Buzz Pollination Is Aninteraction Between Beesand Flowers Introduction II

View metadata,citationandsimilarpapersatcore.ac.uk Vibrations and their effect pollenon release V. Characterising floral vibrations IV. Bee vibrations III. Buzz pollination is aninteraction between beesand flowers Introduction II. I. Summary Contents Accepted: 17 December 2018 Received: 12 November2018 Author* for correspondence. Telephone: +44 (0) 1786 467822. Email: [email protected] Scotland. FK9 Email: 4LA. [email protected] 1 Mario Vallejo-Marín flowers pollination: onBuzz beevibrations Studying Tansley insight This article isprotected by All copyright. doi: lead todifferencesbetween thisversionandthe been and through typesetting, thecopyediting, proofreading pagination This article has for accepted been Articletype :Commissioned Material DR MARIO VALLEJO-MARIN (Orcid ID : 0000-0002-5663-8025) The definitiveversionis availableat Accepted ArticleBiological and Environmental Sciences, School Naturalof Sciences, University of Stirling. Stirling, 10.1111/nph.15666 1, * publi – www.newphytologist.com Tansley Insight cation andcation r ights reserved. Version of Record. Please Version of unde rgone f ull pe er review buthaser not review pro cite cess, which may whichmay cess, this articleas provided byStirlingOnlineResearchRepository brought toyouby CORE I. This article isprotected rights by All copyright. reserved. summarise classic and recentwork buzzon pollination, a with particul complexof motor routines in (Mesquita‐Neto 1999) 2013) evolution flowerof form and function across disparateplant families includingorigin the and demise of complexfloral adaptations generally, buzz pollination provides the opportunity to investigatebasic evolutionaryquestions laboratory settings fieldboth morphologies the study of buzz pollination, from and pollinator as wellthe as behaviour of bees, influencethe release and collection pollen,of and ultimately stages understandingof howfloral a pollination being known for more thanhundred a years from flowers Buzz pollination is sonication,vibrations. Keywords: pollination release may bee ov vibrating the anthers pores slits.or Approximately 6% of Summary References Acknowledgements VII. VI.

erview of Accepted Article

Introduction morphology and behaviour influence , , the evolutionary biomechanics, , and ultimately bee and plantfitness Conclusions Measuring vibrations transmitted frombee the to the anther (Corbet Huang& balancebetween antagonistic and mutualistic interactions between plantsand pollinators

Bees, requires studyingbiomechanics the beeof vibrations and their transmission

studying vibrations produced by

incidentally fertilising

Extracting pollen from this type specialisedof flower is achieved

(Dellinger fitness the

et al. behaviour,

a type of pollination inwhich bees usevibrations to removeand collectpollen transmission of

(Russell

,behaviour a that flowering plant , 2018) (De Luca Vallejo &

et al. , 2014; Switzer Combes,& 2017; Mesquita‐Neto

et al.et , as well as bio , 2018) invertebrates

affectthe mechanics , 2016; Whitehorn those vibrations from the the evolutionary ecology pollenof rewards documenting the them nd bee characteristics,including their biomechanical properties

to characterising buzz pollination species

has evolved to to address - Marín, 2013) (Michener, 1962; Buchmann, 1983) mechanical properties ,

(Russell biotremology, .

possessflowers with anthers that open through b I

ees ees and theireffects pollen on release suggestunderstanding that the fundamental questions on learning and cognition

et al. repeatedly et al. macro . Recently, there hasbeen a surgeof interest in (Teppner, 2018) , 2017; Arroyo , 2016) evolution buzzof buzz pollination,floral evolution,

bee to the anther

( Dellinger among bees .

The goalThe thisof reviewis to of vibrations,of

(DeLuca & Valle ar emphasis howbuzz on

- ecology and Correa

, we are still at the early et al. .

et al.et

- Here I . Despitebuzz pollinated floral , 2018)

