Authors: Running Head: Title: Cadotte Marc : Editor Commentary : type Article 9-Aug- : Date Accepted Revised Date : -Jun- -Apr- : Date Received article is This protectedAll rights byreserved. copyright. 10.1111/1365-2664.12769 Version the and version this between differences throughcopyediting, the typesetting, pagination and proofreading proce This articlehas beenaccepted for publicationundergone and full peer review buthas not been 1 2 Winterthurerstrasse 190,CH-8057 Zürich, Switzerland. 3 Ecology, Überlandstrasse 133, CH-8600 Dübendorf, Switzerland interactions species ecology, spatial restoration, meta-ecosystem, meta-community, change, environmental words: Key 735State Street, Suite Santa 300, Barbara, CA, USA 93101-5504 Affiliations: Affiliations: Author: Corresponding Department of EvolutionaryBiology and Envi Eawag:SwissFederal Institute of Aquatic Science and Technology, Departmen AcceptedNational Center for Ecologicaland Analysis Synthesis, UniversityCalifornia, of San Article Bridging ecology and conservation: from ecological networks to ecosystem function function networks toecosystem ecological and from ecologyBridging conservation: Eric Harvey ecological network, conservationbiology, ecosystem functioning,global From ecological networks to ecosystem function function ecosystem to networks ecological From 1,2 , Isabelle Gounand Isabelle , [email protected] [email protected] 1,2 , Colette Ward, Colette ronmental Studies, University of Zurich, Zurich, of University Studies, ronmental of Record. Please cite this article as doi: asdoi: article this cite Please Record. of 3 and Florian and Altermatt ss, which may leadto t of Aquatic oft 1,2

Eawag_09538 ta Barbara,ta Introduction - linking conservation science with 21 with science conservation linking - Introduction article is This protectedAll rights byreserved. copyright. Summary and 1992Janeiro RioDe convention on biodiversity). theAt intersection betweenecology a humanon impact the planet that developedduring the 20 national parkmovements, wildlife conservation,the andbroad recognition international of

AcceptedConservation biologyand restoration ecologyaretwo modern research areasfostered b Article 1. 2. 3. 4. 5.

ecosystem integrity. integrity. ecosystem maintain to targets conservation appropriate more to lead networks ecological of protection the on focusing approaches Alternatively, significance. functional than rather status of organisms rarity on are they mostly based because integrity Currentapproaches toconservation may of ecosystem services. services. ecosystem of conserving biodiversity,ecosystem processesultimately and landscape-scale delive achieve pressing conservation management and restoration ecologygoals of to necessary is networks interaction to species from focus in ashift that propose We identify clear conservation targets with flexible data requirements. datarequirements. with flexible conservation targets identify clear to ecological networkconservation, providinga novel ready to useapproach to map road a We propose also forward. move to ways and challenges, current advances, conceptual and historical discuss we literature, the from examples topical Using predict their response tochangeand to conserve them. This will better protect theaffect nature and ofstrength inte local Synthesis and applications. species, ecosystem processes, and the resulting ecosystem services we depend on. Integration of how environmental and spatial constraints be inadequate tomaintainecosystem be inadequate raction networks will improve our ability to to ability our improve will networks raction th century (e.g., 1987 Montreal protocol, st century ecology ecology century y nd ry article is This protectedAll rights byreserved. copyright. methodological paradigm at shifts the onset of 21 the 1997),and gap the iswideningas the fieldecof conservation measures and development of new policies. This schism has been noted (Pulliam divide betweencurrent conceptsknowledge and thefield in of ecologytheprescriand and journalscommunities. Asanunintscientific social sciences, conservation biologyevolved as anindependent science own its bodywith of conceptual bridging toward ( networks asconservation integration ofecological From species to interaction networks to interactionnetworks From species targets. conservation clear step roadmap to ecological networkconservation using aand novel ready-to current examples, and suggest productive ways moveto forward. Finally, by illustrated challenges, weidentify points two these eachFor of 1). (Fig. services emerging argue that addressing the gap between conservation management and ecology requires in developments recent of light In change. global of face the in integrity ecosystem and diversity predict and protect efficiently to capacity our enhance could that science ecological perspectives. restoration and conservation into conservation, involvingcomplete landscape protection throughcreation the of nationa change,and increasing demand for and food goods production, ‘glass the bell’ appr Incontext of the increasing humanpopulation, reduction inhabitablelandowin Accepted Article from advances conceptual major identify is to article commentary our of objective The Current state of knowledge ii )prediction the of ecosystem-level supporting processesand ology has experienced significant conceptual and and conceptual significant experienced has ology ended consequence, there is now a significant is nowasignificant consequence,thereended target,which would,turn, in allow forbetter st century whichyet have be to integrated we propose a step-by- -useidentify tool to g toclimate ecology we we ecology oachto l parks, ption of ( i ) a better better a )

approaches are often costly and ineffective (Laycock (Laycock costly and ineffective are often approaches Ark’ ‘Noah's however can species be successful, endangered rareor for legislation Protective 1). (Fig. focus is aspecies-level perspective park holistic more the to alternative often-perceived limited return in terms of ecosystem ecosystem of returninterms limited with species single a even or species group of aspecific to allocation resource significant to lead tobe reactive and targets speciesbased onrarity rather than function discussing this in the context discussing context this inthe resulted indirectly frombiocontrolthe of European rabbits ( 2010).For instance, of the the extinction butterfly article is This protectedAll rights byreserved. copyright. poses important societal and spatial challenges (Millenium AssessmentEcosystem Acceptedlinks(Tylianakisbetween mutualistic) species and indirect trophic, (e.g., interactions below).The effect net perturbations of is not always intuitive,owing diff to further section conservation” network ecological to map “a road see example an (for species changes,howthese and changes would spread across the interaction networkand affect other predictions aboutspecies which or functional groups arelikelymost torespond tofuture priorities (Simianer 2007). However,accurately to rank conservation priori conservation reverse can completely account into interactions species taking that shown within probabilities survival of interdependent to complex direct and indirect interactions (Courtois, Figuieres& M an assessment cannot beachieved without considering inter-dependencies among species owing such matter because complicated is a habitats or species among priorities conservation ranking Articledevelopment of cost-effective trade-offs inconservationefforts (Weitzman1998). Howe woodpecker).Frequent lack of resources forconservation managementled hasto the of resource-allocations tothe resource-allocations of integrity andfunctioning Gotelli (e.g., conservation projects prioritization models has models conservation projects prioritization Phengaris et al. 2009).Moreover, thisapproach tends presumably extinct ivory-billed Oryctolagus cuniculus ( Maculinea) arion ulier 2014). The integration alsignificance, which can ties, onewould need erenttypesof et al. in the UK 2012, ): the butterfly butterfly the ): , 2005). The et al. ver,

