Biocontrol of invasive weeds under climate change: progress, challenges and management implications

Biocontrol

of

invasive

weeds

under

climate

change:

progress,

challenges

and

management

implications

Yan

Sun

,

Jianqing

Ding

,

Evan

Siemann

and

Stephen

R

Keller

Climatechangeispredictedtoincreasethefrequencyand

impactofplantinvasions,creatinganeedfornewcontrol

strategiesaspartofmitigationplanning.Thecomplex

interactionsbetweeninvasiveplantsandbiocontrolagents

havecreateddistinctpolicyandmanagementchallenges,

includingtheeffectivenessandriskassessmentofbiocontrol

underdifferentclimatechangescenarios.Inthisbriefreview,

wesynthesizerecentstudiesdescribingthepotential

ecologicalandevolutionaryoutcomesforbiocontrolagents/

candidatesforplantinvadersunderclimatechange.Wealso

discusspotentialmethodologiesthatcanbeusedasa

frameworkforpredictingecologicalandevolutionary

responsesofplant-naturalenemyinteractionsunderclimate

change,andforrefiningourunderstandingoftheefficacyand

riskofusingbiocontroloninvasiveplants.

Addresses

1_{DepartmentofBiology/Ecology&Evolution,UniversityofFribourg,}

1700Fribourg,Switzerland

2_{SchoolofLifeSciences,HenanUniversity,Kaifeng,Henan475004,}

China

3

BiosciencesDepartment,RiceUniversity,Houston,TXUSA

4

DepartmentofPlantBiology,UniversityofVermont,USA Correspondingauthor:Sun,Yan(yan.sun@unifr.ch)

Introduction

Climatechangeandplant invasionssignificantlyimpact

biodiversity,humanwelfare,andtheeconomy,makingit

criticaltopredicttheinteractiveeffectsofclimatechange

oninvasiveplantsandtheirmanagement.Anthropogenic

climate changes driven by greenhouse gas emissions

include alterations in temperature, precipitation, CO2,

insolationand thefrequencyofextreme climaticevents

(i.e., flood, fires, intense storms, heat waves). These

changescaninfluencemultiplestagesof theplant

inva-sion process, from initial introduction through

establishment, spread and impact [1,2]; consequently,

interactionsbetweenclimatechangeand plant invasion

mayhave a profoundinfluence on speciesinteractions,

ecosystemservicesand people’slivelihoods[3].

Classicalbiocontrol(’biocontrol’hereafter)hasprovento

beaneffectiveandcost-efficientapproachtomitigating

plant invasions [4], but consideration of how climate

change may alter the dynamics between plant hosts

andbiocontrolagentsisrelativelyunexplored.Biocontrol

involvesthedeliberaterelease ofspecialist natural

ene-miesfromtheplant invader’snativerangeto reduceits

abundanceintheintroducedrangebelowanecologicalor

economicthreshold [4].The complexity of interactions

involvinginvasiveplantsandthebioticandabiotic

com-ponentsoftheinvadedhabitatsunderdifferentclimatic

scenarios has created distinct policy and management

challengesincludingtheeffectivenessofbiocontrol.

Cli-matechange isexpected to impact invasiveweeds and

biocontrol agents (e.g., through effects on metabolism,

phenology,physiology) and theirinteractions as wellas

theeffects onnon-targetattack ofnativeplant species.

Inparallelto thegrowing concernof climatechangeand

plantinvasions,therehasbeenalargeincreaseinstudieson

climatechangeandbiocontroloverthepast10years

(Appen-dixFig.S1).However,ourunderstandingoftheresponseof

theseplant-herbivoreinteractionstothefullcomplementof

climate-driven changes remains rudimentary. Multiple

reports suggest that climate change may promote plant

invasionsandincreasetheirimpact[5],whileotherstudies

reportbothpositiveandnegativeeffectsofclimatechange

ontheperformanceofbiocontrolagents,withvarious

con-sequencesfortheirefficacy(Table1;Figure1).

