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ADVANCES IN ECOLOGICAL RESEARCH Series Editors DAVID A. BOHAN Directeur de Recherche UMR 1347 Agro(cid:1)ecologie AgroSup/UB/INRA Po^le GESTAD, Dijon, France ALEX J. DUMBRELL School of Biological Sciences University of Essex Wivenhoe Park, Colchester Essex, United Kingdom AcademicPressisanimprintofElsevier TheBoulevard,LangfordLane,Kidlington,OxfordOX51GB,UnitedKingdom 125LondonWall,London,EC2Y5AS,UnitedKingdom 50HampshireStreet,5thFloor,Cambridge,MA02139,UnitedStates 525BStreet,Suite1800,SanDiego,CA92101-4495,UnitedStates Firstedition2017 ©2017ElsevierLtd.Allrightsreserved. Nopartofthispublicationmaybereproducedortransmittedinanyformorbyanymeans, electronicormechanical,includingphotocopying,recording,oranyinformationstorageand retrievalsystem,withoutpermissioninwritingfromthepublisher.Detailsonhowtoseek permission,furtherinformationaboutthePublisher’spermissionspoliciesandour arrangementswithorganizationssuchastheCopyrightClearanceCenterandtheCopyright LicensingAgency,canbefoundatourwebsite:www.elsevier.com/permissions. Thisbookandtheindividualcontributionscontainedinitareprotectedundercopyrightby thePublisher(otherthanasmaybenotedherein). Notices Knowledgeandbestpracticeinthisfieldareconstantlychanging.Asnewresearchand experiencebroadenourunderstanding,changesinresearchmethods,professionalpractices, ormedicaltreatmentmaybecomenecessary. Practitionersandresearchersmustalwaysrelyontheirownexperienceandknowledgein evaluatingandusinganyinformation,methods,compounds,orexperimentsdescribed herein.Inusingsuchinformationormethodstheyshouldbemindfuloftheirownsafetyand thesafetyofothers,includingpartiesforwhomtheyhaveaprofessionalresponsibility. Tothefullestextentofthelaw,neitherthePublishernortheauthors,contributors,oreditors, assumeanyliabilityforanyinjuryand/ordamagetopersonsorpropertyasamatterof productsliability,negligenceorotherwise,orfromanyuseoroperationofanymethods, products,instructions,orideascontainedinthematerialherein. ISBN:978-0-12-804338-7 ISSN:0065-2504 ForinformationonallAcademicPresspublications visitourwebsiteathttps://www.elsevier.com/ Publisher:ZoeKruze AcquisitionEditor:AlexWhite EditorialProjectManager:HeleneKabes ProductionProjectManager:MageshKumarMahalingam CoverDesigner:MarkRogers TypesetbySPiGlobal,India CONTRIBUTORS O.Anneville UMR42CARRTEL,INRA-Universit(cid:1)eSavoieMontBlanc,Thonon-les-Bains,France T.J.Bartley UniversityofGuelph,Guelph,ON,Canada D.A.Bohan UMR1347Agro(cid:1)ecologie,AgroSup/UB/INRA,Po^leGestiondesAdventices,Dijon Cedex,France J.R.Boutain BotanicalResearchInstituteofTexas,FortWorth,TX,UnitedStates V.Calcagno Universit(cid:1)eCo^ted’Azur,CNRS,INRA,ISA,France K.Cazelles Universit(cid:1)eduQu(cid:1)ebecàRimouski,Rimouski;QuebecCenterforBiodiversityScience, Montr(cid:1)eal,QC,Canada;UMRMARBEC(MARineBiodiversity,Exploitationand Conservation),Universit(cid:1)edeMontpellier,Montpellier,France E.Chapuis UMR3PPVBMT,CIRAD-Universit(cid:1)edelaR(cid:1)eunion,SaintPierre;UMRIPME,IRD- Universit(cid:1)edeMontpellier-CIRAD,Montpellier,France R.I.Colautti Queen’sUniversity,Kingston,ON,Canada P.David Centred’EcologieFonctionnelleetEvolutive,UMR5175,CNRS-Universit(cid:1)ede Montpellier-UMIII-EPHE,Montpellier,France I.Domaizon INRA,Universit(cid:1)edeSavoieMontBlanc,UMRCARRTEL,ThononlesBains,France M.Dubart CNRS,Universit(cid:1)edeLille-SciencesetTechnologies,UMR8198Evo-Eco-Paleo,SPICI Group,Villeneuved’Ascq;InstitutdesSciencesdel’E(cid:1)volution,Universit(cid:1)edeMontpellier, CNRS,IRD,EPHE,CC065,Montpellier,France P.