Received 13February 2003 Accepted 10 June 2003 Publishedonline 28August 2003

Pulsedmass recruitmen tbya stinglessbee, Trigonahyalin ata James C.Nieh 1* ,Felipe A.L.Contrera 2 and PauloNogueira-Neto 2 1Section ofEcology, Behavior, and Evolution,Division ofBiological Sciences, University ofCalifornia San Diego, MC#0116,9500 Gilman Drive,La Jolla, CA 92093,USA 2Laborato´riode Abelhas,Departamento de Ecologia,Instituto de Biocieˆncias, Universidade de Sa˜o Paulo, Sa˜oPaulo05508-900, SP, Brazil Researchon communication has focusedon the ability ofthe highly social ,stingless bees (,, Meliponini) andhoneybees (Apidae, Apini), tocommunicate food location to nest-mates.Honeybees can communicate food location through thefamous waggle dance.Stingless bees are closely related tohoneybees and communicate food location through avariety ofdifferent mechanisms, many ofwhich are poorly understood.We show that astinglessbee, Trigonahyalinata, usesa pulsed mass-recruitmentsystem that ishighly focusedin time andspace. Foragers producedan ephemeral, polar- ized,odour trail consistingof mandibular gland secretions.Surprisingly, theodour trail extendedonly a shortdistance away from thefood source, instead of providing acompletetrail betweenthe nest and the foodsource (as has beendescribed for other stinglessbees). This abbreviated trail may representan intermediate strategy betweenfull-trail marking, foundin somestingless bees, and odour marking ofthe foodalone, found in stinglessbees and honeybees. Keywords: recruitment;; foraging; polarized shortodour trail

1. INTRODUCTION recruitmentmechanisms used by suchaggressive foragers are poorly understood. Stinglessbees live in competitive environmentsin which Odourorientation plays amajor role in meliponine foodresources are highly soughtafter, and they exploit recruitment.Stingless bees can orient tofloral andlocale theseresources with strategies ranging from solitary forag- odours(Slaa et al. 1998) andcan assist forager orientation ing tothe mass recruitment of nest-mates ( Johnson1980; by odourmarking theresource alone (Nieh 1998; Agui- Johnson& Hubbell 1987). Stinglessbees employ amatch- lar &Sommeijer 2001; Jarau et al. 2002; Hrncir et al. ing diversity ofrecruitment communication strategies, 2003; Nieh et al. 2003) or odourmarking theresource ranging from odourcommunication to the potential com- andusing odour trails that extendfrom theresource to munication ofresource location through soundsproduced thenest (Lindauer & Kerr 1958; Kerr 1973; Johnson& insidethe nest (Lindauer & Kerr 1958; Esch et al. 1965; Hubbell 1974; Hubbell &Johnson1978; Schmidt et al. Biesmeijer et al. 1998; Nieh &Roubik 1998; Aguilar & 2003). Meliponineodour trails consistof odour droplets Bricen˜o2002; Slaa et al. 2003). The aggressive defence placedevery fewmetres to form atrail leading from the andattack ofgood food sources is akey elementin meli- nestto the indicated resource and can be up to 900 m ponineforaging competition (Roubik 1980, 1982), andis long (Kerr 1960). Odourtrails are thought toprovide thought toplay asignificant role in theevolution of meli- additional guidanceto groups ofrecruitsled by anexperi- ponineforaging strategies (Kerr 1960, 1969; Johnson encedforager (Lindauer& Kerr 1958; Kerr 1972, 1973; 1974; Johnson& Hubbell 1974, 1987; Roubik 2002). Kerr et al.1981). However,the extent of these trails, the Several speciesof stingless bees such as T.fuscipennis , spatial distribution ofodourdroplets and the influence of T.silvestriana , T. williana and T.hyalinata readily attack suchtrails onforager orientation have notbeen clearly anddisplace conspecifics and interspecifics on rich food elucidated. sources( Johnson& Hubbell 1974, 1975; Roubik 1980; Our studytherefore had twogoals: (i) todeterminethe Johnson1981). Trigonahyalinata isone of the most mechanismsunderlying recruitmentin T.hyalinata , and aggressive ofthese species. It isfound throughout South (ii) todetermine the role ofodourtrails in therecruitment America, andlives in large coloniesof up to 40 000 for- system of T.hyalinata . agers. Moreover,its aggression is notlimited tofood sources. A T.hyalinata colonywill attack stinglessbee col- oniesup to200 maway from its nest(P. Nogueira-Neto, 2. MATERIALAND METHODS personal communication).Roubik (1980) reportedthat T. (a) Measuring recruitment andthe frequency hyalinata wouldattack andcould successfully displace ofodour marking other stinglessbee species and a small colonyof African- Weconducted these experimentsat the FazendaAretuzina izedhoneybees from rich foodsources. However, the (21°26.4329 S, 047°34.9109 W),inthe state of Sa˜oPaulo,Bra- zil,during the spring of 2001.To investigatethe recruitment communicationsystem of T.hyalinata ,we trainedindividually markedforagers to asimulateddense flower patch (Johnson *Authorfor correspondence ([email protected]). 1981),a grooved-plate feedercontaining a rich2.5 M scented