, thus mediating

(Larson & Barrett, evolution of most efficiently et al. and how , 2018)

providea brief behaviour in , 2018) , . I the jo

discuss how -

on flowers.on floral Marín, and convergent

. buzz More

small

traits plant pollen by

III. II. This article isprotected rights by All copyright. reserved. may differ in their generated 2014) behaviouralof contexts,including communication properties vibrationsof characteristicsBee including identity, species indiv B vibrations pollen on release. separate phenomena: (1)The production of vibrationsbees, by and (2) the effects of those captures aninteraction between bees and flowers representing theconfluence of tworelated but syndromeor ( reliance on vibration distinguish between the behaviour (producing vibrations flowers on Cardinal vibrations while visiting flowers has evolved repeatedly inthe evolutionary history of bees differenttypes of pollinated by vibration modification ofstamens the and as being associated with functional specialisation flowersof in which pollen releaseis restricted by rapidlyextract pollen tube,concealing pollen asinporicidal a anther, and bees vibrate thesecorolla tubes in some in addition to poricidal anthers species t vibrations to collectpollen from flowers with varied morphologies fliessome may also collect pollen pollenfor collection a particular type behaviourof Buzz pollination 2016; Mortimer, 2017) namely bioa methodological and conceptual developed tools for studying vibrations in other biological fields, invibrational a context, studies of buzz pollination can take advantage someof of the pollination. Becauseinteraction the betw pollination works ypically, theseflowers have poricidal anthers Accepted specee Article Buzz pollination is an interaction between bees and flowers Bee vibrations Although plantswith poricidal anthers areassumed to be commonlymost or exclusively , and (Buchmann, 1983)

species of et al.et

through thesame mechanism thoracicof musclecontractions pollen collection ies, morphology and behaviour affect behaviour and morphology ies, cousticsand substrate , 2018) buzz pollination describes , and flowers mechanical Pedicularis

(DeLuca Vallejo & - , butnot all bees can use vibrations to collect pollen producing t bees (Macior, 1968; Corbet Huang, & 2014) - to . producing bees

(King, 1993; Arroyo

provideframework a to study the vibrational component buzzof

(De Luca Vallejo&

an int across multipledifferent families

(Buchmann

, longitudinally

exhibited by some bees ) p , thereare other ways buildto buzz a

(for definitions seeSupplementary Materials S1) roperties eraction between

in somecase, other floral using vibrations - borne o o set seed - (Buchmann, 1983) Marín, 2013)

etal. . een flowers and during bees buzz pollination occurs ma animal For example, - Correa - - Marín, 2013; Russell al.,et 2017) dehiscent anthers are insidekept a narrow corolla , 1977) , which s communication

( (Buchmann plantswith characteristic floral morphologies idual size,and behaviour influencethe mechanical (Hrncir buzz

et al. . ,

are present Although although — - bee species pollinated plants b , 2018) ees

, beesuse vibrations to collectpollen from et al.et parts. . (Vallejo

Thus

arethe only animals

floral vibrations floral et al.

, 2008) more workneeded is todetermine if thesedifferent vibrations . Bees produce vibrations ina variety

(biotremology) in roughly 6% of , buzz (De Luca Vallejo & , 1977) - differin

- or or Marin pollinated flower. For example, , floral vibrations defence - pollinationbest is thought . Thus it is important to (Hrncir and), the pollination type .

et al.et Although use bees the . T

(De Luca . Buzz pollination heability to produce , 2010) frequenc

etal. (Hill Wessel, & that angiosperm

in orderto - Marín, 2013) , 2008)

usevibrations . ), the), Moreover,

etal. y are

(45 times; of floralof , they ,

and i nly

IV. This article isprotected rights by All copyright. reserved. substrate (King 1978; Arroyo the stiffness, mass and material properties offlower the (King, 1993) with the peak or dominant frequency Materials S1) definea “buzz”an as uninterrupted vibration, independently itsof duration De Luca Vallejo& vibrations can consist single a of continuous vibration lasting up to a couple of seconds or of F Bee vibrations: componentsborne (Figure 1A). buzzcase, pollination is a vibrational phenomenon characterisedboth by acoustic and substrate “floral vibrations” or “vibrations flowers”on (See Supplementary Material S1 forglossary). a maya be misleading term lesser extent thelegs head muscles extraction that sounda by is “acoustic turbulence” and anther vibrations Although, it previouslywas suggested that pollen releasewas the result of the combined vibrations while collecting pollen bee vibratesflower a Buzz pollination takesname its from the audible produced during floral visitation characteristics,including Switzer Combes,& 2016) unknown theextent to which this represents 2016) Whitehorn same plantspecies in experimental arenasindicate frequencythat the 2011; De Luca vibration amplitude(peak velocity) produceduring floral visitation. Co& produces vibrations vibrations Acceptedloral vibrationsrelatively are complex. Article Characterisingfloral vibrations mbes, 2017)