-F.Duyck CIRAD,UMRPVBMT,97410SaintPierre,LaR(cid:1)eunion,France C.Fontaine Mus(cid:1)eumNationald’HistoireNaturelle—CESCO,UMR7204MNHN-CNRS-UPMC, Paris,France D.Gravel Universit(cid:1)eduQu(cid:1)ebecàRimouski,Rimouski;QuebecCenterforBiodiversityScience, Montr(cid:1)eal;Facult(cid:1)edesSciences,Universit(cid:1)edeSherbrooke,Sherbrooke,QC,Canada ix x Contributors C.Jacquet Universit(cid:1)eduQu(cid:1)ebecàRimouski,Rimouski;QuebecCenterforBiodiversityScience, Montr(cid:1)eal,QC,Canada;UMRMARBEC(MARineBiodiversity,Exploitationand Conservation),Universit(cid:1)edeMontpellier,Montpellier,France S.Kamenova UniversityofGuelph,Guelph,ON,Canada S.K(cid:1)efi InstitutdesSciencesdel’E(cid:1)volution,Universit(cid:1)edeMontpellier,CNRS,IRD,EPHE, CC065,Montpellier,France I.LeViol Mus(cid:1)eumNationald’HistoireNaturelle—CESCO,UMR7204MNHN-CNRS-UPMC, Paris,France A.Lemainque Commissariatàl’EnergieAtomiqueetauxEnergiesAlternatives(CEA),Institutde G(cid:1)enomique(IG),Genoscope,Evry,France N.Loeuille InstituteofEcologyandEnvironmentalSciencesUMR7618,SorbonneUniversit(cid:1)es- UPMC–CNRS-IRD-INRA-Universite´ ParisDiderot-UPEC,Paris,France N.D.Martinez PacificEcoinformaticsandComputationalEcologyLab,Berkeley,CA;Universityof Arizona,Tucson,AZ,UnitedStates F.Massol CNRS,Universite´ deLille,UMR8198Evo-Eco-Paleo,SPICIGroup,Lille,France G.Mollot SupAgro,UMRCBGP(INRA/IRD/CIRAD/MontpellierSupAgro),Montferrier-sur- Lez;CESAB-FRB,ImmeubleHenriPoincar(cid:1)e,AixenProvence,France J.H.Pantel Centred’EcologieFonctionnelleetEvolutive,UMR5175,CNRS-Universit(cid:1)ede Montpellier-UMIII-EPHE,Montpellier;CentreforEcologicalAnalysisandSynthesis, FoundationforResearchonBiodiversity,B^atimentHenriPoincar(cid:1)e,RueLouis-Philibert, 13100Aix-en-Provence,France M.-E.Perga INRA,Universit(cid:1)edeSavoieMontBlanc,UMRCARRTEL,ThononlesBains,France V.Ravign(cid:1)e CIRAD,UMRPVBMTPo^ledeProtectiondesPlantes,Saint-Pierre,R(cid:1)eunion,France T.N.Romanuk DalhousieUniversity,Halifax,NS,Canada;PacificEcoinformaticsandComputational EcologyLab,Berkeley,CA,UnitedStates E.Th(cid:1)ebault InstituteofEcologyandEnvironmentalSciencesUMR7618,SorbonneUniversit(cid:1)es- UPMC-CNRS-IRD-INRA-Universit(cid:1)eParisDiderot-UPEC,Paris,France Contributors xi P.Tixier CIRAD,URGECO,MontpellierCedex,France;CATIE,Cartago,CostaRica F.S.Valdovinos UniversityofArizona,Tucson,AZ,UnitedStates Y.Zhou PacificEcoinformaticsandComputationalEcologyLab,Berkeley,CA;SchoolofPublic Policy,UniversityofMaryland,CollegePark,MD,UnitedStates PREFACE Biological invasions are considered one of the pre-eminent sources of dis- turbance of ecosystems, causing marked loss of biodiversity at large spatial scalesandconcomitantchangesinfunctionandecosystemserviceprovision (Ehrenfeld,2010;MurphyandRomanuk,2014;Vilàetal.,2006).Thepast halfcenturyhasseenincreasedconcernabouttheimpactsofbiologicalinva- sions(GurevitchandPadilla,2004),fromlocalspeciesextinctiontochanges inecosystemfunctioning,aswellaseffectsongeneticdiversityorfacilitation of further invasions through invasion meltdown (Murphy and Romanuk, 2014; Paolucci et al., 2013; Simberloff et al., 2013; Strayer, 2012; Vilà etal.,2011).Inordertopreventinvasions,muchefforthasalsobeendevoted towards understanding conditions favouring the success of invasions (Beisner et al., 2006; Pyˇsek et al., 2010; Romanuk et al., 2009). In spite of numerous empirical and theoretical developments, understanding, predicting and managing species invasions remain one of the main issues of ecology today, with potentially massive costs now