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Linking Biodiversity Above and Below the Marine SedimentndashWater Interface The organisms living on the ocean floor are linked to those living in the ocean above but whether or how the biodiversity in these two realms is linked remains largely unknown Author(s) PAUL V R SNELGROVE MELANIE C AUSTEN GUY BOUCHER CARLO HEIP PATRICIA A HUTCHINGS GARY M KING ISAO KOIKE P JOHN D LAMBSHEAD and CRAIG R SMITH Source BioScience Vol 50 No 12 (December 2000) pp 1076-1088Published by on behalf of the Oxford University Press American Institute of Biological

SciencesStable URL httpwwwjstororgstable1016410006-3568(2000)050[1076lbaabt]20co2Accessed 11-05-2015 0506 UTC

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1076 BioScience bull December 2000 Vol 50 No 12

Articles

Changes in the marine environment are evident ona global scale (McGowan et al 1998) and although bio-

diversity in the oceans is poorly described abundances anddistributions of both commercially exploited (Safina 1998) andnonexploited (Pearson and Rosenberg 1978) species havechanged Not only have major changes occurred but the rateof alteration of marine ecosystems appears to be accelerating(eg Cohen and Carlton 1998) Unfortunately the impact ofthese changes in biodiversity on the basic functioning of ma-rine ecosystems remains uncertain as does the oceansrsquocapacityto withstand multiple human disturbances (Snelgrove et al1997) The dynamics of many marine ecosystems as well asof important fisheries depend on close coupling betweenbenthic (bottom living) and pelagic (water column) organ-isms (Steele 1974) Our knowledge of the natural history ofthese systems remains limited and scientific interest in map-ping the diversity of organisms and how they live has beenmarginalized in recent years Given the expanding sphere ofhuman influence on the oceans it is imperative to understandnot only patterns of biodiversity and the extent to whichchanges in biodiversity are occurring but also how changes inthe benthic and pelagic realms might affect each other Theoceans provide many important ecosystem services includ-ing production of food stabilization of shorelines trappingand removal of excess nutrients and pollutants and cyclingof nutrients and organic matter How does biodiversityabove and below the sedimentndashwater interface influencethese services and will biodiversity loss on one side of the in-terface impact the services provided by the other

The sedimentndashwater interface (SWI) in marine ecosystemsis one of the most clearly defined ecological boundaries onEarth Many organisms in the water column such as salpsand jellyfish have flimsy and attenuated morphologies thatallow near-neutral buoyancy in their fluid habitat where hor-izontal advection turbulent mixing and gravitational set-tling dramatically influence the relative distributions oforganisms and transport of materials around them Physi-cal and chemical gradients in the water column (eg fromoxic to anoxic waters) occur over scales of meters or moreSurface waters are always well oxygenated and watersnear the bottom are usually well oxygenated except wherelarge amounts of decomposition occur and bacterial res-piration drives down oxygen concentration Below thesedimentndashwater interface the morphology of organisms andthe physical attributes of the environment differ markedly

Paul V R Snelgrove (e-mail psnelgrocariboumimunca) is an associate chair in fisheries conservation in the Fisheries and Marine Institute

Memorial University of Newfoundland St Johnrsquos Newfoundland Canada A1C 5R3 Melanie C Austen is a senior research scientist in the marine

biodiversity group at the Centre for Coastal and Marine Sciences Plymouth Marine Laboratory Plymouth PL1 3DH United Kingdom Guy Boucher

is a research director of the National Center for Scientific Research in the Biology of Marine Invertebrates Laboratory National Museum of Nat-

ural History 75231 Paris France Carlo Heip is acting director of the Netherlands Institute of Ecology and director of research of the Centre of Es-

tuarine and Coastal Research of the Netherlands Institute of Ecology 4400 AC Yerseke Netherlands Patricia A Hutchings is a principal research

scientist at the Australian Museum Sydney NSW Australia 2010 Gary M King is a professor of microbiology and marine science at the Darling

Marine Center University of Maine Walpole ME 04573 Isao Koike is a professor at the Ocean Research Institute University of Tokyo Tokyo 164

Japan P John D Lambshead is a principal research scientist in the Nematode and Polychaete Research Group Natural History Museum London

SW7 5BD United Kingdom Craig R Smith is a professor in the Department of Oceanography University of Hawaii at Manoa Honolulu HI 96822

copy 2000 American Institute of Biological Sciences

Linking Biodiversity Aboveand Below the MarineSedimentndashWater InterfacePAUL V R SNELGROVE MELANIE C AUSTEN GUY BOUCHER CARLO HEIP PATRICIA A HUTCHINGSGARY M KING ISAO KOIKE P JOHN D LAMBSHEAD AND CRAIG R SMITH

THE ORGANISMS LIVING ON THE OCEAN

FLOOR ARE LINKED TO THOSE LIVING IN

THE OCEAN ABOVE BUT WHETHER OR

HOW THE BIODIVERSITY IN THESE TWO

REALMS IS LINKED REMAINS LARGELY

UNKNOWN

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December 2000 Vol 50 No 12 bull BioScience 1077

Articles

Even the muddiest sediments are morelike solids than seawater with mixingfrequently controlled by biological ac-tivities such as feeding and burrowing(bioturbation) Infauna the organ-isms living within sediments such aspolychaete worms or shrimp-like crus-taceans are usually denser than thosein the water column because sur-rounding sediments remove the prob-lem of avoiding sinking Body formsare more robust to permit the bur-rowing that can be essential to exis-tence Physical and chemical gradientsare steep for example the transitionfrom oxic-to-anoxic sediments oftenoccurs on millimeter scales In addi-tion organisms and nutrients are usually orders of magnitude moreabundant in sediments than in over-lying waters materials sinking fromabove accumulate on sediments andfuel bottom-living organisms

Because of differing ecosystemstructure above and below the SWIthe ecologists who study these do-mains must use different techniquesand often ask different research ques-tions This specialization can oftenlead to scientific isolation of the twodomains For example a recent work-shop of hydrozoan specialists em-phasized the problem of duplicationof species descriptions by those fo-cusing on benthic versus pelagic stagesof a given species (Boero and Mills1999) Despite the dichotomy in re-search communities there are nu-merous strong connections across theSWI These are seen not only in life cy-cles (eg Marcus and Boero 1998)but also in the dissolved and particu-late materials that routinely cross thewaterndashsediment boundary (Figure 1)

Chemical energy for marine ben-thic systems is often provided bysingle-celled and chain-forming phytoplankton (algae)which are the dominant primary producers in the ocean Liv-ing cells may sink or be physically mixed to the bottom ordead cells may sink to the bottom as phytodetritus In sur-face waters crustaceans and other groups of zooplanktonfeed on phytoplankton and defecate fecal pellets whichmay then sink to the bottom and provide undigested phy-todetritus and associated bacteria as an important foodsource for the benthos Plant material from coastal envi-ronments such as seagrass mangal (mangrove habitat)

and salt marsh plant detritus may be carried away from thenearshore environment before sinking to the bottom andproviding another potential food source A less predictablebut sporadically important food source for the benthos is car-casses of fish whales and invertebrates that sink from thewater column above (Smith et al 1998) The benthos in turnhelps to recycle the nutrients required by the planktonic al-gae that fuel much of the oceanrsquos benthic and pelagic pro-duction (Graf 1992) Clearly individuals of different speciestraverse andor impact other species on more than one side

Figure 1 Schematic representation of abovendashbelow sediment linkages in shallowhabitat with structural vegetation (top) coastal areas without structural vegetation(middle) and open ocean systems (bottom) Stippled area denotes photic zone wherephotosynthesis is occurring

