shellfish aquaculture and the environment (shumway/shellfish aquaculture and the environment) ||...

Chapter 10

Bivalves a s b ioturbators and b ioirrigators Joanna Norkko and Sandra E. Shumway

Bivalves a re k ey s pecies in s oft - s ediment h abitats

Both natural and cultured populations of bivalve molluscs provide a range of important ecosystem functions and services (see Chapters 1 , 4 , 8 , and 9 in this book), some of which stem from the activities of different bivalve species living buried in the sediments. Bioturbation and bioirrigation are the mixing and fl ushing of sediments that are the result of the burrowing, feeding, and other activities of the animals in the sediment. Thus, bioturba-tion and bioirrigation are integral to a healthy soft - sediment ecosystem and, in general, infau-nal bivalves such as clams have a positive, desirable infl uence on the sand or mud in

which they live, just as the earthworms in a vegetable patch or garden compost.

Soft sediments are the most widespread habitats in the sea, extending from coastal estuaries and sandy shores, to continental shelves and the open ocean abyssal plains. Bivalve molluscs are often dominant in terms of biomass and/or abundance in estuarine and coastal soft - sediment habitats. Due to their habitat engineering and their infl uence on benthic - pelagic coupling and nutrient cycling, bivalve molluscs are key species in many habi-tats (Chapters 4 and 9 in this book; Jones et al. 1994 ; Dame et al. 2002 ). Consequently, changes in the condition, abundance, or distri-bution of different bivalve species may have cascading effects on both benthic and pelagic

Shellfi sh Aquaculture and the Environment, First Edition. Edited by Sandra E. Shumway.© 2011 John Wiley & Sons, Inc. Published 2011 by John Wiley & Sons, Inc.

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298 Shellfi sh Aquaculture and the Environment

ecosystems (Vaughn and Hakenkamp 2001 ; Dahlhoff et al. 2002 ; Newell 2004 ; Norkko et al. 2006 ). In addition, bivalves are relatively long - lived and are therefore often used as indi-cator species when monitoring environmental change.

Bivalves are linked to their environment through a multitude of processes that operate over different spatial and temporal scales. Large - scale processes, such as oceanographic conditions, and hydrodynamic and nutrient regimes, defi ne the more general settings and the environmental framework that defi nes, for example, species distribution ranges and the level of primary production. Small - scale pro-cesses, such as individual physiology or behav-ior, are easier to study and amenable to experimental manipulation, but the extrapola-tion and scaling up of the results to the scale of an estuary or ecosystem are much more dif-fi cult. Therefore, generalizations based on small - scale studies are often not accurate at the larger scales of relevance to environmental problems and management practices. The way a pattern or a process is perceived, and there-fore its accuracy, depends to a large extent on the scale at which the phenomenon is studied (Hewitt et al. 2007 ). This highlights the impor-tance of explicitly incorporating scale in all environmental issues, for example, in the way the role of bivalves is assessed. This includes considering which processes operate at which scales, how they are linked, and which ones are most relevant for a particular issue, such as the most effi cient and sustainable siting of aquaculture installations in different types of estuaries (Dumbauld et al. 2009 ).

This chapter focuses on the mechanisms, dynamics, and effects of the bivalve bioturba-tion and bioirrigation processes and how these infl uence the health and stability of marine ecosystems. Particular attention is given to aspects of bioturbation/irrigation and other related sediment processes that are relevant for sustainable management of bivalve aquacul-ture operations.

What a re b ioturbation and b ioirrigation?

Soft - sediment habitats are greatly infl uenced by the activities of different taxa living within the sediment, including bivalves, crustaceans, and polychaete worms. The combination of their movements, feeding, ventilation, burrow-ing, tube construction, and biodeposit produc-tion results in structuring, mixing, and fl ushing of the sediment (Fig. 10.1 , Table 10.1 ). The term “ bioturbation ” refers to the reworking of aquatic sediments by the organisms in the sedi-ments and, in its broadest sense, includes the structuring activities of both burrowing animals and rooting plants, as well as microbes. In addition, animals living on the sediment surface (epifauna) and animals just visiting the sediment in search of food, such as rays and dugongs, may have bioturbating effects. The corresponding processes also occur in terres-trial soils, where earthworms are the most commonly used example. “ Bioirrigation, ” on the other hand, refers to the enhanced trans-port of solutes between the sediment and the overlaying water. This is the fl ushing of burrows that stems from the suspension feeding of the animals and their ventilation activities to facilitate transport of oxygen and excretory products. Bivalves are major players in the modifi cation of sediments, and the effects we observe are a combination of both bioturbation and bioirrigation. In the follow-ing sections, “ bioturbation ” will be used to describe both phenomena, that is, to include both particle and solute transport.

Bioturbation fundamentally affects the physical and chemical characteristics of soft - sediment habitats (Rhoads 1974 ; Aller 1988 ; Kristensen 1988 ; Levinton 1995 ; Aller 2001 ; Reise 2002 ; Meysman et al. 2006b ) and can transform a homogenous sandy or muddy bottom into a heterogeneous landscape with physical structures such as burrows, pits, and mounds. Also, the mere physical presence of, for example, shells of both live and dead

Figure 10.1 Schematic diagram of the processes around a bivalve buried in the sediment.

Excretion of nutrients and CO2

biodeposition of feces and pseudofecesSuspension and/or deposit feedingconsumption of O2

Sediment mixing, flushing,and oxygenation

Added structure

Water column

Oxidized sediment

Reduced sediment

RPD layer

Nut

rient

s

Table 10.1 Combined effects of bivalve physical structure, bioturbation, bioirrigation, and feeding activities in natural bivalve populations in soft - sediment habitats. In addition, the relevance of these processes to aquaculture is summarized.