Thegoalofthispaperistoreviewtheavailableevidenceof

climatechangeeffectsonweedbiocontroloutcomes,

pro-videanoverviewofthe biocontrol methodologiesusedwith

key examples, discusspotentialecological and evolutionary

outcomesfor the interaction of plant invadersandtheir

biocontrol candidates/agents under climate change, and

raiseawarenessofhowclimatechangemayalterbiocontrol

efficacyand risk to increase our abilityto predict these

outcomesthroughpre-releaseassessment.

Climate

change

and

weed

biocontrol:

a

complex

interplay

Ecologicaleffects

Climatechangehasthepotentialtoalter interactionsof

invasive weeds and biocontrol agents by phenotypic

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changes in traits (physiology,biochemistry, life history,

phenology)orbychangingtheabioticand/orbiotic

envir-onments inwhich interactionsoccur,both aboveground

and belowground.This inturn canalter thefrequency,

timing, intensity, and duration of interactions between

plantinvadersandbiocontrolagentsandsotheimpactof

agents on plant invaders maybe enhanced or reduced.

For instance,elevated CO2maychangetheamountof

herbivoredamage byaltering plantprimary metabolism

(e.g., increased tissue C:N, which typically increases

herbivore consumption [6,7]). CO2-driven changes in

secondary metabolism that underlie plant chemical

defenses [8,9,10] or volatiles [11] may also influence

herbivore damage (e.g., phenolics typically increase

under elevated CO 2 and can reduce herbivore attack

[12], but other chemicalshavevariable responses [12]).

Elevated CO 2 also often increases plant growth rates

[9,13]whichmaycontributetoincreasedplanttolerance

to herbivoredamage[7,14].Increasedtemperature,and

potentiallylongergrowingseasons,canchangethe

inter-actionsofbiocontrolagentsandweedsbyincreasingthe

number of generations per year of the agents[15] and

potentially increase its impacts on the weed host

[6,16,17].Because plantsdifferin theirsusceptibilityto

damage at different life stages (e.g., vegetative growth

versusseedproduction)changesintimingofemergence

of insectsand weedswithclimatechange couldmodify

the consequences of insect feeding [18]. Changes in

geographic distributions, especially as the climate

con-tinues to warmandextreme events becomemore

com-mon,canimpactinteractionsbetweenbiocontrolagents

andweedsasdifferentialmigrationratesof insects,host

plants, higher trophic levels and other species create

novel biotic interactions and new above- and

below-ground communities [19,20,21,22,23].The net effect

ofclimatechangeonweedbiocontrolwilldependonthe

relative strengthsof thesevariousresponsesto multiple

factorsofclimatechange[6].

Evolutionaryaspects

Recentstudieshavehighlightedthatrapid evolutionary

change can occur in both invaders and their biocontrol

agentsinresponsetoashiftinenvironmentalconditions

[24,25].Manycasesofrapidadaptiveevolutionhavebeen

reportedfor invasive plants,includingshiftsin resource

Table1

Examplesofstudiesonweedbiocontrolunderclimatechange

Issues Methods Climatechangeaspects hostinvasive

plant Biocontrol agent Findings Ref. Temp. CO2 precipitation Ecological effects Chambers/lab û Parthenium hysterophorus Zygogramma bicolorata

Occurrenceofheatwavesmay influencetheperformanceand survivalofZ.bicolorata

[64]

Commongarden _{û û} Alternanthera

philoxeroides

Agasicles hygrophila

MinoreffectsofelevatedCO2onthe

efficacyofthebiocontrolagent

[65]

Fieldexperiment û Centaureadiffusa Larinus

minutus

ElevatedCO2increasedplant

fitness,butalsoagentdensity

[66]

Evolutionary aspects

Commongarden _û Jacobaea

vulgaris

Longitarsus jacobaeae

post-introductionclimate adaptationbylife-historychanges

[36] Efficacy prediction Speciesdistribution model û û û Ambrosia artemisiifolia sixpotential agents

