Shellfish Aquaculture and the Environment (Shumway/Shellfish Aquaculture and the Environment) || Bivalve Shellfish Aquaculture and Eutrophication

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  • Chapter 7

    Bivalve s hellfi sh a quaculture and e utrophication JoAnn M. Burkholder and Sandra E. Shumway

    Summary

    Increased nutrient supplies and associated pol-lutants from land - based human activities have pervasively degraded coastal ecosystems worldwide, destroying habitats, causing fi nfi sh and shellfi sh disease and death, and promoting harmful algal blooms. While these effects of cultural eutrophication (anthropogenic nutri-ent overenrichment) from land - based human activities are well known, recent controversy has focused on another source of nutrient enrichment, aquaculture, as potentially a major contributor to eutrophication. Here we evaluate the signifi cance of bivalve shellfi sh aquaculture in the eutrophication of coastal waters based on the available evidence and,

    conversely, the impacts of land - based nutrient pollution and associated pollutants on bivalve aquaculture.

    Of the 62 ecosystems reviewed here, 7% or four ecosystems have sustained system - level adverse impacts from large, intensive bivalve culture operations. The other 93% have sus-tained either negligible or only localized sig-nifi cant adverse effects contributing to eutrophication from bivalve shellfi sh aquacul-ture. Thus, the great majority of ecosystems with bivalve aquaculture studied to date have been described as sustaining minimal or only localized signifi cant eutrophication effects from shellfi sh farming. Instead, the utility of bivalve aquaculture in effectively reducing phytoplankton and the nutrients available for

    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.

    155

  • 156 Shellfi sh Aquaculture and the Environment

    contribute little to eutrophication except in some poorly fl ushed areas with high shellfi sh density, and aquaculturists should strive to maintain cultures below ecological carrying capacity to prevent such ecosystem - level adverse effects. In contrast to the generally minimal effects of bivalve aquaculture on eutrophication, major, pervasive nutrient pol-lution from many urban and agricultural sources is seriously affecting shellfi sh popula-tions and shellfi sh aquaculture in many coastal waters of the world, and these impacts are expected to increase with rapidly expanding coastal development. Considering that shell-fi sh aquaculture is vital to meet the seafood demands of the rapidly increasing global human population, there is a pressing need for resource managers and policymakers to increase protection of shellfi sh aquacul-ture operations from land - based nutrient pollution.

    Introduction

    Cultural eutrophication, the process of over-enriching of surface waters with excessive nutrients from human activities, is among the most serious recognized threats to present - day coastal ecosystems (National Research Council [NRC] 2000 ; GEOHAB, Global Ecology and Oceanography of Harmful Algal Blooms Programme 2006 ). Increased nutrient supplies from land - based human activities have perva-sively degraded coastal ecosystems to the extent that more than two - thirds of coastal rivers and bays in the United States are now moderately to severely degraded from cultural eutrophication, exacerbated by poor fl ushing and signifi cant human population growth in coastal areas (Bricker et al. 1999 , NRC 2000 ). The excessive nutrients can stimulate blooms of noxious and toxic algae, and increase water column turbidity from the algal overgrowth together with pollutants such as suspended sediments that accompany nutrient loading. The reduced light causes benefi cial seagrass

    blooms is being harnessed by some nations for economic benefi t to offset nutrient overenrich-ment from land - based sources.

    The effects of bivalve culture on the sur-rounding environment are site - specifi c and especially depend on the hydrography (fl ush-ing and water exchange) and shellfi sh density. Exceptions to minimal or localized effects have been documented at the ecosystem scale, mostly in poorly fl ushed lagoons with high - density shellfi sh culture. These exceptions underscore the need to consider the ecosys-tem s carrying capacity, rather than only the carrying capacity for maximal shellfi sh pro-duction, in bivalve aquaculture over large areas within a given system. Such consider-ations increasingly are assisted by models such as the Farm Aquaculture Resource Management ( FARM ) model and the shellfi sh aquaculture waste model DEPOMOD.

    In contrast to the localized effects generally reported for bivalve aquaculture, land - based sources of eutrophication have overwhelmed many coastal ecosystems worldwide, and coastal population growth and associated nutrient pollution are continuing to increase rapidly. The acute, obvious effects of urban and agricultural nutrient pollution, often accompanied by loadings of suspended sedi-ments, microbial pathogens, and toxic sub-stances, are fi sh kills and high - biomass algal blooms. Much more serious chronic impacts, however, include long - term shifts in nutrient supplies, increased dead zones of low - oxygen bottom water, loss of critical habitat such as seagrass meadows, stimulation of harmful algal species that are low in food quality, reduction of shellfi sh recruitment and grazing, and increased shellfi sh physiological stress, disease, and death. Increasing tempera-tures from present warming trends in climate change can stress shellfi sh, and would be expected to interact with pollution to weaken shellfi sh hosts further and facilitate pathogen attack.