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of this interface but is biodiversity above and below the SWIinterface linked The goals of this article are to summarizethe state of knowledge concerning connections and direc-tionality of effects between organisms living above and be-low the SWI that may be related to biodiversity to identifyor hypothesize connections that are likely to be importantand to outline approaches that might clarify mechanisms ofacross-interface biodiversity linkages Specifically are thereldquowater column-downrdquo effects in which pelagic diversity af-fects sedimentary diversity Are there ldquosediment-uprdquo effectsin which the reverse is true The potential impact of globalchange processes on these relationships is reviewed separately(Smith et al 2000)

For this article we separate marine ecosystems into threedistinct groups based on potential relationships betweenabove- and below-SWI biota First shallow sedimentarysystems with structural vegetation such as mangals saltmarshes and seagrass beds support unique faunas andprocesses within this grouping we will also briefly considergreen algal and kelp beds which are primarily hard substratecommunities but occasionally contain sediments Secondwe consider nonvegetated shallow-water coastal systems inwhich wind and turbulence mix the water column to the SWIduring part of the annual cycle These habitats encompasshighly dynamic environments such as sand beds on ex-posed coastline and relatively quiescent muddy areas insheltered regions that are physically disturbed only rarely Fi-nally we consider open ocean systems in which mixing andlight never penetrate to the SWI We also divide organismsinto those that occur above or below the SWI and treat or-ganisms that live predominantly on or above the sedimentsurface (seagrasses and green algae salt marsh plants pelagicorganisms hyperbenthos etc) as above-SWI In making thisdistinction we acknowledge that many benthic species havea pelagic reproductive dispersal stage and some above-SWIspecies have a below-SWI component (eg salt marsh grassroots) or life stage (eg hydrozoans) In addition we con-fine our discussion of linkages to sedimentary benthic sys-tems and largely ignore hard substrate communities coralreefs and kelps except where sediments are present Wealso acknowledge that the information presented declinesas a function of ocean depth this pattern reflects not onlythe differences in present knowledge but also our best guessas to the strengths of linkages between above- and below-sediment biodiversity

The meaning of biodiversityIn keeping with common usage and the Convention on Bi-ological Diversity we define biodiversity in the broadestsense to encompass the variability of nature in terms of ge-netics species habitats and even ecosystems This usage iskept deliberately broad and is not confined to a unit assuch Some of the best examples of abovendashbelow linkages thatwe will summarize are known to directly involve only oneor a few species nevertheless we feel that they do representan aspect of biodiversity In more specific terms species

richness refers to numbers of species in an area and compositediversity refers to measures of species diversity that incor-porate not only species number but also how individuals areapportioned among those species (evenness) Commonmeasures of composite diversity include the ShannonndashWeiner (H) diversity index and Hurlbert rarefaction (ex-pected species or E[Sn]) Where possible we will use the spe-cific measure of diversity given in a particular study but theuse of different measures in different studies can make com-parisons difficult Moreover a change (or lack of change) inone measure does not always mean there is no change in an-other aspect of diversity We also consider diversity on mul-tiple scales following the conceptualization of Whittaker(1972) Within this framework alpha diversity is the diver-sity within a small relatively homogeneous area which forthe benthos is operationally the smallest scale sampled (thespatial scales of the smallest core sampler used) Clearly thisscale will vary depending on the organism size-fractionconsidered being smaller for bacteria than for urchinsGamma diversity is the total diversity of a region obtainedby integrating diversity across all patch types

Whittakerrsquos framework is useful for the many relevantscales (centimeters to hundreds of kilometers) but also re-flects a fundamental difference in pelagic and benthic realmsBenthic ecologists who tend to focus on habitat comparisonsand the associated communities usually sample alpha di-versity and sometimes extrapolate from these samples to es-timate gamma diversity The sampling units for most pelagicstudies (plankton tows) often cut across multiple patches inthe fluid and dynamic water column and thus may samplegamma rather than alpha diversity Indeed pelagic biologistsare more comfortable stating numbers of species in a givenarea of the ocean than are benthic ecologists who recognizethat very few bottom areas have been sufficiently sampledfor them to be confident that rare species have not beenmissed

Structural vegetation and connectionswith sedimentary biotaThere are approximately 50 described mangrove speciesand 45 species of seagrass but in both of these systems agiven area typically will contain only a few relatively com-mon species Kelp beds which occasionally have associatedsedimentary habitat are also dominated by only a few plantspecies although globally there are thousands of macroal-gal species There is evidence from research on seagrass(Edgar 1983) mangal (Gee and Somerfield 1997) and saltmarsh ecosystems (Levin and Talley in press) that differentfauna tend to be associated with different vegetation typesboth above and below the SWI However the above SWI di-versity of structural plants within a given location in the ma-rine environment is relatively low with one or only a handfulof species represented and even within these groups thereis often zonation of species with tidal and salinity variation

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December 2000 Vol 50 No 12 bull BioScience 1079

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Teasing out relationships between structural vegetationand sedimentary fauna is therefore difficult because the environmental conditions that regulate distribution of veg-etation may be more important in regulating the associatedfauna than the vegetation itself For example Hutchings etal (1991) found greater similarity between infauna associ-ated with different seagrass species within one patch than be-tween those associated with the same species of seagrass indifferent patches Similarly Collett et al (1984) demon-strated that local environmental conditions determine themacroinfaunal composition associated with the seagrassPosidonia australis along the Australian coast As a result ofoverriding environmental variables the species pool associ-ated with a patch of a given seagrass is often much smallerthan that associated with that seagrass species over a broaderscale Further evidence for an absence of a direct diversity link-age between above-sediment structure and below-sedimentbiota was found in a Fiji lagoon where above-SWI structuralcomposition is a poor predictor of below-sediment diver-sity (Schlacher et al 1998) In summary there are potentiallinkages between species associated with structural vegeta-tion and the sediment beneath (Figure 1) but evidencesuggests that linkages are coincidental in that both com-munities are affected by similar environmental variables Onecomplication in linking above- and below-SWI speciesnumbers and composition is seasonal and annual variabil-ity in below-SWI organisms

Structural vegetation Water column-down linkagesAlthough specific biodiversity links are poorly documentedthere are numerous examples of above-SWI vegetationstructuring the sedimentary environment below Sedimenttrapping and water flow baffling by structural vegetation canoften alter the grain size of sediments near the vegetationGiven that sediment grain size is a major delimiter of infaunaldistribution there should be a clear linkage of structural veg-etation to below-SWI biodiversity and composition Pro-ductivity of vegetated habitats often exceeds that of adjacentareas Stimulation of microbial growth by root exudatesmay enhance resources and diversity of nematodes andother below-SWI organisms particularly in seagrasses (Os-enga and Coull 1983) A recent study found little variationin sedimentary species colonizing litter from different man-grove species but some differences depending on which liv-ing mangrove species the litter was associated with (Gee andSomerfield 1997) Variability in sedimentary fauna was at-tributed to the root structure and geochemistry of the man-grove species Structural vegetation can also depress diversitylarge detrital production combined with the reduced wa-ter flow often observed in mangals and salt marshes can leadto organic loading and reduced sediment oxygen availabil-ity (Alongi 1997) with a subsequent depression of below-SWIspecies richness Indeed the geochemistry of structural-vegetation habitats is markedly different from that of non-vegetated areas as a result of increased productivity

increased sedimentary nutrients and a greater propensity foranoxia related to the large amounts of detritus produced