, 1993) (bees usually bitethe anthers whilevibrating, Russell

changesas anindividual beegains exper are transmitted to the flower via direct physical contact theof bee’s body including the -

borne vibrations theon flower e lastin (Buchmann, 1983; Cocroft & Rodriguez, 2005)

et al.et ven ven when visitingsame the plant . Thecharacteristics theof vibrations experienced byanthers the are . - The vibrations produced by bees flowerson can be . Correa

Floral vibrations contain etal. g fromfew a tens to , 2017) . - - Marín, 2013; Arroyo Yet,it product theof bee’s vibrations (Figure1A) which do notcontribute to pollen , 2013; Rosi with different

et al.et (Macior, 1964) (King, 1993)

oustic and substrate oustic and the magnitudeand duration of their floral

remains unclear what characteristics ofbee a influence the vibrations they . areWe still theat early stagesin understanding to whatextent bee morphology,

, 2018) when studied in the contextof pollen extraction

- Denadai Someevidence suggestthat bee sizeis positively associated with

and more workis needed in thisarea , and should from flowers is often called sonication

(Figure 1A). Thus frequency and duration when visiting different plant (De Luca . For this reason, thebehaviour in which bees produce hundreds of milliseconds , and - behaviour and learning, i a fundamental frequency Correa The vibrations produced by bees during collection, pollen

etal. (Figure1

multipleharmonics

(DeTar

et al.et species

associative , 2018) changeas bee the adjusts grip its onto the flower

et al. ienceat manipulating flowers, althoughis it still component

, 2013)

A -

, ) , 2018) et al.

borne components components borne , and b sonication (applying sound to agitate particles)

. Moreover, observations of bees visiting the (De Luca

, butnot with frequency , 1968) (DeTar learningthe by bee

oth canbeoth described with the samebasic (Figure 2). et al. .

, or “buzz”, thatcan heard be when a The vibrations

etal. (King, 1993; King Buc& of nfluencethe types of vibrations

, currentour understanding suggests et al.et , 2016)

characterised

(1 rapidlydecreasing 00 , 2014) , 1968; Buchmann & Hurley, - For clarity, itmay be useful to .

400 Hz)

vibrations (Morgan , thorax,abdomen, and to a

(Cardinal , and th , and itmay be be producedthe by thoracic

(Supplementary

(Russell

, which often coincides

acoustically as or

etal. (Russell also (Burkart

e samee et al.et multiple short

magnitude

, 2016; et al.

hmann, 1996; influenced by , 2018) taxa

e beespecies etal.

, 2016; et al.et ffects of

(Switzer st to use In any . ,

, - V. This article isprotected rights by All copyright. reserved. vibrating anthers, i but anther walls effects and amplitude through elasticcollisions kinet Buchmann, 1996) centrifugal forces on the pollen grains causing them to be expelled outof the apical pore pollen ejection W to the flower oscillation force with whichbee a vibrates depending the on acce is essential as v pollination requires measuring of two these variables Supplementary Materi Hz and acceleration in ms related to each ot Denadai variable interestof (bee size or pollen release), depend will howamplitude on is expressed Supplementary Materials S2 becausethese different measurements amplitudeof are not (VA),peak acceleration amplitude(AA) necessa Because a per simple sinusoi (Supplementary Materials S1) and methodology to characterise the vibrations producedb by A major challengein currentstudies buzzof pollinationto is achieveconsistency inthe terminology F correlated from acoustic or substrate 2017) properties, particularly intheir energy transferto a substrate Nevertheless, the parameters of oscillatory movement (frequency, amplitude,dur requency and and requency Acceptedaree still Article

second, Hz there isthere no direct evidencefor this yet. Vibrations and ic energy transmitted . For instance, t , it has, it been suggested that electrostatic ry thatthe In sinusoidal simple motion,

etal. mplitude (Figure 3) between in

mayalso play a significantrole in expelling from pollen anthers

(Buchmann & Hurley, 1978)

, 2018) dal the early stages ) and) . velocity ibrations of the samefrequency have may drastically differentconsequences for the Theoretically,

. waves( her acoustic and substrate n principle, In variable described analysedor can be quantified using

. This in turn change will force the of the substrate acoustic and plant amplitude amplitude amplitude . hefrequency . Buchmann and Hurley