Proc.R. Soc.Lond. B (2003) 270, 2191–2196 2191 Ó 2003 TheRoyal Society DOI10.1098/ rspb.2003.2486 2192J. C.Niehand others Stinglessbee pulsed mass recruitment sucrosesolution (100 m lof aniseextract perlitre of solution, agers to odour-mark the ropefor 30min.In the test phase, we McCormick& Co.Inc.) located 146 m SWofthe nest (method removedthe originaltraining feeder, sealed it inside a plastic of von Frisch1967). The controland experimentalfeeders were bag, and set out two identical,clean feeders, 10 mto the left identicaland containedthe samequantities of scented2.5 M and right of the traininglocation. We then movedthe distalend sucrosesolution. However, we immediatelycaptured all bees ofthe markedrope to oneof the cleanfeeders and attached an landingon the controlfeeder to eliminaterecruitment to the identicalbut unmarked ropeto the other cleanfeeder. We controlfeeder. We marked each visiting bee with an individual attached the proximalends of both ropes to the sametripod and combinationof paint marks on the thorax. Wemonitored the thus formeda V-shaped ropearray. Wealternated the position visitingforagers each15 minand allowedonly 10 individually ofthe markedrope from trial to trial. markedforagers to feed.We captured all other foragers with aspirators and didnot releasethem. Thus foragers werenot mul- (d) Thespatial distribution of odour marks tiply counted. To determinethe spatial distributionof odourmarks, we Anewcomeris aforager fromthe subjectcolony who has not intersectedtwo perpendicularcrossed ropes at the training previouslyvisited any feeder(Biesmeijer & deVries 2001). To feeder.From the feeder,the ropes extendedfor 100m inthe determinewhether foragers visitingthe feedercame from the directionof the nest,20 minthe other threedirections. Three subjectcolony and weremotivated by recruitersto findthe food observersrecorded the locationand sequenceof allodour marks source,we countedthe numberof newcomersarriving after we depositedon the ropes to an accuracyof 0.5m. eliminatedrecruitment by capturing allforagers. Weconducted threehour-long controltrials on threeseparate days. Stinglessbees deposit odour trails by preferentiallyplacing (e) Testingthe polarity ofthe odour trail odourmarks onprominent leaves elevated above the substrate. Wetestednewcomer orientation within the trailby providing They willalso odour mark leavesplaced on an elevatedrope, achoicebetween the trainingfeeder and an identicalcontrol creatinga trailwith odourmarks spacedalong the rope,as they feederlocated within the trailbut 20mcloserto the nest.The areon a natural substrate (Lindauer& Kerr1958; Kerr et al. trailextended 27 maway fromthe feederin the directionof the 1963).To study the odourtrail, we thereforeattached a100m nest,as determinedby the maximumextent of odourmarking ropeleading from the feedertowards the nest and fastened on the rope(see § 3). leavesat 1mintervalsalong the rope(method of Lindauer& Kerr1960). We attached leavesat 1mintervalsto allropes used (f ) Testingmandibular glandextracts inourexperiments. This techniqueallows one to movestingless Severalstingless bee species use mandibular gland pheromone beepheromone trails by shifting the locationof the rope. to odour-mark food sourcesand to createodour trails (Kerr et Observersfollowed odour-marking beesand recordedmark al. 1963; Blum et al. 1970).We observed T.hyalinata foragers locationsto the nearest0.5 m. appearing to odour-mark by brieflylanding and rubbing their To analysemarking behaviour indetail, we digitallyvideo- mandiblesagainst the substrate. Wetherefore extracted and taped foragers depositingodour marks onaleafattached to the testedthe attractiveness of T.hyalinata mandibulargland phero- feeder,and analysedthe video(30 frames s 2 1)ona Macintosh mone. iBookcomputer with iM ovie software. Wepreparedextracts by using plasticbags to carefullycapture non-alarmedforagers leavingthe feeder,chilling the bees,and (b) Testingthe attractiveness of odour marks dissectingout the mandibularglands. Wecrushed three glands depositedon the resource in1.5 ml of hexane (tostandardize extract concentration),and Wetested the attractiveness of putative odourmarks ina stored0.5 ml ofthe extract inasealedcentrifuge vial at 220 °C paired-feederassay. Weoffered newcomers a choicebetween untilthe beginningof the bioassay, when we attached and two identicalclean feeders. Around each feeder, we placeda openedthe tube onthe sideof afeeder.Control vials contained ringof filterpaper: onepaper that had beenputatively marked 0.5ml ofhexane and werehandled and storedin the sameway, by foragers for 60min,and onethat foragers had not contacted. but didnot containmandibular gland pheromone. Weplacedfeeders 1 mto the right and to the leftof the original During the collectionand test phases, we usedtwo cleanfor- feedingsite and capturedbees as soon as they landed.During ceps,one to handlethe test filterpaper and oneto handlethe odourbioassays, we immediatelycaptured all bees as soon as controlfilter paper. Wekept asupply of severalclean glass feed- they landedon afeederand onlycounted individual choices erson hand. Onceused, we washed the forcepsand test feeders madein the absenceof other bees.We exchanged the control inastrong detergent,rinsing thoroughly with hot water followed and experimentalfeeder positions at 1minintervals to eliminate by two washes of 95%ethanol. We air-dried all apparatus for sitebias (total trialtime of 5min)and discontinuedthe bio- at least3 hbeforereuse. Even without washing, this time-inter- assays when the winddirection was not parallelto the feeder- val ismore than sufficientfor any odourmarks to completely to-nest axis and thus couldhave biasedforagers to visitone evaporate (seefigure 4). The experimenterwore disposablelatex feederover the other. During the trials,such windconditions gloves duringall feeder choice experiments and whilewashing occurredtwice for intervalsof ca.15mineach. glassware. Aftereach trial, we discardedthe gloves and allpaper and plasticitems used in the trial. (c) Testingthe attractiveness of the odour trail To test the attractiveness of the odourtrail, we performed aV-shaped ropeexperiment with the leaf-bedeckedropes. We (g) Statisticalanalyses attached oneend of a50mrope(the nest-proximal end)to a We use the x 2-test to determinethe significanceof the recruit- tripod 96mfromthe nest.We attached the distalend of the mentcontrol trials. In two-feeder experiments, we calculate ropeto afeeder146 m fromthe nest.The ropepointed directly probabilitiesfrom a two-tailed binomialdistribution with towards the nest.In the odour-collectionphase, we allowedfor- p = q = 0.5.

