees of the world, Johns African and Neotropical bees, Ecology 64, 971– Hopkins university Press, Baltimore Maryland. 978. Michener C.D., McGinley R.J., Danforth B.N. (1994) Roubik D.W. (1983b) Nest and colony characteristics The Bee Genera of North and Central America, of stingless bees from Panama (Hymenoptera: Smithsonian Institution Press, Washington. Apidae), J. Kans. Entomol. Soc. 56, 327–355. Nagamitsu T., Inoue T. (1997) Aggressive foraging of Roubik D.W. (1989) Ecology and Natural History of social bees as a mechanism of floral resource Tropical Bees, Cambridge University Press, New partitioning in an Asian tropical rainforest, York. Oecologia 110, 432–439. Roubik D.W. (1992) Stingless bees: a guide to Nagamitsu T., Momose K., Inoue T., Roubik D.W. Panamanian and Mesoamerican species and their (1999) Preference in flower visits and partitioning nests (Hymenoptera: Apidae: Meliponinae), in: in pollen diets of stingless bees in an Asian Quintero D., Aiello A. (Eds.), Insects of Panamá tropical rain forest, Res. Popul. Ecol. 41, 195– and Mesoamerica, Oxford University Press, 202. Oxford, pp. 495–524. Nieh J.C., Roubik D.W. (1995) A stingless bee Roubik D.W., Buchmann S.L. (1984) Nectar selec- (Melipona panamica) indicates food location tion by Melipona and Apis mellifera (Hymenop- without using a scent trail, Behav. Ecol. tera: Apidae) and the ecology of nectar intake by Sociobiol. 37, 63–70. bee colonies in a tropical forest, Oecologia 61, 1–10. Nieh J.C. (2004) Recruitment communication in stingless bees (Hymenoptera, Apidae, Meliponini), Roubik D.W., Moreno J.E. (2000) Pollen specializa- Apidologie 35, 159–182. tion and generalization by stingless bees (Apidae: Meliponini), in: IBRA (Ed.), Proc. 6th Int. Conf. Nieuwstadt M.G.L. van, Sanchez L.A., Biesmeijer Apiculture in Tropical Climates, IBRA, Cardiff, J.C., Arce H.G., Sommeijer M.J. (1997) Foraging pp. 112–118. behavior of stingless bees: are their diets really so Roubik D.W., Wolda H. (2001) Do competing honey diverse? in: Mardan M. et al. (Eds.), Proc. Int. bees matter? Dynamics and abundance of native Conf. Tropical Bees and the Environment, Beenet bees before and after honey bee invasion, Popul. Asia, Univ. Pertanian, Malaysia, pp. 100–110. Ecol. 43, 53–62. Pedro S.R.M., Camargo J.F.M. (2003) Meliponini Roubik D.W., Moreno J.E., Vergara C., Wittmann D. neotropicais: O genero Partamona Schwarz, 1939 (1986) Sporadic food competition with the Afri- (Hymenoptera, Apidae), Rev. Bras. Entomol. 47, can honeybee: projected impact on neotropical 1–117. stingless bees, J. Trop. Ecol. 2, 97–111. Pessotti I., Lé’Sénéchal A.M. (1981) Aprendizagem Roubik D.W., Smith B.H., Carlson R.G. (1987) em abelhas. I- Discriminação simples em onze Formic acid in caustic cephalic secretions of espécies, Acta Amaz. 11, 653–658. stingless bee, Oxytrigona (Hymenoptera: Api- Ramalho M., Kleinert-Giovannini A., Imperatriz- dae), J. Chem. Ecol. 13, 1079–1086. Fonseca V.L. (1989) Utilization of floral Roubik D.W., Yanega D., Aluja S.M., Buchmann resources by species of Melipona (Apidae, S.L., Inouye D.W. (1995) On optimal nectar Meliponinae): floral preferences, Apidologie 20, foraging by some tropical bees (Hymenoptera: 185–195. Apidae), Apidologie 26, 197–211. Ramalho M., Kleinert-Giovannini A., Imperatriz- Schmidt V.M., Zucchi R., Barth F.G. (2003) A Fonseca V.L. (1990) Important bee plants for stingless bee marks the feeding site in addition to stingless bees (Melipona and Trigonini) and the scent path (Scaptotrigona aff. depilis), Africanised honeybees (Apis mellifera) in Apidologie 34, 237–248. neotropical habitats: a review, Apidologie 21, Schwarz H.F. (1932) Stingless bees in combat, Nat. 469–488. Hist. 32, 552–553. Ranger S., O'Donnell S. (1999) Genotypic effects on Seeley T.D. (1983) Division of labour between scouts forager behavior in the neotropical stingless bee and recruits in honeybee foraging, Behav. Ecol. Partamona bilineata (Hymenoptera: Meliponi- Sociobiol. 