Disturbance to Marine Benthic Habitats by ... - Paul K. Dayton Lab

Disturbance to Marine Benthic Habitats by Trawling and Dredging: Implications for Marine Biodiversity Author(s): Simon F. Thrush and Paul K. Dayton Source: Annual Review of Ecology and Systematics, Vol. 33, (2002), pp. 449-473 Published by: Annual Reviews Stable URL: http://www.jstor.org/stable/3069270 Accessed: 16/07/2008 00:56 Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at http://www.jstor.org/page/info/about/policies/terms.jsp. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at http://www.jstor.org/action/showPublisher?publisherCode=annrevs. Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed page of such transmission.

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Annu. Rev. Ecol. Syst. 2002. 33:449-73 doi: 10.1146/annurev.ecolsys.33.010802.150515 Copyright? 2002 by AnnualReviews. All rightsreserved

TO MARINE BENTHICHABITATS DISTURBANCE AND DREDGING:Implications for BY TRAWLING Marine Biodiversity Simon E Thrush' and PaulK. Dayton2

1NationalInstituteof Waterand AtmosphericResearch,PO Box 11-115, Hamilton, New Zealand; email: [email protected] 2ScrippsInstitutionof Oceanography,Universityof California,San Diego, La Jolla, California92093-0201; email:[email protected]

Key Words fishing,resilience,habitatstructure,bioturbation, benthic-pelagic coupling,biocomplexity * Abstract Thedirecteffectsof marinehabitatdisturbanceby commercialfishing have been well documented.However,the potentialramificationsto the ecological functionof seafloorcommunitiesand ecosystemshave yet to be considered.Softsedimentorganismscreatemuchof theirhabitat'sstructureandalsohavecrucialroles in manypopulation,community,and ecosystemprocesses.Manyof these roles are filledby speciesthataresensitiveto habitatdisturbance. Functionalextinctionrefersto the situationin which species become so rarethatthey do not fulfill the ecosystem rolesthathaveevolvedin the system.Thisloss to theecosystemoccurswhenthereare restrictionsin the size, density,anddistributionof organismsthatthreatenthe biodiversity,resilience,orprovisionof ecosystemservices.Oncethefunctionallyimportant componentsof anecosystemaremissing,it is extremelydifficultto identifyandunderstandecologicalthresholds.The extentandintensityof humandisturbanceto oceanic ecosystemsis a significantthreatto bothstructuralandfunctionalbiodiversityandin manycases this has virtuallyeliminatednaturalsystemsthatmightserveas baselines to evaluatetheseimpacts.

INTRODUCTION The marinebiota is remarkablydiverse.Therearewell over 50 phyla andonly one is strictlyterrestrial;all the resthavemarinerepresentatives.Interestingly,all these phyla had differentiatedby the dawn of the Cambrian,almost 600 million years ago, andall evolved in the sea. Since thattime the sea has been frozen,experienced extensive anaerobicconditions,been blastedby meteorites,and undergoneextensive variationsin sea level. Also duringthis time the continentalshelves have been fragmented,reshuffled,and coalesced in such a way that the biotic communities havebeenexposedto a wide arrayof environmentalconditions.Thepresentdiverse 0066-4162/02/1215-0449$14.00

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THRUSH* DAYTON biota reflectsthe combinationof historicalevents and presentphysical, chemical, and biological dynamics.We review structuralpatternsand functionalprocesses importantto the perseveranceof this ecosystem and discuss the impactof fishing on these patternsand processes. Whereas great attentionhas been paid to the decline in species diversity in terrestrialecosystems, it is apparentthattherehave also been substantialchanges in diversity in aquatic systems, albeit changes that may not be so readily detected. A common perceptionof marineseafloorbiodiversityreflectsa disproportionate interest in hard bottoms such as coral reefs, kelp forests, and the rocky intertidal.This bias is understandablebecause these hard-bottomcommunities lend themselvesto terrestrialcomparisonsandecological studies.However,about 70% of the earth'sseaflooris composed of marinesoft sediments(Wilson 1991, Snelgrove 1999). These soft-sedimenthabitatscan be highly heterogeneousowing to interactions between broad-scale factors (e.g., hydrodynamic and nutrientregimes) and smaller-scalephysical and biological features; nonetheless, the apparentthree-dimensionalhabitat structureimposed by this heterogeneity may not be as obvious as that observed on hard-bottomhabitats. Althoughthese habitatsdo not always appearas highly structuredas some terrestrial or marinereef habitats,they do supportextremely high species diversity (Etter & Grassle 1992, Grassle & Maciolek 1992, Coleman et al. 1997, Gray et al. 1997, Snelgrove 1999). In fact, the organismsthat inhabitthe sediments create much of the structurein soft-sediment habitats, ranging from the micro-scale changes aroundindividualanimalburrowsto the formationof extensive biogenic reefs. As well as adding substantivelyto the varietyof species found on earth,softsedimentmarineorganismshave functionalroles crucialto many ecosystem processes. The provision of protein for human consumption and the ecosystems that sustain fisheries are clear examples of the products and functions of marine ecosystems thatbenefithumankind.Otherprocessesin which marinebenthos play importantroles include their influence on sediment stability,water column turbidity,nutrientandcarbonprocessing,andcontaminantsequestering,as well as the provisionof pharmaceuticalsand nutraceuticalsand recreationaland amenity values. There is now good evidence that commercial fishing has a profound effect on marine ecosystems. Although there is a long history of concern about the environmentaleffects of fishing(Graham1953, de Groot 1984), it is really only in the pastdecadeor two thatecological researcheffortshave focused in this arena.In turnthis focus has spawneda numberof review articlesandbooks thatsummarize and synthesize the environmentaleffects of fishing (Dayton et al. 1995, Auster & Langton 1999, Jennings & Kaiser 1998, Watling & Norse 1998, Hall 1999, Kaiser& de Groot2000). This informationhas informedthe debateover fisheries managementand marineconservation,but it also highlights both the challenges and opportunitiesto test our currentunderstandingof interactionsbetweenbroadscale habitatdisturbanceto seafloorcommunitiesand the functioningof benthic ecosystems.

