水研センター研報，第19号，1−7，平成19年
Bull. Fish. Res. Agen. No. 19, 1‑7, 2007

博士号論文
rd

The 33 UJNR Aquaculture Panel Symposium

Ecosystem and Carrying Capacity of Aquaculture Ground-for sustainable development of aquaculture and stock enhancementSeikai National Fisheries Research Institute, NAGASAKI 2-3 November 2004
Organizers
Satoru Toda（National Research Institute of Aquaculture: NRIA）,
Osamu Matsuda（Hiroshima University）,Shusaku Kadowaki（Kagishima
University）, Hisashi Yokoyama（NRIA）,Junya Higano（NRIA）,
Makoto Yamasaki（Seikai National Fisheries Research Institute）
Keynote of the symposium The role of the fisheries industry as a supplier of healthy foodfor human has become more important in recent years. Marine aquaculture and stock enhancement have been developed and can now compensate the reduced productivity of thewild catch.
Aquaculture creates impacts on the surrounding environment and ecosystem in various
ways. Intensive feeding fish-farming often results in adverse effects on both the fish farmitself and the ecosystem beneath and around the fish farm through changes such as oxygen
deficiency, generation of hydrogen sulfide, and blooms of harmful plankton.
On the other hand, non-feeding aquaculture and stock enhancement of seaweeds and shellfish potentially prevent eutrophication by removing nutrients and particulate organic matterfrom the surrounding water. The integration of fish farming with non-feeding aquacultureis therefore a useful approach to mitigation of the environmental problems associated withmarine aquaculture.
To achieve sustainable development of aquaculture, we need to deepen our understanding of the environmental problems associated with aquaculture activities, especially their effect on the ecosystem and carrying capacity of aquaculture ground. In this symposium wewould like to discuss future perspectives of sustainable and responsible aquaculture, particularly in regard to the natural environment and ecosystem, methods of managing aquaculture
grounds, and new approaches to integrated aquaculture management.

Ariake Bay − present conditions of fisheries andresearch for its restoration −Tokimasa KOBAYASHIThis theme is one of the symbol of a microcosm＊

in Japan.

that includes many complicated issues related to

In Ariake Bay, the event occurred in 2000-2001

social and scientific problems in the coastal fisherythat the Porphyra（Nori）culture suffered from2006年 月26日受理（Received. June 26, 2006）* Seikai National Fisheries Research Institute, Fisheries Reseach Agency, Taira-machi, Nagasaki, 851-2213, Japan

Tokimasa KOBAYASHI
huge damage of discoloration by the environmental

the Bay. Western part of the Bay is muddy sedimentchange for worse.

and eastern part is mainly sandy sediment due toMany factors are included, such as oceanic

the current direction counterclockwise.

condition, decreasing of current speed, rise of water

Looking at from historical aspect, as the bay istemperature, reduction of concentration of nutrients,

shallow and flat tides are distributed widely, theweakened wind blows, much rain by typhoon andreclamation had already begun in Shogun period

after that sunshine lasted for a long time, andto ensure the increase of food and protect theirartificial matters, reclamation, dam, pollution etc.

houses and farm from disaster. And after the world

So briefly I introduce the research to restore thewar two it was getting rapidly to solve the scarcity

environment and fisheries production being done inof food with the advance of technology. Until now

the bay.

about 26 600 ha, about 57% of the flat tide, had been
reclaimed.

What is Ariake Bay？

One more feature of the bay is the large tidal
range. Fast tidal currents and strong vertical

Ariake Bay is located in northwestern Kyushu

mixing have been observed in the bay due to theIsland and a nutrient enriched productive sea. Its

large tidal range（the maximum is about 6m）andarea is about 1700 square kilometers. The bay isshallow water depth（mean depth is 20m）. Such asemi-enclosed, being connected to the East China

mixing process promotes oxidative decomposition

Sea through the narrow Hayasaki-Seto Strait. Theof organic matter in the bottom layer and brings

bay environment is strongly influenced by thethe regeneration of nutrients up to the surface

environmental conditions of the East China Sea（Fig.

from the bottom. This nutrient cycling provides a1）.

high productivity and has prevented bottom-water

The main features of the bay are tidal flats, ahypoxia in the inner part of the bay.

large tidal range and enriched with nutrients. The
tidal flats cover about 20 000ha along the coast of

Fig. 1. Ariake Bay and adjacent area in north western Kyushu Island

Ariake Bay − Present conditions of fisheries and research for its restoration

Fig. 2. Fluctuation of temperature（SST）,salinity（PSU）and DO（mg/l）in Ariake Bay.
F：Fukuoka
S：Saga
K：KumamotoFig. 3. Fluctuation of plankton（ml/m3）,transparency and COD in Ariake Bay.
F：Fukuoka
S：Saga
K：Kumamoto

Tokimasa KOBAYASHILong term fluctuation of environmental indicessummer to late fall and the concentration ofdissolved oxygen falls drastically especially during

Water temperature is a well-used environmental

neap tides（Fig. 4）.

parameter for fisheries grounds, higher watertemperature than a normal year has been recorded

Fluctuation of fisheries

at the bottom of the bay in recent years（Fig. 2）.
The transparency has also been increasing.

1）Bivalves

The area of muddy sediment has extended to the

The catch of bivalves was large and the major

western part of the bay, where the sediment waspart of the fisheries in the bay. The amount of theformally sandy. Furthermore, COD is graduallycatch reached more than 80 000 tons in the 1970s.

increasing, implying the deterioration of the bay

Since then, however, the production of short-necked

environment（Fig. 3）.
The total number of the occurrence and the daysclam（）, jack-knife clam（）and pen shell（of appearance of excessive algal blooms are rising）has been diminishing. The catch fell toin recent years. Particularly

the level of 30 000 tons early in the 1990s, and it has

was appeared as a dominant species for a long timefurther fallen to less than 20 000 tons in recent years

from September in 2000 to January in 2001. The（Fig. 5）.

reduction of nutrients by the algal bloom affected toFollowing causative factors for decreasing yields

the discoloration of Nori is estimated as one of theof bivalves are considering;

most important factor so far.

1）Over fishing

The tidal range has become also smaller, resulting
from a decrease of the area of the tidal flats
especially during neap tides. Moreover, hypoxia
is formed in the inner part of the bay from early2）Environmental deteriorations
a. Reductions in dissolved oxygen contents inwater column
b. Blooms of toxic micro algae

Fig. 4. Distribution of dissolved oxygen（mg/L）of bottom layer（−0 2 〜 0 5m）
at neap tide at 07：00 on Aug. 22, 2003.

Ariake Bay − Present conditions of fisheries and research for its restoration

Fig. 5. Fluctuation of the catch of jack-knife cram in Ariake Bay

c. Unsuitable sediment conditions for larval
settlement

widespread in the winter of 2000-2001, damaging theporphyra production. The discoloration was thought3）Impact of predation

to be caused by a shortage of nutrients as a result ofa. Predator such as crabs and rays

the unusual environmental conditions such as a large4）Outbreak of diseases

amount of precipitation in the fall, longer daylighta. Protozoan and viral diseases

hours far exceeding normal years and repeatedParticularly, mass mortality due to hypoxia wasoccurrence of atypical algal blooms. The production

reported for jack-knife clam in the aquaculture

felt to 91 146 ton in that year. It showed the lowest

grounds. And the predation by the ray, which

value in the past 25 years（Fig. 6）.

inhabitants generally in southern waters, has also
reported to be causing serious damage to the bivalve
stocks.
One species of ray,3）Fish and Crustacea
Commercially important fishes such as flat fishes,, whichpuffer and crustaceans such as blue crab are caught

eats two to three hundred of jack-knife crab perin the bay. However, their share in the total catch is

day was caught to decrease the damage more thansmall and the amount of catch has never exceeded

eighty tons in 2003 in the bay.

20 000 tons. Annual fluctuation is relatively small
but a gradual declining tendency has also been

2）Norinoticeable in the 1990s（Fig. 7）.

The Nori production has been increasing since1960 s, and it reached 60 639 ton in 1970, 92 913

Present and future program

ton in 1980, 121 732 ton in 1990, and it reached the
maximum of 168 250 ton in 2001. The production of

1. Monitoring

cultured Nori in the bay occupies about 40% of the・Ocean environment （physical, chemical andtotal amount of Japan. And its economic value isestimated about 40 to 45 billion yen in recent years.
However, discoloration of cultured porphyra wasplankton data）
・Harmful algal bloom（resting spore）
・Eggs and larvae distribution

Tokimasa KOBAYASHI

Fig. 6. Nori production in Ariake Bay

Fig. 7. Catch of the wild fish in Ariake Bay・Hypoxia : mechanism of trigger technique ofbay, but the production is not stable. Therefore,

elimination

it is an important issue to restore the bivalve

The bivalve catch and Nori production are

resources and to maintain the steady production ofundoubtedly the main fisheries production in theNori. Additionally, it is requested to improve theAriake Bay − Present conditions of fisheries and research for its restoration
habitat environment, especially quality of water

2. Restorationand sediment. It is known that the improvement

・Release of seeds（fish, bivalve, shrimp, crab）

of sediment quality can be achieved by irrigation

・Breeding（algae）

and/or covering by sand. More investigation of the・Sediment quality（ irrigation, covering by sand）

effectiveness and long-term persistence of theseWe also have strong research programs on seeds

methods are necessary and also trying to develop

for release including fish and shellfish, breeding of

more effective techniques to restore the sedimenthigh-temperature, low-nutrient resistance Nori inenvironment is needed. And also investigatingorder to restore fisheries resources and to maintainformation mechanisms of hypoxia is proceeding insustainable fisheries in the bay. So it should beorder to find where hypoxic conditions will form,

continued to monitor the present status and to bewhen they will form, how large an area it will affect,

developed some techniques on the restoration. And

what will trigger hypoxia, and how to eliminate it.

it would be considered to synthesize the carrying

Other related research includes a development ofcapacity and production in the bay.

techniques to prevent harmful effects of excessive
algal blooms on cultured Nori as well as to predict

References

an outbreak of excessive algal blooms.
Sato M. and Takita T., 2000: Fauna and flora, andenvironment of Ariake Bay, in Lives in Ariake
Bay （Written in Japanese）,（ed. By Sato M.）,
Kaiyo-sha, Tokyo, PP.15-35.

水研センター研報，第19号，9−15，平成19年
Bull. Fish. Res. Agen. No. 19, 9‑15, 2007

博士号論文

Effects of resuspended sediments on the environmental changes
in the inner part of Ariake Bay, Japan
Katsuhisa TANAKA＊1

and Masashi KODAMA＊2

Abstract: Turbidity,
fluorescence of phytoplankton pigments and dissolved oxygen
concentration were monitored and their relationships to tidal variations investigated in the
inner part of Ariake Bay. Turbidity during spring tides showed large short-term variations
due to the tidal resuspension of bottom sediments. The phytoplankton biomass increased
from neap tides to before spring tides, because of the higher nutrient availability in the surface low salinity water caused by the stratification and the higher transparency due to the
low turbidity. While during the spring tides, the increase of phytoplankton biomass was restricted by the low light availability due to the turbid water caused by the resuspended sediments, strong mixing with offshore water and possibly flocculation of phytoplankton withthe resuspended sediments. During the neap tides in summer, large scale hypoxia was also
observed in the offshore area of tidal flats, where resuspended sediments accumulate on thesurface sediments. These observations indicate that the recent reduction of tidal currents is
one of the contributing factors to the decrease of resuspension of the bottom sediments andincrease in hypoxic areas within the bay.
Key words: Ariake Bay, resuspended sediments, phytoplankton, turbidity, tidal flats, hypoxia

However, red tides are frequently observed in
Introduction

recent years, especially in the winter season of2000 to 2001 when the extensive bloom of diatom

2

Ariake Bay（1 700km ）, located in the western

seriously damaged Nori（; Rhodophyta）

part of Kyushu Island, is a shallow semi-enclosed

farming production （Watanabe

estuary with maximum tidal range over 5 m in the

Ariake Bay, increase of transparency from 1980s is

inner part. The strong tidal current and large tidal

reported, which seems to be caused by the reduction

flats areas are produced by the large tidal range.

of bottom sediments resuspension（Tanaka

Bottom sediments are resuspended by the strong2004）. From 1980s, the gradual reduction of tidal

tidal current and high turbidity zone（up to 4 000

amplitude and mean sea level rising are also pointed

mg･L − 1）is formed around the tidal flats（Shirotaout（Takigawa and Tabuchi, 2002; Unoki, 2003）,

and Kondo, 1985）. Dynamics of resuspended

which was attributed to the topographic changes

sediments strongly influences on phytoplankton

due to the reclamation projects and the effects ofproductivity through light availability （Cloern,decrease of tidal amplitude in the outer sea. Those1987）. Besides, mutual flocculation of phytoplankton

may reduce the bottom sediments resuspension.

and resuspended sediments leads to the removal of

Moreover, hypoxia is formed in the bottom water

phytoplankton from the water columns（Avnimelechin the inner part of the bay from summer to fall., 1982）, by which large scale red tide was scarceand the concentration of dissolved oxygen fallsin Ariake Bay（Shirota and Kondo, 1985）.

., 2004）. In.,

drastically especially during neap tides（Tanaka and2006年 月26日受理（Received. June 26, 2006）＊1
Seikai National Fisheries Research Institute, Fisheries Research Agency, Taira-machi, Nagasaki, 851-2213, Japan＊2
National Research Institute of Fisheries Science, Fisheries Research Agency, Yokohama, Kanagawa, 236-8648, Japan

Katsuhisa TANAKA and Masashi KODAMA
suspended sediments concentration（SS: mg ･ L−1）.

Kodama, 2004）.
In this paper, the results of continuous monitoringof turbidity,

Continuous monitoring of turbidity,

chlorophyll fluorescence andchlorophyll fluorescence, salinity and temperature

dissolved oxygen in the inner part of Ariake Bay

at 1m depth were carried out from 20 Sept. 2002 toduring the Nori farming season of 2002 to 2003

10 April 2003 at T4 located in the middle of the Nori

（Tanaka., 2004）and summer 2003（Tanaka

farming ground in the Chikugo River Estuary（Fig.

and Kodama, 2004）were summarized and their1）. Continuous monitoring of turbidity and dissolved

relationships to tidal variations were discussed.

oxygen in bottom water（0 5m above the bottom）
in the inner part of Ariake Bay were made at 4Materials and Methods

stations（T1-T4）from 9 July to 3 Sept. 2003.
Turbidity,

chlorophyll fluorescence

Data were collected using the towers constructed

and dissolved oxygen concentration（DO）were

for observation of temperature and salinity for Nori

measured with Chlorophyll/Turbidity sensors

farming（Fig. 1: T1-T4）.

（ALEC COMPACT CL/W）and DO sensors（ALEC

Light penetration was measured with an under

COMPACT DO/W）. They were set 1m depth

water quantum sensor（ALEC MDS-MkV/L）at T4

using buoys or 0 5m above the bottom by attaching（Fig. 1）in the north-eastern part of inner Ariake

to the towers. Time series data were collected at

Bay（Chikugo River Estuary）on 25 Nov. 2003. At

10 min intervals. Salinity and temperature data

the station, measurements were taken every 10

were collected by using a telemetry system andmin. at 0, 0 5, 1 0, and 1 5m depths to obtain datatime series data of 1-hour intervals were obtained.

to calculate the attenuation coefficient （k）. At

Maintenance of instruments was carried out oncethe same time, turbidity was measured with aor twice a month to clean up attached organisms on

sensor（ALEC COMPACT CL/W）calibrated with

the instruments together with water sampling for

Fig. 1. Distribution of tidal flats areas and environmental monitoring towers for Nori
farming in the inner Ariake Bay（T1-T4）. Each station is located in the middle of theNori farming grounds and outer edges of tidal flats.

Resuspended sediments in the inner part of Ariake Bay
calibration.

which was commonly observed in the shallow

Water samples for calibration of instruments

well-mixed type estuary, such as the Chikugo

were filtered with Whattman GF/F filters andRiver Estuary（Shirota and Tanaka, 1981）. Fig. 3

concentration of suspended sediments （SS）

shows variations in the tidal level at Miike（A）,

a n d c h l o r o p h y l l p i g m e n t s （c h l o r o p h y l l＋daily mean salinity and water temperature（B）,

phaeo-pigments）were determined. Relationships

in situ chlorophyll fluorescence（C）, SS（D）, daily

between SS and turbidity（NTU）, and between

average compensation depth（E）, and chlorophyll

chlorophyll pigments and in situ fluorescencepigments at high water（F）at T4（1m）. The data

were both linearly related as follows. [SS＝2 16

of chlorophyll fluorescence and turbidity from 18

×NTU＋2 74, r＝0 99, n＝62], [Chl.

Oct. to 2 Dec. 2002 could not be obtained by the＋phaeo. ＝

2 99×（fluorescence）＋1.97, r＝0.92, n＝62]. These

instrument trouble.

relationship curves were used to convert turbidity

SS was higher during spring tides and lower

a n d f l u o r e s c e n c e d a t a t o S S （m g ･ L −1 ） a n dduring neap tides（Fig. 3（D））. During spring tides,

chlorophyll pigments（μg ･ L−1）
, respectively.

higher SS was observed at low water while lower SS
was observed at high water. These results indicate

Results and Discussion

high turbidity water formed by the resuspensionof bottom sediments in the upper reaches of theLight limitation by the resuspended sediments

estuary was tidally transported to the offshore

Fig. 2 shows linear regression of Light extinction

area of the tidal flats. In this manner, SS exhibitedcoefficient against SS measured at T4. We obtained

semi-diurnal variations during spring tides, howeverstrong correlation（k＝0 062×SS＋0 28 r＝0 98）,

it was not clear during neap tides. During springwhich imply that light attenuation is primarilytides, variations ofa function of suspended sediment concentration.

exhibited similar pattern to SS, due to the tidal

Using this equation, we calculated the compensation

resuspension of bottom sediments which contained

depth（depth of 1% surface irradiance）from SS,

large amounts of chlorophyll pigments（Tanaka

assuming the vertically uniform SS distribution,

chlorophyll fluorescence., 1982）. Over 100mg・L−1 of SS was commonly

Fig. 2. Linear regression of extinction coefficient（k）against SS
concentration, for measurements made at T4 on Nov. 25, 2003.

Katsuhisa TANAKA and Masashi KODAMA

Fig. 3. Variations in tidal level at Miike（A）, daily mean salinity and temperature（B）,
fluorescence（C）, SS（D）, daily average compensation depth（E）and chlorophyll pigments at high water（F）at T4（1m）.
SS, chlorophyll pigments and compensation depth were estimated from turbidity andfluorescence.

Resuspended sediments in the inner part of Ariake Bay
observed in the inner Ariake Bay during spring tidewhich is equivalent to compensation depth lower
than 0 7m. On the other hand, compensation depth
was higher during neap tides, and occasionallyreached to 6 m during the high season of Nori
farming（late October to March）.
As variations of in situ chlorophyll fluorescence
include the influence of chlorophyll pigments in
the resuspended sediments, especially at low water
during spring tides, it is difficult to identify variationof phytoplankton biomass itself from Fig. 3（C）.
Therefore, in order to minimize the influence ofchlorophyll pigments in the resuspended sediments,
chlorophyll pigments data only at high water
were plotted in Fig. 3（F）
. Phytoplankton biomass
increased from neap tides to before spring tides,

Fig. 4. Relationship between tidal range at Miikeand daily average SS at T4.
○ : during high season of the Nori farming,● : before and after the season of the Nori farming.

and decreased or stable during spring tides. During
neap tides, lower salinity was observed （Fig. 3

years is reported to approximately 4%（Takigawa（B））. These results indicate that the phytoplankton

and Tabuchi, 2002; Unoki, 2003）, which is equivalentbiomass increase from neap to before spring tides

to the SS decrease of 11% on average and 17% on

was caused by the higher nutrient availability inmaximum, using the equations of Fig. 4. Thesethe surface low salinity water by the stratification

observations indicate that the recent reduction

and higher light availability with low turbidity.

of tidal currents is one of the contributing factors

Significant increase of chlorophyll pigments（up toto the decrease of resuspension of the bottom

30μg･L−1）were observed in the middle of January

sediments. Therefore, the resuspended sediment isand March, when compensation depth reachedconsidered to have key roles linking currents andto 6m. Blooms of diatom species （

phytoplankton production through light availability.

,

spp.,

spp. in Jan.,in Mar., respectively）were

Hypoxia and resuspended sediments

recorded in those periods. While, during spring tides,

Fig. 5 shows variations in the tidal level at T3,

phytoplankton bloom may be suppressed by low

DO and SS at T1-T4 in the bottom water（0.5m

light availability with turbid water, strong mixing

above the bottom）during summer（9, July-3 Sept.,with offshore water and possibly mutual flocculation

2003）. The data of 6-10, Aug. and DO data at T4of phytoplankton together with resuspended（25, July-10, Aug.）could not be obtained by the

sediments（Avnimelech

instrument trouble or typhoon. At all stations, the., 1982）.

During high season of Nori farming（from middle

high SS concentrations in spring tides decreasedof December to March）, SS was lower compared

to below 10mg ･ L−1 during neap tide. As the SSwith other periods（from October to November andconcentrations decreased during the neap tides, DOfrom end of March）. Fig. 4 shows the relationshipalso decreased. At the north-western part of inner

between tidal range at Miike and daily average SS

Ariake Bay, T1 and T2, DO decreased drastically toat T4. Daily average SS increases exponentially withalmost 0mg ･ L−1 in late August. Mutual flocculation

the tidal range, however, increasing rate during highof phytoplankton and resuspended sediments

season of Nori farming was lower in comparison

leads to the removal of phytoplankton cells fromwith other periods. These results suggest that tidal

the water column and their accumulation at thecurrent was reduced and resuspension of sedimentsbottom（Avnimelech

was suppressed by the Nori farming gears.

of drastic decrease of DO and SS during the

The gradual reduction of tidal amplitude in recent., 1982）. The coincidence

neap tides indicates that the rapid decomposition

Katsuhisa TANAKA and Masashi KODAMA

Fig. 5. Variations in SS, DO（B-0 5m）at T1-T4 and tide level at T3 during summer 2003.

Resuspended sediments in the inner part of Ariake Bayof phytoplankton cells is taking place after theof tidal current and influence of coastal

sedimentation.

structures in Ariake Sea by numerical analysis.
, 49, 1061-1065. （inConclusion

Japanese）
Tanaka, K., Hamada, S. and Shirota, A., 1982: Studies

The phytoplankton biomass increase from neapon the suspended matter in the Ariake Bay-Ⅱ.

to before spring tides was caused by the higher

Distribution and behavior of phytoplankton andnutrient availability in the surface low salinity waterorganic detritus in the Chikugo River Estuary.

by the stratification and the higher transparency,（57）, 19-30.（inwith low turbidity. While, during the spring

Japanese）

tides, the increase of phytoplankton biomass was

Tanaka, K., Kodama, M., Kumagai, K. and Fujimoto,restricted by the low light availability with turbidH., 2004: Variations in in situ fluorescence ofwater by the resuspended sediments, strong mixing

phytoplankton pigments and turbidity duringwith offshore water and possibly mutual flocculation

winter in the Chikugo River Estuary, Ariakeof phytoplankton with resuspended sediments. In

Bay, Japan.

the Inner Part of Ariake Bay, tidal currents have173-183.（in Japanese）, 13（2）,

become slower resulted from gradual reduction

Tanaka, K., and Kodama, M., 2004: Effects ofof tidal range and mean sea level rising, which

Resuspended Sediments on the Environmental

weakened resuspension of bottom sediments andChanges in the Inner Part of Ariake Bay.
., 27（5）, 307-311.（inincreased transparency and light availability for
phytoplankton. Red tide phytoplankton cells andJapanese）

resuspended sediments accumulate on the bottom by

Shirota, A. and Kondo M., 1985: Chapter 21, Ariake

the mutual flocculation during neap tides. Therefore,

Bay Ⅲ, Chemistry, Coastal Oceanography

the drastic decrease of DO during the neap tidesof Japanese Islands, Coastal Oceanography

indicates the rapid decomposition of phytoplankton

research Committee, The Oceanographic Society

cells is taking place after the sedimentation. Theseof Japan, Tokai Univ. Press, pp. 846-862.（inobservations indicate that reduction of tidal currents

Japanese）

is one of the contributing factors to the changes

Shirota, A. and Tanaka, K., 1981: Studies on theof ecosystem in Ariake Bay, such as the frequentsuspended matter in the Ariake Bay-Ⅰ.

occurrence of red tide and hypoxia.

Transport of clay floc-suspension from the
Chikugo River to the Estuary.

References.,（56）,27-38.（in Japanese）
Unoki, S., 2003: Why did the tide and the tidal current

Avnimelech, Y., Troger, B. W. and Read, L. W., 1982:
Mutual flocculation of algae and clay: evidence
and implications.

, 216
（2）
, 63-65.

Cloern, J. E., 1987: Turbidity as a control on
phytoplankton biomass and productivity inestuaries.

., 7（11/12）, 1367-1381.

Takigawa, K. and Tabuchi, M., 2002: Characteristics

decrease in the Ariake Bay?
, 12（1）,85-96.（in Japanese）
Watanabe, Y., Kawamura, Y. and Handa T., 2004:（or）aquaculture and nutrient

condition in the Ariake Bay, Japan.
., 42（1）,47-54.（in Japanese）

水研センター研報，第19号，17−25，平成19年
Bull. Fish. Res. Agen. No. 19, 17‑25, 2007

博士号論文

Observation on behavior of the large suspension feeding bivalve
under natural conditions＊

Kengo SUZUKI , Setuo KIYOMOTO ＊ , and Yuichi KOSHIISHI ＊Abstract To evaluate an effect of environmental changes on the pen shell, we conducted research on the valve movement of the pen shell; an indicator of
their activity. We developed two types of data logger to measure the valve movement of the
pen shells under field conditions. One is a wire-communication type for regions close to theshore while the other is an underwater type for offshore regions. The measurements were
performed in a tidal flat and in a subtidal station in Ariake bay in 2004. The measurement in
tidal flat revealed a distinct emersion effect, where the pen shells were closing their valves
and remaining motionless during the emersion. This type of motionless period did not, however, occur when they were submerged. Measurement in the subtidal station revealed posttransplantation burrowing behavior and unusual single close-open actions during a storm.
Key words: Pen shell,

The pen shell, valve movement, data logger

is a large

concentration（Yamamoto. 1993）and the lethalsuspension feeding bivalve and one of the mostlevel of dissolved oxygen（Akimoto. 2004）

important species in shell fisheries in Ariake bay

were reported. However, the description of the pen

Japan. The pen shell is also an important species

shell activity under natural fishing ground conditionsin terms of its ability to construct benthic fauna.

has yet to be produced.

