A SCIENTIFIC REVIEW
OF THE POTENTIAL ENVIRONMENTAL EFFECTS OF AQUACULTURE IN AQUATIC ECOSYSTEMS
- VOLUME 3
Table of Contents
NEAR-FIELD ORGANIC ENRICHMENT
FROM MARINE FINFISH AQUACULTURE
D.J. Wildish1, M. Dowd2, T.F. Sutherland3
and C.D. Levings3
1Marine Environmental Sciences, Fisheries and
Oceans Canada
St. Andrews Biological Station, St. Andrews, New Brunswick
2Dept. of Mathematics and Statistics, Dalhousie
University
Halifax, Nova Scotia
3Marine Environment and Habitat Sciences, Fisheries
and Oceans Canada
West Vancouver Laboratory, West Vancouver, British Columbia
EXECUTIVE SUMMARY
This paper reviews the literature on near-field organic enrichment associated
with intensive marine finfish aquaculture. Fish farms are a source of
suspended and dissolved organic matter, originating as fish feces, excess
fish feed and net-cleaning wastes. The term “near-field” is
used to differentiate between local (footprint limited) and more distant
(far-field) effects, and refers to effects within the sedimentary footprint
and between the population and community level. Near-field effects of
mariculture are bounded by the physical limits of particulate waste dispersal
and sedimentation from individual cages or farms.
PARTICLE TRANSPORT, DISPERSION AND BEHAVIOUR
To investigate the biogeochemical fate of organic matter in the benthic
or pelagic ecosystem, it is necessary to understand how this material
is transported and dispersed from the fish farm. Organic matter is transported
from fish cages to the surrounding marine environment by the action of
all types of water movements in the immediate vicinity of the cages. As
this material moves, it spreads out and its concentration decreases, both
by dilution and sedimentation.
Canadian coastal environments where aquaculture occurs are characterized
by irregular coastlines and complex topography. Consequently, they often
exhibit highly structured and quite complex flow fields. In strongly stratified
marine systems, dissolved material can be effectively trapped in the upper
or lower parts of the water column. In an aquaculture context, stratification
can be an important factor in the dispersal of organic matter from certain
farms in the inner portions of fjords in British Columbia.
Observational studies and numerical modelling are used to study transport
and dispersion in the coastal zone. Observational studies of mixing often
rely on the deployment of drifting buoys that mimic the movement of water
parcels. Field experiments releasing coloured dye into the ocean are better
able to characterize dispersion from a point source, but these are often
expensive, logistically difficult and environmentally sensitive. Numerical
circulation models, based on a set of mathematical equations that govern
fluid motion, provide a practical solution to the problem of coastal mixing.
In the water column, the behaviour of particles of organic matter is
characterized by settling and deposition. Settling rate depends on the
size, density and shape of particles. Stokes’ law provides a basic
framework for predicting the size dependence of particle settling. While
discrete particles exhibit Stokes’ settling behaviour, attractive
forces also cause the formation of particle aggregates. Particle aggregation
can effectively increase the settling flux of the original disaggregated
particle mixture by repackaging small particles into larger, more rapidly
sinking ones.
When particles settle from the water column, they may accumulate at the
sediment-water interface or be subject to further transport and redistribution.
When bottom shear stress exceeds a critical value, particles at the boundary
between the sediment and water can be set in motion. Susceptibility to
resuspension is set by a variety of sediment characteristics, including
particle density and size, and degree of consolidation. Factors such as
bioturbation have also been shown to effect erodibility of sediments (Andersen
2001). Numerical models are used to predict the temporal and spatial distribution
of particulates in the marine environment.
ORGANIC ENRICHMENT AS A PROCESS
Organic matter flux of fish feces, waste feed and detached fouling organisms
from cage surfaces, as well as natural particles, is monitored by measurements
based on nitrogen or carbon in sedimentation traps. In the context of
aquaculture, many authors examine carbon determined pyrolitically as a
measurement of organic matter flux. However, the chemical and physical
state of organic matter in sediments is not well understood. Thus, quantitative
measures of total organic carbon are poor indicators of biochemical availability
to biota.
The input of organic carbon to sediments, or sedimentation rate, is measured
in suspended sediment traps. Reported sedimentation rates under and near
salmon mariculture cages vary from 1 to 181 g C·m-2·day-1.
Notwithstanding differences in environmental conditions, farm size and
fish stocking densities, some of the variation in sedimentation rates
is due to inherent difficulties in suspended sediment trap methodology.