IMPACTS OFFISHINGONMARINEBIODIVERSITY 451 In this review we place studies of the environmentaleffects of fishing into the context of direct and indirecteffects on marinebiodiversity.We consider biodiversity to have both structuraland functionalcomponents.The distributionand abundancepatternsof landscapes,habitats,communities,populations,and genotypes form the structuralcomponentof biodiversity.Functionalcomponentsinvolve mechanismsthatdriveinteractionsbetweenspecies themselvesandbetween them and other componentsof the environment,as well as other processes generatingfluxes of energy and matter.We considerimpactson communitystructure andphysicalchangesin habitatstructurealong with functionalchangesto seafloor ecosystems (benthic-pelagiccoupling,nutrientrecycling,andbiogeochemicalprocesses). Ouraim is not to reviewthe literaturethataddressesthe issues of fisheries, marinebiodiversity,and the spatial and temporalscales of ecosystem resilience, but to draw togetherecological processes and fishing impacts to focus attention on new and integrativeresearchdirections.

Scale-DependantDisturbance Disturbanceregimes play a key role in influencingbiodiversity (Connell 1977, Huston 1994). In marine benthic habitats small-scale naturaldisturbanceplays an importantrole in influencingcommunitiesby generatingpatchiness (Dayton 1994, Hall et al. 1994, Sousa 1984). Many of the small-scale disturbancesthat impactbenthiccommunitiesand generateheterogeneityresultfrom the biological activitiesof organismsthatlive in or feed on the seafloor.The spatialheterogeneity createdby local disturbanceevents can account for resourcepatchiness (Thistle 1981, VanBlaricom 1982), andubiquityof opportunisticspecies in soft-sediment habitats. Such heterogeneity is an importantcomponent of the functioning of ecological systems (Kolasa& Pickett 1991, Legendre1993, Gilleret al. 1994) and has implicationsfor the maintenanceof diversityand stability at the population, community,and ecosystem levels (e.g., De Angelis & Waterhouse1987, Pimm 1991, Loehle & Li 1996). The fact thatnaturaldisturbanceis importantto soft-sedimentcommunitieshas led to the suggestionthatfishingdisturbancecan positivelyeffect biodiversity.This applicationof Connell's (1977) intermediatedisturbancehypothesisis not appropriatebecause this hypothesisis predicatedon disturbanceas a means of reducing resourcemonopolizationsuch that diversity is enhanced.Direct competitionfor food or space,however,has been difficultto demonstrateas an importantprocessin soft sediments,especially over broadspatialscales (Olafssonet al. 1994, Peterson 1979, Wilson 1991). Theoreticalconsiderationof the intermediatedisturbancehypothesis demonstratesthatthe effects of disturbanceon multitrophiclevel systems can, in many situations,have no effect on the coexistence of competitors,as necessitatedby the hypothesis, or may even cause a monotonicdecline in diversity (Wootton 1998). Furthermore,the intermediatedisturbancehypothesis has not been adequatelytested over broad spatial scales relevantto fishing disturbance. Thusits applicationacross species, communityandhabitattypes, andovervarious scales of disturbanceand recoveryis unfounded.

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Spatial heterogeneityin community structureis related to the spatial extent and/orthe frequencyof disturbanceevents;for disturbanceto createpatchinessit must be small relativeto the colonizationpotentialof the benthiccommunity,but not so small as to enable the adjacentassemblage to quickly infill the disturbed patch.This concept is encapsulatedin a simple ratio-basedmodel of the effect of disturbanceon landscapes(Turneret al. 1993). The temporaldimensionis considered by the ratio of disturbanceinterval(time between events) to recovery time, andthe spatialdimensionis consideredby the ratioof size of the disturbedareato size of the habitat.The model simplifiesmany of the complexitiesof disturbancerecoverydynamics and the potentialfor recoveryprocesses to change with scale in a nonlinearfashion. Nevertheless,considerationof these ratios indicates disturbanceregimes that, throughtheir frequency,extent, or intensity,could result in catastrophicchange across the seafloor landscape.Even such a simple model emphasizes the need to understandthe scales of mobility and the processes affecting successful establishmentand growth of potential colonists. Typically in soft sedimentsa wide arrayof species and life stages areinvolvedin recoveryprocesses withina disturbedpatch(Zajacet al. 1998, Zajac 1999, Thrush& Whitlatch 2001, Whitlatchet al. 2002). The ratio model implies that significantthreatsto the integrity and resilience of marine benthic communities arise when the rate of human-inducedchange exceeds the rate at which naturecan respond.This is particularlylikely to occur where habitatstructureand heterogeneityare reduced and large areas of habitathave been modified. Slow-growing and -reproducing species will be strongly affected, vastly reducing the potential for such species to reestablishthemselves or colonize new areas.The homogenizationof habitats and the loss of small-scale patchinessresult in the risk of the loss of ecological functionand naturalheritagevalues in marineecosystems.

Fishing as a DisturbanceAgent on the Seafloor Many types of trawls, dredges, and trapsare draggedover or sit on the seafloor (Jennings& Kaiser 1998). The type of physical impactthe fishing gearhas on the seafloordependson its mass, degree of contactwith the seafloor,and the speed at which it is dragged.The way the gearis designedandoperatedalso influenceshow it interactswith the seafloor and how many species other than the targetspecies the gearremovesfromthe seaflooror damagesin situ (i.e., by-catch).Not all types of gear are used in all locations, and the impactof the gear dependson the habitat in which it is used. Unfortunatelytherearelimiteddataon the locationandfrequencyof the areaof the seafloorswept by fishing gear.The data availableusually are based on broadscale fisheriesmanagementunits andnot necessarilyrelatedto the spatialvariation in seafloor habitatsor biodiversity.For example, Churchill(1989) summarized trawlingeffortoff the MiddleAtlanticBight, an areaof intensivefishingpressure. The rangeof effort was quite variablealong the coast because fishersdo not work wherethereareno fish, but some areasoff southernNew Englandwere on average