Structural vegetation influences food webs at many levels Many primary producers particularly vascular plantsproduce ldquosignaturerdquo compounds including lipids polysac-charides and antiherbivory chemicals that may favor specificbacterial and fungal populations the effects of these com-pounds may have ramifications up through the food chainThe tannin-rich detritus produced in mangals for exampleis used by a tannin-tolerant fauna with low compositediversity (Alongi and Christoffersen 1992) But for macro-faunal species able to cope with productive environments suchas mangals competitors are presumably few and organicmatter is abundant

Habitat complexity generally enhances diversity in bio-logical communities and structural vegetation and rootstructures provide critical habitat for a diversity of species(Figure 1) An increase in above-SWI macrofaunal rich-ness and composite diversity in seagrass sediment commu-nities has been linked to abundance and numbers of speciesof seagrass on regional and latitudinal scales (Stoner andLewis 1985) Species richness of infauna within vegetated ar-eas is elevated in comparison with that of adjacent baresand habitat (See Peterson 1979 for macrofauna defined asorganisms retained on a 300- or 500-micro sieve Boucher 1997for meiofauna defined as organisms retained on a 40-microsieve) The explanation for this pattern is that predatorstend to depress diversity in soft-sediment systems at smallscales and seagrasses may provide a predation refuge (Pe-terson 1979) The structural complexity of sediments withinsalt marshes and mangals cannot be used by many speciesbecause of the variability in salinity temperature expo-sure and oxygenation in coastal habitats In mangals for ex-ample the below-SWI community is often reduced indiversity relative to adjacent nonvegetated subtidal sedi-ments (Gee and Somerfield 1997) Habitat complexity mayalso have negative effects on species the roots of seagrassesand marsh grasses likely exclude some burrowers tubebuilders and infauna (Levin and Talley in press)

Predators living above the SWI may in some instancesprey upon infauna Caging experiments focusing on meio-fauna living in mangal sediments suggest that the impactof predation on infauna is modest and the predator andprey communities operate largely independently (Schrijverset al 1995) Salt marsh microcosm experiments with grassshrimp indicated that although the shrimp reduced meio-faunal densities ShannonndashWeiner diversity was largely un-affected (Bell and Coull 1978) It is possible that predationeffects in these habitats like those described below mayprove more important in terms of habitat modificationthan for predation per se These findings contrast with theseagrass studies described above suggesting no simple re-lationships between predators vegetative structure andinfaunal diversity

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Structural vegetation Sediments-up linkagesThe effects of below-SWI organisms on above-SWI organ-isms are likely to be indirect and therefore difficult to doc-ument Microbes living within sediments are critical formineralization of detritus generated by vegetation theyprovide nutrients to roots and above-SWI components ofthe vegetation (Alongi 1997) Burrowing by macrofaunacan improve sediment aeration with positive effects onmangrove growth (Smith et al 1991) likely through alter-ation of porewater sulfide and ammonium concentrationsAlthough one might predict that burrowers would enhancemicrobial biomass and diversity within sediments few datasuggest an effect on above-sediment diversity In coastalecosystems and particularly coral reefs organisms thatmigrate out of sediments at night can be a significant com-ponent of the above-SWI fauna (Sorokin 1993) providinga possible opportunity for interaction between above- andbelow-SWI organisms Infaunal grazers on seedlings androot structures can also regulate mangrove distributions (seeTomlinson 1986) These examples of bottom-up effects invegetative systems do not link to biodiversity per se and of-ten involve individual speciesndashspecies or trophic group in-teractions Whether the lack of evidence for bottom-upeffects of biodiversity on structural vegetation reflects an ab-sence of interaction or simply inadequate data is difficultto say

Linkages in coastal areas lacking structural vegetationMany coastal areas lack obvious physical structures such asthose associated with structural vegetation although reefscreated by polychaete worms and bivalves and other biogenicstructures such as feeding pits and tubes may fill a similarrole Aside from these structures potential effects of above-SWI diversity on below-SWI diversity in most areas arelikely to be expressed through productivity predation andassociated sediment disturbance (bioturbation) and re-cruitment processes In some shallow areas benthic di-atoms and cyanobacteria may form mats on top of sedimentsthat can influence rates of nutrient exchange between sed-iments and the overlying water column (Sundbaumlck andGraneacuteli 1988) But for most marine sediments light is at-tenuated or lacking at the sediment surface and primary pro-duction occurs only in surface waters Some of this primaryproduction will sink to the sea floor and fuel the sedimen-tary system but the structural complexity of the habitat isnot enhanced as it is in systems with structural vegetationEpifaunal species such as sponges and anemones formabove-sediment structures but given that epifaunal organ-isms do not usually occur over the large spatial scales andhigh densities typical of many vegetated areas the scale ofimpact is probably reduced Coral and coralline algal reefsare notable exceptions but these communities includemostly nonsedimentary species Nonetheless even non-vegetated sedimentary habitat has a three-dimensional

spatial structure that affects benthic composition as seen instudies of trawling impacts (Hutchings et al 1991)

Studies to test specifically the hypothesis that productiv-ity predation and recruitment may be related to above-SWIspecies richness and composite diversity are virtually nonex-istent but some qualitative comparisons can be made andcompelling data suggest the existence of linkages Long-term pelagic and benthic data sets from the North Sea sug-gest that changes in biomass and species abundance haveoccurred in both habitats since the 1970s but linkages be-tween community structure of habitats are weak (Austen etal 1991)

Above-SWI productivity may impact sedimentary di-versity through three potential routes Amounts of organicloading timing and biochemical composition of productsof photosynthesis all can affect sedimentary organisms andtheir composition When productivity is extremely high(such as under organic loading) macrofaunal (Pearson andRosenberg 1978) and meiofaunal (Coull and Chandler1992) richness and composite diversity are often depressedbut these changes relate to hypoxia resulting from increasedproductivity rather than to changes in pelagic diversity perse Increasing areas of ocean bottom are experiencing hypoxicevents that can cover thousands of km2 of sea floor and elim-inate most resident fauna (Malakoff 1998) Toxic algalblooms can have a similar impact

The anticipated impact of variability in organic loadingon sedimentary diversity is even more tenuous Schratzbergerand Warwick (1998) demonstrated in microcosm experi-ments that continuous inputs at moderate levels promotegreater nematode diversity than episodic inputs By contrasttemporal variability in resource supply combined with non-linear responses of different species to resources is onemodel to explain high species richness and composite di-versity in the deep sea (Grassle and Sanders 1973) Com-parison of microbial diversity in shallow and deep tropicaland temperate systems with that in deep pelagic systemscould provide further insight into the role of variability inresource supply by testing whether microbial diversity is af-fected by differences in seasonality and the pulsed or episodicnature of organic inputs

Biochemical diversity of organic inputs from above theSWI could affect diversity of microbial and potentiallymeiofaunal and macrofaunal taxa (Dauwe et al 1998) Ma-jor groups of primary producers including various groupsof phytoplankton macroalgae and vascular plants in shal-low systems produce specific polysaccharides or lipids thatcan favor specific species of hydrolytic bacteria (Percivaland McDowell 1967) For example the capacity for hy-drolysis of agaropectin and carrageenans compounds pro-duced by red algae is limited to relatively few bacterial taxaThus inputs of these polymers may affect both the diversityand biogeography of below-SWI bacteria The nature ofpolysaccharide inputs including contributions from ter-restrial systems might also play a role in the diversity andrelative importance of fungi some of which possess unique