K al S of theof vibrations experienced antby the nowing . Box 1

- Here, 2 theireffect on pollenrelease 2 - ) allow) from the internal walls theof vibrating antherand borne components,borne but ). )

, and thus, the relationship between amplitude Thus a

the acceleration theof anther tip during vibrations should create

the of

) Vibrations can be characteriseddecomposing by (the magnitude of change sinusoidalof motion) , which can be the absolute magnitude of pollen ejection isfunction a of

understanding the mechanism by which floral vibrations result in s

accumulation of kinetic energy, cent

are and duration estimating the other two (

full characterisation of the vibrations observed during buzz peak - borne or needed to characterise vibrations characterise to needed - . borne vibrations

velocity, accelerat peakdisplacement amplitude (DA). This isalso important

Although stillwe lackfull a model of pollen release in velocity, a ’s

(1978) components described interactions between the pollen grains and the of beevibrations is the

clearly

model cceleration displacementor (King Buchmann, & 1996) leration, velocity and displacement theof amplitude by their

do not necessarily sharethe same two (De Luca , specified, e.g., peak velocity amplitude

ion, displacement and pollen is expelled asresult a of equally related to frequency e.g., (Cocroft& Rodriguez, 2005; Mortimer,

eesand transmitted toflowers anthergeometry of theseof her. ation)

are of theof vibrationpoorly is velocity and displacement) (See equency (

In addition to these mechanical et al.et

accurately estimated either

(Cocroft - rifugal forcesand borne vibrations transmitted variables ( , 2018)

, frequency (Corbet & Huang, 2014) e.g.,

the grains pollen

et al.et (Sueur, 2018) . Full characterisation

them . andfrequency the number cyclesof

(Sueur, 2018) e.g., frequency in

frequency , 2006)

into a sum of

and a ,

(King & perhaps, (Figure 3 . (Rosi the .

are

it is - ; , VI. This article isprotected rights by All copyright. reserved. v structur related plant speciesdiffer in theircapacity to transmitvibrations differentparts of the same flower andamplitude the (acceleration) subsof However, characteristics vary over therelatively shortdistances between the antherand otherfloral parts aboutknown the material properties flowersof inthe context of vibrations structures the material prop sensor path between the (De Luca Measurementsusing either laser vibrometry or accelerometersare usually not taken onanthers the vibromet buthave the disadvantage addingof a the calyx accelerometersattached to another part theof flower, during natural pollination is anthers whilevibrating the flower measurement theof anthers’ movementcomplicated is asthebee partially or en velocity displacementor amplitude) when a bee vibrates a flower is technically challenging. Direct 2018) While estimating the frequency beeof floral buzzesis relatively straightforward effect pollen on release (e.g., frequency), may not besufficient to describethe force being transmitted to the anther influen (negativeassociation) includedwas ascovariate a velocity as amplitude(positive association) accelerationor amplitude r displacement) Intriguingly,a recent playbackstudy found that amplitude(measured acceleration as stronger, positive effect on release pollen during artificial vibrations release frequencies produced by pollenmuch than vibrations of 400 Hz pollen release vibrations. electrostaticinteractions could jointly contribute to theexpulsion of pollen grains elationship Acceptedibrations Article Empirical studies suggestthat the characteristics of thevibrations applied to the anthers affec Measuring v , measuring th

ced by multiple characteristics theof vibration, andstudying that one variable isolation” “in (King, 1993; Gibson Cocroft,& 2018) (De Luca al properties theof flowerare important in mediating the transmission of substrate

et al.et ers (Arroyo

available (Arroyo

connecting the anthers to therest theof flower

of pollenof release can measure

, 2013) (King Buchmann,& 1996) is

positively etal. - erties flowers of and their Correa - vibrati Correa

worksuggests that e magnitudeof the vibrations experienced by the anthers (e.g., acceleration, . This addsvariable a to the measurements,namely the structural transmission ibrations

, 2013) (Rosi .

on source et al. some

movement etal. associated with - Denadai practically . In contrast, peakvelocity amplitudean with frequency depended whether on the , 2018) , 2018) bumblebees (24 (King, 1993; Arroyo (Buchmann, 1983)

(thebee) transmitte

etal. . Accelerometers can measure movement with high precision, without .