IMPACTS OFFISHINGONMARINEBIODIVERSITY 453 exposed to 200% effort. Another typical fishery in northernCaliforniatrawled across the same section of seaflooran averageof 1.5 times per year, with selected areas trawledas often as 3 times per year (Friedlanderet al. 1999). For a scampi fisheryon the continentalslope off New Zealand(200-600 m waterdepth),Cryer et al. (2002) calculatedthaton averageabout2100 km2of the seafloorwas swept each year by trawlers.The statistics suggest that within the study area trawlers swept about 20% of the upper continentalslope each year, althoughabout 80% of all scampi trawls were made in an area of about 1200 km2. In some areas the extent and frequency of disturbancecan be extreme, Pitcher et al. (2000) identifiesone harborin Hong Kong where every squaremeterof the seafloorwas trawledthreetimes a day. The ecological intensityof responseis also determined by the resident species; even low-intensity disturbancecan significantly affect sensitive species (Jenkinset al. 2001). The spatialdistributionof fishing effort on the seafloor is patchy,reflectingthe relative availabilityof the target species. In some cases refiningthe scale of measurementrevealshigherlevels of aggregation of fishing effort (e.g., Pitcher et al. 2000). Actually, we really do not know the global extent of disturbanceto the seafloorby fishing. However,the magnitudeof exploitationof global fishery resourcesprovides some importantclues as to the generalextentof disturbance,with about25-30% of the world'sfisherypopulations overexploitedor depletedand a further40% consideredheavily to fully exploited (Pauly et al. 1998). Often the scales of measurementof fishing effort (e.g., tens to hundredsof squarekilometers) are difficult to match with ecological effects, as they do not match well with the scales of variabilityin seafloor ecological communities.

Evaluating the Direct Effects of Habitat Disturbance by Fishing Manystudieshavebeen conductedto assess the directeffects of habitatdisturbance by trawlingor dredgingon benthiccommunities(Table1). These studieshavebeen conductedin a variety of habitatsand locations, generally in shallow water.We have reviewed a large numberof these studies to offer examples from a varietyof habitatsand locations, ratherthanattempta complete list. Ouraim is to provide a brief summaryof the rangeof effects observed.We hope this list, as well as previously mentionedreviews, offer the readeran entr6einto this literature.There are a numberof importantissues to considerwhen summarizingsuch a diverse array of studiesbecause they encompassa range of intensitiesand spatialand temporal scales of fishing disturbance.Study designs and assessment approachesare also widely different.We have summarizedstatisticallysignificantor nonsignificanteffects describedin theindividualpapersbutreferthereaderto Loftis et al. (1991) and Nelder (1999) for commentson "significance."We recommendthatreadersstudy papers of interestin detail to assess for themselves the magnitudeof ecological effects. Marinebenthicecosystems are often challengingsystems to study,and precise data are rare.Furthermore,the interpretationof results is frequentlydifficult.For

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THRUSH ? DAYTON TABLE 1 Summary of effects on subtidal benthic communities reported in recent assessments of fishing impacts Effects

Habitats/depths/location

Source

Removal of biogenic and physical habitatstructure Decreaseddiversity in trawledplots

Sand, 30 m depth; NorthwestAtlantic

Austeret al. 1996

Mud, 75 m depthand heavily trawled; 35 m less frequently trawled;IrishSea

Ball et al. 2000

Decreaseddensity of common echinoderms, polychaetes,and molluscs

Sand, 30 m depth; NorthSea

Bergman& Hup 1992

Direct mortalityof 5-60% for species following single passage of trawl Decreasednumberof organisms,biomass, species richness,species diversity,and biogenic habitatstructure

Sand/mud,10-45 m depth;North Sea

Bergman& van Santbrink2000

Gravelpavement,40-80 m depth;GeorgesBank; NorthwestAtlantic

Collie et al. 1997

6 of 10 common species decreasedin abundance

Sand/coarsesilt, 10-20 m depth;PortPhillip Bay, Vic., Australia

Currie& Parry1996

No consistenttrendsin epifaunaor infauna; high site-to-sitevariability Decreasedabundanceof large epifauna and infaunal species abundance

Sand/coarsesilt, 10-20 m depth;PortPhillip Bay, Vic., Australia

Currie& Parry1999

Sand, 10 m depth;Loch Ewe, Scotland

Eleftheriou& Robertson1992

Higherdensities of epifauna in lightly trawledarea; higherdensities of predator/ scavengerworms in heavily trawledarea Largeepifaunaremovedand damaged;bouldersdisplaced Temporaltrendsin community compositiondifferentiate underheavy fishingpressure No detectablechanges in macrobenthicfauna

Sand, 180 m depth;central California

Engel & Kvitek 1998

Pebble/cobble/boulder,200 m depth;Gulf of Alaska

Freese et al. 1999

Mud, 80 m depthfished and 50 m unfishedsites; North Sea

Fridet al. 2000

Sand, 10 m depth;Botany Bay, NSW, Australia Mud, 73-96 m depth; Gullmarsfjord,Sweden

Gibbs et al. 1980

Sand/mud,6-15 m depth; Firthof Clyde, Scotland

Hall-Spencer& Moore 2000

Overalldecreasesin biomass and abundance,but site and time interactiontermsmake detectionof effect difficult 70% reductionof mearla habitatover 4 years

Hanssonet al. 2000

(Continued)

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TABLE 1

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(Continued)

Effects


Source

No significanteffects on biomass or productionin area of low fishing pressure;under high fishing pressure, significantdecreasein biomass and production Decrease in infaunaland epifaunalbiomass, particularly bivalves and burrowingurchins, only detectedat high impact site

High impactsite muddy sand 55-75 m depth,low impact site sand40-65 m; North Sea

Jenningset al. 2001a

High impact site muddy sand 55-75 m depth,low impact site sandy40-65 m; North Sea

Jenningset al. 2001b

Decrease in density of epifauna and diversityin stable sand habitat;no effects detected in unstablesandhabitat

2 habitats:one stable sand with rich epifauna,the other mobile sand, 26-34 m depth; Anglesey Bay, IrishSea 2 habitats:one stable sand with rich epifauna,the other mobile sand, 26-34 m depth; Anglesey Bay, IrishSea