article is This protectedAll rights byreserved. copyright. depended of onthe ant nest the direct causal explanation for species’ th species’ for explanation causal direct may networks interaction that indicating concern”, “least as than endangered” “critically more as “regionally often listed are significantly strictly oligophagous or monophagous be threatened: to likely are species which to respect with important also is the network structure, more and specifically connectancethe (number of interacti biolog conservation In a species. endangered already to resources allocating of instead chan global of face the in integrity ecosystem maintain to way a pro-active be can species, that illustrates This abundance). low at persisted (plants richness species in decline actual any before lost be can interactions that illustrating havecascading effects extinction onhighertrophic levels before theactually plants occurred beforeactual the extinctionofthe host-plant. Thus, strong decli Importantly, all 8 observed regional extinctions of Lepidopteraassociated with 59 observedregional Lepidoptera of extinctions were associated withhost-plant loss. Lepidopteraand 2403 hostplant potential speciesin CentralEurope. They reported that 8of the of900 network in a trophic extinctions regional analyzed & (2013a) Altermatt Pearse example, stabilit community ecological for structure network & Clarke 2009). turn, depended on open areas supplied by grazingrabbit to establish their n The study of species interactions has greatly improved our appreciation of the importance of of importance the of appreciation our improved greatly has interactions species of study The Accepted Article Myrmica sabuleti reat status (Pearse & Altermatt 2013a). 2013a). & (Pearse Altermatt status reat preserving keystone interactions, rather than than rather interactions, keystone preserving for the development of its larvae; y, sensitivity to invasion, and extinction. For extinction. y, and sensitivity toinvasion, neshost-plants of can ests (Thomas,ests Simcox host-plant loss ons per node), extinct” or extinct” Myrmica, goextinct, y context, y context, give a give ge in

article is This protectedAll rights byreserved. copyright. (Russo trophic interactionscommunity on structure, speciesinvasions, and response toperturbations managementabetter is understanding of biocontrolfailure or potential indirect e ( extensions of the Tussock ( such significance, forestry or agricultural species of included also herbivores lepidopteran observed,accurately and predicted, novel trophic interactions betweennative plant hostsand theirnativehostsaswell with couldbeaccurately predicted a by simple model based onlytheoninteract integration ofnon-native 459 plants the intodiet ofnative, 900 Central Europea interactions in a straightforwardmanner (Pearse & Altermatt 2013 also be a powerful toolfor predicting potential novel trophic interactions based onexisting gooseberry species (e.g., (e.g., species gooseberry ( desp effects indirect non-target have can agents increase naturalenemies abundance and diversity.Moreover, introduced aphid ( important control to fail potentially could enemies maniculatus superabundant and subsidized populations of thegeneralist deermouse ( of knapweeds ( knapweeds of mammals (Pearson & Callaway 2003). Quercus rubra Quercus Urophora affinis

Accepted ArticleA possible further contribution of studies of pairwise species interactionsfor c et al. al. et Myzus persicae ), which in turn triggered several decl several whichinturntriggered ), 2014, Wood Centaurea maculosa ) or sesiid moth sesiid ) or and and ) has devastated potato fields (Straub & Snyder 2006), despite efforts to U. quadrifasciataU. Ribes aureum et al. et as a plant phylogeny (Pearse & Altermatt 2013b). Some of the the of Some 2013b). & Altermatt (Pearse phylogeny as aplant 2014,Alexander Synanthedon tipuliformis pudibunda and and ). If). such among-species inte ), introduced in North Amer introduced), inNorth C. diffusa ite high host-specificity. For instance gall flies gall instanceFor high host-specificity. ite et al. et ines of native plants, and insects small ofnativeplants, ines agricultural pests, for instance the green peach peach green the instance for pests, agricultural ), failed in their biocontrol role but became became but role biocontrol their in failed ), 2015). Among-species interactions can ) larval diet to the non-native red oak red non-native the to diet ) larval larval diet to a non-native, introduced b).For instance, the ractions are ignored, natural ractions ica tocontrol the expansion non-native biocontrol Peromyscus ions ofionslepidoptera n lepidopteran ffectsofnovel onservation as article is This protectedAll rights byreserved. copyright. (McGill (McGill environmenta the consider not did they because produce general principles for the organization context (Leibold successfully integrated biotic in and resource-consuming methods is that they can lead to false negatives (missing links that are that links (missing negatives false to lead can they isthat methods resource-consuming and with these The problem data). co-occurrence contents, gut knowledge, expert (e.g. sources contra many from information integrate and years many over built often are they because (Morales-Castilla (Morales-Castilla constr to challenge is the sciences conservation coexistence would beimpossible. foodwebs cana structured persist in landscape aon single resource, basal ev andlocal For scales. regional instance Pillai and colleagues (2011) that demonstrated complex at occurring oninteractions depends biodiversity thatlocal strongly research meta-community Thus,there is now compelling evidence from bothbiogeography(AraújoLuoto& 2007) and into and established,rather complex divers migratevacuums acknowledginginto emptynotchange, do thatspecies but following climate en climatic the useofspecies-specific question Unfortunately, despiteimportantthese contributions, early ecologicalnetwor Accepted in research network ecological of development abroader to impediments greatest the of One Article Caveats and future perspective et al. 2006). However, recent conceptual developments in community ecology have et al. et al. 2004). During the same period, the fieldofbiogeography began to 2015). Complete species networksarerare andto resolution prone issues teractions within both their lo e biotic communities (Pearson & 2003). communities Dawson (Pearsonebiotic velopes for predicting species forrange-shifts predictingvelopes species uct accurate and meaningful interaction networks interaction meaningful and accurate uct and dynamics of natural communities, largely largely communities, natural dynamics of and l context in which thesel context interactions occur cal environment and their spatial spatial their and cal environment en though local k studies didnot sting sting time- time- change in space as a function as space in change and quan mutualistic) predator-prey, (competitive, breakthroughs Recent knowledge. empirical and (Bascompte 2009). interactionsforthe and facilitation mutualistic also need to understand mechanistically how multiple perturbations spread throughspread multiple perturbations local mechanistically how to understandalso need al. (Poisot anemic shockingly remains context environmental of function asa change interactions predicted. Howeverourmechanistic understanding of the nature how and strength o interactionseach atgradient the endof couldsupport better persistence rates than pre positive increasing because drought) climatic, (e.g., gradients degradation environmental Callaway2006). has This obvious implicationsthe forstudy of species range shifts along &dominating (Lortie inhigh habitats and stress habitats facilitation dominatinglow stress in between co net balance modify the cangradients article is This protectedAll rights byreserved. copyright. (Morales-Castilla co-occurrences simple on based interactions assuming when realized) are not that links (hypothesized positives false importantly most and – even or links, some of importance the of overestimation important), interactions (Morales-Castilla (Morales-Castilla interactions thestudy towardsbias antagonistic resulting of inhistorical beyondwebs, networks food are methods traditional these Moreover, networks. speciesmost knowledge network has been produced fromsubset a small ofnon-reproducible 2012). Incontextthe of increased frequency ofperturbations and landscapealterations, we

