Will climate change affect insect pheromonal communication?

Will

climate

change

affect

insect

pheromonal

communication?

Antoine

Boullis

,

Claire

Detrain

,

Fre´de´ric

Francis

and

Franc¸ois

J

Verheggen

Understandinghowclimatechangewillaffectspecies

interactionsisachallengeforallbranchesofecology.Wehave

onlylimitedunderstandingofhowincreasingtemperatureand

atmosphericCO2andO3levelswillaffect

pheromone-mediatedcommunicationamonginsects.Basedonthe

existingliterature,wesuggestthattheentireprocessof

pheromonalcommunication,fromproductiontobehavioural

response,islikelytobeimpactedbyincreasesintemperature

andmodificationstoatmosphericCO2andO3levels.Weargue

thatinsectspeciesrelyingonlong-rangechemicalsignalswill

bemostimpacted,becausethesesignalswilllikelysufferfrom

longerexposuretooxidativegasesduringdispersal.We

providefuturedirectionsforresearchprogrammes

investigatingtheconsequencesofclimatechangeoninsect

pheromonalcommunication.

Addresses

1_{EntomologieFonctionnelleetEvolutive,GemblouxAgro-BioTech,} Universite´ deLie`ge,2PassagedesDe´porte´s,5030Gembloux,Belgium 2

Serviced’EcologieSociale,Universite´ libredeBruxelles,Campusdela Plaine,BoulevardduTriomphe,1050Brussels,Belgium

Correspondingauthor:Verheggen,Franc¸oisJ.(fverheggen@ulg.ac.be)

CurrentOpinioninInsectScience2016,17:87–91

ThisreviewcomesfromathemedissueonGlobalchangebiology EditedbyVladimirKosˇta´landBrentJSinclair

http://dx.doi.org/10.1016/j.cois.2016.08.006 2214-5745/#2016ElsevierInc.Allrightsreserved.

Introduction

Sincethe19thcentury,theatmosphericconcentrationof greenhousegases,particularlycarbondioxide(CO2),have

drastically increased causing changes to environmental parameters at aglobal scale, including temperature [1]. Recentstudiesnowhighlighttheimpactofsuch modifica-tionsonthewholedynamicsoflife[2].Throughcascade effects,entireecosystemsarebeingdisturbed,impacting thepopulationdynamicsofinhabitingspeciesandaltering theways thatthey interactwithoneanother. This phe-nomenon has been well documented for insect–plant

interactions mediated by plant secondary metabolites [3,4].

Communication between insectsrelies mainly on semi-ochemicals,whichareorganicmoleculesinvolvedinthe chemical interactions between organisms [5]. They in-cludepheromones(intraspecificcommunication)and alle-lochemicals (interspecific communication). Pheromones have a variety of important roles, especially related to foraging, aggregation or sexualbehaviour[6].Using be-haviour-changing pheromones (named releaser phero-mones) iscentral tointegrated pest management(IPM) [7],so predictingthe impactof climate changeon IPM programmes depends on understanding the impact of changesinrelatedabioticparametersoninsect pheromon-alcommunication.However,fewstudieshavefocusedon how changes in climate will disturb each stage in the pheromonepathwayfromemitterstoreceivers(Figure1).

A

pheromone’s

long

journey

Biosynthesis

Most insect pheromones are synthesised de novo and secreted in specialised glandular tissues, regulated by variousenzymaticactivities[8,9].Othersaresequestered and/orderivedfromdietaryprecursorsanddependonthe nutritive qualityof thediet. Elevatedtemperatures will likelyhavepronouncedeffectsonpheromone biosynthe-sis. Because insectsare ectothermicand poikilothermic, changingtheirbodytemperaturewillinfluenceenzymatic activities [10], andimpactpheromonebiosynthesis both quantitatively and qualitatively. For example, tempera-ture modifies the ratio of compounds in the sex phero-mone of the potato tuber worm moth Phthorimaea operculella [11]. Moths (Lepidoptera:Heterocera) differ-entially use the same precursors to synthesise different pheromone components, thanks to a wide variety of enzymes (i.e. oxidase, desaturases, reductase), allowing specificrecognition[12].Althoughtheseinsectscan per-ceiveawiderangeofpheromonecomponents,the activa-tionofneuronsintheirmacroglomerularcomplexes,and the elicitationof relevantbehaviouralresponses,is com-binatorial:itwillhappenonlywhentherightcombination andratioofcomponentsisperceivedatthesametime[6].

Developmentaltemperaturehasastronginfluenceonadult lifehistory,morphology,andphysiology.Furthermore,in some species, pheromone production and availability is

dependentonlarval,pupation,and/oradultdevelopmental conditions[8,13,14],hencetheeffectofabioticparameters on all the insect life stages is important. In the male beewolf, Philanthus triangulum, an increase of 58C in thelarvalrearingtemperatureledadultmalestoproduce morepheromonalsecretions[13].Moreover,warmer rear-ingconditionsledtohigherrelativeamountsofcompounds withhighmolecularweight.Asaconsequence,ashiftin temperature could weaken intraspecific relationships of theseinsectspeciesbyreducingtheefficiency(i.e. speci-ficity,activity,timingofproduction,etc.)oftheirchemical communication.

