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Potential application of the bumblebee foragingrecruitment pheromone for commercial greenhouse

pollinationMathieu Molet, Lars Chittka, Nigel E. Raine

To cite this version:Mathieu Molet, Lars Chittka, Nigel E. Raine. Potential application of the bumblebee foraging re-cruitment pheromone for commercial greenhouse pollination. Apidologie, Springer Verlag, 2009, 40(6), <10.1051/apido/2009034>. <hal-00892041>

Apidologie 40 (2009) 608–616 Available online at:c© INRA/DIB-AGIB/ EDP Sciences, 2009 www.apidologie.orgDOI: 10.1051/apido/2009034

Original article

Potential application of the bumblebee foraging recruitmentpheromone for commercial greenhouse pollination*

Mathieu Molet, Lars Chittka, Nigel E. Raine

Queen Mary University of London, Research Centre for Psychology, School of Biological and ChemicalSciences, Mile End Road, London E1 4NS, UK

Received 8 January 2009 – Revised 9 March 2009 – Accepted 11 March 2009

Abstract – Commercial bumblebee colonies are important crop pollinators. Here we assess whether ap-plication of artificial foraging recruitment pheromone can increase foraging activity in Bombus terrestriscolonies on a relevant timescale for commercial pollination. We measured bee traffic from the nest to aforaging arena, which is correlated with foraging activity under natural recruitment conditions. Duringcontinuous pheromone exposure bee traffic increased by 1.5 to 3.6 times, and this increase lasted up to105 minute. Repeated 20 minute exposures of a colony to recruitment pheromone, with at least 30 minutesintermissions, triggered consistent traffic increases over a four week period. We conclude that artificial re-cruitment pheromone can reliably boost bee traffic leaving previously inactive colonies. This method couldimprove foraging activity and pollination in greenhouse colonies, especially young colonies reluctant tostart foraging after introduction to the crop.

artificial recruitment pheromone / Bombus terrestris / chemical communication / crop yield / foragingactivity

1. INTRODUCTION

Bumblebees are important pollinators usedextensively for pollination of greenhouse com-mercial crops such as tomato, sweet pepperand avocado (Dasgan et al., 2004; RoldanSerrano and Guerra Sanz, 2006; Ish-Am et al.,1998; Velthuis and van Doorn, 2006). Com-mercial bumblebee nest-boxes contain an adlibitum artificial nectar reservoir to feed thecolony during transport from bee breederto crop grower. These nectar feeders re-main inside the colony even after they havebeen placed in greenhouses because manycrop plants, e.g. tomato, produce no nectar(McGregor, 1976). The reservoir in the nest-box provides the colony with nectar, thus thenumber of full honeypots is always high. Over-

Corresponding author: M. Molet,mathieu.molet@gmail.com* Manuscript editor: Jacqueline Pierre

feeding colonies with nectar in greenhousescould constitute a problem because it can de-crease overall worker motivation to forage,as shown in laboratory conditions by Moletet al. (2008). Indeed, in colonies with largenectar reserves stored in honeypots, successfulforagers make fewer excited recruitment runswhen they come back to the nest, and non-foraging workers are less responsive to nectarinflux to the honeypots as a cue to initiate for-aging (Dornhaus and Chittka, 2005).

Commercial bumblebee colonies are notprovided with pollen in their nest-box so theyhave to forage for this essential resource fromthe crop plants. In contrast to honeybees, anindividual bumblebee forager often collectsboth nectar and pollen during a single forag-ing trip; their propensity to focus on collectingone or the other resource is affected by supplyand demand (Plowright et al., 1999) and alsoenvironmental conditions (Peat and Goulson,

Article published by EDP Sciences

Pheromone promotes bumblebee activity 609

2005). Hence a reduction in motivation to for-age for nectar is also likely to affect pollen for-aging. Thus decreased motivation to exit thenest will probably lower rates of flower vis-itation, reducing pollination success and ulti-mately crop yield and quality. However bum-blebee breeders or glasshouse crop growerscannot limit food supplies to colonies with aview to increasing their motivation to foragebecause the risks of colony mortality by star-vation would be high since bumblebees onlystore a few days worth of food. Instead, grow-ers buy larger numbers of colonies than mightbe needed if bees were fully motivated to for-age.