Kaiser & Spencer 1996

Largerindividualsand increased density of epifaunain unfished area

Sand, 18-69 m depth; English Channel

Kaiseret al. 1999

Loss of sessile, emergent,high biomass species, increasein small-bodiedinfauna

Gravel/sand;Isle of Man, Irish Seab

Kaiseret al. 2000

No effect detected

Sand, 120-146 m depth; GrandBanks of Newfoundland

Kenchingtonet al. 2001

Trawlreduceddensity of large epifaunaabout 15%on each pass; trawlflown 15 cm above seafloorhad no detectable impacton large epifauna Higherdiversityin unfishedarea; sedentarymacrofaunamore abundantin unfishedsites; mixed responseby motile species and infaunalbivalves

50 m depthc;north-west shelf, Australia

Moran& Stephenson2000

Sand,44-53 m depth; easternBering Sea

McConnaughey et al. 2000

Trawlstypically removed5-20% of large benthicfauna Short-termdecreasesin biomass and abundanceof macrofauna; numberof taxa showed no immediateeffect but increased in trawledarea after7 days

Sandb,GreatBarrier Reef Region, Australia Sand, 24 m depth; AdriaticSea

Pitcheret al. 2000

Slight changes in community compositionin stable habitat;no detectableeffects on a numberof species or diversityindices in eitherhabitat

Kaiseret al. 1998

Pranoviet al. 2000

(Continued)

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THRUSH ? DAYTON TABLE 1

(Continued)

Effects


Source

Decrease in epifaunalbiomass following disturbance;no significantimpactson dominant molluscs


Prenaet al. 1999

Decrease in species richness and diversity Decrease in small-scale heterogeneityof sedimenttexture aftertrawling Highernumbersof epifaunaand diversity,abundance,and biomass of macrofaunaoutside trawledarea

Mud, 30-40 m depth; Catalancoast

Sanchez et al. 2000


Schwinghameret al. 1996

Mud, 200 m depth;Crete

Smithet al. 2000

Changesin communitystructure, decreaseddensity of common bivalves and polychaetes, increaseddensity of nemerteans Density decreased,effects on numberof taxa detectedat one site only Fishing decreaseddensity of burrowingurchins,long-lived surfacedwellers, and diversity and increaseddensity of deposit feeders and small opportunists Numbersof species, individuals, and variousdiversityindices increasedin fished area

Mud, 60 m depth;Penobscot Bay, Maine

Sparks-McConkey& Watling2001

Sand, 24 m depth.Mercury Bay, New Zealand

Thrushet al. 1995

Variedsediments 1-48% mud, 17-35 m depth;Hauraki Gulf, N.Z.

Thrushet al. 1998

Mud, 30-35 m depth;Gareloch, Scotland

Tucket al. 1998

Barrelsponges (Cliona) significantlyreducedin abundance butrecoveredin 12 months

Low relief hard-bottomhabitat, 20 m depth;Georgia

VanDolah et al. 1987

No detectableeffect of trawling

Sand,PortRoyal (8 m depth) and St. Helena (30 m depth) sounds, S. Carolina Sand, 20-67 m depth;north IrishSea

VanDolah et al. 1991

Species diversity,richness,total numberof species decreased with increasedfishing effort Decrease in numericaldominants and changes in sedimentfood quality

Silty sand 15 m depth. DamariscottaRiver,Maine

asedimentswith a surfacelayer of slow-growingunattachedcorallinealgae. bdepthnot given. Csedimenttype not given.

Veale et al. 2000

Watlinget al. 2001

OFFISHINGONMARINEBIODIVERSITY 457 IMPACTS example, Pitcher et al. (2000) documentedthe removal of 7 tonnes of epifaunal biomass during experimentaltrawling,but were unable to detect significant changes by surveyingthe density of epifaunaon the seafloor.Whereasthe direct effect of such an impact on benthic communitiesappearsobvious, its magnitude has been difficultto evaluate with regardto other componentsof the ecosystem. There is often a failure to detect the effect of experimentalfishing disturbance in areas exposed to extreme naturaldisturbanceto the seafloor (e.g., storms or very strongtidal flows) (Hall et al. 1990, Brylinskyet al. 1994, Kaiser& Spencer 1996, DeAlteris et al. 1999). Effects are not always consistent across sites, even within studies. Given the variety of experimentaldesigns and habitats studied, these variationsin response are far from surprising.Nevertheless these studies emphasizea numberof changes in benthiccommunitiesincludingloss of habitatstructuringspecies, changes in species richness, and loss of large and long-lived organisms. One of the most conspicuous long-termphysical effects of bottom fishing is the homogenizationof the substratumand reducedspecies diversity(Veale et al. 2000). Thus, apartfrom all the usual difficulties of study design, the history of fishing disturbancecan make it impossible to controlexperimentalstudies. Some Europeanand Adriaticwaters have a long history of fishing by bottom trawling (de Groot 1984, Kaiser & de Groot 2000, Pranoviet al. 2000). Frid et al. (2000) consideredreportsfrom the NorthSea going back to the 1920s andconcludedthat fishingpracticeshavechangedbenthiccommunitiesin some partsof the NorthSea; in otherareasfishing impactscould not be evaluatedwithouta longer time series of data. Aronson (1989, 1990) arguedthat overfishinghas virtually eliminated the evolutionarilynew teleost predators,resultingin a rebirthof the Mesozoic-like system dominatedby echinodermsandcrustacea.Recentanalysesof fishpredation in the North Sea provide some supportfor this view (Frid et al. 1999). There is also a long historyof transformationof marinecoastal ecosystems in the western Atlantic (Steele & Schumacher2000, Jackson2001) and easternPacific (Dayton & Tegner1984, Dayton et al. 1998). There are few, if any,unfishedhabitatswith economicallyexploitablestocks outsidethe Antarcticregion (Daytonet al. 2000). Humandisturbancesthatexceed the rate of naturalrecoverydynamicshave been underwayfor decades and possibly centuries.Some marineorganismshave been driven to extinction by human activities (e.g., the Atlantic gray whale, the great auk). Othersare probablyclose to extinction,for example, the Irishray (Brander 1981), the barndoorskate (Casey & Myers 1998), and the white abalone(Tegner et al. 1996). A recent review listed 82 species and subspecies of endangeredfish in the United States (Musicket al. 2000). Over time, repeatedintense disturbance will select for species with appropriatefacultativeresponses, and communities are likely to become dominated by juvenile stages, mobile species, and rapid colonists. Such broad-scaledescriptionspointto the problemof identifyingeffects in ecological systems thatare potentiallyalreadyaffected.The importantpoint is that the potential for both direct and indirect effects on biodiversity cannot be ignored because of variabilityin ecological response across such a diverse array