Accepted experimental process-based accurate more and new of development for aneed also is There Article of local conditions (Poisot et al. 2015), despite increasing awareness of the importance of of importance the of awareness increasing despite 2015), et al. et 2015). This is problematic because it means that that means it because problematic is This 2015). maintenance diversity of ecosystem and processes have shown that the qualitative nature nature qualitative the that shown have mpetition and facilitation, with competition and with mpetition facilitation, titative strength of species interactionscan strength titative ofspecies not amenable to construction of interaction of amenablenot toconstruction et al. 2012). For stressinstance, f these viously

– to to – et within controlledwithin laboratoryexperiments (Carrara purposes,accessible methods havebeen recentlyproposed measure to interaction stre For these alteration. landscape of effects mitigate to target wrong be the would themselves entirelymediated bottom-up by and top-downtrophic interactions, suggesting importantly, the study demonstrated thesethat perturbation effects on herbivor regional dominance by a few Hemipteran herbivoregeneralists (mainlyMir constraints,fa inbottom-up significant increase a to led effects These diversity. plant host altered fertilization and fragmentation both while abundance, predator reduced fragmentation because unfolded This regulation. herbivore insect grasslandshomogenize to in interact fertilization fragmentation andlandscape local how regional (e.g., stable isotopes, eDNA) promise anpromise eDNA) isotopes, stable (e.g., empirical data beyond species level information (Smith article is This protectedAll rights byreserved. copyright. networks (Tylianakis (Valiente-Banuet (Valiente-Banuet pollination, herbivoreregulation) 2005), is concerning because itdemonstrates that essential functions performed by specie Altermatt 2013a)through or thedesynchronization species of activityperiods (Visse & (Pearse plants host of extinction local the through instance for degradation, environmental youngling development (Fig. 2b). Earlier springs and longer growingto climate due and longer seasons springs Earlier developmentyoungling 2b). (Fig. major

Accepted following species than pace aquicker at lost be can interactions that evidence Recent Article ), hatch in synchrony with the emergence of high-protein insect prey necessary to sustain sustain to necessary prey insect high-protein of emergence the with synchrony in hatch ), From ecological network conservation to ecosystem functioning et al. et al. 2015). For instance, many insectivorous birds, such as the great tit ( tit great theas such birds, insectivorous many For instance, 2015). 2010). Ina recent study, Harvey and MacDougall (2015) showed can be lost despite species remaining present in asystem speciesremaining present canbelost despite exciting future of generation for the cilitating a reduction in insect diversity andreductionin insectdiversity cilitating a et al. et 2015), anduse theof molecular toolkits et al. et 2011).

idae family). Most in situ that herbivores new r & Both r es were ngths s (e.g., Parus article is This protectedAll rights byreserved. copyright. diversity and ecosystem processes (Pearse & Altermatt 2013b). of maintenance the for consequences important equally with emerge also can interactions relevant, especially underhigh a extinction level of debt. Interactions canbe lost, bu always is not functioning or integrity ecosystem for asasurrogate richness species monitoring of practice common the that means It also 2c). 2a, (Figs. interest agricultural of is herbivores of resource the if instance for services, and control, as herbivory such functions, ecosystem effects on negative mayThis cascading have mismatches. with phenological disappear, 2005).Despite the presence of bothprey and predator,theinteraction can beweakened, and & Gienapp (Visser, Holleman fledged chicks of fitness and number the a of leading to decrease emergence, its prey and tit great the of time hatching between mismatch a generate change species can all share the same type of interactions (Poisot (Poisot all samespecies ofinteractions the share can type different while always interact, not do species co-occurring same the because composition ecosystem functions and services (Nelson services (Nelson and functions ecosystem resultiprocesses thelandscape,varylikely across the system. from lose we species, the than rather interactions, the are matters what level, process ecosystem atthe Therefore 2011). & Loreau Gonzalez strength (Pillai, and identity, diversity, interaction of arrangement and up build spatial the is processes ecosystem and structure community of driver main the eventually that and identity, species trump can themselves interactions There is now good evidence that species interactions vary in space independently of spec of independently space in vary interactions species that evidence good now is There Accepted variati spatial of implication The mainlogical Article et al. 2009;Steffen on in biotic interactions is thatecosysteminteractions is on inbiotic ng in spatial variation in theprovision of variation ngspatial in et al. et et al. 2012). This suggeststhat 2012). This 2015). The causes of these these of causes The 2015). t novelt even ies article is This protectedAll rights byreserved. copyright. by nativetrees facilitated is nut pelagic of translocation the Atoll, Palmyra the dispersal or indirectenergy and material flux (Loreau, Mouquet& Holt 2003). Fore have important effects on diversity and functioning of neighbouring ecosyste demonstrated thatstructural attributes ofspecies ainteraction networkecosin one Mouquet & Holt 2003). Indeed, theoretical work using the meta-ecosystem framewo (Loreau, interactions local affect certainly resources) (detritus, organisms dead and (dispersal) living of exchange the and habitats of coupling consumer through ecosystems between variations inecosystemfunctionsyet are not understood, well however spatial connections (Mccauley (Mccauley disruptedbyreplacement the of native trees withcultivated coconut palm nesting androosting habitat for pelagic-foragingmarine birds. This nutrient conveye bird guano), which are associated with greater ni greater with associated are which guano), bird Tournefortia otherwise nutrient-poor, low-productivity (Tanentzap lakes to is exported matter organic forest boreal deciduous the in instance, For mosaics. agricultural naturally connected ecosystems or2013), (Altermatt heterogeneous landscapes such as among observed processes ecosystem in variation spatial wide the part, in least at explain, localenvironmental variation,possibly inducedanthropogenic by perturbations. This changewith interactions howpredict may species flux help spatial to ecosystems due between biomass in a food chain leading from bacteria bacteria from leading chain afood in biomass ( turn associatedwith enhanced phytoplankton, zooplankton,finally and planktiv AcceptedManta birostris Article et al. have greater marine bird abundance, greater soil and foliar nitrogen (attributed to to (attributed nitrogen foliar and greater soil abundance, bird marine greater have 2012) )