ThespatialmismatchofA. artemisiifoliaanditspotentialagents isfurtheramplifiedbyclimate change

[38]

Populationdynamics model

û Prosopisspp. Evippespp. Theeffectbeingdampenedby

herbivorysuppressingseed productionirrespectiveofpreceding rainfall

[67]

non-target attack

Fieldsurveyandfield experiment

û Alternanthera

sessilis

Agasicles hygrophila

Climatewarmingincreases biocontrolagentimpactona non-targetspecies [22] Figure1 Climate change 0/+/– – – +/– +

Plant invaders Weed biocontrol agents

Non-target effects Ecosystem impacts

Current Opinion in Insect Science

Impactofclimatechangeonplantinvasions,weedbiocontroland theirinteractions(dashlines)asevidencedfromliterature.Signsof0/ +/ representno-,positiveandnegativeeffects.

allocationfromdefensetogrowth[26],localadaptationto

newhabitats[27]andclimatessuchasbytheevolutionof

phenotypicclinesalongclimaticgradients[28],the

evo-lutionofgreaterdispersalability[29]andincreasesinthe

rateof populationgrowthandexpansion[30,31].

Evo-lutionaryadaptationisalsoexpectedforbiocontrolagents

whentheyencounternovelenvironmentsor changesin

climaticconditions,especiallyforspecieswithshort

gen-erationtimes[31,32,33].

We argue that evolutionary studies should be better

integratedintothedifferentstagesof aweedbiocontrol

program (Figure 2). For example, by using reciprocal

transplantsorcommongardenexperimentscoupledwith

populationmodeling,researcherscouldmatchup

climat-ically adapted biocontrol candidates with their target

releaseenvironments,orevaluatetheirpotential

evolva-bilityunderchangingselectionpressures(Figure2).High

geneticvarianceinlifehistoryandabioticstresstolerance

traitsmayallowresearcherstoscreenforstrainsor

popu-lationsthatcouldadapttofutureclimaticconditions[34].

Forinstance,Reddyetal.[35]comparedfourbiotypesof

the weevil, Neochetina Eichhorniae Warner (Coleoptera:

Curculionidae), a biocontrol agent of water hyacinth,

Eichhorniacrassipes(Mart.)Solms.They foundvariation

intolerancetocoldamongpopulationsandsuggestedthat

the introduction of N. Eichhorniae from Australia into

northern California would result in climate matching

betweensource and release environments and increase

the distribution and densities of weevils, and by this

improve biocontrol efficacy. Szács et al. [36] found

post-introductionclimaticadaptationthroughlife-history

changesin aestival diapauseand shifts in phenology in

LongitarsusJacobaeaeWaterhouse

(Coleoptera:Chrysome-lidae),abiocontrolagentof Jacobaeavulgaris Gaert.

In the following, we explore how specific studies of

ecological and evolutionary processes during a weed

biocontrol program can incorporate implications of

cli-matechangescenarios,andhelpinformtheselectionof

effectiveandsafeagents.

Weed

biocontrol

efficiency

under

climate

change

Ecologicalcontext

Responses of plant and natural enemy populations to

climate change through short-term (within-generation)

shifts in their geographical distribution or timing of

growthandspeciesinteractionscanbepredictedthrough

field surveys along latitudinal transects, experimental

measurementsundercontrolledconditions,andthrough

predictive modeling. For example, using field surveys

alonglatitudinaltransectsandsimulatedwarming

experi-ments,Luetal.[22]showedthatclimatewarmingmay

allow the beetle Agasicles hygrophila Selman and Vogt

(Coleoptera:Chrysomelidae), a biocontrol agent of the

invasive weed Alternanthera philoxeroides (Mart.)Griseb,

toexpanditsrangeandbenefitbiocontrolinregionsthat

arecurrentlytoocoldfortheinsect.However,becauseA.

philoxeroides will also expand its range further north in

responsetowarming, andtheplanttoleratescoldbetter

thanA.hygrophila,theoveralleffectofbiocontrolmaybe

weakinsomehigherlatituderegionsiftheinsectcannot

establishrobustpopulationsduetothecoldclimate.