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THRUSH? DAYTON of studies.As always, manipulativeexperimentsare useful but difficultto control properlyand limited in scope. The broader-scaleimplicationsof fishingimpactshave been inferredfrombenthic surveysand time-seriesdata(Reise 1982, Holme 1983, Langton& Robinson 1990, Cranfieldet al. 1999, Kaiser et al. 2000). One valuable approachto integratingexperimentalresults into broader-scalepatternsis to develop iterative proceduresandtest a priorihypotheseswith datacollected over broadscales. This process can providegood evidence of large-scalechange (Thrushet al. 1998). The use of effort data in the rapidly expandingtrawl fisheries of the eastern Bering Sea enabled McConnaugheyet al. (2000) to contrastareas with differentexposureto fishingdisturbanceandinvestigatethe long-termconsequencesfor benthic communities.They found that the numbersof sedentaryepifauna(animals such as anemones, soft corals, sponges, bryozoans,etc.) and diversity and the niche breadthof sedentarytaxa decreasedwith fishing.Mixed patternsof responsewere apparentfor mobile epifauna and infaunalbivalves, suggesting species-specific responsesbasedon life-historycharacteristics.It is importantto note thatthe clear changesrecordedin this studywere documentedin an areawith a high potentialfor storm-generatedwave disturbance,emphasizingthe value of carefully designed and analyzedassessments.

The Potentialfor FunctionalChangesin Biodiversity The studies described above provide evidence for direct changes in response to habitatdisturbanceby fishing,butwe mustalso considerthepotentialfor changesin the functionalroles played by organisms,communities,and ecosystems. Usually, as density declines the size of the individualsand their spatial distributionalso change;thus, althoughnot biologically extinct,they may be functionallyso, being unableto fulfill theirnaturalroles in communityand ecosystem function(Dayton et al. 1998). In soft-sedimenthabitatsthe creationof small-scale habitatstructureby biogenic features can play key roles in influencing diversity and resilience. Some benthic fishes, such as rays, have an importantinfluence on small-scale habitat structure(Van Blaricom 1982, Levin 1984, Thrushet al. 1994). Organismsthat live at the sediment surface or create mounds, tubes, and burrowswithin it also provide habitatstructureand frequentlyhave importantroles in the sequestering and recycling processes essential to ecosystem function.Studies listed in Table 1 provide evidence of direct effects on the density and distributionof such organisms; in some cases theyarethe most susceptibleto habitatdisturbanceby dredging and bottom trawling.As yet, however,there have been no direct assessments of the implicationsof the loss of these functionallyimportantspecies to ecosystem functionand resilience. Alterationto marine food webs throughchanges in the abundanceand size distributionof fish populationscould have importantconsequences for benthic communities.Many types of fish prey upon and disturbthe seafloor;all rays and

IMPACTSOF FISHINGON MARINEBIODIVERSITY

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some sharks and bony fishes that make up many importantdemersal fisheries (e.g., sparids, scorpaenids,labrids, gadoids, pleronectids)are importantbenthic predators,althoughtheir wider ecological role is rarely studied (but see Sala & Ballesteros 1997). Many fishes have life-history characteristicsthat make them extremely vulnerableto over exploitation,thus highlightingthe potentialfor the role of these animalsto be diminished.Jenningset al. (1999) examinedlong-term trendsin the abundanceof NorthSea demersalfishes and demonstratedthatthose species thatdecreasedin abundancecomparedwith theirnearestrelativematured later, grew larger,and had a lower potentialfor rapidpopulationincrease. Many importantdemersal fish stocks (gadoids, sparids,pleronectids,and scorpaenids) appearto show limited recoverabilityafter over exploitation (Hutchings2000). We do not have a good understandingof the role of broadercommunity- and ecosystem-level processes in the resilience of fish stocks. Declining density of a species is usually associatedwith reductionsin both the geographicdistributionand the size of individuals.Steele & Schumacher(2000) discussed the implications for marine food webs of historic fish stocks in the NorthwestAtlanticpossibly being an orderof magnitudehigherthanstocks in the last half of the twentiethcentury.Density changes of this magnitudecould result in a profoundlyalteredecosystem. Forexample,in the Gulf of Maine,the removal of top fish predatorsthroughintensivefishing apparentlyreleasedotherpredators such as crabs and starfish,thus changing the benthic communities (Witman & Sebens 1992, Steneck 1997). Fridet al. (1999) also providean examplethatlinks changes in the abundanceof fish to changes in benthos:Changesin fish biomass in the NorthSea appearto have resultedin changes in the taxonomiccomposition of benthos consumed by fish and an overall increase in predationpressure on benthos. However, such effects are difficult to identify without extensive study; trackingeffects throughmarine foodwebs is difficult because of the inherently complex interactionsand weak and indirecteffects (Micheli 1999). Fishing can also directlyalterthe physicalhabitatby influencingsedimentparticle size, resuspensionregimes, and biogeochemical flux rates (Churchill1989, Currie& Parry1999, Mayeret al. 1991, Palanqueset al. 2001). Sedimentquality is importantbecause of the intimaterelationshipbetween particle size and benthic communitystructureandfunction(Gray1974, Rhoads 1974, Whitlatch1980, Snelgrove& Butman 1994). One study found significantdeclines in some organisms (70% for scallops and 20-30% for burrowinganemones and fan worms) owing to a scallop-fishing-inducedshift in sediment (organic-richsilty sand to sandy gravel with shell hash) (Langton & Robinson 1990). Caddy (1973) also documentedthe smotheringof suspensionfeeders as a result of sedimentresuspendedby fishing.Othereffects includemodificationsto microbialactivity(Mayer et al. 1991, Watlinget al. 2001), resuspensionof contaminants,and increases in benthic/pelagicnutrientflux (Krost 1990). Trawling-inducedresuspensionof sediments in the Gulf of Maine has been hypothesizedto have changedthe natureof nutrientsupply from the seafloor with potentiallyecosystem-wide consequences on phytoplanktongrowth(Pilskalnet al. 1998).