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hydrolytic capabilities Because proteins nucleic acids andlipids are ubiquitous they are probably less important thanpolysaccharides in determining benthic microbial diver-sity Distinctive groups of bacteria from species to phylumlevels of organization also exhibit substrate preferences forproteins sugars lipids etc and the relative abundance ofpolymer classes may therefore affect microbial functional di-versity Abundance of polymer classes varies with planktonicspecies composition terrestrial organic loading and watercolumn depth Thus there is good reason to believe thatabove-SWI diversity will affect below-SWI bacteria andperhaps fungi but whether this linkage extends to below-SWImeiofauna and macrofauna remains untested One mightpredict that higher diversity low in the food chain (ie bac-teria) could enhance diversity in larger organisms if food di-versity enhances feeder diversity Given the limited dataavailable on diversity of microbial groups however we ac-knowledge the highly speculative nature of these hypothe-ses and offer them as ideas to motivate research directions

Evidence suggests that predation and disturbance byabove-SWI epifaunal predators (eg crabs shore birdsflatfish) can affect diversity by removing individuals butalso through habitat modification Caging studies suggestthat predators reduce macroinfaunal diversity (Peterson1979) presumably because they often selectively removeslow-growing and vulnerable species Because these con-clusions are drawn from caging studies rather than directcomparisons of above- and below-SWI diversity they tell uslittle about changes at scales larger than the cages but theydo suggest that above-SWI diversity can have a direct impacton below-SWI diversity at small scales

It is likely that the greatest effect of predation on speciesdiversity is through habitat modification the habitat het-erogeneity that predators may introduce can result in en-hanced diversity at larger scales Large and mobile above-SWIbottom feeders such as rays tend to cause an initial de-pression of local diversity as they remove prey and physicallydisturb the sediment sometimes followed by transient in-creases in species richness or evenness enhancing diversity(VanBlaricom 1982) This sort of biological disturbanceopens up habitat and eliminates most species resulting ina succession through an initial low-diversity stage dominatedby a few opportunistic or ldquoweedyrdquo species an intermediatestage characterized by high diversity because opportunistsand background species co-occur and finally a moderate-diversity late stage in which opportunists have declinedand background species again dominate A similar sequenceoccurs when pelagic carcasses fall to the bottom providingfood and a localized disturbance benefiting species that arenot abundant otherwise (Smith et al 1998) Thus althoughdiversity at the local (sample) scale may often be reducedspecies numbers at the landscape scale may be enhanced In-terestinglymost of what we know about predation is from stud-ies of above-sediment species rather than interactionsamong infaunal species This raises the intriguing ques-tion of whether there are fundamental differences in the

effects of above-SWI versus infaunal predators on sedi-mentary biodiversity

Large sediment diggers above the SWI such as rays (Van-Blaricom 1982) crabs and shrimp may also affect sedi-mentary community diversity through geochemicalmechanisms For example sediment disturbance such asfrom burrowing polychaetes (eg Kristensen et al 1985) canintroduce oxygen into anaerobic sediments (Aller 1982) andabove-sediment diggers will have a similar effect Burrowsmay also help concentrate organic matter through deposi-tion or active sequestration by organisms that live within theburrows Alternatively burial of organic detritus can resultin increased sediment oxygen demand and production ofcompounds rich in organic material Clearly these activitieswill influence microbial meiofaunal and most likely macro-faunal diversity but studies explicitly addressing geochem-ical effects on diversity are lacking (although see Soetaert andHeip 1995) As an analog to predator disturbance animalburrows produce biogeochemically distinct conditionsthat may be used by specific microbial and meiofaunalpopulations (Dobbs and Guckert 1988) For example de-halogenating populations may be enriched in burrows ofhaloorganic-producing enteropneusts (King 1988) Al-though it is clear that animalndashmicrobe interactions may beresponsible for unique microbial associations with bur-rows planktonic diversity could provide an indirect controlon microbial diversity in sediments because benthic bio-geography is likely related to composition and processeswithin the plankton

The co-occurrence of the pelagic stage of some benthicspecies with holoplanktonic species provides ample op-portunity for interaction in the water column Many ben-thic species produce planktonic larval stages that may spendanywhere from minutes to months in the water column po-tentially interacting with a broad suite of holoplanktonicspecies through predation or competition for food Thedispersal stages of benthic species usually experience veryhigh levels of mortality but whether diversity of the plank-ton plays a role in rates of mortality is untested For exam-ple greater diversity of predators could increase thelikelihood that meroplankton will suffer from predationMesocosm experiments offer one approach to test thesehypotheses

Coastal habitats lacking structural vegetation Sediments-up linkagesFunctional groups within sediments can affect above-sediment diversity via selective transfer of matter throughthe SWI particle exchange through biological mechanisms(feeding of pelagic species on the benthos and vice versa mi-grations from benthic species into the water column in-cluding reproductive propagules) and release of dissolvedsubstances after mineralization of organic matter or trans-formation of pollutants in sediments (Henriksen et al1983)

December 2000 Vol 50 No 12 bull BioScience 1081

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1082 BioScience bull December 2000 Vol 50 No 12

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Nutrient regeneration is critical in fueling coastal pro-ductivity above the SWI interface and sedimentary mi-crobes play a key role in the regeneration process (seeSnelgrove et al 1997) In tropical areas this seasonal effectis less pronounced and benthic algae may capture mostnutrients as they diffuse out of sediments (Alongi 1997) Thefeeding movements and respiration of macrofaunal taxa af-fect the porewater concentrations and availability of oxygennitrate sulfate and other electron acceptors in marine sed-iments which in turn affects carbon and nitrogen rem-ineralization rates by microbes (Rhoads et al 1978) Theinfluences of regeneration rates on diversity are undoubt-edly complex but high regeneration can result in blooms ofa few dominant phytoplankton species Rates of regenera-tion and their temporal variation can affect phytoplanktoncomposition and diversity Pulsed areas often have a fewdominant phytoplankton species at any one time but lesstemporally variable areas may be more species rich unlessnutrient levels are highly elevated

Pollutants much like regenerated nutrients are affectedby microbial diversity and macrofaunal activity that influ-ence the magnitude and timing of release of modified anduntransformed pollutants from sediments into the water col-umn Impacts may be direct such as when pollutants boundto sediment particles are moved by macrofauna so that theybecome deeper or shallower in the sediment horizon or link-ages may be less direct For example when macrofauna col-onize polluted sediments their reworking typically changesredox conditions and enhances porewater efflux from sed-iments triggering release of heavy metals Degradation oforganic pollutants may also depend on the presence ofspecific microorganisms (eg Geiselbrecht et al 1996)which may in turn depend on macrofaunal activities Link-ages between the nature and magnitude of pollutant releasefrom sediments and pelagic biodiversity are undoubtedlycomplex and a descriptive framework does not exist butspecies-specific transfers and pollutant effects are knownDemersal fish that feed on the benthic organisms such asshrimp and polychaetes provide an obvious conduit for sed-iment contaminants (eg heavy metals PCBs) to the above-SWI domain

Active vertical migration at night for feeding and repro-duction characterizes some adult meiobenthic (Armonies1988) and macrobenthic species that migrate from below theSWI interface up into the water column (Sorokin 1993)Adults of benthic species will leave sediments at night andmake excursions into the water column but interactions withthe above-SWI fauna have not been well studied (Mees andJones 1997) Often they are eroded from the sediment bystrong bottom currents generated by wind or tides butmollusks and polychaetes are also known to move aftermetamorphosis perhaps in search of better food (Olivier etal 1996) The effects of these excursions and interactions withthe above-SWI fauna have not been quantified but thesebenthic migrants lengthen the list of taxa found in the wa-ter column