Proc.R. Soc.Lond. B (2003) Stinglessbee pulsed mass recruitment J.C.Niehand others 2193

(a) 40 30

s 30 e t e n b u 15 f o c o

r 20 e b

0 m u 0 40 80 120 160 n 10 time from start of trial (min) (b) 0 160 trial 1 2 3 4 p < 0.00010.0004 0.026 0.009

Figure 2. Attractiveness of odours deposited byforagers on )

n thefeeder. Feeder choice experiment. Black bars, previously i 120

m visited feeder; open bars, clean feeder. (

e s l u p

t therope andfeeder. Foragers didnot land onany other n e 80 substrate.The putative odour-marking behaviour con- m t i sistedof a forager landing for 1.35 ± 0.66 s(s.d.)while u r c

e rubbing her mandibles for 0.66 ± 0.64 sagainst the r

f substrate.In 57% oflandings, foragers also rubbedtheir o 40

e tonguesagainst thesubstrate for 0.13 ± 0.06 s (n = 32 m i t observations).

0 (b) Testingthe attractiveness of odour marks depositedon the resource 0 40 80 120 160 Significantly more newcomerschose the feeder with the time of odour-marking pulse (min) forager-marked filter paper in all trials (figure 2; two-tailed binomial probability, pooleddata, two-tailed binomial Figure 1. Temporal synchronization of recruitment and probability, p 0.000 01, fourtrials, n = 118 newcomers). odour marking. ( )Recruitment occurs in pulses (trial 1, a Thusforagers ¿ evidently depositedattractive odourmarks 10.00 start time, n = 231 newcomers). Black barsshow the number of recruits. Open barsshow intervals of forager onthe feeder. odour marking. ( b)Timing of major recruitment pulses is tightly linked to odour deposition. Start(open circles) and (c) Testingthe attractiveness of the short odour stop (filled circles) times of recruitment and odour-marking trail pulses are plotted. Datafrom fivetrials. Linear regression Wenexttested the attractiveness of odour marks onthe line shown: r2 = 0.98, p , 0.0001. Scalebar, 5mm. rope with theV-shaped rope experiment. Asignificant majority ofnewcomers (61 –94%) chosethe feeder linked tothe forager-marked rope over thefeeder linked tothe 3. RESULTS unmarkedrope within thefirst 15 min (pooleddata, two- (a) Measuring recruitment andobserving odour tailed binomial probability , p 0.000 01, five trials, marking n = 244 newcomers).Thus forager-deposited ¿ odour marks Foragers recruitedin large pulsesin which over 100 onthe rope couldalso guidenewcomers to a feeder. newcomerscould arrive within a15 –20 min interval (five trials, 3heachtrial; figure 1 a).Nonewcomers arrived (d) Thespatial distribution of odour marks oncethe marked foragers werecaptured during three Unlikeprevious descriptionsof stingless bee recruit- hour-long controltrials conductedover 3days,although menttrails, theseodour marks didnot form atrail leading asignificantly greater numberof newcomers had arrived theentire distance from thenest to the food source in an equal time-period immediately beforeeach forager- (Lindauer& Kerr 1960). Instead,the marks extendedonly removal trial (threetrials, x2 = 8, 1 d.f., p < 0.005). New- ashortdistance from thefood source. We therefore call comerarrivals thereforedecreased significantly oncewe this formation ashortodour trail. Whenwe centred removedthe foragers at thefeeder. Based upon these crossedropes on the feeder, foragers laid mostmarks in results,we countedunmarked foragers asnewcomers from thenest direction and occasionally depositedmultiple oursubject colony. marks during asingle marking run(figure 3 a,b). The The largest recruitmentburst was 201 newcomersin marks formeda decreasingconcentration gradient 11 min. In addition,foragers landedand deposited puta- extendinga maximum of27 mfrom thefeeder (three tive odourmarks onthe feeder and rope during large trials; figure 3 c). recruitmentbursts. The start andstop times of major recruitmentpulses (more than onenewcomer per min) are (e) Testingthe polarity ofthe short odour trail highly correlated with thestart andstop times ofthe puta- Becausethe concentration gradient polarizes theshort tive odourmarking (figure 1 b).Foragers landedonly on odourtrail, it may allow newcomersto determine the cor-

Proc.R. Soc.Lond. B (2003) 2194J. C.Niehand others Stinglessbee pulsed mass recruitment