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Habitat-StructuringOrganisms,Functions,and Biodiversity Interactionsbetweenhydrodynamicconditionsandthe benthichabitatdrivemany of the importantprocessesoccurringat the sediment-waterinterface.The increased dragcreatedby structuresprotrudinginto the near-bedwaterflow and active feeding currentsgeneratedby suspensionfeeders influencelocalized rates of erosion anddeposition(Eckman& Nowell 1984, Frechetteet al. 1989, Shimeta& Jumars 1991, Dame 1993, Wildish & Kristmanson1997). Common benthic suspension feedersincludea diversearrayof corals,bryozoans,sponges,gorgonians,seapens, echinoderms,brachiopods,and bivalves. Patches of these organismscan further modify hydrodynamicsover a wide rangeof spatialscales, significantlyinfluencing both the vertical and horizontalflux of food and larvae at the seafloor.Both the size of the organismsand the patch are importantfactors influencingthese interactions(Greenet al. 1998, Nikora et al. 2002). Bivalves expend high levels of energy drawing water over their gills to feed (Rhodes & Thompson 1993). Thus,suspension-feedingbivalvesarecapableof activelyremoving60-90% of the suspended matter from the horizontal particle flux (Loo & Rosenberg 1989). These bivalves package any particlesthat are unsuitablefor ingestion in mucous and eject them as pseudofeces, thus appreciablyinfluencingthe rate of particle depositionto the seafloor(Graf& Rosenberg1997). These processes createvariation in seafloorecosystems and add to theirbiodiversity(Cummingset al. 2001, Norkkoet al. 2001). Organismsthat live at the sediment surface,as well as the small-scale disturbancescreatedby benthic-feedingpredators,can also increasethe three-dimensional structureof the habitat.Forexample, small heterogeneitiesin sedimenttopography(e.g., tubesandburrows)andeven sparselydistributedepifaunacharacterize most soft-sedimenthabitats.Such structureat the sediment-waterinterface,along with variationsin sedimentparticlesize, is positively relatedto macrobenthicdiversity (Thrushet al. 2001). Spatiallythese small-scale featuresare often highly variable(e.g., Schneideret al. 1987) and can be importantto commerciallyvaluable species (Austeret al. 1995). The shearvastness of the areacovered by such habitatsresultsin an importantrole for these small-scalefeaturesin biogeochemical processes and species and habitatdiversity,and it is these elements that are most susceptibleto habitatdisturbanceby dredgingand bottomtrawling. Highly structuredhabitatscanproviderefugesforbothpredatorsandprey.Many studies show significantvariationsin predator-preyinteractionsassociated with variationsin habitatcomplexity(e.g., Woodin1978, Ruiz et al. 1993, Irlandi1994, Skilleter 1994). Habitatstructureinfluences predationrates on fish, particularly juvenile life stages (e.g., Heck & Thoman 1981, Persson & Eklov 1995, Rooker et al. 1998). Topographiccomplexitycan have a significantandpositive influence on the growth and survivorshipof juvenile life stages of commerciallyvaluable species, often as a result of reducedrisk of predation(Tupper& Boutilier 1995, Lindholmet al. 1999). On theAustraliannorthwestshelf, Sainsbury(1988) showed a decreasein the numberand varietyof epifauna,particularlysponges, collected


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over time as by-catch. This reductionwas associated with shifts in the fishery from high- to low-value species. A probableexplanationwas a positive role for epifaunain affectingthe survivorshipof the commerciallyvaluablefish species. In many cases the habitatsdamagedby trawlingprobablyconstitutevery important nursery areas for many species, often including some of the target species of fisheries(Turneret al. 1999). The importanceof habitat-structuringorganismsis not restrictedto shallow water because shelf-breakand seamount habitats can exhibit marvelous levels of habitatcomplexity generatedby biogenic structure.Even the deep-sea basins once consideredconstantand uniformexhibit high levels of both local biogenic complexity (e.g., Jumars& Eckman 1983, Levin & Gooday 1992) and regional diversity(Levin et al. 2001). Improvedtechnologies and the demandfor fish are opening up deep-waterhabitatsto exploitation.Cryeret al. (2002) provideempirical evidence of the large-scaleeffects of trawlingon a deep-watersoft-sediment system by demonstratingsubstantivedecreases in the diversity of large benthic invertebratesassociatedwith a continentalslope (a depth of 200-600-m) scampi (Metanephropschallengeri) fishery.This result emphasizes that the impacts on seafloorcommunitiesthathave been more readilydocumentedin shallowerwater are also occurringin deeper water.In these environmentseffects on biodiversity are likely to be exacerbatedbecause deep-sea communitiesare generallycharacterizedby life-historyadaptationssuch as slow growth,extremelongevity,delayed age of maturation,and low naturaladultmortality,and they exhibit slow rates of recoveryfrom disturbance. Deep-watercorals occur in the upperbathylzone throughoutthe world and are underthreatfrom humanactivity,particularlyfishing andoil exploration(Roberts et al. 2000, Rogers 1999). The biology of most of these deep-watercoral species is unknown,butthey appearto have exceptionallyslow growthandlow reproductive rates, with individual colonies being hundredsto thousandsof years old (e.g., Druffel et al. 1995). These thicket-formingcorals are often associated with a diverse fauna, and levels of diversity appearto be similar to those of shallow water tropical coral reefs. Squires (1965) reports the first detection of a deepwatercoral structurein the Pacific, at a depthof 320 m on the CampbellPlateau. These coral structuresgeneratedabout40-m-high relief on the seafloor.Lophelia pertusa is a deep-watercoral thatoccurs in discretepatcheshundredsof metersto severalkilometersin diameter,and up to 45 m high. Off Norway and the Faeroe IslandsLophelia reefs have severalhundredspecies in association, and with the exception of small areas off Norway, most have been heavily damaged (Roberts 1997). Seamountstoo have been the focus of intensive deep-waterfisheries. In the southernhemispherethese fisherieswereusuallyinitiatedto captureorangeroughy (Hoplostethusatlanticus).When the New Zealandfisherytargetingspawningaggregationsof orangeroughybegan, the trawlsbroughtup a great deal of benthic by-catch, but these levels decreasedwith repeatedtrawling(Probertet al. 1997). For the orange roughy fishery on seamountsoff Tasmania,Koslow et al. (2001)