Process Effects on local environment Relevance to aquaculture

Physical structure Added heterogeneity; burrows, pits, mounds, shell material

Racks, bags, and longlines also provide structure; at high stocking densities, the habitat is homogenized and the diversity reduced

Individual bivalves provide substrate and habitat

Promotes overall higher diversity

Bioturbation; sediment reworking

Oxygenation of the sediment; oxygen penetrates deeper into the sediment

Only applies if bivalves are able to bury into the sediment

Sediment mixing and sorting affects grain size Racks, bags, and longlines may increase siltation

Sediment destabilization, resuspension, and erosion

Prevents siltation

Bioirrigation; ventilation/feeding

Flushing of sediments with overlaying water Only applies if bivalves are able to bury into the sediment

Transport of oxygen into the sediment and excretory products out of the sediment

Biodeposition of feces and pseudofeces on the sediment surface

Benthic - pelagic coupling Potential negative effects are highly dependent on fl ow, depth, and stocking density Increased organic content of the sediment; may

provide food for other benthic species

- Higher microbial activity and oxygen demand in the sediment; potential for hypoxia

Altered nutrient fl uxes at the sediment - water interface

299


tion to the underlying darker reduced sediment layer (Fig. 10.1 ). Depending on sediment type (oxygen penetrates deeper into porous sandy sediments compared with cohesive mud; Volkenborn et al. 2007 ) and the species com-position and abundance of the benthic com-munity, this lighter layer may range from just a millimeter to several centimeters thick. The border between oxidative and reducing reac-tions is called the redox potential discontinuity layer ( RPD ). Bioturbators may substantially extend the depth of this layer, and the depth of the RPD layer is often used as an indicator of environmental status, with deeper oxidized sediment layers indicating the presence of more animals and thus better conditions. This can roughly be measured in sediment cores taken with a see - through corer or quantifi ed, for example, using sediment profi le imagery ( SPI ), where vertical images are taken into the sediment with a prism mounted on a digital camera and subsequently analyzed using image analysis software (Grizzle and Penniman 1991 ). On a fi ner scale, the depth profi les of pH, oxygen, sulfi des, and other compounds can be measured with millimeter accuracy using microsensors penetrating the sediment (Glud 2008 ).

Present - day bioturbation generally does not affect more than about the top 30 cm of the sediment, that is, the sediment layers where most of the infaunal species live (although there are exceptions, such as deep - burrowing geoducks). Where sediment accumulates over time, however, some traces of bioturbation activities are preserved and can be seen in thick sediment layers that are thousands of years old (Erwin 2008 ). Similarly, absence of fauna is also recorded in the sedimentary record in the form of layers upon layers of undisturbed, laminated sediments, which are formed during periods of either natural or eutrophication - induced anoxic conditions (Schaffner et al. 1992 ; Karlson et al. 2002 ; Fig. 10.2 ).

The mechanisms of bioturbation and bioir-rigation have been studied through a number

bivalves in the sediment creates added struc-ture and heterogeneity. Reworking of the sedi-ment affects the sorting of the sediment, its grain size distribution, porosity, and the verti-cal profi les of both solids and solutes. It changes the rates and pathways of reaction processes within the sediment, and between the sediment and the overlaying water (Table 10.1 ). This subsequently affects biodiversity and ecosystem function in soft - sediment habi-tats. In general, bioturbation increases all fl uxes at the sediment – water interface, includ-ing both particulates and solutes. Effi cient fl uxes are a prerequisite for any well - functioning ecosystem and are at the base of all ecosystem services society needs from the environment. Understanding these fl uxes will help manage our coastal ecosystems effi ciently and sustainably.

Bioturbation increases the depth of oxygen penetration into the sediment from the over-laying water. The presence or absence of oxygen governs a multitude of both chemical and biological processes in the sediment, and therefore bioturbation affects the composition of both the invertebrate and microbial com-munities in the sediment (Glud 2008 ). The burrowing, mixing, and tube construction of different invertebrate species substantially increases the area of the sediment – water inter-face, by extending this layer deeper into the sediment as an irregular surface. In combina-tion with active suspension feeding and burrow ventilation, this allows oxygen - rich water to penetrate deeper into the sediment, thereby oxygenating otherwise reduced and anoxic sediments. Bioturbation thus affects the area available for aerobic microbial activity, which affects the functioning of the whole system, since the sediment microbial community per-forms essential functions such as decomposi-tion of deposited organic material and mineralization of nutrients.

The depth of oxygen penetration may be seen as an upper, lighter oxidized sediment layer, with a sometimes relatively sharp transi-

Bivalves as bioturbators and bioirrigators 301

patterns, processes, and types and magnitudes of effects. Bioturbating species have been divided into a range of different functional groups, but fi ve broadly defi ned groups com-monly used are biodiffusers, upward convey-ors, downward conveyors, gallery diffusers, and regenerators (Fran ç ois et al. 2002 ; Gerino et al. 2003 ). Biodiffusers randomly move par-ticles over short distances. This frequent, small - scale particle movement results in dif-fusive mixing and transport of sediment, and most bivalve species belong to this group. On the other hand, upward and downward conveyors, for example, many bioturbating polychaetes, transport particles through their guts, resulting in a nonlocal transport from deeper sediment layers up to the sediment

of different methods since a combination of methods is required to clarify the small - scale mechanisms in the bioturbation processes (Quintana et al. 2007 ). Each method has its limitations and the choice of method or com-bination of methods depends on the question being posed and the timescale of interest; however, the necessity of always also conduct-ing fi eld experiments and fi eld measurements needs to be emphasized, as they often yield contradicting results compared with labora-tory and modeling studies (Table 10.2 ).

All benthic species are different in terms of their bioturbation behavior and thus the net effects of bioturbation depend on the suite of species present and their abundances. This necessitates consideration of species - specifi c

Figure 10.2 Photos of laminated sediments, indicating absence of bioturbation (A), and bioturbated sediments, with an oxidized lighter layer several centimeters thick (B). (Courtesy of H.C. Nillson.)

