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Coastal and Estuarine Studies 60 Erik Kristensen, Ralf R. Haese, and Joel E. Kostka (Eds.) Interactions Between Macro- and Microorganismsi n Marine Sediments American Geophysical Union Washington, Published under the aegis of the AGU Books Board Jean-Louis Bougeret, Chair; Gray E. Bebout, Carl T. Friedrichs,J ames L. Horwitz, Lisa A. Levin, W. Berry Lyons, Kenneth R. Minschwaner,A ndy Nyblade, Darrell Strobel, and William R. Young, members. Library of Congress Cataloging-in-Publication Data Interactionsb etween macro- and microorganismsin marine sediments. p. cm. -- (Coastal and estuarine studies, ISSN 0733-9569; 60) 1. Marine sediments-Microbiology2. . Biogeochemicalc ycles. I. American GeophysicalU nion. II. Series. QR106.156 2005 577.7'7---dc22 2005016172 ISSN 0733-9569 ISBN-10: 0-87590-274-X ISBN-13:(978)-0-87590-2746 Cover image: Burrow of Polychaeta Nereis diversicolorf, rom Kristensena nd Kostka, this vol- ume. Copyright2 005 by the American Geophysical Union, 2000 Florida Ave., NW, Washington,D C 20009, USA. Figures, tables, and short excerpts may be reprinted in scientificb ooks and journals if the source is properlyc ited. Authorizationt o photocopyi tems for internal or personal use, or the internalo r personal use of specificc lients, is granted by the American GeophysicalU nion for librariesa nd other users reg- istered with the CopyrightC learance Center (CCC) TransactionalR eportingS ervice, provided that the base fee of $1.50 per copy plus $0.35 per page is paid directlyt o CCC, 222 Rosewood Dr., Danvers, MA 01923. 0733-9569/05/$1.50+0.35. This consentd oes not extend to other kinds of copying,s uch as copyingf or creating new col- lective works or for resale. The reproductiono f multiplec opies and the use of full articleso r the use of extracts, includingf igures and tables, for commercial purposes requires permissionf rom the American GeophysicalU nion. Printed in the United States of CONTENTS Preface Erik Kristensen,R alf R. Haese, and Joel E. Kostka ............... vii Introduction E. Kristensen, R. R. Haese, and J. E. Kostka ..................... 1 Plant-Microorganism-Sediment Interactions 2 Interactions Between Benthic Macroalgal and Microalgal Mats Kristina Sundbiicka nd Karen McGlathery ...................... 7 3 Plant-Microbe Interactions in SeagrassM eadows Carlos M. Duarte, Marianne Holmer, and Ntiria Marba ........... 31 Belowground Interactions Among Salt Marsh Plants and Microorganisms Charles R. Lovell ........................................ 61 5 Mangrove-Microbe-Soil Relations Daniel M. Alongi ........................................ 85 Animal-Microorganism-Sediment Interactions 6 BiogenicP article Reworking and Bacterial-Invertebrate Interactions in Marine Sediments M. Solan and B. D. Wigham ............................... 105 7 Macrofaunal Burrows and Irrigation in Marine Sediment: Microbiological and BiogeochemicalI nteractions E. Kristensen and J. E. Kostka ............................. 125 BiogeochemicalC onsequenceso f Infaunal Activities Yoko Furukawa ......................................... 159 Macro- and Microorganism Interactions and the Structuring of Benthic Communities Interactions Between Microorganisms and Intertidal Plant Communities J.P. Bakker,T . J. Bouma, and H. J. van Wijnen ................. 179 10 SeagrassR hizosphereM icrobial Communities RichardDevereux ....................................... 199 11 Setting Diversity and Community Structure in Subtidal Sediments: The Importance of Biological Disturbance S. Widdicombe and M. C. Austen ............................ 217 12 Plant-Animal-Microbe Interactions in Coastal Sediments:C losing the Ecological Loop Roberta L. Marinelli and George G. Waldbusser. ............... Deep-Sea Communities of Macro- and Microorganisms 13 AllochthonousD eep-Sea Benthic Communities: Functioning and Forcing Olaf Pfannkuche ........................................ 