The recruitment of non-foraging bumblebeeworkers by successful foragers returning to thenest with nectar relies on the release of a re-cruitment pheromone (Dornhaus et al., 2003).The major components of this pheromone (eu-calyptol, farnesol and ocimene) have beenshown to produce short term increases inforaging activity when applied singly (MenaGranero et al., 2005) or in combination (Moletet al., 2008). Although the effectiveness ofthis pheromone is reduced when colonies havelarge nectar reserves, applying the artificialpheromone (a combination of eucalyptol, far-nesol and ocimene) to such well-fed coloniescan increase the number of foragers by 60%and the number of foraging bouts by 40% dur-ing a 30 minutes period after pheromone ap-plication (Molet et al., 2008). These resultssuggest that artificial recruitment pheromonecould be applied to commercial colonies ingreenhouses to trigger an increase in foragingactivity.

Here we explored whether the artificialpheromone technique could be used to en-hance colony foraging activity over long pe-riods. We measured bee traffic from the nestto a foraging arena as a proxy measure of for-aging activity because traffic and actual forag-ing activity are correlated (Kwon and Saeed,2003; see discussion). Therefore, we testedthe efficiency of an artificial pheromone mix-ture at increasing bumblebee traffic over pro-longed periods during which colonies receivedeither extended continuous exposure or briefrepeated exposures to the artificial pheromone.

2. MATERIALS AND METHODS

2.1. Bumblebees

Across the three experiments, we used a total ofsix queenright Bombus terrestris dalmatinus (DallaTorre) colonies, supplied by Syngenta Bioline Bees(Weert, Netherlands). They were each housed in abi-partite wooden nest-box connected to a foragingarena (see Molet et al., 2008). Colonies were fedon ad libitum 50% sucrose solution (v/v) placed ina gravity feeder in the foraging arena, as well asdefrosted honeybee-collected pollen (Koppert B.V.,Berkel en Rodenrijs, Netherlands) added directly tothe nest every other day.

2.2. Measurement of bee traffic duringcontinuous pheromone exposure

In a first set of three colonies (colonies a–c),we recorded the movement of bumblebees from thenest to the foraging arena (traffic) using Ethom soft-ware (Shih and Mok, 2000). Ten minutes beforestarting each trial (i.e. one control phase followedby one test phase), the feeder was removed fromthe foraging arena to avoid successful foragers re-leasing recruitment pheromone when returning tothe nest. Traffic (i.e. the number of bees leaving thenest) was recorded during a 30 minute control phasebefore the artificial recruitment pheromone was ap-plied: a vial containing a mixture of 400 µL euca-lyptol + 400 µL farnesol + 400 µL ocimene per Lacetone, the three major bioactive components iden-tified by Mena Granero et al. (2005), was suspendedabove the nest. The solvent alone (acetone) was notused during the control phase as earlier experimentsby Mena Granero et al. (2005) indicate that ace-tone had no effect on traffic levels. The pheromonecould evaporate via a cotton wick (DE HealthcareProducts, Gillingham, UK). Each pheromone com-ponent was released into the nest at a similar rate tothose reported by Mena Granero et al. (2005), i.e.0.24 µL.h−1. Traffic was recorded for 120 minutes(test phase) after pheromone application. In total,traffic was thus recorded for 150 minutes: 30 min-utes control + 120 minutes test. The percentage offull honeypots in the nest was recorded as an indexof colony nutritional status.

2.3. Data analysis

Traffic data were divided into consecutive fiveminutes intervals: accordingly each trial consisted

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Figure 1. Effect of continuous exposure to the artificial recruitment pheromone on bumblebee traffic fromthe nest to the foraging arena for three colonies (colonies a–c). (a) Columns show mean (± 1 s.e., N = 8 tri-als) increase in traffic in each five minute interval relative to the traffic during the first five minutes interval.The arrow indicates when the pheromone vial was introduced inside the nest. White columns representperiods with no pheromone whereas grey columns represent periods during which a pheromone vial wassuspended above the nest. (b) Only trials in which the first 30 minutes of testing showed significantly higherlevels of traffic (based on t-tests) than during the 30 minute control phase were used, and these two valueswere used to compute the magnitude of the pheromone effect (which ranged from 1.5 to 3.6). Moving t-testscomparing the six intervals in the control phase to six contiguous five-minute test intervals were performedto determine the duration of the pheromone effect, which was defined as the central value of the movingsections (thick lines in the diagram). The maximum pheromone effect duration was 105 minutes, and theminimum was 40 minutes.