Their filtration and bio-deposition may affect the

The activity of bivalves has been also studiedcomposition of the benthic fauna and environmental

by measuring valve movement for mussels

conditions（Cummings.,（Ameyaw-Akumfi 1987, Fujii and Toda 1991）,

2001）. Therefore, the pen shell is important as a key

scallops（Fujii and Sugiyama 1991）, and short-neck

species in the benthic community in Ariake bay.

clams（Fujii 1977, Fujii 1979）. Most of these studies

However, the pen shell production in Ariake bay has

focused on the rhythmic activity of bivalves but

been decreasing since the 1960 s. In a recent survey,

Tyurin demonstrated that the valve movement ofmass mortality of the pen shells was observed in thescallop and mussel can be a possible bio-monitor

fishing grounds（Matsui, 2002, Kawahara and Ito,for unfavorable environments（Tyurin 1990）. He

2003）. Certain factors such as the development of areported that the frequency of valve movement was

hypoxic water mass（Matsui, 2002）, an increase ofincreased under low oxygen condition in Scallop.

the muddy bottom area（Ito, 2004）, and predation

We found the valve movement of the pen shell also

（Kawahara. 2004）have been blamed for its

increases under hypoxic condition by laboratory

decline. Despite intensive research, the mechanism

experiment（Suzuki, unpublished data）.Therefore, if

for the decrease in the pen shell resources remains

the valve movement of the pen shell is monitored., 1998; Norkko

unclear. In previous studies, the gill activity of, it is expected to contribute for understanding

the pen shell related to the dissolved oxygenthe mechanisms of the decrease of the pen shell. In

2006年 月26日受理（Received. June 26, 2006）＊
Seikai National Fisheries Research Institute, Fisheries Research Agency Taira 1551-8, Nagasaki, 851-2213, JAPAN
Correspondence, e-mail: skengo@fra.affrc.go.jp

Kengo SUZUKI, Setuo KIYOMOTO, and Yuichi KOSHIISHI
the present study, the valve movements of the pen

Takesaki. The expected tide level at Takesaki wasshells under natural conditions were measured andavailable from the URL of the Japan Coast Guard.

the resulting data revealed typical patterns which

The depth at the subtidal station, meanwhile, wasare discussed in relation to environmental conditions,ca. 11m in mean low water level.

as are the devices we developed.

The pen shells used were collected from mudflats off Yanagawa about two weeks before theMaterials and Methods

experiment. They were identified as, based on the shell squamation（Yokogawa

The experiment was carried out at the west

1996）. The shells were then kept in holding tankpart of Ariake bay in Kyushu, Japan. One station

without being fed. Eight shells（138-190mm in SL）

was situated in the mud flat near Konagai, and thewere used for the experiment. Shells were fitted

other in the subtidal area off Ohura（Fig. 1）. The

with a sensor on one side of the valve and a magnet

measurement period was from May 19 to June 30 infitted on the opposite side by a plastic clip or

the mud flats and from August 24 to September 8 incyanoacrylate instant glue. A hall element（THS130,

the subtidal station in 2004, respectively. Pen shells

Toshiba Semiconductor Co., Tokyo, Japan）and awere found to occur naturally in the vicinity of bothmagnet（Wilson

experimental sites. The station in the mud flats

for measuring the valve movement. The sensors

emerged when the tide level went below 60cm inwere molded by Epoxy resin and were connected toFig. 1. The map of the study sites.

., 2002）was used as sensors

Behavior of the pen shell under natural conditions

Fig. 2. The wire communication type data logger（A）and the under water type data logger（B）.

the amplifier by 1m flat cables. The amplifier circuit,of flash memory, with a recording period of about

meanwhile, was built based on a gauss meter circuit

two weeks for 8 channels at one second intervals.

（Shimada, 2003）. When the shell closed their valves,the distance between the hall element and theResults and Discussion

magnet shortened, causing the output voltage of thehall element to rise.

The measurements in the mud flats were carried

Two types of data loggers were developed toout from May 19 to June 30. Unfortunately, themeasure the valve movement of the pen shell. One

available data was recorded only for the first week

was of the wire communication type while the otherbecause of the transfer cable being damaged by

was an underwater type（Fig. 2（A）
,（B）
）
. The

drift wood. The valve movement records of two

wire communication type data logger was used forindividuals and the expected tide level at Takesaki

measuring in the mud flat while the underwater

are shown in Fig. 3. Two shells opened their valvestype was used in the subtidal station.

for most of the recorded period. They also had

The amplifier circuit was molded by Epoxy resin

frequent short term valve closures. The valve

to render it waterproof for the wire communication

movement pattern showed both single and multiple

type. The signal from the amplifier circuit wasclose-open actions. The former is characterized by atransmitted to a data storage device using a multiclose-open action occurring over an interval of morewire cable. The data storage device（LAB-MIC 2A,

than a few minutes and the latter is characterized

ROHRM RIKEN. Co. Ltd, Shizuoka, Japan）used forby a series of close-open actions repeated at intervals

the wire communication type data logger includedof less than 30 seconds. Our preliminary observation

32 megabits of flash memory, with a recording

in the aquarium showed that the single close-open

period of about 10 days for two channels at intervals

action occurred during the vomiting behavior

of 0.5 seconds.

to expel the sand from within the shell. ThisThe underwater model was assembled by Little

observation also showed that the multiple close-open

Leonard Co. Ltd., Tokyo, Japan. The amplifier circuit

action was apparent during burrowing behavior

and data storage device were built in a waterproof（Suzuki, unpublished data）. The valve movement

casing on the underwater type data logger. The

recorded in the mud flats demonstrated that the pen

casing was a cylindrical shape（10cm in diameter,

shells remained still, closing their valves during the

60cm in length）with 8 waterproof sockets used toemersion and they experienced burrowing behavior

connect the sensor cables. The data storage device

after they were submerged.

（UL81, Unipulse Co., Tokyo, Japan）used for the

The measurements at the subtidal station were

underwater type data logger included 512 megabits

carried out from August 24 to September 8, with

Kengo SUZUKI, Setuo KIYOMOTO, and Yuichi KOSHIISHI

Fig. 3. （A）One week recordings obtained for valve movement of two pen shells on the mud
flat.（B）Motionless period during the emersion and（C）multiple close-open action（burrowing）
followed the motionless period.

Behavior of the pen shell under natural conditions

Fig. 4. The recordings obtained for valve movement of eight pen shells at
subtidal station.

the records are shown in Fig. 4. Unfortunately there

shells. This method could also be used to monitor

were two typhoons during this period and fivethe state of the pen shells within natural fishingshells were lost. Valve movement was most frequent

grounds. To clarify the effects of environmental

just after the shells were transplanted and also

conditions such as oxygen deficient water onfrequently occurred following the encounter of thethe pen shells, the activity of the pen shells andtyphoon #16. By examining the details of the record,prevailing environmental conditions must be

we found that the shells experienced multiple

monitored at the same time. Further studies underclose-open actions just after being transplantedlaboratory condition are also required to understand（Figs. 5A, B）. So the pen shells are considered tothe meanings and causes of change in the patterns

have burrowed extensively after being transplantedof valve movement.

to fix themselves in position. On the contrary, mostof the valve movements during the encounter of the

Acknowledgment

typhoon #16 were single close-open actions（Figs.

This study was carried out with the help of Dr.

6A, B）. This type of valve movement is similar to

Akihiko Fujii of the Nagasaki Prefectural Institute ofthat of vomiting behavior, meaning these actions

Fisheries, Dr. Siro Ito of the Saga Ariake Prefectural

were thought to be a reaction of the pen shells to

Fisheries Research and Development Center. Shirohigh turbidity or since they were covered with sandTajitu and Toshihisa Kohda assisted us in the field.

from heavy waves.

We would also like to thank the members of the

In the present study, the valve movement records
assess the change in activity or behavior of the pen

Seikai National Fisheries Research Institute for theirhelpful assistance.

Kengo SUZUKI, Setuo KIYOMOTO, and Yuichi KOSHIISHI

Fig. 5. （A）The recordings obtained for multiple close-open actions appeared
just after pen shells were transplanted.（B）A 16-miutes portion of the record.
Close-open actions were repeated within a minute.

Behavior of the pen shell under natural conditions

Fig. 6. （A）The recordings obtained for single close-open actions appeared
during a storm.（B）A 16-miutes portion of the record. Close-open actions wererepeated at least one or more minutes interval.

Kengo SUZUKI, Setuo KIYOMOTO, and Yuichi KOSHIISHI
in Northeast Part Fishery ofReferences

Ariake Sound‑Ⅱ. Bull. Saga Prefect. Ariake
Fish. Res. Dev. Cent., 22, 17-23.（in Japanese

Ameyaw-Akumfi C. and Naylor E., 1987: Temporal
patterns of shell-gape in. Marine

Biology, 95, 237-242.

with English abstract）
Matsui S., 2002: Resources change of the Pen-shell（）in Northeast part

Akimoto T., Hayashi M., Iwabuchi M., andfishery of Ariake sea. Bull. Fukuoka Fisheries

Yamamoto K., 2004: Lethal Oxygen-saturation

Mar. Technol. Res. Cent., 12, 29-35.（in Japanese）

for the Pen Shell（）, 52(2), 199-200.（in Japanese withEnglish abstract）

Norkko A., Hewitt J. E., Thrush S. F., and Funnell
G. A., 2001: Benthic-pelagic coupling andsuspension-feeding bivalves: Linking site-specificCummings V.J., Thrush S.F., Hewitt J.E., andsediment flux and biodeposition to benthic

Turner S.J., 1998: The influence of the pinnid

community structure. Limnol. Oceanogr., 46(8),bivalve

2067-2072.

（Gray）on benthic

macroinvertebrate communities in soft-sediment
habitats. J. Mar. Biol. Ecol. 228, 227-240.

Shimada Y., 2003: HORU SOSHI WO TSUKATTAG A U S S M E T E R N O S E I S A K U （M a k i n g

Fujii T., 1977: Measurement of periodic openof Gauss meter by using a Hall element）.

and shut shell movement of bivalves by the

TRANSISTOR GIJYUTSU, 465, 107-112. （instrain-gauge method. Bulletin of the JapaneseJapanese）.

Society of Scientific Fisheries. 43(7), 901.

Tyurin A. N., 1991: Behavioral Reactions of the

Fujii T., 1979: The Study for Periodic Behavior of

Scallop, Mizuhopecten yessoensis, and theBivalves‑Ⅰ Periodic Observed in Short-Necked

Mussel, Crenomytilus grayanus, to Reduced

Clam

Salinity and oxygen and Exposure to Synthetic

DESHYES Put in Natural

Environment. Bull. Tohoku Reg. Fish. Res. Lab.,40, 37-46.（in Japanese）

Detergents. HYDROBIOL.J., 27(4), 13-19.
Wilson R. P., Steinfurth A., Ropert-Coudert Y.,

Fujii T and Sugiyama M., 1991: The Effect of Water

Kato A., and Kurita M., 2002: Lip-reading inpressure Change on the Scallop Appeared inremote subjects: an attempt to quantify andPeriodic Expansion-contraction Movement of its

separate ingestion, breathing and vocalization in

Adductor Muscle. Bull. Natl. Inst. Aquaculture,free-living animals using penguins as a model.

19, 27-30.（in Japanese with English abstract）
Fujii T. and Toda S., 1991: Open and Close

Marine Biology, 140, 17-27.
Yamamoto K., Tanaka M., Tanaka N., Kamizono M.,

Shell-Movement of the Mussel,and Akimoto T., 1993: Effect of Hypoxia andL. under Natural conditions. Bull. Natl. Inst.

Water Temperature on the Crawling Speed

Aquaculture, 20, 33-40. （in Japanese withof the Gill Piece of Three Bivalvia Specieses,

English abstract）s,

Ito S., 2004: The Status and Recovery of Marine

（

and
）

, 41

Resources in the Ariake Sound. Bull. Saga(4), 435-438.（in Japanese with English abstract）

Prefect. Ariake Fish. Res. Dev. Cent., 22, 69-80,

Yokogawa K., 1996: Genetic Divergence in Two（in Japanese）

Forms of Pen Shell

Kawahara I., Ito S., 2003: Mortality of Pen-Shells,, Jap. Jour.

Malac. 55(1), 25-39.

in Northeast Patr Fishery of
Ariake Sound in Summer, 2000 and 2001‑Ⅰ.

和文要旨

Occurrence of Mortality. Bull. Saga Prefect.

環境変化がタイラギの活動に与える影響を把握する

Ariake Fish. Res. Dev. Cent., 21, 7-13. （in

ため殻体運動を測定する装置を開発し，小長井地先のJapanese with English abstract）

干潟と大浦沖の潮下帯でタイラギの殻体運動を測定しKawahara I., Ito S., Chikushi Y., Aishima N., andた。干潟上のタイラギは，干出時に殻を閉じて静止しKitamura H., 2004: Mortality of Pen-Shells,ており，潮が満ちると殻体運動が増加した。潮下帯のBehavior of the pen shell under natural conditions
タイラギでは移植直後の潜砂行動に伴う連続した殻体運動が記録され，その後殻体運動の頻度は減少したが，台風の接近以降に潜砂行動とは異なる単独の殻体運動が増加した。

水研センター研報，第19号，27−32，平成19年
Bull. Fish. Res. Agen. No. 19, 27‑32, 2007

博士号論文

Appropriate release number of juvenile red spotted grouper,, into nursery reef and fishing port habitats
Shigenobu OKUMURA＊

Abstract Six nursery reefs of ca. 20m3 were installed off Shiraishi Island, central Seto Inland Sea, Japan in July 2000. Juvenile red spotted grouper were released into the reefs on
October 2001. The densities of released juveniles were arranged at three levels, 500, 1,000
and 2,000 fish per reef. Part of the reef was salvaged from each reef three times to estimate
the number of residual fish. The numbers of residual fish were directly proportional to
the numbers of released fish until one month after release; however they were nearly evenamong the three levels at four months after release. Retention rates were inversely proportional to the released number. Release experiments into a fishing port were carried out in
Ishima West Port located in central Seto Inland Sea, Japan. A total number of 15,000 and 1,500
juveniles were released into the port on October 1998 and November 1999, respectively.
Respective recapture operation took place 16 and 28 days after the release using 16 and 20
fishing traps in the port. CPUE were 0.38 and 0.05 directly proportional to the number of
released juveniles.
Key words: red spotted grouper, release experiment, stock enhancement, nursery reef, fishing port

Introduction

Release experiment into nursery reefs

The red spotted grouper is a temperate grouper

Materials and Methods

which is distributed from Southeast Asia to Far
East. It has a high market price and seems to be a

Prior to this experiment, materials and structure

prominent species for stock enhancement becauseof the nursery reef were designed in the laboratoryof its non-migratory habitat and relatively small（Okumura., 2002）and under natural conditions

stock size. Stocking efficiency was obvious when 1+（Okumura., 2003a）. Fig. 1. shows schematic

year old fish were released into natural conditions;diagram of the nursery reef. The nursery reefs

however 0+ year old fish release had little efficiency

consisted of a 3 6 m square concrete base, 4 ironin this species（Okumura., 2002）. It was a large

poles of 1 6 m tall, and a top panel. Top panel was

problem that how to care the released 0+ year fish

filled up with oyster shells（250 kg/m3）to enhanceand nurse them to 1+ year old. One of the solutions

the food organisms for released fish. Each nurseryof this problem is caring the juveniles by using

reef had 6 test units of 75 cm cube. Test unit was

artificial nursery reef or fishing port. In this paper,

consisted of iron frame and 25 mesh pipes, 15

three release experiments were introduced andcm in diameter and 75 cm long. Each pipe had adiscussed on the carrying capacity of the nurserystring of scallop shells in it. The mesh size of thereefs and fishing port.

pipe and space between the shells were planed tomatch with the released fish size. These test units

2006年 月26日受理（Received. June 26, 2006）＊
Yashima Station National Center for Stock Enhancement Fisheries Research Agency, Yashima-higashi Takamatsu, Kagawa 761-0111, Japan
Email: sokumura@fra.affrc.go.jp

Shigenobu OKUMURA

Fig. 1. Structure of the nursery reef.
A, top panel; B, test unit; C, side panel; D, concrete base; E, meshpipe filled with string of scallop shells. Values are in cm.

were detachable from the nursery reef in order toper reef, and each density level tested at 2 reefs.

estimate the number or conditions of the residual

Underwater observation took place five times, 7,

fish by salvage operation. Side panel was attached27, 56, 92, and 119 days after release to count theto prevent the fish escaped from the reef and/or

number of residual fish in the reefs. A test unit was

propagate the food organisms. Six nursery reefs

salvaged from each nursery reef three times, 7, 27,

were built and installed on the bottom（5-6 m inand 128 days after release, to estimate the number

water depth）off Shiraishi Island, central Seto Inlandof residual fish. Salvaged test units were took apart

Sea, Japan （Fig. 2., 3.）in July 2000. Artificiallyon the boat and each number of the recaptured fish

reared red spotted grouper juveniles（67 6 ± 7 0

was counted. After the operation, the test units were

mm in total length）were released into the reefs onrebuilt and returned to the original reef. Recaptured

16 October 2001. All fish were marked by clippingfish were also re-released into their own reef.

the left or right ventral fin. The fish were packed
in a basket and divers delivered the basket into

Results and Discussion

the reef and opened it in each reef. The densities
of released juveniles were arranged at three levels,

Each number of fish in the reefs observed

500 fish per reef, 1 000 fish per reef and 2 000

underwater is shown in Fig. 4. At first operation

Release experiments of red spotted grouper into reefs and port

Fig. 2. Location of the experimental area.

Fig. 3. Experimental area, nursery reefs arrangement, and release
number of juveniles into each reef.

the numbers of observed fish were parallel to theshows transition of the retention rates which werereleased density. From the second observation,

calculated from estimated number of residual fish

the observed numbers of fish in 2 000 fish per reef

divided by numbers of released fish. The retention

group decreased and were close to 1 000 fish per

rates were almost inversely proportional to thereef group. At 92 days after release, numbers of

released number through the experimental duration.

fish decreased to 4-10 per reef and were close to

These results indicate that releasing 2 000 fish pereach other. At the final observation the observed

reef is effective to retain a large number of released

numbers were almost even and partly reversed likefish in a reef for a month; and releasing 500 fish

8 fish in 500 fish per reef group versus 0 in 1 000

is efficient to obtain a high retention rate at four

fish group. Fig. 5. shows the results of three salvage

months after release. Thus the appropriate number

operation. The upper figure shows transition ofof released fish should be determined depending on

the estimated number of fish per reef, number ofthe duration spent in the nursery reef.

recaptured fish multiplied 6（number of test units ineach reef）. In this figure, tendency of the decrement
was the same as Fig. 4. The lower figure of Fig. 5.

Shigenobu OKUMURA

Fig. 4. Number of residual fish observed under water.

Fig. 5. Number of the residual fish and retention rateestimated from salvage operations.

Release experiments of red spotted grouper into reefs and port
release.
Release experiment into fishing port
Results and Discussion
Materials and Methods
Table 1. shows the results of these release
These experiments were carried out in Ishima

experiments. Total number of recaptured fish inWest Port（Fig. 6.）which is shallow（2-4 m）and

1998 was 6 and catch per unit effort（CPUE）wassmall（4500 m2）port located in central Seto Inlandcalculated as 0 38（6 fish per 16 traps）.Only one fishSea, Japan（Fig. 2.）. The port had many crevices on

was recaptured in 1999 and CPUE was 0 05（1/20）.

its wall and bottom, since it was mainly built of rock

Although these operations were experimental

arrangement. A total number of 15 000 artificiallyand the calculated figures were estimates, CPUE

reared juveniles（69 mm, mean total length）wereseemed to be directly proportional to the number of

released into the port on 13 October 1998. Recapture

released juveniles. The retention rate may be fixed

operation took place 16 days after the release using

unrelated to the number of released fish within the

16 fishing traps（60 × 45 × 20 cm）in the port. All

limits of 1 500-15 000 fish per port. Further releasetraps with bait fish were spaced evenly on theexperiment, less than 1 500 fish or more than 15 000

seabed in the port along a pier on noon 28 October.

fish into the port, will be useful to estimate the

The traps were salvaged 24 h after setting andcarrying capacity of the port.

organisms in it were caught. A total number of 1 500
Acknowledgements

juveniles（109 mm）were released into the same
port on 11 November 1999. Recapture operation was
similarly conducted using 20 traps 28 days after the

The nursery reef study was granted by Fishery

Fig. 6. Ishima West Port.

Shigenobu OKUMURA
Table 1. Results of the recapture operations in Ishima West Port

Agency Japan to develop the nursery reef for stock

under reared condition.
, 68, 186-191.

enhancement from 1999 to 2001. The nursery reef
study was collaborated with Okayama Prefecture

Okumura S., Tsumura S., and Maruyama K., 2003a:

Office Fisheries Division and Okayama Prefectural

Comparison with two types of artificial nursery

Fisheries Experimental Station. I thank members oftest reef by releasing experiment of juvenile

the nursery reef development committee for their

red spotted grouper

under

useful advice and suggestion. Thanks are also to thenatural conditions.

, 69,

staff of Tamano Station of former JASFA for their

57-64.

assistance.

Okumura S., Kayano Y., Kusaka K., Tsumura S.,
and Maruyama K., 2003b: Experimental release
Referencesof juvenile red spotted grouper
into the artificial reefs made of scallop

Okumura S., Tsumura S., and Maruyama K., 2002:
Evaluation of artificial nursery reef materials
for juvenile red spotted grouper

shells.
, 69, 917-925.

水研センター研報，第19号，33，平成19年
Bull. Fish. Res. Agen. No. 19, 33, 2007

An appropriate stocking size of juvenile Japanese flounder,, in consideration of carrying capacity
Yoh YAMASHITA＊1and Yutaka KURITA＊2

Japanese flounderis a major coastal commercial fish. The total
catch of the flounder is stable between 6 500 and 8 400 tonnes in the last decade. It is also
one of the major target species of stock enhancement in Japan. A total of 30 million juveniles
are released every year. Economic return rate（amount of catch / cost of stocking）can increase to 2.5 in the case appropriate releasing techniques are applied. Stocking size is one of
the most important techniques to be considered as well as the size at release and the timingof release. We applied an ecophysiology model to predict the growth of juvenile Japaneseflounder and to evaluate an appropriate stocking size under the criterion that released fish,
as a competitor of wild one for food, do not restrict the growth of wild fish. This model consists of 5 compartments（i. e. wild flounder, released flounder from hatchery as a competitor,
other competitors, mysids as a main food item, predators）and includes various physiologicalresponses to varying environments（mainly temperature）and ecological interactions（i. e.
prey-predator relationship and competition for food）among these compartments. The predicted growth of both wild and released flounders until 65 days after stocking（9 November）
well agreed with the observed ones at Ohno Bay, a small shallow sandy area up to 10m deepin the northwest of Japan. Wild flounder would reach to 141mm in TL on 9 November without any released flounder, while in fact they grew only to 109mm. The model explained thatthe standing biomass of mysids decreased because the amount of predation on mysids byboth wild and released fish exceeded the production which was controlled by temperature
and abundance of mysids themselves, and that led to the restricted growth of wild flounder.
An appropriate stocking level below which release of hatchery-raised flounder would not
retard the growth of wild one was predicted as 49 000 individuals while actual stoking level
was 76 300.

＊1

Fish. Res. Stn. Kyoto Univ., Maizuru, Kyoto 625-0086
Tohoku Nat. Fish. Res. Inst., Shiogama, Miyagi 985-0001
E-mail: kurita@affrc.go.jp＊2

水研センター研報，第19号，35−40，平成19年
Bull. Fish. Res. Agen. No. 19, 35‑40, 2007

博士号論文

Impacts of oyster cultures on nitrogen budgets in Hiroshima Bay,the Seto Inland Sea of Japan
Kenji TARUTANI＊Abstract The impact of oyster culture on the nitrogen budget was demonstrated for thenorthern Hiroshima Bay. The output from a simple two-layer box model and nitrogen measurements in the bay over a 1 year period were used to estimate the nitrogen budget in
the northern Hiroshima Bay（NH）. The annual dissolved inorganic nitrogen（DIN）budgets
indicated that all input terms to the northern Hiroshima Bay were equivalent to 22±7 8 ton
N d−1, whereas DIN export to the central part of the bay was equivalent to 14±13 ton N
d−1. These results suggest that a significant part of DIN input is consumed by phytoplankton and converted into the particulate form in the NH region. Estimated filtration rates ofcultured oysters（7 3 ton N d−1）suggested that oyster cultures play a significant role for removing the particulate N from the water column in Hiroshima Bay. In addition, the amountof nitrogen harvested as oyster products was about 0 66 ton N d−1, which is about 6% ofdaily terrestrial DIN input into the NH region. The removal rate through oyster harvestingis five times higher than that by fishing activities, suggesting that oyster culture plays a significant role on the recycling of nitrogen from Hiroshima Bay to the land.
Key words: environmental impacts, Hiroshima Bay, nitrogen budgets, oyster cultures

Bivalve aquaculture has some additional functionof the Seto Inland Sea of Japan, having a surface

other than food production, and can have a variety

area of ca. 1 000km2 and a mean depth of ca. 25mof effects on coastal and estuarine ecosystems. For（Fig. 1）. The annual oyster production in the bay is

example, bivalves filter suspended particle matter,

15,000-30,000 tons, which accounts for about 60-70%

both living and detrital, in the water column. It hasof oyster production in Japan. A method of hanging

been suggested that the grazing activity of bivalve

oysters under a floating raft with a size of 20×10m

populations controls phytoplankton dynamics on

has been used for oyster culture in the bay. A large

the scale of entire embayments（Cloern 1982）. Highnumber of floating rafts can lead us into a belief that

rates of organic biodeposition near aquaculture sites

oyster cultures have some impact on the ecosystemhave been shown to result in anaerobic benthicof Hiroshima Bay.

environments（e.g. Hatcher. 1994）, and change

the benthos community（e.g. Crawford

The objectives of this study were twofold.

. 2003）.

