aquaculture in japan
TRANSCRIPT
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Environmental quality criteria for fish farms in Japan
Hisashi Yokoyama*
National Research Institute of Aquaculture, Fishery Research Agency, Mie 516-0193, Japan
Abstract
Environmental deterioration around fish farms has been widespread in Japanese coastal areas.
In order to prevent self-induced deterioration of the surrounding environment, the Law to
Ensure Sustainable Aquaculture Production was enacted in 1999. Criteria based on three
indicators, i.e., (1) dissolved oxygen content of water in fish cages, (2) acid volatile sulfide
content (AVS-S) in the sediment and (3) the occurrence of macrofauna under the fish cages were
determined to promote the Aquaculture Ground Improvement Program by applying this Law.
The second criterion (AVS-S) is based on the assimilative capacity of the sediments to organic
wastes from a fish farm. For applying this criterion to each farm, the maximum phase in the
process of biological remineralization must be detected for a farm site when the benthic oxygen
uptake (BOU) rates shows maximum. The peak of BOU, however, could not be determined
during a survey in Gokasho Bay, suggesting a need for reexamination regarding the practical
application of this criterion. In order to obtain data for refining the third criterion (macrofauna), a
quantitative survey was conducted at 22 fish farms (red sea bream and yellowtail) along the
Kumano-nada coast, central Japan. The biomass of the macrobenthos peaked in sediments
containing 1.2 mg/g of total nitrogen, where the majority of aerobic mineralization of the loaded
organic matter is supposed to occur. In summer, animals were scarcely found in sediments with
AVS-S>1.7 mg/g, suggesting that this is a critical condition for the fish farm environment. An
index embayment degree (ED), which represents the topographic conditions of a farm site, is
proposed to discriminate artificial factors arising from fish farming activities from the naturalfactors related to the topography. Community parameters of the macrobenthos and environmental
factors were significantly correlated with ED (P< 0.001). In shallow, semi-enclosed sites (larger
ED values), environmental deterioration and decreases in the benthic biomass were more
conspicuous in large-scale farms than in small-scale farms. Six assemblages of the macrobenthos
were identified by cluster analysis and were classified into three groups, indicating conditions as
healthy, cautionary and critical, respectively. As fish production increased, habitat of the
assemblage in the cautionary zone shifted to the offshore, deeper areas (smaller ED values),
indicating that both of aquacultural activities and topographic conditions affect the species
0044-8486/$ - see front matterD 2003 Elsevier B.V. All rights reserved.
doi:10.1016/S0044-8486(03)00466-6
* Tel.: +81-599-66-1830; fax: +81-599-66-1830.
E-mail address: [email protected] (H. Yokoyama).
www.elsevier.com/locate/aqua-online
Aquaculture 226 (2003) 4556
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composition. Macrofauna, sediment parameters and the index ED are concluded as useful to
develop pragmatic guidelines for site selection of fish farms.
D 2003 Elsevier B.V. All rights reserved.
Keywords: Criteria; Fish farm; Assimilative capacity; Macrobenthos; Sulfide; Law
1. Introduction
Aquaculture of fish has become a well-established industry in Japan during the last four
decades. The present output from fish farming is 26,400 metric tons with an economic
value of 274 billion yen (approximately US$23 billion). This accounts for 9% by weight
and for 23% by value of the total coastal fisheries (including aquaculture) production
(Ministry of Agriculture, Forestry and Fisheries, 2001). Intensive culturing, however,
generates large amounts of organic wastes, which are released to the immediate
environment around the fish farm, which often results in adverse environmental changes
such as deoxygenation (Hirata et al., 1994), outgassing of hydrogen sulfide (Tsutsumi,
1995) and blooms of harmful plankton (Nishimura, 1982), leading to negative conse-
quences for both farm management and the environment. Therefore, we need to clarify the
criteria and critical thresholds for fish farm environments that allow sustainable aquacul-
ture. For this purpose, many investigations have been conducted in coastal areas of Japan
(reviewed by Yokoyama, 2000).