and in the years to come (Bradshaw et al., 2016). Invasionbiology,bornasanewdisciplinemorethanhalfacenturyago (Elton, 1958), is only now coming of age. Despite an accumulation of detailed case studies, a growing theoretical corpus and connections made tomanyareasofecology,evolutionarybiologyandeconomy,thereremain somekeygapsinthestudyofinvasions.Oneistheneedforamoreintegra- tive,systems-basedviewofaninvasivespeciesencounteringanestablished, recipientcommunity,withanemphasisplacedonthecomplexityofrecip- rocalrelationships,includingtherealizationthatthelatterisitselfacomplex entity.Theresearchthatresultswilllikelybeneitherasimple,linearaddition of a species to a community nor the summation of all pairwise interactions between the constituent species. Untilrecently,relativelylittleinvestigationofspeciesinvasionshasbeen doneusingsystems-ornetwork-basedapproaches(butseeRomanuketal., 2009),despitegrowingevidencethatconsiderationoftheinvaderalone,or thespeciesitappearstodisplace,isnotenough.Inbiocontrol,wherebyspe- cieshavebeendeliberatelyintroducedtocounteracttheeffectsofparticular pestspecies,thereisampleevidencethattheinsertionofanovelspeciesinto an established community can markedly modify community structure and functioning in ways that are often unexpected (Lombaert et al., 2010; xiii xiv Preface Royetal.,2011).Theresultsofsuchintroductionsrangefrommerepersis- tenceofthebiocontrolagent,tosuccessfulintroductionandcontroleffect, throughtowholesaleswitchingtootherunintendedpreyspeciesandtheloss of these from the system instead (Clarke et al., 1984; Phillips et al., 2006). These findings in biocontrol, when placed alongside others from ‘natural’ invasion events, argue for the effects of invading species ramifying across whole ecosystems and that systems- or network-based approaches would have great power to resolve mechanisms and understand invasion. ‘Networks of invasion’, understood both through biological invasions into ecological interaction networks and through the web-like nature of invasionpatterns,spatiallyandintermsofsequentialinvasions,arethesub- ject of two thematic issues of Advances in Ecological Research. These deal, in turn,withpaperssynthesizingconceptsininvasionecologyandtheempir- icalevidenceandcasestudiesofinvasionsviewedwith anetworkperspec- tive. This first volume opens with a set of papers, both empirical and theoretical, which set out the general Perspectives in Invasion Ecology, when viewed from the network standpoint. These papers first synthesize knownimpactsofinvadersonfoodwebs,withbothageneralreviewfocus- ing on the ‘insertion point’ of invaders within food webs (David et al., Chapter 1) and a meta-analysis (Mollot et al., Chapter 2) which detail how often and under which conditions species invasions lead to species losses. Chapter 3 (Kamenova et al.) introduces current tools—genetic, iso- topic, participatory, model based, etc.—available to monitor, detect and predict invasions in ecological networks. The following two chapters (Massoletal.,Chapter4;Romanuketal.,Chapter5)presenttwodifferent models aimed at elucidating the effects of food web topology on invasion probabilityandimpact.WhileChapter4developsaspatialfoodwebmodel basedon MacArthurandWilson’s(1963)theoryof islandbiogeographyto understand the effects of food web properties on sequences of invasions, Chapter 5 focuses on what makes a food web robust to species invasions, elaboratingonthenichemodelofWilliamsandMartinez(2000)toexplore whetherquantitativeandqualitativerobustnessaretradedoffalongthefood