abundance. Taking into account the potential impacts of reciprocal effects effects impacts reciprocal theof potential account into Taking abundance. . Relative to Pisonia grandis Pisonia Cocos stands, forest patches dominated bydominated forest stands, patches and and to zooplankton andyellow( ultimately perch trogen runoff into coasta into runoff trogen Tournefortia argentea rients tootherwise oligotrophic coastal waters et al. et 2014). subsidyThis enhances , which are preferred arepreferred which , l waters, which is in waters, whichis l Cocos nucifera nucifera Cocos ms through direct Pisonia Pisonia orous mantaorous ray ystemcan xample, in r belt isthusbelt r rk recently should and Perca Perca

2013; Schleuning, Fründ & García 2015; Creamer article is This protectedAll rights byreserved. copyright. (Tomczak processes ecosystem of predictor and proxy better amuch provide therefore will interactions keystone Targeting conservation. to approach reactive more but necessary, current, the than rather significance functional on based interactions keystone targeting global change affectwill biodiversity (McCann 2007) also andwill offer pro-act a 3). Fig. (see services gr of algal boosts and loadings nutrient cause on bio effects cascading spatially matter todownstream lakes.Such effect forest of harvestingon riverin harvestingasthe resultant reduced vegetationpoorly and developedsupply soils less organ flavescens (Tylianakis (Tylianakis and whichcurrent management toolscouldhelprestore to or protect ecological ne network conservationshould takeform inpractice: which specific metricsshould bemeasured, conservation network map ecological A road to demonstrate a novel approach to ecological networ to ecological approach a novel demonstrate of how interactions changeacross localcontexts. Here,given state the current of knowled frequentlack oflocalized abundance and interaction data,gaps andmechanistic in unders thetechni by hindered its infancy, remains in Moving from a species to an interaction network perspective is necessary to understand how how understand to isnecessary perspective network interaction an to a species from Moving Accepted how unclear remains it advances, logistical and conceptual above-discussed the Despite Article ), a species of commercial and recreational value. The subsidy is disrupted by timber timber by disrupted is subsidy The value. recreational and commercial of a species ), et al. et 2010; Hagen et al. tic interactions downstream Fig. (see which mayultimately3), 2012)? Theuse of interaction networksmanagementin cal and scientific caveats highlighted above, above, highlighted caveats scientific and cal owth, resulting in loss of important ecosystem ecosystem loss ofimportant resultingin owth, et al. k conservation allowing for a direct stability stability adirect for allowing conservation k 2016). e zooplanktonmay have ive alternativeive tworks et al. tanding ge,we ic

methodological goal. towarddevelopments this Perhaps most promising and exciting is usethe new hastriggered networks in interest interaction of resurgence recent the Fortunately, article is This protectedAll rights byreserved. copyright. network. ecological an build to necessary information minimum the constitutes and cost, low at available readily often is occurrence, overall each species’ on information as well as information trait functional quantitative or qualitative with associated list aspecies Therefore, survey. biodiversity of kind some include already plans most assume that conservation reasonable to It is, however, management. conservation with associated constraints resource time and with well agree not does laborious and costly for most managers. Thus, the general ecology motto “the mo change. climate or fragmentation habitat invasion, as species s perturbations of consequences the prevent and predict accurately to interactions quantitative management withinspatially explicit contexts, integratinglocal co in technique) this (or networks interaction use to possible become will it understood, better become dependencies context of underpinnings mechanistic as and available become In its simplestimplementation the technique is suitable for data-p network,metrics whichto measure andhow, and briefly then manage discuss possible We address questionsrelated to the minimum amount of information needed, how tobuildthe identification the and community the of assessment Quantifying interaction strength between each pair of species in an ecological network is too too is network ecological an species in of pair each between strength interaction Quantifying AcceptedSimplifying the process of building ecologic Article 1.

Building ecological networks networks ecological Building al networksremains a work inprogress. of clear conservation targets to maintain it. tomaintainit. targets conservation of clear oor systems; aslocalized data ntext dependenciesand re the better” ment tools. uch uch article is This protectedAll rights byreserved. copyright. construction and validation of food webs using algorithms (Bohan (Grace integration ofpr flexible the for which allow of inferentialmethods onlikelihood based estimators (i.e.maximum likelihood or Ba Nezhad Nezhad similar ecologicalnetworks (Poisot already compile ecological network data that can data that network ecological compile already promising example see Morales-Castilla Morales-Castilla examplepromising see (for networks reproducible and highly standardized, accurate, generate can data, co-occurrence implementation of networkapproaches inconservation science. essentia value; all predictive important most quantitatively affected landby use changes, perturbations,and which networkat how directtesting of allow will large datasets network studies. The construction of interaction networks using time series or spatial orinsu ill-suited considered previously datasets available empirical currently of collection vast the represents mine” that “gold the to access allow developments (Martinez 1991; Tylianakis Tylianakis 1991; (Martinez requir often metrics these measuring furthermore, theseareaffect how it unclear remains however propose to extend the already well proven and extensively used keystone spec

Accepted metricsMany known to are network befor important ecological community stability, Article et al. et 2. et al. et