Speciesdistributionmodels(SDMs)[37]areoftenusedto

predict the efficacy of potential biocontrol agents in

currentand futureconditionsbymeasuringtheoverlap

of predicted habitat suitability with that of theirtarget

host plant. For example,based on habitat suitability in

SDMs, the invasive plant Ambrosia artemisiifolia L. is

predicted to experience decreased geographic overlap

with six biocontrol candidates under climate change in

itsintroducedEuropeanrange[38].SDMscanalsouse

climatesuitabilityto predictdemographic ratesandthe

ability of biocontrol agents to quickly attain high

Figure2

Research opportunities under climate change WBC Processes

Target weed ecology

Exploration for potential WBC agents

Selection of effective WBC agents

Host-specificity testing

Agent release & distribution

Agent evaluation

Phenotype environment correlations to select populations of the biocontrol agent pre-adapted to conditions in the introduced range under climate change and release in areas where the plant invader is expected to increase/spread under climate change

Host specificity/range under climate change Selection of efficient agents under climate change with regard to effect on plant performance, abundance and distribution

Potential methods

Survey Enlarge the area to search for potential agents

Experiments Common garden under different climate conditions Biotic interactions under different climate conditions

Artificial selection for genotypes adapted to future climate conditions

Models

Population dynamicsunder different climate conditions SDM for both current and future climate scenarios Mechanistic models including climate change scenarios

Current Opinion in Insect Science

Schematicoverviewofprocessesinaweedbiocontrol(WBC)project,researchopportunitiesthatincludeclimatechangescenariosandtheir potentialmethods(SDM:speciesdistributionmodels).

population densities, which are critical for significant

impactsonthetargetplantinvader[39]andmanagement

success[40].Moreover,combiningSDMandmechanistic

(process-based)modelsbyintegratingphysiological

mod-els of insect developmentinto SDMs based on habitat

suitability may enable more robust predictions of both

range shifts [41] and population abundances [42,43].

Using suchacombined approach,Augustinus etal. [44]

identified the climatic factors limiting the population

build-upofOphraellacommunaLesage(Coleoptera:

Chry-somelidae),abiocontrolcandidateof invasiveA.

artemi-siifolia, and predicted its potential population density

acrossitssuitableEuropeanrangeandtherelative

impor-tance of those climatic factors on population growth.

Population dynamics models are also commonly used

to explore and predict changes in population densities

overtime,suchasIntegralProjectionModels(IPMs)[45]

and DYMEX(HearneScientificSoftware)[46].Kriticos

et al. [47] used a process-based population dynamics

model to predict that invasiveBuddleja davidiiFranch.

would succumb rapidlyto herbivoredamageby its

bio-control weevil Cleopus japonicus Wingelmu¨ller

(Coleop-tera: Curculionidae)under warmingconditions. Further

studieswouldbenefitfromintegratingtheoretical

model-ing, physiological/behavioral experiments and

experi-mental population studies under climatechange

condi-tions(i.e.,latitudinalspace-fortimeandclimatron/FACE

(free-air CO2 enrichment) type experimental settings

[13])intoabiocontrolprogram(Figure 2).