(A) (B)


bottom of the burrow after it has been deserted. Common to all of these groups is that they facilitate fl uxes of particulate matter and solutes between the sediment and the overlay-ing water, but models of bioturbation need to consider the different types of bioturbation (Michaud et al. 2006 ).

surface or from the sediment surface down, respectively. Gallery diffusers create tube systems and mix sediment in the process. Regenerators also dig tube systems, with addi-tional release of large amounts of sediment into the overlaying water during digging and transport of sediment from the surface to the

Table 10.2 Examples of methodological approaches used for studying bioturbation and bioirrigation (not restricted to only bivalves), the spatial scale these methods apply to (individual organism, laboratory studies, fi eld experiments, fi eld surveys and monitoring, ecosystem level effects), and selected references to studies utilizing these methods.

Method Bioturbation - related effect/process studied Spatial scale Example reference

Visual assessment, photographs, video

Tracks, pits, burrows, mounds Laboratory, fi eld experiments, surveys

Rhoads and Young (1971)

Visual assessment of RPD layer depth

Net effects of bioturbation; oxygen penetration in the sediment

Laboratory, fi eld experiments, surveys

Sediment analysis (including slicing)

Depth distribution of sediment grain size, water content, pelletization, organic content

Laboratory, fi eld experiments, surveys

Maire et al. (2008)

Inert particle addition (e.g., luminophores, glass beads) or natural tracers (radionuclides)

Particle mixing, sediment reworking

Laboratory, fi eld experiments

Gerino et al. (1998) ; Montserrat et al. (2009)

Flume studies Sediment resuspension and erosion

Laboratory Willows et al. (1998)

Inert solute addition (e.g., bromide)

Pore water irrigation Laboratory, fi eld experiments

Martin and Banta (1992)

Microelectrodes, planar optodes

Depth profi les of nutrients, O 2 , S, H 2 S

Very fi ne - scaled; laboratory, fi eld experiments

Glud (2008)

Sediment incubations Fluxes of nutrients, solutes and gasses across the water – sediment interface

Laboratory, fi eld experiments

Asmus et al. (1998) ; Michaud et al. (2006)

Sediment profi le imaging

Two - dimensional structures and oxygen penetration in the sediment

Surveys Grizzle and Penniman (1991) ; Solan et al. (2004)

Computer - aided tomography

Three - dimensional structures in the sediment

Individual cores (slow/expensive)

Perez et al. (1999) ; Bouchet et al. (2009)

Models Nutrient profi les and fl uxes, sediment reworking and transport

Individual bivalves, cores, ecosystems

Willows et al. (1998) ; Meysman et al. (2006a)

See Maire et al. (2008) for a review of methods for quantifying sediment reworking rates.


variable and dependent on species, and the density and size structure of the population. The basic increased fl uxes of particulates and solutes that bioturbation induces are rather straightforward, but they have a range of complex and context - dependent effects. In the following sections these different mechanisms by which soft - sediment bivalves infl uence their surroundings are described. In particular the aim is to illustrate the numerous multiway interactions between bioturbation, benthic biodiversity, and ecosystem function.

Provide s tructure, h eterogeneity in s ediments, s tabilize/ d estabilize the s ediment

Bivalve beds physically infl uence the diversity and functioning of surrounding communities in a number of ways (see Chapter 9 in this book for an in - depth discussion on reef - forming bivalves as ecosystem engineers). Although infaunal species such as clams do not provide the same type of three - dimensional habitat as do mussels and oysters on hard substrates, the presence of bivalves neverthe-less provides increased structural heterogene-ity within the sediments, with potential for a larger number of different favorable micro-habitats in the interstitial spaces and thus increased diversity (Guti é rrez et al. 2003 ). Even the very small - scale movements around individual bioturbating bivalves are important and add heterogeneity to the soft - sediment system. Further, infaunal species have either siphons, feeding shafts, or parts of their shells reaching the sediment surface, which create additional bed roughness and heterogeneity. Bivalves protruding above the sediment surface will also affect fl ow in the benthic boundary layer, both due to their physical structure and to their feeding currents (Green et al. 1998 ). Shells provide hard substrate for recruitment in otherwise soft, unconsolidated sediments, which increases the diversity of epifaunal

How d o h ealthy s oft - s ediment b ivalve p opulations a ffect t heir s urroundings?

Bivalves have profound infl uences on sur-rounding macrobenthic communities. In com-parison with many other bioturbating species such as highly active crabs, shrimp, and poly-chaete worms, bivalves may seem rather sta-tionary and, at fi rst glance, not seem to be doing much, at least not in terms of bioturba-tion. Due to their frequently dominating abun-dances and biomasses, however, and active fi ltration of large volumes of water, the net impact of their bioturbation and bioirrigation activities on the system are considerable (Jackson et al. 2001 ; Vaughn and Hakenkamp 2001 ; Jaramillo et al. 2007 ; Petersen et al. 2008 ). Although most soft - sediment bivalves can be classifi ed as biodiffusers in terms of their bioturbation mode, different species have different burrowing depths (Table 10.3 ), which in turn infl uences their impact on sediment mixing, irrigation, and nutrient fl uxes, and their effects on the surrounding communities. Moreover, the juveniles of most soft - sediment bivalves live at or close to the sediment surface, and move successively deeper into the sedi-ment as they grow. Burrowing depth depends on siphon length (Zwarts and Wanink 1989 ); bivalves with short siphons live just under-neath the sediment surfaces (e.g., hard clams or northern quahog, Mercenaria mercenaria ), while species with longer siphons may be buried up to 40 cm down in the sediment (e.g., soft - shelled clams, Mya arenaria ) or even 80 cm (geoducks, Panopea abrupta ); however, shallow - burying bivalves (such as clams) tend to move more, thereby bioturbating the upper-most sediment layers more than the deep bur-rowers. Sediment reworking rates may further differ with season and food availability, even within a bivalve species (Stead and Thompson 2006 ; Maire et al. 2007 ). Thus, the patterns of bivalve bioturbation and facilitation effects on surrounding communities are temporally


important and diversity no longer increases (Whitlatch et al. 1997 ).