Identifying conservation targetsIdentifying conservation 2012; Hooten & Hobbs 2015), and machine learning, which facilitates the whichfacilitates &machineandHooten 2015), Hobbs 2012; learning, 2013). These approaches,mixed available with functional traits, phylogenetic, and et al. et 2010). Instead, and until more information available, is we et al. et al. al. et 2015).For conservation purposes, these new l and previously unavailable keys for the ior knowledge and measurement error estimation estimation error measurement and knowledge ior interaction networks are qualitatively andare qualitatively networks interaction 2015).Furthermore, publically available platforms ed byed sampling effortand perturbations; be used togain essen es extensive knowledge of species interactions knowledgeof speciesinteractions es extensive et al. fficiently complete for for fficiently complete tial information totial build 2011; Tamaddoni- 2011; ies concept (Paine tributes holdthe ly explicit yesian) a more details on how to proceed). on howtoproceed). more details technique readilyapplicable is toother types of Importantly,Fig.we document in 4 anexample for consumptive interactions, however th conservation targetsholistic forthe protection bothof network structureand stability (F identity of especially sensitive network nodes. Ther network nodes. sensitive especially ofidentity manage provides step This 4c). (Fig. areidentified extinctions, cascading to leading likely togo following extinct theremoval preyof their (e.g. specialist consumers managers from attentions specific need interactions article is This protectedAll rights byreserved. copyright. interaction sequentially (with replacement, based on Tang, Pawar & Allesina 2014 a each removing after stability changesevaluatestructural innetwork method bootstrapping to composed of 1 (interaction) and 0 (no interaction, seeFig. 4b)we usea r matrix adjacency asimple with Starting 4). Fig. in concept of proof (see strengths interaction interactions canachieved be easily with a directed networkwithout prior knowledge keys identifying Moreover, connectance). network protecting metrics (e.g. diffused conservation clear provides it that is interactions impacts oncommunity stability following their removal.advantage The keystoneusing of Jordán1995; 2009)defining by hereas it the in effect on network structural stability. This This stability. structural network on effect conservation targetsecological in networks:(i)each pairwise interaction is annotated code R toperformanalysis). the We propose a two-stepapproach to identify al. 2016, see Appendix 1inSupportingInformation foradetailed description andaready-

Accepted Article step provides informa provides step teractions betweenteractions the species two with strongest interactions (e.g. mutualisms, see Appendix 1 for 1 seeAppendix mutualisms, interactions (e.g. targets, in contrasttargets, to other holistic but more (see Fig. 4c). (ii) Sensitive species that are are species that Sensitive Fig. (ii) 4c). (see efore, together thesetw efore, tion on pairwise which tion ecently developed ranked basedits on o steps lead to clear leado steps toclear ), potentially tone tone rs with the the rs with nd Sauve of ig. 4d). e

to-use

et networks isparamountecological to networkconservation (Hamilton networks (Hagen configuration.Extensive researcheffects on of habitat lossandfragmentation on an network structure or conserve ecological knowled Basedon current protection. their achieve article is This protectedAll rights byreserved. copyright. current failures and future challenges in targe in challenges future and failures current restoration managementactions. However, currentrates of biodiversityloss speak volume Back to conservation et al. on research needgreat for a thereisstill interest network conservationbeyondare scope the this work,of butwebelieve despite that gr a Gouhier & Guichard 2016). Specific recommendations on spatial management for ec ecosystem services (Fig. 1b). 1b). services (Fig. ecosystem of delivery the and biodiversity conserving of goals ecology restoration and management inte to species from infocus shift directlyexplain patterns of diversityandecosystem function.In this contex interactions of biotic diversity in and the nature that changes suggests evidence Instead, 1a). (Fig. approaches conservation land integral and species-specific by realized than rather hypothesized ar integrity ecosystem and biodiversity of maintenance the that argue we Here approaches. isimportantcontext, it questionto some assumptions ofbasic our about classical conservation Once keystone and interactions sensitive nodes are Accepted or is at allconservation of the diversity species core and integrity ecosystem Protecting Article 2012). 3. Management tools et al. 2012) suggests 2012) that re-thinking thespatial configuration of reserve raction networks is necessary to achieve pressing conservation conservation pressing necessary achieve is to networks raction d stability is the management of spatial of is themanagement stabilityd ting appropriateting conservati the subject an (for extensive review Hagen see ge, we suggest that the main lever to restore torestore mainge,that lever the we suggest identified, themainidentified, i et al. on priorities. Inon priorities. this 2010; Spiecker, ssue is to efficiently efficiently ssue isto t, we propose that a ecological ological owing s to theto s e article is This protectedAll rights byreserved. copyright. and ecological whichsciences, constitutes the on of social, economic, integration abetter on also fostering focus should research Future sciences. ecological advance to challenges current on focus we Here, services. essential several of provision the in collapses sudden to lead to likely are processes ecosystem of erosion associated globaland biodiversityloss knowledge, current In of light services. to these related directly cycles biogeochemical many for space’ operating ‘safe the crossed likely have we that suggest by supporting maintained all are services, which Altermatt, F. Altermatt, (2013) Diversity in metacommunities: ariverine network perspective. Alexander, J. M., Diez J. M., and Levine J. M. (2015) Novel competitors shape species’ species’ shape competitors Novel M. (2015) J. Levine and M., J. Diez M., J. Alexander, References data. contain not article does this because archived been not have Data accessibility Data ScienceFoundation Grant PP00P3_150698, University of Zurich and Eawag. Nat Swiss the from funding FA acknowledge and IG, EH, manuscript. our improved enlightening discussions, and D. Bohan and one anonymousreviewer forcomments that for group research E.M.E.R.Ge the and Thébault E. Sauve, Lortie,A. C. thank to like would We Acknowledgements so. calledachange for perspective of yetthat needsbefully to implemented;now ecosystemservice (Consortium provision 2016).The Millennium EcosystemAsse

Accepted ArticleEcosystems provide benefits tohumansmyriad via a of provisioning,cultural, andreg responses to climate change. climate change. responses to Ecology , 47 , 365–377. Nature , 525 , 515-518. ly way toward a unified a lyunified toward way ecosystem processes.Recentglobal indicators

framework tomaintain is the is time do to ssment (2005) Aquatic ional ional ulating