251 14 Interactions Between Fluid Flow, Geochemistry,a nd Biogeochemical Processesa t Methane Seeps W. Ziebis and R. R. Haese ................................. 267 15 Biotic Interactions and Feedback Processesin Deep-Sea Hydrothermal Vent Ecosystems R. J. Ldveilld,C . Levesque,a nd S. K. Juniper .................. 299 Models of Interactions Between Macro- and Microorganisms 16 Modelling Mixing and Diagenesis Bernard P. Boudreau ..................................... 323 17 Incorporating Ecologicala nd BiogeochemicalI nformation Into Irrigation Models Carla M. Koretsky,C hristofM eile, and Philippe Van Cappellen ................................... 341 18 Modelling Biological Interactions in Aquatic Sedimentsa s Coupled Reactive Transport Filip J. R. Meysman,O leksiyS . Galaktionov, StepbaneM adani, and Jack J. Middelburg .................... 359 List of Contributors ................................................ PREFACE Interactionsb etweenm acroorganism(sb enthicf aunaa nd macrophytesa) nd the biogeo- chemistrya nd microbiologyo f aquatics edimentsh ave provede ssentialf or the function- ing of most benthic marine ecosystemsW. hile our knowledge of the biogeochemical consequenceosf macrobiologicaal ctivity has grown considerablyd uring the last two decadest,h e feedbackm echanismsa ndp hysicochemicafol rcesc ontrollingt he abundance and diversityo f benthica nimalsa nd plantss till eluded efinitivea nalysis.I n ordert o clar- ify the stateo f the sciencea ndp rovidea frameworkf or futurer esearchw, e presentin this volume a synthesiso f latest developmentsin researcho n interactionsb etweena nimals, plants, and microorganismsin marine sedimentarye nvironments( including intertidal areas,c ontinentasl helvesd, eep-seas edimentsa, nd cold seeps).O f particulari mportance are the new experimenta(lf ield studiesl,a boratorye xperimentsa) nd theoretica(l modeling) approachesw, hich we alsod iscuss. The book is intendedf or a broad audiencew ithin science,e ngineeringe, ducation,a nd resourcem anagementI.n teractionsb etweenm acro- and microorganismsa nd their effect on water quality and ecologicalf unctioningh ave recently received significantr esearch attention,b ut coastala nd marinem anagersh ave only startedt o recognizet he importance of the issue for environmentaml anagementW. e, therefore,h ope that this volume will proveu sefult o professionalisn thesef ields and can be useda s a basico r supplementary textbooka t universitiesa nd engineerings chools. The volume grew out of a special session,t itled "InteractionsB etween Macro- and Microorganismsin Aquatic Sediments,"t hat we (the three editors)c onveneda t the 2002 ASLO/AGU Ocean SciencesM eeting in Honolulu, Hawaii. The quality of talks and the large audiencem ade clear that our efforts had been successfual nd that information on theset opicss houldb e madea vailablet o a wider audienceT. hesec onsiderationsto, gether with encouragemenftr om AGU, gave birth to the currentb ook. Given the need for an authoritativea ccounto f the researche, xperimentationa,n d modelinga pproacheisn use, we invited renowneds cientistst o contributec hapterso n their own fields of expertise, allowingf or completec overageo f the topici n an interdisciplinarcyo ntext:a comprehen- siveo verviewo f interactionsb etweenm acroscopico rganismsa nd microbialc ommunities in marine sedimentsa; n integrationo f biogeochemicaal nd ecologicalk nowledge.A s a result, the volume complementsb, ut does not overlap, other recent texts on benthic biogeochemistroy r benthice cology. We could not have completedt his book without the assistanceo f many people and organizationsW. e, thereforew, ish to thankt hosei nvolvedi n all stageso f the processp, ar- ticularlyt he reviewers( PaulA dam, RobertA ller, Gary Banta,P eterB erg, Mark Bertness, David Billett, Eric BoschkerD, avid Burdige,J aneC affrey,J eff Chanton,T ony D'Andrea, Daniel Desbruy(cid:127)res,R ich Devereux, SergioF agherazzi,S tefanF orster,Y oko Furukawa, Mark Hines, Rick Lovell, Filip Meysman,C arla Koretsky,K irsten