Aquaculture 226 (2003) 45 56 www.elsevier.

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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 natural factors 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

* Tel.: +81-599-66-1830; fax: +81-599-66-1830. E-mail address: hyoko@fra.affrc.go.jp (H. Yokoyama). 0044-8486/$ - see front matter D 2003 Elsevier B.V. All rights reserved. doi:10.1016/S0044-8486(03)00466-6

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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 consequences for both farm management and the environment. Therefore, we need to clarify the criteria and critical thresholds for fish farm environments that allow sustainable aquaculture. 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 to promote the improvement of aquaculture grounds by the fishermens cooperative associations, 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 referred to as the Law) consists of two major parts: the Aquaculture Ground Improvement 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 Fisheries). 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 aquacultural improvement. 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 critical environments 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). These criteria 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 Water in cages Bottom environment Indicator Dissolved oxygen Sulfide (AVS-S) Criteria for identifying healthy farms >4.0 ml/l Less than the value at the point where the benthic oxygen uptake rate is maximum Occurrence of macrobenthos throughout the year Criteria for identifying critical farms < 2.5 ml/l >2.5 mg/g dry sediment

Benthos

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 situ oxygen 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 remineralization. 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 is identified 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 communities 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 sediment water 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 sediment; (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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Fig. 3. BOU. (A) BOU rates determined by monitoring the dissolved oxygen of the in situ overlying water during October 26 November 4, 1999 at stations 1 5, 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).

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 loading and 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 the water 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 of Kumano-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-

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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 15,000 20,000 metric tons of fish has been annually produced mainly of red sea bream (Pagrus major) and yellowtail. In 1998, annual fish production in each farm ranged 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) and significant 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 be determined 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=W 20=Ds 45=Dm ; where L is the shortest distance from the bay mouth to the sampling station, W is 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 =W2 20=Ds 45=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 W and 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 food supply 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 as an indicator of fish farm environments. They found six assemblages (A F) in August September 1998 at the same fish farms along the Kumano-nada coast by cluster analysis

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Fig. 5. Analyses of the benthic impact based on the embayment degree index ED in fish farms along the Kumanonada 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, 601 1507 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).

(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 (A D), a group characterized by an impoverished fauna (E) and an azoic site group (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

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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).

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 modeling studies, which demonstrated that dispersive environments are less susceptible to environmental 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 oceanographic conditions, however, benthic impacts from fish farming might depend largely on the topographic conditions. Results obtained from these surveys demonstrated the importance of topographic factors for assessing the impact of organic wastes and for developing guidelines for siting fish farms.

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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, have suggested 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. Macrofauna 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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