IncreasingatmosphericCO2concentrations[1]couldalso

affectthebiosynthesisofinsectpheromones.Changesin CO2concentrationsaffectplant biochemistry,including

thesynthesisof secondarymetabolites [4].Sincesome phytophagous insect species produce their pheromone components based on precursors taken from their host plant,wehypothesisethatphytophagousinsectscouldbe among the most vulnerable to changes in atmospheric CO2concentrations, through cascade effects of CO2on

plantchemistry [15,16].InHolomelina spp.moths, leu-cineisthestartingmaterialforsexpheromoneproduction [17]. In bark beetles, while pheromones are produced primarilyde novo mainly through the mevalonate path-way,someaggregationpheromonecomponentsarisefrom thehydroxylationofhosttree-derivedsecondary metab-olites[18].

Emission

Fewstudieshavespecificallyinvestigatedhowchangesin temperature and atmospheric gas composition act on pheromone release. In themoth Striacosta ablicosta, in-creaseinaveragetemperaturedoesnotaffectthecalling behaviour of females, while an increasing variation be-tween photophase and scotophase temperatures alter significantlythisbehaviour,asalsoobservedin Phyllonor-ycterjunoniella [19]. Ladybirdlarvae deposit more long-chained hydrocarbons — used as oviposition deterring pheromone—whenexposedtorisingtemperature[20]. An increase in atmospheric CO2concentration reduces

theemissionrateof thealarmpheromoneinpea aphids (Acyrthosiphonpisum)(Boullisetal.,unpublished).

Signaldispersal

After pheromone release by the emitter, volatile pher-omonesmaybealteredbyoxidativegasessuchasozone ontheirwaytothereceiver.Mostpheromonesaresimple, lipophilicand of low molecular weight, which facilitate theirlong-distancedispersalintheair.Otherpheromones are heavier molecules, including semi-volatile phero-monesandcuticularhydrocarbons(CHC),whichareused inshort-rangeorcontactcommunication[6].Like phyto-genic volatile organic compounds (VOCs), insect pher-omones made of unsaturated terpenes may be decomposedbyozone[21–23].Similarterpenesare con-stitutive of sexual, aggregation or alarm pheromones in several insect taxa, such as ladybirds [24,25], aphids

Figure1 2 3 Emission Biosynthesis Dispersion 4 Perception 5 Behavioural response 1

Current Opinion in Insect Science

Intraspecificchemicalcommunicationininsectsmaybesubdividedintofivestepsthatareprobablyimpactedbymodificationstoatmospheric gascompositionandassociatedraiseinambienttemperature.GraphicartbyCarolinaLevicek.

[26,27],barkbeetles[28]andfruitflies[29].As highlight-ed for Drosophilamelanogaster,terpenes couldlose their biological activity after short-term ozone fumigation at environmentally-realistic concentrations (ranging from 40 to 120ppb) [30]. The lifespan of trail-pheromones andalarm-pheromones,whichactinashorttimewindow and small spatial scale [31,32], may thus be further reduced in an ozone-rich atmosphere. In addition to the effect of ozone on pheromones, temperature acts onthevolatilityof semiochemicals.Inthecaseof pher-omones dispersed over long distances such as sex or aggregationpheromones,temperaturechangesmay mod-ifytheshapeofscentplumesanddisturbtheefficiencyof insects toreachtheirtarget[33].

Increased temperature may also alter heavy molecules, suchascuticularpheromonesinvolvedincontact recog-nition. Because of their low volatility,temperature will likely more affect the chemical composition of phero-monal blends (ratios of components). Insects’ cuticular lipidsexistinasolidstateatambienttemperatures,but they can partially melt upon contact with the animal’s surface(withhigherthanambienttemperature),which,in turn, induces modifications in the ratios of cuticular composition [34].Asobservedin D.melanogaster,a48C increase of ambient temperature changes cuticular hy-drocarboncomposition,whichleadtosexualisolationand affectthestabilityofecologicalcommunities[35].

Perception

Pheromoneperceptionoccursthroughacomplexseriesof events, starting when pheromones enter the sensilla lymph and ending at brain processing [36–38]. Very few data are available on how environmental changes willimpactpheromoneperception,butonerecentstudy showedthatthesexpheromoneperceptionwasalteredin malemoth Caloptilia fraxinellaunderelevated tempera-ture[39].

Becauseinsectsarepoikilotherms,changesintheirbody temperaturemayaltertheaffinitybetweenapheromone and itsbindingprotein(PBP) thattransports this mole-cule through the sensillumlymph to olfactory receptor neurons.InApismelliferaandA.cerana,ASP1actsasPBP thathasagoodaffinitytothequeenmandibular phero-mone [40]. However, increasing temperature weakens the van derWaals and hydrogenbonds established be-tweenthequeenmandibularpheromoneandPBP,which impliesthatbindingaffinitybetweenthesemoleculescan belessened, inducingareduced efficiency ofthesignal transportation troughthehydrophiliclymph[41].