12, 253–259. dae), Naturwissenschaften 86, 187–190. Seeley T.D. (1995) The wisdom of the hive, Harvard Robinson G.E. (1987) Regulation of honey bee age University Press, Cambridge, Massachusetts. polyethism by juvenile hormone, Behav. Ecol. Sociobiol. 20, 329–338. Seeley T.D., Visscher P.K. (1988) Assessing the benefits of cooperation in honeybee foraging: Roubik D.W. (1978) Competitive interactions search costs, forage quality, and competitive between neotropical pollinators and africanized ability, Behav. Ecol. Sociobiol. 22, 229–237. honey bees, Science 201, 1030–1032. Seeley T.D., Kühnholz S., Weidenmüller A. (1996) Roubik D.W. (1980) Foraging behaviour of compet- The honey bee’s tremble dance stimulates ing Africanized honey bees and stingless bees, additional bees to function as nectar receivers, Ecol. 61, 836–845. Behav. Ecol. Sociobiol. 28, 277–290. Roubik D.W. (1983a) Experimental community Slaa E.J. (2003) Foraging ecology of stingless bees: studies: Time-series tests of competition between from individual behaviour to community Information flow and stingless bee foraging 157

ecology, Dissertation Utrecht University, The Apinae) in Trinidad, West-Indies, Apidologie 14, Netherlands. 205–224. Slaa E.J., Cevaal A., Sommeijer M.J. (1998) Flower Sommeijer M.J., de Bruijn L.L.M., van der Guchte C. constancy in Trigona stingless bees foraging on (1985) The social food-flow within the colony of artificial flower patches: a comparative study, J. a stingless bee Melipona favosa (F.), Behaviour Apic. Res. 37, 191–198. 92, 39–58. Slaa E.J., Tack A., Sommeijer M.J. (2003a) The effect Spaethe J., Weidenmüller A. (2002) Size variation of intrinsic and extrinsic factors on flower and foraging rate in bumblebees (Bombus constancy in stingless bees, Apidologie 34, 457– terrestris), Insectes Soc. 49, 142–146. 468. Spaethe J., Tautz J., Chittka L. (2001) Visual Slaa E.J., Wassenberg J., Biesmeijer J.C. (2003b) The constraints in foraging bumblebees: flower size use of field-based social information in eusocial and color affect search time and flight behavior, foragers: local enhancement among nestmates Proc. Natl. Acad. Sci. 98, 3898–3903. and heterospecifics in stingless bees, Ecol. Suka T., Inoue T. (1993) Nestmate recognition of the Entomol. 28, 369–379. stingless bee Trigona (Tetragonula) minang- Sommeijer M.J. (1984) Distribution of labor among kabau, J. Ethol. 11, 141–147. workers of Melipona favosa F.: age-polyethism Theraulaz G., Bonabeau E. (1995) Coordination in and worker oviposition, Insectes Soc. 31, 171– distributed building, Science 269, 686–688. 184. Thierry B., Theraulaz G., Gautier J.Y., Stiegler B. Sommeijer M.J., Beuvens F.T., Verbeek H.J. (1982) (1996) Joint memory, Behav. Proc. 35, 127–140. Distribution of labour among workers of Melipona favosa: construction and provisioning Thorpe W.H. (1956) Learning and instinct in animals, of brood cells, Insectes Soc. 29, 222– Methuen and Co., London. 237. Villa J.D., Weiss M.R. (1990) Observations on the Sommeijer M.J., de Rooy G.A., Punt W., de Bruijn use of visual and olfactory cues by Trigona spp. L.L.M. (1983) A comparative study of foraging foragers, Apidologie 21, 541–545. behavior and pollen resources of various stingless Wenner A.M., Johnson D.L. (1966) Simple condi- bees (Hym., Meliponinae) and honeybees (Hym., tioning in honeybees, Anim. Behav. 14, 149–155.

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