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0 10 20 30 40 (m) –1 0 1 2 3 4 5 6 7 8 9 time (min) (c) Figure 4. Mandibular gland extracts attract foragers toland and to begin feeding from 7to 20 min after deposition. Inset (m) showsdissected mandibular gland (m) attached to a 0510 15 20 25 30 mandible (scale bar, 1mm). Thegraph shows the results of Figure 3. Short, polarized odour trail created byrecruiting three trials. foragers. (a)Crossed-ropes experiment. Odour marks (n = 81) are most concentrated atthe food source (0 m), and recruitersmay have guidedrecruits from thenest and decrease in number in thedirection of thenest. Area of circles corresponds to thenumber of marks. Isoclines give assistedfinal recruit orientation with ashort,polarized thepercentage of markswithin setdistances. ( b)Deposition odourtrail. This shortodour trail extendedonly ashort sequence of multiple marksduring individual marking runs distancefrom thefood source instead of providing acom- on crossed ropes. Initial markshown asa circle. Arrows plete trail betweenthe nest and the food source. The indicate subsequent marks. Pathsvertically displaced to show stinglessbee Scaptotrigonapostica also depositsa polarized themarking pattern better. ( c)Maximumextent of short odourtrail (Kerr et al. 1963). However,most previously odour trail ( n = 103 marks). reportedstingless bee odour trails have extendedfrom the nestto the food source (Lindauer & Kerr 1958; Kerr et rectendpoint. Significantly more newcomerschose the al. 1963, 1981). Kerr &Rocha (1988) reportedpotential training feederin all polarity-test trials (six trials, pooled odour-marking behaviour that may have createda short data: p 0.000 01, n = 75 newcomers).Thus newcomers odourtrail in Meliponarufiventris and M.compressipes , but preferred¿ to land in theregion ofhighest pheromone it is unclearwhether the potential marks wereattractive mark concentration. tonest-mates. Mandibular gland volatiles serveas alarm odoursin (f ) Testingmandibular glandextracts honeybeesand many stinglessbee species (Cruz-Landim Usingthe paired-feeder assay, we presentedthe equival- 1967; Collins et al. 1989). Trigonahyalinata recruitersevi- entof onemandibular gland in hexane at theexperimental dentlyuse mandibular gland secretionsto create the short feederand a hexane blank at thecontrol feeder. From 0 odourtrail toguide nest-mates. Chemical analysis ofthe to8 min,newcomers attacked the extract vial by hovering odourmarks is necessaryto confirm their identity,but the andbiting thevial lip. Newcomersdid not land andfeed depositionbehaviour is characteristic ofstinglessbee man- until after 8min had passed.From 8to20 min,they dibular gland marking, andmandibular gland extracts showeda strong preferencefor landing andfeeding on the attracted foragers andexhibited asimilar decaytime to experimental feederover thecontrol feeder (60 –91% on natural odourmarks. Mandibular gland pheromonemay theexperimental, threetrials, two-tailedbinomial prob- also releasean aggressive responsein T.hyalinata , as it ability, p = 0.0003, n = 273 newcomers;figure 4). Attrac- doesin other highly social bees(Cruz-Landim 1967; tionto the mandibular gland extract thuspersisted for Williams 1982; Collins et al. 1989). Trigonahyalinata is 12 min, correspondingwell tothe15 min period in which knownto be an aggressive speciesthat attacks anddis- thenaturally depositedshort odour trail influencednew- placesother speciesat foodsources (Roubik 1980). comerchoice. Recruitednest-mates were drawn to the highest concen- tration ofodourmarks, andthus mandibular gland phero- monecould enable foragers todraw in reinforcements 4. DISCUSSION precisely wherethey are mostneeded to take over arich Our experiments reveal that T.hyalinata foragers can foodsource. recruit alarge numberof nest-mates in recruitmentpulses Food-sourcecompetition may bean important factor in that are highly focusedin time andspace (figure 1 a): 10 stinglessbee evolution ( Johnson1974; Johnson& Hubbell foragers recruitedup to 201 newcomersin 11 min. 1974, 1987; Hubbell &Johnson1978; Slaa et al. 1997). Becauserecruiters and newcomers arrived in large groups, Several stinglessbee species are reportedto forage