Behaviouralresponse

Althoughinsectresponsestopheromonesareinnate,they may be conditional and influenced by direct (age, sex, hormonalstatus,experience)andindirect(cascadeeffect) factors[6].Temperatureisamajorabioticfactortogether

withphotoperiodthatdeterminestheintensityand tim-ing of various insects’ activities [42,43]. Field studies relatedtoIPMapproachesonseverallepidopteranshave shownthatthedielperiodicityoftheirsexualattractionis modifiedbybothphotoperiodandambienttemperature

[44–46].Moreover, the seasonal rate of capture by trap

catching is generally related to theassociated tempera-ture, depending on specific seasonal degree-days that insectsaresubjectedto[47,48].Bythislogic,anincrease in global surface temperature may shift the seasonal periodicity of sex-relatedflights in insects,requiring an adaptation of monitoring and treatment periods against these pest insects. Another example is the impact of changingtemperaturesonantforagingactivity.Antsthat use chemical recruitment tend to forage at lower tem-peraturescomparedtothosethatdonot[49].Therefore, acceleratedpheromone decaycaused byincreased tem-peratures is expected to alter trail-following behaviour andtobemoredetrimentaltoforagingbymass-recruiting antspecies[50].

Inadditiontoageneralincreaseininsectmobility,some specific behavioural responses to pheromones can be altered by elevated temperature. For instance, male moths C. fraxinella reared under increased temperature during their reproductive diapause and subsequently exposedtofemalesexpheromonesinawindtunnelshow more pronounced sexualresponses [39].At higher tem-peratures,malemothsalsoshowalowerlevelof specific-ity towards their sex pheromones, due to shifts in behavioural thresholdsrelated toplumeorientationand to theelicitation ofupwindflight [51].

Withregardsto theimpactof atmosphericCO2

concen-tration, the escape behaviour of aphids reared under elevated CO2concentrations (i.e.2100predictedlevels)

is lower compared to those reared under ambient CO2

conditions[52,53,54].Theincrease in CO2

concentra-tion could affect the escape behaviour of aphids by reducing theenzymatic activityof acetylcholinesterase, which is involved in neuronal transmission related to alarmsignalperception[55].Thisalteredabilityofaphids to produceand/orrespondtothealarmpheromonemay altertheirdefensivebehavioursunderchangingclimatic scenarios.

Conclusions,

wider

context

and

future

directions

Based ontheexistingliterature,wesuggest that phero-monal communication in insects will be disturbed by increasesintemperatureandatmosphericgas concentra-tions. Insectsrelying onlong-range chemicalsignalling, involving complexblendsof molecules,arelikelyto be moreimpacted,duetothepossibleperturbationof enzy-matic properties (leading to modification in compound ratio) or signal degradation by oxidative gases during dispersal (disrupting pheromone plumes). Behavioural

aspects of chemical communication (emission of the signal and induced behaviours) could also be affected asaconsequenceofshiftsinoptimalconditionsaffecting phenologyand/orphysiology.However,becauseclimate change effects on pheromonal communication may be maskedbythedailyand seasonalrhythmsof behaviour andphysiology,ourknowledgeofthespecificeffects of climatechangeonpheromonesignallingissparse. Inthisreviewweonlyfocusedonintraspecific (pheromon-al)chemicalcommunication,although allelochemical-me-diatedcommunicationinthebroadersensewilllikelyalso be affected by climate change. Indeed, as already sug-gestedinplant–insectrelationships,thechangesofseveral abiotic parameters could affect interactions between organisms from different trophic levels, and thus affect thedynamicsofecologicalsystems.However,itisdifficult topredicthowclimatechangewillimpactchemical com-munication between insects for several reasons. Abiotic factors could affect the different stagesof insect phero-mone communication (Figure 1), and the response of insects to particular environmental conditions could be species-specific.Moreover, theinteractive effectsof ele-vatedatmosphericozoneandCO2concentrations,aswell

as temperature increase, on chemical-mediated interac-tions havereceived limitedattention, despitethatall of these factors are affecting ecosystems’ stability. A key solutionlies intheuse ofmesocosmsandotherfacilities where multiple components of climate change can be manipulatedinamultispeciescontext[56].Thisapproach couldbeusedtoassesshowallclimaticchangesassociated with a predicted scenario in the coming century might interacttoimpacttheproductionofplantsecondary me-tabolites,andtheassociatedcascadeeffectsonthe phero-moneproductioninphytophagousinsects.

In an IPM context, the efficiency of pheromone slow-releasedevicescouldbereducedfollowingclimatic mod-ifications, since their release kinetics are sensitive to variousclimatic parameters including temperature[57]. Moreover,becausethebehaviouralresponseofinsectsto pheromonesandallelochemicalscouldalso bemodified asaconsequenceof climatechange,we suggestthatall semiochemical-based IPM strategies will be impacted, includingmasstrapping,mating disruption, monitoring, push-pullstrategiesandother intercroppingsystems.

Acknowledgements

A.BoulliswasfinanciallysupportedbyaPhDgrantfromtheFondspourla Formationa` laRecherchedansl’Industrieetl’Agriculture(FRIA),Belgium.

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