Hagen, M., Kissling, W.D., Rasmussen, C., De Aguiar, M.A.M., Brown, L.E., Carstensen, D.W., D.W., Carstensen, L.E., Brown, M.A.M., Aguiar, De C., Rasmussen, W.D., Kissling, M., Hagen, Grace, J.B., Schoolmaster, D.R., Guntenspergen, G.R., Little, A.M., Mitchell, B.R., Miller, K.M. K.M. B.R., Miller, Mitchell, Little, A.M., G.R., Guntenspergen, D.R., J.B., Schoolmaster, Grace, Hamilton, S.L., Caselle,J.E., Malone, D.P.& Carr, M.H. (2010)Incorporat Gotelli,N.J., Chao, A., Colwell, R.K.,W.-H. Hwang, &Graves, G.R. (2012) Spec Courtois, P., Figuieres, C. P., & Figuieres, Courtois, Mulier,C.(2014)C. Co Creamer, R.E., Hannula, S.E., Leeuwen, J.P.V., Stone, D., Rutgers, M., Schmelz, R.M., Ruiter, Ruiter, R.M., M., Schmelz, Rutgers, D., Stone, J.P.V., Leeuwen, S.E., Hannula, R.E., Creamer, article is This protectedAll rights byreserved. copyright. M.B. Araújo, Luoto, M. & The (2007) importance Consortium, T.Q. (2016)Networking ourbetter to way ecosystem service prov Bascompte,(2009)Mutualistic J. networks. Bohan, D.A.,Caron-Lormier, Muggleton, G., Raybould, S., & A. Tamaddoni-Nezhad, Accepted ArticleCarrara, F.,Giometto, A., Seymour, M., Rinaldo, A. & Altermatt, Research world. afragmented in networks ecological and interactions J.M., Vidal, M.M.,Woodward, G. & Olesen, J.M. (2012) 2 - Biodiversity, specie K., Tylianakis, E.J., Trøjelsgaard, L.P.C., O’Gorman, Morellato, Ó., Mclaughlin, F.M.D., Marquitti, K.P., Maia, M.E., Ledger, C.N., Kaiser-Bunbury, P., Jordano, G.B., Jenkins, P.R., Jr., Guimarães J., F.K., Genini, Edwards, Y.L., I.,Dupont, Alves-Dos-Santos, equation modeling. structural of implementation graph-theoretic a for Guidelines (2012) E.W. Schweiger, & 89–210. AcademicPress. National Academy of Sciences of the United States of America of States United the of Sciences of Academy National network. reserve marine Islands Channel the of evaluations into Conservation Biology Woodpecker.of theIvory-Billedandmodeling, theextinction stoppingrules, by land use across Europe. Europe. across by use land as affected function ecosystem and biodiversity soil between inter-connection the reveals J., Sousa,J.P.,Wouterse, M.&Lemanceau, P. (2016) Ecological network D., Römbke, P.,Redecker, L.,Plassart, Philippot, C., Pereira, P.V., Morais, S., Mendes, Francisco, R., Dirilgen, T., B.S., Griffiths, D., F., Costa, Carvalho, M., Buee, M.L., Bouffaud, T., Bolger, N.B., Hendriksen, de, P.C. noah’s arkmetaphor revisited. distributions underclimate change. Ecology & Evolution complexity. complexity. interactions ecological in communities: a comparison of methods levels of atdifferent 436. learning. Automated discoveryfood of webs fromecological data using logic-base Global Change inMultispeci Change Global PLOS ONE PLOS Methods in Ecology and Evolution and Ecology in Methods Ecosphere , , , 6 31 26 , e29028. , 105–115. , 47–56. Applied SoilEcology , PLoS ONE 3 , art73. Global Ecologyand Biogeography Frontiers in Ecology and the Environment es SystemsWoodward), Part 1. (ed U.J.and G. pp. , of biotic interactions for modelling species for ofbioticinteractions nservation priorities when species interact: the the speciesinteract: when nservation priorities Griffiths, R., Martin, F., Silva, P.M. da, F., P.M. Silva, R., Martin, Griffiths, 9 , e106073. , , 6 97 , 895–906. , 112–124. F. (2015) Inferring species Advances in Ecological Ecological in Advances , 107 Proceedings of the of Proceedings , 18272–18277. ingbiogeography , ision. 16 d machined , 743–753. analysis imen-based Trends in in Trends A. (2011) , 7 s , 429– Leibold, M.A., Holyoak, M., Mouquet, N., Amarasekare, P., Chase, J.M., Hoopes, M.F., Holt, M.F., Holt, Hoopes, P., Chase, J.M., N., Amarasekare, Mouquet, M., M.A., Holyoak, Leibold, Loreau,M.,Mouquet, & N. Holt, R.D. (2003)Me Laycock, Smart, Moran, H., &White,J., Raffaelli, D., D. P. (2009) Evaluating cost-the Lortie, C.J. & R.M.Callaway, (2006) Re-analy Hooten, M.B. & Hobbs, N.T. (2015) A guide to Bayesian model selection for ecologists. article is This protectedAll rights byreserved. copyright. A.S. Spatiall (2015)Harvey, & E. MacDougall, Jordán, F. (2009) Keystone species and food webs. Martinez, N. (1991) Artifacts orAttributes Artifacts (1991) N. Martinez, McCann, K. (2007)Protecting biostructure. Morales-Castilla, I., Matias, M.G., Gravel, D. Gravel, M.G., I., Matias, Morales-Castilla, Millenium Ecosystem Assessment, Ecosystemsand HumanWell-Bei Nelson, E., Mendoza, G., Regetz, J., Polasky, S., Tallis, H., Cameron, Dr., Chan, K.M., Dail K.M., Chan, Dr., Cameron, H., Tallis, S., Polasky, J., Regetz, G., Mendoza, E., Nelson, Mccauley, D.J., Desalles, P.A., Young, H.S., Dunbar, R.B., Dirzo, R., Mills, M.M AcceptedMcGill, B.J., Enquist, B.J., Weiher, E.Westoby,& M. (2006) Rebuilding co Article Letters ecology. community multi-scale for a framework concept: metacommunity R.D., Shurin,J.B.,Law, R., Tilman, Loreau, D., &M. Gonzalez, A. (2004) The Conservation Plan. Action The UK Biodiversity conservation: of effectiveness Ecological Monographs gradient hypothesis. spatial ecosystem ecology. Society B: \ldots Society B: regulation of insect herbivores. web. web. production, and tradeoffsat landscape scales. (2009)Modeling multiple ecosystem services, biodiversity conservation, commodity Mr. & Shaw, T.H. Ricketts, R., Naidoo, E., Lonsdorf, P.M., Kareiva, J., Goldstein, G.C., 7 Island Press, Washington, DC. DC. Washington, Press, Island interactions from proxies. from functional traits. Reports (2012)Long ecologicalinteraction chains inless-disturbed ecosystems. , 4–11. Ecological Monographs , , 10.1038/srep00409. 7 , 601–613. , 142 , 364 , 3120–3127. Journal of Ecology of Journal , 1733–1741. Trends in Ecology & Evolution Ecology in Trends , 85 Trends& inEcologyEvolution Ecology Letters , 3–28. , 61 The American Naturalist American The , 367–392.