Proc.R. Soc.Lond. B (2003) Stinglessbee pulsed mass recruitment J.C.Niehand others 2195 aggressively, andelements of thepulsed mass-recruitment Hubbell, S.P.&Johnson, L.K.1978 Comparative foraging system—mandibular gland marking ofresources, massive behavior of six stingless bee speciesexploiting astandardized recruitmentand aggressive attacks at andthe defence of resource. Ecology 59,1123–1136. rich resources —are foundto varying degreesin theMeli- Jarau, S., Hrncir, M., Zucchi, R.&Barth, F.G.2002 Foot ponini (Kerr et al. 1963; Blum et al. 1970; Roubik 1980). print pheromones used to markfood sources bystingless bees. In XIVInt. Congr.IUSSI: the Golden Jubilee Proceedings Someaggressive speciesappear tospecialize in discovering (ed. J.Billen), p. 16. Sapporo, Japan: Hokkaido University andexploiting goodfood sources found by other bees Coop. (Johnson1974; Hubbell &Johnson1978; Nagamitsu & Johnson, L.K.1974 The role ofagonistic behavior in the foraging Inoue1997). Thus,it ispossible to view theprecise spatial strategies of Trigona bees.Berkeley, CA:University of Califor- andtemporal communicationoffered by theephemeral, nia. shortodour trail in an alternative light: crypsis.An Johnson, L.K.1980 Foraging strategies and thestructure of extended,consistently renewed odour trail offersa more stingless bee communities in CostaRica. In Proc.1st Int. conspicuoustarget than atemporary, shortodour trail Symp. organized bythe International Union forthe Study of (Bradbury &Vehrencamp 1988; Ho¨lldobler &Wilson Social and the Sociedad Mexicana de Entomologia , vol. 1990). The workof Kerr et al. (1963) suggeststhat some 2(ed. P.Jaisson), pp. 31–58. Cocoyoc, Morelos, Mexico: meliponine species, Scaptotrigonapostica and S. xantho- Centre Re´gional de Publications de la 5e`meCirconscription tricha,candetect and use interspecific odour trails. Thus du C.N.R.S. Johnson, L.K.1981 Effectof flower clumping on defense of anabbreviated trail may beless conspicuous to foraging artificial flowers byaggressive stingless bees. Biotropica 13, competitors,and may representan intermediate strategy 151–157. betweenpoint-source marking ofthe resource alone and Johnson, L.K.&Hubbell, S.P.1974 Aggression and compe- full-trail marking from theresource to the nest. tition among stingless bees: field studies. Ecology 55, 120– 127. Theauthors thankSantiago Ram ´õ rez, EdaF. L.R.A.Patricio Johnson, L.K.&Hubbell, S.P.1975 Contrasting foraging and VeraL. Imperatriz-Fonseca for their assistance. Thecom- strategies and coexistence of two bee specieson asingle ments of three anonymous reviewers substantially improved resource. Ecology 56,1398–1406. our manuscript. Financial support camefrom theHeiligenberg Johnson, L.K.&Hubbell, S.P.1987 Defenseof food supply Chair Endowment atUCSD and FAPESP of Brazil. byeusocial colonies. Am. Zool. 27, 347–358. Kerr, W.E.1960 Evolution of communication in beesand its REFERENCES role in speciation. Evolution 14, 326–327. Kerr, W.E.1969 Some aspectsof theevolution of social bees. Aguilar, I.&Bricen˜ o, D.2002 Sounds in M.costaricensis Evol. Biol. 3, 119–175. (Apidae: Meliponini): effect of sugar concentration and nec- Kerr, W.E.1972 Orientac¸a˜opelo sol em Trigonaspinipes . Cieˆn. tar source distance. Apidologie 33, 375–388. Cultura (Suppl.), 341–342. Aguilar, I.