webconnectancegradient.Thisfirstvolumecloseswithageneralperspec- tivepapers(Panteletal.,Chapter6)whichfocuseson14differentquestions for future studies on invasions in ecological networks. The second volume consists of a series of papers that detail invasions of particulartypesofinvaders(e.g.parasites)orintoparticulartypesofecosys- tems (e.g. freshwater ecosystems). It begins with M(cid:1)edoc et al., which syn- thesizes predictions of impacts of parasite invasions in food webs. The Preface xv following chapter (Jacksonet al., Chapter2) focuses on shifts in freshwater foodwebtopologiesduetospeciesinvasionsandemphasizesthepossibility oftrophiclinkdisruptioninsuchsituations.Chapter3(Amsellemetal.)then synthesizescurrentevidenceandhypothesesregardingtheeffectsofmicro- organismsonspeciesinvasions,fromtheclassicenemyreleasehypothesisto spillback and spillover effects linked to the co-invasion of organisms with theirsymbionts.Plant–pollinatorinteractionsandthetopologyoftheasso- ciated networks under a regime of massive species introductions are the focusofChapter4(Geslinetal.),whichdetailthepotentialimpactsofsuch massive management of both plants and insects on nearby, non-managed ecosystems. The volume then ends with Chapter 5, by Murall et al., with a change of scale to describe invasions in microbial networks within hosts, emphasizing what is already known regarding mammal microbiota and suggesting ways in which interdisciplinary dialogue between ecologists, microbiologists and physiologists might pave the way for a better under- standing of problems such as the emergence of antibiotic resistance. Thesetwovolumespresentasnapshotofthecurrentstateoftheartinthe study of invasion ecology, emphasizing species interactions and using network-basedapproaches.These11chaptersrevealthatthereisgreatvalue inusingnetworkstostudyinvasion,bothfromaconceptualviewpointand in practicaltermsto measure, predictand monitortheimpactsof invasions onecosystems.Whentakentogether,theworkpresentedheresuggeststhat buildingaricherunderstandingofinvasion,whichnetworksafford,couldbe animportantstepforwardindevelopingpredictiveapproachestomanaging or preventing invasions. We hopethat the variety of approaches and ques- tionstonetworksofinvasioncontainedwithinthesepagesprovideafruitful and stimulating framework for future studies and research programmes aimed at tackling invasions. F. MASSOL P. DAVID D.A. BOHAN ACKNOWLEDGEMENTS Thisseriesofpaperscame,inpart,outoftheCOREIDSproject,cofinancedbyTOTALand theFondationpourlaRecherchesurlaBiodiversit(cid:1)e(FRB),attheCentrefortheSynthesis andAnalysisofBiodiversity(CESAB)inAix-en-Provence,France.TheCOREIDSproject has the goals of unifying and analyzing databases on species invasions into sensitive communities and zones using network ecological approaches, with the aim of identifying the generic processes and mechanisms of invasion that might be used in invasion predictionandmanagement. xvi Preface REFERENCES Beisner,B.E.,etal.,2006.Environmentalproductivityandbiodiversityeffectsoninverte- bratecommunityinvasibility.Biol.Invasions8,655–664. Bradshaw,C.J.A., etal., 2016.Massive yetgrosslyunderestimated globalcostsof invasive insects.Nat.Commun.7,12986. Clarke,B.,etal.,1984.Theextinctionofendemicspeciesbyaprogramofbiologicalcontrol. Pac.Sci.38,97–104. Ehrenfeld, J.G., 2010. Ecosystem consequences of biological invasions. Annu. Rev. Ecol. Evol.Syst.41,59–80. Elton,C.S.,1958.TheEcologyofInvasionsbyAnimalsandPlants.Methuen&CoLtd., London,UK. Gurevitch,J.,Padilla,D.K.,2004.Areinvasivespeciesamajorcauseofextinctions?Trends