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reporttonnes of coralline materialbroughtto the surface in a single trawl when fishinga new area.Surveysconfirmedcharacterizationsof changesin benthiccommunitiesbased on by-catch(de Forgeset al. 2000, Koslow et al. 2001). These authorsreportat least 299 species froma single shortseamountcruisenearTasmania; 24-43% of these were new to science. The benthicbiomassfromfishedseamounts was 83% less thanfrom lightly fished or unfishedhabitats.

Fluxes,EcosystemEffects,and Biodiversity Sedimentsplay importantroles in transformationand exchange processes of organic matterandnutrients.Forexample,sedimentson marinecontinentalshelves, while occupyingonly 7%of the areaof the planetcoveredby marinesediments,are responsiblefor 52%of global organicmattermineralization.Slope sediments(i.e., 200-2000-m depth,9% area)remineralizeanother30% (Middleburget al. 1997). These disproportionatelylarge contributionsto organicmattermineralizationreflect the importanceof biological activitywithinmarinesedimentsinfluencingsolute andparticletransport.By enhancingthe transportof labile particulateorganic carbonto subsurfacelayers within the sediment, organismsstimulateanaerobic degradationandso affect the formandrateat which metabolitesarereturnedto the watercolumn(Hermanet al. 1999). The seas abovecontinentalshelf environments typicallyreceive one thirdto half theirnutrientsfor primaryproductionfrom sediment (Pilskalnet al. 1998). These nutrientsarederivedfrom organicmatterdecay and nutrientremineralizationwithin the sediments,followed by moleculardiffusion or biological irrigationback into the watercolumn. The process of sediment manipulationby residentanimals(i.e., bioturbation)is the dominantmode of sediment transportin the uppercentimetersof oceanic sediments(Middleburget al. 1997). Solute pumping,burrowing,and feeding increasethe areaof the sedimentwater interface (Aller 1982). Bioturbationaffects the stability and composition of marine sediments and influences their role as geochemical sources and sinks (McCall & Tevesz 1982, Marinelli 1994, Bird et al. 1999). Thayer(1983) extensively reviewed estimates of the rate of bioturbationfor a wide varietyof marine organisms,with rates of sediment reworkingrangingfrom 5 x 10-5 to 2.1 x 106cm3day-1 per individualanddepthsto which sedimentwas reworkedranging from 0.1 to 400 cm. Largerorganismsplay a particularlyimportantrole in influencing sediment-reworkingrates (Thayer 1983, Sandnes et al. 2000). Typically animalsincreasethe particleexchangebetween waterand sedimentby a factorof 2 to 10 (Graf 1999). Direct disturbanceof the seafloor enhances the upwardflux of nutrientsby releasing pore-waternutrientsas a pulse, ratherthan a more steady release controlledby bioturbation(Pilskalnet al. 1998). Fanninget al. (1982) estimatedthata stormthatimposed sufficientenergy on the seafloorto resuspendthe top 1 mm of sedimentcould intermittentlyaugmentoverlyingproductivityby as much as 100200%.This depthof sedimentdisturbanceis muchless thanwhatoccursas a result of manytypes of trawlinganddredging.Dredgesusuallydisturbthe top 2-6 cm of

IMPACTS OFFISHINGONMARINEBIODIVERSITY 463 sediment,while the doorsthathold open trawlnets in the watercan ploughfurrows from 0.2-2 m wide and up to 30 cm deep in the sediment(e.g., Caddy 1973, Jennings & Kaiser 1998, Krost 1990). However,it is not appropriateto equate storm disturbanceswith fishingbecausethe lattermay involve a muchhigherintensityof disturbance,althoughits frequencyand extent will be highly location dependent. The rate and efficiency of bioturbationprocesses are determinedby interactions between organismsand between the organismsand their environment.The degree of particle flux enhancementvaries with faunal composition and density (Cadee 1979, Thayer 1983) in conjunctionwith organic carbonflux to the sediment (Legeleux et al. 1994). Interactionsbetweenbioturbationandmineralization processes in sedimentsarehighly nonlinearand are characterizedby the presence of strongfeedback loops between deposit feeders, their food, and their chemical environment(Hermanet al. 1999). Variationin largeburrowstructuresandanimal activity can result in markedlydifferentbiogeochemical fluxes, in terms of both rates and chemicals (Hughes et al. 2000). As well as influencingwater column production,bioturbationcan also affect the growth of benthic species that use this resource (Weinberg& Whitlatch 1983). Deposit-feeding typically controls the biological mixing of near-shoreand, probably,deep-sea sediments. Soetaert et al. (1996) measuredand modeled the total flux of 210Pbenteringthe sediment (used as a markerof particletransport)along a transectfrom 208-4500 m over the Goban Spur in the northeastAtlantic. Their analysis showed that between 8 and 86%of the particleflux was derivedfromnonlocalexchangeprocesses (i.e., active pumping/flowthroughburrows),with these processesmost importantin shallower waterswhere trawlingis most intense. Apartfrom burrowingand actively pumpingwater and particlesthroughburrows, animalscan also influencefluxesby modifyingsurfacesedimenttopography, which then interactswith sediment boundarywater flows. Huettel et al. (1996) demonstratedhow shrimpmoundsprotrudingfrom sandysedimentscan alterflow patternsto increasethe flux of fineparticulatematterinto the sediment.Smallpressure gradientsgeneratedby boundaryflow-topographyinteractionsalso increase the flux of oxygenated water into the pore waters of sandy sediments, thus increasingthe oxic volume of the sedimentsandaffectingbiogeochemicalprocesses (Forsteret al. 1996, Ziebis et al. 1996). Fromthese studies it is clear thatbioturbationis importantin ecosystem functioning. There is some evidence that bioturbationhas been a significant factor influencingthe evolutionandenhancementof marinebiodiversityover geological time scales. Regenerationof nitrogenfrom the seafloormay exceed inputs from freshwaterin the coastal zone (Rowe et al. 1975). The faster recycling of nutrients by increased rates of bioturbationover evolutionarytime scales may have contributedto the diversity of phytoplanktonand zooplanktonin the Mesozoic (Thayer 1983). Martin (1996) contends that elevated nutrientlevels associated withincreasedratesof oceancirculation,continentalerosion,andbioturbationhave played a key role in enhancingthe productivityand diversityof marine systems over the Phanerozoic(i.e., essentially post-Precambrian).