of a control phase of six five-minutes intervals,followed by a test phase of 24 five-minute inter-vals. Because we wanted to assess the duration ofthe pheromone effect, we used only those trials inwhich the pheromone elicited an effect at the begin-ning of treatment. This was determined by compar-ing the traffic levels recorded during the six controlintervals and the first six test intervals using a t-test(Fig. 1; t and P values are not reported here becausethis procedure is a tool to select meaningful data –i.e. if P > 0.05 there was no significant increase inbee traffic following pheromone application. Logi-cally, the duration of pheromone effect could not beassessed for trials in which there was no significantpheromone effect). The duration of the pheromoneeffect was determined by performing successivet-tests between the six control intervals and amoving window of six contiguous test intervals

(Fig. 1). We considered the pheromone effect tohave ceased when the t-test became non-significant.Finally, the magnitude of the effect was computedas the ratio of the mean traffic levels during thefirst six test intervals divided by the mean dur-ing the six control intervals (Fig. 1). We also per-formed standardised major axis linear regressions(Fairbairn, 1997) between the three variables: dura-tion of pheromone effect, magnitude of pheromoneeffect, and percentage of full honeypots (using(S)MATR 1.0 software developed specifically forthis type of analysis (Warton and Weber, 2002)).As this method takes into account the measure-ment error in both dependent and independent vari-ables it is more suitable than type I regression(which assumes that the independent variable iscontrolled by the experimenter and is thus error-free).

Pheromone promotes bumblebee activity 611

2.4. Measurement of bee traffic duringbrief exposures to pheromone

Traffic was recorded in a second set of threecolonies (colonies d–f) using similar methods, asabove (see Sect. 2.2.). Each trial started with a20 minute control phase, followed by the appli-cation of artificial recruitment pheromone for 20minute (time needed to reach maximal effect fol-lowing continuous exposure to pheromone, see Re-sults). The pheromone vial was then removed fromthe nest for either 30, 50 or 70 minutes, before be-ing replaced back above the nest for another 20 min-utes. Once again the solvent alone (acetone) was notused during the control phase and the ‘gap’ phase(between pheromone application phases) because ithas no activity (Mena Granero et al., 2005). Datawere divided into five minute intervals. In order totest the effect of the second application, we usedonly those trials in which the pheromone elicitedan effect during the first application, i.e. where themean traffic during the first four test intervals washigher than during the previous four control inter-vals. Statistical tests were not performed due to lowsample sizes; means were simply compared. Wemeasured the magnitude of the pheromone effectduring both first and second exposures as the ratioof the mean traffic levels during the four test inter-vals divided by the mean traffic during the four re-spective control intervals.

2.5. Effect of repeated exposuresto pheromone

In order to test whether repeated exposures topheromone could lead to colony habituation, i.e.a gradual decline in colony response with succes-sive applications, we assessed the effect on coloniesof receiving repeated brief exposure to recruitmentpheromone over an extended period (to do this, were-analysed the data collected in Sect. 2.4). Onlytwo of the three colonies were exposed to a suf-ficient number of trials that appropriate long-termdatasets could be obtained (colony d: 32 exposures– 16 trials with two exposures each – over 32 days;colony e: 14 exposures – 7 trials with two exposureseach – over 19 days; colony f was not included asonly 6 exposures – 3 trials- were performed). Allanalyses were performed using Statistica 7.1 (Stat-Soft, www.statsoft.com).