Ecol.Evol.19,470–474. Lombaert, E., etal.,2010. Bridgehead effectinthe worldwide invasion of the biocontrol HarlequinLadybird.PLoSOne5,e9743. MacArthur, R.H., Wilson, E.O., 1963. An equilibrium theory of insular zoogeography. Evolution17,373–387. Murphy,G.E.P.,Romanuk,T.N.,2014.Ameta-analysisofdeclinesinlocalspeciesrichness fromhumandisturbances.Ecol.Evol.4,91–103. Paolucci,E.M.,etal.,2013.Originmatters:alienconsumersinflictgreaterdamageonprey populationsthandonativeconsumers.Divers.Distrib.19,988–995. Phillips,B.L.,etal.,2006.Invasionandtheevolutionofspeedintoads.Nature439,803. Pyˇsek,P.,etal.,2010.Disentanglingtheroleofenvironmentalandhumanpressuresonbio- logicalinvasionsacrossEurope.Proc.Natl.Acad.Sci.U.S.A.107,12157–12162. Romanuk,T.N.,etal.,2009.Predictinginvasionsuccessincomplexecologicalnetworks. Philos.Trans.R.Soc.B364,1743–1754. Roy, H.E., et al., 2011. Living with the enemy: parasites and pathogens of the ladybird Harmoniaaxyridis.Biocontrol56,663–679. Simberloff,D.,etal.,2013.Impactsofbiologicalinvasions:what’swhatandthewayforward. TrendsEcol.Evol.28,58–66. Strayer,D.L.,2012.Eightquestionsaboutinvasionsandecosystemfunctioning.Ecol.Lett. 15,1199–1210. Vilà,M.,etal.,2006.Localandregionalassessmentsoftheimpactsofplantinvadersonveg- etationstructureandsoilpropertiesofMediterraneanislands.J.Biogeogr.33,853–861. Vilà, M., et al., 2011. Ecological impacts of invasive alien plants: a meta-analysis of their effectsonspecies,communitiesandecosystems.Ecol.Lett.14,702–708. Williams, R.J., Martinez, N.D., 2000. Simple rules yield complex food webs. Nature 404,180–183. CHAPTER ONE Impacts of Invasive Species on Food Webs: A Review of Empirical Data P. David*,1, E. The(cid:1)bault†, O. Anneville{, P.-F. Duyck§, E. Chapuis¶,k, † N. Loeuille *Centred’EcologieFonctionnelleetEvolutive,UMR5175,CNRS-Universite´deMontpellier-UMIII-EPHE, Montpellier,France †InstituteofEcologyandEnvironmentalSciencesUMR7618,SorbonneUniversit(cid:1)es-UPMC-CNRS-IRD- INRA-Universit(cid:1)eParisDiderot-UPEC,Paris,France {UMR42CARRTEL,INRA-Universit(cid:1)eSavoieMontBlanc,Thonon-les-Bains,France §CIRAD,UMRPVBMT,97410SaintPierre,LaR(cid:1)eunion,France ¶UMR3PPVBMT,CIRAD-Universit(cid:1)edelaR(cid:1)eunion,SaintPierre,France kUMRIPME,IRD-Universit(cid:1)edeMontpellier-CIRAD,Montpellier,France 1Correspondingauthor:e-mailaddress:[email protected] Contents 1. Introduction 2 2. DefinitionsandLimits 3 2.1 InvasiveSpecies:An“AnthropocentricConcept” 3 2.2 MeasuringImpactsonFoodWebs:ObjectsofStudyandMethodology 4 3. LocalEffects:EffectofInvadersatOneorTwoStepsofDistance 6 3.1 Top-DownEffects 7 3.2 LateralEffectsofInvaders:ExploitativeCompetition 12 3.3 Bottom-UpEffectsofInvaders 16 3.4 ApparentCompetitionBetweenInvadersandResidents 19 3.5 Facilitation,Mutualisms,andEngineering:NontrophicIndirectInteractions 21 4. GlobalEffects:InvasionsatFoodWebScale 22 4.1 FoodWebStructureasaBioticFilter 22 4.2 PositionofInvasiveSpeciesinFoodWebs 26 4.3 ImpactsofInvasionsonFoodWebStructure 29 5. HowDoesaNetworkPerspectiveInfluencetheManagementofInvasive Species? 35 5.1 PreventingInvasionsFromaNetworkPerspective 36 5.2 UsingEcologicalNetworkstoLimitImpactsorExcludeInvaders 39 5.3 ImplicationsofInvaderRemovalFromaNetworkPerspective 42 6. Conclusion 44 6.1 FutureDirections 47 Acknowledgements 48 Glossary 49 References 50 AdvancesinEcologicalResearch,Volume56 #2017ElsevierLtd 1 ISSN0065-2504 Allrightsreserved. http://dx.doi.org/10.1016/bs.aecr.2016.10.001

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