(Harder& Barclay, 1994)

mass mass toflower the difficult flowers indeed dampen vibrations even shortover distance . A trate , 2018)

rtificial vibrations pollen releasein . architecture

, The structural transmission path shoulda function be of

- theplant structure mass loading borne vibrations can vary significantly between . An indirectapproach 0 . - 405 Hz),frequency hasa modesteffect pollenon Theseresults d fromd ,

- and measuring the vibrations the on bee itself Correa e.g. , includingcharacteristics the theof

(Cocroft

(DeTar

(King Buchmann, & 2003) the pedicel Solanumlycopersic

between the

et . indicate

al. However, w of interest

suggesting that the material and

etal. bee to et al.et , 2018) (De Luca d duration have consists of 450

, 1968) (King & Buchmann, 1996)

, 2014) amplitude that pollen releaseis jointly . Interestingly, - 1000 Hz removetwice as

or howor vibration (the anther) the the ithin the range of

et al.et . . um To date, In contrast, (De Luca using tirely coverstirely the anther following ,

, 2013) of the vibration but

, . a m

velocity or the littleis and even closely

uch etal. .

- laser bee

borne

the and its ,

or or t s , VII. This article isprotected rights by All copyright. reserved. Cocroft RB,Rodriguez RL. 2005. Cocroft RB,Hamel Cardinal S, Buchmann SL, Russell AL. 2018. Burkart A, LunauSchlindwein K, C. 2011. Buchmann SL Buchmann SL, Hurley JP. 1978. Buchmann SL 1983. Arroyo References in mystudies plantof reproduction. 2018 insightful commen discussions I Acknowledgements predictivefield. thehave opportunity to take buzz pollination from an initial discovery phase Cocroft, 2018) development in the young biotremologyfield of vibrational properties plantof structures King, 1993) pioneering work bee characteristics will require, developing understanding our the of evolutionary biomechanics of buzz pollination.first The area testing evolutionary theorieson the evolution and adaptive significance buzzof pollination, and (2) evolution buzzof pollination, however, Overlast the

Accepted Articlethank Conclusions - 235 for - Paul DeLuca Correa B, Beattie CE, Vallejo Bioscience Communication solutions. In: Cocroft RB, Gogala HillM, PSM, Wessel A eds. behavior usedby bees (Anthophila). neotropical bees. (Solanaceae) inSouthern California USA. Theoretical Biology Experimental Pollination Biology the vibrations experienced by flowers during buzz , and P. De Luca, Callin Switzer, Stephen Buchmann and two anonymous reviewers for , with a profoundmore understanding of among other things,estimation the of thefitness consequenceof different floral and years support , Jones, CE, Colin LJ. 1977. . By integratingareas the of animal behaviour, floral evolution and

ts an on earlierdraft. Iam grateful to the , preferablyunder field , 55 J,Su Q, Gibson J 2014.

wehave made

buzz pollination , Buzz pollination in angiosperms. In: Jone . This Avery R (4): 323 . Heidelberg: Springer, Journal of Pollination Ecology paper

ussell - 334. (4): 639

Biophysical model for buzz pollination inangiosperms.

The behavioral ecology

i s

, large dedicated to SpencerBarrett Patricia Nunes

- biomechanics Marin M. 2018. - 657.

two areas that Vibratilepollination of

. NY: Scientific. NY: and Academic Editions, advancesin studying the

(Arroyo

Comparativebioacoustical studies on flighta Vibrational playback experiments: challengesand realisticconditions. The second will require bridging the

The evolution floralof sonication,pollen a foraging Evolution

249 (Hill Wessel,& 2016; Mortimer, 2017; Gibson & - Wasmann Journal ofBiology Correa - - (DeTar Silva 274. bee vibrations

Bee andBee floral traits affect thecharacteristics of

72 are

6 and Jeremy Gibson for of insect vibrational communication.

et al. (16): 118 (3): 590

etal. still pollination. Leverhulme Trust s CE, LittleRJ eds.