&Sommeijer, M.2001 Thedeposition of anal Kerr, W.E.1973 Sun compassorientation in thestingless excretions by foragers (Apidae: Meliponinae): favosa bees, Trigona (Trigona) spinipes (Fabricius 1793) (Apidae). behavioural observations concerning thelocation of food Anais Acad.Bras. Cie ˆn 45, 301–308. sources. Apidologie 32, 37–48. Kerr, W.E.&Rocha, R.1988 Comunicac¸a˜o em Melipona rufi- Biesmeijer, J.C.&de Vries, H.2001 Exploration and exploi- ventris e Melipona compressipes . Cieˆn. Cultura 40,1200–1203. tation of food sources bysocial colonies: arevision of Kerr, W.E.,Ferreira, A.&Simo˜esde Mattos, N.1963 Com- thescout-recruit concept. Behav. Ecol. Sociobiol. 49, 89–99. munication among stingless bees—additional data Biesmeijer, J.C., vanNieuwstadt, M.G.L.,Lukacs,S. & (Hymenoptera: Apidae). J.NYEntomol. Soc. 71, 80–90. Sommeijer, M.J.1998 Therole of internal and external Kerr, W.E.,Blum, M.&Fales, H.M.1981 Communication information in foraging decisions of Melipona workers of food sources between workers of Trigona(Trigona) spin- (Hymenoptera: Meliponinae). Behav. Ecol. Sociobiol. 42, 41 107–116. ipes. Rev. Bras.Biol. , 619–623. Blum, M.S., Crewe, R.M., Kerr, W.E.,Keith, L.H., Garri- Lindauer, M.&Kerr, W.E.1958 Die gegenseitige Versta¨ndi- son, A.W.&Walker, M.M.1970 Citral in stingless bees: gung bei den stachellosen Bienen. Z.Vergl.Physiol. 41, isolation and functions in trail-laying and robbing. J. Insect 405–434. Physiol. 16,1637–1648. Lindauer, M.&Kerr, W.E.1960 Communication between Bradbury, J.&Vehrencamp, S.L.1988 Principles ofanimal theworkers of stingless bees. Bee World 41,29–41, 65–71. communication .Sunderland, MA:Sinauer. Nagamitsu,T. &Inoue, T.1997 Aggressive foraging of social Collins, A.M., Rinderer, T.E., Daly,H. V., Harbo, J.R.& beesas a mechanismof floral resource partitioning in an Pesante, D.1989 Alarm pheromone production bytwo Asian tropical rainforest. Oecologia 110, 432–439. honeybee (Apis mellifera ) types. J.Chem.Ecol. 15, 1747– Nieh, J.C.1998 Therole of ascent beacon in thecommuni- 1756. cation of food location in thestingless bee, Melipona panam- Cruz-Landim, C.da 1967 Estudo comparativo de algumas ica. Behav. Ecol. Sociobiol. 43, 47–58. glaˆndulas dasabelhas (Hymenoptera, Apoidea) erespectivas Nieh, J.C.&Roubik, D.W.1998 Potential mechanismsfor implicac¸o˜esevolutivas. Arq.Zool. Sa ˜o Paulo 15, 177–290. thecommunication of height and distance byastingless bee, Esch,H., Esch,I. &Kerr, W.E.1965 Sound: an element com- Melipona panamica . Behav. Ecol. Sociobiol. 43, 387–399. mon to communication of stingless beesand to dances of Nieh, J.C., Ram ´õ rez, S.&Nogueira-Neto, P.2003 Multi- thehoney bee. Science 149, 320–321. source odor-marking of food bya stingless bee, Melipona Ho¨lldobler, B.&Wilson, E.1990 The .Cambridge, MA: mandacaia. Behav. Ecol. Sociobiol. (In thepress.) TheBelknap Press of Harvard University Press. Roubik, D.W.1980 Foraging behavior of competing African- Hrncir, M., Jarau, S.,Zucchi, R.&Barth, F.G.2003 Onthe ized honeybees and stingless bees. Ecology 61, 836–845. origin and properties of scent marksdeposited atthe food Roubik, D.W.1982 Theecological impactof nectar robbing source bya stingless bee, Melipona seminigra Friese 1903. beesand pollinating hummingbirds on atropical shrub. Apidologie (In thepress.) Ecology 63, 354–360.