Bivalve bioturbation has the potential to modify signifi cantly the coastal sea and land-scape. The prevalence of different types of soft - sediment habitats in coastal areas depends on the stability of the sediments, that is, the balance between rates of sediment deposition and sediment erosion. These processes are ulti-mately governed by hydrodynamic forcing (currents, waves) transporting the sediment

species in the system (sponges, bryozoans, tunicates, algae, etc.) (Guti é rrez et al. 2003 ). The bivalves affect the sedimentary habitat even after they die, as the shell debris contin-ues to provide structure in the habitat (Hewitt et al. 2005 ; Erwin 2008 ) with positive infl u-ences on biodiversity. The effect of bivalves on the physical heterogeneity of the habitat is naturally dependent on bivalve density and aggregation. For example, at very high bivalve densities, competition for space becomes

Table 10.3 Adult burrowing depth in natural populations of selected bivalve species and the type of shellfi sh aquaculture they are used in. In addition, their potential to actively bioturbate sediments in different types of culture is indicated with ( + ) or ( − ).

Species Burrowing depth Type of culture Potential for bioturbation in culture

Mercenaria mercenaria (northern quahog, hard clam)

1 – 3 cm (up to 20 cm) Bottom ( “ free ” ) +

On - bottom bags, cover nets

+

Mya arenaria (soft - shelled clam)

10 – 20 cm (up to 40 cm) Bottom +

Panopea abrupta (geoduck clam)

60 – 80 cm Bottom +

Crassostrea gigas (Pacifi c oyster)

0 Bottom −

Longlines, off - bottom bags and racks

−

Crassostrea virginica (eastern oyster)

0 Bottom −

Suspended −

Mytilus edulis (blue mussel) 0 Bottom −

Suspended −

Mytilus galloprovincialis (Mediterranean mussel)

0 Bottom −

Suspended −

Ruditapes philippinarum (Manila clam)

0 – 5 cm Bottom +

For many species, the burrowing depth differs between summer and winter (Zwarts and Wanink 1989 ). In cold climates, bivalves move deeper into the sediment in winter to avoid freezing, whereas in hot climates, bivalves may move deeper in summer to avoid overheating.


philippinarum ), and Baltic clams ( Macoma balthica ) (Widdows and Brinsley 2002 ; Sgro et al. 2005 ; Ciutat et al. 2007 ). Although natural clam populations may act to destabilize sediments, enhance erosion rates, and prevent siltation, the nets used to keep clams in place in aquaculture installations increase the rates of sedimentation and increase the sediment silt content (Kaiser et al. 1996 ; Chapter 9 in this book). Problems with sedimentation can, however, be avoided with development of better culture methods, such as the bags used for clam culture in Cedar Key, Florida (http://shellfi sh.ifas.ufl .edu). These bags also provide habitat for other species and enhance diversity, provided the siting and layout of the bags is appropriate and coordinated. To predict sedi-ment transport patterns, the critical thresholds for sediment erosion need to be identifi ed (Le Hir et al. 2007 ). Faunal effects on sediment erosion, transport, and deposition have mainly been studied in intertidal areas, and our knowl-edge about these effects in deeper areas is much more limited.

The interactions between sediment stabiliz-ing and destabilizing processes are complex, dynamic, and continually at work. While bio-turbating bivalves may destabilize the sedi-ment, their bioturbation may simultaneously enhance nutrient fl uxes from the sediment, which promotes the growth of sediment stabi-lizing microphytobenthos (Sandwell et al. 2009 ). Within a bivalve bed the continuous reworking of the sediment, which is character-istic for biodiffusers such as most infaunal bivalves, homogenizes the sediment and pre-vents formation of permanent structures and may prevent establishment of, for example, invasive salt marsh species. Conversely, spread-ing salt marshes reduce the habitat available for shellfi sh (Neira et al. 2006 ). Sediment sta-bilizers and destabilizers have spatially and temporally variable effects on the community, usually favoring their own type, which facili-tates the persistence of patches (Volkenborn

and affecting its sorting and grain size, but biota signifi cantly infl uences the formation and persistence of different habitat types by affecting the stability of the sediment (Widdows et al. 2004 ; Le Hir et al. 2007 ).

In aquatic ecosystems some species act as sediment stabilizers (enhance sediment deposi-tion, inhibit erosion), while other species act as sediment destabilizers (enhance erosion and sediment transport) (Widdows et al. 2000 ; Bouma et al. 2009 ). By providing physical pro-tective structures, for example, mussel beds, oyster reefs, seagrass meadows, salt marsh plants, and tube - building polychaetes stabilize the sediment, modify the local hydrodynamics, and enhance sediment deposition. Also, micro-phytobenthos (i.e., microalgae/microorganisms living on the sediment surface) enhance sedi-ment cohesiveness through the extracellular polymeric substances they secrete, which form a protective biofi lm on the sediment surface.