, 2018)

in their infancy Solanumdouglasii , 1968; Buchmann Hurley, & 1978;

- for i for 600. biomechanics, - 124. (e.g., Hrncir Studying Vibrational , whicha is nspiration

bioRxiv

to a more mature,

: doi:: 10.1101/494690. are 35 Research G

73 stimulating Handbookof

, advice etal. topic (1): 1 ecology and biomechanics, : - and

113. (1) (1) , 2008)

- Solanumxanti experimentally underrapid 25.

nd buzzing of Journal of

and support rant RPG

and

we -

This article isprotected rights by All copyright. reserved. AcceptedKing MJ, Buchmann SL. 2003. King MJ, Buchmann SL. 1996. King MJ. 1993. Hrncir M, GravelSchorkopf AI, Schmidt DLP, VM, Zucchi R, Barth FG. 2008. Hill PS,Wessel A. 2016. Harder LD, Barclay RMR. 1994. Gibson JS, Cocroft RB. WR,DeTar Haugh C, Hamilton1968. J. Dellinger AS, Chartier M,Fernández‐Fernández Penneys D, DS, Alvear M, AlmedaMichelangeli F, ArticleDe Luca PA, Vallejo De Luca PA, Giebink N,Mason Papaj AC, D, Buchmann 2018. SL. De Luca PA, Cox DA,Vallejo De Luca PA, Bussiere SoutoLF, CorbetSA, Huang S Cocroft RB,Shugart Konrad HJ, KT, Tibbs K. 2006. of theKansasEntomological Society Xylocopa Functional Ecology 49. Experimental Biology associated with flightbut not thoseassociated with sound production. stinglessbees ( Controlled pollen removal from 221 and sampling strategies in a complexsensory environment. induceto pollination. doi.org/10.1111/nph.15468 from anadaptiveplateau lead to new StaedlerFA, Y, Armbruster WS,Schönenberger J. 2018. significanceof buzz 10.1080/09524622.09522018.01511474. International Journal ofAnimal Sound and Its Recording characterize properties of bee (Anthophila) floral sonication vibrations? Naturwissenschaften bumblebees indicates species Oecologia in bumblebee pollination buzzesaffects quantity the of pollen released from flowers. 114 it does involve vibration insectfor vibrational communication.

(8): 1665 (6).

Buzz foraging mechanism b of , butnot

172 - - Marín M. 2013. Q. Q. 2014. - 1674. (3): 805 2018. Melipona seminigra

Biotremology. Apis

10 - - pollination.

Marín2014. M.

Vibration

Buzz pollination in eight bumblebee 101 211 (4): 449 Transactionsof theASAE - Floral sonicationbees: by Mesosomal vibra Sonication dispensing of pollenfrom 816. (Hymenoptera Apidae), : ejects from pollen poricidal anthers. -

Vilaros D, Goulson D, Mason AC, Vallejo The functionalThe significanceof poricidal anthers and - induced triboelectriccharging pollen of grains? (4): 331 (5): 678

What's the ‘buzz’about? The ecology and evolutionary - - 456. - specific and context

Current Biology guided mate searching intreehoppers: directional accuracy Acoustically forced vibration greenhouseof tomato blossoms Current Opini Dodecatheon - - 338. 685.

): resonances of thethorax influence vibrations

Comparison pollinationof and defensivebuzzes in umble bees. Ethology

pollination syndromes.

(2): 295

Variation inplant substrates andconsequences its on inPlantBiology .

Functional Ecology -

26 11 112 305. (5): R187 (5): 731 Journal ofApicultural Research - dependent vibrations. (8): 779

: 1 :

Beyond buzz‐pollination

Howwell do acousticrecordings - - pollinated - 0735. - 14. doi:14. - Solanumlaciniatum R191. 789. Journal ofExperimental Biology NewPhytologist

- 16

Marín

tion by 8 (4): 429 (4): 509

Thoracic vibr Pedicularis Journal of

M. 2013. Bioacoustics Annals of Botany Bombus - - buzz pollination: 435. 517. .

flowers.

species: –

ations in and 32 Variability departures (1): 41 - Journal the

This article isprotected rights by All copyright. reserved. and studies suggestionspollination for it. standardising AcceptedSupporting Whitehorn PR, Wallace C, Vallejo Vallejo Teppner H. 2018. Switzer CM, Combes SA. 2017. Switzer CM, Combes SA. 2016. Sueur2018. J. Russell AL, Leonard AS, Gillette HD,Papaj DR. 2016. Russell AL, Bu Rosi ArticleMortimer B. 2017. Morgan T, Whitehorn P, LyeVallejo GC, Michener CD. 1962. Mesquita‐Neto JN, BlüthgenSchlindwein N, C. 2018. Macior LW. 1968. Macior LW. 1964. Larson BMH, Barrett SCH. 1999. - Denadai CA, Araujo PCS,Campos LAO,Cosme L, Jr., Guedes RNC. 2018. - Marin M, DaSilva SargentEM, RD, BarrettSCH. 2010. buzzbumblebees. pollination by significanceof heteranthery inflowering plants. Botanicae environmental conditions. 25 (bumblebee)s exp collection diverseon floral resources. release. Neotropical bees: genus information? InsectBehavior bumblebees that canfine be anthers. Functional Ecology complexinteraction networks 55 Botany ( Melastomataceae). (6): 1150 (8): 927 eriencein floral sonicationbees. by Information. Note chmann SL, Papaj DR. 2017.