3. RESULTS

3.1. Bee traffic during continuousexposure to pheromone

The artificial recruitment pheromone pro-duced a significant increase in bee traffic fromthe nest to the foraging arena in eight trialsout of 13 (t-tests not reported, see methods,P-values for the 8 significant t-tests rangedfrom 0.0003 to 0.0063). This effect lasted for67.5±7.4 minutes (mean ± s.e.), and the trafficwas 2.7 ± 0.3 times higher during the first halfhour following pheromone application thanduring the half hour control (Fig. 1). There wasa delay of approximately five minutes follow-ing pheromone application before an increasein traffic was observed, and the increase lastedfor at least 40 minutes, and up to 105 min-utes. In trials where a significant effect wasdetected, the magnitude of the pheromone ef-fect ranged from an increase of 1.5 to 3.6 timescontrol traffic levels, and the effect magnitudedecreased with an increase in the percentage offull honeypots (Pearson correlation: r2 = 0.55,t7 = 2.69, P = 0.036; linear regression: mag-nitude = –0.038× percentage full pots + 3.58).There were no correlations between the du-ration of the pheromone effect and either thepercentage of full honeypots (r2 = 0.01, t7 =0.25, P = 0.81) or the magnitude of the effect(r2 = 0.28, t7 = 1.55, P = 0.17). Thus theduration of the pheromone effect on traffic ap-pears to be independent of both the amount ofstored nectar and how strongly non-foragingworkers respond to pheromone application. Inthe five trials in which the pheromone did notproduce any significant increase in bee trafficthe average number of nest-leaving events dur-ing the 30 minute control period was signifi-cantly higher (mean ± s.e. = 173 ± 29) thanfor the 8 trials in which pheromone applica-tion did elicit a significant increase in bee traf-fic (86 ± 16; t-test: t11 = 2.87, P = 0.015).

3.2. Bee traffic during brief exposuresto pheromone

The artificial recruitment pheromone pro-duced an increase in traffic in 28 trials. After

612 M. Molet et al.

removal of the vial from the nest, traffic beganto decrease until it returned to control levelsafter about 25 minutes (Fig. 2). In trials wherethe first exposure had been effective, the sec-ond (20 min) exposure to pheromone also trig-gered an increase in traffic, but this was con-sistently lower in magnitude than the responseto the first exposure (mean (± s.e.) increasein traffic: 1.94 ± 0.15 (first exposure) versus1.16± 0.11 (second exposure), pairwise t-test:t26 = 4.04, P < 0.001; Fig. 3). The magnitudeof response to the second pheromone applica-tion did not change with the time elapsed sincethe first application (General Linear Model(GLM) including exposure number and mag-nitude of the response to the first pheromoneapplication as continuous factors, and gap du-ration as categorical factor: gap duration effectF1,21 = 0.17, P = 0.84).

3.3. Bee traffic after repeated exposuresto pheromone

There was no effect of repeatedly exposingcolonies to artificial recruitment pheromoneon the magnitude of their response (Fig. 3;GLM including exposure number as continu-ous factor and phase – first or second exposure– as categorical factor: exposure number effectcolony d: F1,29 = 2.22, P = 0.15; colony e:F1,11 = 3.27, P = 0.10). This indicates that nosignificant habituation to artificial recruitmentpheromone occurred even over one month ofrepeated exposures. The slight trend towards adecrease in response (Fig. 3) can be explainedby the large increase in basal traffic levels ascolonies age and grow over the same period.As a result of colony growth, control trafficincreased by 3375% in colony d and 75% incolony e, leaving fewer bees available to be ac-tivated by the recruitment pheromone.

4. DISCUSSION

Continuous exposure of bumblebeecolonies to artificial recruitment pheromoneresulted in significantly increased bee trafficfrom the nest to the foraging arena for amaximum period of 105 minutes (mean

67.5 minutes) under laboratory conditions.This suggests that such a simple continuousapplication system would be inappropriateto produce durable, long-term increases intraffic in colonies used for commercial croppollination. However, we found that applyingthe artificial pheromone can elicit increasesin traffic of up to 3.6 times control levels,which shows that colony traffic can be given astrong boost for a short period of time usingartificial pheromone. This could be useful toinduce young or particularly inactive coloniesto start foraging, thus compensating for thepotentially detrimental effect of overfeedingwith artificial nectar.

Kwon and Saeed (2003) have shown ingreenhouses that the level of bumblebee trafficleaving the nest is correlated with actual lev-els of foraging activity on the flowers of hotpepper (Capsicum annuum L.), a crop that ex-hibits a very low nectar production. Moreover,Mena-Granero et al. (2005) have shown in thelaboratory that bumblebees leaving the nest asa result of artificial foraging pheromone stim-ulation indeed forage, i.e. collect nectar fromfeeders in the foraging arena. This is likely tobe true for our study as well. Thus, our studyprovides a first step in assessing the applica-bility of the artificial recruitment pheromoneto boost greenhouse pollination. Our resultssuggest that growers could achieve long-termimprovement of forager traffic by applying ar-tificial pheromones for short periods at reg-ular intervals, so that several boosts occureach day. Indeed we found that brief (20 min)pheromone applications were sufficient to trig-ger a maximal increase in traffic. Moreoverthe effect did not disappear immediately afterthe removal of the pheromone vial but fadedslowly (taking on average 25 minutes to re-turn to control levels). On average, a secondpheromone application, performed between 30and 70 minutes after the first, produced a15% ± 12% (mean ± s.e.) increase in traf-fic. Although the boost to traffic provided bythis second application is somewhat (around32%) lower than the first it is still effective.In addition, it is likely that, once foragershave discovered a profitable food source in thegreenhouse they will continue to forage longafter the effect of the artificial pheromone has