Other species act as sediment destabilizers by disrupting the cohesiveness of the sediment, which decreases the sediment mud content and increases erosion rates. The sediment is desta-bilized, for example, by clams, crustaceans, and lugworms that bioturbate or mix the sedi-ment and facilitate resuspension (Widdows and Brinsley 2002 ). The sediment is also desta-bilized by grazers removing the protective microphytobenthic biofi lm. Further, increased bed roughness and scouring around patches of animals or plants can destabilize sediments and enhance erosion locally. Bioturbating bivalves affect resuspension rates, both directly and indirectly, actively and passively (Graf and Rosenberg 1997 ). Experiments in nonaquacul-ture settings have demonstrated a positive rela-tionship between bivalve density and sediment erosion, which is likely a combination of the bivalve - induced bioturbation and increased bed roughness, both of which promote sedi-ment erosion. These patterns have been found for a number of species, including cockles ( Cerastoderma edule ), Manila clams ( Ruditapes


impact benthic ecosystems also during seed collection and harvesting. These other aspects, however, concern management practices and are dealt with in Chapters 3 and 11 in this book.

Bivalves have a dominating organizational role in ecosystems as they shunt a lot of the production from the pelagic to the benthic system in the form of biodeposits (Dame 1993 ; Newell 2004 ). Both feces and pseudofeces are ejected as mucus - bound aggregates, which sink faster than nonaggregated particles, thus aiding the vertical downward fl ux and increas-ing the deposition locally above background levels of sedimentation (Chapter 4 in this book; Ward and Shumway 2004 ). Rates of biodeposit production, and the ratio of feces to pseudofeces depends on the concentrations of food particles (phytoplankton, some detri-tus) and suspended sediment (inorganic matter), all of which vary seasonally, and also on the bivalve species, as different species have different clearance rates and abilities to select particles preferentially (Kautsky and Evans 1987 ; Jaramillo et al. 1992 ; Newell 2004 ; Ward and Shumway 2004 ; Giles et al. 2006 ). High loads of suspended sediments in the water (e.g., in sheltered, turbid estuaries) lead to larger amounts of pseudofeces being pro-duced, which also increases the downward fl ux of particulate matter to the sediment (Iglesias et al. 1996 ; Norkko et al. 2001 ).

Effects of w ater fl ow

Patterns of biodeposit accumulation or erosion in bivalve beds or underneath suspended bivalve cultures are mainly driven by the water fl ow at the site, with higher current velocities promoting erosion and effi cient dispersal of the biodeposits (Chamberlain et al. 2001 ; Hartstein and Rowden 2004 ; Weise et al. 2009 ; Chapters 4 , 6 , and 9 in this book). With greater tidal currents and wave action, resuspension of biodeposits is more likely in intertidal or shallow bivalve beds, compared

et al. 2009 ). These processes thus act both to modify and to maintain specifi c habitats. The antagonistic interactions between bioturbators and habitat - forming ecosystem engineers such as seagrasses, salt marshes, or oyster reefs create patchiness and habitat diversity, thereby favoring an overall higher biodiversity at the estuary scale (Jones et al. 1994 ; Bouma et al. 2009 ).

To minimize disruption of sediment trans-port patterns in an estuary and thus maintain the current extent of the existing habitat types in the estuary, the complex interactions between sediment stabilizers and destabilizers need to be considered. This has implications for where bivalve aquaculture plots should be located in an estuary and what the spatial scale, type of culture, and layout of the instal-lations should be, for example, continuous cover or several separate sections (Dumbauld et al. 2009 ).

Biodeposit p roduction and d egradation: e ffects on s ediment b iogeochemistry

Bivalves affect fl uxes of particles to and from the seafl oor, both by directly intercepting and ejecting particles as part of their feeding, and by physically altering the hydrodynamic conditions that govern sedimentation and erosion rates (Graf and Rosenberg 1997 ; Widdows et al. 1998 ) (Chapter 9 in this book). Through their feeding, bivalves produce feces and pseudofeces, collectively termed biodeposits when they reach the seafl oor. Chapter 4 (in this book) on “ Bivalves as bio-fi lters ” provides details on regulation of feeding and production of feces and pseudofe-ces. In this section the focus is on biodeposits after they have been deposited on the seafl oor and their context - dependent effects on benthic nutrient fl uxes and surrounding benthic habitats. In addition to the ongrowing phase considered here, bivalve aquaculture may


subsidy to benthic systems (Wotton and Malmqvist 2001 ). As the biodeposits may be rich in carbon and nitrogen, surrounding deposit - feeding macro - , meio - , and micro-fauna can benefi t from increased food quality (Kautsky and Evans 1987 ; Norkko et al. 2001 ; Giles et al. 2006 ). The effects of increasing biodeposition follow the general hump - shaped benthic responses to organic enrichment, with increasing benthic diversity, abundance, and biomass at early stages of enrichment, and increasing sediment oxygen demand and anoxic conditions with benthic community disruption after severe enrichment (Pearson and Rosenberg 1978 ) (Fig. 10.3 ). The effects are directly related to the amounts of organic matter deposited and remaining on the sea-fl oor, and as noted earlier, these amounts are dependent on bivalve species and density, the quality and quantity of their food supply, and the hydrodynamic setting, water fl ow, and depth at the site (Fig. 10.3 ).

with bivalve beds or suspended aquaculture systems in deeper waters. In enclosed embay-ments, however, the tidal fl ushing may not be suffi cient and biodeposits accumulate under-neath shellfi sh farms (Cranford et al. 2009 ; Chapters 4 and 6 in this book) (Fig. 10.3 ). In deeper waters the biodeposits from suspended culture may be dispersed over a larger area before reaching the seafl oor and thus have no detectable impact on the benthic habitat. The rates of biodeposit accumulation or erosion are further affected by the density of biotur-bating infaunal bivalves and other fauna as they enhance resuspension and dispersal of biodeposits by acting as sediment destabilizers (see previous section).