First, I wished to construct a nitrogen budget for

Harvesting activities can remove nutrients such

Hiroshima Bay, based on the field observations andas nitrogen and phosphorus from coastal anda simple box model analysis. My second objective

estuarine areas（e.g. Songsangjinda

2000）.

was to examine filtering activity of phytoplankton

As such, bivalve aquaculture can significantly alter

particulate nitrogen by cultured oysters and removal

material and energy flows in coastal and estuarine

efficiency of nitrogen from the bay by oyster

ecosystems.

harvesting. The results and discussions of this study

Hiroshima Bay is located in the western partwill be elaborated in detail elsewhere, and briefly

2006年 月26日受理（Received. June 26, 2006）＊
National Research Institute of Fisheries and Environment of Inland Sea, Fisheries Research Agency, Maruishi 2-17-5, Hatsukaichi, Hiroshima
739-0452, Japan

Kenji TARUTANI

Fig. 1. Study area and sampling stations in Hiroshima Bay. Box
dimensions for the model analysis are also given.

outlined here.

the following relationships can be described for thebudget of salinity in each box

Nitrogen budgets in the northern part ofHiroshima Bay
A simple box model was used to characterize
the residual circulation in the bay and then to

Qf＋Q21−Q13＝０

V1

dS1＝S2 Q21＋D12（S2−S1）−S1 Q13
dt

estimate the nitrogen budgets in the northern partof Hiroshima Bay. Hiroshima Bay was divided into

Q42−Q21＝０

two adjacent boxes, northern Hiroshima Bay（NH）
and central Hiroshima Bay（CH）, depending on
the hydrological characteristics（Fig. 1）. On theV2

dS2＝−S2 Q21＋D12（S1− S2）−S4 Q42
dt

basis of a two layered circulation pattern, eachbox was segmented into two layers separated by awhere Qf is the freshwater inflow, Qij is the transfer

zero-velocity level which was fixed at 5m depth（Fig.

coefficient from Box-i to Box-j, D12 is the vertical2）. Assuming that the volume of each box remains

mixing between Box-1 and Box-2, V1 and V2 are theconstant over time scales greater than 1 tidal cycle,

volume of Box-1 and Box-2, respectively, and Si areImpacts of oyster cultures on nitrogen budgets

Fig. 2. Schematic diagram for the box model used in this study. Qf , Qij andD12 represent the freshwater inflow, the transfer coefficient from Box-i to
Box-j and the vertical mixing between Box-1 and Box-2, respectively.

the averaged salinity in Box-i. Q f was calculated

to the NH region（Fig. 3A）. DIN export to the CH

as the sum of the discharge from the Ohta Riverregion was 3 7 ± 1 3 ton N d−1, significantly lower

and sewage treatment plants, precipitation andthan a sum of DIN input from the river, sewage

evaporation. Dissolved inorganic nitrogen（DIN）

and the CH regions（5 2 ± 2 0 ton N d−1）. Riverfluxes in the NH region of Hiroshima Bay wereand sewage DIN inputs to the NH region were 3 7

estimated from the output of the box model± 1 7 and 6 4 ± 0 8 ton N d−1, respectively, during

combined with measurements of DIN in the river,the vertically mixed season（September to March）,

the sewages and the bay.

similar to those during the stratified season（Fig. 3B）.

Monthly measurements of water temperature,

On the other hand, DIN export to the CH region（22salinity and DIN concentration were made from

±12 ton N d−1）was significantly greater than thatApr 2001 through March 2002 at 3 stations in NH

during the stratified season.

region and one station in CH region（Fig. 1）. The

The average terrestrial DIN input during the

Ohta River discharge and DIN concentration in

study period was 10 ± 2 6 ton N d−1. Based on thethe river were obtained from the River Bureau,

data during April 1996 to March 1997, Lee andMinistry of Land, Infrastructure and Transport,

Hoshika（2000）estimated the combined river andJapan and the Hiroshima Prefecture Environmental

sewage DIN inputs to the NH region to be 327

Bureau, respectively. The sewage discharge andton N month−1（11 ton N d−1）which was similar

DIN concentration data were provided by theto the estimate made by the present study. The

Hiroshima City Sewage Bureau. Rainfall data wasannual DIN budget（Fig. 3C）indicated that all input

obtained from the Hiroshima Meteorological Local

terms combined river, sewage and the CH region,

Observatory. Evaporation was calculated from anto the NH region were equivalent to 22 ± 7 8 ton

empirical relationship based on wind velocity andN d−1. On the other hand, DIN export to the CH

vapor pressure.

region was equivalent to 14 ± 13 ton N d−1. These

During the stratified season（April to August）,the

results suggest that a significant part of DIN input

Ohta River and sewage treatment plants suppliedis consumed by phytoplankton and converted into−1

4 2±2 5 and 6 3±1 3 ton N dof DIN, respectively,

the particulate form in the NH region, especially inKenji TARUTANI

Fig. 3. DIN budget in the northern Hiroshima Bay. A）stratified
season （April to August 2001）, B）vertically mixed season（September 2001 to March 2002）, and C）annual mean during April
2001 to March 2002. Arrows represent mean fluxes（±1 SE）in ton
N d−1. Values within square represent mean standing stocks（±1SE）in ton N.

Impacts of oyster cultures on nitrogen budgets
the upper layer. Phytoplankton productivity in the
NH region of Hiroshima Bay was measured at theRemoval efficiency of nitrogensame time as nutrient samples were collected forfrom Hiroshima Bay by oyster cultures

this analysis. High phytoplankton nitrogen demand（228 mg N m−2 d−1）
, which estimated from annual

Annual oyster production in Hiroshima Bay

carbon productivity with the Redfield ratio（Redfield

was about 19 500 ton during April 2001 to March1958）, strongly supports the suggestion driven from2002. Given that the nitrogen content of cultured

the box model analysis.

oyster was account for 1 24% of fresh meat wet
weight production（Whyte and Englar 1982）, thenitrogen removal rate through oyster harvesting

Filtering activity of phytoplankton particulate

was estimated to be 0 66 ton N d−1. On an annual

nitrogen by oyster culturesbasis, this rate is account for 6 4% of daily terrestrial
DIN input into the NH region. On the other hand,

The grazing activity of oyster cultures was

the nitrogen removal rate through fisheries wasdetermined from the filtration rate and the ambient

estimated to be 0 15 ton N d−1, from annual catches

phytoplankton biomass. In the present study, oysterof 5 030 ton with fish nitrogen composition of,filtration rate was estimated as a function of total

indicating that oyster cultures recycled nitrogen tooyster biomass and water temperature（Chapelle etterrestrial areas in quantities approximately 5-foldal. 2000）. The monthly cultured oyster biomass was

greater than fisheries in Hiroshima Bay.

estimated by working backward from the harvest
with first-order approximation for two year of

Conclusion

cultivation period.
On an annual basis, Chl.

loss through oyster

In summary, the present study has shown

grazing was estimated to be 0 83 ton Chl.

that oyster cultures have a significant impact on

d −1 , corresponding to be 7 3 ton N d −1 with athe nitrogen cycles in Hiroshima Bay in terms

phytoplankton C: N ratio of 5 7 and a C: Chl.

ratio

of removing the particulate matter and nitrogenof 50: 1. This result suggests that an average 20%

from the water column. These results suggest thatof the phytoplankton production（36 ton N d−1）isoyster cultures could be used as a possible toolconsumed by cultured oysters in the NH region offor suppressing eutrophication in addition to their

Hiroshima Bay.

primary function of food production. However, large

Micro- and macro-zooplankton are generallyoyster populations can lead to a variety of negative

principle consumers for phytoplankton community.

effects on the benthic ecosystems. Therefore,

Extrapolating from the biomass data measured

appropriate management of oyster cultures isduring the same study period in accordancenecessary for beneficially operating their removalwith Uye et al. （1996）and Uye and Shimazu

efficiency of nitrogen.

（1 9 9 7 ）, annual grazing rates of micro- andmacro-zooplankton were estimated to be 2 4

Acknowledgements−1

and 4 0 ton N d , respectively in the NH region（unpublished data）. Therefore, oyster grazing

The author thanks Drs. T. Uchida and Y.

accounts for 53% of daily phytoplankton nitrogen

Hanamura for their cooperation throughout theloss, suggesting that oyster cultures play a

study. Thanks are also extended to Drs. K. Usuki

significant role for removing the particulate N fromand M. Hamaguchi for their helpful discussions

the water column in Hiroshima Bay.

and Mr. H. Suzuki for providing with unpublishedsewage data. This work was performed as a part of
the Integrated Study on the Development of Natural
Cyclical Functions through Forest, Agricultural andAquatic Ecosystems program supported by theKenji TARUTANIMinistry of Agriculture, Forestry and Fisheries ofJapan.

Redfield A. C., 1958: The biological control ofchemical factors in the environment.

.,

46, 205-221.
References

Songsangjinda P., Matsuda O., Yamamoto T.,
Rajendran N. and Maeda H., 2000: The role ofChapelle A., Menesguen A., Deslous-Paoli J-M.,
Souchu P.,Mazouni N., Vaquer A. and Millet B.,

suspended oyster culture on nitrogen cycle in., 56, 223-231.

Hiroshima Bay.

2000: Modelling nitrogen, primary production

Uye S. and Shimazu T., 1997: Geographical andand oxygen in a Mediterranean lagoon.

seasonal variations in abundance, biomass

Impact of oysters farming and inputs from theand estimated production rates of meso- andwatershed.

., 127, 161-181.

macrozooplankton in the Inland Sea of Japan.

Cloern J. E., 1982: Does the benthos control., 53, 529-538.

phytoplankton biomass in southern San

Uye S., Nagano N. and Tamaki H., 1996: Geographical., 9, 191-202.

and seasonal variation in abundance,

Hatcher A., Grant J. and Schofield B., 1994: Effects

biomass and estimated production rates ofFrancisco Bay?
of suspended mussel culture（spp.）onsedimentation, benthic respiration and sedimentnutrient dynamics in a coastal bay.
., 115, 219-235.

., 52, 689-703.
Whyte J. N. C. and Englar J. R., 1982: Seasonalvariation in the chemical composition and

Lee I-C. and Hoshika A., 2000: Seasonal variations inpollutant loads and water quality in HiroshimaBay.

microzooplankton in the Inland Sea of Japan.

., 23, 367-373（inJapanese with English abstract）.

condition indices of pacific oyster,, grown in trays or on the sea bed.
., 39, 1084-1094.

水研センター研報，第19号，41−51，平成19年
Bull. Fish. Res. Agen. No. 19, 41‑51, 2007

博士号論文

A framework for developing ecological carrying capacity
mathematical models for bivalve mollusc aquaculture
Roger I. E. Newell＊

Abstract Aquacultural production of suspension-feeding bivalve molluscs can profit frominformation on the stocking density at which commercially valuable meat production is
maximized. Predicting these stocking densities in the natural environment is difficult a priori because of the complex interacting effects of environmental variables on bivalve growth（e.g., food availability varies with rates of phytoplankton production, water currents affectfood flux to the bivalves, etc.） In an effort to integrate the influence of environmental
variables on bivalve growth a number of mathematical carrying capacity models havebeen developed that estimate the standing stock at which commercial harvests are maximized. This emphasis means that other important aspects of ecosystem carrying capacity, such as the ability of the culture site to process the excrement produced by the animals,
may not be adequately modeled. I recommend that an open source- code community model
be developed to assess ecological carrying capacity for bivalve aquaculture. The overall
objective should be to develop a well-parameterized model that will allow a comprehensive
assessment of the major interactions between cultivated bivalves and the ecosystem. For
example, in addition to predicting tissue production, this model can be used to assess theability of suspension-feeding bivalves to exert top-down control on phytoplankton stocks,
reduce turbidity, enhance nutrient removal, and provide habitat for other organisms. These
secondary benefits can have economic value to the aquaculturists as part of polyculture systems, environmental remediation, and nutrient trading schemes. By modeling major aspectsof ecosystem function, such as competition for food with other suspension feeding organisms,
rates and location of biodeposition etc., models can be used to predict and possibly minimize
potential adverse effects of bivalve aquaculture.
Key Words: Aquaculture, Bivalves, Carrying Capacity, Nutrient Removal, Polyculture

achieve this maximum production is often simply
INTRODUCTION

referred to as the

carrying capacity.

Carrying

capacity is quite a widely-used term in biological
All models are wrong. Some models are usefulscience and, confusingly, has acquired a number of（DiToro 2001）

different meanings. Originally, it was a concept inCommercial aquaculture of suspension-feeding

ecology that was applied to the population density

bivalve molluscs, such as oysters and mussels, canachieved at the asymptote in the logistic population

benefit from quantitative estimates of how muchgrowth equation （Odum 1983, Dame and Prins

production can be obtained from a location. The

1998）. More recently, the term has broadly come tonumber of individuals that have to be stocked tomean the maximum biomass that can be sustained

2006年 月26日受理（Received. June 26, 2006）＊
Horn Point Laboratory,
University of Maryland Center for Environmental Science
PO Box 775, Cambridge, MD 21613, USAemail: newell@hpl.umces.edu

Roger I. E. Newellby the available resources （Odum 1983）. Thiselsewhere into the system（e.g., from finfish that areecosystem-based concept forms the basis of Carver

intensively fed）. Furthermore, in some countries

and Mallet s（1990）definition of carrying capacity as（e.g., USA）there is a move toward nutrient trading

the maximum standing stock of a particular cultured

schemes where industries that pollute aquatic

species at which production is maximized without

systems with nutrients pay other industries tonegatively affecting growth rates. That definition

remove nutrients from the same body of water. It

may not always apply to commercial aquaculture,

is possible that shellfish aquaculture may qualify

however, because production may be maximal evenfor payment under such nutrient trading schemes

though individual growth rates are low（Smaal

if the aquaculture facility is managed in such a way

1998）. Because of such inconsistencies, Smaal

to maximize nutrient removal（Newell 2004）. Only（1998）proposed a definition for aquacultural

by developing predictive models will it be possible

production where

exploitation carrying capacity

is the stock size at which a maximum yield of themarketable cohort is achieved.
Estimating

to design systems that maximize levels of nutrient
removal.
In order to accommodate this broader ecosystem

exploitation carrying capacityforperspective, I propose that

ecological carrying

aquaculture sites in the natural environment, andcapacity for bivalve aquaculture be defined as The

thereby assessing potential economic returns priorstanding stock of suspension-feeding bivalves whereto establishing an aquaculture operation is difficult.

the consumption of phytoplankton, enhancement

This is because food availability, which is one of theof nutrient removal, and other ecosystem services

prime factors governing bivalve growth, is spatiallyare maximized without negatively affecting waterand temporally variable because of changes in rates

quality, sediment biogeochemistry, and overallof phytoplankton production and water currents

ecosystem function.

that regulate

of carrying capacity proposed by Duarte

food flux

through the grow-out

sites（Wildish and Kristmanson 1997, Bacher

This is similar to the definition（2003）of the level to which a process or variable

2003）. In an effort to integrate these complex

may be changed within a particular ecosystem,

environmental variables a number of different

without driving the structure and function of thecarrying capacity models have been specificallyecosystem over acceptable limits. Both definitions

developed in order to predict optimum bivalve

suffer from ambiguous definitions of an unacceptable

stocking densities（e.g., Bacher

outcome（i.e.,

1997, Dowd

1997, Campbell and Newell 1998, Smaal
Chen

1999, Bacher

2003, Nunes

1998,

2003, Duarte

2003）
.

without negatively affecting

andover acceptable limits. ） It is necessary for there
to be greater discussion as to what constitutes theproper criteria and methods for assessing ecosystem

Restricting models to predicting the stocking

influence.

It is overly optimistic to think that any

density that maximize harvest yields means thataquaculture operation will have no adverse impacts

there is no consideration of possibly adverse effects

whatsoever; consequently, the question becomesof the cultivated bivalves on important aspects ofwhat level of impact is considered acceptable given

ecosystem function, such as the ability of the culture

the benefits accrued from that activity. Ultimately

site to process excrement. In addition, possible

because that is a societal, and not an objective

ecosystem benefits are not modeled, such as bivalvesscientific question, the acceptable levels will likely

feeding on phytoplankton and in the process

vary from country to country.

removing nutrients from the water column（Newell

Some criteria for monitoring ecosystem influences

2004）. This concept is the basis of integratedof bivalve aquaculture have been developed

ecologicalaquaculture

and can be used both as modeling criteria and2004）inthen objectively measured in field situations.

orbalanced ecosystem

operations（McVey

2002, Neori

which commercially valuable species from different

For example, Grant（1995）performed a

trophic levels（e.g., algae and bivalves）are cultured

detailed study of a mussel aquaculture site andso that they extract nutrients that are being added

used a sophisticated benthic faunal analysis andEcological carrying capacity models for bivalve aquaculture
measurements of sediment biogeochemistry to

production to higher trophic levels, are difficult toquantify ecosystem impacts. Both of these criteria

model but can be important ecosystem benefits ofare highly sensitive to sediment redox balance.

bivalve aquaculture systems.

The depth of the redox potential discontinuity
MODEL COMPONENTS（RPD）in sediments can be measured directly,
either in sediment cores collected in transparent
acrylic plastic tubes（Grizzle and Penniman 1991）,

1 ） T o p - d o w n c o n t r o l o n p h y t o p l a n k t o n andor by using a remotely operated camera system

microzooplankton

that directly photographs the sediment profile（OSuspension-feeding bivalves remove particles

Connor1989）. This photographic technique> 3 μm diameter from the water column withcan also provide quantitative information on changes

high efficiency when water temperatures are highin the infaunal macrofauna community.

These

enough to promote activity（Bayne and Newell 1983）.

criteria are similar to those adopted in Japan, where

This feeding activity can have the beneficial effectthe accumulation of acid volatile sulfide in theof exerting exert top-down control on phytoplankton

sediment and changes in macrofauna abundance are

populations that may be stimulated by nutrient

used to monitor the influence of fin fish cultivation

inputs from point and diffuse terrestrial sources,on the surrounding environment（Yokoyama 2003）.

adjacent fin-fish aquaculture sites, etc.（Newell 2004,

This approach of objectively specifying certain

Newellkey ecosystem processes and then monitoring

microzooplankton, may also reduce the dominancethese at aquaculture sites allows deviation fromof carbon flow through microbial loop pathways

predetermined values for each variable to be（Sherr and Sherr 1988, Kreeger and Newell 1997,

discerned. These key ecosystem processes can also

Kamiyama 2004）.

2005）. Bivalves, by directly grazing on

be incorporated as output parameters in a model toSize selective feeding by bivalves means thatpredict the effects of balanced aquaculture on thelarger nanoplankton cells （>3 μm diameter）

ecosystem.

are preferentially removed in comparison with

The objective of this paper is to provide asmaller and less efficiently retained picoplankton

framework to help stimulate a discussion of what

species.

should be included in future

resources available to suspension-feeding bivalvescapacity models

ecological carrying

for bivalve aquaculture.

In order to accurately model the foodThisin any particular location, the size structure of themodel should only include the essential elements as

phytoplankton and microzooplankton community

it would be counterproductive to develop an overly

needs to be assessed.

complex model, with time spent parameterizing

to include size-specific rates of phytoplankton

details that do little to improve the overall accuracy

production rather than use total chlorophyllof the model predications. I briefly review here

concentrations as a proxy for food available tosome of the information that needs be included

bivalves, which is the approach adopted in manyfor the main four ecosystem processes thatexisting bivalve carrying capacity models（Campbell

suspension-feeding bivalves influence: 1）top-down

and Newell 1998, Smaal

control on phytoplankton and microzooplankton; 2）

2003, Duarte

sediment hypoxia; 3）inorganic nutrient cycling; 4）

grazing by bivalves can lead to the situation where

reduction in turbidity. I also briefly draw attention

picoplankton species are subject to reduced grazer

to the fact that the culture gear （rafts, cages,

control compared to larger species and henceropes, etc.）and the animals themselves can provide

become relatively more abundant（Olsson

important habitat for other ecologically valuable

Prins

This will require models

1998, Nunes

2003）. Furthermore, differential

1992,1998）. Such an increase in picoplankton

fouling community organisms. Transfer of organic

was documented by Vaquermaterial to the sediment surface in biodeposits may

Souchu（1996）andalso stimulate benthic production. Such effects on

the Mediterranean that has high abundances ofsecondary production, and the likely transfer of thisaquacultured bivalves.

（2001）in a poorly flushed lagoon inRoger I. E. Newell
An additional reason for not simply using totalcomponent of the zooplankton, rely on a relatively

chlorophyll as an estimate of food availability is that

small number of adults to survive overwinter thatsome species of phytoplankton possess toxins that

can then feed and reproduce in order to rebuild the

reduce bivalve feeding activity（Shumway 1990）. It

population. As discussed above, bivalve grazing may

is thought that blooms of such toxin producing algae

alter phytoplankton species and size composition

may be increasing in distribution and frequency

and thereby affect the food resources available toworldwide and anthropogenic nutrient enrichment

other benthic and pelagic suspension-feeding fauna.

is a likely causal factor（Cloern 2001）. Even if thealgal toxins do not adversely affect the bivalves

2）Sediment hypoxia

directly, toxins can be bioaccumulated to levels that

Aquacultured finfish require an external foodrender the flesh unsafe for human consumption

source and this feeding results in the addition to（Shumway 1990）. Because the exact causes of

the water surrounding the aquaculture facility

harmful algal blooms are uncertain, it will be difficultof

to incorporate their occurrence into predictive

urine and feces that can stimulate high levels of

ecosystem models but that does not mean that theirphytoplankton production. The situation is very

influence should be ignored.

different for bivalve aquaculture because thenewdissolved inorganic nutrients from fish

There can also be deleterious ecosystem

dissolved and particulate excrement released toeffects of high rates of phytoplankton removal

the environment by bivalves is solely from themby suspension-feeding bivalves. At high bivalve

consuming autochthonous production that utilizes

densities there can be intraspecific competition forambient dissolved inorganic nutrients. However,food that can be partially reduced by configuringpotentially adverse effects from both finfish andthe culture system to increase water throughshellfish aquaculture facilities can result from excess

the site, thereby minimizing refiltration.

Thisdeposition of fecal material that may overload thepurely physical influence of water flow on foodunderlying sediments with particulate organic

flux can now be efficiently modeled using coupledmaterial. Bacterial decomposition of this organic

physical and biogeochemical models（e.g., Campbell

material can release more inorganic nutrients and in

and Newell 1998, Chen

1999, Duarte et al.

extreme situations cause sediment anoxia, thereby

2003）. Interspecific food competition between

reducing the biomass and species diversity ofhigh abundances of cultured bivalves andbenthic fauna.

other ecologically valuable benthic and pelagic

Undigested organic material in the feces andsuspension-feeders（e.g., zooplankton）should be

pseudofeces of bivalves are voided as mucus-boundmodeled explicitly.

pellets（collectively called biodeposits）that can be

For example Lam-Hoai（1997）reported that in areas with shellfish

as long as several millimeters. As a consequence of

aquaculture there were appreciable differences

this aggregation, biodeposits have a faster sinking

in abundances of 40 to 300 μm diametervelocity that is up to 40 times that of the component

microzooplankton compared to areas with noparticles（Widdows

aquaculture farms. They ascribed these differences

settle where the friction velocity（u＊）, which isin community structure to microzooplanktona function of current velocity and bed roughness,being directly grazed by bivalves and by otheris below a critical velocity required to suspend

suspension-feeding invertebrates attached toparticles of that particular mass （Miller

the aquaculture structures.

1998）. These biodeposits

Bivalves may also2002）. In locations with sufficient physical mixing,

out-compete some types of zooplankton forbiodeposits can become disaggregated into smaller

phytoplankton because bivalves overwinter as

particles that sink more slowly and are resuspended

adults and are able to start feeding when waterat lower friction velocities. Where bottom friction

temperatures reach the threshold necessary

velocities remain below the critical erosion velocity,

to promote an active metabolism.

In contrast,

biodeposits undergo a consolidation process andtemperate copepod species, that form a dominantbecome incorporated into the sediments around theEcological carrying capacity models for bivalve aquaculture
bivalve population, hence increasing particulate andfeeding.

dissolved nutrient concentrations within that zone

assimilated are excreted and returned to the water（Kasparcolumn nutrient pool. A majority of the nitrogen

1985, Miller

2002）
.

Nutrients that are digested but not

Because bivalves filter phytoplankton from large

is excreted in the form of ammonium and this may

volumes of water, and these biodeposits are voided

have a stimulative effect on local phytoplankton

in the relatively small region around the aquaculture

production（Dame 1996, Newellsite, bivalves do serve to concentrate and focus
nutrients （for review see Newell2005）.

Food-based carrying capacity models（e.g., Smaal
1998, Duarte

2003, Nunes

2003）can2005）.

Undigested organic material is transferred to thesediment surface in biodeposits where it is degradedthrough complex microbial processes （DiToro
2001, Newell2002）. A large proportion of thepredict the locations with the highest phytoplankton

nitrogen（N）and phosphorus（P）is regenerated

production that can support the greatest density

back to the water column （Newellof aquacultured bivalves. Unfortunately, in such

Inorganic nutrient regeneration from the sediments

productive locations bivalves can be stocked at suchis not 100% efficient, however, which leads to thehigh densities that their biodeposits are focusedloss of some nutrients each time phytoplankton

onto a small area of sediments. When receiving

are consumed by bivalves and the resulting

sediments become overloaded with organic material

biodeposits transferred to the sediment surface.

the resulting bacterial respiration can consume

Where sediments remain oxygenated, some of theoxygen at rates faster that it can be resuppliedP that was originally incorporated in phytoplankton,by diffusion.

In such circumstances anaerobic

but was not digested by the bivalves, can become

microbial pathways dominate, and sulfur reducing

sequestered and buried as iron-bound complexes.

bacteria produce high levels of hydrogen sulfide

Where biodeposits are incorporated in aerobic

that are toxic to benthic infaunal species（Diaz andsurficial sediments that overlay deeper anaerobic

Rosenberg 1995）. This loss of infauna exacerbates

sediments, microbially mediated coupled nitrifica

the adverse effects of excessive biodeposition ontion-denitrification can remove as N2 gas some of

sediment biogeochemical processes because of athe nitrogen that was originally incorporated in

reduction in bioturbation processes that serve tophytoplankton. Some N can also become buried

bring oxygen into the sediments（Aller 2001, DiToro

in the accumulating sediments. In locations with

2001）
. Loss of infauna also reduces food resources

sufficient light at the sediment surface, however,for carnivores at higher trophic levels.

benthic microalgae compete with nitrifying bacteria

2005）
.

