Aquatic Food Webs This page intentionally left blank Aquatic Food Webs An Ecosystem Approach EDITED BY Andrea Belgrano National Center for Genome Resources (NCGR), Santa Fe, NM, USA Ursula M. Scharler University of Maryland Center for Environmental Science, Chesapeake Biological Laboratory (CBL), Solomons, MD, USA and Smithsonian Environmental Research Center, Edgewater, MD, USA Jennifer Dunne Pacific Ecoinformatics and Computational Ecology Lab, Berkeley, CA USA; Santa Fe Institute (SFI) Santa FE, NM, USA; Rocky Mountain Biological Laboratory, Crested Butte, CO USA AND Robert E. Ulanowicz University of Maryland Center for Environmental Science, Chesapeake Biological Laboratory (CBL), Solomons, MD, USA 1 1 GreatClarendonStreet,OxfordOX26DP OxfordUniversityPressisadepartmentoftheUniversityofOxford. ItfurtherstheUniversity’sobjectiveofexcellenceinresearch,scholarship, andeducationbypublishingworldwidein OxfordNewYork Auckland CapeTown DareesSalaam HongKong Karachi KualaLumpur Madrid Melbourne MexicoCity Nairobi NewDelhi Shanghai Taipei Toronto With offices in Argentina Austria Brazil Chile Czech Republic France Greece Guatemala Hungary Italy Japan South Korea Poland Portugal Singapore Switzerland Thailand Turkey Ukraine Vietnam OxfordisaregisteredtrademarkofOxfordUniversityPress intheUKandincertainothercountries PublishedintheUnitedStates byOxfordUniversityPressInc.,NewYork #OxfordUniversityPress,2005 Themoralrightsoftheauthorshavebeenasserted DatabaserightOxfordUniversityPress(maker) Firstpublished2005 Allrightsreserved.Nopartofthispublicationmaybereproduced, storedinaretrievalsystem,ortransmitted,inanyformorbyanymeans, withoutthepriorpermissioninwritingofOxfordUniversityPress, orasexpresslypermittedbylaw,orundertermsagreedwiththeappropriate reprographicsrightsorganization.Enquiriesconcerningreproduction outsidethescopeoftheaboveshouldbesenttotheRightsDepartment, OxfordUniversityPress,attheaddressabove Youmustnotcirculatethisbookinanyotherbindingorcover andyoumustimposethissameconditiononanyacquirer BritishLibraryCataloginginPublicationData (Dataavailable) LibraryofCongressCataloging-in-PublicationData Aquaticfoodwebs:anecosystemapproach/editedbyAndreaBelgrano ... [etal.]. p.cm. Includesbibliographicalreferencesandindex. ISBN0-19-856482-1(alk.paper)–ISBN0-19-856483-X(alk.paper) 1. Aquatic ecology. 2. Foodchains(Ecology) I. Belgrano,Andrea. QH541.5.W3A682252004 577.6016–dc22 2004027135 ISBN0 19 856482 1(Hbk) 9780198564829 ISBN0 19 856483 X(Pbk) 9780198564836 10 9 8 7 6 5 4 3 2 1 TypesetbyNewgenImagingSystems(P)Ltd.,Chennai,India PrintedinGreatBritain onacid-freepaperbyAntonyRowe,Chippenham FOREWORD CURRENT AND FUTURE PERSPECTIVES ON FOOD WEBS Michel Loreau Food webs have been approached from two basic onfoodwebsthatiscomplementarytotheenergetic perspectives inecology. Firstisthe energetic view approach (DeAngelis 1992). Material cycles are articulatedbyLindeman(1942),anddevelopedby among the most common of the positive feedback ecosystem ecology during the following decades. loops discussed by Ulanowicz in his concluding In this view, food websarenetworks of pathways remarks, and may explain key properties of eco- for the flow of energy in ecosystems, from its systems(Loreau1998).Thestoichiometryofecolo- capture by autotrophs in the process of photo- gical interactions may further strongly constrain synthesis to its ultimate dissipation by hetero- food-web structure (Sterner and Elser 2002; Elser trophicrespiration.Iwouldventuretosaythatthe and Hessen’s chapter). There has also been con- ecological network analysis advocated by siderable interest in the relationship between bio- Ulanowicz and colleagues in this book is heir to diversityandecosystemfunctioningduringthelast this tradition. A different approach, rooted in decade(Loreauetal.2002).Mergingthetheoriesthat community ecology, was initiated by May (1973) bearuponfoodwebsandthemaintenanceofspecies and pursued by Pimm (1982) and others. This diversityisurgentlyneededtoday,andmayprovide approach focuses on the dynamical constraints newinsights intofood-webs structure andecosys- that arise from species interactions, and