Sound Analysisand Synthesis with R

51 Insect Science Revista BiologiaDe Tropical

The fi The (1): 96 - Pollination adaptation in Experimental study of floral ecology of 57

932. Biotremology: Do physical constraintslimit the propagation of vibrational -

1159. An interesting method pollenof collectingbees by from flowers with tubular (1 Animal Behaviour onication behavior when consumed at below doses the LD50. -

rst records of vibratory pollen 2): 135 29 - 108.

(2): 233

32 American Journal ofBotany

(10): 2 : 1 -

Bumblebee sonication behavior changes plant with species and neonicotinoidThe pesticide,imidacloprid, affects 141. -

- The pollination ecology of buzz dependent frequenciesand lackof optimal frequency for pollen 10. doi: 10.1111/1744 - -

Marin M. 2017. 241. Apidologie S1. S1.

321 - tuned with experience in manipulating flowers. —

Glossary

130 - Disentangling legitimate pollinators and illegitimate visitors. - 2332. Sci Rep Marin M. 2016.

Howa generalist bee achieves high efficiency pollenof : : 165 Pedicularisgroenlandica

Behavioral Ecology 48

Animal Behaviour (2): 167

7 - (2): 223

174. of terminology commonly used in buzz inbuzz of terminology commonlyused (1): 15562.

. TheNetherlands: Springer. Neonicotinoid pesticidelimits improvementin

Concealed floral rewards androle the of

Flowers with poricidal anthersand their collection by bees. - - 175.

7917.12602. - New Phytologis 86 233. Floral sonicationan is innate behaviour i Dodecatheon meadia

(4): 502

Traitcorrelates and functional - pollinated

28 120 - 511. (4): 991 .

American Journal ofBotany : : 83 t

188 - Phyton 91. Rhexia virginica - 1003. (2): 418

Buzz

. American Journal of - AnnalesRei Bombusimpatiens

- pollination in Ecotoxicology - Journal of 425.

This article isprotected rights by All copyright. reserved. during floralvisitation (e.g. 300Hz). However, a givenat frequency,amplitude the (e.g. peak canapplied be to the flower. Alargeand a small bee can achieve,in principle, the samefrequency Fig Correa the flower using a metallic pin, ( produced by overlap between windows howtheof frequency scales. Increased resolution atthe frequency level come a at cost decreasedof resol lengthwindow whichover the represent frequencies higheof vibrations (relativeamplitude, dB)across range a frequenciesof (0 dominant frequency ( a time. ( Oscillogram showing properties theof floral organs,well as asthe by way in whichbee a grasps the anthers. ( experienced in the anthers flower a of are also collection can consist aof series Fig vibrates along either the the rate pollenof from the bee to the anthers. In Buchmann theof anthersnegligible. is name (i.e. sonication or buzz pollination), the contribution theof acoustic component toshaking the which result inan audible includingpetals and the sepals and vibrations are transmitted to the anther cone flightmuscles cause cyclical deformation theof bee’s thorax, which resultin vibrations d vibrating the Fig parameter peak (peak displacement). velocity, acceleration or peak visualising waves from sinusoidal user Supporting d ). Amplitudeshown is in iagram showingsingle a poricidal anther (in yellow) and ) . . Accepted. . Article

The accelerationThe of the vibrations 2 1 3 to ato lesserextent the legs

Vibrations produced by bees of different Floral vibrations arerelatively complex. Vibration b

et al.et )