? Effects of resolutionLittlethe on Rock lake food Nature & Araújo,M.B. Inferring (2015) biotic sis ofmeta-analysis: sis support for the stress- , y heterogeneous perturbations homogenize the 94 ta-ecosystems: a theoretical framework for a for framework a theoretical ta-ecosystems: , , 7–16. , Philosophical TransactionstheRoyal of 6 446 , 673–679. Frontiers in EcologyFrontiers the and Environment , 29–29. , 21 , , 178–185. , 186 30 , 347–356. , 623–633. ng

: Synthesis. (2005) Biological mmunity ecology Scientific Scientific . & Micheli, F. Ecology Ecology

y, , Smith, M.A., Eveleigh, E.S., McCann, K.S., Merilo, M.T., McCarthy, P.C. & Van Rooyen, K.I. & P.C. Van Rooyen, McCarthy, M.T., K.S., Merilo, McCann, E.S., M.A., Eveleigh, Smith, Pulliam, H.(1997) Conservation ecology: brid Russo, Laura, Memmott J., Montoya D.,Shea K., and Buckley Y. M. (2014) Pattern Poisot, T., Canard, E., Mouillot, D., Mouquet, N., Gravel, D. & Jordan, F. (2012) The The (2012) F. & Jordan, D. Gravel, N., Mouquet, D., Mouillot, E., Canard, T., Poisot, Simianer, H. (2007) inthe probabilities for Accounting non-independence H. Simianer, extinction of Sauve, A.M.C., Thébault, E., Pocock, M.J.O. & Fontaine, C. (2016) How plants connect connect plants How (2016) C. Fontaine, & M.J.O. Pocock, E., Thébault, A.M.C., Sauve, Schleuning, M.,Fründ, J. & García, D. (2015) Predicting ecosystem functions fr Pillai, P., Gonzalez, A. & Loreau, M. (2011) Metacommunity theory explains the emergence of of emergence the explains theory Metacommunity M. (2011) Loreau, A. & Gonzalez, P., Pillai, Poisot, T., Baiser, B., Dunne, J.A., Kéfi, S., Massol, F., Mouquet, N., Romanuk, T.N., Stouffer, Stouffer, N.,Romanuk, T.N., F.,Mouquet, Massol, S., Kéfi, J.A., Baiser,B.,Dunne, T., Poisot, Pearse,I.S.& Altermatt, (2013b)F. Predicting novel trophic interactions a non-native in w Pearson, R.G. & Dawson, T.P. (2003) Predicting the impacts of climate change the on ofclimate change impacts the Predicting T.P. (2003) R.G. & Dawson, Pearson, Pearson, D.E. & Callaway, R.M. (2003) Indirect effects of host-specific biolo Pearse, I.S. & I.S.Pearse, F. ca (2013a)Altermatt, Extinction article is This protectedAll rights byreserved. copyright. Accepted ArticlePaine, R.(1995)conversation A onrefining the conceptkeystone of species. , pollinator communities.pollinator plant– in structure network of aspects multiple affect interactions species introduced PLoS ONE (2011) Barcodinga quantified food web: crypsis, concepts, ecology and hypothe interactions. and mutualistic networks: an extension of management, http://www.ecologyandsociety.org/vol1/iss1/art14/ dissimilarity of species interaction networks. Conservation Genetics Conservation derivation of conservation priorities basedWeitzman’s on diversity concept. Ecology pollination and herbivory networks and thei States of AmericaStates of food web complexity. simple. simple. D.B., Wood, S.A.& Gravel, D. (2015) mangal – making ecological network an Biogeography distribution of species: are bioclimateenvelope models useful? Ecology Letters agents. complete Lepidoptera--plant food web. Trends in Ecology &Trends inEcology Evolution Ecography , 97 , , 908–917. 6 Ecography , e14424. , 12 , 16 , , 361–371. , 108 , 1088–1094. 39 Proceedings of the National Academy of Sciences of the United the United of Academy Sciences of the National of Proceedings , 384-390. , 19293–8. , , 9 Ecology 38 , 171–179. , 380–392. , 95 , 2953–63. , ging betweengap resource ecology the and Ecology 18 trait-based concepts to plant– trait-based to concepts scades partially estimate partially scades , 456–461. r contribution communityto stability. r contribution Ecology letters Ecology , 94 , 1785–1794. , 15 Global Ecology and , 1353–61. herbivore losses in a gicalcontrol 9 , 962–964. om biodiversity s of alysis ses. orld. Weitzman, M.L. (1998) The Noah’s Ark problem. Visser, M.E., Holleman, L.J.M. & Gienapp, P. (2005) Shifts in caterpillar biomass phen biomass caterpillar in Shifts (2005) P. & Gienapp, L.J.M. Holleman, M.E., Visser, Visser, M.E. & Both, C. (2005) Shifts in phenology due to global climate change: the need for a for need the change: climate global to due phenology in Shifts (2005) C. & Both, M.E. Visser, Valiente-Banuet, A., Aizen, M.A., Alcántara, J.M., Arroyo, J., Cocucci, A., Galetti, M., García, M., García, Galetti, A., Cocucci, J., Arroyo, J.M., Alcántara, M.A., Aizen, A., Valiente-Banuet, Tomczak, M.T., Heymans, J.J., Yletyinen, J., Niiranen, S., Otto, S.A. & Blenckner, T. (2013) (2013) T. & Blenckner, S.A. Otto, S., Niiranen, J., Yletyinen, J.J., Heymans, M.T., Tomczak, Tylianakis,J.M.,Laliberté, E., Nielsen,A.&Bascompte, J.(2010) Conservation of Tanentzap, A.J., Szkokan-Emilson, E.J.,Kielstra, B.W., Arts, M.T Tang,S.,Pawar,Allesina, S. & S. (2014)Correlation between interaction strengths drives article is This protectedAll rights byreserved. copyright. F. Guichard, & T.C. Gouhier, B., Spiecker, Thomas, J.A., Simcox, D.J. & Clarke, R.T. (2009) Successful conservation of a threatened a threatened of conservation Successful (2009) R.T. Clarke, & D.J. Simcox, J.A., Thomas, Tamaddoni-Nezhad, A., Milani, G.A., Raybould, A., Muggleton, S. & Bohan, D.A. (2013) Straub, Straub, W.E.&C.S. (2006) Snyder, Species identity dominates betweenthe relationship predator Accepted Article R., Biggs, E.M., Bennett, I., Fetzer, S.E., Cornell, J., K., Rockström, W.,Richardson, Steffen, Oecologia bird. insectivorous an of biology breeding the on impact its and change climate to due 2561–2569. 29 yardstick. loss:the extinction ofecological species Beyond (2015) R. Zamora, & M. Verdú, A., Traveset, P.J., Rey, N., Ramírez, R., Oviedo, J.R., L., Obeso, Navarro, R., Medel, P., Jordano, J.M., Gómez, D., García, M.B., (2014) Forests fuel fish growth in freshwater deltas. deltas. freshwater in growth fish fuel Forests (2014) ONE inthe baltic sea. change and status ofecosystem indicators network Ecological AgriculturalWorld. (ed G.W. and D.A. Bohan), pp. 225–289. Academic Press. stability in large ecological networks. ecological stability inlarge interaction networks. Maculinea subsidies and reserve networksin coral reef meta-ecosystems. learning andmining. text Chapter Four - Construction and validation of food webs using logic-based machine biodiversity andsuppression. herbivore 26 boundaries: Guiding human developmentchanging ona planet. Planetary S.(2015) & Sörlin, B. Reyers, V., Ramanathan, L.M., Persson, G.M., Carpenter,S.R., Vries, W.Wit, de, C.A. de,Folke, C., Gerten, D , 299–307. , 264–278. , 8 , e75439. , Proceedings of the Royal Society Londonof B: Biological Sciences butterfly. butterfly. 147 , 164–172. Science Biological Conservation Advances in Ecological Research Ecological in Advances , 325 interactions ina interactions , 80–83. (2016) Reciprocal feed Reciprocal (2016) Ecology Letters Ecology Ecology Econometrica , 143 , 87 changing world. world. changing , 2270–2279. , 277–282. Nature Communications , 17 , , 1094–1100. 66 ., Yan, N.D. & Gunn, J.M. Ecological Networks in an in Networks Ecological backs between spatial spatial between backs , 1279–1298. Ecological Applications Science ., Heinke, J., Mace, Functional Ecology , 347 species , 1259855. , , 5 272 PLOS PLOS . ology ology , , , ecosystem services. For services.ecosystem instance, (a)Interaction networks drive ecosystem processes, which in turn determine th FigureFrom 2. to interactions ecosystem services (proximate values) are maintained. valu services(ultimate ecosystem both Thereby, article is This protectedAll rights byreserved. copyright. Wilmshurst J.M. and K.I., G., Rattray D. Bonner Peltzer A., H., I.,Moeller J. Wood, R., Dickie and interaction networksand interaction realized.We(b) proposethatfuture conservation effortsfocus onprot implicit protection of ecosystem processesbiological or communities, whichmaymaor assume approaches These species). (umbrella key role hypothesized species of or value iconic (a)Current conservation approaches focuson protecting lands (national parks) biology. conservation in focus A New 1. Figure legends Figure ecological networks S1 Appendix Information Supporting Interactions are ranked on the X-axis from those having the largest positive effect (green colours) colours) (green effect positive largest the having those from X-axis the on areranked Interactions 0. setto is each interaction occurs when which perturbation) to stability (resilience community structural in change the shows (c) Panel columns. in species consuming rows in species (b)shows the corresponding adjacencywith matrix, black squares representing arrows representingconsumption linksgoingfro interactions.Panel (a) illustrateshypothetical a food web composed ofspeciesto Q, A key such and target can identify conservation ofhow workflow give a and communities, Based ona hypotheticalweb food wedescribe howthe lossof interactions affects stability of networks. in targets conservation Identifying 4. Figure loss. service ecosystem and ofl disruption to density (attributable bacterial is cut, if forest (b) the However, interactions. via maintained are services ecosystem scenario, (in green),growing algae whose abundance is boos supporting high zooplankton abundance. This,turn, in enableszooplankton regul to Accepted(brown arrows resources of flows spatial by influenced are arrows) black and (circles networks Interaction feedbacks. spatial and flows Resource 3. Figure birds wouldlonger no regulatecaterpillars. This interaction may loss impact f before eggs hatch. Although all species would re peak may abundances caterpillar and species phenology shift may warming global (c) However, protein-richfor food their offspring; regulation this of herbivoresensuresgood fr Article establishmentpines. of invasive mammals facilitate and fungi betweennon-native interactions Novel(2014) . Practical assessment of species interactions and their effect on the stability of stability of the on effect and their interactions species of assessment . Practical ). For instance, (a) litter inputs from rive from inputs litter (a) For instance, ).