In 1999, the Law to Ensure Sustainable Aquaculture Production was established topromote the improvement of aquaculture grounds by the fishermens cooperative associ-
ations, which supervise farmers in each local farm, and to prevent spread of contagious
disease of cultured organisms. To promote improvements of the environmental quality in
the vicinity of aquaculture activities, the Law established environmental criteria and
indicators. These criteria and indicators should now be revised to more appropriate criteria
on the basis of more recent scientific data. In order to examine the applicability of the
environmental criteria of sediments to fish farms, and to specify new criteria for
assessment of the environment around fish farms, surveys of the bottom environments
and the macrobenthos were conducted in fish farms in Kumano-nada, central Japan
(Yokoyama and Sakami, 2002; Yokoyama et al., 2002a,b).In this review, the environmental criteria that were established by the Law to Ensure
Sustainable Aquaculture Production (1999) are described, and problems are discussed
from the viewpoint of their practical use in fish farms. Thereafter, possible new criteria
based on the macrobenthos are proposed and discussed.
2. Environmental criteria used in the Law to Ensure Sustainable Aquaculture
Production
The Law to Ensure Sustainable Aquaculture Production (1999) (hereinafter re-ferred to as the Law) consists of two major parts: the Aquaculture Ground Improve-
ment Program, and measures to prevent the spread of Specific Diseases (contagious
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disease stipulated under the Decree of the Ministry of Aquaculture, Forestry and Fish-
eries). As a fundamental guide for putting the Law into practice, the Minister of
Agriculture, Forestry and Fisheries produced the Basic Guidelines to Ensure Sustainable
Aquaculture Production, which detailed the matters relevant to the goal of aquaculturalimprovement. The Law stipulates that fisheries cooperative associations should enact the
Aquaculture Ground Improvement Program so that they can ensure sustainable
aquaculture and get approval from the prefectural governor. This system is legally based
on voluntary activities of the licensed cooperative associations. The Law also stipulates
the mechanism to make the system effective in practice, i.e., a recommendation made by
the prefectural governor. If a cooperative association does not utilize its aquaculture
grounds in line with the Basic Guidelines, and the environmental conditions of its
aquaculture grounds deteriorate, the prefectural governor may recommend that the
cooperative association take measures necessary for improving aquaculture included in
the development of the Aquaculture Ground Improvement Program. If the cooperative
association does not follow the recommendation, the prefectural governor may make the
environmental status public.
To indicate a practical goal for aquacultural improvement, the Minister of Agriculture,
Forestry and Fisheries established environmental criteria under the provision of the Basic
Guidelines by using three indicators: dissolved oxygen (DO) of the water within fish
cages, sulfide content (acid volatile sulfide, AVS-S) of the sediment and macrofauna
beneath the fish cages (Table 1). The farm environments are identified as healthy when
the values of these indicators are within the thresholds. At the same time, the director
general of the Japan Fisheries Agency established criteria for identifying criticalenvironments by using the same indicators, which signal that urgent countermeasures
are necessary.
It is well documented that DO in the water column is one of most important factor for
maintaining life of cultured organisms. Harada (1978) described that yellowtail (Seriola
quinqueradiata) requires more than 4 ml/l (5.7 mg/l) of DO for normal growth. This value
was adopted in the criterion for the healthy environment used in the Law (Table 1). The
Law also established 2.5 ml/l (3.6 mg/l) of DO as a minimum limit for fish farm
environments. This value is an intermediate value between 2.0 and 3.0 ml/l; the former is
the value at the extreme margin of survival for cultured fish (Harada, 1978), while the
latter is the value when feeding activity of fish begins to decrease (Harada, 1978). Thesecriteria are generally accepted by fish farmers except those in localities where the DO of
Table 1
Environmental criteria adopted in the Law to Ensure Sustainable Aquaculture Production
Item Indicator Criteria for identifying healthy farms Criteria for identifying
critical farms
Water in cages Dissolved oxygen >4.0 ml/l < 2.5 ml/l
Bottom environment Sulfide (AVS-S) Less than the value at the point
where the benthic oxygen uptake
rate is maximum
>2.5 mg/g dry sediment
Benthos Occurrence of macrobenthos
throughout the year
Azoic conditions
for >6 months
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the surrounding water decreases frequently to a level lower than the standard values
mainly due to sewage and other industrial wastes.