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Implicationsfor Researchand BiodiversityManagement We have tried to synthesize the effects of fishing disturbanceon the biodiversity of the seafloorby reviewing studiesof directeffects and discussingthe functional roles of soft-sedimentorganisms.In doing this we have summarizedimmediate effects that include changes in species diversityand ecosystem processes, habitat modification,and loss of predators.Because of the high variabilitywithin and between studies, there is no single definitive study that adequatelydescribes the rangeof impactsof fishing disturbance.Nevertheless,thereis evidence of effects on seafloorcommunitiesthathave importantramificationsfor ecosystem function and resilience. Whereas gatheringgood data on the magnitudeand extent of disturbanceat appropriatespatial scales is important,from both a scientific and management perspective,we have moved beyond the question of what the immediate effect of habitatdisturbanceby fishing is and now need to focus on the implicationsof loss of structuraland functionalbiodiversityover various space and timescales. Pitcher(2001) arguesthatthe only hope for fisheriesthemselves is to move their managementto a focus on ecosystem rebuilding.He contends that the goal of sustainableyield of single species in a fishery is a fundamentalmistake. The potential for the change in functionallyimportantecosystem processes leads us to ask very broadquestionsand test the generalityof many fundamentaltheories. The themes of scale, complexity,resilience, and strongcoupling of physical and biological processes in marinebenthicecosystems are pervasive. We have emphasizedthe functionalroles of marinebenthic organisms.To develop this themefurtherwe need a muchbetterunderstandingof the basic ecology of these species, how their ecosystem roles may be modified by their size, density, and spatial arrangement,and how these characteristicsenable them to cope with disturbance.The integrationof small-scale variationinto broaderpatterns is importantbecause we should expect thresholdeffects and nonlinearitiesin the multispeciesbiotic and environmentalprocesses that create biodiversity.For example, differencesin density and species among a functionallysimilar group of bioturbatorscan resultin differenteffects on biodiversity(Widdicombe& Austen 1999, Widdicombeet al. 2000). The potentialfor differentresponsesof macrobenthic assemblages to the presence of a large epifaunalbivalve under a numberof different physical regimes and local species pools has also been demonstrated (Cummingset al. 2001). We must use naturalhistoryand environmentalinformation to bothdesign andinterpretmechanisticstudiesbecauseresponsesareusually scale dependent(Thrushet al. 1999). Standingback from the detail and looking for moregeneraland abstractpatternsalso providesa basis for revealingemergent phenomena(Brown 1995). Natural systems have a great deal of structurein time and space, and it is importantto identify thresholdsof change in this structureand the processes it influencesto gauge ecosystem resilience. This means that our predictionsof the ecological consequencesof humanactivity in the marineenvironmentrequirean


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understandingof broad-scaleforcingfunctionsas well as knowledgeof the natural and life-history characteristicsof individualspecies. The removalof small-scale heterogeneityassociatedwith the homogenizationof habitatsis, by definition,loss of biodiversity.We arguethis is importanteven over the extensive sand-and mudflats of the seafloor that are often considered"featureless."Spatial mosaics that resultfromlocal biological disturbanceevents, as well as the organismsthatcreate them, can be obliteratedby intense broad-scaledisturbances.There are winners and losers in the ecological response to any disturbance,but a key issue is understandingecological heterogeneityand its role in modifying the consequences of habitatdisturbanceto ecosystem processes. We need to betterunderstandthe implicationsof naturaland anthropogenichabitatfragmentationandhow it relates to the intensity and frequencyof disturbance.Empiricaland theoreticalstudies addressingthis issue will need to integratebiogeochemistry,hydrodynamics,and ecology. Site historyand the effect of multiplestresseswill be particularlyimportantin many areasin orderto addressthe role of the residentspecies assemblage and environmentalcontext in affecting disturbance-recoverydynamics in fragmentedhabitats.Once the functionallyimportantcomponentsof an ecosystem are missing, it is extremelydifficultto identify and understandecological thresholds that are violated beyond the point of recovery,at which point the anthropogenic disturbancesare less obvious. Some knowledge of these issues will be necessary to address the more fundamentalquestion, "At what point are there ecosystem thresholdsbeyond which recoveryis unlikely?"Ecological systems can shift into alternativestates as a result of the loss of ecosystem functions, and we must be able to assess the consequences of these shifts in terms of loss of diversity and ecological services (e.g., Carpenteret al. 1999, Schefferet al. 2001). ACKNOWLEDGMENTS We dedicatethis review to the memory of Mike Mullin and Mia Tegnerfor their deep concernfor fisheriesand relatedconservationissues. We thankJudi Hewitt, VondaCummings,and Bob Whitlatchfor commentson the manuscriptand Mary Powers and Dan Simberlofffor theirinsightfulreviews. FRST CO1804 supported this research. The Annual Reviewof Ecology and Systematicsis online at http://ecolsys.annualreviews.org LITERATURE CITED Aller RC. 1982. The effects of macrobenthos tion anachronismsin the BritishIsles. Ecolon chemical propertiesof marine sediment ogy 70:856-65 and overlying water.See McCall & Tevesz, Aronson RB. 1990. Onshore-offshorepatterns of humanfishing activity.Palaios 5:88-93 pp. 53-102 AronsonRB. 1989. Brittlestarbeds: low preda- Auster PJ, Langton RW. 1999. The effects of

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