Meroplankton the pelagic larvae that are produced bymany macrobenthic species in coastal areas remain in theplankton for hours weeks or even months depending onthe taxon The meroplankton on continental shelves oftendominate the holoplankton (wholly planktonic organisms)during a large part of the year and different species tend topeak at different times of year particularly in the spring andautumn when phytoplankton blooms occur The effects ofmeroplankton grazing on phytoplankton are expected to beconsiderable Meroplankton can also be an important foodsource for water column species and meroplankton diver-sity could impact holoplankton diversity and pattern An in-triguing example is seen in the North Sea where long-termplankton data indicate that meroplankton have become thedominant taxon in shelf waters in recent years with corre-sponding decreases in the formerly abundant copepods(Lindley et al 1995) This change has been linked to increasesin biomass of benthic echinoderms which in turn may berelated to eutrophication or fishing disturbance (Duineveldet al 1987) Whether increases in meroplankton are re-sponsible for the decline in holoplankton is impossible to de-termine without experimental data but the pattern raisesinteresting questions on above- and below-SWI linkagesHow changes in species composition affect the ecosystem willbe difficult to determine given the confounding impacts offishing disturbance pollution and climatic factors that in-fluence the North Sea ecosystem Fishing impacts on sedi-mentary fauna remain a difficult question to address in anyecosystem given that virtually any area that can be fished hasbeen fished and unimpacted ldquocontrolrdquo areas either are en-tirely lacking from a region or represent fundamentally dif-ferent habitats that also happen to be untrawlable Smith etal (2000) discuss fishing impacts in greater detail

Suspension feeding activity by benthic organisms providesa mechanism of interaction between pelagic and benthic sys-tems (Officer et al 1982) Suspension feeders often transfermuch larger quantities of material to sediments than wouldbe possible by sedimentation alone and they may deplete thelower water layers of particles and increase transparency(Butman et al 1994) The intriguing example of the Asianclam Potamocorbula amurensis and the effects of its intro-duction into San Francisco Bay are discussed by Smith et al(2000) Elmgren and Hill (1997) point out that despitemuch lower diversity in the Baltic Sea ecosystem processessuch as carbon cycling and trophic transfer occur as they doin the North Sea (Steele 1974) suggesting that total diver-sity may not be important to these processes But in one areaof the Baltic where suspension feeders are absent energy flowis markedly different with reduced phytoplankton flux to thebenthos and reduced importance of macrofauna relativeto meiofauna How the absence of suspension feeders affectspelagic processes remains unclear but primary productiv-ity and fisheries yields are both considerably reduced inthis area

Resting stages in the form of eggs and cysts are producedby a number of pelagic phytoplankton and zooplankton

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species and these stages can be abundant in coastal sediments(Marcus 1996) Among the best known of these are di-noflagellate cysts which serve as a hardy resting stage andcan seed toxic blooms leading to paralytic shellfish poisoningthrough ingestion of toxic dinoflagellates by suspension-feed-ing bivalves During unfavorable conditions the sedimentsprovide a refuge for resting stages of various taxa which maybecome active when conditions become more favorable orstorm events resuspend them (eg Marcus and Boero 1998)Emergence from sediments may be suppressed by anoxiadarkness or physical contact with the sediment and maytherefore be affected by the bioturbation activities of below-SWI organisms Copepod eggs for example are extremelyhardy and can pass through digestive tracts of macrofaunaunharmed although predation by meiofauna may occurResting stages may be relocated by dredging activities or inguts of organisms that are transplanted for aquacultureSediments may also provide refugia for other pelagic or-ganisms such as fungi viruses and parasites (See discussionof the predatory dinoflagellate Pfiesteria piscicida in Smithet al 2000) The linkage to above-SWI diversity is very ten-tative but removal of key fish predators is likely to affectpelagic food chains

The benthos can be an important food resource for above-SWI organisms Changes in size and species composition ofinfauna such as after chronic bottom trawling or short-term anoxia events resulting from eutrophication influ-ence above-SWI species feeding at the sediment-waterinterface Bottom-feeding fishes that depend on infaunamay then switch to other prey or migrate elsewhere (Federand Pearson 1988) As described above a variety of above-SWI species feed on below-SWI organisms including manythat contribute to important commercial fisheries

Linkages in the open oceanWithin the open ocean a significant portion of the water col-umn is spatially decoupled from the sediment-water inter-face and most organisms living near the oceanrsquos surfacehave no direct contact with the sediment Unlike thenearshore environment described above there is no primaryproduction near the bottom and the exchange of dissolvedmaterials including nutrients and dissolved gases is ex-tremely slow relative to biotic lifetimes The water columndepths involved may be several kilometers and vertically mi-grating predators span the full water column only in shal-lower areas Thus linkages between diversity in the above-and below-SWI fauna are likely to be even less direct thanin other marine systems although the potential mecha-nisms have some similarities This decoupling presentsproblems in defining biogeographical provinces (eg An-gel 1997) which though well defined in shallow water andopen-ocean surface waters are probably blurred in deeperwater where temperature and light are less variable

A number of studies have suggested that latitudinal di-versity patterns exist in above- and below-SWI communi-ties Although ocean currents and wind patterns greatly

complicate simple generalizations it has been suggestedthat phytoplankton diversity decreases toward higher-productivity areas as a few dominant species take over Datafrom McGowan and Walker (1985) suggest a general decreasein pelagic copepod diversity with latitude within the NorthPacific although regional oceanography blurs any simpletrend Angel (1997) suggests a decline in diversity with in-creasing latitude in the North Atlantic for several pelagic an-imals a pattern seen to at least 2000 m depth In general thispattern is consistent with macrofaunal shallow-water anddeep-sea data but it contradicts patterns in nematodes(Figure 2a) Although it is tempting to suggest that the di-versity of pelagic organisms that provide food for the ben-thos may be linked to the diversity of below-SWI organismsthe patterns represent a weak correlation

Another pattern that can be compared between above- andbelow-SWI communities is the relationship with depthRex et al (1997) reviewed depth-related patterns in the be-low-SWI fauna and observed highest diversity at interme-diate depths of approximately 2000 m Other studies havealso observed peaks at intermediate depths although peaksare not necessarily at the same depths Local diversity of phy-toplankton tends to increase with depth until light becomeslimiting Zooplankton diversity may also reach a peak at in-termediate depths in the North Atlantic (Angel 1997Figure 2b) Water column diversity has also been comparedalong a transect running perpendicular to shore (Angel1997) and suggests a pattern of low diversity across shelfdepths a peak at the shelf break and a decline over thecontinental slope (Angel 1997) the sampling transect did notextend to mid-continental slope depths where Rex et al(1997) observed a diversity peak There are also intriguingexamples of high-diversity shelf habitats (Gray et al 1997)illustrating the need for better sampling coverage to achievegeneralizations

Although there are some similarities in patterns of above-and below-SWI communities over broad spatial scales(Boucher and Lambshead 1995 Angel 1997) there is littleevidence for cause and effect It is equally plausible thatsimilar processes (eg productivity energy) affect above- andbelow-SWI biota similarly and that diversity patterns are un-related Geological history (eg Jablonski 1993) which mayhave similar consequences for above- and below-SWI or-ganisms adds further complication

The open ocean Water column-down linkagesProductivity is the most likely mechanism by which above-SWI organisms affect the sedimentary infauna living in thehighly food-limited deep sea Materials sinking from surfacewaters fuel the benthos far below and it is possible thatpatterns in the deep-sea benthos may be linked to diversityand temporal variability in food resources There is ampleevidence that food pulses support a somewhat-specializedsubset of species in this environment and there is some evi-dence that different food resources may support different