Frequency spectrum theof first vibration in the buzz (indicated vibration , 2018) Bombus terrestris audax anther cone (in yellow) of a Information. Note s

produced beeby a visiting buzz a release

and plotted in the changesthrough time. Herethe window size setwas to instantan c . 370 y f a - component .recording The rom the anther is proportional to the velocity with which

or or relative Pollen is expelled from the anthersbecause of the vibrations transmitted

z (1

eous ; ; window length 512= r amplitude. FFT - (5) recorded in an oscilloscopeat a sampling rate of Hz 5000 axes. – of of multiple short 3 . The vibratin

is calculated ) S2.

scale . changesin amplitude(measured as acceleration, m Vibrations are also transmitted to other

while visitingflower a of was R (sound

Interactive (Shiny application App) computing for and package . fundamentalThe frequency Solanum -

shown here provided of values frequency and o measured with anaccelerometer & The choice analysis of parameters, particularlythe

Hurley’s ; 6 ; The vibrations produced bybee a during pollen (4)

sizelikely differ inthe g bee transfersalso energy to thesurrounding air, affected , ). Although thissoundwhat is gives this behaviour its

determines the resolution ateither temporal or s by direct contact with the thor - vibrations eewave - pollinated flower. like flower with pori ) . (1978) representssample a of the vibrations (

c by the stiffness, andmass material )

three axesthree of vibration (

Spectrogram (Sueur, 2018)

( biophysical model of buzz pollination a

) Sol . The characteristicsof the vibrations anum citrullifolium - 2.5 kHz). Upper magnitude theof

in this vibration

cidal anthers. showing themagnitude of .

inside

panel: attached to the base of Lighter ( 128 partsof flower the

the ax, ne additional

samples x d ,

dashed head y iagram ofbee a the anther yellow ,

Lower (Solanaceae) z

). is also the (1) force that

s a ,

The indirectThe (Arroyo -

) 2 abdomen with 75% . These ) through)

lines

) panel: areas ution

in - , This article isprotected rights by All copyright. reserved. properties plantstructuresof is still littleunderstood in nature force boundaries perpendicular waves produced at the boundarybetween media which propagate in media includesRayleigh waves communication 2005) particle oscillationperpendicular is to the direction of wavepropagation 2017) Bendingform waves when rod geometriccontexts, and describewave propagation in three, twoand dimensions, one respectivel (Cocroft Rodriguez, & 2005; Mortimer, 2017) substrate properties, the medium thatsurrounds substrate, the and the type of vibration produced The magnitude a of vibrationaffected is damping by energyor loss, which isfunction a theof summation of simplesine waves,each themof with itsown magnitudeand frequency simultaneously 2017) Vibrations candescribed be the as oscillation aof particlearound anequilibrium position B = 2 vibrations of different peak displacements. between frequency and eitherpeak velocity ( in turn,force the that can betransmitted to the flower( harmonic vibrations. Changesin both acceleration theof vibration and mass of thebee change, will acceleration and pe increase indisplacement (specifically peakdisplacement) affect will the magnitudeof peak the small displa ox

Accepted Articleµ m. er

that is perpendicular to the plane propagationof . P . Bending wavesa are . Vibrations a on substrate have complexpatterns and contain multiplefrequencies cement) theof 1

bee

erpendicular waves are thoughtto bethe mostimportant waves insubstrate Properties of vibrations s (Hill Wessel,& 2016)

(Corbet Huang,& 2014) (Mortimer, 2017) (Cocroft& Rodriguez, 2005; Cocroft ak velocity of the vibration produced, asall these quantities arerelated in maximum (Mortimer, 2017) type of perpendicular waves,that is, waves where thedirection of - like structures, for example plant stems, are vibrated vibration

. Both Rayleigh and bendingdisplace waves particles with ashear . Thesesignals can be analysed by decomposing vibrations into a

dueto their

thatcan be produced . Rayleigh wave Solid line . Body, boundaryand bending waves form indifferent a ) peakor acceleration ( increased

et al. ,

peak displacementpeak (Hill & Wessel, 2016) f m= a x s are a mix longitudinalof and , 2006; Gibson Cocroft,& 2

thorax

(Cocroft Rodriguez,& 2005) shouldlarger be for ).

Lines in Lines

size b . For agiven frequency, an )

for , (Cocroft Rodriguez,&

D dicaterelationship the A simplesinusoidal . Thevibrational

= 4 µ m; dashed line bigger 018) (Mortimer, - borne (Sueur, 2018) , and (Mortimer

than .

for ,

D y. y. A , .

This article isprotected rights by All copyright. reserved. Accepted Article