aquaculture in japan

7/30/2019 aquaculture in japan

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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

H. Yokoyama / Aquaculture 226 (2003) 455646


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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

H. Yokoyama / Aquaculture 226 (2003) 4556 47


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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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