December 2000 Vol 50 No 12 bull BioScience 1083

Articles

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faunas (Snelgrove et al 1992) Benthic infaunal species alsoaggregate possibly because detritus distribution is not uni-form or because different types of detritus might attract dif-ferent types of species One current theory is that small-scalepatchiness in food supply is critical in promoting deep-seadiversity (Grassle and Sanders 1973) But again it is unclearwhether diversity of food resources (and thus pelagic di-versity) makes any real difference There is some congruencein global-scale patterns of surface productivity and deep-seabiodiversity patterns that suggests ecological couplingthrough the water column (Rex et al 1993) The bathy-metric diversity pattern has been related to a gradient in pro-ductivity that decreases from the coast to the deep oceanThere is sufficient benthic and pelagic biodiversity data tobegin testing this idea more thoroughly

Correlative linkage between broad-scale surface produc-tivity and benthic diversity can be tested with existing dataon global export production (Falkowski et al 1998) and re-gional studies of infauna Plotting species counts for dif-ferent taxa on Falkowski et alrsquos estimates for carbon exportsuggests that there may indeed be a relationship betweenproductivity and diversity for some taxa with a decline indiversity as productivity increases (Figure 3 Table 1 See alsoWatts et al 1992 for a more detailed analytical approach)Whether this pattern relates to amounts or to variability ofcarbon export is difficult to judge since sample sizes aresmall and many highly productive areas are also quite sea-sonal Unfortunately the spatial coverage that has beenachieved in the sampling of benthic organisms in the oceansis insufficient to be certain that such relationships exist

1084 BioScience bull December 2000 Vol 50 No 12

Articles

Figure 2a Patterns of diversity withlatitude for a variety of pelagic andbenthic taxa Sources of data are Royet al (1998) for shallow gastropodsAngel (1997) for ostracods Rex et al(1993) for deep-sea gastropods andisopods Lambshead et al (2000) fornematodes and PierrotndashBults (1997)for euphausiids Different samplingintensities and measures were used indifferent studies so that comparisonshould be only between patterns indifferent groups rather than betweensamples

Figure 2b Changes in diversity withdepth for benthic and pelagic taxaOstracod data are from Angel (1997)and gastropod data are from Rex et al(1997) Again different samplingintensities and measures were used indifferent studies so that comparisonshould be only between patterns indifferent groups rather than betweensamples

(deg)

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December 2000 Vol 50 No 12 bull BioScience 1085

Articles

Again the importance of above-sediment diversity as op-posed to productivity is unclear

Predation effects in the deep sea and particularly effectson diversity are not well understood Predation by above-SWI organisms was one of the first processes suggested tobe important in structuring deep-sea biodiversity (Daytonand Hessler 1972) although shallow-water data suggestthat predators depress diversity at small scales The role ofpredators in creating disequilibria that were described forshallow water has a similar potential application here Thereis little evidence that pelagic predators feeding on infaunaare particularly selective with respect to species compositionbut successional mosaics may be created by patchy preda-tion Recent caging experiments in the San Diego Trough(Eckman et al 1999) tested the role of predation in main-taining deep-sea diversity No studies have been designed totest whether the diversity of these predators is significant for

infaunal communities Another possible effect of preda-tion occurs during the reproductive phase when some deep-sea species release reproductive propagules into surfacewaters where they may be subject to predation or compe-tition with pelagic species The magnitude of this impact isdifficult to evaluate but given the lesser importance ofplanktotrophic larvae in the deep ocean than in shallowwater and the large spatial decoupling involved a diversitylinkage seems unlikely One final point regarding deep-seapredators is that many are essentially decoupled from sur-face waters where production takes place Although somespecies make extensive diel migrations many deep-seapredators are more tightly coupled to the benthos than theymight be in shallow water

Habitat complexity in the deep sea is considerably less thanin shallow water with bioturbation predation and foodflux contributing to benthic diversity through creation of

Figure 3 Estimates of deep-sea diversity for various taxa superimposed on an image of global carbon export pattern asestimated by Falkowski et al (1998) Carbon export image reproduced from Falkowski et al (1998) Numbers in red arenematode species counts from Lambshead et al (2000) numbers in white are shallow mollusk species counts from Roy et al(1998) and numbers in black are expected species in sampling 50 individuals from Rex et al (1993) Because of differentsampling intensities and measures used comparison should be only between patterns in different groups rather thanbetween samples

This content downloaded from 1297813929 on Mon 11 May 2015 050627 UTCAll use subject to JSTOR Terms and Conditions

microhabitat As mentioned earlier it is thought that micropatches create habitat heterogeneity that is critical inpromoting deep-sea diversity thus a greater diversity ofpredators bioturbators and food types should create agreater diversity of patch types and therefore a greater diversityof benthos (eg Snelgrove et al 1992) Sediment diversity hasbeen shown to be a significant predictor of biological diver-sity in the deep sea (Etter and Grassle 1992) suggesting thathabitat is indeed important to deep-sea organisms on manyscales However linkages of diversity and habitat patchinesshave not been broadly established

The open ocean Sediments-up linkagesAs indicated earlier there are likely very few bottom-up ef-fects of open-ocean infauna although their role in global car-bon (benthic mineralization) and nitrogen (denitrification)cycles may be underestimated (Heip et al in press) The hugescales involved suggest that biodiversity likely plays a minorrole except perhaps in terms of functional groups As in shal-low systems some benthic species produce pelagic larvae Butlow faunal densities in the deep sea suggest that repro-ductive propagules will be few and their impact on above-SWI organisms minimal

How can abovendashbelow SWIlinkages be more effectivelytestedGiven the potential relationships outlined aboveand the current interest in biodiversity it iscritical that we strive for a better understandingof how above- and below-SWI diversity arelinked in the oceans before too many of thesehabitats and their linkages are unwittingly al-tered by human disturbance Determining in-teraction of above- and below-SWI diversity isa great challenge Analysis of natural patternswith more complete spatial coverage globally in-cluding areas with unusual characteristics willclarify whether latitude productivity and depthinfluence diversity within the pelagic and ben-thic domains Experimental studies will be nec-essary to determine causality within domainsand will be critical for linking above- and below-SWI diversity An obvious means of testing theimportance of diversity in one domain relativeto the other is to manipulate diversity in one andmonitor response in the other Unfortunatelymanipulation of sedimentary habitats is extra-ordinarily difficult because removal of specificgroups of organisms usually disturbs the sedi-ments and alters basic geochemistry Baitedtraps and selective poisoning offer one approachto ldquoremovingrdquo certain groups It is also feasibleto build on caging experiments by excludingpelagic species either completely or selectivelyallowing effective in situ tests of impacts Theimportance of organic-matter diversity could

also be tested by manipulating the types of food resourcessupplied to sediments and below-SWI organismsMesocosms where species composition can be carefullyregulated in the above- and below-SWI communities offeranother effective means of studying abovendashbelow processes(eg Widdicombe and Austen 1998) The trick is to strikea balance between ease of control and maintaining a ldquonaturalrdquo ecosystem In short the linkages between above-and below-SWI diversity have received little attention andare an area where many research opportunities exist andmany questions remain to be answered

AcknowledgmentsWe wish to thank to Diana Wall for her leadership in tack-ling soil and sediment biodiversity We also thank the SCOPECommittee on Soil and Sediment Biodiversity and Ecosys-tem Functioning an anonymous US foundation and theMinistries of Agriculture and the Environment The Nether-lands for providing funds to host the workshop ldquoThe Relationship between Above- and Belowsurface Biodiversityand Its Implications for Ecosystem Stability and GlobalChangerdquo in Lunteren The Netherlands The efforts of GinaAdams in orchestrating the workshop that led to this

1086 BioScience bull December 2000 Vol 50 No 12

Articles

Table 1 Correlational relationships among latitude productivity exportand diversitya