Evolutionarycontext

Examplesofevolutionaryresponsestoclimatechangeare

accumulating,suggestingsomeorganismsarecapableof

rapidevolutiononatimescaleconcomitantwithongoing

changesinclimate[28,32].Whilethetoolsofecological

genetics are ableto test for andidentify genetic

differ-ences attributable to local environments, predicting

futureresponsesismoredifficult.Thebreeder’sequation

postulatesthattheresponse(R)ofapopulationto

selec-tion on a quantitative trait will be proportional to the

product of thetraitheritability(h2,theratioof additive

geneticvariance,VA,tototalphenotypicvariance,VP)and

thestrengthofselection(S),wherebyR=h2S[48].Thus,

predicting evolutionary responses of weed biocontrol

efficacyunderclimatechangerequiresinformationabout

thecurrentamountofstandinggeneticvariance present

fortraitsinvolvedintheagent-hostinteractioninboththe

native and introduced ranges that may become

mis-matched under climate change. Accurate predictions

mayrequireknowledgeofhow thisvariationisspatially

distributed among geographic regions of current (and

possiblyfuture)overlap.Inaddition,geneticcorrelations

amongtraitscreatetradeoffsthatresultinindirect

selec-tion that may constrain the response of traits to direct

selection during climate change [49,50]. Given these

biological complexities, a promising approach is to use

experimentalevolutionorartificialselectionexperiments

that measure the change in trait means over multiple

generations in response to selection under controlled

conditions[51]. Such experimentsmayallow thedirect

measurement of each population’s evolvability in

response to selectiononafocaltrait,such ashost plant

lifehistoryorallocationtogrowthanddefense,aswellas

revealing changes in correlated traits that may have

evolvedas aresultof indirectselection[52].

While it would be logistically challenging to carry out

experimentalevolutionfor bothhostplantsand

biocon-trol agents, one feasible solution might be to evolve

agents reared on host plant tissues developed under

controlledgrowingconditionsmimickingclimatechange

(e.g.,earlierspringwarmup,droughtstress).Trackingthe

across-generationresponseoftraitsmeasuredinthe

bio-control agent to this change in selective environment

wouldallowarealizedmeasureofevolutionarypotential

that integrates over existing trait correlations. This

approach could becoupledwith thestrategy of ‘evolve

and re-sequence’ [53],in which thegenomic targets of

selection and evolutionary responsecanberevealed by

performinggenome-wideDNAorRNA(transcriptomic)

sequencing of populationpools to test for gene-specific

changesinallelefrequenciesfromthestarttotheendof

the experiment.This wouldrequirelarge experimental

populationsofthebiocontrolagent(intheseveral

thou-sandsormore);thus,logisticsandpermittingmay

neces-sitatethatsuchstudiesberestrictedtothenativerange

before theintroduction of biocontrol,or perhaps in the

introduced range in cases where biocontrol has already

beenaccidentallyintroduced.Suchanapproachcouldbe

particularly useful for identifying large effect genetic

variantsthatmight serveasusefulbiomarkersforgenes

in biocontrol agents that are likely to be responsive to

selection under changing climates. Traits such as host

plant chemical defenses or insect metabolic genes that

detoxify these compounds would be ideally suited

towardsthisgoal;howeverothermorequantitativeforms

of plant defense and many other life history traits are

likelytobehighlypolygenic[54],andthusbettersuited

to aquantitativegeneticframework.

Recently,theintegrationofgenomicpolymorphismdata

with SDMs haveenabled modelingintra-specific

varia-tioninspecies-climaterelationships,includingthe

poten-tial toidentifywhich areaswithinaspecies’ geographic

rangemaybecomemostaffectedbyachangeinclimate

[55,56]. If local selection by climate has shaped the

genomic diversity of the plant host, then

genomics-enabled SDMs could help predict portions of the host

rangethatcouldbemostvulnerabletoshort-termfitness

impacts fromclimatechange.Genomics-enabledSDMs

ofbiocontrolagentsmayalsobeusefulinpredictingthe

bestmatchbetweensourceandreleaseclimates.Another

possibilityinvolvestheuseofgeographicvariationinhost

traitexpression(forexample,inpalatabilityordefense)as

predictorsofgenomicvariabilityunderlyinglocal

adapta-tionoftheagenttoitshostinthenativerange[57].This

typeofanapproachcouldhelprevealpotential

co-evolu-tionaryhotspotsbetweenhostplantsandtheirbiocontrol

agentsthatcouldbeusedto targetagentsources in the

nativerangeandreleaselocationsintheintroducedrange.