Organic e nrichment

Bivalve biodeposition represents an organic enrichment of the sediment and this additional organic matter provides an important food

Figure 10.3 Schematic diagram of the context and density dependence of the effects of bivalve populations and their biodeposits on surrounding benthic communities. Panels A – C represent increasing densities of bivalves in either natural or bottom - cultured populations, while panel D represents a high - density suspended culture, where the bivalves are not able to bioturbate the sediments. Computational model by Alf Norkko.


may also develop in areas of high biodeposi-tion and high sediment oxygen demand. Since Beggiatoa requires both oxygen and H 2 S for metabolism, its presence indicates that the reducing conditions in the sediment have reached the sediment surface.

Effects of b ioturbation on b enthic n utrient fl uxes and the p rocessing of b iodeposits

The biogeochemical effects of biodeposition from shellfi sh aquaculture are strongly depen-dent on the quantity and quality of the mate-rial deposited. Effi cient bivalve bioturbation does, however, ameliorate the potentially neg-ative effects of excessive biodeposition since particle and solute transport by bioturbating fauna signifi cantly infl uences rates and path-ways of organic matter mineralization, par-ticularly by increasing the oxygen penetration depth in the sediments. For example, Mya arenaria burrows are sites of enhanced micro-bial activity and high rates of sulphate reduc-tion (Hansen et al. 1996 ) and burrowing Mercenaria mercenaria increase benthic fl uxes of oxygen and nutrients (Doering et al. 1987 ). Bioturbation enhances coupled nitrifi cation - denitrifi cation, and under fully oxygenated conditions any remaining phosphorus in the biodeposits is also permanently buried with the accumulating sediments.

Infaunal bivalves both produce biodeposits and facilitate the remineralization of them in the sediment (Figs. 10.1 and 10.3 ). Thus, the combination of biodeposition and bioturba-tion by clams maintains a balanced benthic metabolism (Nizzoli et al. 2006 ), with the benthic nutrient fl uxes being dependent on bivalve density (Sandwell et al. 2009 ). In natural infaunal bivalve beds and bottom cul-tures of clams and mussels, rates of biodeposi-tion are not likely to reach high - enough levels to induce anoxic conditions and high levels of sulfi de in sediments due to the negative feed-back excessive biodeposition would have on

Effects of b iodeposition on s ediment b iogeochemistry

Biodeposits affect the biogeochemistry in the sediment and at the sediment – water interface. Although bivalves also directly excrete inor-ganic nutrients, the remineralization processes of the biodeposits in the sediment are usually more important for nutrient regeneration and fl uxes (Prins et al. 1998 ; Newell 2004 ). Accumulation of biodeposits increases sedi-ment organic content, promotes high micro-bial activity and increases the sediment oxygen demand (Rodhouse and Roden 1987 ; Wotton and Malmqvist 2001 ; Nizzoli et al. 2006 ; Hargrave et al. 2008 ; Cranford et al. 2009 ), but the effects of biodeposition are site specifi c (Chamberlain et al. 2001 ; Hartstein and Rowden 2004 ).

The decomposition of organic material con-sumes oxygen and increased sediment oxygen demand is commonly recorded, for example, under mussel culture longlines. High rates of biodeposition may adversely affect the sedi-ment microbial community by shifting it from an aerobic to an anaerobic metabolism. The changing oxygen conditions subsequently affect nutrient fl uxes in and out of the sedi-ment. Under anoxic conditions phosphorus is released from iron compounds in the sediment. Biodeposition also affects the cycling, reten-tion, and loss of nitrogen from the sediment (Cranford et al. 2007 ). Coupled nitrifi cation - denitrifi cation removes nitrogen from the system in the form of N 2 gas, but requires adjacent oxygenated sediments with nitrifying microbes and anoxic sediments with denitrify-ing microbes (Newell et al. 2002 ). Thus, the process is inhibited if the overlying water turns anoxic. Sediments underlying intensive shell-fi sh aquaculture release ammonium since the coupled nitrifi cation - denitrifi cation has been disrupted (Hatcher et al. 1994 ; Newell et al. 2002 ). If the sediments turn anoxic, concentra-tions of H 2 S may build up to toxic levels. White sulfur bacterial mats ( Beggiatoa spp.)


and added physical structure from either bivalve shells or farming installations. The effects of organic enrichment from biodeposi-tion, however, have proven to be highly site specifi c and context dependent, and range from signifi cant positive effects (Inglis and Gust 2003 ; D ’ Amours et al. 2008 ), to no or minimal effects (Hatcher et al. 1994 ; Grant et al. 1995 ; Kaiser et al. 1996 ; Chamberlain et al. 2001 ; Crawford et al. 2003 ), to signifi -cant negative effects with impoverished benthic communities under/near the farms (Smith and Shackley 2004 ; Hargrave et al. 2008 ; Cranford et al. 2009 ). Inside bivalve beds and under lines of suspended bivalves, the benthic infau-nal species composition generally shifts toward species smaller, opportunistic detritivores, more tolerant to higher organic content, such as Oligochaeta and capitellid polychaetes (Beadman et al. 2004 ; Commito et al. 2005 ; Norling and Kautsky 2007 ; Ysebaert et al. 2009 ). Shells falling from mussel lines may also provide additional habitat and heteroge-neity, with positive effects on the surrounding fauna (Grant et al. 1995 ). At very high rates of biodeposit accumulation, however, the sedi-ment becomes anoxic and the macrofauna dis-appears. The net effects will depend both on the scale, stocking densities, and intensities of farming, as well as the hydrodynamic regime at the site (water depth, currents, sedimenta-tion rates), which will interact to determine the amount of waste products accumulating on the seabed (Fig. 10.3 ). It has, however, repeat-edly been reported that effects of, for example, mussel beds are relatively local and depend on bivalve density (Beadman et al. 2004 ; Hartstein and Rowden 2004 ; Ysebaert et al. 2009 ). Therefore, using a somewhat lower stocking density in combination with suffi cient fl ow can reduce the potential negative effects on the benthic environment (Beadman et al. 2004 ).