The benthic input from fish feces and waste feed can also be measured
by mass balance calculations: based on total organic carbon accumulated
in sediment, total input of fish feed, growth period and surface area
of the cage footprint. However, all farm sites have some water movement
and therefore require an examination of where the particles are deposited.
Cromey et al. (2002) developed a particle tracking model that uses depth
and particle settling rates as affected by observed currents with modelled
shear velocity and turbulence.
In soft sediments receiving natural background levels of sedimentation
(0.1 - 1.0 g C·m-2·day-1), the sediment-water
interface is aerobic, and this aerobic layer contains abundant macrofauna
and meiofauna. In contrast, soft depositional sediments receiving a continuous
elevated level of sedimentation, for example due to fish feces and waste
feed, become anoxic at the interface and develop a black, top-down sulfide
layer. Some of the sulfide produced may also be oxidized by other chemoautotrophic
bacteria (e.g. Beggiaotoa sp.) (Lumb and Fowler 1989). The white
patches of this bacteria may be seen on the sediment surface under fish
cages. Hargrave (1994) considered that flux rates of fish feces and waste
feed of >1.0 g C·m-2·day-1 caused
marked organic enrichment effects in net depositional sediments under
salmon cages. The process of organic enrichment in farm footprints requires
a varying amount of time to reach an equilibrium point, depending on oceanographic
and substrate conditions. Some studies have shown that organic enrichment
can be reversed if the increased levels of sedimentation are stopped (Brooks
et al. 2003).
The initial effect of a sudden addition of a high flux of readily decomposable
organic carbon to sediments is increased metabolism by aerobic bacteria,
leading to hypoxia and anoxia causing death of the most susceptible aerobic
life forms (Gray et al. 2002). In the fish cage footprint, the bulk of
the metabolism is by sulfate reduction at a higher rate than at reference
stations (Holmer and Kristensen 1992) and results in the loss of nitrification
and denitrification pathways (Kaspar et al. 1988). The death of burrowing
macrofauna leads to a rapid decline in the capability for irrigation or
aerated water within the upper profile and a more rapid development of
anoxia. The predominant bacteria become anaerobes, principally sulfate
reducers and methanogenic bacteria. Methane makes up the bulk of the outgassing
from heavily impacted farm sediments (Wildish et al. 1990), and sulfate
reduction produces hydrogen sulfide, which is readily oxidized in aerobic
seawater.
Organic enrichment indices may be regarded as proxies of the ecosystem
to indicate extent or amount of organic enrichment. The most widely accepted
index is based on macrofaunal species, abundance and biomass. Organic
enrichment gradients by Pearson and Rosenberg (1978) and Poole et al.
(1978) can be arbitrarily divided into four groupings based on the species
and density of macrofauna present. Both of these older indices suffer
because the macrofaunal or microbial surveys required to determine them
are expensive in time to obtain. Other methods can be linked to spatial
or temporal versions of the organic enrichment gradients based on macrofauna.
They include sediment profile imaging (Rhoads and Germano 1986; Nilsson
and Rosenberg 1997) and sediment geochemistry by redox and sulfide measurements
(Wildish et al. 2001).
Hargrave (1994) proposed a benthic enrichment index based on the product
of organic carbon and redox. The concept is to determine the sedimentation
rate from the carbon present in interfacial sediments. Cranston (1994)
described a geochemical method that is a direct measure of net carbon
burial rates. The method is based on downcore concentrations of sulfate
and ammonium, as indicators of the remineralization rates, and requires
large cores and numerous, expensive chemical determinations. However,
the method appears to be robust, and there is a positive linear relationship
between sedimentation and carbon burial rates. Recently, Dell’Anno
et al. (2002) suggested a suite of environmental variables to assess the
organic enrichment status of the coastal zone in the Mediterranean sea,
based on interfacial sedimentary variables.
ECOLOGICAL EFFECTS OF ORGANIC ENRICHMENT
Numerous reviews of organic enrichment associated with many industries
show two important generalities: the ecological response is complex, involving
pelagic-benthic coupling and both water column and sediments; and the
effects include all sources of organic matter, both natural and anthropogenic.
Different physical and biological conditions on the Atlantic and Pacific
coasts of Canada result in differing ecological responses to aquaculture.
In the Bay of Fundy, the salmon aquaculture industry does not usually
experience severe hypoxia in seawater because of energetic tidal mixing.
If hypoxia occurs, it is in sediment pore water and localized to the benthic
footprint area. There are few available data on dissolved oxygen in the
sediments and water column near fish farms in British Columbia. However,
naturally occurring low (<4 mg·L-1) dissolved oxygen
levels are present on the west coast of Vancouver Island and in Queen
Charlotte Strait during the late summer and early fall (Levings et al.