Understanding and modeling the biotic and abiotic

for N regenerated from the bivalve biodeposits,changes in the receiving sediments associatedthereby reducing or even precluding coupled nitr

with organic loading from bivalve excrement is

ification-denitrification（Newellnecessary in order to accurately parameterizesediments become anaerobic, coupled nitrification-de2002）. If theshellfish ecological carrying capacity models.

nitrification is inhibited, P is mobilized and released

Accurately modeling water flow is especially criticalto the water column, and the resulting build-up ofsince strong water currents can distribute bivalve

H2S can be toxic to other benthic animals. Loss of

biodeposits widely over the bottom, hence reducing

these bioturbating fauna reduces sediment irrigation

their adverse effects on sediment. Water flow is alsothat is an important mechanism for sedimentcrucial in supplying oxygenated water to hypoxic

oxygenation, and hence further increases thesediments.

likelihood that the sediment will remain anoxic.
Duarte3）Inorganic nutrient cycling（2003）suggested that spatially

explicit hydrological models be used as the basis of

Nutrients incorporated in phytoplankton biomass

carrying capacity models. By modeling water flow

are filtered from the water column by bivalves,and food fluxes the optimum spatial distribution

ingested, and digested in seasons when waterof aquaculture farms within coastal systems may

temperatures are warm enough to promote active

be accurately predicted.

The influence of theRoger I. E. Newellaquaculture systems themselves（rafts, ropes, etc.）

reducing sediment suitability for seagrasses,

in imposing drag, and hence reducing water flow,

sediment erosion associated with on-bottom

also needs to be considered（Grant and Bacher

racks altering bottom water currents, and severe

2001）. Better information on water currents also

disturbance associated with husbandry activities

means that the possible distribution of biodeposits（Everett

1995）.

over the surrounding sediment surface can be

A potential adverse effect of an increase in light

predicted. This distributional data, when linked withat the sediment surface is that nuisance macroalgae

information on the biotic and abiotic characteristics

may become established, rather than a more normalo f t h e r e c e i v i n g s e d i m e n t （e . g . , g r a i n s i z e ,flora of seagrasses and microphytobenthos. Some

porosity, influence of periodic storms in scouringtypes of macroalgae（e.g., Cladophora spp.）flourish

bottom sediment, etc.）will allow the influence ofin locations that have elevated levels of inorganic

biodeposition on sediment biogeochemistry andnutrients and relatively low irradiances（from 18 tobenthic organisms to be modeled（DiToro 2001）.

175 μmol photons-2 s-1）, and under such conditions

Information on rates of nutrient regeneration, burial,

can out-compete other macroalgae （Rafaelli

and denitrification becomes even more crucial if1998）.

bivalves are being cultivated as part of a poylculture
system in order to enhance nutrient removal（Newell
2004）.

5）Provision of food resources and habitat for otherorganisms.
Bivalve biodeposits have a high residual organic4）Reduction in turbidity
In locations with high bivalve biomass andcontent, with a C:N ratio similar to phytoplankton（Newell2005）, and can therefore provide a

relatively restricted water exchange withnutritious food source for benthic deposit feeders.

surrounding waters, the feeding activity of bivalves

An increase in sediment organic N content has

can remove sufficient organic and inorganic

frequently been observed near large aggregations

seston particles that the amount of light reachingof bivalves（Kaspar

1985, Kautsky and Evans

the sediment surface is increased. This has the

1987, Deslous-Paoli

1992, Hatcher

effect of reducing the dominance of phytoplankton

Stenton-Dozey

production and extending the depth to whichobserved in benthic communities adjacent to bivalve

ecologically important benthic plants, such as

stocks is very dependent on the magnitude ofseagrasses and benthic microalgae, can grow.

sediment enrichment by biodeposits. The degree ofNewell and Koch（2004）developed a simple model

enrichment is governed not only by the abundanceof the effects of suspension-feeding bivalves onof bivalves but also the area of bottom over whichaltering light penetration and the consequent

their biodeposits are distributed, which is dependent

benefits to seagrass beds. Their model showed thaton the magnitude of water currents and wave action

reestablishing seagrass beds may be facilitated by（Millerfirst rebuilding depleted oyster stocks to increase

above, high levels of biodeposition can stimulate

light penetration. It is apparent that aquacultured

sediment microbial metabolism to the point thatoysters could provide similar improvements to water

oxygen becomes limiting. At this point bacterial

clarity, therefore potentially allowing management

anaerobic metabolic pathways start to generateauthorities to permit aquaculture in regions

toxic hydrogen sulfide（Aller 2001）.

1994,2001）. The type of response

2002, Newell 2004）. As discussed

generally considered too ecologically sensitive for

In response to low to moderate organic loadingssuch commercial uses. It has been shown, however,by bivalves, species diversity and biomass ofthat there are severe reductions in seagrass beds inmeiofauna and macrofauna deposit feeders are

the immediate vicinity of oysters cultivated on theo f t e n i n c r e a s e d c o m p a r e d t o a r e a s w i thoutbottom in Oregon, USA. The causes of this seagrassbivalves（Kautsky and Evans 1987, Dittmann 1990,

loss were multifaceted, including direct shading

Ragnarsson and Raffaelli 1999）. Grantby the aquaculture gear, enhanced biodeposition

reported relatively minor changes in macrobenthic（1995）

Ecological carrying capacity models for bivalve aquaculturebiomass and diversity associated with biodeposition

2001）that then provide a food source for manyfrom suspended mussel culture.

The benthic

animals. A simplifying approach for including thecommunity underlying intensive rope-cultivation ofprovision of habitat in ecosystem models would bemussels has often been observed to change from one

to calculate the amount of surface area available

with a diverse species composition to one composed

to be colonized by plants and animals on the

predominately of infaunal polychaetes（e.g., Kaspar

aquaculture system（Dealteris

1985, Stenton-Dozey2004）. Then

2001）
. Increases

using simple empirically derived relationships

in polychaetes can leads to enhanced bioturbation

estimate the amount of biomass that may be present

which has the beneficial effects of increasing rates

for secondary consumers. Such estimates can thenof coupled nitrification-denitrification compared withbe refined by sampling the aquaculture system oncethe control sites（Kaspar

it is in operation to quantify the biomass of plants

1985）. Tenore（1982）reported that excessive biodeposition from a

and animals. The extreme periodic disturbanceshigh density of mussel aquaculture rafts changed theassociated with cultivation and harvest practices,benthic infauna from one with high species diversity

especially those required for on-bottom culture ofand biomass to one characteristic of a pioneering

infaunal bivalves（e.g., Everett

community, with low species diversity and biomass.
There was also reduction in bioturbation associated1995, Kaiser1998）,will negatively affect the habitat and should
be included in the model.

with the loss of the diverse infaunal community as
CONCLUSIONS

the dominant species in the pioneering community
were tube-building worms with little influence on
sediment vertical mixing and sediment irrigation.

I recommend that new

exploitation carrying

These types of secondary effects from shellfish

capacitymodels for suspension-feeding bivalve

aquaculture are difficult to model because theaquaculture be developed that can also serve as

responses are so variable between locations. In

ecological carrying capacity models. The modelorder to capture at least some of these ecosystemshould include sufficient detail of major ecosystemchanges, three-dimensional physical models can beprocesses to predict possible beneficial and negative

used to predict the amount and spatial distribution of

influences that the aquaculture facility may haveorganic material transferred to the sediment surface.

on the environment. Properly designed models will

Models of sediment biogeochemical processes

allow regulatory authorities to assess the secondary（DiToro 2001）can be used to predict the depth ofbenefits of using bivalves to provide ecosystem

oxygen penetration into the sediment and this used

services, such as graze phytoplankton and thereby

to predict if there will be negative effect on infauna.

remove some of the excess anthropogenic inorganic

In locations where sediments remain aerobic it will

nutrients present in many of the world s coastal

be possible to predict the amount of organic material

waters. Modeling rates of nutrient regeneration

available to be supplied to the benthic deposit feeder

to the water column and removal is especiallycommunity and this can then be used to estimate

relevant torates of carbon transfer to higher trophic levels.

aquaculture operations where bivalves and seaweed

An important ecosystem benefit of natural
shellfish beds is that they provide habitat for many
invertebrate and vertebrate species（Coen
1999, Ragnarsson and Raffaelli 1999, Peterson
2003）. Dealteris

ecologicalorbalanced ecosystem

are cultivated to help remove nutrients generated
from finfish aquaculture（McVey

2002, Neori2004）.
Many different research groups have developed（2004）have shown that bothcarrying capacity models for bivalve mollusc

on-bottom and off-bottom aquaculture holding gear

aquaculture. These models, some of which are cited

also provides the type of spatially complex habitat

above, have all been undertaken as independentthat is sought by many species of mobile animals.

projects and have rarely directly incorporated

These aquaculture structures provide a surface

relationships parameterized for earlier models. I

for plant and animal colonization（Mazouni

think that it would be advantageous to all concernedRoger I. E. Newell
if new ecosystem models are developed as open

predictions about ecosystem effects.

sourcethat enable free andsignificant logistical problems that have to be solved

open access to the relevant code. Community models

before embarking on developing such a community

allow various investigators to parameterize and add

based model. Primarily this will require ensuring

in specialized sub-models that ultimately constitutethat sufficient long-term funding is committed fora single, fully parameterized, model. For example,

the support personnel who can maintain model code.

three-dimensional physical models have beenOnce a model is implemented it must be refined anddeveloped by Chen

（1999）that could serve as

validated using monitoring data that is frequently

the central core of a new bivalve aquaculture model.

required to be collected by regulatory authorities to

The complex sediment biogeochemical processes

ensure that the aquaculture facility complies withthat will be affected by bivalves are included

permit requirements.

community models

There arein the sophisticated sediment diagenesis model
developed by DiToro（2001）which can be added as

Acknowledgments

a component to an aquaculture model. The influenceThis paper was presented to the 33rd meeting of theof bivalve on light penetration and the growth of

United States-Japan Natural Resources Aquaculture

benthic plants could be based on models developed

panel symposium Ecosystem and Carrying Capacity

by Alvera-Azcarate（2003）for macroalgaeof Aquaculture Ground as part of an internationaland Newell and Koch（2004）for seagrasses. In thisexchange agreement between the governments ofway essential elements are gradually incorporated

Japan and the United States at the November 2004

into the core model in order to improve the overall

meeting in Nagasaki, Japan. I am grateful to Dr.

accuracy of the model predications.

Jeff Cornwell, Dr. Tom Fisher, and Dr. Jim McVey

The approach I advocate of developing an
open source code

Community Modelfor their scientific discussions that helped develop

withmy thinking on this topic. Dr. Jack Rensel kindly

well-parameterized compartments has been widelycommented on an early draft of this manuscript.

adopted by physical oceanographers, who haveThis research was supported in part with funding

developed the Princeton Ocean Model（www.aos

from Maryland Sea Grant（SA07528051-F）through.princeton.edu/WWWPUBLIC/htdocs.pom/）and

NOAA award NA16RG2207.

the Regional Ocean Model System （www.marincontributed toward my travel expenses. The US

e.rutgers.edu/po/）. This approach is also being

government is authorized to publish reprints of thisadopted for ecosystem models.

NOAA kindly

For example, awork, and the author reserves the right to post amodel is under development for the Chesapeakecopy on his academic website for the private and

Bay watershed and estuary that will enable free

non-commercial use of individuals, notwithstanding

and open access to source code. This is intended

any copyright notations hereon.

to be a web-based model that will include a base
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水研センター研報，第19号，53−68，平成19年
Bull. Fish. Res. Agen. No. 19, 53‑68, 2007

博士号論文

Microbial activity and community structure
in a net pen aquaculture area
Tomoko SAKAMI＊1, Katsuyuki ABO＊1and Kazufumi TAKAYANAGI＊2

Abstract Excess organic matter production from net-pen aquaculture farms operated inopen water causes serious seawater pollution. To develop sustainable aquaculture systems
we need to consider the mechanisms of organic matter cycling. Microbial communities havevery important roles in cycling organic matter in seawater. To elucidate how microbial communities are affected by aquaculture activities, we examined the bacterial activity and community structure in a red sea bream aquaculture area and a neighboring, non-aquaculture,reference area in Gokasho Bay, Japan.
The bacterial activity parameters examined - abundance, production rate, and extracellular hydrolytic enzyme activity- were always higher in the aquaculture area than in thereference area, and these differences were most pronounced in surface waters in summer.
The annual mean bacterial abundance and production rate in the aquaculture area were 4 7
×109 cells L−1 and 82 mg C m−3 day−1 : about 1 4 and 3 5 times, respectively, those in thereference area. The annual bacterial production per unit area was estimated as 608 g C m−2
y−1 in the aquaculture area. The difference of bacterial production between the two examined areas was 444 g（37 mol）C m−2 y−1, which was equivalent to the organic matter loads
from fish farming. This fact suggests that bacterial community in seawater could utilize organic matters as much as fish farms released into the surrounding water in this aquaculturearea.
The annual mean extracellular leucine aminopeptidase activity（which represents bacterial protein degrading activity）in seawater in the aquaculture area was about twice that in
the reference area. On the other hand, the activity of β-glucosidase（which represents polyhydrocarbon degrading activity）in the aquaculture area was about five times that in thereference area, indicating that, overall, β-glucosidase activity was promoted more than leucine aminopeptidase activity. These microbial activity parameters were positively correlatedwith the organic matter concentrations in the water, suggesting that input of organic matterfrom the fish farms to the surrounding waters promoted microbial activity.
We examined bacterial community structure in seawater by using a PCR-denaturant gradient gel electrophoresis（DGGE）method based on 16S-rRNA gene fragment fingerprinting.
Since the level of leucine aminopeptidase activity was closely correlated with the particulateorganic matter concentration, the bacterial community was separated into two categories,
particle-associated（>1μm）and free-living（<1μm）. In the free-living bacterial community,
the number of DGGE bands（which corresponded to bacterial species）ranged from 2 to 12,
and the DGGE profiles were similar in the aquaculture area and in the reference area. However, some bands identified as representing alpha and gamma proteobacteria were observed
only in the aquaculture area from spring to autumn. In the particle-associated bacterial community, the number of DGGE bands was less than in the free-living one, and most of thebacteria were identified as cyanobacteria. However, in summer, when the particle-associatedbacterial community had high hydrolytic enzyme activity, bands identified as representing
2006年 月26日受理（Received. June 26, 2006）＊1
National Research Institute of Aquaculture, Nansei, Mie, 516-0193, Japan＊2
Seikai National Fisheries Research Institute, 1551-8, Tairacho, Nagasaki, 851-2213, Japan

Tomoko SAKAMI, Katsuyuki ABO and Kazufumi TAKAYANAGI

thegroup, most isolates of which have the ability todegrade biomacromolecules, were detected in the aquaculture area, together with those ofalpha and gamma proteobacteria. These results suggest that the variation in bacterial activity was related to bacterial community structure and that aquaculture activity affects thebacterial community in seawater, both quantitatively and qualitatively.
Key words: Bacterial production, hydrolytic enzyme, particle-associated bacteria, DGGE

Net pen culture is the most common form of fishin aquatic ecosystems, and therefore ectoenzymatic

aquaculture in Japan. Because it is usually conductedactivity is a good indicator of organic matterin small inlets where water circulation is rather small

degradation by bacterial communities （Chrost,and a large amount of organic matter is input into

1990; Chrost

the net pen as fish food, it can lead to the formation

quality and quantity of organic matter loaded intoof harmful algal blooms and oxygen-deficient water

an aquaculture area to be different from that inmasses, which are detrimental to cultured fish

oligotrophic areas where the major organic matter（Ministry of Agriculture, Forestry and Fisheriessource is phytoplanktonic primary production. The

of Japan, 2000）. To resolve these problems we firstmain ingredient of fish food is fishmeal and effluentsneed to elucidate the cycling of the organic matterfrom fish farms contain large amounts of polymericthat is added to the aquaculture area. In a fish cage

nitrogen compounds（Foy and Rosell, 1991; McCaig., 1993）. We can expect theaquaculture, it is estimated that approximately 80%., 1999）. Mesocosm studies have reported thatand 75% of input fish food carbon and nitrogen areprotein enrichment triggers a dynamic response

released into the environment（Hall1990,

in ectoenzymatic activity and population dynamics

1992）. It is consumed by bacteria directly or after

from the microbial community, whereas enrichment

reconstructed to organic matters by phytoplankton.

with starch has no effect（Chrost, 1993; Pinhassi

Bacterial production contributes to biological., 1999）. We can also expect the qualitative

production at higher trophic levels in aquaticdifferences in organic matter between the two areas

ecosystems via bacterivorous nanozooplankton

to lead to differences in bacterial organic matter（Carrick

utilization property indicated by ectoenzymatic., 1991; Sanders., 1996; Fukami., 1992; Jurgens., 1999; Wieltschnig.,

activity（Sinsabaugh., 1997）.

2000）. This process is now viewed as an important

We also need to elucidate structures of microbial

pathway for the energy and material flow as wellcommunities to understand their qualitative

as the large-organisms-dominated classic food chain.

variation. However, there are few studies

There have been many studies of the balance ofabout whole community structure of bacteriaorganic matter cycling in aquaculture areas（Tanaka,

in aquaculture areas because most of bacteria

1977; Hallin seawater cannot culture in ordinal bacterial., 1990, 1992; Foy and Rosell, 1991;

Holby and Hall, 1991; Johnsen, 1993）. However,culturing methods（Giovannoni and Rappe, 2000）.

there have been few studies of microbial activity and

Because bacteria in seawater are the first organisms

its contribution to organic matter cycling in thesethat act on organic matters loaded from fish farms,

areas（Moriarty, 1997; Patel

their variations of community structure may become., 2000; Sakami, 2003）, though the microbial community plays animportant role in degradation and remineralizationof organic matters.

a good indicator to assess effects of aquaculture
activities on surrounding environment.
The object of this study is to elucidate how

Most dissolved organic matter in seawater ismicrobial communities are affected by aquaculture.

polymeric and is degraded mainly by bacterial

We examined bacterial activity parameters such

ectoenzymes. Extracellular hydrolysis is thought toas abundance, production rate, and extracellular

be the limiting step of organic matter degradationhydrolytic enzyme activity in a red seabreamMicrobial activity and community structure in a net pen aquaculture areaaquaculture area. We found that these parameters

Administration Office, 1999）. In 1996 the fish feed

were always greater in the aquaculture area thanadded to the Hasama-ura aquaculture area wasthose in the reference area, and positively correlated

equivalent to a total of about 2225 t of carbon or 328

with the concentrations of organic matter int of nitrogen（Yokoyama, 2002）. This Hasama-ura

seawater. We also examined bacterial community

aquaculture area often suffers hypoxic water

structure in seawater and could detect someconditions and harmful algal blooms in summer

distinctive bacteria in the aquaculture area in warm

（Toda., 1994; Abo and Toda, 1995）.

water season. These facts indicates that aquaculture
activity affects the bacterial community in seawater,

Bacterial abundance, production and ectoenzymatic

both quantitatively and qualitatively.

activity
1. Sampling Water samples were collected from theMaterials and methods

aquaculture area of Hasama-ura inlet（Stn A, water
depth about 18 m）and from the central part of theStudy area

Gokasho Bay is located in the Sea

bay as a reference area（Stn R, water depth aboutof Kumano, which is contiguous with the Pacific

23 m）monthly from June 1999 to September 2000.

Ocean（Fig. 1）. The bay s mean depth is 18 m, andWater samples were obtained at depths of 0 5 m, 10

2

its area is 22 km . The main current runs into them and 1 m above bottom for bacterial production

eastern part of the bay. Intensive fish farms are

and ectoenzymatic activity measurements. In

operated in a small inlet in the western part of theaddition to them, water samples were also obtained

bay, the Hasama-ura inlet. The area where net-pensat depths of 2 5 m, 5 m（Stn R, Stn A）and 15 m

are set covers about 2×1 km. The major product（Stn R）for measurement of chemical parameters.

of this area is red sea bream. In 1999 the annual

Because water samples for bacterial production

fish production was 1578 t and the total area of

measurement had to be treated quickly after2

net-pens was 23 000 m （Tokai Regional Agriculturalcollection, they were collected separately（generally

Fig. 1. Map of the Gokasho Bay study area, showing sampling stations.

Tomoko SAKAMI, Katsuyuki ABO and Kazufumi TAKAYANAGI
the next day）from those collected for assessment of

extracellular hydrolytic activity, we measued theectoenzymatic activity and measurement of chemical

potential activity of two enzymes: β-D-glucosidase

parameters. We checked bacterial abundance,and leucine aminopeptidase, which are responsible

chlorophyll-α concentrations and dissolved organicfor the hydrolysis of predominating organiccarbon concentrations in both water samples.

constituents in the dissolved organic carbon pool,

Water temperature, salinity and chlorophyll-αi.e., β-linked polysaccharides and proteins（Chrost,

concentrations were measured1993）.

with aCTD device（Alex, Kobe, Japan）. Chlorophyll-αAminopeptidase and β-glucosidase activities

concentrations were calibrated on each sampling

were measured by using fluorophore-labeled analog

occasion by testing 3 or 4 water samples. The

substrates, namely L-leucine 7-amino-4-methyl-couma

chlorophyll-α concentrations were measured

rylaminide（leucine-MCA）and 4-methylumbelliferylby the N, N-dimethyl formamide extraction and

β-D-glucoside （MUF-β-glucoside）respectively

fluorescence method（Suzuki and Ishimaru, 1990）.

（Hoppe, 1983）. The substrates were added to

The water samples were carried to a land-based

duplicate water samples and 1 heat-killed（boiledlaboratory under cool and dark conditionsfor 20 min）blank at 4 different concentrations,

immediately after collection and treated as describedranging from 1 to 20μM for leucine-MCA and 0.04

below.

to 4μM for MUF-β-glucoside. We chose these

2. Bacterial abundance

Samples（30 mL）for

substrate concentrations after Rath

（1993）

assessment of bacterial abundance were preserved

and from the results of preliminary experiments.

with filtered formaldehyde（2% final concentration）

The samples were incubated for 1 to 3 h at theand stored at 4 ℃ . All samples were analyzed

surface water temperature. Fluorescence waswithin 1 month of collection. Bacterial abundance

measured with a spectrophotometer（RF-5300PC,

was determined by epifluorescence microscopy in

Shimadzu, Kyoto, Japan）at 365 nm excitation and

DAPI-stained samples collected on 0 2-μm black

445 nm emission. The average difference between

Nuclepore filters（Porter and Feig, 1980）. Duplicate

the two replicates was less than 10%. The increase

filters were prepared for each sample, and morein fluorescence was linear with time for incubation

than 400 cells were counted per filter.

times used. Calibration was performed with

3. Bacterial production

Bacterial production was

3

14

standard solutions of 7-amino-4-methylcoumarinestimated from [ H]-thymidine and [ C]-leucine

and 4-methylumbelliferone. The potential maximum

incorporation rates（Chin-Leo and Kirchman, 1988）.

substrate degradation rate（Vmax）was estimatedDuplicate 5-mL water samples were incubated inby the Michaelis-Menten kinetic model（Dowd andthe dark at theRiggs, 1965; Unanue

surface water temperature1999）.

for 30 min with 10 nM [ 3 H]-thymidine and 50

5. Chemical analysis Seawater samples for dissolvednM [ 14 C]-leucine. Duplicate controls killed withorganic carbon （DOC）analysis were passed

formaldehyde（4% final concentration）were run

through pre-combusted（450℃, 4 h）Whatman GF/F

in tandem with every live incubation. Samples

glass-fiber filters. The filtrate was collected directly

were ice-cooled and precipitated by adding 0 5

in muffled glass tubes sealed with Teflon-lined caps,

mL of ice-cold 50% trichloroacetic acid（TCA）forand stored frozen until analysis. DOC concentrations

more than 5 min, then passed through a 0.2-μm

were determined by high-temperature catalytic

membrane filter and washed 3 times with 1mL ofoxidation using a Shimadzu TOC-5000 analyzer.

5% ice-cold TCA. Filters were dissolved in 10mL of

Seawater samples for dissolved organic nitrogena scintillation cocktail（Clear-sol Ⅱ, Nacalai tesque,（DON）analysis were passed through Whatman

Kyoto, Japan）, and radioactivity was read in a liquid

GF/F glass-fiber filters and stored frozen until

scintillation counter（LSC-6101, Aloka, Tokyo Japan）.

analysis. Dissolved nitrogen was determined as total

The average difference between the two replicatesdissolved nitrogen（TDN）, including both DON and

was 11%.

dissolved inorganic nitrogen（DIN）, by catalytic

4. Ectoenzymatic activity

To estimate bacterial

oxidation followed by chemiluminescent detection

Microbial activity and community structure in a net pen aquaculture areaof nitric oxide in a Mitsubishi Kasei Corporation

alchole mixture and purified by ethanol precipitation.

TN-05 analyzer. Ammonium, nitrate, and nitrite

Bacterial 16S-rRNA genes were amplified by PCRconcentrations were determined by standard

using a primer set reported by Muyzer et al.（1993）.

colorimetric techniques（Strickland and Parsons,

The amplified gene fragments were analyzed by

1977）. DON was calculated by subtracting the sum

a denaturant gradient gel electrophoresis methodof nitrate plus nitrite and ammonia from TDN.

（Muyzer1993）. Denaturant concentrations in

For particulate organic carbon and nitrogenthe gel ranged from 30 to 60%. Electrophoresis was（POC and PON）determination, seawater samples

performed at 110V for 16hours in TAE buffer using

were passed through pre-combusted（450 ℃, 4 h）

the D-Code system（BioRad）. The gel was stained

Whatman GF/F glass-fiber filters. The filters wereby ethydiumbromide and its image was recorded

dried at 80 ℃ and kept in a desiccator until analysis.

using a Polaroid camera. Some bands were excised

POC and PON concentrations were determinedfrom the DGGE gel for sequence analysis. DNA

by using a CHN analyzer（EA1110; Thermoquest,

was extracted in distilled water and reamplified.

Milano, Italy）.

Sequence was determined after cloning using the
TA Cloning Kit（Qiagen）.

Particle associated and free-living bacterial
communities and their community structure

Results

Since the level of leucine aminopeptidase activity
was closely correlated with the particulate organic

Bacterial abundance, production and ectoenzymatic

matter concentration, we separated the bacterial

activity

community into two categories, particle-associatedWater temperature and salinity at both stations（>1μm）and free-living（<1μm）, and examined

showed typical seasonal variations, and thetheir abundance, hydrolytic enzyme activities andprofiles at the 2 stations were almost identical.

community structures respectively.