empha- temfunctioning(HillebrandandShurin’schapter). sisesthefactthattoomuchinteraction(whetherin The structure and functioning of ecological sys- the form of a larger number of species, a greater tems is determined not only by local constraints connectance among these species, or a higher andinteractions,butalsobylarger-scaleprocesses. mean interaction strength) destabilises food webs The importance of regional and historical influ- and ecological systems. The predictions resulting ences has been increasingly recognised in com- from this theory regarding the diversity and con- munity ecology (Ricklefs and Schluter 1993). The nectance of ecological systems led to a wave of extent to which they shape food webs, however, comparativetopologicalstudiesonthestructureof has been relatively little explored. The recent food webs. Thus, the two traditions converge in development of metacommunity theory (Leibold the search for patterns in food-web structure et al. 2004) provides a framework to start exam- despite different starting points. This book results ining spatial constraints on the structure and from the confluence of these two perspectives, functioning of local food webs (Melian et al.‘s which are discussed in a number of chapters. chapter).Atevenlargertimescales,foodwebsare Patterns, however, are generally insufficient to the result of evolutionary processes which deter- inferprocesses.Thus,thesearchforexplanationsof minetheircurrent properties.Complex foodwebs thesepatternsintermsofprocessesisstillverymuch may readily evolve based on simple ecological alive,andinthissearchtheenergeticanddynamical interactions(McKane2004).Theevolutionoffood- perspectives are not the only possible ones. Bio- web and ecosystem properties is a fascinating geochemicalcyclesprovideafunctionalperspective topic for future research. v vi FOREWORD This book provides a good synthesis of recent Loreau,M.1998.Ecosystemdevelopmentexplainedby research into aquatic food webs. I hope this competitionwithinandbetweenmaterialcycles.Pro- synthesis will stimulate the development of new ceedingsoftheRoyalSocietyofLondon,SeriesB265:33–38. Loreau,M.,S.Naeem,andP.Inchausti.Eds.2002.Bio- approachesthatlinkcommunitiesandecosystems. diversityandecosystemfunctioning:synthesisandper- spectives.OxfordUniversityPress,Oxford. References May,R.M.1973.Stabilityandcomplexityinmodelecosys- tems.PrincetonUniversityPress,Princeton. DeAngelis,D.L.1992.Dynamicsofnutrientcyclingand McKane,A.J.2004.Evolvingcomplexfoodwebs.The foodwebs.Chapman&Hall,London. EuropeanPhysicalJournalB38:287–295. Leibold,M.A.,M.Holyoak,N.Mouquet,P.Amarasekare, Pimm,S.L.1982.Foodwebs.Chapman&Hall,London. J.M.Chase,M.F.Hoopes,R.D.Holt,J.B.Shurin,R.Law, Ricklefs,R.E.,andD.Schluter.Eds1993.Speciesdiversity D.Tilman,M.Loreau,andA.Gonzalez.2004.The inecologicalcommunities:historicalandgeographicalper- metacommunityconcept:aframeworkformulti-scale spectives.UniversityofChicagoPress,Chicago. communityecology.EcologyLetters7:601–613. Sterner,R.W.,andJ.J.Elser.2002.Ecologicalstoichiometry: Lindeman,R.L.1942.Thetrophic-dynamicaspectof thebiologyofelementsfrommoleculestothebiosphere. ecology.Ecology23:399–418. PrincetonUniversityPress,Princeton. Contents Foreword v MichelLoreau Contributors ix Introduction 1 AndreaBelgrano PARTI Structure andfunction 5 1 Biosimplicity viastoichiometry: theevolutionoffood-web structure andprocesses 7 JamesJ.ElserandDagO.Hessen 2 Spatial structure anddynamics inamarinefoodweb 19 CarlosJ.Melia´n,Jordi Bascompte,andPedroJordano 3 Roleofnetwork analysisincomparative ecosystem ecology ofestuaries 25 RobertR.Christian,DanielBaird,JosephLuczkovich,JeffreyC.Johnson, UrsulaM.Scharler,and RobertE.Ulanowicz 4 Foodwebsinlakes—seasonal dynamics andthe impact of climatevariability 41 DietmarStraile 5 Patternandprocessinfoodwebs: evidencefromrunningwaters 51 GuyWoodward,RossThompson, ColinR.Townsend,and AlanG.Hildrew PARTII Examining food-webtheories 67 6 Somerandomthoughtsonthestatistical analysisoffood-web data 69 AndrewR.Solow 7 Analysis ofsize andcomplexity ofrandomlyconstructed food webs byinformationtheoretic metrics 73 JamesT.Morris,RobertR. Christian,and RobertE.Ulanowicz 8 Size-based analysesofaquatic foodwebs 86 SimonJennings vii viii CONTENTS 9 Food-web theoryinmarineecosystems 98 JasonS.Link,WilliamT.Stockhausen,andElizabeth T.Methratta PARTIII Stability anddiversityinfoodwebs 115 10Modelingfood-webdynamics:complexity–stability implications 117 JenniferA.Dunne,UlrichBrose,RichardJ.Williams,andNeoD.Martinez 11Isbiodiversitymaintainedbyfood-webcomplexity?