Pheromone promotes bumblebee activity 613

Figure 2. Effect of two brief daily exposures to the artificial recruitment pheromone on bumblebee trafficfrom the nest to the foraging arena, depending on the gap between exposures (top: 30 min, N = 18; middle:50 min, N = 5; bottom: 70 min, N = 5) in a second set of three colonies (colonies d–f; the data for thethree colonies are pooled). Columns show mean (± 1 s.e.) increase in traffic levels for each five minuteinterval relative to the activity during the first five minute interval. The black arrows indicate when thepheromone vial was introduced inside the nest and the white arrow indicates when it was taken out of thenest. White columns represent periods with no pheromone whereas grey columns represent periods duringwhich the pheromone vial was suspended above the nest. The introduction of the pheromone vial triggers alarge increase in traffic. Its removal leads to a gradual decrease in bee activity level. The magnitude of theresponse to the second exposure is lower than the first.

614 M. Molet et al.

Figure 3. Effect of repeated exposures to artificial recruitment pheromone over several weeks on bumble-bee traffic from the nest to the foraging arena in two colonies (colonies d and e). Each column shows themagnitude of increase in bumblebee traffic leaving the nest during a period of pheromone application com-pared to control activity period. Light grey (a) and dark grey (b) columns correspond respectively to the firstand second exposures to the pheromone in the ‘brief exposures’ experiment (second exposures generallyproduced a lower increase in traffic). The magnitude of the response to the pheromone does not decreasesignificantly with the number of repeated exposures. The potential trend towards a decrease in effectivenessof pheromone application at increasing bee traffic is due to an increase in the basal traffic level as coloniesage and grow in size over time (colony d: from 1 bout per five minutes during exposure 1a to 35 bouts dur-ing exposure 16b; colony e: from 8 bouts per five minutes during exposure 1a to 24 bouts during exposure7b). As greater numbers of bees are active during control phases, fewer bees can be recruited followingpheromone application.

disappeared, which will help maintain a highlevel of colony foraging activity through regu-lar releases of natural recruitment pheromoneinto the nest from successful returning for-agers. This effect could not be assessed in ourexperiments since they were unrewarding, i.e.there was no feeder in the arena during tests.Therefore, our experiments suggest that theefficiency of artificial pheromone may be in-creased if it were delivered in pulses separatedby gaps of at least 30 minutes. Automatic dis-pensers could be developed for such purpose.Importantly, the effect of the pheromone wasmaintained across repeated applications span-ning 19–32 days, which means that this treat-ment would be robust over the functional lifes-pan of colonies pollinating greenhouse crops.

Among continuous exposure experiments,only eight trials out of 13 showed a significantchange in traffic following pheromone appli-cation. During the unsuccessful trials, the lack

of response was mainly due to the high levelsof basal traffic during control phases. Accord-ingly, we were unable to produce any increaseby application of the artificial pheromone, be-cause all (or almost all) potential foragers werealready active. This confirms that using artifi-cial pheromone is particularly useful to trig-ger bee movement from the nest to the outsidewhen a colony is less active.

The recruitment pheromone is unlikely tobe the only factor involved in foraging recruit-ment in bumblebees. For instance, the excitedruns performed in the nest by successful for-agers involve bumping into and climbing overother workers (Dornhaus and Chittka, 2001),and these mechanical stimuli could also con-tribute to the recruitment of new foragers. Inaddition, we do not yet know whether pollenand nectar foraging rely on distinct recruit-ment mechanisms, or whether foragers decidewhich type of food to collect based solely on

Pheromone promotes bumblebee activity 615

individual assessments of pollen and nectarstores (Molet et al., 2008; Kitaoka and Nieh,2009). Further research on the mechanisms ofrecruitment may thus suggest new ways to pro-mote foraging activity and ultimately improvethe effectiveness of bumblebees as commercialgreenhouse pollinators.