Omori et al. (1994) presented a model to determine the limit of organic loading to the
bottom using the rate of benthic oxygen uptake (BOU), which was defined as the in situoxygen consumption by sediments, as an indicator of the activity of the benthic
ecosystem (Fig. 1). They found a peak of BOU along a gradient of organic loading,
and took this peak as an indicator of the maximum phase in the process of remineraliza-
tion. Based on this model, Takeoka and Omori (1996) presented a method to determine
the assimilative capacity of fish farms by using the acid volatile sulfide content (AVS-S)
in the sediment, because there is usually a positive correlation between the organic
loading and AVS-S. Their concept, named the Omori-Takeoka theory, was adopted as
a criterion in the Law. It states that AVS-S should be less than the maximum value of
BOU at each fish farm.
Macrofauna are sensitive to changes in organic inputs (Pearson and Rosenberg, 1978)
and have been often used as a sensitive indicator in environmental monitoring of fish
farms in Japan (Tsutsumi, 1995; Sasaki et al., 2002; Yokoyama, 2002) and in other
countries (e.g., Gowen et al., 1991). These studies show that a reduction in species
richness and/or species diversity, appearance of dense populations of the opportunistic
polychaete Capitella sp., which often results in the increase in total macrofaunal
abundance, decrease of large-sized species and disappearance of echinoderms are typical
effects of fish farming on the benthic community. The criteria used in the Law, however,
only specify that the benthos should be alive (Table 1), because the species composition of
macrofauna is difficult for most fish farmers to analyze. A healthy environment isidentified in terms of the existence of live macrofauna throughout the year, while a
critical environment is identified from the azoic conditions during half a year or more.
Criteria such as these have no biological basis, but they were determined to be convenient
in terms of the ease of monitoring by farmers. For the future, it is important to establish
more detailed criteria by analysis of the relationship between the macrobenthic commu-
nities and environmental conditions in the vicinity of the mariculture farms.
Fig. 1. Schematic model for determining the limit of organic loading from fish farming (adapted from Takeoka
and Omori, 1996).
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3. Examination of the Omori-Takeoka theory in Gokasho Bay
Yokoyama and Sakami (2002) collected sedimentwater interface samples from five
stations ( < 10, 50, 100, 200 and 500 m away from a fish cage) in Gokasho Bay, central
Fig. 2. Environmental parameters in a fish farm in Gokasho Bay, Japan. (A) Nitrogen content in sinking particles
collected from the water column of 0 to approximately 15 m depth; (B) nitrogen content in the sedimen t; (C) acid
volatile sulfides in the sediment; and (D) dissolved oxygen of the near-sediment-surface water (after Yokoyama
and Sakami, 2002).
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Japan, with a corer set inside an Ekman Grab (Yokoyama and Ueda, 1997), to clarify
whether the criteria based on the Omori-Takeoka theory are applicable to fish farms in
this bay. Yokoyama and Sakami (2002) found that nitrogen in sinking particles
collected by sediment traps, nitrogen in the sediment and sulfides in the sediment
decreased with increasing distance from the cage, and that there was no clear gradient
of the DO concentration of the bottom water (Fig. 2). A peak of biological BOU
(oxygen consumption in the process of aerobic respiration by microbes and benthic
animals), however, was not found in the observed gradient of organic matter loadingand reduced conditions (Fig. 3). Therefore, the criteria based on the Omori-Takeoka
theory cannot be applied to the fish farms in Gokasho Bay. This finding may be
explained by the possible variation of biological BOU in its immediate response to the
change of DO in the bottom water, as suggested by the small value of biological BOU
at Stn. 4 (0.15 g O2/m2/day), where DO was smaller than that in other stations (Fig.