The temperature ranged from 14 2 to 30 0 ℃ and

Water samples were collected at a depth of 0 5

salinity from 25 37 to 34 78 PSU. These parameters

m at Stn A and Stn R monthly from March 2000 to
March 2001. Collected water was filtrated througha nucleopore filter of 1μm pore size with natural
gravity. The filtrated fluid was again filtrated
through a nucleopore filter of 0 2μm pore size.
Bacterial abundance and extracellular hydrolytic
enzyme activity was measured as described above
both in the intact seawater sample and the filtrated
fluid through 1μm pore size filter. The abundanceand enzymatic activity in the filtrated fluid wereregarded as those of free-living bacterial community
and the differences between intact seawater andfiltrated fluid were regarded as those of particle
associated community.
Particles trapped on the filter of 1μm pore size
was regarded as a particle associated community
and that on the filter of 0 2μm pore size wasregarded as a free-living community. Each of thefilters were put into a NET buffer（400 mM NaCl
-20 mM EDTA-50 mM Tris; pH 9.0）and freeze
immediately at −80℃ until further analysis. DNA
was extracted by phenol-chloroform-isoamyl-Fig. 2. Isopleth diagrams of seasonal and spatial
distribution bacterial abundance in aquaculture area
（Stn A）and reference area（Stn R）.

Tomoko SAKAMI, Katsuyuki ABO and Kazufumi TAKAYANAGI
indicated that the water column was stratified ataround 10 m depth in summer（June to September）
and well mixed in winter（October to May）.

cells L −1 at Stn R.
In general, at both stations bacterial production
was high in the surface waters in summer, except in

Bacterial abundance exhibited similar profiles atAugust 2000, and vertically uniform in winter（Fig.

both stations（Fig. 2）. It was high in the surface3）. The thymidine incorporation rates ranged fromwaters in summer （with the exception of June

undetectable（nd）to 144（23 in annual average）

2000）and vertically uniform in winter. Bacterial

pmol L − 1 h − 1 at Stn R and from nd to 436（85 inabundance at Stn A was significantly higher thanannual average）pmol L −1 h −1 at Stn A. The leucinethat at Stn R（p < 0 0001,

incorporation rate ranged from 0 04 to 2（0 64 in）. It ranged from 0 99
9

at Stnannual average）nmol L −1 h −1 at Stn R and from 0.18

A and from 0.51 to 4.5（1.8 in annual average）×109

to 9 2（1 9 in annual average）nmol L −1 h −1 at Stn A.

to 8 4（2 4 in annual average）
×10 cells L−1

Fig. 3. Isopleth diagrams of seasonal and spatial distribution of thymidine and leucine
incorporation rate in aquaculture area（Stn A）and reference area（Stn R）.

Fig. 4. Isopleth diagrams of seasonal and spatial distribution of leucineaminopeptidase and β-glucosidase activity in aquaculture area（Stn A）and referencearea（Stn R）.

Microbial activity and community structure in a net pen aquaculture area
The bacterial production at Stn A was significantly
higher than that at Stn R in both of the parameters（p < 0.0001 in thymidine incorporation rate and
p=0 0003 in leucine incorporation rate,）.

aminopeptidase and p<0 0001 in β-glucosidase,）.
Organic matter concentration at both stations
was shown in Table 1. The concentrations of DOC

The profiles of potential ectoenzymatic activity

and DON were also high in the surface waters inwere similar to those of bacterial abundance andsummer and vertically uniform in winter at bothbacterial production（Fig. 4）. The activities were

stations. DOC concentrations were in the range frommarkedly higher in the surface water in summer,

51 to 116（76 in annual average）μM at Stn R andand were vertically uniform in winter at both

50 to 161（85 in annual average）μM at Stn A. DON

stations. However, high leucine aminopeptidase

concentrations were in the range of 4 7 to 10（7 8 in

activity was observed in the bottom waters inannual average）μM at Stn R and 3 9 to 23（8 6 in

October, just after destratification, at Stn A. Leucine

annual average）μM at Stn A. Both of the DOC andaminopeptidase activity ranged from 1 7 to 165（32

DON concentrations were significantly higher at Stn−1

in annual average）nmol L−1hat Stn R and from−1

13 to 604（74 in annual average）nmol L−1hat StnA than at Stn R（p=0 0002 in DOC and p= 0 0245 in
DON,

）.

A, whereas β-glucosidase activity ranged from nd

The profiles of the POC, PON, and chlorophyll-α

to 9 5（1 8 in annual average）nmol L−1 h−1 at Stn R

concentrations were different between the two−1

and from 0 4 to 37（8 9 in annual average）nmol L

stations. Particulate organic matter concentrations

h−1 at Stn A. Both of the leucine aminopeptidase andwere high in the surface and middle layers in May,β-glucosidase activities at Stn A were significantly

June, and October at Stn R, and high in the surface

higher than those at Stn R（p =0 0004 in leucine

layer in the summer at Stn A. POC concentrations

Table 1. Ranges of values （annual average from June 1999 to May 2000）of
estimated parameters related to microbial activity and organic matter concentrations
in aquaculture area（Stn A）and reference area（Stn R）of Gokasho Bay.（nd-not
detected）

Tomoko SAKAMI, Katsuyuki ABO and Kazufumi TAKAYANAGI

Fig. 5. Seasonal variations in bacterial production and ectoenzymatic activity perunit area in aquaculture area（Stn A; solid symbols）and reference area（Stn R;
open symbols）.

Table 2. Correlation coefficients between microbial activity parameters andenvironmental parameters in aquaculture area（Stn A）and reference area（Stn R）of
Gokasho Bay.（ < 0 05 are shown）

Microbial activity and community structure in a net pen aquaculture area
were in the range of 3 3 to 101 （7 8 in annual

the two stations, the correlation between POC andaverage）μM at Stn R and 7 5 to 117（8 0 in annual

bacterial abundance was significantly stronger at Stn

average）μM at Stn A. PON concentrations wereA than at Stn R. Bacterial production（TdR）werein the range of 0 70 to 14（1 0 in annual average）

significantly negatively correlated with salinity（Sal）

μM at Stn R and 0 86 to 18（1 1 in annual average）

at Stn A but not at Stn R. Leucine aminopeptidase

μM at Stn A. Chlorophyll-α concentrations were in

activity showed a strong positive correlation withthe range of 0 1 to 26（3 7 in annual average）μg

particulate organic matters（POC, PON, and Chl α）,

L−1 at Stn R and 0 20 to 45（4 7 in annual average）

which was significantly greater than that with DOC

μg L

−1

at Stn A. Differences in POC, PON, andat Stn A.

chlorophyll-α concentrations between the stations

Abundance, hydrolytic enzyme activity andwere not significant（p>0 05,

community structure of particle associated and）.

The annual fluctuations of bacterial production

free-living bacterial communities

and ectoenzymatic activity per unit area（water

Bacterial abundance of particle associatedcolumn integrated values）are shown in Figure 5.

community was high in warm water season（Fig. 6）.

All of these microbial parameters showed greater

Percentage of particle associated bacterial number

values at Stn A than at Stn R, especially in lateto the total bacterial abundance was 20% in average,summer/early autumn（August and September）.

indicating that free-living community was a major

Total annual bacterial production was about threepart in view of the abundance. In β-glucosidase

times greater at Stn A than at Stn R in terms ofactivity, percentage of particle associated bacterial

both thymidine and leucine incorporation. Total

community was fluctuated widely but 30% in

annual leucine aminopeptidase activity was about

average, indicating that 70% of the enzyme activity

twice, and that of β-glucosidase was about five

was in the free-living community. On the other handtimes greater at Stn A than at Stn R.

in leucine aminopeptidase, the particle-associatedStatistical analysis indicated that the microbialcommunity was responsible to about 60% of theactivity parameters were positively well correlated

total activity, and the ratio was greater in summer

with organic matter concentrations in the water atwith the exception of August. This fact agrees withboth of the stations, with exception of DON at Stn

the former observation that leucine aminopeptidase

A（Table 2）. Comparing the relationship between

activity was strongly correlated with POM

Fig. 6. Bacterial abundance and hydrolytic enzyme activities in total（gray circle with dotted line）, particle associated（solid circle）, andfree-living（open circle）bacterial communities in surface water inaquaculture area（Stn A）, and percentage of the values of particle
associated community to the total.

Tomoko SAKAMI, Katsuyuki ABO and Kazufumi TAKAYANAGI

Fig. 7. DGGE profiles of the free-living （<1μm）bacterial
community composition over a year in surface water at aquaculturearea and reference area.

Fig. 8. DGGE profiles of the particle associated（>1μm）bacterial
community composition over a year in surface water at aquaculturearea and reference area. Bands marked by star symbols wereidentified as representing the cyanobacteria.

concentration in the seawater.

the samples were loaded on one gel. However, someIn free-living community, the community structure

bands marked by star symbols as #1〜#3 in theshows clear seasonal variation（Fig. 7）. The number

figure were observed only in the aquaculture areaof DGGE bands ranged from 2 to 12. The DGGE

from March to November. From sequence analysis,

profile changed obviously between November andthe band of #1 was identified as representing

December. The DGGE profile in the aquaculture areaalpha subclass of the proteobacteria whose closest

was similar to that in the reference area. We haveidentified relatives was

confirmed that most of the bands were identicalof #2 was as representing gamma subclass of theposition at both stations in the same month when

proteobacteria whose closest identified relatives

sp.. The band

Microbial activity and community structure in a net pen aquaculture area
wassp., and the band of #3 was

as representing

fluctuation of bacterial production in the aquaculturearea and found that the bacterial production wass group whose closest identified relatives wassp.

correlated with organic matter concentrations in thewater（Table 2）and that it was strongly stimulated

In the particle-associated bacterial community,

in late summer/early autumn（Fig. 5）. Yokoyama

the number of DGGE bands was less than in the（2002）has shown seasonal fluctuation of organic

free-living community（Fig. 8）. Most of the bands

carbon and nitrogen load in the form of fish feed

were identified as representing cyanobacteria. In

into fish cages in this study area. It exhibited a

July and September when the particle-associatedsimilar pattern with those of bacterial production

bacterial community had high hydrolytic enzyme

measured in this study. This fact may suggest

activity, the DGGE profiles were different between

that organic matter from fish farms supported

aquaculture area and reference area. The bands

the high bacterial production in the aquaculture

observed specifically in the aquaculture area inarea. We show the annual mean of organic carbon

July were identified as representing thecomponents in seawater measured in this study ingroup （#4）
, andFig. 9. Bacterial cellular carbon and production wasalpha （#5）and gamma （#6）subclass of theestimated using the ordinal conversion factors; 2×proteobacteria. On the other hand, the bands

1018 cells mol−1 thymidine incorporated, and 20 fg C

observed in the reference area （#7, 8）werecell−1（Ducklow and Carlson, 1992）. It shows that

identified as representing cyanobacteria, indicatingorganic matters deposited in the aquaculture areathat bacterial community composition was different

by 9μM as dissolved organic carbon and by 1μfrom that in the aquaculture area.

M as bacterial cellular carbon. Bacterial production
rate stimulated due to aquaculture activity（theDiscussion

difference between both stations）was estimatedto 5μmol C L−1 day−1. This indicates that potential

Bacterial production in the aquaculture area inturn over time of the deposited organic matters in

Gokasho Bay

seawater was about 2 days in this aquaculture area.

In this study, we examined annual

Fig. 9. Mean values of organic matter components in seawater at
the aquaculture area（whole circle area）and at the reference area
（shaded part）, and organic matter input from fish farms.

Tomoko SAKAMI, Katsuyuki ABO and Kazufumi TAKAYANAGIThe Bacterial production rate stimulated due toalthough the bacterial production was much higher

aquaculture activity was also calculated to be 37 molin the aquaculture area. Functions of phytoplankton

−2

Cm

−1

y

as the sum of depth - integrated values ofcommunity must be cleared to understand wholeeach month for a year. It was also estimated to beorganic matter flow in the aquaculture area.

6 3 mol N m−2 y−1 in the aquacultrue area, using theEctoenzymatic activities in the aquaculture area

conversion factors as C to N ratio of 5 9（Fukuda

should be evident that we measured the Vmax , which

1998）. On the other hand, the total amount ofis the estimated maximum enzymatic potential atfish feed added to this aquaculture area in 1998 wasItsaturated substrate concentration, not the direct

estimated as 1494 t of carbon or 238 t of nitrogen

activity. Nevertheless, our values for both of the（Yokoyama H, pers. comm. 2001）. If the loss to theectoenzymatic activities were within the range ofenvironment in the dissolved fraction of fish feed

reported activities in eutrophic estuaries（Karneris assumed to be 58% for carbon（Hallor 48% for nitrogen（Hall

1990）

1992）
, then 867 t, 1992; Rath

1993; Talbot

1998; Patel

1997; Nausch2000）. It should also be notedof carbon and 124 t of nitrogen would have beenthat higher values of leucine aminopeptidase activity,

released into the surrounding water. Considering

ranging from about 1000 to 4000 nmol L−1 h−1 have

2

that the actual fish farming area is 2 km , it iscalculated that 36 mol C or 4 4 mol N m

−2

−1

y

would

been reported with organic matter enrichment
in some mesocosm studies（Chrost and Rai 1993;

have been released into the surrounding water.

Pinhassi

Although these estimations depend heavily

yellowtail aquaculture area（Patelon conversion factors translating thymidine

somewhat lower peaks of leucine aminopeptidase

incorporation rate into bacterial carbon production

activity at the study site（604 nmol L−1 h−1）may（Fukudaindicate a relatively low organic matter burden in1998）and the extents of the area

affected by aquaculture and feed loss, it seems that

1999; Riemann2000）and in a
2000）
. The

this area.

bacterial secondary production was equivalent to the

Seasonal fluctuation of the ratio of β-glucosidase

amount of the organic carbon and nitrogen entering

to leucine aminopeptidase activity was shown in

into the water from fish farming.

Fig. 10. In general, the ratio was always high in the

When the bacterial growth efficiency in theaquaculture area（Stn A）than that in the reference

aquacultrue area was assumed to be 0 43 from delarea（Stn R）. Especially the ratio was high in the

Giorgio and Cole s empirical model（del Giorgio andsurface water at September, October, and theCole, 1998）, the bacterial carbon demand exceededsurface and middle layer water at November when

the carbon input from fish farms. This fact suggests

fish food input was high（Yokoyama, 2002）. These

that primary production by phytoplankton might
have been also accelerated by the high load ofnitrogen and phosphorous from fish farms in thisstudy area. Sakami（2003）has shown from ashort-term observation conducted at the same study
area in summer that the relative bacterial production
to the chlorophyll

concentration was high only inthe deep water in the aquaculture area, but it wasinvariable in surface to middle water comparedwith reference area. It seems that most of organic
matters released from fish farms utilized by bacteria
not directly but after mineralized and reconstructedby phytoplankton. On the other hand, we has
shown in this annual study that the chlorophyll
α concentration in the aquaculture area did not
differ significantly from that in the reference area

Fig. 10. Seasonal variations in ratio of β-glucosidase（β-Glc）to leucine aminopeptidase（AMP）activity
at surface （circle symbols）, middle （triangle
symbols）and bottom （square symbols）waterin aquaculture area（Stn A; solid symbols）andreference area（Stn R; open symbols）.

Microbial activity and community structure in a net pen aquaculture area
results may indicate that aquaculture activity

surface where concentration of organic nitrogenous

have stronger stimulatory effect on β-glucosidase

substrate is high（Karner

activity than on leucine aminopeptidase activity in

1988; Smith

1992; Hoppe

1992; Grossart and Simon,

the aquaculture area. Previous studies have also

1998; Unanue

shown that glucosidase activity is accelerated moreparticle-associated community was responsible

prominently than aminopeptidase activity in somefor only 20% of abundance but 60% of LAP

eutrophic environments（Chrost and Rai 1993; Rathactivity（Fig.6）. In summer when their activity

1993; Sinsabaugh1998）. We also showed that1997）
. On the otherwas very high, we could observe some specifichand, some studies also indicated that the synthesis ofbacteria and their closest identified relatives were

glucosidase and aminopeptidase in aquatic bacteria
is repressed in the presence of low-molecular weightsp.,sp., andsp.

（Fig. 8）. Generally, in thesubstrates, including inorganic nitrogen, directly

group, most isolates have the ability toavailable for bacterial metabolism in concentrations

degrade biomacromolecules, such as protein, nucleic

that do not limit their growth （Chrost, 1990）.

acid, and polysaccharide. Its member is expected

Ammonia is the major excretory product of cultured

to have a high organic matter degrading ability.

fish and it might repress the aquatic microbial

Moreover, beta-subclass proteobacteria groupaminopeptidase activity in the aquaculture area.

includes a majority of culturable marine bacteria,

Moreover, if the β-glucosidase activitiy was relatedsuggesting that this group may adapt to eutrophic

to bacterial carbon requirements, the observation

condition （Giovannoni and Rappe, 2000）. The

that bacterial community in the aquaculture areabacteria observed particularly in the aquaculture

had relatively higher β-glucosidase activity thanarea probably have high organic matter degrading

leucine aminopeptidase activity might suggest thatabilities, which explainin the high hydrolytic enzyme

the bacterial community was under more carbon

activities observed in the aquaculture area.

limit condition than that in the reference area. We

On the other hand, free-living bacterial community

measured β-glucosidase activity to assess bacterial

in the aquaculture area was responsible for 80% of

extracellular hydrolytic activity because β-linked

abundance and 70% of β-Glc activity in averagepolysaccharides are a predominating organic（Fig. 6）
. In this community, some specific species

constituent of DOC pool in an aquatic environment（DGGE bands）were also observed in warm water,（Chrost and Rai, 1993）. On the other hand, a main

namely high activity season（Fig. 7）. The closest

carbohydrate ingredient in fish food is flour, which

identified relatives of them wereis α-linked polysaccharides rich, and β-glucosidase

subclass of proteobacteria）,

activity does not concern its degradation directly.

subclass of proteobacteria）, and

α-Glucosidase activity might promote more in the（alpha（gamma（group）. They also

aquacultrue area than in the case of β-glucosidase.

might have high organic matter degrading ability,

Particle associated and free-living bacterial

especially in β-linked polysaccharides.

community

In conclusion, we examined microbial community

Leucine aminopeptidase activity was strongly

in an aquaculture area and have shown that

correlated with particulate organic matter or

aquaculture activity affects the microbial community

chlorophyll-α concentrations at the aquaculture

in seawater, both quantitatively and qualitatively.

area（Table 2）. The strong relationship between

The examined microbial activities were promoted

aminopeptidase activity and POM concentration

markedly in the aquaculture area and the stimulated

has been reported in several previous studies

bacterial secondary production was estimated to（Middelboe., 1997; Nauschbe equivalent to the organic matter loads from fish., 1995; Talbot, 1998）. It has also been shown that particle

farming. In the organic matter degrading activity,

associated bacterial communities have higher

poly-hydrocarbon degrading activity was promoted

per-cell activity and predominantly degrade themore than protein degrading activity. Frompolymeric nitrogen substances on the particle

community structure study, some specific bacterial

Tomoko SAKAMI, Katsuyuki ABO and Kazufumi TAKAYANAGI
species were observed at high activity season bothPress, New York, 113-181.

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Foy, R.H. and Rosell, R., 1991: Loadings of nitrogen

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水研センター研報，第19号，69−77，平成19年
Bull. Fish. Res. Agen. No. 19, 69‑77, 2007

博士号論文

Effect of effluents from a new fish farming siteon the benthic environment
Takashi TANIGAWA＊1, Azumi YAMASHITA＊1, and Yoshitsugu KOIZUMI＊2

Abstract : In relation to improvement of the environment around fish (red seabream andyellowtail) farms in Shitaba Bay, Uwajima, Ehime Prefecture (Japan), about half of fish cages
were shifted from the inside (ca. 20-50 m depth) to the outside (60 m depth) of the bay during May-November 2001. The spatio-temporal variability of the benthic environment at the
newly established fish farm site was investigated, by analyzing the sediments at both thenew (outside) and the old (inside) farm sites before and after the shift of fish cages. For example, the organic matter load from the new farm was measured to determine the assimilative capacity of the benthic ecosystem.
Acid volatile sulfides (AVS-S) of sediment at the center of the new farm were 0.03 mg/g
dry weight in February 2001 without fish cages. As soon as the fish cages were set, AVS-S
drastically increased (0.11 mg/g dry weight in July) and reached 0.26 mg/g dry weight inNovember when the fish cage shift had been completed. Moreover, AVS-S continued to increase and reached its maximum (0.46 mg/g dry weight) in April 2002. However, it remainedat ca. 0.3-0.4 mg/g dry weight thereafter. Although AVS-S increased also at the edges andsurrounding areas of the new site, concentrations were lower than those at its center. AVS-S
increased slightly at areas over 50 m distance from the edges. Total phosphorus (TP) was
about 2 times higher in the old farm site than that of the new farm site, while no marked
differences of total organic carbon (TOC) and total nitrogen (TN) were detected between thetwo sites. TN and TP of sediment at the new farm site were slightly higher than concentrations observed in a pearl farm and a non-farming site (as reference sites).
From data on the amount of feed sold, production and feeding amount to cultured fish forsome cages, about 50% (5,000 ton in dry weight) of the total amount of feeds sold by the fisheries cooperative association was consumed in the new farm site in 2002. These feeds may
be reflected in the TOC, TN and TP flux caught using sediment traps set at 5 m depth above
the bottom, which were equivalent to or more than the concentrations at the old farm site.
Thus, it was suggested that the AVS-S increase was largely due to effluent of organic
matter (uneaten food and fecal) from fish farming activities closely linked with the shift offish cages, and that the effect of the loaded organic matter on the benthic ecosystem was
low in areas more than 50 m away from fish farming site.
Key words : New fish farming site, Organic matter lord, Benthic environment, AVS-S, TP
Recently, the impacts of coastal aquaculture

aquaculture for evaluating the effects of newlyon the environment become serious problems,

established fish farm sites on the benthic

and attentions on environmentally sustainable

environments. However, few studies have beenaquaculture production are increasing at local,

made so far on this subject in Japan.

national and international levels. So it is necessary

In 2001, new fish farming site was established out

to clarify the load processes of effluents fromof Shitaba bay, Uwajima, Ehime, for ensuring and2006年 月26日受理（Received. June 26, 2006）＊1
Ehime Prefectural Fisheries Experimental Station 5516 Shitaba, Uwajima, Ehime, Japan, 798-0104＊2
Ehime Prefecture Uwajima Regional Office 7-1 Tenjin, Uwajima, Ehime, Japan, 798-8511

Takashi TANIGAWA, Azumi YAMASHITA, and Yoshitsugu KOIZUMI
promoting sustainable production of cultured fishfor the analysis of acid volatile sulfide（AVS-S）.

by avoidance of environmental impact on a limited

Surface layer（0-1 cm）of AVS-S in sediment wasarea. And also, it was estimated that organic mattermeasured with a H 2 S absorbent columns（GASTEC,

lord would reduce inside the bay but the benthic

Kanagawa, Japan）.Sediment were collected monthly

environment would change at outside of the bay

at the stn. 1, 17 and 18 from February 2001 to

by increase of organic matter lord. It was expected

September 2003 and at the other stations, February,

to work out the environmental control plan of fish

July, September, November in 2001, January, May,

farming site, from quantitative relationship between

July, September, November in 2002 and February,organic matter lord and pollution in fish farming site

May, August in 2003.

by investigation of this process of change in detail.

Total organic carbon（TOC）, total nitrogen（TN）

So, the spatio-temporal variability in organicand total phosphorus（TP）contents in sedimentmatters loaded from the new fish farm site waswere analyzed. Sediment samples were obtained ininvestigated, by the analysis of sediments andthe same way with AVS-S in August and September

settling flux at both the new and the old farming

2002, at the 5 stations in the new site and 2 stations

sites before and after the shift of fish cages.

in the old site. And 2 stations in pearl farming site
（Stn. 19, 20）and 1 station outside of the farm sites
as a reference site（Stn. 21）were added. Sediments

Materials and Methods

were dried in 60 ℃ until it became constant weight
Shitaba bay is located at western coast ofand sieved with 0.25 mm mesh. After removal of

Shikoku Island, Uwajima and characterized bycarbonate with HCl（1N）, TOC and TN contents

the intermittent inflows of warm water from thewere measured with CN coder. TP contents inKuroshio and cold water from the shelf slope

sediment was measured with the following method.

（Takeoka and Yoshimura, 1988; Hashimoto

,

1995）
.

The sediment samples were autoclaved for an hour
in a closed bottle with 4% potassium peroxodisulfate

Fish farming in this bay started in 1960 s, andat first, yellowtail

was thesolution. The filtrate through GF/F was measured
with auto analyzer（BRAN + LUEBBE, Germany）.

farming fish. Then aquaculture in this bay became

And also, settling flux of particulate matter was

more active and now beside yellowtail, red seabreammeasured with sediment traps （type Montani :and pearl oyster

Montani, 1988）set at 5 m above the bottom.

are the common fish farmed here.

At 1 station in the new site（Stn. 16）, 1 station in

Before the shift of cages, all of them were situatedthe old site（Stn. 17）and 1 station in the pearl site

inside the bay, about 20 to 50 m depth and total（Stn. 20）from April 2002 to January 2003 almost

area of cages were about 43,000 m 2 , maximum

monthly. Traps were set in the water during 24

in regulation. After the shift, about half of cages

hrs, then taken to the laboratory and settling flux

（21,600 m2）were set to the new site, which has aof particulate matter was collected on GF/F filter

depth of about 60 m and other cages（21,382 m2）

which was combusted in 450 ℃ during 2 hrs. The

were remained inside the bay, and rearranged.

filters were dried in 60 ℃ until it became constant

Sampling and data analysis
The changes in benthic environment were

weight, then weighed. On a part of samples, TOC,
TN, TP contents were measured with the same
method as the sediment samples.

investigated at 21 stations in and around of theFeeds consumed to the new and old fish farm

new fish farming site, the old fish farming site andsite in 2001 and 2002 were calculated from the feed

pearl oyster farming site（Fig. 1）. Stn. 6 to 10 weresold data of fishermenʼs cooperative association,

located about 50 m, and stn. 11 to 15 were locatedstock number of farming fish and feeding amount toabout 200 m from edges of the new site.

cultured fish for some cages. The monthly amount of

At the 20 stations among them, sediment
samples were obtained using gravity core sampler,

feeds to the each sites were calculated from below
method.

Effect from a new fish farming site to the environment

Fig. 1. Map showing sampling stations and farming sites. Stations were shown with following simbols by
investigated parametersthere.
● : AVS, TOC, TN, TP and settling flux.
▲ : AVS, TOC, TN and TP■ : AVS◇ : Settling flux
Xn=A ×Σ（Bij × Cij）/（Σ（Bij × Cij）
+ Σ（Bij ×

Cij: Regulation maximum number of fish per cageDij））

decided by fishermenʼs cooperative association ×

Xo=A ×Σ（Bij × Dij）/（Σ（Bij × Cij）
+ Σ（Bij ×

number of cages by fish kind and age in the new

Dij））fish farming site in September 2002.