Kuesel,H eath Mills, Lois Nickell, Emil Olafsson,D eniseR eed, Danny Reible, Bill Savidge,F rank Wenzh6fer, Macro- and Microorganismsin Marine Sediments Coastal and Estuarine Studies 60 Copyright2 005 by the AmericanG eophysicaUl nion 10.1029/60CE01 Roman Zajac, Anne Thistle, and six who remain anonymous)w, hosei ndispensablhe elp has significantlyi mprovedt he quality of individualc haptersa nd of the book as a whole. Erik Kristensen Ralf R. Haese Joel E. Kostka Editors Introduction E. Kristensen, R. R. Haese, and J. E. Kostka Abstract Interactionsb etweenm acro- and microorganismisn volveb iogeochemicaal nd ecologi- cal consequenceosf macrobiologicaal nd microbiologicala ctivity as well as feedback mechanismsc ontrollingt he abundancea nd diversity of benthic microbial, meiofauna, macrofaunaa, nd plant communitiesT. his volume attemptst o combinef ield observations with experimentala nd model resultst o presentt he current knowledgea nd the latest discoveriesa bout how marine macroorganismsr,a nging from rooted mangrovet rees to deep-seaf auna,i nteractw ith the many microorganismisn the nearbys edimentT. he inter- actionsr angef rom predationt hroughn onobligatoryc ommensalismm, utualisma, nd com- petitiont o strictlys ymbiotics ystemsT. he chaptersa re dividedi nto five thematics ections devotede ithert o particulart ypeso f organismso r to particularc ommunities. Many exampleso f interactionsb etweenm acro- and microorganismasr e well known, but mosto f thesea re obviouss ymbioticr elationshipisn whicht he partnersd ependh eavily on one another.A n example is the symbiotica ssociationb etween sulfide- or methane- oxidizing bacteriai n specializedo rganso f gutlessf auna in deep-seav ent communities. Lessi ntimatea ndm uch more numerousr elationsb etweeno rganismsw ith differentm etab- olisms,t rophicf unctions,a nd sizesa s well as interactionsb etweeno rganismsa nd their geochemicael nvironmenat re oftenc omplexa nd canb e elucidatedin many caseso nly by comprehensivien terdisciplinarys tudies.M ost interactionsb etweenm acro- and micro- organismsm ustb e emphasizedt,h ereforei,n the frameworko f sedimentaryo rganicm atter transformationt, he structureo f benthic communities,a nd benthic nutrient dynamics.I n this context,i t is importantt o focuso n biogeochemicaal nd ecologicalc onsequenceosf macrobiologicaal nd microbiologicaal ctivitya s well as physicochemicafol rcesa nd feed- back mechanismcso ntrollingt he abundancea nd diversityo f benthicm icrobial,m eiofauna, macrofaunaa, ndp lant communitiesS. tateo f the art techniquesa re neededf or the studyo f specifici nteractionsO. f particulari nteresti n this respecta re numericalm odelsa nd the applicationo f new moleculart echniquesfo r phylogeneticid entificationo f microbialc om- munities associatedw ith various types of macroorganismsT. he presentv olume is an attemptt o combinef ield observationws ith experimentala nd model resultst o highlight strengthsa nd discrepancieos f variousr esearcha pproachesw ith respectt o interactions betweenm acro- and microorganismisn marine sediment,w hich, we hope, will lead to valuable recommendations for future research in the field. Macro- and Microorganismsin Marine Sediments Coastal and Estuarine Studies 60 Copyright2 005 by the AmericanG eophysicaUl nion 2 INTRODUCTION The structureo f the booki s intendedto presenct urrentk nowledgea ndt he latestd iscov- eriesa bouth ow macroorganismrsa,n gingf rom rootedm angrovetr eest o deep-seafa una, interactw ith the manym icroorganismins the nearbys edimentT. he interactionrsa ngef rom predationt hroughn onobligatoryc ommensalismm, utualism,a nd competitionto strictly symbiotics ystemsT. he chaptersa re dividedi nto five thematics ectionsd evotede ithert o particularty peso f organismos r to particularc ommunitieasn df ocuso n how theses ystems can be describede xperimentallya nd theoreticallyH. ere we provides hortg limpseso f the articlesi n eacht hematics ectionf ollowingt his introduction(s ection1 ) and try to empha- sizeh ow andw hy the variousc ontributionasn ds ectionsa re organizeda st hey are. Benthicp lantc ommunitiesa reg enerallyc onsideredto be "nutrientf ilters"t hati ntercept or remove land-derivedn utrientsa long the land-to-seac ontinuum,t hereby regulating water colunto primary productiona nd modifying trophic structurei n coastal marine ecosystemsH. owever,t he physicala nd biologicalc omplexityo f thesee nvironmenthsa s madei t difficult to predictt he factorsc ontrollinge lementalc yclingp rocessesa,n d the mass balance of sourcesa nd sinks of carbon and nutrients remains uncertain. In section 2, ther elationshipbse tweenp lantso r thep redominanbt enthicp rimaryp roducers(a lgae,s ea- grassess, altmarshg rassesa, nd mangrovet rees) and microorganismisn mediatingd ia- genetic reactions and nutrient cycles of shallow marine sedimentsa re reviewed. The compiledr eviewsp rovidet he latesti nformationo n the longstandinvgi ew that inter- tidal and subtidalp lant communitiesa re an importantc onduit for chemicale xchange between the sedimentsa nd the overlying water column or the atmosphereC. ommon themesr esonatet hrougha ll of shallowm arinep lant communitiesd iscussedF. oremost amongt hesei s that plant communitiesa ct as a primary sourceo f organicm attera t the sediment-wateinr terfaceP. lantsa lsol argelyi mpactm icrobiallym ediatedr edoxr eactions by injectingo xygeni nto subsurfacsee dimento, r in the caseo f algal mats,t hey may con- tributet o the generationo f anoxiab y coveringa nd sealingt he sedimenst urface. Sundb(cid:127)ick and McGlathery examinet he modes of interactionb etweenm acro- and microalgaml ats,e speciallya s the interactioncso ntributeto nutrientc yclinga ndr etention in shalloww aters.T hey observet hat the two mat typesi nteractd irectlya nd indirectly throught heir impactso n light, oxygen,a ndn utrientd ynamicsO. xygend eficiencyb elow densea nd decomposingm acroalgalm ats causesa shift towarda noxicm icrobialm eta- bolism and increasedn utriente ffiux from the sediment,t herebyp roducinga feedback mechanismth at favorsm acroalgagl rowth.O verall,m atsa re shownt o be temporarys inks for inorganicn utrientsth atr educee ffiux of nutrientso ut of the sedimentsth, erebyd ecou- pling benthica nd water columnn utrientt urnover. Duarte and colleagues review the ecology and biogeochemistryo f seagrass- microorganismin teractionsin sedimentsf,o cusingo n the rhizospherea nd its associated microbialp rocessesT.h e authorsb eginb y describingth e interdependencoef root/rhizome productions, edimentc hemistrya, nd nutrientd ynamicsin seagrasbs eds.K ey microbial processess,u cha s sulfater eductiona ndn itrogenf ixation,a re shownt o be tightlyc oupled to the growths tateo f seagrassesS.u chp rocesseds emonstratae symbioticr elationship betweens eagraspsl antsa nd sedimentarmy icrobesth at is regulatedb y carbona ndn utri- ent exchangein the rhizosphereS. eagrassse dimentasr er evealeda sh ot spotso f microbial activity,n ot only becauseo f root-microbere lationsb ut alsod ue to the trappingo f plank- tonic organicm atterb y the seagrassc anopy. Feedbacksb etweent he plant rhizospherea nd microbialc ommunitiesa re furtherd is- cussedf or saltmarshe cosystemfsr om a microbiologist'ps erspectivein the chapterb y Lovell. Consideringa ll of the marine plant communitiesc overedi n this volume, more informationo n sedimentarym icrobialc ommunitiesis availablef rom saltmarshesT.h us, the communityc ompositiono f microorganismthsa tc atalyzec arbona ndn utrientc ycles KRISTENSEN ET AL. 3 discussedin detail. Similar to seagrassb eds, nitrogenf ixation and sulfater eductiona re implicateda s key processesin the saltmarshr hizosphere,a nd this chapterr evealst hat sulfate-reducerpsl ay a dual role in catalyzingb oth thesep rocessesT. he authora lsoi ndi- catest hat a larged iversityo f aerobica nd anaerobicb acteriam ay be simultaneouslya ctive in supportingn itrogenf ixationi n the marshr hizosphereH. e concludesth at the