2D). In addition to this, it may be difficult to detect a peak of biological BOU from
field surveys, because (1) it is difficult to obtain complete data sets both on the
increasing and decreasing phases in biological BOU in the gradient of organic matter
loading within a fish farm, (2) the model was devised on the assumption that the
system is in a stationary state, whereas in a practical farm, the oxygen flux between thewater column and the sediment is usually variable over a short period even within a
day due to the irregular water flow (Abo, 2000), and (3) biological BOU depends
largely on the flow velocity and oxygen supply, which are variable within a short
distance in a farm (Abo and Yokoyama, 2003).
4. New criteria based on the macrobenthos
Yokoyama et al. (2002a,b) conducted a quantitative survey of the macrobenthos
from 1998 to 1999 in 22 fish farms distributed in ten small bays along the coast ofKumano-nada, central Japan, in order to assess the environmental impacts of fish-farm
wastes under a variety of topographic conditions and to suggest site selection guide-
Fig. 3. BOU. (A) BOU rates determined by monitoring the dissolved oxygen of the in situ overlying water during
October 26November 4, 1999 at stations 15, Gokasho Bay; and (B) relationship between BOU and acid
volatile sulfides in the sediment. The numbers inside or near the circles in (B) are the station number (after
Yokoyama and Sakami, 2002).
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lines for sustainable fish farms. In this area, fish farming has developed steadily since
the introduction of yellowtail culture in the early 1960s. Since the middle of the 1970s,
a total of 15,00020,000 metric tons of fish has been annually produced mainly of red
sea bream (Pagrus major) and yellowtail. In 1998, annual fish production in each farmranged from 61 to 1507 metric tons (Tokai Regional Agricultural Administration
Office, 1999).
Fig. 4A shows the relationship between the biomass of the macrobenthos and the
nitrogen content in the sediment. A curve obtained by plotting the upper end values (see
Fig. 4A) of the biomass had a peak at 1.2 mg/g of total nitrogen (TN). Peak values of
other parameters related to the sediment organic content, i.e., 9 mg/g of total organic
carbon (TOC), 2 mg/g of total phosphorus (TP) and 23 mg/g of chemical oxygen demand
(COD) were also obtained from similar analysis. In the area with lower sediment values,
aerobic mineralization of the loaded organic matter is presumed to occur, and the organic
enrichment could provide an enhanced food supply to benthic animals. On the other
hand, the decline of biomass in areas with sediment values higher than these may result
from reducing conditions with associated deoxygenation and the occurrence of sulfides.
In fact, significant negative correlations between parameters related to sediment organic
content and DO of the bottom water (P< 0.001, 0.763 < r< 0.686, n = 51) andsignificant positive correlations between those and acid volatile sulfide (AVS-S) in the
sediment (P< 0.001, 0.778 < r< 0.925, n = 51) indicate that large inputs of organic wastes
cause environmental degradation. AVS-S in excess of 1.7 mg/g is predicted as the
threshold value at which the azoic situation would be observed (Fig. 4B). These results
suggest that one of the criteria for identifying a healthy environment should bedetermined from an increasing phase of the benthic biomass against the organic matter
loading, and that another criterion for identifying critical environment should be
determined from azoic conditions.
Fig. 4. Relationships between the biomass of the macrobenthos and sediment parameters in fish farms along the
Kumano-nada coast, Japan. (A) Relationship between the biomass and the nitrogen content; and (B) relationship
between the biomass and the acid volatile sulfide content. Dashes indicate the value of nitrogen content when the
biomass of the macrobenthos reached a maximum, and the value of acid volatile sulfide content when near-azoic
conditions were found (adapted from Yokoyama et al., 2002a).