—the adaptivefood-webhypothesis 130 MichioKondoh 12Climateforcing,foodwebstructure,andcommunity dynamics inpelagicmarineecosystems 143 L.Ciannelli,D.Ø. Hjermann,P.Lehodey,G.Ottersen, J.T.Duffy-Anderson, andN.C.Stenseth 13Food-web theoryprovides guidelinesformarineconservation 170 EnricSalaandGeorgeSugihara 14Biodiversityandaquaticfood webs 184 HelmutHillebrandandJonathanB.Shurin PARTIV Concludingremarks 199 15Ecological networkanalysis: anescapefromthemachine 201 RobertE.Ulanowicz Afterword 208 MathewA.Leibold References 211 Index 255 Contributors DanielBaird,ZoologyDepartment,UniversityofPort SimonJennings,CentreforEnvironment,Fisheries Elizabeth,PortElizabeth,SouthAfrica. andAquacultureScience,LowestoftLaboratoryNR33 JordiBascompte,IntegrativeEcologyGroup,Estacio´n 0HT,UK.Email:[email protected] Biolo´gicadeDon˜ana,CSIC,Apdo.1056,E-41080, JeffreyC.Johnson,InstituteofCoastalandMarine Sevilla,Spain.Email:[email protected] Resources,EastCarolinaUniversity,Greenville,NC AndreaBelgrano,NationalCenterforGenomeResources 27858,USA. (NCGR),2935RodeoParkDriveEast,SantaFe,NM PedroJordano,IntegrativeEcologyGroup,Estacio´n 87505,USA.Email:[email protected] Biolo´gicadeDon˜ana,CSIC,Apdo.1056,E-41080, UlrichBrose,TechnicalUniversityofDarmstadt, Sevilla,Spain. DepartmentofBiology,Schnittspahnstr.3,64287 MichioKondoh,CenterforLimnology,Netherlands Darmstadt,Germany. InstituteofEcology,Rijksstraatweg6,Nieuwersluis, RobertR.Christian,BiologyDepartment,EastCarolina P.O.Box1299,3600BGMaarssen,TheNetherlands. University,Greenville,NC27858,USA.Email: Email:[email protected] [email protected] P.Lehodey,OceanicFisheriesProgramme,Secretariat LorenzoCiannelli,CentreforEcologicaland ofthePacificCommunity,BPD5,98848Noumea EvolutionarySynthesis(CEES),DepartmentofBiology cedex,NewCaledonia. UniversityofOslo,PostOfficeBox1066,Blindern, MathewLeibold,SectionofIntegrativeBiology,The N-0316Oslo,Norway.Email:lorenzo.ciannelli@ UniversityofTexasatAustin,1UniversityStation, bio.uio.no. C0930Austin,TX78712,USA.Email:mleibold@ JanetT.Duffy-Anderson,AlaskaFisheriesScience mail.utexas.edu Center,NOAA,7600SandPointWayNE,98115 JasonS.Link,NationalMarineFisheriesService, Seattle,WA,USA. NortheastFisheriesScienceCenter,166WaterSt., JenniferA.Dunne,PacificEcoinformaticsandComputa- WoodsHole,MA02543,USA.Email:jlink@ tionalEcologyLab,P.O.Box10106,Berkeley,CA94709 whsunl.wh.whoi.edu USA;SantaFeInstitute,1399HydeParkRoad,SantaFe, MichelLoreau,Laboratoired’Ecologie,UMR7625 NM87501USA;RockyMountainBiologicalLaboratory, EcoleNormaleSuperieure46,rued’UlmF-75230, P.O.Box519,CrestedButte,CO81224USA Email: ParisCedex05,France.Email:[email protected] [email protected]. JosephLuczkovich,BiologyDepartment,EastCarolina JamesJ.Elser,SchoolofLifeSciences,ArizonaState University,Greenville,NC27858,USA. University,Tempe,AZ85287,USA.Email:j.elser@ NeoD.Martinez,PacificEcoinformaticsand asu.edu ComputationalEcologyLab,P.O.Box10106, DagO.Hessen,DepartmentofBiology,Universityof Berkeley,CA94709RockyMountainBiological Oslo,P.O.Box1050,Blindern,N-0316Oslo, Norway. Laboratory,P.O.Box519,CrestedButte,CO81224 AlanG.Hildrew,SchoolofBiologicalSciences,Queen USA. Mary,UniversityofLondon,MileEndRoad,London, CarlosJ.Melia´n,IntegrativeEcologyGroup,Estacio´n E14NS,UK.Email:[email protected] Biolo´gicadeDon˜ana,CSIC,Apdo.1056,E-41080, HelmutHillebrand,InstituteforBotany,Universityof Sevilla,Spain. Cologne,Gyrhofstrasse15D-50931Ko¨ln,Germany. ElizabethT.Methratta,NationalMarineFisheries Email:[email protected] Service,NortheastFisheriesScienceCenter, D.Ø.Hjermann,CentreforEcologicalandEvolutionary 166WaterSt.,WoodsHole,MA02543,USA. Synthesis(CEES),DepartmentofBiologyUniversityof JamesT.Morris,DepartmentofBiologicalSciences, Oslo,PostOfficeBox1066Blindern,N-0316Oslo, UniversityofSouthCarolina,Columbia,SC29208,USA. Norway. Email:[email protected] ix