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Pulsed Mass Recruitment by a Stingless Bee, Trigona Hyalinata

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Pulsed Mass Recruitment by a Stingless Bee, Trigona Hyalinata 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 bee communication has focusedon the ability ofthe highly social bees,stingless bees (Hymenoptera,Apidae, 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 is highly 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;stingless bee; 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 ofnest-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 an experi- 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 conspecificsand interspecifics on rich food elucidated. sources( Johnson& Hubbell 1974, 1975; Roubik 1980; Our studytherefore had twogoals: (i) todeterminethe Johnson1981). Trigonahyalinata is oneof the most mechanismsunderlying recruitment in T.hyalinata , and aggressive ofthese species. It is foundthroughout 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),in the state of Sa˜oPaulo,Bra- zil,during the spring of 2001.To investigate the 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 on prominentleaves elevated above the substrate. Wetested newcomerorientation 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 anatural 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 oneto 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 tested the 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 on the 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
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