per se , with explicit positive effects on habitats and biodiversity. and on habitats positive effects with explicit , (b) some bird species feed on feed birdspecies (b) some Journal of Ecology algae escape zooplankton regulation owingzooplankton tolow algae escaperegulation itter input), potentially leading to eutrophication potentiallyinput), leading to itter e) and the diversity of habitats and and species ofhabitats the diversity e) and spatial spatial feedbacks of resource flows on species m the resource to the consumer species. Panel Panel species. consumer the to resource them main present (no change in species richness), species richness), in change (no present main tedIn by fertilizer leachate. this agricultural rine forest rine for supply forest food bacteria,

103 : 121–29. insects, while caterpillars supplyinsects, while ecting ecosystemprocesses ruit production. or individual or e provision of interactions with uit production.uit ate fast- with y notbe article is This protectedAll rights byreserved. copyright. Accepted Article interaction. eachwith arrow’scolourgivingthe expected change network in stability followin (c) panel from ranking interaction the illustrate we (d) In panel extinct. go to expected species numb the represents arrow each below number The extinctions). cascading (i.e., prey their of loss the following goextinct would which species, specialist ultra indicate arrows blue The removed. when stability structural on colours) (red effect negative largest the having those to g a lossof an er of of er article is This protectedAll rights byreserved. copyright. Accepted Article article is This protectedAll rights byreserved. copyright. Accepted Article

article is This protectedAll rights byreserved. copyright. Accepted Article