Xn: Monthly amount of feeds consumed in the newi, yellow tail, red seabreamfish farming site.

j, age0, age1+

Xo: Monthly amount of feeds consumed in the old

Dij: Regulationary maximum number of fish per

fish farming site.

cage decided by fishermenʼs cooperative association

A: Monthly amount of feeds sold by the fishermenʼs

× number of cages by fish kind and age in the oldcooperative association. It was converted to dry

fish farming site in September 2002.

weight.

i, yellow tail, red seabream

Bij: Monthly feeds consumption by fish kind andj, age0, age1+

age per thousand fish, from some cages. They were

The shift of cages was carried out from May toconverted to dry weight.（Yellow tail was cultured

November in 2001 and it was assumed the cages

from 2000 to 2002 and red seabream was cultured

were shifted in a fixed pace for this period. And thefrom 2001 to 2003）

feeds to the new site were calculated by multiplying

i, yellow tail, red seabream

below number to the monthly feeds with abovej, age0, age1+

method.

Takashi TANIGAWA, Azumi YAMASHITA, and Yoshitsugu KOIZUMI
Mn/7

Feeds to the new and old fish farming site were

Mn = progress months number from April（fromestimated for 2001 and 2002.

Amount of feeds

Jan. to Apr. is 0 ; Nov. and Dec. is 7 ）sold by fishermenʼs cooperative association wereFeeds consumed in the old site for this period

8,742 dry ton in 2001 and 9,776 dry ton in 2002. But

were calcultated taking feeds to the new site fromin 2001, when the shift of cages was carried out,

monthly feed sold data.

there is no data for exactly number of fish cages
for calculation of organic matter lord. Monthly

Results
Organic matter lords and AVS-S

feed consumption in the both fish farming sites
became minimum in April, then increased until
September, and it became almost constant until

Fig. 2 shows the change in AVS-S content ofDecember, thereafter. This quantitative change of

sediment at the newly established fish farming

feeds shows similar tendency every year. Moreover,site and surrounding areas from February 2001

it was estimated about 5,000 ton in dry weight ofto December 2003. At the center of the new site

feeds were consumed in the new site in 2002 after（Stn.1）, AVS-S content was 0.03 mg/g dry weightthe completion of the shift, this number was nealy

in February 2001 when there was no fish cages.

equal to the it in the old site in this year. EstimatedAs soon as the fish cages were set in May, AVS-S

organic matter lords to the new fish farming site

drastically increased and it reached 0.26 mg/g dry

were gradualy increased from May to November

weight in November when the fish cage shift hadin 2001 and AVS-S at Stn. 1 also increased in the

been completed. Moreover, AVS-S continued tosimilar way of feeds consumption（Fig.3）.

increase and topped in 0.46 mg/g dry weight in

Fig. 4 shows a comparison of AVS-S between the

April 2002 and after that, it kept about 0.3-0.4 mg/g

center of the new fish farming site and the old site.

dry weight until August 2003. AVS-S contents

In the old site AVS-S content was about 0.3-0.5 mg/g

increased in the similar way at the edges anddry weight before the shift of cages. Even thoughsurrounding areas of the new site. But the contents

after the shift, AVS-S content remained constant for

were lower than the center.

about 3 years in the similar value, it didnʼt decrease.

Fig. 2. Change of AVS-S in and around new fish farming site out of Shitaba bay: Stn. 1（Center of new fish farming site）: Average of Stns. 2-5（Edges of new fish farming site）: Average of Stns. 6-10（50m away from the edge of new fish farming site）: Average of Stns. 11-15（200m away from the edge of new fish farming site）

Effect from a new fish farming site to the environment

Fig. 3. Change in feeds used to new and former fish farming sites in 2001
Value were converted to dry weight for each site per month.
: Feeds used to new fish farming site per month: Feeds used to former fish farming site per month: Monthly change of AVS-S at Stn. 1

Fig. 4. Change of AVS-S in new and former fish farming sites from january
2001 to August in 2003
: Stn. 1（Center of new fish farming site）: Average of Stns. 17 and 18

Takashi TANIGAWA, Azumi YAMASHITA, and Yoshitsugu KOIZUMI
shows TP content among them. TP content in the
TOC, TN and TP content in sediment and settling

settling flux was 91-263 mg/m2/day in the new fish

flux

farming site. It increased from April to October,

TOC, TN and TP content in sediment have been

similarly to the trend of feeds amount. In the old fishused for the indicators of artificial effect to benthic

farming site, TP content in the settling flux topped

environment similarly to AVS-S. TOC content was

in 299 mg/m2/day in December, but it varied widely

14.1-14.5 mg/g dry weight in the new fish farming

compared to the new site. And also, the TP content

site, 12.2 mg/g dry weight in the pearl farming site,

in the settling flux in the new site was higher than

13.5 mg/g dry weight in the non-farming site andin the old site, except for December. On the other15.1 mg/g dry weight in the old fish farming site

hand, TP content in the settling flux in the pearl（Fig. 5）. TN content was 1.7-1.8 mg/g dry weightoyster farming site was lower compared to both fishin the new site, 1.5 mg/g dry weight in the pearl

farming sites, except for May and June. And it wassite, 1.5 mg/g dry weight in the non-farming site

12-50 mg/m2/day for the investigation period. TP

and 2.0 mg/g dry weight in the old site. TP content

was higher in the both fish farming sites than thewas 0.6-0.7 mg/g dry weight in the new site, 0.5

pearl oyster farming site.

mg/g dry weight in the pearl farming site, 0.5 mg/g

Fig. 7 shows the change of TP content in sediment

dry weight in the non-farming site and 1.5 mg/g

in the old fish, new fish and pearl oyster farming

dry weight in the old site. TP was about two times

sites from February 2001 to February in 2003. In thehigher in the old site than the new site. Although,old site, though sediment TP was remarkably higher

TOC and TN content were slightly higher in the oldthan the other sites in all investigations, it continued

site, no marked differences were detected between

to decrease from July 2001. At first, there was no

all the sites. In contrast, TP content is remarkably

difference between stations in and around the newhigh in only the old site.

fish farming site, but at the center of new site, it

The settling flux of TOC, TN and TP wasincreased slightly, in contrast to the other stations.

measured from April 2002 to January 2003. Fig. 6

Fig. 5. TOC, TN and TP concentrations in sediment in new fish, former
fish and pearl oyster farming sites.
Vertical lines indicate the standard deviations. Samples were collectedin August and September in 2002

Effect from a new fish farming site to the environment

Fig. 6. TP concentration in settling flux to bottom in new fish, former
fish and pearl oyster farming sites.

Fig. 7. Change of TP concentrations in sediment from February 2001 to
February 2003
: Stn. 1（Center of new fish farming site）: Average of Stns. 2-5（Edges of new fish farming site）: Average of Stns. 17 and 18（Former fish farming site）: Average of Stns. 19 and 20（Pearl oyster farming site）

Takashi TANIGAWA, Azumi YAMASHITA, and Yoshitsugu KOIZUMIOn the other hand, rise of AVS-S were recognized
Discussion

at the edge of the new fish farming site but at thestations from the edge more than 50m, the rise was

It is necessary to keep balance between organic

slight. It was indicated that the effect to benthic

matter lord and itʼs decomposition for sustainable

environment from fish farming cages was limited

production of aquaculture. So, the environment

within 50m from the cages（Kubota, 1977）. Thisof fish farming site should be monitored withagree with the investigation of the new fish farm

appropriate method. Until now, many indicatorssite of Shitaba bay.

were proposed to evaluate the impact of aquaculture

Before this investigation, it was expected thaton the environment （Yokoyama, 2000）. Amongthe sediment AVS-S would decrease in the old site

them, AVS-S is one of the most common parameter,

after the shift. The effect of shift of fish cages onused to many investigations in Japan, from itʼsthe benthic environment has not been found yet.

easiness to measure and unnecessary expensive

As mentioned above, the effect from the new fish

tools（ex. Tsutsumi and Inoue, 1995; Pawar

farming site was limited within about 50 m. In this2001; Yokoyama, 2002 etc.）. On the other hand,investigation, the stations in the old fish farming

most of these investigations were carried out in thesite were situated just under the fish cages, it

old fish farming sites established many years ago,

was thought that there was not major change ofthere was not so much examples of investigations oforganic matter lord from cages. For the estimation

AVS-S against to increasing of organic matter lordof removal of fish cages from inside the bay, it isby establishment of new fish farming site. And it

needed to continue the investigations added otherwas insufficient to clarify quantitative relationshipstations far from fish cages more than 50 m.

between organic matter lord and change of benthic

Not only AVS-S but also TOC, TN and TP

environment. So, it was expected to establish thecontents are often used for the indicators of benthic

method to control benthic environment in andenvironment. There were not large difference aboutaround fish farming sites, by examination of AVS-S

TOC and TN contents in the sediment between theand organic matter lord in 2001.

new and the old fish farming sites. But, only TP

The shift of fish farming cages to the new fishcontent in sediment among these three parameters

farming site was carried out from May to November

was always 2 times higher in the old site than that

2001. AVS-S in the new site were very low beforeof the new site in this investigation. Though, thethe shift of fish farming cages, but AVS-S drasticallyamounts of the feeds consumed in the new and theincreased at the same time with the start of shift ofold sites were nearly equal in 2002.

cages to the new site. This rise of AVS-S in the new

To clarify the reason for this difference, thesite suggest increase of organic matter lord withsettling flux of particulate was measured, near thethe shift of cages. Usually in this investigation area,bottom in the new, old and pearl oyster farming

fish seeds for aquaculture were introduced in Springsite. TP content in the settling flux was higher inand begun to take from the next Autumn. In thethe both fish farm sites than that of the pearl oyster

new site, it seems that organic matter lord increased

farm site. But TP content in the settling flux in thedue to shift of fish cages, rise of feed consumption

new site was higher than in the old site, except

with growth and high water temperature more thanfor one month. This result show that though the19.6 ℃ from May to September in 2001. Artificial

sediment TP in the old site was quit high compareorganic matter lord to the new site increased fromto the other sites, the settling flux of TP in the new

0 to the level shown in Fig. 3 in November in 2001,

and old sites are almost equal or higher in the newwhen cageʼs shift was completed. It was obviously

site.

that AVS-S increased consistently with increasing

The main material of fish feeds is fish meal,

feeds used from April to November. This result

including large amount of phosphorus derived

indicates that AVS-S of sediment is one of the mostfrom fish bones（Satoh, 2003）. Decomposition of

appropriate indicators.

phosphorus derived from fish bone would occur

Effect from a new fish farming site to the environment
slowly, so they would remain in the sediment for a619-627.

long time. Most of it is the poor solubility（Satoh,

Satoh S., 2003: Minerals, in Micronutrients and health2003）, and the possibility of the storage to theof cultured fish（ed. by Nakagawa H. and Satosediment has been indicated. So, it was estimatedM.）, Koseisha Koseikaku, Tokyo, pp22-30.（Inthat the TP concentration of sediment will keep

Japanese）

increasing in the new fish farming site during thefish culture was continued.

Takeoka, H. and Yoshimura T., 1988: The Kyucho in
44, 6-16.

Uwajima bay.

AVS-S in sediment is an appropriate indicator

Tsutsumi H. and Inoue. T.,1996: Benthic environment

for monitoring the quick response of the benthic

and macrobenthic communities in a cove withenvironment to the organic matter lords fromorganically enriched bottom sediment due tofish farming. The response of the sediment TP

fish farming for two decades.

concentration to the influent from fish farm is quite

50,39-49.（In Japanese with English abstract）

slow compared to AVS-S. So, TP in sediment is an

Yokoyama H., 2000: Environmental quality criteria

appropriate indicator of long time influent from fish

for aquaculture farms in japanese coastal

farming.

areas -a new policy and its potential problems-.
29, 123-134.（InJapanese with English abstract）

References

Yokoyama H., 2002: Impact of fish and pearl farming
Hashimoto T., Matsuda O., Takeoka H., Yamamotoon the benthic environments in Gokasho bay:

T. and Yokozeki K., 1995 : Shelf slope upwelling

Evaluation from sesonal fluctuations of theof high nutrient bottom water in the Bungo

macrobenthos.

34, 161-165.

channel.

Kubota T., 1977: Fish farming site, in Shallow water

Acknowledgements

aquaculture and self pollution（ed. by Nippon
Suisan Gakkai）, Koseisha Koseikaku, Tokyo,
pp9-18.（In Japanese）

We are gratefully acknowledges Dr. Kazumasa
Hirakawa, Hokkaido National Fisheries ResearchMontani S., Tada K. and Okaichi T.,1988: Purine andpyrimidine bases in marine particles in the Seto
Inland Sea.

68, 258-268.

25, 359-371.

Institute Fisheries Research Agency, for his many
helpful comments.
We are grateful to Dr. Yuichi Hayami, Center

Pawar V., Matsuda O., Yamamoto T., Hashimoto T.
and Rajendran N.,2001: Spatial and temporal

for Marine Environmental Studies（CMES）, Ehime
University, for his comments and suggestion.

variations of sediment quality in and around

The research presented in this paper was madefish cage farms: A case study of aquaculture inpossible by grant from the Japanese Fisheries

the Seto Inland Sea, Japan.

67,

Agency.

水研センター研報，第19号，79−87，平成19年
Bull. Fish. Res. Agen. No. 19, 79‑87, 2007

Assimilative capacity of fish farm environments as determined by
the benthic oxygen uptake rate: Studies using a numerical model
Katsuyuki ABO * and Hisashi YOKOYAMA *Abstract : In order to promote improvements in the environmental quality of aquaculture
grounds, the Japanese government enacted the Law to Ensure Sustainable Aquaculture
Production in 1999. In the Basic Guidelines for this law, an environmental criterion basedon the benthic oxygen uptake (BOU) rate was adopted to assess the quality of aquaculture
environments. Biological mineralization is considered to peak when the BOU rate reaches its
maximum, which is an indicator of the maximum desirable level of organic matter loading.
The acid volatile sulfide (AVS-S) content of the sediment increases in direct correlation tothe organic matter loading, and is used as an indicator of the assimilative capacity of bottom
sediments. The AVS-S value corresponding to organic matter loading when the BOU rate is
at its maximum is defined as the standard value. Recent studies, however, have suggested
that it is difficult to detect the maximum (peak) BOU and to determine the standard value
through in situ investigations. The practical applicability of this criterion therefore needs tobe re-examined scientifically. To do this, we developed a three-dimensional numerical modelthat takes into account advection, dispersion, sedimentation, and decomposition of organic
matter from fish farming systems. The numerical model should be used instead of in situ
investigations for the practical application of the criterion. We also used this model to assess
the assimilative capacity of an existing fish farm on the basis of the criterion. The model
proved to be an effective tool for evaluating the assimilative capacity of the environment offish farms.
Keywords: environmental criteria, fish farm, numerical simulation, Law to Ensure Sustainable Aquaculture Production

Introduction

environmental quality of aquaculture grounds. In the

Supported by the development of production

so-called Basic Guidelines for this law, environmental

techniques and by economic growth, Japan has

criteria and indicators were adopted to identify

succeeded in increasing its aquaculture production,

healthy farms and critical farms (those not being

while the total amount of fishery products has

managed sustainably). These criteria and indicators

been decreasing for the last 10 consecutive years.

should now be revised, however, on the basis of

Aquaculture, however, has had a large impact

more recent data (Yokoyama, 2003). Specifically,on the environment. In particular, overstocking

sediment sulfide content, which was adopted as anof aquaculture pens has caused environmental

indicator of the benthic oxygen uptake (BOU) rate,

deterioration such as eutrophication, hypoxia, andis difficult to apply (Yokoyama, 2000; Yokoyama

occurrences of noxious red tide.

and Sakami, 2002). The practical applicability of this

The Japanese government enacted theLawcriterion needs to be re-examined. We therefore

to Ensure Sustainable Aquaculture Production

developed a numerical model to examine thein 1999 in order to promote improvements in thepractical application of the criterion and studied the

2006年 月26日受理（Received. June 26, 2006）*National Research Institute of Aquaculture 224-1 Nakatsuhama-ura, Minamiise, Mie 516-0193, Japan E-mail: abo@fra.affrc.go.jp

Katsuyuki ABO and Hisashi YOKOYAMA
assimilative capacity of fish farms.

in the feed may be lost to the environment in asalmonid farm using artificial feed.

Environmental impact of fish farms
Fish farms discharge large amounts of organic
matter into the environment. Comparison of the

The Law to Ensure Sustainable Aquaculture
Production

ratio of the distribution of feed to wastage, fish

To improve the environmental quality ofgrowth, and excretion and feces shows consistently

aquaculture grounds and maintain suitablehigh discharge rates for different species and feed

conditions for stable aquaculture production, thetypes and varying assessment measures (Table 1).

Law to Ensure Sustainable Aquaculture Production

Based on an assessment of nitrogen content, it has(hereinafter referred to as the Law) was enacted inbeen estimated that 80% of the feed inputs to fish

1999. As a fundamental guide for putting the Law

farms is discharged out of the culture cages: 20% in

into practice, the Minister of Agriculture, Forestry,

the form of feed wastage, and 60% in the form of fishand Fisheries produced the “Basic Guidelines toexcretion and feces production (Itoh, 1994). On the

Ensure Sustainable Aquaculture Production , whichbasis of protein content, Yamaguchi (1978) estimateddetailed matters relevant to the goal of improving

the ratio in fish farms that rear red sea breams. He

aquacultural practices. The Law stipulates that

estimated that 20% of the feed is discharged into

fisheries cooperative associations should enact an

the environment directly as feed wastage and that

Aquaculture Ground Improvement Program

60% of the feed is discharged as excretion and feces.

so as to ensure sustainable aquaculture, and also

Watanabe (1991) studied the distribution of feed insecure the approval of the prefectural governor. The

fish farms that rear yellowtails based on dry matter

Basic Guidelines contain environmental criteria tocontent. He showed that in fish farms that feedmeasure the environmental condition of aquaculture

moist pellets a total of 74% of the feed is discharged

grounds. The criteria utilize three indicators: theinto the environment, 19% as feed wastage anddissolved oxygen content of the water within fish

55% as excretion and feces, while in fish farms thatcages, the condition of macrofauna beneath the fish

use raw fish, 85% of the feed is discharged, withcages, and the sulfide content (acid volatile sulfide,

feed wastage accounting for 72% and excretion and

AVS-S) of the sediment beneath the cages (Table

feces for 13%. Bergheim et al. (1991) estimated that2). The criteria serve to identify healthy and criticalin salmonid farms that feed dry pellets, 75% of thefarms; farm environments are identified as healthy

feed is discharged: 10% as feed wastage and 65%

or critical based on the values measured for theseas excretion and feces. According to Wu (1995),

indicators, relative to established thresholds.

eventually some 80-84% C, 52-95% N, and 82% P

Dissolved oxygen is an important factor for

Table 1. Comparison of the ratios of the distribution of feed to wastage, fish growth, andexcretion and feces in fish farms, for different species and feed types and varying assessment
methods.

Assimilative capacity of fish farms as determined by BOU
Table 2. Environmental criteria adopted in the Basic Guidelines for the Law to Ensure Sustainable
Aquaculture Production.

maintaining the life of cultured organisms. The

content to identify healthy farms.

criteria established 4.0 ml/L and 2.5 ml/L of
dissolved oxygen as thresholds for identifying

Assimilative capacity based on benthic oxygen

healthy and critical farms, respectively. Macrofauna

uptake rate

have often been used as a sensitive indicator

The use of sulfide content as an indicator considers

to assess fish farms environments (Yokoyama,

the capacity of bottom sediments to assimilate2002). The criteria used in the Basic Guidelines

organic wastes, and it is based on the relationshiponly specify that the benthos beneath the culture

between the organic matter loading and the BOU

cages should be alive. The farm environments arerate in the bottom water. An increase in the organic

identified as healthy when macrobenthos occur

matter loading to the sea bottom is accompanied bythroughout the year, and they are identified as

an increase in the aerobic degradation of organic

critical when azoic conditions occur for more thanmatter in the sediment. Increases in organic matter6 months in a year. Sulfide content (AVS-S) levels

loading also lead to a decrease in dissolved oxygen

are used as an indicator of the assimilative capacity

content, however, causing benthic conditions toof bottom sediments. The threshold AVS-S level

become anaerobic, at which point the BOU rate

for healthy farms is determined by reference tobegins to decrease. Consequently, organic matterthe BOU rate; the threshold for critical farms is >loading should be limited to the level at which

2.5 mg/g dry sediment. Using a simple numericalthe BOU rate is at its maximum, because thismodel, Omori et al. (1994) found a peak in the BOU

corresponds to the point at which the greatest

rate which they took to be an indicator of the level

biological re-mineralization of organic matter takesof organic matter loading that would result in theplace (Fig. 1). There is a positive correlation between

maximum rate of re-mineralization. Takeoka andthe organic matter loading and sulfide content in the

Omori (1996) proposed a method to determine thesediment, and thus the AVS-S level that corresponds

assimilative capacity of fish farm environments byto the BOU maximum is used as an indicator of theusing the sulfide content as an indicator, because

assimilative capacity of fish farms, and to determine

sulfide content is positively correlated with organic

which are healthy.

matter loading. In the criteria, farm environments

There are problems in applying this criterion toare identified as healthy when AVS-S is less thanexisting aquaculture farms. Recent studies havethe AVS-S value at the point where the BOU ratesuggested that it is difficult to detect the maximum

is maximized. The concept of using sulfide content(peak) BOU and to determine the standard AVS-S

as an indicator to identify healthy farms is unique,value through in situ investigations (Yokoyama andbut there are problems in its practical application,

Sakami, 2002; Yokoyama, 2003; Abo and Yokoyama,

as described below. In the following section, we2003). In order to determine the standard AVS-S

examine the practical use of the indicator of sulfide

value of the criterion, it is necessary to detectKatsuyuki ABO and Hisashi YOKOYAMA

Fig. 1. Acceptable limits for organic matter loading fromfish farms, and the relationship to benthic oxygen uptake andsediment sulfide content (adapted from Takeoka and Omori,1996).

the maximum value of the BOU rate relativeis possible, however to utilize a numerical model toto the organic matter loading rate from a farm.

determine the standard value. By using a numerical

Theoretically, we have to investigate the BOU

model, we can simulate benthic quality when therate when the level of organic matter loading isorganic matter loading rate is changed in a farm.

changed, but this is almost impossible to do in an

The BOU rate can then be calculated as a function

existing farm. In addition, it takes many years toof variations in the organic matter loading rate,

investigate, even if the organic matter loading isand the maximum and standard values for sulfide

altered. Consequently, it is almost impossible tocontent estimated.

determine the standard BOU value by this method.
Another method involves investigating the BOU

Numerical model

rate in several farming areas whose topography

The numerical model to estimate the maximum

and hydrodynamic conditions are very similar, andBOU rate and determine the standard AVS-S value

detecting the maximum among the similar farming

defined in the criteria used in the Basic Guidelines

areas. Many researchers have carried out these infor the Law deals with three spatial dimensions,situ investigations in Japan; however, they wereand considers advection, dispersion, sedimentation,

unable to detect the maximum because BOU rates

and degradation of organic matter loading from fish

are very sensitive to changes in oxygen supply,

farms (Fig. 2). We first calculate water movements

induced by water exchange. It is also impossible tousing a multi-level density primitive flow model.

select a sufficient number of farming areas whose

The flow model divides the area into meshes,

topography and hydrodynamic conditions areand solves the fundamental equations obtained

similar enough to enable detection of the maximum.

by integrating the equations within the meshes.

Moreover, some researchers intend to detect theSecondly, we calculate advection and diffusion of

maximum by measuring BOU rates at many points

dissolved oxygen, and advection and diffusion of

in one fishing area. This approach is unsound,organic matter loadings from fish farms, including

however, because the BOU rate depends largely on

their sedimentation (Fig. 2b). We also calculate theoxygen flux, which varies significantly within a shortaerobic and anaerobic degradation of the organic

distance in a farming area (Abo and Yokoyama,

matter. In this model we express the flow of organic2003).

matter very simply (Fig. 2c). Organic matter loading

These problems suggest that we cannot determine

from fish farms sinks at some sedimentation rate,

the standard value through in situ investigations. It

and organic matter in the water column degrades

Assimilative capacity of fish farms as determined by BOU

Fig. 2.

Schematic views of the three-dimensional numerical model. (a) Multi-level stratified flow model.

(b) Advection and diffusion of organic matter and dissolved oxygen. (c) Flow chart of the sedimentation,oxidation and anoxic decomposition of organic matter.

aerobically. Once organic matter accumulates

tons of fish are produced annually. We divided theon the bottom, it degrades both aerobically and

Gokasho Bay area into meshes of 100 m2 and 5 manaerobically. Reduced substances derived from

depth, and identified some meshes as fish farming

anaerobic degradation of organic matter consume

sites (Fig. 4). Organic matter is assumed to be loaded

oxygen through chemical oxidation.

into the surface layers from fish farming site meshes.

The relational equations and parameters used

With this geometry, we simulated changes in thewere according to Omori et al. (1994). Using this

BOU rate relative to the organic matter loading rate

model, we calculated approximate stationary

from the fish farming sites.

solutions under the given conditions.