Since shellfi sh aquaculture is based on natural food sources, no additional nutrients or organic matter are added to the system. Therefore, the amount of biodeposition, and

bivalve densities. Nizzoli et al. (2006) com-pared mussel and clam farming and found that overall impacts of suspended mussel farming on oxygen and nutrient dynamics were greater than those of infaunal clam farming, and attributed this to the fact that infaunal, biotur-bating bivalves stimulate transfer of both organic matter and oxygen in to the sediment, whereas suspended bivalves only enhance transfer of organic matter to the sediment via biodeposition. This also affected the pathways of nitrogen cycling.

The feedback mechanisms between sedi-ment organic content, oxygen conditions, and bioturbation are complex. For example, hard clams do not burrow as deep under hypoxic conditions, with a potential for cascading negative effects on sediment oxygenation (Weissberger et al. 2009 ). It is therefore impor-tant to limit rates of biodeposit accumulation to a level at which the bioturbators can still process effectively. Model calculations indicate that even though the harvest represents a net removal of phosphorus and nitrogen from the ecosystem, the deposition of feces and pseu-dofeces from a mussel farm increases the reten-tion time of nutrients in some coastal areas (Cranford et al. 2007 ; Brigolin et al. 2009 ). With careful scaling and placement of farms in areas with suffi cient fl ow, and by maintain-ing suffi cient levels of bioturbation under the farms, mussel aquaculture can be used to remove nutrients from the system and thus combat eutrophication (Newell 2004 ; Lindahl et al. 2005 ; Gren et al. 2009 ; Chapter 8 in this book).

Effects of b iodeposits on b enthic c ommunity c omposition

Shellfi sh aquaculture infl uences the surround-ing benthic habitat through three main mecha-nisms: increased input of organic matter through biodeposition; increasing hypoxic and sulfi dic sediments due to increasing oxygen demand from decomposition of biodeposits;


Heck, 2001b ). Bioturbating bivalves inside seagrass meadows also renew the water at the sediment surface and thereby reduce the risk of oxygen depletion. Nevertheless, particularly in eutrophic areas, high levels of biodeposition may lead to toxic sulfi de concentrations in the sediment and increase the ammonium effl ux from the sediment, which facilitates epiphyte growth, resulting in impaired growth of sea-grass (Vinther and Holmer 2008 ; Vinther et al. 2008 ). Also, rack and stake oyster culture negatively infl uence seagrasses through physi-cal disturbance and shading (Everett et al. 1995 ). If densities of aquaculture gear are suf-fi ciently low, however, there are only minimal effects on seagrasses of, for example, oyster depuration gear (Vaudrey et al. 2009 ). Therefore, the multiple interactions between seagrass habitats and shellfi sh aquaculture need to be considered and managed at appro-priate scales (Dumbauld et al. 2009 ).

Effects of b ioturbation on c ontaminants and r esting s tages in the s ediments

Bivalve bioturbation also affects the mixing and depth distribution of contaminants and has the potential to either bury these elements deeper or to bring them back into circulation. For example, Ciutat et al. (2006) found a posi-tive correlation between the density of cockles ( Cerastoderma edule ) and the resuspension of both sediment and polycyclic aromatic hydro-carbon s ( PAH s). Similarly, bioturbation by the bivalve Tellina deltoidalis in metal contami-nated sediments caused metal release from the pore waters and higher concentrations of iron and manganese in overlying waters (Atkinson et al. 2007 ). On the other hand, bioturbation by Baltic clams increased the retention of cadmium and a hydrophobic organic pollutant in the sediment (Hedman et al. 2008 ). Thus, the fate of contaminant is dependent both on

thus organic enrichment and potential subse-quent negative effects, is signifi cantly less under shellfi sh aquaculture installations com-pared with fi nfi sh aquaculture (Folke and Kautsky 1989 ; Naylor et al. 2000 ; Newell 2004 ). In fi nfi sh farming stocking densities are higher and the fi sh are fed artifi cial diets, resulting in a net addition of nutrients and organic matter to the site, which may result in waste accumulation and anoxic bottoms under the fi sh cages, disturbed benthic communities, and eutrophication of the surrounding ecosys-tem (Gowen and Bradbury 1987 ; Wu 1995 ; Kalantzi and Karakassis 2006 ). Due to this fundamental difference, it is important and essential to consider fi nfi sh and shellfi sh aqua-culture as two separate industries.

Interactions between b ivalve b ioturbation and s eagrasses

In coastal areas, seagrass meadows are impor-tant structured habitats, providing nursery areas for fi sh and shellfi sh (Heck et al. 2003 ). Suspension - feeding bivalves reduce water tur-bidity, which enhances light penetration and thereby potentially promotes benthic primary producers, such as seagrasses and microphyto-benthos. For example, successful recruitment of Mya arenaria was instrumental in turning a Danish lagoon from a turbid state to a clear - water state (Petersen et al. 2008 ). In some areas, improved water clarity resulting from large beds of cultured bivalves has even led to the reestablishment of seagrasses (Shumway and Kraeuter 2004 ). The effects are, however, species dependent and, for example, eastern oysters ( Crassostrea virginica ) have higher clearance rates than hard clams and therefore promote seagrass production more (Newell and Koch 2004 ). Sediment nutrient enrich-ment by biodeposits from natural bivalve pop-ulations can also elevate seagrass productivity (Peterson and Heck 2001a ; Peterson and


organic content, hydrodynamic conditions, and environmental stress. Nevertheless, we are lacking in our understanding of the generality and ecosystem - scale consequences of these fl uxes. Since the positive or negative effects of bivalve biodeposits are quality, quantity, and context dependent, and modifi ed by bivalve bioturbation, studies of the effects of organic enrichment from shellfi sh aquaculture on sedi-ment biogeochemistry, benthic communities, and seagrass beds have yielded site - specifi c and sometimes nonconclusive results. The associ-ated complex biogeochemical processes are diffi cult to measure over larger scales in the fi eld, but at the same time results gained from laboratory experiments are diffi cult to general-ize to, for example, sites with different hydro-dynamic regimes (Porter et al. 2004 ). Therefore, an integrated approach consisting of well - designed laboratory experiments, fi eld studies across different sites and along gradients within sites, and modeling is required to understand these processes and to apply them at the appropriate scale to sustainable manage-ment of shellfi sh aquaculture (Dumbauld et al. 2009 ).