2002). On the Pacific coast, fish farms are located over deeper and more
diverse seabed habitats and most tenures include a mosaic of sediment
types and are not characterized by homogenous level mud bottoms. Rock
terraces, cliff walls and boulder fields are also under fish farms in
some locations (see Levings et al. 2002 and references therein).
The general response of soft-sediment macrofaunal populations and communities
to organic enrichment gradients is well established. It involves the local
extinction of the resident equilibrium community, followed by the re-establishment
of opportunists if conditions improve. Some species are more resistant
to hypoxia than others (Diaz and Rosenberg 1995). In general, the crustaceans
and echinoderms are most sensitive. Field studies suggest that, where
seasonal hypoxia occurs, dissolved oxygen (DO) levels of 1 ml·L-1
begin to cause macrofaunal invertebrate mortality (Diaz and Rosenberg
1995). In areas of permanent oxygen deficiency, the benthic communities
appear to be adapted to an even lower critical DO level. Although very
low DO levels are seen as the major limiting factor for macrofauna, the
role of H2S (and ammonia) is less clear. Where severe hypoxia
is present, both may be released.
Relatively little is known about the effects of organic enrichment on
ecosystem functioning. Simplistic approaches to assess ecosystem effects
assume that all of the secondary benthic production that becomes anoxic
or hypoxic is lost to the next trophic level of predators. However, these
approaches ignore that many individual predators are adapted to prey on
a specific set of a few species in an equilibrium community.
Azoic or anoxic sediments could cause a significant shift in pelagic-benthic
coupling. The effect of organic enrichment in sediments is to move the
system to one dominated by bacteria, ciliates and meiofauna, and where
the trophic links to the next level of the food web are broken. In bays
heavily occupied by salmon farms, Pohle et al. (2001) analyzed the macrofaunal
community at reference stations and found significant structural change.
While the cause could not be identified, the most probable explanation
is that an aspect of enrichment linked to salmon farming caused changes
in benthic-pelagic coupling in such a way as to exclude some species and
encourage others. Although the severely hypoxic areas caused by fish farming
in the Bay of Fundy are relatively small, no studies have examined benthic-pelagic
coupling in the vicinity of fish farms.
TOWARDS PREDICTIVE MODELS
Prediction of benthic organic enrichment from fish farms requires the
application of mathematical models. Process-oriented models use mathematical
frameworks that describe the major physical and biogeochemical components
and the processes through which they interact. Ocean circulation models
predict the transport and mixing in the coastal zone, including the dispersion
of organic matter from fish farms. Comprehensive ocean models, such as
the Princeton Ocean Model (Blumberg and Mellor 1987) and the CANDIE ocean
model (Sheng et al. 1998), have been successfully applied to coastal waters.
Sediment transport models predict the time evolution of the spatial distribution
of suspended particulate matter, as well as the exchanges of material
between the water column and the benthos. Diagenetic models couple water
column processes to vertically resolved sediment biogeochemical models
(Wijsman et al. 2000).
Empirical models use statistical descriptions of the relationships between
observable quantities that are indicators for key environmental components
or processes. Findlay and Watling (1997) proposed an oxygen-based framework,
based on the balance between benthic oxygen supply to oxygen demand, for
assessing the benthic response to organic enrichment from salmon aquaculture.
Dudley et al. (2000) developed a more process-oriented approach using
a transport model to estimate dispersion of wastes from a fish farm to
the benthos. DEPOMOD uses a hybrid approach to model benthic enrichment
effects, and includes a particle tracking model and empirical relationships
between the spatial distribution of solids and changes in benthic community
structure (Cromey et al. 2002). In British Columbia, Carswell and Chandler
(2001) and Stucchi (in prep.) have developed particle tracking models
that give estimates of size of the sediment field under and near fish
farms, but these models are not yet linked with benthic biological data.
TOWARDS METHODS OF MONITORING ORGANIC ENRICHMENT
Several variables to assess organic enrichment in seawater have been
identified, including phytoplankton species and abundance matrices, dissolved
oxygen concentrations, and total nutrient concentrations. Because none
of these variables is accepted as the single indicator of the trophic
status of seawater, multiparameter classifications have been used. For
example, the OECD classification is based on chlorophyll a, plant nutrients
and Secchi depths (Vollenweider and Kerekes 1982).
There are several methods to assess organic impacts in sediments. Those
methods based on classical macrofaunal sampling and analysis are among
the best known, although most costly. Alternative methods, such as sediment
profile imaging or geochemistry, are more cost-effective. Recently developed
methods, such as aerial photography, video photography and multibeam acoustics,
have the potential to produce detailed and accurate maps over large areas.