Latitude Productivity Diversity

Deep-sea gastropods Latitude ndash 0612 ndash0591

Productivity 0180 ndash ndash0888

Diversity 0216 0002 ndash

Shallow-water mollusks Latitude ndash 0631 ndash0798

Productivity 0280 ndash ndash0840

Diversity 0053 0027 ndash

Deep-sea nematodes Latitude ndash 0534 0225

Productivity 0824 ndash 0561

Diversity 100 0741

aThese analyses are based on different types of diversity estimates as described andfrom the same sources as in Figure 3 and approximate measures of productivityexport as extracted from the color image in Falkowski et al (1998) As such thisshould be treated as an exploratory analysis designed to stimulate more rigorous com-parisons Values above dashes are Pearson correlation coefficients and those belowdashes are Bonferroni-adjusted probability values with significant values shown inbold It should be noted that more detailed analysis by Lambshead et al (2000) hasindicated a significant positive relationship between productivity and deep-sea nema-tode species richness

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December 2000 Vol 50 No 12 bull BioScience 1087

Articles

synthesis are also greatly appreciated Thoughtful reviews by Rebecca Chasan Paul Dayton Diana Wall and three anony-mous reviewers improved this manuscript and are much appreciated

References citedAller RC 1982 The effects of macrobenthos on chemical properties of ma-

rine sediment and overlying water Pages 53ndash102 in McCall PL TeveszMJS eds AnimalndashSediment Relations New York Plenum

Alongi DM 1997 Coastal Ecosystem Processes Boca Raton (FL) CRCPress

Alongi DM Christoffersen P 1992 Benthic infauna and organismndashsediment relations in a shallow tropical coastal area Influence of out-welled mangrove detritus and physical disturbance Marine EcologyProgress Series 81 229ndash245

Angel MV 1997 Pelagic biodiversity Pages 35ndash68 in Ormond RFG Gage JDAngel MV eds Marine Biodiversity Patterns and Processes Cambridge(UK) Cambridge University Press

Armonies W 1988 Active emergence of meiofauna from intertidal sedimentMarine Ecology Progress Series 43 151ndash159

Austen MC Buchanan JB Hunt HG Josefson AB Kendall MA 1991 Com-parison of long-term trends in benthic and pelagic communities of theNorth Sea Journal of the Marine Biological Association of the UnitedKingdom 71 179ndash190

Bell SS Coull BC 1978 Field evidence that shrimp predation regulatesmeiofauna Oecologia 35 141ndash148

Boero F Mills CE 1999 Hydrozoan people come together Trends in Ecol-ogy and Evolution 14 127ndash128

Boucher G 1997 Structure and biodiversity of nematode assemblages in theSW lagoon of New Caledonia Coral Reefs 16 177ndash186

Boucher G Lambshead PJD 1995 Ecological biodiversity of marine nema-todes in samples from temperate tropical and deep-sea regions Con-servation Biology 9 1594ndash1604

Butman CA Freacutechette M Geyer WR Starczak VR 1994 Flume experi-ments on food supply to the blue mussel Mytilus edulis L as a functionof boundary-layer flow Limnology and Oceanography 39 1755ndash1768

Cohen AN Carlton JT 1998 Accelerating invasion rate in a highly invadedestuary Science 279 555ndash558

Collett LC Hutchings PA Gibbs PJ Collins AJ 1984 Comparative study ofthe macrobenthic fauna of Posidonia australis meadows New SouthWales Australia Aquatic Botany 18 111ndash134

Coull BC Chandler GT 1992 Pollution and meiofauna Field laboratory andmesocosm studies Oceanography and Marine Biology An Annual Re-view 30 191ndash271

Dauwe B Herman PMJ Heip CHR 1998 Community structure and bio-turbation potential of macrofauna at four North Sea stations with con-trasting food supply Marine Ecology Progress Series 173 67ndash83

Dayton PK Hessler RR 1972 Role of biological disturbance in maintainingdiversity in the deep sea Deep-Sea Research 19 199ndash208

Dobbs FC and Guckert JB 1988 Callianassa trilobata (Crustacea Tha-lassinidea) influences abundance of meiofauna and biomass composi-tion and physiologic state of microbial communities within its burrowMarine Ecology Progress Series 45 69ndash79

Duineveld GCA Kuumlnitzer A Heyman RP 1987 Amphiura filiformis (Ophi-uroidea Echinodermata) in the North Sea Distribution present and for-mer abundance and size composition Netherlands Journal of SeaResearch 21 317ndash329

Eckman JE Thistle D Burnett WC Robertson CT 1999 Performance of cagesas predator-exclusion devices in the deep sea EOS Transactions of theAmerican Geophysical Union 80 296ndash297

Edgar GJ 1983 The ecology of south-east Tasmanian phytal animal com-munities I Spatial organization on a local scale Journal of Experimen-tal Marine Biology and Ecology 70 129ndash157

Elmgren R Hill C 1997 Ecosystem function at low biodiversitymdashThe Balticexample Pages 319ndash336 in Ormond RFG Gage JD Angel MV eds

Marine Biodiversity Patterns and Processes Cambridge (UK) CambridgeUniversity Press

Etter RJ Grassle JF 1992 Patterns of species diversity in the deep sea as a func-tion of sediment particle size diversity Nature 360 576ndash578

Falkowski PG Barber RT Smetacek V 1998 Biogeochemical controls and feed-backs on ocean primary production Science 281 200ndash206

Feder HM Pearson TH 1988 The benthic ecology of Loch Linnhe andLoch Eil a seandashloch system on the west coast of Scotland V Biology ofthe dominant soft-bottom epifauna and their interaction with the infaunaJournal of Experimental Marine Biology and Ecology 116 99ndash134

Gee JM Somerfield PJ 1997 Do mangrove diversity and leaf litter decay pro-mote meiofaunal diversity Journal of Experimental Marine Biologyand Ecology 218 13ndash33

Geiselbrecht AD Herwig RP Deming JW Staley JT 1996 Enumeration andphylogenetic analysis of polycyclic aromatic hydrocarbon-degradingmarine bacteria from Puget Sound sediments Applied EnvironmentalMicrobiology 62 3344ndash3349

Graf G 1992 Benthicndashpelagic coupling A benthic view Oceanography andMarine Biology An Annual Review 30 149ndash190

Grassle JF Sanders HL 1973 Life histories and the role of disturbanceDeep-Sea Research 20 643ndash659

Gray JS Poore GCB Ugland KI Wilson RS Olsgard F Johannessen Oslash 1997Coastal and deep-sea benthic diversities compared Marine EcologyProgress Series 159 97ndash103

Heip C et al In press The role of the benthic biota in sedimentary metab-olism and sedimentndashwater exchange processes in the Goban Spur area(NE Atlantic) Deep-Sea Research

Henriksen K Rasmussen MB Jensen A 1983 Effect of bioturbation in thesediment and fluxes of ammonium and nitrate to the overlying waterEnvironmental Biogeochemistry and Ecology Bulletin 35 193ndash205

Hutchings PA Wells FE Walker DE Kendrick GA 1991 Seagrass sedimentand infaunamdashA comparison of Posidonia australis Posidonia sinuosa andAmphibolis antartica in Princess Royal Harbour South-Western AustraliaII Distribution composition and abundance of macrofauna Pages611ndash634 in Wells FEWalker DI Kirkman H Lethbridge R eds The Floraand Fauna of the Albany Area Western Australia Records of the West-ern Australian Museum 1

Jablonski D 1993 The tropics as a source of evolutionary novelty throughgeological time Nature 364 142ndash144

King GM 1988 Dehalogenation in marine sediments containing naturalsources of halophenols Applied Environmental Microbiology 543079ndash3085

Kristensen E Jensen MH Andersen TK 1985 The impact of polychaete(Nereis virens Sars) burrows on nitrification and nitrate reduction in es-tuarine sediments Journal of Experimental Marine Biology and Ecology85 75ndash91