The benthic effects of bivalve aquaculture differ signifi cantly between cultured species and also between different types of culture of the same species (Nizzoli et al. 2006 ; Ysebaert et al. 2009 ). Suspended culture generally only affects benthic environments through their biodeposition, while on - bottom culture affects benthic habitats through both biodeposition, altered physical structure at the sediment surface, and bioturbation of the sediments. Therefore, for example, clam farming results in a more balanced benthic metabolism, although it may be limited by available space. As the effects of biodeposition on the benthic environment are relatively local and dependent on the hydrodynamic regime, in order to mini-mize negative impacts on the benthic commu-nities, farms should be sited in areas with relatively high current velocities and suffi cient

the type of compound and the rates of biotur-bation in the habitat.

Many planktonic species form dormant cysts or resting stages under adverse environ-mental conditions. The bioturbation - induced mixing processes apply to these cysts as well and the burial and reemergence of these is part of the natural cycle for many species. For example, Baltic clams extend the distribution of cladoceran resting eggs deeper into the sedi-ment (Viitasalo 2007 ) and also differentially affect the emergence of several zooplankton species from the sediment (Viitasalo et al. 2007 ).

Summary

Bioturbation and bioirrigation are very small - scale activities by individual bivalves, but the net effects of a whole bivalve population may have consequences for the long - term develop-ment of an entire coastal system, both in terms of nutrient dynamics and sediment stability. This highlights the importance of considering the appropriate spatial and temporal scales for both studying and managing any particular process, installation, or environmental effect, including shellfi sh aquaculture operations.

Bivalve bioturbation facilitates transport of particulate and dissolved material between the sediment and the overlying water, oxygenates the sediment, and produces complex and favorable microhabitats, which facilitate benthic communities with higher overall diver-sity. It is commonly assumed that there is a general positive relationship between high diversity and well - functioning, healthy ecosys-tems. One way to assess ecosystem function is to estimate rates of nutrient fl uxes in and out of the sediments (Lohrer et al. 2004 ). There are numerous studies on nutrient fl uxes and bivalves, and we know that they are infl u-enced, for example, by the interactions between bivalve density and species, sediment type,


Journal of Experimental Marine Biology and Ecology 371 : 20 – 33 .

Bouma , T.J. , Olenin , S. , Reise , K. , and Ysebaert , T. 2009 . Ecosystem engineering and biodiversity in coastal sediments: posing hypotheses . Helgoland Marine Research 63 : 95 – 106 .

Brigolin , D. , Dal Maschio , G. , Rampazzo , F. , Giani , M. , and Pastres , R. 2009 . An individual - based population dynamic model for estimating biomass yield and nutrient fl uxes through an off - shore mussel ( Mytilus galloprovincialis ) farm . Estuarine, Coastal and Shelf Science 82 : 365 – 376 .

Chamberlain , J. , Fernandes , T.F. , Read , P. , Nickell , T.D. , and Davies , I.M. 2001 . Impacts of biode-posits from suspended mussel ( Mytilus edulis L.) culture on the surrounding surfi cial sediments . ICES Journal of Marine Science 58 : 411 – 416 .

Ciutat , A. , Widdows , J. , and Readman , J.W. 2006 . Infl uence of cockle Cerastoderma edule biotur-bation and tidal - current cycles on resuspension of sediment and polycyclic aromatic hydrocar-bons . Marine Ecology Progress Series 328 : 51 – 64 .

Ciutat , A. , Widdows , J. , and Pope , N.D. 2007 . Effect of Cerastoderma edule density on near - bed hydrodynamics and stability of cohesive muddy sediments . Journal of Experimental Marine Biology and Ecology 346 : 114 – 126 .

Commito , J.A. , Celano , E.A. , Celico , H.J. , Como , S. , and Johnson , C.P. 2005 . Mussels matter: postlarval dispersal dynamics altered by a spa-tially complex ecosystem engineer . Journal of Experimental Marine Biology and Ecology 316 : 133 – 147 .

Crawford , C.M. , Macleod , C.K.A. , and Mitchell , I.M. 2003 . Effects of shellfi sh farming on the benthic environment . Aquaculture 224 : 117 – 140 .

Cranford , P.J. , Strain , P.M. , Dowd , M. , Hargrave , B.T. , Grant , J. , and Archambault , M. - C. 2007 . Infl uence of mussel aquaculture on nitrogen dynamics in a nutrient enriched coastal embay-ment . Marine Ecology Progress Series 347 : 61 – 78 .

Cranford , P.J. , Hargrave , B.T. , and Doucette , L.I. 2009 . Benthic organic enrichment from sus-pended mussel ( Mytilus edulis ) culture in Prince Edward Island, Canada . Aquaculture 292 : 189 – 196 .

water exchange (Hartstein and Rowden 2004 ; Dumbauld et al. 2009 ) since in enclosed embayments the dispersive capacity may be surpassed (Cranford et al. 2009 ).

Finally, homogenization of habitats removes the small - scale heterogeneity that sustains diversity, and loss of biodiversity will ulti-mately lower the ocean ’ s capacity to provide food for human consumption (Worm et al. 2006 ). Thus, shellfi sh aquaculture should be managed in the light of minimizing negative impacts on diversity.

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