    Overall, relative to land - based pollution sources, bivalve aquaculture has been found to

  • Bivalve shellfi sh aquaculture and eutrophication 157

    of balance, these multiple stressors interact to cause the disease and death of higher trophic level organisms such as wild fi nfi sh and shell-fi sh (Wiegner et al. 2003 ).

    While the effects of eutrophication from land - based human activities are well known, recent controversy has focused on another source of nutrient overenrichment, aquacul-ture, as potentially a major contributor to cul-tural eutrophication (Goldberg and Triplett 1997 ; Kaiser et al. 1998 ; Newell 2004 ; Richard 2004 ) (Fig. 7.1 ). Finfi sh culture requires direct inputs of nutrient - rich feed, whereas shellfi sh culture relies mostly on naturally occurring phytoplankton and suspended matter, with no

    meadows to die because of depressed photo-synthesis (Burkholder et al. 2007 and refer-ences therein). In addition, while the excess algae photosynthesize and increase the dis-solved oxygen (DO) during the day, at night their respiration can deplete most or all of the available oxygen so that fi sh suffocate to death (Breitburg 2002 ). As the algal blooms senesce and die, their decom position contributes to this oxygen sag. Harmful microbial pathogens viruses, bacteria, fungi, and protozoans also frequently are added along with nutrient overenrichment (Burkholder et al. 1997 , and references therein; Paul and Meyer 2001 ). As the ecosystem is driven out

    Figure 7.1 Conceptual diagram of land - based nutrient sources from watershed runoff and atmospheric pollution (nitrogen [N] as inorganic forms [N i nitrate, ammonium], particulate N, dissolved organic N [DON]; phosphorus [P]; and carbon, especially considering dissolved organic carbon [DOC]), and bivalve shellfi sh aquaculture (bivalves) interactions with nutrient supplies in coastal ecosystems as related to (1) removal of seston (suspended particulate material) during fi lter feeding, (2) biodeposition of feces and pseudofeces, (3) excretion of nutrients (especially ammonia, which is ionized to ammonium; also phosphate and various organic nutrient forms), (4) removal of N, P, and organic carbon in bivalve harvest, and (5) resuspension of nutrients, detritus, and sediments into the water column during some harvesting activi-ties. (Modifi ed from Cranford et al. 2006 .) Note that 1 = primary; and that this diagram depicts oxygenated (aerobic) sediments beneath the shellfi sh cultures, although localized impacts often include anoxic sediments beneath farms in poorly fl ushed areas.

    Land-basedatmospheric

    Land-basedrunoff

    Sunlight

    Detritus

    Phytoplankton

    Sediment

    Seston

    Tidalexchange

    N, P, C

    Benthic 1 Producers

    Harvest

    Nutrients

    Grazers,bacteria,

    fungi

    Biodeposits

    Mix

    ing

    Bivalves

    5

    41

    23

    NO3

    NO3

    NO2

    PO43

    NO2

    NH4+

    NH4+

    Organic N, P,C

    DOC

    Nitrification

    DenitrificationN2

    N2

    Burial

    N, P

    Aerobicsediment

    Anaerobicsediment

    N, P

    , O2

    Exc

    hang

    e

  • 158 Shellfi sh Aquaculture and the Environment

    Kautsky 1989 ). Others describe extreme adverse impacts on benefi cial naturally occur-ring macrofauna and plankton (Mattsson and Lind n 1983 , da Costa and Nalesso 2006 ). It has been suggested by some authors that, because of high regeneration of nutrients by shellfi sh, shellfi sh cultures may increase eutro-phication (Baudinet et al. 1990 ) by reducing nutrient limitation and stimulating algal growth rates (Prins et al. 1998 ). Decreased water movement and current velocity caused by the structural features of shellfi sh cultures (e.g., Nugues et al. 1996 ) would be expected to exacerbate these effects in the localized area. On the other hand, high densities of fi lter - feeding shellfi sh can depress phytoplank-ton biomass while promoting higher turnover rates (Doering et al. 1986 ; Sterner 1986 ; Doering 1989 , Asmus and Asmus 1991 ), and it has been argued that this control on phyto-plankton biomass can stabilize the ecosystem (Herman and Scholten 1990 ) as long as the algal assemblage does not escape control by shifts to species that are ineffi ciently fi ltered (Prins and Smaal 1994 ).

    This chapter addresses two questions: How signifi cant is bivalve shellfi sh aquaculture in the eutrophication (nutrient pollution, oxygen defi cits) of coastal waters, based on present evidence? Conversely, what are the impacts of land - based nutrient pollution and association pollutants on bivalve aquaculture?