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Yokoyama et al. (2002a) devised an index, the embayment degree (ED), of the
topographic situation of a sampling site to discriminate between artificial factors arising
from aquaculture and natural factors related to the topography. ED is expressed by:
ED L=W20=Ds45=Dm;
where L is the shortest distance from the bay mouth to the sampling station, Wis the width
of the bay mouth, Ds is the water depth at the sampling station or, if present, the depth of
any sill which exists between the sampling station and the bay mouth, Dm is the maximum
depth at the bay mouth, 20 is the mean depth of all the sampling stations, and 45 is
the mean depth of the bay mouths in the study area. When the fish farm is located in an
inlet whose axis crosses the axis of the main bay at an angle of < 90j, ED is expressed by:
ED L1=W1 L2=W220=Ds45=Dm;where L1 is the shortest distance from the bay mouth to the inlet mouth, W1 is the bay
width, L2 is the shortest distance from the inlet mouth to the sampling station and W2 is the
width of the inlet mouth. A crucial aspect of this model is L relative to Wand Dm, which
influence the water exchange rate between the coastal sea and the farm site, and Ds, which
influences the dispersion and input of organic wastes to the seabed.
Yokoyama et al. (2002a) examined the impacts of fish farms on the macrobenthos
(biomass, abundance, number of species and the species diversity HV) and the water and
sediment qualities (DO of the bottom water, and total organic carbon, total nitrogen, total
phosphorus, COD and AVS-S in the sediment) under a variety of topographic conditions.They found that fish production showed no correlation with the community parameters
and environmental factors excluding DO of the bottom water (P< 0.05, r= 0.379,n =51), TN (P< 0.05, r= 0.287, n =51) and TP (P< 0.05, r= 0.409, n =51) in the
sediment, although there were significant correlations between ED and all of these
community parameters and environmental factors (P< 0.001, 0.566 < jrj < 0.827, n =51;see Fig. 5 for an example). Environmental deterioration does not occur in the deeper
offshore areas with ED values < 2, even though the high production (>1000 metric tons/
year) of fish is maintained. In fact, within the deeper offshore areas, DO was usually more
than 5 mg/l, and AVS-S was usually less than 0.6 mg/g, even for large-scale farms (fish
production >601 metric tons/year). Such an undisturbed condition and an enhanced foodsupply from the fish cages resulted in large biomasses, which were generally encountered
>10 g/m2. On the other hand, deterioration of the sediment quality, deoxygenation of the
bottom water and decreases in biomass were found in the inner and shallower parts of the
bay. This tendency was more conspicuous in large-scale farms than in small-scale farms,
resulting in significant differences between the two regression slopes (P< 0.05, see r1 and
r2 in Fig. 5). This finding suggests that variability of the macrobenthos and environmental
factors are attributed first to the topography and, secondly, to aquacultural activities and
that topography is the most important factor in the location of environmentally efficient
fish farms.
Yokoyama et al. (2002b) also examined the species composition of the macrobenthos asan indicator of fish farm environments. They found six assemblages (AF) in August
September 1998 at the same fish farms along the Kumano-nada coast by cluster analysis
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(Fig. 6). These assemblages were classified into three groups according to the gradients of
fish production and ED. The three groups consisted of a group with high density and high
diversity (AD), a group characterized by an impoverished fauna (E) and an azoic sitegroup (F), which indicate conditions as healthy, cautionary and critical, respectively. As
fish production increased, the habitat of the assemblage in the cautionary zone shifted to
the offshore, deeper areas (smaller ED values), suggesting the influence of aquacultural
activities on the macrobenthos.
By identifying the community types of the macrobenthos, environmental conditions
may be evaluated, and the assimilative capacity and suitable siting for fish farming can be
determined. For instance, in case a fish farm with 1400 metric tons of annual fish
production is located in the critical zone with an ED value of 6, this farm should be shifted
to the area with ED values of smaller than 4, or an annual production should be lowered to
be less than 600 metric tons, in order to alleviate the critical conditions (Fig. 6).Many mathematical models have been developed to predict benthic impacts and
responses to organic enrichment associated with fish farming (reviewed by Henderson
Fig. 5. Analyses of the benthic impact based on the embayment degree index ED in fish farms along the Kumano-
nada coast, Japan. (A) Nitrogen content in the sediment, (B) dissolved oxygen of the bottom water, (C) acid
volatile sulfide content in the sediment and (D) biomass of the macrobenthos. Plots are clustered into two
categories in terms of fish production in 1998. Solid lines: the regression line (correlation coefficient: r1) based on
data from large-scale farms (annual fish production, 6011507 t); broken lines: the regression line (correlation
coefficient: r2) based on data from small-scale farms (annual fish production, 61 545 t) (adapted from Yokoyama
et al., 2002a).