Lambshead PJD Tietjen J Ferrero T Jensen P 2000 Latitudinal gradients inthe deep sea with special reference to North Atlantic nematodes MarineEcology Progress Series 194 159ndash167

Levin LA Talley TS In press Influence of vegetation and abiotic environmentalfactors on slat marsh benthos In Weinstein MP Kreeger DA eds Con-cepts and Controversies in Salt Marsh Ecology Amsterdam (The Nether-lands) Kluwer

Lindley JA Gamble JC Hunt HG 1995 A change in the zooplankton of thecentral North Sea (55deg to 58deg N) A possible consequence of changes inthe benthos Marine Ecology Progress Series 119 299ndash303

Malakoff D 1998 Death by suffocation in the Gulf of Mexico Science 281190ndash192

Marcus NH 1996 Ecological and evolutionary significance of resting eggsin marine copepods Past present and future studies Hydrobiologica 320141ndash152

Marcus NH Boero F 1998 Minireview The importance of benthicndashpelagiccoupling and the forgotten role of life cycles in coastal aquatic systemsLimnology and Oceanography 43 763ndash768

McGowan JA Walker PW 1985 Dominance and diversity maintenance inan oceanic ecosystem Ecological Monographs 55 103ndash118

McGowan JA Cayan DR Dorman LM 1998 Climatendashocean variabilityand ecosystem response in the Northeast Pacific Science 281 210ndash217

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1088 BioScience bull December 2000 Vol 50 No 12

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Mees J Jones MB 1997 The hyperbenthos Oceanography and Marine Biology An Annual Review 35 221ndash255

Officer CB Smayda TJ Mann R 1982 Benthic filter feeding A natural eu-trophication control Marine Ecology Progress Series 9 203ndash210

Olivier F Vallet C Dauvin JndashC Retiegravere C 1996 Drifting in post-larvae andjuveniles in an Abra alba (Wood) community of the eastern part of theBay of Seine (English Channel) Journal of Experimental Marine Biol-ogy and Ecology 199 89ndash109

Osenga GA Coull BC 1983 Spartina alterniflora Loisel Root structure andmeiofaunal abundance Journal of Experimental Marine Biology and Ecol-ogy 67 221ndash225

Pearson TH Rosenberg R 1978 Macrobenthic succession in relation to or-ganic enrichment and pollution of the marine environment Oceanog-raphy and Marine Biology An Annual Review 16 229ndash311

Percival E McDowell RH 1967 Chemistry and enzymology of marine al-gal polysaccharides New York Academic Press

Peterson CH 1979 Predation competitive exclusion and diversity in the soft-sediment benthic communities of estuaries and lagoons Pages 223ndash264in Livingston RJ ed Ecological Processes in Coastal and Marine SystemsNew York Plenum Press

PierrotndashBults AC 1997 Biological diversity in oceanic macrozooplanktonMore than counting species Pages 69ndash93 in Ormond RFG Gage JD An-gel MV eds Marine Biodiversity Patterns and ProcessesCambridge (UK)Cambridge University Press

Rex MA Stuart CT Hessler RR Allen JA Sanders HL Wilson GDF 1993Global-scale latitudinal patterns of species diversity in the deep-sea ben-thos Nature 365 636ndash639

Rex MA Etter RJ Stuart CT 1997 Large-scale patterns of biodiversity in thedeep-sea benthos In Ormond RFG Gage JDAngel MV eds Marine Bio-diversity Patterns and Processes Cambridge (UK) Cambridge Univer-sity Press

Rhoads DC McCall PLYingst JY 1978 Disturbance and production on theestuarine seafloor American Scientist 66 577ndash586

Roy K Jablonski DValentine JW Rosenberg G 1998 Marine latitudinal di-versity gradients Tests of causal hypotheses Proceedings of the Na-tional Academy of Science 95 3699ndash3702

Safina C 1998 Song for the Blue Ocean New York Henry Holt and Com-pany

Schlacher TA Newell P Clavier J SchlacherndashHoenlinger MA Chevillon CBritton J 1998 Soft-sediment benthic community structure in a coral reeflagoonmdashThe prominence of spatial heterogeneity and ldquospot endemismrdquoMarine Ecology Progress Series 174 159ndash174

Schratzberger M Warwick RM 1998 Effects of the intensity and frequencyof organic enrichment on two estuarine nematode communities MarineEcology Progress Series 164 83ndash94

Schrijvers J Okondo J Steyaert M Vincx M 1995 Influence of epibenthoson meiobenthos of the Ceriops tagal mangrove sediment at Gazi BayKenya Marine Ecology Progress Series 128 247ndash259

Smith TJ III Boto KG Frusher SD Giddins RL 1991 Keystone species and

mangrove forest dynamics The influence of burrowing by crabs on soil

nutrient status and forest productivity Estuarine and Coastal Shelf Sci-

ence 33 419ndash432

Smith CR Maybaum HL Baco AR Pope RH Carpenter SD Yager PL

Macko SA Deming JW 1998 Sediment community structure around a

whale skeleton in the deep Northeast Pacific Ocean Macrofaunal mi-

crobial and bioturbation effects Deep-Sea Research II 45 335ndash364

Smith CR Austen MC Boucher G Heip C Hutchings PA King GM Koike

I Lambshead PJD Snelgrove P 2000 Global change and biodiversity link-

ages across the sedimentndashwater interface BioScience 50 1108ndash1120

Snelgrove PVR Grassle JF Petrecca RF 1992 The role of food patches in main-

taining high deep-sea diversity Field experiments with hydrodynamically

unbiased colonization trays Limnology and Oceanography 37 1543ndash1550

Snelgrove PVR et al 1997 The importance of marine sediment biodiversity

in ecosystem processes Ambio 26 578ndash583

Soetaert K Heip C 1995 Nematode assemblages of deep-sea and shelf

break sites in the North Atlantic and Mediterranean Sea Marine Ecol-

ogy Progress Series 125 171ndash183

Sorokin YI 1993 Coral reef ecology Ecological Studies 102 Berlin

SpringerndashVerlag

Steele JH 1974 The Structure of Marine Ecosystems Oxford (UK) Black-

well Scientific Publications

Stoner AW Lewis FG III 1985 The influence of quantitative and qualitative

aspects of habitat complexity in tropical seagrass meadows Journal of

Experimental Marine Biology and Ecology 94 19ndash40

Sundbaumlck K Graneacuteli W 1988 Influence of microphytobenthos on the nu-

trient flux between sediment and water A laboratory study Marine

Ecology Progress Series 43 63ndash69

Tomlinson PB 1986 The Botany of Mangroves Cambridge (UK) Cambridge

University Press

VanBlaricom GR 1982 Experimental analyses of structural regulation in a

marine sand community exposed to oceanic swell Ecological Monographs

52 283ndash305

Watts MC Etter RJ Rex MA 1992 Effects of spatial and temporal scale on

the relationship of surface pigment biomass to community structure in

the deep-sea benthos Pages 245ndash254 in Rowe GT Pariente V eds Deep-

Sea Food Chains and the Global Carbon CycleAmsterdam (The Nether-

lands) Kluwer

Whittaker R 1972 Evolution and measurement of species diversity Taxon

21 213ndash251

Widdicombe S Austen MC 1998 Experimental evidence for the role of Bris-

sopsis lyrifera (Forbes 1841) as a critical species in the maintenance of

benthic diversity and the modification of sediment chemistry Journal of

Experimental Marine Biology and Ecology 228 241ndash255

This content downloaded from 1297813929 on Mon 11 May 2015 050627 UTCAll use subject to JSTOR Terms and Conditions