Proc.R. Soc.Lond. B (2003) 2196J. C.Niehand others Stinglessbee pulsed mass recruitment

Roubik, D.W.2002 Tropical bee colonies, pollen dispersal, M.J.1997 Foraging strategies of stingless bees(Apidae, and reproductive gene flow in tropical trees. In Modeling and Meliponinae): therelation between precision of recruitment, experimental reseach ongenetic processes in tropical and temperate competition and communication. Acta Horticult. 437, 193–197. forests (ed. B.Degen, M.D.Loveless& A.Kremer), pp. 31 – Slaa,E. J., Wassenberg, J.&Biesmeijer, J.C.2003 Theuse 41. Belem, Brazil: EMBRAPA. of field-based social information in eusocial foragers: local Schmidt, V.M., Zucchi, R.&Barth, F.G.2003 Astingless enhancement among nestmatesand heterospecifics in sting- bee marksthe feeding site in addition to thescent path less bees. Ecol. Entomol. 28, 369–379. (Scaptotrigona aff. deplis). Apidologie 34, 237–248. von Frisch, K.1967 The dance language and orientation ofbees . Slaa,E. J., Cevaal, A.&Sommeijer, M.J.1998 Floral con- Cambridge, MA:Belknap Press. stancy in Trigona stingless beesforaging on artificial flower Williams, I.H.1982 Chemical communication in honeybees. patches:a comparative study. J.Apicult. Res. 37, 191–198. In Honeybee biology (ed. J.B.Free), pp. 139 –147. Ilford, Slaa,E. J., Nieuwstadt, M.G. L.v., Pisa, L.W. &Sommeijer, Essex:Central Association of Bee Keepers ’ Publications.

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