First, we calculated movement of organic matter

Assessment of the assimilative capacity ofloaded from fish farming sites when the organic

aquaculture environment in Gokasho Bay

matter loading rate was equal to the real value for

We examined application of the numerical model

the existing farms in Gokasho Bay. The organic

to assess the existing aquaculture environment

matter content of the sediment and the BOU rate

in Gokasho Bay. Gokasho Bay is located on thewere compared for Gokasho Bay (Fig. 5), with asouthern coast of central Japan facing the Pacificunit of organic matter content given as an oxygen

Ocean (Fig. 3). This bay is a typical semi-enclosed

equivalent ( μmolO2/cm3). Organic matter from fish

estuary consisting of three branches: the main inlet,

farms accumulated mainly on the sea bottom near

the Hasama-ura inlet, and a third branch. Fish farms

the fish farming sites. The BOU rate was high nearare concentrated in Hasama-ura inlet. In this bay

the shore of Hasama-ura inlet because of the large

aquaculture is prosperous and about 1000 metric

oxygen supply at the sea surface; the dissolved

Katsuyuki ABO and Hisashi YOKOYAMA
oxygen concentration in the bottom water of thematter loading rate, with the maximum BOU rateshallow area was consequently high. Other thanoccurring when the organic matter loading rate wasin the shallow area, the BOU rate was high at the

3 μmolO2/cm2/day. This value was an allowable

outer side of the fish farming area (at the mouth oforganic matter loading rate maximum for farming

Hasama-ura inlet), where there was high organicsite 1, with the aquaculture environment of farming

matter loading and a large supply of oxygen. The

site 1 regarded as healthy when the organic matter

BOU rate was low at the inner side of the fishloading rate was within 3 μmolO 2/cm 2/day. In

farming area, where the oxygen supply was very

farming sites 5, 7, and 11, the BOU rate reached its

small due to oxygen depletion.

maximum when the organic loading rate was 10, 25,

Next, we simulated the BOU rate when theand 95 μmolO2/cm2/day, respectively; these values

organic matter loading was changed, in orderwere taken as the allowable organic matter loading

to estimate the maximum BOU rate at each fishrate maximums for each farming site. These values

farming site (Fig. 6). The organic matter loading rate

are plotted and contour lines drawn showing thewas represented as a unit of oxygen equivalent oforganic matter loading rate limits in Gokasho Bay

2

feed fed per day ( μmolO2/cm /day), and the organic(Fig. 7). The values are high at the mouth of thematter loading rate to the sea surface was assumed

Hasama-ura inlet and very low at the innermost

to be the same at each farming site. At farming

part of the inlet. The limit values increase sharply

site 1, the BOU rate varied relative to the organic

towards the mouth of the inlet. As the actual organic

Fig. 3. Map of Gokasho Bay. Solid areas denote fish farming sites.

Assimilative capacity of fish farms as determined by BOU

Fig. 4.
1-24.

The model geometry of Gokasho Bay. Squares with crosses indicate fish farming sites

Fig. 5. Distribution of organic matter content in (a) sediment and (b) benthic oxygen uptake rate, calculatedby the numerical model.

Katsuyuki ABO and Hisashi YOKOYAMA

Fig. 6.

The relationships between the benthic oxygen uptake rate andorganic matter loading rate at fish farming sites 1, 5, 7, and 11 (see Fig. 4), as
calculated by the numerical model.

Fig. 7.

Isopleths of the limit values of the organic matterloading rate（ μmolO2/cm2/day）in Gokasho Bay, estimatedby the numerical model.

Assimilative capacity of fish farms as determined by BOU
matter loading rate in each mesh of the farming sites

and C. Y. Cho (Eds). Nutritional strategies andis estimated at about 20 μmolO2/cm2/day, there isaquaculture waste. Proceedings of the firstsufficient capacity for aquaculture at the mouth ofinternational symposium on nutrient strategies

the inlet. However, the capacity is very small at thein management of aquaculture waste. University

inner part of the inlet, where it is one-tenth of theof Guelph, Ontario, Canada, 1990. 275p.

capacity at the inlet mouth.

Itoh, K. 1994. Environment of mariculture field andConclusion

Omori, K., T. Hirano, and H. Takeoka. 1994. The

its problems. Yoshoku, 3, 33-36 (in Japanese).
The numerical model is an effective tool for

limitations to organic loading on a bottom of aassessing the limit of organic matter loading

coastal ecosystem. Mar. Pollut. Bull. 28, 73‑80.

from fish farms for ensuring healthy aquaculture

Takeoka, H. and K. Omori. 1996. Methods ofenvironments, on the basis of the environmental

determining the limit of suitable fish culture

criterion adopted in the Basic Guidelines for thebased on the oxygen consumption rate by the

Law to Ensure Sustainable Aquaculture Production.

sediment. Bull. Jpn. Soc. Fish. Oceanogra. 60,

Before the model can be practically applied

45‑53 (in Japanese with English abstract).

to determine the standard sulfide value of the

Watanabe, T., 1991. Past and present approaches

criterion, the model needs to be reexamined andto aquaculture waste management in Japan.

the parameters defining the aquaculture ecosystem137-154. In: C.B. Cowey and C. Y. Cho (Eds).

refined. We will also attempt to carry out an in situ

Nutritional strategies and aquaculture waste.

investigation of the benthic quality of a fish farming

Proceedings of the first international symposium

area to refine the model for practical application.

on nutrient strategies in management of

To improve aquaculture environments withthe goal of sustainable aquaculture production,aquaculture waste. University of Guelph,
Ontario, Canada, 1990. 275p.

we should ensure that production levels are

Wu, R. S. S. 1995. The environmental impact ofwithin an area s capacity; infection caused bymarine fish culture: Towards a sustainable

overstocking can be addressed through reduction

future. Mar. Pollut. Bull. 31, 159‑166.

in production or rearrangement of aquaculture

Yamaguchi, M. 1978. Basis and practice of seabreampens within an aquaculture area. The model canfarms. Kouseisha-Kouseikaku, Tokyo, 414p. (inserve as an effective tool for suggesting appropriate

Japanese).

spatiotemporal use of aquaculture grounds.

Yokoyama H. 2000. Environmental quality criteria
for aquaculture farms in Japanese coastal areas

References- a new policy and its potential problems. Bull.
Nat. Res. Inst. Aquacult. 20, 123‑134 (in JapaneseAbo, K. and H. Yokoyama. 2003. Examination of thewith English abstract).

environmental criterion for mariculture based

Yokoyama H. 2003. Environmental quality criteria

on benthic oxygen uptake rate and an attempt

for fish farms in Japan. Aquaculture 226, 45-56.

to evaluate assimilative capacity, by using a

Yokoyama H. and T. Sakami 2002. Examination

three dimensional numerical model. Bull. Jpn.

of the benthic oxygen uptake rate as an

Soc. Fish. Oceanogra. 67, 99‑110 (in Japanesewith English abstract).
Bergheim, A., J. P. Aabel, and E. A. Seymour. 1991.
Past and present approaches to aquaculture
waste management in Norwegian net pen
culture operations, 117‑136. In: C.B. Cowey

environmental criterion for fish farms in
Gokasho Bay. Nippon Suisan Gakkaishi 68,
11‑19 (in Japanese with English abstract).

水研センター研報，第19号，89−96，平成19年
Bull. Fish. Res. Agen. No. 19, 89‑96, 2007

博士号論文

Macrobenthos, current velocity and topographic factors as indicators toassess the assimilative capacity of fish farms: Proposal of two indices
Hisashi YOKOYAMA＊1, Misa INOUE＊2, and Katsuyuki ABO＊1

Abstract In order to provide site selection guidelines for fish farming, two indices havebeen previously proposed based on surveys of the macrobenthos and bottom environments
conducted at fish farms in Kumano-nada, central Japan. In this review, these results are
summarized, and requisites for determining the limit of maximum fish production are discussed from a standpoint of assimilative capacity of fish-farm environments. An index ED（Embayment Degree）is calculated from the distance from a bay mouth to a fish-farm site,
the width of the bay, the water depth of the site and the maximum depth at the bay mouth.
Another index, ISL （Index of Suitable Location）is calculated from the water depth andcurrent velocity under a fish cage. Current velocities can be estimated by plaster balls readily and simultaneously at many stations. Biotic and abiotic factors at the fish farms were
found to be changed along gradients of fish production and ED or ISL, suggesting that these
indices are effective for estimating the assimilative capacity. ED can be used as a simple indicator for the site selection. ISL has a wider potential application to assess the assimilative
capacity under a variety of topographical conditions.
KEY WORDS: Fish farm, Assimilative capacity, Current velocity, Environmental criteria,
Plaster ball

The macrobenthos community has often been
Introductionused as a sensitive indicator for environmental
monitoring of organically polluted areas（reviewed

Intensive net-pen fish farming generates large

by Pearson and Rosenberg, 1978）. Assessments ofamounts of uneaten food and fish feces. Thesefish-farm environments using the macrobenthos

particulate organic wastes generally settle on thehave also been conducted in many countries of theseabed near to the cages. When the accumulationworld. These studies have shown that a reductionof wastes exceeds the assimilative capacity ofin species richness and/or species diversity; athe water body, negative effects on the benthic

decrease in the number of large-sized species; theecosystem such as impoverished infauna anddisappearance of echinoderms; and the appearance

outgassing of hydrogen sulfide often occur（reviewedof dense populations of the opportunistic polychaete

by Gowen., 1991; Pearson and Black, 2001）. To

Capitella species （especially species Ⅰ）, which

maintain sustainable aquaculture, it is necessaryoften result in an increase in the total macrofaunal

to assess farm environments objectively, andabundance, are typical effects of mariculture farming

to conduct cultivation within the range of theon the macrobenthos（reviewed by Gowen

assimilative capacity, which is defined as the ability

1991; Pearson and Black, 2001）.

of an area to maintain a healthy environment andaccommodate wastes（Fernandes., 2001）.

In Japan, the.,Law to Ensure Sustainable

Aquaculture Production （hereinafter referred

2006年 月26日受理（Received. June 26, 2006）＊1
National Research Institute of Aquaculture, Fisheries Research Agency, Minami-Ise, Mie 516-0193, Japan＊2
Mie Prefecture Kihoku Branch Office, Department of Agriculture, Fisheries, Commerce and Industry, Owase, Mie 519-3695, Japan

Hisashi YOKOYAMA, Misa INOUE, Katsuyuki ABO
to as

the Law ）was established in 1999 todetermined for each individual farm. From this pointpromote the improvement of aquaculture grounds.

of view, the Law determined another environmental

Based on the Law, environmental criteria for

criterion as acid-volatile sulfide（AVS）should beindicating practical goals for the improvement ofless than the maximum value of benthic oxygen

aquacultural environments were established. In one

uptake（BOU）at each fish farm . However, it isof these criteria, the macrobenthos was used asdifficult to specify the maximum BOU value froma bio-indicator for identifying healthy and criticalthe field survey（see Abo and Yokoyama, 2006 inenvironments of mariculture farms. This criterion,

this volume）.

however, only specifies that the macrobenthos

In order to assess the assimilative capacity ofshould be alive. A healthy environment is identified

fish-farm environments, and to provide site selectionin terms of the existence of live macrofauna

guidelines, surveys of the bottom environments

throughout the year, while a critical environment isand macrobenthos were conducted in fish farms

identified from azoic conditions during half a year orin Kumano-nada, Pacific coast of central Japan

more. This criterion has limited ecological relevance,（Yokoyama

however it was pushed through as the criterion

these results are summarized, and requisites

is considered convenient in terms of the ease offor determining the limit of the maximum fish

monitoring by farmers themselves. For the future, aproduction are discussed from a standpoint of themore detailed criterion should be established based

assimilative capacity.

. 2002a, b, 2004）. In this review,on scientific data.
Index incorporating topographic factors

Under aerobic conditions, organic wastes fromaquaculture are liable to be incorporated by benthic
animals directly or indirectly through the microbial

Yokoyama. （2 0 0 2 a , b ） c o n d u c t e d afood chain. Increased benthic animals acceleratequantitative survey of the macrobenthos in August

the oxygenation process of the sediment by theirand September 1998 at 22 fish farms distributed

bioturbation activities. Benthic animals may be fed

in ten small bays along the coast of Kumano-nada,

on by predators, resulting in increase of consumer

central Japan, in order to assess the environmental

populations in higher trophic levels.

impacts of fish-farm wastes under a variety of

The remineralization of loaded organic wastes

topographic conditions and to suggest site selection

by benthic animals begins originally from supply ofguidelines for sustainable fish farms. In this area,oxygen, which is controlled by the water flow and/or

fish farming has developed steadily since thewater exchange between the fish-farm grounds andintroduction of yellowtail（the surrounding water. Increased current velocities

culture in the early 1960 s. Since the middle of the

not only increase the oxygen supply（Jørgensen

1970 s, a total of 15 000‑20 000 metric tons of fish

and Revsbech, 1985; Findlay and Watling, 1997）but

has been annually produced mainly of red sea breamalso reduce the loading of particulate organic wastes（

per unit area of the seabed due to waste dispersion

production of each farm in this area ranged from 61（Gowen and Bradbury, 1987; Chamberlain

to 1 507 metric tons（Tokai Regional Agricultural

.,

2001）
. Lumb（1989）demonstrated the importanceof avoiding sites with low water movement for））and yellowtail. In 1998, annual fish

Administration Office, 1999）.
Yokoyama（2002a）devised an index ED

reducing the risk of environmental deterioration.

（Embayment Degree）of the topographic situation

Water depth under fish cages also potentially hasof a sampling site. When a fish farm is located ina great effect on the waste dispersion（Gowen anda secondary bay whose axis crosses the axis of

Bradbury, 1987; Hevia

the main bay at an angle of <90ﾟ（Fig. 1）, ED is., 1996）.

As the assimilative capacity is different fromexpressed by ED =（ 1 /

1

+ 2/

2

（ /
）

（ /
）

）
,

farm to farm depending on the physical components

where

1 is the distance from the mouth of the mainsuch as the topography and the current velocity,

bay to the mouth of the secondary bay,

the maximum limit of fish production should be

distance from the mouth of the secondary bay to the2is theAssimilative capacity indices of fish farms>30 species/0 04 m 2, respectively. On the other
hand, deterioration of the sediment quality（AVS,>1 mg S/g dry）, deoxygenation of the bottom water（DO, <2 mg/l）and decreases in biomass（<1 g/m2）,
density（<500 individuals/m2）and species richness（<5 species/0 04m2）were often found in the innerand shallower parts of the bay （ED, >5）. Thistendency was more conspicuous in large-scale farms（fish production, >1 000 t/yr）than in small-scale
farms（<500 t/yr）. These findings suggest thatvariability of the macrobenthos and environmental
factors are attributable to the topography aswell as to the aquacultural activities, and that
topography is the important factor in the location ofenvironmentally efficient fish farms.
Fig. 1. Parameters for the calculation of ED（after
Yokoyama
2002a）.

Yokoyama. （2002b）also examined thespecies composition of the macrobenthos as anindicator of fish farm environments. They found
six assemblages（A‑F）in August‑September 1998

fish-farm site,

1is the width of the main bay,is the width of the secondary bay,2

at the fish farms in Kumano-nada by the cluster

is the water

analysis. These assemblages could be classified into

depth at a sampling site or, if present, the depth of

three groups, i.e., a group characteristic of a healthy

any sill which exists between the site and the bayzone（A‑D）, a group characteristic of a cautionary

mouth,

zone（E）, and an azoic group characteristic of ais the maximum depth at the bay mouth,is the mean depth of all the sampling sites, andcritical zone（F）, based on the macrofauna andis the mean depth of the bay mouths in the study

chemical factors of the bottom water and thearea. Yokoyama

sediment. These assemblages were placed in a.（2002a）adopted= 20, and= 45 in their case study conducted in Kumano-nada.

gradient of ED versus fish production（Fig. 2）. Fig.

When a fish farm is located in a secondary bay

2 suggests that all levels of fish production（<1 500

whose axis crosses the axis of the main bay at ant/yr）could be sustained in areas where ED is <3angle of >90ﾟ, ED is expressed simply by ED =
（ /

（ /
）

（ /
）

）
, whereis the distance fromthe mouth of the main bay to the fish-farm site, andis the width of the main bay.
Environmental deterioration does not occur inthe deeper offshore areas in Kumano-nada withED values <2, even if a high production（>1 000t/yr）of fish is maintained. In fact, within the
deeper offshore areas, DO（dissolved oxygen）was
usually more than 5 mg/l, and AVS（acid-volatilesulfide）was usually less than 0 6 mg S/g, even for
medium- and large-scale farms（fish production,>500 t/yr）. Such an undisturbed condition and anenhanced food supply from the fish cages resulted
in large macrofaunal biomasses, high densities
and high species richness, which were generally
encountered >10 g/m2, >2 000 individuals/m2 andFig. 2. Distribution of the six assemblages（A‑F）
in a gradient of ED versus fish production（after
Yokoyama et al., 2002b）.

Hisashi YOKOYAMA, Misa INOUE, Katsuyuki ABO
and smallest-scale fish production（<200 t/yr）could

Yokoyama.（2004）conducted a survey of thepossibly be conducted in areas where ED is <10,

water flow to examine whether the current velocity

but medium- and large-scale production should be

and water depth in fish farms can be used aslimited to areas where ED is <5. A fish farm withindicators for site selection guidelines. They proved

large-scale production（e.g., 1 400 t/yr）and locatedthat plaster balls（plaster of Paris : water = 100 gin the critical zone（e.g., ED = 6）should be shifted: 70 ml）can be used as a convenient and effective

to an area with ED values <4 or annual production

tool for measuring the time-averaged current

should be reduced to <600 t to alleviate the criticalvelocity. They revised the method for the calculation

conditions.

of the time-averaged intensity of water motion that

Many mathematical models have been developed

was presented by Komatsu and Kawai（1992）andto predict benthic impacts and responses to organic

Komatsu（1992）.Yokoyama

enrichment associated with fish farming（reviewed

equation,by Henderson., 2001）. Most of them recognizedthat the current flow is a key factor in predicting thedispersion and input of organic wastes to the seabed（e.g. Hevia

（

v＝

−

−

0

−

.（2004）showed the（284−4 03 ）−0 048 −0 27）, 1996; Findlay and Watling, 1997）.

ED is an index based on the same concept as thosewhere v is the time averaged current velocity

adopted in the previous modeling studies, which（cm/s）,

demonstrated that dispersive environments areball including an iron bolt before setting on theless susceptible to environmental degradation thanseabed,semi-enclosed systems, but a novel aspect is that theincluding the iron bolt after being retrieved fromindex is readily applicable for use in decisions about

the seabed,the siting of fish farms. Factors such as the inflow ofis the average water temperature（℃）during the

freshwater into the bay, the current outside the bay,

immersion period, and0is the wet weight （g）of a plasteris the wet weight（g）of the plaster ballis the weight（g）of the iron bolt,
is the immersion period

and wind velocity and direction, which may varyin 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 fordeveloping site selection guidelines.
Index incorporating the current velocity and water
depth
ED is an index based on topographic factors
only, and has proved helpful to develop guidelines
for siting fish farms within the Kumano-nada area,
however, it is unknown whether this index isapplicable to other localities exhibiting different tidal
ranges or different bay sizes. The current flow andwater depth are the most important factors that
control directly the waste dispersal and loading.
These factors are essential to assess the assimilative
capacity of fish-farm environments.

Fig. 3. Distribution of the three assemblage groups
in a gradient of ISL versus fish production（adaptedfrom Yokoyama
2004）. Symbols represent thegroup characteristic of the healthy zone（○）, thegroup characteristic of the cautionary zone（■）,
and the group characteristic of the critical zone（×）,
respectively.

Assimilative capacity indices of fish farms（hours）. Plaster balls（diameter = 48 mm）, whichwastes, the value obtained by multiplying

were fixed on a stand using a bolt and nuts, werei.e.,

put 1 0 m above the seabed at 20 stations in 8 fish

the water body.

2

by

,

will represent the assimilative capacity offarms in Gokasho Bay and Owase Bay for about 50

Three zones of fish-farm environments, i.e.,hours at the same time during neap- and spring-tide

healthy, cautionary and critical zones, which had

periods in September 2003.

been defined on the basis of the macrofauna andYokoyama.（2004）devised an index ISL（Index of Suitable Location）. ISL is expressed as
ISL =

2

chemical factors（Yokoyama., 2002b）, were also

arranged in a grid of ISL versus fish production（Fig.

, whereis the water depth（m）at a3）. The healthy zone was located at areas having

fish-farm site andis the time-averaged current

large ISL values, whereas the critical zone wasvelocity（m/s）. The mathematical derivation of thelocated at areas having small ISL values and highindex is as follows: the loading rate of organic wastes

levels of fish production.

to the seabed has an inverse relationship to; as

the current velocity maintains the oxygen supply
that serves to remineralize the loaded organic

Field data on biotic and abiotic factors that havebeen obtained from the same stations（Yokoyama., 2002a）were used to validate ISL（Fig. 4）.Values

Fig. 4. Distribution of values of six abiotic（A‑F）and three biotic（G‑I）factors in a gradientof ISL versus fish production（after Yokoyama., 2004）. Dark, gray, and white areas
show critical, cautionary, and healthy zones, respectively（defined in Fig. 3）.（A）Dissolved
oxygen of the bottom water,（B）total organic carbon in the sediment,（C）total nitrogen in thesediment,（D）total phosphorus in the sediment,（E）chemical oxygen demand of the sediment,（F）acid-volatile sulfides in the sediment,（G）biomass of the macrobenthos,（H）density of themacrobenthos, and（I）number of species of the macrobenthos.

Hisashi YOKOYAMA, Misa INOUE, Katsuyuki ABO
Table 1. Values of benthic components for identifying cautionary and critical conditions offish-farm environments（adapted from Yokoyama. 2004）
Benthic components

Cautionary condition

Critical condition

Total organic carbon（mg C/g dry）

20−30

> 30

Total nitrogen（mg N/g dry）

2.5−4.0> 4.0

Total phosphorus（mg P/g dry）

4−6

>6

Chemical oxygen demand（mg/g dry）

30−75

> 75

Acid-volatile sulfide（mg S/g dry）

0.5−1.5> 1.5

Biomass ＊（g/m2）

< 10

0

Density（individuals/m2）< 15000

Number of species（/0.04 m2）

< 20

0

Sediment

Macrobenthos＊

Wet weight of animals excluding the shell of mollusks.

of biotic and abiotic factors changed along a gradientsediment and community parameters（Table 1）areof ISL versus annual fish production. As ISL values

useable as environmental quality standards, however

decreased and fish-production levels increased,further verification in other localities is necessary.

values of DO of the bottom water decreased, valuesof sediment total organic carbon （TOC）, total

Comparison between ED and ISL

nitrogen（TN）, total phosphorus（TP）, chemical
oxygen demand（COD）and AVS increased, andED and ISL were proposed based on the concept

values of biomass, density and number of species ofthat assimilative capacity of fish-farm environments

the macrobenthos decreased. These findings suggest

is determined by waste dispersal and oxygen supply.

that environmental conditions are predictable in

It was hypothesized that waste dispersal and oxygen

gradients of ISL and fish production, and that ISL

supply are influenced by topographic conditions

is an effective indicator in the assessments of the（ED）and by water depth and current velocity（ISL）.

assimilative capacity and the upper limit of fish

Surveys of the macrobenthos and environmental

production. For instance, at farms showing ISL offactors conducted at the fish farms in Kumano-nada

0 05, it is recommended to restrict fish production

indicate that both indices are indicative of thewithin 500 t/yr, while at farms having ISL of 0 1,

assimilative capacity of environments. ED is easy

allowable production may increase to 1 000 t/yr（Fig.

to calculate from a nautical chart, and is effective

3）.

for comparison of the suitability for fish farming

Since benthic impacts are integrated over time,

between neighboring areas that are located underchemical factors of the sediment and community

similar oceanographic conditions. However, toparameters of the macrobenthos are convenientcompare fish farms in a variety of topographic

for environmental monitoring. Threshold values

situations under different oceanographic and/orof these factors and parameters that classify

geographic conditions this index may be lessfish-farm environments into healthy, cautionary andsuitable. ISL incorporates factors of the water

critical conditions can be roughly estimated from

depth and current velocity, which are more directa comparison of Fig. 3 with Fig. 4. These values ofvariables that control waste dispersal and loadingAssimilative capacity indices of fish farms（Gowen and Bradbury, 1987; Chamberlain,2001）and oxygen supply（Jørgensen and Revsbech,

ecological impact of salmonid farming in coastal
waters: a review.
, 25, 563 575.

1985; Findlay and Watling, 1997）. ISL has a wider
potential application to assess the suitability of fish

Gowen, R. J., Weston, D. P., and Ervik, A., 1991:

farms under a variety of topographical conditions

Aquaculture and the benthic environment:

as a simple and effective tool for locating suitablea review. in

culture sites in coastal areas.

Aquaculture Waste （eds. by C. B. Cowey and

The plaster-ball technique was successfully used
to estimate the current velocity at the fish farms in
Kumano-nada（Yokoyama

Nutritional Strategies and

C. Y. Cho）, Fish Nutrition Research Laboratory,
University of Guelph, Guelph, pp. 187 205.

., 2004）. However, aHenderson, A., Gamito, S., Karakassis, I., Pederson,

series of checks and calibrations by a current meter

P., and Smaal, A., 2001: Use of hydrodynamic

may be necessary before use in other localities,

and benthic models for managing environmental

because this method needs to be used with caution

impacts of marine aquaculture.

in different flow environments（Porter, 17, 163 172.

., 2000）.

Advantages of using plaster balls are that the device

Hevia, M., Rosenthal, H., and Gowen, R. J., 1996:

is easy to construct with readily available materials

Modelling benthic deposition under fish cages.
, 12, 71 74.

at a low price and that fish farmers can measure thecurrent velocity readily and simultaneously at many

Jørgensen, B. B., and Revsbech, N. P., 1985: Diffusive

stations. The use of plaster balls will be an effective

boundary layers and the oxygen uptake

and pragmatic approach to estimate the assimilativeof sediments and detritus.
, 30, 111 122.

capacity of the water body, and to decide thesuitable location for fish farming.

Komatsu, T., 1992: Improvement of the method
for measuring time averaged intensity ofReferences

water motion by plaster balls, and examples, 24,

of its application.
Abo, K., and Yokoyama, H., 2006: The assimilative

503‑511.（In Japanese）

capacity of the fish-farm environments based on

Komatsu, T., and Kawai, H., 1992: Measurements

the benthic oxygen uptake rate: Examination byof time-averaged intensity of water motion

using a numerical model.

with plaster balls.

, 19, 79‑87.

, 48,

353‑365.

Chamberlain, J., Fernandes, T. F., Read, P., Nickell, T.
D., and Davies, I. M., 2001: Impacts of biodeposits
from suspended mussel （Lumb, C. M., 1989: Self-pollution by Scottish salmon, 20, 375 379.

farms?

L.）

Pearson, T. H., and Black, K. D., 2001: The

culture on the surrounding surficial sediments.

environmental impacts of marine fish cage

, 58, 411 416.
Fernandes, T. F., Eleftheriou, A., Ackefors, H.,
Eleftheriou, M., Ervik, A., Sanchez-Mata, A.,culture. inEnvironmental impacts ofaquaculture （ed. by K. D. Black）, Sheffield
Academic Press, Sheffield, pp. 1 31.

Scanlon, T., White, P., Cochrane, S., Pearson, T. H.,

Pearson, T.H., and Rosenberg, R., 1978: Macrobenthic

and Read, P. A., 2001: The scientific principles

succession in relation to organic enrichment

underlying the monitoring of the environmental

and pollution of the marine environment.

impacts of aquaculture.
, 17, 181 193.