physically and chemicallyc omplexr hizospherem icroenvironmenst upportsa diverse,d ynamic,a nd still mostlyu nidentifiedm icroflora. A!ongi points to the highly efficient interrelationshipsb etweenm icrobial processes, sedimentb iogeochemistrya,n d mangrovet reesa s a major factor in explainingw hy man- grove forestsm aintain a high productivityi n otherwiseo ligotrophice nvironmentsH. e explainst hatb iogenics tructuresp, rimarilyc rabb urrowsa ndt ree roots,c oupledw ith tidal flushing,f oster spatiallyc omplexp atternso f organicm atter decompositiona nd nutrient cycling on the forest floor. Though sulfater eductionh as been consideredto be the pre- dominanto rganicm atter degradationp athway that is tied to root activity in mangrove sedimentsr,e cente videncei ndicatest hat microbiali ron and manganesere ductionm ay be importanti n closea ssociationw ith rootsa nd crab activitiesA. longi considersth e driving factors in plant-sedimentr elationsi n mangrovef orestst o be high nutrient and water requirementsn eededt o fuel high rateso f tree photosynthesis. Section 3 takes a closer look at how the activities of benthic animals interact with the sedimenta ndi ts associatedm icroorganismsF.o r many years,t he scientificc ommunityh as knownt hatb enthica nimals,p articularlyt he infauna,s ubstantiallya ffecta lmosta ll marine sedimentsf rom the intertidal zone to the deep sea. These burrowingc reaturesa ctively move aroundi n the sedimentw, heret hey construcbt urrowsa ndt ubes,i ngestt he sediment to obtainf ood in the form of microorganismsa,n d pump oxygenatedw ater into otherwise anoxic sedimentb y irrigation.A ll these activitiesh ave profounde ffects on the micro- biology andb iogeochemistroyf the sedimentsw, hich, in many cases,r esulti n both posi- tive and negativef eedbackc ontrolso n the macrofaunait self. The chaptersi n this section review currentk nowledgeo f thesei nteractionsa nd emphasizeth e latestd evelopmentsa nd suggestionfso r future studies. Solan and Wigham focuso n the role of sedimentr eworkingb y benthica nimals.T hey discussth e mechanismso f particled isplacemenat nd the ways bacterialc ommunitiesa re affectedb y sucha ctivities.C learly, bacteriala ssemblageisn habitingm arineb enthics ys- tems potentiallyr epresenta mechanisticl ink between macrofaunald iversity and key ecosystemp rocessesT. he interactionb etweenm icro-, meio-, and macrofaunao ften has significanti mpacts on sedimentp rocessesi,n cluding sedimentt ransport,n utrient flux, contaminantm obilization,a nd organicm atter remineralizationT. he authorsb elieve that new and imaginativei nterdisciplinaryre searchis neededt o solvet he empiricalc hallenge of discerningth e connectionb etweena nimal-mediatedp articlet ransportb, acteriala ssem- blages,a nd the integrityo f ecosystemfu nction. The role of biogenics tructuresin organismailn teractionsin sedimente nvironmentsis pursuedf urther in the chapterb y Kristensen and Kostka. The authorsr eview current understandingo f how the structurea nd functiono f irrigatedb urrowsa ffect the composi- tion of microbialc ommunitiesa nd associatedb iogeochemicapl rocessesin marine sedi- ments. The trophic mode of burrow inhabitantsi s clearly important, as it controlst he burrow structurea nd irrigationr ate. Irrigation affectss ubsurfacem icrobialr eactionsb y translocationo f electrona cceptorsin to andi nhibitorym etaboliteso ut of the sedimentT. he authorse mphasizeth at microbialc ommunitiesa roundb urrows tructuresm ustn ot be con- siderede quivalentt o thosei n surficials edimentsb ecauseo f large differencesin environ- mental conditions, but generalizationsa bout direct relationshipsb etween burrows, irrigation,a ndt he distributiono f microorganismasr ep rematureM. uch progressis 4 INTRODUCTION to resultf rom new and excitinge xperimentatlo ols,s ucha s microsensorasn d cultivation- independenmt oleculart echniques. Furukawa pointso utt he importanceo f oscillationsin ducedb y the intermittenat ctivity burstso f