However, these methods require further research and groundtruthing. For
benthic monitoring, the presence of predominantly hard or soft substrates
will dictate the type of sampling. Other considerations include size of
the ecosystem and the primary goal of the study.
General types of monitoring to detect organic enrichment in the marine
environment are distinguished by their purpose. Geographical studies determining
the limit of impact benefit primarily from synoptic survey methods, such
as remote sensing of chlorophyll a in surface waters, underwater photography,
video photography and acoustic surveys of soft sediments. Studies involving
site comparison (treatment/reference sites), temporal trends (before/after)
and practical monitoring (relative impact) can use a few alternative methods.
Sediment profile images and sediment geochemical methods provide a much
more cost-effective and credible alternative to the use of macrofaunal
sampling and analyses for routine monitoring purposes.
RESEARCH NEEDS
Research is needed to provide an understanding of processes and to provide
input to models and monitoring programs. Research is also needed to aid
the scientific assessment of organic enrichment from marine finfish aquaculture
(or near-field enrichment of marine finfish aquaculture). The following
specific research needs are identified:
- Conduct sedimentology and physical and chemical oceanography studies,
including coastal circulation, mixing, dispersion and transport processes
in support of process models, and observation and modelling studies
of water column particle dynamics.
- Conduct seasonal studies of organic enrichment (such as redox potential
and sulfide) to examine ecological factors affecting organic enrichment
events from salmon farming.
- Measure the availability of carbon to microbial decomposers.
- Determine effects of organic enrichment on coarse and hard substrates
in British Columbia where fish farms are located over mosaics of sediment
types.
- Determine effects of organic enrichment on ecosystem functioning
to establish cause-effect relationships.
- Investigate how organic enrichment from aquaculture affects benthic-pelagic
coupling.
- Undertake further fallowing studies in Pacific and Atlantic Canada.
- Verify models, such as Lagrangian-based particle models, sediment
transport models and biogeochemical models, through collaborative efforts
between modellers and field biologists.
- Predict holding capacity or assimilative limits related to the amount
of local organic enrichment.
- Develop geographical survey methods, such as satellite, aerial surveillance,
underwater video photography and acoustics.
- Devise new environmental monitoring methods.
- Calibrate, standardize and audit existing environmental monitoring
methods.
REFERENCES
Andersen, T.J. 2001. Seasonal Variation in erodibility of two temperate,
microtidal mudflats. Estuar. Coast. Shelf Sci. 53: 1-12
Blumberg, A.F., and G.L. Mellor. 1987. A description of a three dimensional
coastal circulation model, p. 1-16. In N.S. Heaps [ed.]. Three
dimensional coastal ocean models, Coastal and Estuarine Studies (vol.
4). Am. Geophys. Union, Washington.
Brooks, K.M., A.R. Stierns, C.V.W. Mahnken, and D. Blackburn. 2003. Chemical
and biological remediation of the benthos near Atlantic salmon farms.
Aquaculture 219: 355-377.
Carswell, L.B., and P. Chandler. 2001. A modular aquaculture modelling
system (MAMS) and its application to the Broughton Archipelago, British
Columbia (BC) Coastal Engineering V Computer Modelling of Seas and Coastal
Regions Editor C.A. Brebbia, Wessex Institute of Technology, UK 2001.
Cranston, R. 1994. Dissolved ammonium and sulfate gradients in surficial
sediment pore water as a measure of organic carbon burial rate, p. 93-120.
In B.T. Hargrave [ed.]. Can. Tech. Rep. Fish. Aquat. Sci. 1949.
Cromey, C.J., T.D. Nickell, and K.D. Black. 2002. DEPOMOD - modelling
the deposition and biological effects of waste solids from marine cage
farms. Aquaculture 214: 211-239.
Dell’Anno, A., M.L. Mei, A. Pusceddu, and R. Danovaro. 2002. Assessing
the trophic state and eutrophication of coastal marine systems: a new
approach based on the biochemical composition of sediment organic matter.
Mar. Pollut. Bull. 44: 611-622.
Diaz, R.J., and R. Rosenberg. 1995. Marine benthic hypoxia: a review
of its ecological effects and the behavioural responses of the benthic
macrofauna. Oceanogr. Mar. Biol. Annu. Rev. 33: 245-303.
Dudley, R.W., V.G. Panchang, and C.R. Newell. 2000. Application of a
comprehensive modeling strategy for the management of net-pen aquaculture
waste transport. Aquaculture 187: 319-349.