ACKNOWLEDGEMENTS

We thank Syngenta Bioline Bees for supply-ing bumblebee colonies, Oscar Ramos Rodríguez,Daniel Stollewerk, Nazmeen Hussain and Eliza-beth Walker for help with experiments and colonymaintenance, and two anonymous referees for use-ful comments. This work was supported by a grantfrom the Natural Environment Research Council(NE/F523342/1).

Possibilité d’appliquer la phéromone de recrute-ment des bourdons à la pollinisation de culturescommerciales sous serre.

Bombus terrestris / communication chimique /butinage / phéromone recrutement / rendementrécolte / pollinisation appliquée

Zusammenfassung – Eine mögliche Anwen-dung des Hummel-Rekrutierungspheromons beider kommerziellen Bestäubung in Gewächs-häusern. Kommerziell erhältliche Hummelkoloni-en sind wichtige Bestäuber verschiedener Nutz-pflanzen. Diese Hummelkolonien werden jedochvon den Lieferanten mit grossen Nektarbehälternverschifft, und dieses Überangebot kann die Mo-tivation der Hummeln zur Sammeltätigkeit ein-schränken, was wiederum den Ertrag der Nutz-pflanzen beinträchtigt. Kürzlich wurde das Phe-romon identifiziert, welches Hummelarbeiterinnenzur Sammeltätigkeit stimuliert. Hier wird unter-sucht, ob eine künstliche Mischung der wesent-lichen Komponenten des Pheromons (Eukalyptol,Ocimen und Farnesol) die Sammeltätigkeit vonHummeln (Bombus terrestris) über Zeitskalen ver-bessern kann, wie sie für die kommerzielle Bestäu-bung angemessen sind. Die Aktivität der Koloni-en wurde gemessen, indem die Zahl der Arbeite-rinnen bestimmt wurde, die während eines Zeitin-tervalls das Nest verliessen, um eine Flugarena zuerreichen. Nistkästen mit sechs Kolonien von Bom-bus terrestris dalmatinus (Dalla Torre) wurden je-weils mit einer Flugarena verbunden. Die Bewegun-gen der Tiere vom Nest zur Arena wurden währendKontrollintervallen oder Tests unter Pheromonein-fluss quantifiziert. Im ersten Experiment wurde die

Dauer des Pheromoneffekts bestimmt, indem dieKolonien (nach einer Kontrolle von 30 Minuten oh-ne Pheromon) für 120 Minuten dem Pheromon aus-gesetzt wurden. Im zweiten Experiment wurde dieminimale Dauer bestimmt, die zwischen zwei Phe-romonexperimenten liegen muss, um beim zwei-ten Test noch einen messbaren Effekt zu erzielen(20 Minuten Kontrolle; danach 20 Minuten Phero-mongabe; danach 30, 50 oder 70 Minuten Pause,und schliesslich nochmals 20 Minutes Pheromon-gabe). Das zweite Experiment erlaubte uns, zu te-sten, ob die wiederholte Gabe des Pheromons überdie Dauer eines Monats zu einer Abnahme des Ef-fektes führt. Während der kontinuierlichen Phero-mongabe nahm der Hummelverkehr um einen Fak-tor von bis zu 3,6 zu, und diese Zunahme hielt fürbis zu 105 Minuten an (Abb. 1). Die wiederhol-te Gabe des Pheromons war effektiv, sogar wenndie Pause zwischen zwei Tests nur 30 Minuten be-trug. Der Effekt der zweiten Pheromongabe war je-doch im Mittel 32 % niedriger als der der ersten(Abb. 2). Die wiederholte Stimulierung der Kolonieüber mehrere Wochen führte nicht zu einer Abnah-me des Effekts (Abb. 3). Unsere Studie legt nahe,dass das künstliche Pheromon verlässlich die Akti-vität von inaktiven Hummelkolonien steigern kann,besonders bei jungen Kolonien, bei denen der Ak-tivitätsbeginn manchmal verzögert ist. Es bleibt je-doch zu zeigen, das solche Aktivitätssteigerungentatsächlich den Nutzpflanzenertrag verbessern.

Synthetisches Rekrutierungspheromon / Bom-bus terrestris /Chemische Kommunikation / Ern-teertrag / Sammelaktivität

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