infaunaf or interactionsb etweeno rganismsin sedimente nvironmentsb, ut notes that manyo f the existingr esultsa ndc onclusionrse mains ite- and species-specifbice cause of the diversea nd highly interrelatedw ays in which sedimentaryin faunai nteractw ith transportr,e action,a ndm icrobialr egimes.S her ecommendtsh att he currente ffortsa t bio- geochemicadl escriptiono f burrowe nvironmentasr e combinedw ith a functional-group classificationto achievea more generalizedu nderstandingo f burrowe nvironmentsS. he alsoa dvocatesa complete,q uantitatived escriptiono f complex,i nterdependenptr ocesses througha comprehensivec,o mputationaml odel framework--a topic dealt with in more detail in the last section of this book. The first two sectionso f the book largely emphasizeo rganismarl elationshipsfr om a biogeochemicaal nd microbiologicapl erspectiveC. onverselys, ection4 is intendedt o compilei nformationo nh owt hei nteractionasf fectt hee cologicasl tructuroe f benthicc om- munitiesi n marine environmentsT. he interactionsin clude impactso f microbiallyp ro- ducedc ompoundosn growtha nds urvivalo f animalsa ndp lantsa sw ell asf eedbacke ffects of animalsa ndp lantso n the functionald iversitya nda ctivityo f microbialc ommunities. The chapterb y Bakker and colleaguesfo cuseso n the interactionb etweenp lantc om- munitiesa ndm icroorganismins intertidals altm arshesA. n importanct onsideratioinn inter- tidal areasi s the elevationagl radiento r the degreeo f inundationw, hichr epresentas stress gradient,e speciallyw ith respectt o soil chemistryM. arsh plantsh avem arkedlyd ifferent roots trategiesd,e pendingo n elevationin them arsha, nda rec haracterizebdy a suiteo f traits thatv aryw ith elevations, ucha sr oota rchitecturero, otl ongevitya, ndr ootp orosityA. ll these traits stronglyi nfluencet he microbesl iving in the sedimentt hroughe ffectso n oxygen, carbon,n utrient, and water availability.M icrobial mobilizationa nd immobilizationo f nutrientso, n the otherh and,m ay controlp lant-communitcyo mpositionb y changingn utri- ent availabilitya ndt hust he outcomeo f competitiona mongp lants peciesfo r nutrientsT. he role of microorganismisn nutrienta vailabilityi s illustratedb y a relevantc ases tudy. Interactionbs etweenm icroorganismasn dt he rootso f submergevda sculapr lantsa ret he focuso f the chapterb y Devereux. By releasingp hotosyntheticalldye rivedo xygena nd organicc arbont hrought heir roots,t hesep lantss timulatet he rhizospherem icrobialc om- munitiesT. he carbons upplyin creasehs eterotrophiacc tivity,p articularlys ulfater eduction. Becauses ulfater eductionis tightly coupledw ith nitrogenf ixation,a synergistirce lation- shipi s possibleb etweent he plantsa nd sulfate-reducinbga cteriaL. eakageo f oxygenf rom ther ootsm ay solvet hep roblemo f sulfidet oxicityt o thep lantsb y oxidizings ulfideb efore it enters the root tissue. Much remains to be learned about interactions between microbial communitieisn rhizospheresh,o weverT. his chaptera rguesth at a betteru nderstandinogf the microbiale cologyi n the seagrasrsh izosphercea np roveu sefulf or determiningfa ctors that lead to seagrassd ecline. In the chapterb y Widdicombe and Austen the focusi s changedt o benthica nimal communitiesin unvegetateds edimentsT. he authorss how that biologicali nteractions, particularlyt hosem ediatedb y bioturbationa ctivities,p lay a centralr ole in structuring macro-,m eio-, and microbenthicc ommunitiesA. lthougha ll organismsc reated isturbance simplyb y theirp resencet,h eb ioturbationa ctivityo f particularo rganismcsa nc learlyh ave a disproportionatellya rge effect. These organismsk, nown as ecosysteme ngineersc, an modify,m aintain,a nd/orc reateh abitats.C urrentt heoreticarl elationshipbs etweend istur- bancea ndd iversitya lsom akec leart hat seasonaal nd spatialp atchinesisn the distribution of bioturbatingo rganismsc an influencec ommunityh eterogeneitya nd maintains pecies

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