Findlay, R.H., and L. Watling. 1997. Prediction of benthic impact for
salmon net-pens based on the balance of benthic oxygen supply and demand.
Mar. Ecol. Prog. Ser. 155: 147-157.
Gray, J.S., R.S-S. Wu, and Y.Y. Or. 2002. Effects of hypoxia and organic
enrichment on the coastal environment. Mar. Ecol. Prog. Ser. 238: 249-279.
Hargrave, B.T. 1994. A benthic enrichment index, p. 79-91. In
B.T. Hargrave [ed.]. Modelling benthic impacts of organic enrichment from
marine aquaculture. Can. Tech. Rep. Fish. Aquat. Sci. 1949.
Holmer, M., and E. Kristensen. 1992. Impact of marine fish cage farming
on metabolism and sulfate reduction of underlying sediments. Mar. Ecol.
Prog. Ser. 80: 191-201.
Kaspar, H.F., G.M. Hall, and A.J. Holland. 1988. Effects of sea cage
salmon farming on sediment nitrification and dissimilatory nitrate reductions.
Aquaculture 70: 333-344.
Levings, C.D., J.M. Helfield, D.J. Stucchi, and T.F. Sutherland. 2002.
A perspective on theuse of performance based standards to assist in fish
habitat management on the seafloor near salmon net pen operations in British
Columbia. DFO Can. Sci. Advis. Secretar. Res. Doc. 2002/075.59 p.
http://www.dfo-mpo.gc.ca/csas/Csas/English/Research_Years/2002/2002_075e.htm
Lumb, C.M., and S.L. Fowler. 1989. Assessing the benthic impact of fish
farming, p. 75-78. In J. McManus and M. Elliott [eds.] Developments
in estuarine and coastal study techniques. Olsen and Olsen, Fredensborg,
Denmark.
Nilsson, H.C., and R. Rosenberg. 1997. Benthic habitat quality assessment
of an oxygen stressed fjord by surface and sediment profile images. J.
Mar. Sys. 11: 249-264.
Pearson, T.H., and R. Rosenberg. 1978. Macrobenthic succession in relation
to organic enrichment and pollution of the marine environment. Oceanogr.
Mar. Biol. Ann. Rev. 16:. 229-311.
Pohle, G., B. Frost, and R. Findlay. 2001. Assessment of regional benthic
impact of salmon mariculture within the Letang Inlet, Bay of Fundy. ICES
J. Mar. Sci. 58: 417-426.
Poole, N.J., D.J. Wildish, and D.D. Kristmanson. 1978. The effects of
the pulp and paper industry on the aquatic environment. CRC Crit. Rev.
Environ. Control 8: 153-195.
Rhoads, D.C., and J.D. Germano.1986. Interpreting long-term changes in
benthic community structure: a new protocol. Hydrobiologia 142: 291-308.
Sheng, J., D.G. Wright, R.J. Greatbatch, and D.E. Dietrich. 1998. CANDIE:
A new version of the DieCAST ocean circulation model. J. Atmosphere. Ocean.
Technol. 15: 1414-1432.
Stucchi, D., Sutherland, T.A. and C.D. Levings. In prep. Near-Field Depositional
Model for Finfish Aquaculture Waste. In B.T. Hargrave [ed.]. Handbook
of environmental chemistry, Springer-Verlag, Berlin.
Vollenweider, R.A., and J.J. Kerekes. 1982. Eutrophication of Waters.
Monitoring, Assessment and Control. OECD, Paris. 164 p.
Wijsman, J.W.M., P.M.J. Herman, J.J. Middleburg, and K. Soetaert. 2002.
A model for early diagenetic processes in the sediments of the continental
shelf of the Black Sea. Estuar. Coast. Shelf Sci. 54: 403-421.
Wildish, D.J., H.M. Akagi, and N. Hamilton. 2001. Sedimentary changes
at a Bay of Fundy salmon farm associated with site fallowing. Bull. Aquacult.
Assoc. Can. 101-1: 49-56.
Wildish, D.J., B.T. Hargrave, and G. Pohle. 2001. Cost effective monitoring
of organic enrichment resulting from salmon mariculture. ICES J. Mar.
Sci. 58: 469-476.
Wildish, D.J., V. Zitko, H.M. Akagi, and A.J. Wilson. 1990. Sedimentary
anoxia caused by salmonid mariculture wastes in the Bay of Fundy and its
effects on dissolved oxygen in seawater, p. 11-18. In R.L. Saunders
[ed.]. Proceedings of Canada-Norway finfish aquaculture workshop, Sept.
11-14, 1989. Can. Tech. Rep. Fish. Aquat. Sci. 1761.
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