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et al., 2001). Most of them recognized that the current flow is a key factor in predicting the
dispersion and input of organic wastes to the seabed (e.g. Hevia et al., 1996; Findlay and
Watling, 1997). Increased flow velocity not only reduces loading rates of particulate
organic wastes to the seabed, but also increases the oxygen supply, resulting in facilitating
aerobic decomposition of organic matter. Lumb (1989) pointed out the importance of
avoiding sites with low water movement for reducing the risk of environmental
deterioration. Bathymetry has also been regarded as one of most important factors (Aure
and Stigebrandt, 1989; Hevia et al., 1996), because the water depth as well as flow
velocities control the dispersal and loading rate of wastes.
ED is an index based on the same concept as those adopted in the previous modelingstudies, which demonstrated that dispersive environments are less susceptible to environ-
mental degradation than semi-enclosed systems, but it is novel to quantify the concept
with an index easily applicable for use in decisions about the siting of fish farms. In this
index, the relative distance from the bay mouth to the farm site and water depth at the bay
mouth are adopted as factors to represent the water exchange rate between the coastal sea
water and the farm site. Other factors such as the inflow of freshwater into the bay, the
current outside the bay, and wind velocity and direction, which may vary in different
localities might also control flushing. In neighboring localities under similar oceano-
graphic conditions, however, benthic impacts from fish farming might depend largely on
the topographic conditions. Results obtained from these surveys demonstrated theimportance of topographic factors for assessing the impact of organic wastes and for
developing guidelines for siting fish farms.
Fig. 6. Distribution of six groups of macrofauna (A F) in gradients of ED and the aquaculture activity in terms of
the fish production. The habitat is divided into the critical area, the cautionary area and the healthy area by the
boundary lines x and y. Six groups are Chaetozone sp.-assemblage (A), Paradoneis sp.-assemblage (B),
Schistomeringos sp.-assemblage (C), Scoletoma longifolia-assemblage (D) and Prionospio pulchra-assemblage
(E), which are prefixed by the dominant, polychaete species, respectively, and an azoic station group (F) (after
Yokoyama et al., 2002b).
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Revision of environmental criteria and indicators for applying the Law effectively are
now under examination by the Japan Fisheries Agency. The present review will be useful
as material for discussion.
5. Conclusion
Environmental degradation around fish farms has been conspicuous in many Japanese
coastal areas. To ensure sustainable production, it is necessary to conduct aquaculture at a
suitable location within the assimilative capacity for each farm, and to monitor the
environment carefully by using appropriate indicators. From this point of view, the Law
to Ensure Sustainable Aquaculture Production was established in 1999. Based on the
Law, three criteria by using DO of the bottom water, AVS-S in the sediment and
macrofauna as indicators were determined. Analyses of these criteria, however, havesuggested that some of these criteria and indicators should be reexamined or revised to
more appropriate ones (Yokoyama, 2000; Yokoyama and Sakami, 2002). The author and
colleagues have attempted to develop guidelines for the suitable siting of fish farms by
proposing an index ED, which represents the topographic conditions of the sampling site
(Yokoyama et al., 2002a,b). This index proved helpful to assess the impact of aquacultural
wastes under a variety of topographic conditions. ED may be used as a simple and
effective indicator to evaluate the assimilative capacity and siting of fish farms. Macro-
fauna and sediment parameters proposed in the present study are of practical use as
possible criteria for assessing fish farm environments.
Acknowledgements
I am grateful to Dr. Cheng-Sheng Lee for the invitation to the AIP Workshop and to the
anonymous referees for giving valuable comments on the manuscript.
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