An important caveat of all SDM methods

(genomics-enabledorotherwise)isthatthesemodelsareinherently

correlative, and thus model predictions require careful

validationtestingbeforemakingchangesinconservation

prioritiesor management[58,59].Further,SDM

predic-tionsofshiftsinsuitablerangesorgenomicvulnerability

ofparticularpopulationsunderclimatechangearelikely

to bemostuseful for short-termprojections (relative to

thegenerationtimeanddispersaldistancesofthe

organ-isms),particularlyforbiocontrolagentswithshort

gener-ationtimesthatmaybecapableofrapidevolutionrelative

tothatof thehost plant.

Climate

change

and

non-target

attack

of

biocontrol

agents

Afewstudiesreportednon-targetattackofintentionally

releasedoractivelyredistributedweedbiocontrolagents

[60] that resulted in direct negative effects on native

plantspecies[61,62],ornegativeindirecteffects[63].Ina

recentreview,Hinzetal.[60]showedthatincidencesof

unpredicted non-target attack decreased over time and

thistrendisthoughttocontinuewithscientific

advance-ment.Theirresultssuggestthatappropriateselectionof

testspeciescouldhaveavoidedmorethan90%of

unpre-dicted non-target attack. Incorporating climate change

factors may further improve such predictions in the

future. This is because climate-induced shifts in the

synchronyofplant–insectinteractionscouldaffectinsect

distributionandabundanceoninvasiveandnativeplants

that may alter non-target effects in biocontrol. For

instance,Luetal. [22]showed thatelevated

tempera-ture can shift the phenology of the non-target native

plant,AlternantherasessilisLinn.fromannualtoperennial

and increase overwintering, damage and impact of the

biocontrol agent A. hygrophila on seedling recruitment.

However,warmingalterstheinteractionsbetween

inva-sive A. philoxeroides and native A. sessilis and shifts the

plantcommunityfrominvader-dominatedto

native-dom-inated,butonlyinthepresenceofA.hygrophilaasaresult

of the disproportionate increases in herbivory on the

invader[21].Thissuggeststhatbiocontrolmayenhance

the competitive ability of native plants under climate

change. Thus, climate change could substantially alter

the interactions of invasive plants, native species and

biocontrolagentsandthe‘net’non-targeteffectsshould

becarefullyassessedbyfieldmonitoring,commongarden

experiments,populationdynamicsmodelsandSDMs.

Climate changeaffects thelikelihood of new invasions

(e.g., disturbanceof communities) directly by changing

invasiveplantdistribution,growthandreproduction,and

indirectly through modifying plant-insect interactions.

Understanding responses of invasive plants and their

natural enemies to climate change is criticalfor future

biocontrol of invasive plants. The effects of climate

change on weed biocontrol management are complex

(positive,negativeorneutral),creatingaparticular

chal-lengeforpredictingitsefficacyandrisk.Althoughmany

currentpre-releasetestsarerobustinpredicting

biocon-trolefficacyandnon-targeteffects,incorporatingclimate

changefactorsmayallowresearcherstopredicthowthey

willaffectthephenology,distributionandabundanceof

biocontrolagentsandinvasiveandnativeplantstogether

with their interactions and biocontrol outcomes.

How-ever,suchstudies(Figure2)wouldgreatly benefitfrom

partnershipsofbiocontrolpractitionerswithevolutionary

biologistsandmodelersinacademia.

Conflict

of

interest

statement

Nothingdeclared.

Appendix

A.

Supplementary

data

Supplementary material related to this article can be

found, in the online version, at doi:https://doi.org/10.

1016/j.cois.2020.02.003.

Acknowledgements

Y.S.acknowledgesfundingthroughtheNovartisFoundation(grantnumber #17B083);J.D.wassupportedbyfundsofChinaNationalKeyResearchand DevelopmentProgram(YFC20171200100)andS.R.K.acknowledges fundingfromaUSDACooperativeAgreement(#58-1907-4-032).Wewould liketothankH.Mu¨ller-Scha¨rerandU.Schaffnerforcommentsand suggestededitstothismanuscript.

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