    Most c ommonly r eported: l ocalized c hanges a ssociated with s hellfi sh a quaculture

    General e ffects

    In moderation, nutrient enrichment regard-less of the source promotes benefi cial incr-eases in phytoplankton and benthic algal production and, in turn, higher production of zooplankton, macroinvertebrates, fi nfi sh, and shellfi sh that use the primary (photosynthetic)

    supplementary food added. Adverse effects of shellfi sh farming on the water column and benthic environments under and near subtidal mussel farms have been described as compara-tively much lower than those around salmon farms (Mirto et al. 2000 ; La Rosa et al. 2002 ; Yokoyama 2002 ; Crawford et al. 2003 ).

    How does shellfi sh aquaculture affect nutri-ent enrichment of coastal areas? The general perception is that shellfi sh aquaculture is benign or benefi cial because it relies on ambient primary production, can improve water clarity and reduce nutrients and phytoplankton con-centrations through shellfi sh fi lter feeding, and does not require addition of fi sh or other food (Folke and Kautsky 1989 ; Crawford et al. 2003 ; Shumway et al. 2003 ). Shellfi sh fi lter feeding can depress phytoplankton biomass and alter phytoplankton assemblage structure, and the shellfi sh also can access carbon from the microbial loop through consumption of heterotrophic and mixotrophic bacteriovores (Lucas et al. 1987 ; Dupuy et al. 2000 ). In addi-tion, large macroinvertebrates and benthic fi shes sometimes respond positively to shellfi sh cultures (D Amours et al. 2008a ; see also Chapter 9 in this book).

    Nevertheless, the effects of shellfi sh culture on nutrient cycling and food web dynamics have received mixed reports. Increased nutri-ent supplies from shellfi sh biodeposits can promote phytoplankton and benthic algal growth, and the increased food supply can enhance shellfi sh growth (Weiss et al. 2002 ). In turn, the removal of phytoplankton by fi lter - feeding shellfi sh can effect a strong top - down control of eutrophication symptoms ( sensu Bricker et al. 2007 ), and the shellfi sh can also infl uence water column biogeochem-istry (Souchu et al. 2001 ). Some authors have reported that high densities of molluscs benefi -cially control eutrophication despite their addition of organic - rich biodeposits as feces and pseudofeces to the bottom sediments, and that mussel culture represents basically a self - regulated aquaculture system (Folke and

  • Bivalve shellfi sh aquaculture and eutrophication 159

    production directly or indirectly for food (Reitan et al. 1999 ; Paterson et al. 2003 ; Zeldis et al. 2008 ; Burkholder and Glibert 2011). But when added in excess, nutrient pollution can cause algal overgrowth. Nighttime respiration of the excess algal growth can cause oxygen depletion in bottom waters and sometimes throughout the water column. Decomposition of this excess production by aerobic bacteria and fungi can also lead to oxygen depletion. As more chronic, long - term effects, nutrient overenrichment promotes major shifts in the structure of plant and animal communities, often resulting in high biomass of a few toler-ant species and loss of overall biodiversity. Where aerobic surface sediments overlay deeper anaerobic sediments, microbially medi-ated, coupled nitrifi cation - denitrifi cation can convert organic and inorganic N from animal wastes, detritus, and other sources to nitrogen gas (N 2 ), which can effectively reduce the N available for most primary producers until the microbial consortium depletes the sedi-ment oxygen content. At that point, the coupled nitrifi cation - denitrifi cation is inhib-ited, more phosphorus can be released to the water column, and toxic hydrogen sulfi de can begin to accumulate (see Newell 2004 , and references therein).

    Shellfi sh beds take up chlorophyll a , seston, and particulate matter (particulate organic carbon, particulate organic nitrogen, and par-ticulate organic phosphorus POC, PON, and POP, respectively), and tend to release ammo-nium, orthophosphate, and silicate (Dame et al. 1991 ; Prins and Smaal 1994 ). Filtration and biodeposition of shellfi sh is considered benefi cial to water quality by controlling phy-toplankton densities and sequestering nutri-ents that are removed from the system when shellfi sh are harvested, buried in the sediments, or lost through denitrifi cation (Kaspar et al. 1985 ; Newell et al. 2002 ). Bivalve shellfi sh enhance benthic/pelagic coupling through fi lter - feeding of phytoplankton, deposition of feces and pseudofeces to the sediments, and

    increase of nutrient remineralization rates (Hatcher et al. 1994 ; Prins and Smaal 1994 ; Dame 1996 ). Thus, large densities of bivalves cultured in poorly fl ushed coastal waters can alter the pelagic - benthic energy fl uxes by depleti...

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