, 16, 229 311.

Findlay, R. H., and Watling, L., 1997: Prediction ofPorter, E. T., Sanford, L. P., and Suttles, S. E., 2000:

benthic impact for salmon net-pens based on the

Gypsum dissolution is not a universal integrator

balance of benthic oxygen supply and demand.

of water motion .

, 155, 147 157.
Gowen, R. J., and Bradbury, N. B., 1987: The,

45, 145 158.
Tokai Regional Agricultural Administration Office,Hisashi YOKOYAMA, Misa INOUE, Katsuyuki ABO
1999: Statistical Report of Fisheries Classified

Yokoyama, H., Nishimura, A., and Inoue, M.,

by Cooperative Associations in Mie Prefecture

2002b: Evaluation of fish farm environments（1998）. Mie Statistics Association of Agriculture

by identifying community types of theand Forestry, Tsu, 62 pp.（In Japanese）

macrobenthos.
, 66, 142‑147. （InYokoyama, H., Nishimura, A., and Inoue, M., 2002a:
Influence of aquaculture and topographic

Japanese with English abstract）

conditions on the macrobenthos and the

Yokoyama, H., Inoue, M., and Abo K., 2004:

sediment in fish farms along the Kumano-nada

Estimation of the assimilative capacity ofcoast.

fish-farm environments based on the current, 66, 133‑141.（In Japanese withEnglish abstract）

velocity measured by plaster balls.
240, 233 247.

,

水研センター研報，第19号，97−111，平成19年
Bull. Fish. Res. Agen. No. 19, 97‑111, 2007

博士号論文

Ecosystem-based management and models insustainable management of coastal aquaculture
＊1

＊2

＊3

＊4

Mac Rawson , Changsheng Chen , DaoRu Wang , Charles Yarish ,＊5＊6

Jim Sullivan , Lu Wang , and MingYuan Zhu＊7

Abstract To be successful, the complex process of ecosystem-based management requires
management tools that can integrate physical, chemical and biological processes, modeling
tool must function at multiple scales, be easily understood by non-scientist and above all reliably predict management alternatives. It must address specific questions about bays, lagoons
or coastal oceans without the ability to predict the cumulative consequences to large marine
ecosystems.
This presentation discusses the concept of ecosystem modeling and focuses on two examples representing small and medium scale semi-enclosed marine ecosystems using a modified
coastal ocean circulation model（Blumberg and Mellor 1987）. Xincun Lagoon in southeast
Hainan Island is a 21 97km2（ 〜 6km X 〜 4km）lagoon with a maximum depth of 10 6m
and a 120m-wide outlet to the South China Sea. Xincun City, a major fishing port of 〜15 000
people, is on one shore of the lagoon and the other shore is a wildlife reserve. The adjacentlagoon experienced a dramatic growth up to 230ha of fish pen aquaculture in 1996 followed
by a catastrophic decline. The natural circulation in the lagoon combined with increased
oxygen demand that was created by the fish pens was the likely reason for the disaster.
Reducing the number of fish pens（33ha）and the advent of a pearl and macroalgae culture
resulted in a more sustainable aquaculture industry and environment. Data indicated thatthe surface water quality did not violate China s National Water Quality Standards, but thepens were responsible for an estimated 5 000 tonnes of organic pollutants. Fish pens reduced
bottom water and sediment quality. Low quality bottom water also flowed in and out of fish
pen area with the tide because of the slow turnover time（up to 90 days）. Further analysis
indicated that macroalgae culture on racks and seagrasses act nutrient scrubbers and could
play an important role by reducing ecosystem risk of less desirable algal blooms（Rawson,. 2002）.
The medium scale modeling experiment was conducted on Jiaozhou Bay that is a shallow
bay of 〜 400km2 with an average depth of 7m and maximum of 50m. The adjacent city is
Qingdao, which is one of China s largest ports and has a population > 2 million people. During the period of this study the bay cotained three areas of scallop aquaculture pens. Simulation experiments with two-pen stocking densities（12 individual m − 3 and 24 individualsm −3）indicated that scallops dramatically decreased the concentration of phytoplankton in
the culture areas. However, the impact that scallop culture had on nutrient concentrations
was small（Chen,
1999）.
A new management model system has been developed with funding from the Georgia Sea
2006年 月26日受理（Received. June 26, 2006）＊1
Georgia Sea Grant College Program, The University of Georgia, Marine Sciences Bldg., Rm 205, Athens, GA 30602-3636, mrawson@uga.edu＊2School for Marine Science and Technology, University of Massachusetts-Dartmouth, New Bedford, MA 02742,＊3
Hainan Marine Development, Planning and Design Institute, 10th Yiyuan Bldg. No. 69, Haifu Rd., Haikou City, Hainan 570203, P.R. China,＊4
University of Connecticut, Department of Ecology and Evolutionary Biology, 1 University Place, Stamford, CT 06901-2315, USA,
＊5
Gray s Reef National Marine Sanctuary, 10 Ocean Science Cir, Savannah, GA 31411, USA,
＊6
Haikou Municipal Government, #19 Lonkun North Rd., Haikou City, Hainan 5701145, P.R. China, and＊7
The First Institute of Oceanography, State Oceanic Institute, P.O. Box 98, Qingdao 266003, P.R. China

Mac Rawson, Changsheng Chen, DaoRu Wang, Charles Yarish, Jim Sullivan, Lu Wang, and MingYuan Zhu

Grant Program based on the unstructured grid, finite-volume coastal ocean model（Chen, 2003）. This system provides a powerful management tool that allows aquaculture to be
integrated into the broader context of coastal and large marine ecosystem management. Fed
aquaculture does create pollution, but aquaculture is rarely the only pollution source. We
must address the issue of aquaculture s contribution to pollution and find practical solutions
to these complex problems.

solutions developed that integrate carrying capacity
Introduction

into the broader concept of ecosystem management.
Polyculture is one approach to reducing impacts ofFor ecosystem-based management to be successful,aquaculture and potentially increasing the carrying

there must be management tools that integrate thecapacity of a body of water. Polyculture can utilize

physical, chemical and biological processes. Until

both fed and extractive aquaculture to increase

recently managers relied on broad science-based

the total productivity. Extractive aquaculture,

regulations and personal knowledge and experience

particularly macroalgae and molluscan shellfish, canto make judgments about the ecosystem impacts ofhelp reduce nutrients and sequester other pollutants

particular human activities on natural systems. It（Yarish,. 2004）.

was the only way to integrate information into an

This presentation will discuss the concept of

ecosystem approach to management. This, however,ecosystem modeling using a modified coastal ocean

leaves managers vulnerable to criticism by politicalcirculation model （Blumberg and Mellor 1987）

leaders and the broader public community who

and focus on two examples representing small andmay not agree with their decisions. Managers needmedium scale semi-enclosed marine ecosystems -the credibility of a scientific tool that integrates the

Xincun Lagoon, Hainan Province and Jiaozhou Bay,knowledge of ecosystem processes and the impacts

Shandong Province, P. R. China.

of human activities to guide and to verify theirdecisions. The output of this scientific tool must

Xincun Bay Example

be easily grasped by non-scientists and above all it
must reliably predict the impacts. The tool also musta. Physical Descriptionfunction at multiple scales. It must address specific

Xincun Lagoon in southeast Hainan Island isquestions about bays, lagoons or coastal oceansa 21 97km 2 （〜 6km X 〜 4km）gourd-shaped

without losing the ability to predict the cumulative

lagoon with a maximum depth of 10 6m and 120m

consequences of numerous small and medium scalewide outlet to the South China Sea. Xincun City,

activities on large marine ecosystems.

a major fishing port of 〜 15 000 people is on one

New modeling technologies provide powerfulshore of lagoon and the other shore is a wildlife

management tools that allow us to integrate

reserve （Figure 1）. Aquaculture in the lagoon

aquaculture into the broader context of coastal andexperienced a dramatic growth in the 1990s,

large marine ecosystem management. Aquaculture

primarily in fish pens. By 1995, fish pens coveredcannot be managed outside the context of integrated

200ha and by 1996 there were up to 230ha of fishcoastal management. Aquaculture is only one ofpens over much of the central and outlet region

numerous human activities that add nutrients,of the lagoon. The fish cages used in Xincun Bay

organic matter and other pollutants, including someare 3m×3m, and are submerged to a depth of 1

types of aquaculture（fish pens）. The aquaculture

to 4m. The shrimp culture industry also thrived

industry cannot escape the fact that it createsand reached a maximum of 100ha ponds in upper

pollution, but it is rarely the only pollution source.

reaches of the lagoon. The shrimp ponds were not

The issue of aquaculture s contribution to pollution

in the lagoon but their effluent was discharged into

should be addressed forthrightly and practical

it resulting in greater eutrophication. In the 1996,

Ecosystem-based management and models in sustainable management of coastal aquaculture

Fig. 1. Map of Xincun Bay with sampling locations

Fig. 2. Histogram of aquaculture area in 90 s of Xincun Bay
catastrophic eutrophication of the lagoon occurred

other hand increased by >150% and reach 133ha inand the water quality declined dramatically, The1999（Figure 2）.

resulting fish kills caused great economic loss andAs part of the Sino-US Marine Resources Panelthe aquaculture industry collapsed. During 1996, fishcooperative program, two field studies of the

pen aquaculture in the lagoon was less than 10% of

lagoon were conducted from July 31 to August

the coverage at its peak. An area of 20ha near the

6, 2000. Standard parameters measured included

mouth of the lagoon. In 1998 the industry diversified

temperature, salinity, COD, DO, DO% saturation,

and added pearl oysters （193ha）and seaweeds

Ph, current speed and direction, turbidity, and tidal（52ha）. Knowingly or not, the industry has created alevel. Primary productivity, nutrients and bacteria

lagoon-wide polyculture system. Pearl oyster culturecommunities also were measured. The study results

apparently was not as successful and the coverage

and existing data from earlier sampling was used

was reduced to 85ha. Seaweeds（macroalgae）on theto create a hydrodynamic model of the lagoon at

Mac Rawson, Changsheng Chen, DaoRu Wang, Charles Yarish, Jim Sullivan, Lu Wang, and MingYuan Zhu
The University of Georgia by visiting scientists

This slow exchange rate means that there is a low

from the Hainan Marine Development, Planning andcapacity to transport pollutants out of the lagoon s

Design Research Institute.（Unless otherwise statedecosystem. The pollutant sources, particular the fishreferences for Xincun Lagoon are excerpted frompens, contribute high levels of organic material from

Rawsonthe residual ground fish feed, fish respiration and2002.）

Analysis of water level data showed that the

fecal wastes. An estimated 5 000 tonnes per year inlagoon has an irregular diurnal tide with a relatively

organic waste were contributed from the fish pens,

small average range of 69cm with a maximum ofcompared to an estimated 500 tonnes from Xincun

1 55m, which resulted in a slow tidal current velocity.

City.

There was a large range in surface velocity, from
2cm s−1 to 155cm s−1. The highest surface velocity

b. Water Quality and Sediment Assessment

was at Station 1 in the 120 m-wide-mouth during

Water quality and sediment survey results are

the spring ebb tide period. During neap tide, theshown in Table 1 and Table 2 respectively. Datamaximum velocity was only 65cm s−1. In the middle

and times from 14 stations were collected duringof the lagoon, the velocity declined to an averagefour cruises on September 10, 1998 and June 28,of 10cm s−1. The estimated water flux of 6×107 m3,

July 31, and August 7, 2000. The dissolved oxygen

occurred at spring tide cycle, is one-thirteenth ofconcentration was 2% lower than the Class Ⅱ

the lagoon s volume. This might lead one to believe

water quality standard, while other water qualitythat the lagoon exchanges in 〜two weeks, but anparameters were normal（

earlier study indicated an exchange rate of 90-days.

quality standard, P.R. China, 2000）. Low dissolved

Table 1. Water Quality Data

Table 2. Sediment characteristics at four sampling stations.

, National water

Ecosystem-based management and models in sustainable management of coastal aquaculture
oxygen concentration can be the result of thesurface to depth. DO at the surface is 5 04mg/L,

sediment oxygen demand and biological activity

very similar to that in stations 2 to 6. At station 1

in the water column. The sulfate and the organic

DO is 6mg/L at depths of 2m. We speculate thatmatter are largely in the sediment. Large organic

this phenomena is the result of the surface waterparticles settling in sediment cause a serious waterout-flow from the bay. At station 7, where there are

quality problem. Decay processes in the sedimentno fish cages, water quality is better. DO is 6mg/L

cause a high demand for oxygen from the overlying

at surface, but at depths >3m; the DO value is below

water column. This demand may excessively stress

5mg/L（Figure 4）.

the oxygen resources of overlying water and deplete

Nitrate concentrations exhibit a peak of about 5 97

the dissolved oxygen concentration. Sedimentμg/L within the channel region near the cage fish

oxygen demand and the biological decomposition in

culture, where organic matter falls to the bottom.

the water column likely are the major reasons for

In both outside lagoon and inner lagoon regions, thelow dissolved oxygen concentrations in the Xincun

nitrate concentration is fairly low with a value of 0 83

Lagoon ecosystem.

to 0 70μg/L（Figure 4）. The nitrate concentration

Dissolved oxygen concentrations were normal
outside the lagoon and in the inner lagoon regions.

in the inner lagoon is the result of nitrate uptake by
the seagrass and it remains generally low.

In the navigational channel region, dissolved oxygen

Ammonium concentrations have a similar

concentrations were low at greater depths. This is

distribution to nitrates in the water column. It

the region where fish cage culture is concentrated.

decreases linearly from the cage fish culture

The vertical distribution of DO is particularly

region to an area outside the lagoon. Ammonium

important in determining the extent to which anconcentrations exhibit a peak of about 14 22μg/L

area is polluted. The vertical characteristics of DO

in station 6# in the cage fish culture region, andat different stations located from the outside bay

reduce sharply to 0 09μg/L in the inner bay where（station 1）to the middle bay（station 7）during theseagrass. beds are dominant（Figure 4）.

neap tide period as shown in Figure 3. DO is lower

The phosphorus concentration is commonly lower

than 6mg/L at stations 2 to 6 in all layers. At area

than nitrate and ammonium concentration in thestations 2, 4, 5, and 6, the DO is less than 5mg/L, andwater column. Phosphorus concentrations are below

the average value is only 4 8mg/L. Vertically, DO

0 5μg/L in six of the seven stations. The maximal

declines sharply and reaches a minimum 2 to 3 m

phosphorus concentration reaches 1 27μg/L atunder the surface in the fish cage culture region. On

station 5# in the fish cage region（Figure 4）.

the other hand, vertical DO distribution is different

The spatial and temporal distributions of nutrientsat station 1 outside the bay; it becomes larger fromreflected the dissolved oxygen distribution in theFig. 3. Dissolved oxygen saturation and salinity in Xincun Bay

Mac Rawson, Changsheng Chen, DaoRu Wang, Charles Yarish, Jim Sullivan, Lu Wang, and MingYuan Zhu

Fig. 4. Nutrient distributions in Xincun Bay.

water column. Within the fish cage area, substantial

by DiToro

quantities of organic matter accumulate in the

we only consider DO, NH3 , NO 3 and their major

sediment. Sediment oxygen consumption increases

kinetic interaction. This is based on evidence thatas a result of chemical oxidation, activity of benthic

low DO is the major problem of eutrophication,organisms, and bacterial decomposition of organicand the nitrate and ammonium concentration are

matter. Oxygen in the water column above therelatively large within the fish cages region in

sediments can then become depleted, leading to

Xincun lagoon.

anoxic conditions. When oxygen above the sediments.（1971）. In our water quality model,

The two major components of the hypolimnetic

is depleted, nitrogen and phosphorus are released

oxygen depletion are water column oxygen demand

to the water column more readily. Phosphorus（WOD）and sediment oxygen demand （SOD）.

is released under anoxic, reducing conditions,

WOD embraces the biological and chemical oxygen

whereas it normally complexes with oxidized irondemand primarily due to algal, bacterial and fish

and becomes immobilized. Previous research has

respiration. SOD reflects utilization of dissolved

examined these relationships between nutrients,

oxygen from overlying and interstitial water ofdissolved oxygen and sediment oxygen consumption

the sediment by biological and chemical oxygenin aquatic systems（Stumm 1973, Frevert. 1980,

demands. As discussed above, DO which acts as

Nixon 1982）.

an eutrophication indicator is predominantly low
within the fish cage culture region, where much ofc. Model Results

the organic matter deposits to the sediment. Low

A three dimensional conventional water quality

chlorophyll , low primarily productivity, even low

analysis simulation model that was originallynutrients in water column, but large quantities

developed by Ambrose. in 1993（known asof organic matter in sediment, SOD is the major

WASP5）was modified and used to study thereason for depletion of DO rather than WOD. For

dissolved oxygen in Xincun lagoon. The equations

this reason, we mainly consider SOD as a importantsolved by WASP5 are based upon the key principle

sink of dissolved oxygen in our water qualityof conservation of mass. They include three major

model. Macroalgal and seagrass photosynthesis andcomponents, the advection and dispersion of

respiration are also considered in this model due totransport, kinetic interaction and transformation,

the fact that they remove the nutrients from theand external loading. WASP5 eutrophication water

water column. Thus, the DO kinetic interaction andquality model considered eight water quality statetransformation includes processes of reaeration,

variables- DO, PHYT, CBOD, NH3 , NO3 , ON, OPO4

macroalgal（

and OP and used the kinetic framework developed（）and seagrass）photosynthesis and respiration,

Ecosystem-based management and models in sustainable management of coastal aquaculture
cage fish respiration, nitrification and SOD.

stratified in Xincun lagoon. Tidal cycle average

Factors that affect SOD are rather complex. Thesesurface temperature and salinity inside the lagoon

factors include temperature, oxygen concentration,is uniform with a magnitude of 30 8℃ and 31 8 ppt.

makeup of the biological community, organic andTemperature is lower and salinity is high in thephysical characteristics of sediment, current velocity,

deepest part of the lagoon. Outside of the entrance

and chemistry of the interface. Velocity effectsof the lagoon, a strong gradient of temperature andon SOD were not due to physical resuspension

salinity is demonstrated by the effect of flood andof bottom material to the overlying water. It was

ebb tidal current.

hypothesized that the increase in turbulence

A uniform DO, NH4 , NO3 field is initialized aftergenerated by increased velocity was responsible

the temperature and salinity field is adjusted. Figure

for increased transport of soluble organic material

5 shows the spatial and temporal distribution of DO

across the sediment interface, resulting in highconcentration in cases（1）and（2）. The distribution

SOD. Measurements of SOD showed that it changes

of DO is closely related to the tide, during flood tidein spatial and temporal variation due to different（upper Figure 5）, the minimum DO concentration

situations（Hickey 1984, Whittemore 1984）.

center occurs not in the channel cage fish culture

Within aquatic systems sediment nutrient fluxes

region but in the inner Bay. During ebb tide, theplay an important role on the nutrient concentration

minimum DO occurs in the outside lagoon near thein the water column. Studies indicate that nitrogenentrance. The lowest DO concentration occurs inand phosphorus may be released to the water

the cage fish culture region only during the middle

column more readily when oxygen above theflood-ebb tide. In cases（1）and（2）, the lowest DO

sediments is depleted（Smith and Fisher 1986）.

concentration is 5 0mg/L and 4 5mg/L, respectively.

Within the large SOD region, sediments were the

The experiments demonstrate that the tidal average

dominant sources of ammonium and phosphorus

DO concentration reduces 10% when the fish cages（Boynton and Kemp 1985; Fisher. 1982）. The

are doubled. It seems that the effect of cage fish inprocesses of nutrient fluxes of sediment are complex

the model is not sensitive to the DO concentration.

and it is necessary to calibrate by the in-situ

The response of this process indicates that strong

measurement. In our model, we simply consider

tidal currents in the channel region enhancenutrient fluxes of sediment as the linear relationshipmixing with outside bay water and increases DO

with SOD and bottom velocity. The ammonium

concentration.

fluxes and nitrate fluxes ranged between 60 and

The DO concentration distribution in selected area

600umol/m2/hour and 3 and 39umol/m2/hour in the

1 had a stratified structure with the lowest DO over

Xincun water quality model.

the sediments in the channel region. Large SOD in

The water quality model is coupled with thephysical model developed by Blumberg andthe fish cage region consumes dissolved oxygen andleads to the DO concentration depletion.

Mellor（1987）. The physical model runs prognostic

When macroalgal culture is considered in sites

problems with tidal and wind driven oscillations

Area 2 and site Area 3 that are further in theand rainfall water discharge. When the physicallagoon, macroalgae seem to not enhance the DOmodel reaches equilibrium state, the water quality

concentration in fish cage region and, obviously,

parameters are added and run with the cases ofin the macroalgal culture regions. The change of（1）
a 450 fish cage platforms at the channel region,

DO concentration in selected points of the bay, fish

without the effect of macroalgal culture;（2）doublecage region and inner bay. Co-incides with the tidal

the fish cages, without the effect of macroalgalelevation（tidal current）. In the fish cage region,

culture; and（3）double the fish cages and factor inlowest DO concentration occurs before lowest tidal

the macroalgal culture.

with a magnitude of 4 2mg/L at the bottom; highest

The model was initialized using the temperature

DO concentration occurs at the beginning of floodand salinity field on 28 July. The model demonstrates

with a magnitude of 5 5mg/L. But in the open partthat the temperature and the salinity remainof the lagoon where macroalgae are cultured, theMac Rawson, Changsheng Chen, DaoRu Wang, Charles Yarish, Jim Sullivan, Lu Wang, and MingYuan Zhu

Fig. 5. DO concentration distribution during the flood tide（upper pair）, ebb tide（middle pair）, flood-ebb
tide（lower pair）under existing conditions（left）and with a 50% increase of fish cages（right）in Xincun
Bay.

Ecosystem-based management and models in sustainable management of coastal aquaculture
surface DO concentration seems unchanged, and the

5 200（70ha）（Table 3）.（Fish pen platforms usually

bottom DO concentration reaches a lowest value of

have nine cages）.）. The macroalgae

4 8mg/L.

culture increased during the 2001 to
2004 period from 146ha to 233ha and the shrimp

d. Follow up sampling on Xincun Lagoon

ponds adjacent to the lagoon are 200ha. The Hainan

Since the 2000 study, the aquaculture mix in andMarine Development, Planning and Design Researcharound the lagoon has changed. The number of 3m

Institute continues to monitor the lagoon. The most

X 3m fish cages increased substantially in 2001 to

obvious change is the continued increase in the

6 500 cages（87ha）then decreased to steadily toaverage ammonia levels in the lagoon from 28 7μ

Table 3. Area of culture species（hectare）

Table 4. Water quality monitoring results in 2003

Table 5. Water quality monitoring results in 2004

Mac Rawson, Changsheng Chen, DaoRu Wang, Charles Yarish, Jim Sullivan, Lu Wang, and MingYuan Zhu
g/l in 2000 to 49 3μg/l in 2004（Tables 4 & 5）The

concentration-modeling support the above viewpoint.

model simulations pointed out that the water column

The model experiments also show that averagein the fish cage area was heavily polluted by organic

DO concentration will decrease by about 10%

matter. The resulting low DO was an indication

when fish cages are doubled. This result shows thethat carrying capacity has been exceeded and theeffect of strong tidal current mixing and transport.

impact of the fish culture must be reduced. Since

Macroalgal culture increases the DO concentration

the study took place four years ago, the fish cages

in the culture region, but contributes less to the DO

and shrimp ponds numbers have been limited andconcentration in the cage fish region

the number of cages reduced. Also, the ecological
Ⅳ. Jiaozhou Bay Example

importance of the seagrass has been recognized anda new seasgrass special protected zone set up（Wang
DaoRu, personal communications）.

a. Physical Description
Jiaozhou Bay is a shallow bay of 〜 400 km 2

e. Discussion of Xincun Lagoon Resultswith an average depth of m and maximum of 50m.

The results showed that the water column in

The adjacent city is Qingdao, which is one of top

the Xincun Lagoon aquaculture region was heavily

five ports in China and has a population >2 million

polluted by organic material and according topeople. During the period of this study the bay

sediment sample analysis, was also high in silicate

contain three areas of scallop aquaculture pens

contents. Except for dissolved oxygen, sampled（Chen,. 1999）.

chemical parameters and nutrients did not exceed
the national water quality standards Class Ⅰ. The

b. The Modeldata were also evaluated according to Criteria

The physical model used in this study was afor Surface Water Quality Classifications, Class Ⅱ

modified version of the coastal ocean circulation（Florida EPA）
. Although the water generally met

model developed by Blumberg and Mellor

standards, the environmental health of the fish cage（1987）. The model s forcing functions are: （1）culture and navigation channel region has declined

tidal oscillations,（2）wind driven features, and（3）considerably as evidenced by the mortality oftime-variable inputs of rivers. The time-variablecultured fish and low DO.

river inputs and onshore intake/outflow discharges

Two kinds of pollutants affect water quality

were used to simulate the buoyancy flow caused byand sediment quality in Xincun Lagoon. One

river discharges. By far, the largest river dischargesource is the pollutant produced by four factories,（85%）into Jiaozhou Bay during summer was fromfour restaurants and seven gasoline stations, andthe Dagu River（87m 3 s −1, Liu and Wang, 1992）.

an estimated 481tons of COD from the sewage

The effects of wind-induced currents and resulting

discharging. The other pollutant is a by-product of

mixing influences on the distribution of temperature,fish cage operations that results in an estimatedsalinity, nutrients, and phytoplankton were examined

5 000tons of organic pollutants annually. Waterin the simulations. The dominant wind forcing inquality samples indicate that DO is always lower

the summer is from strong southeast winds, but forthan the value of national water quality standards

simplification, a constant southeasterly wind of 5m

in fish culture areas. The assessment results show

s−1 was added into the model after 10 model days.

the main source of pollution is the fish cages. WhenThe coupled biological model simulates simple

feeding fish, large amounts of uneaten food and feces

nutrients（N）, phytoplankton（P）, and zooplankton

descend to the bottom. Sediment under the pens（Z）using a modified model developed by Franks

releases NH3H2S and other pollutants by degradation

and Chen（1986）. The biological parameters variedof the organic matter by bacteria. This chemical

widely in time and space. The model was run withreaction requires large quantities of oxygen andan initial set of parameters. Sensitivity analyses

reduces the dissolved oxygen substantially inwere then run over the parameter range. The

the sediment and water column. Results of DO

stock density of shellfish was calculated directlyEcosystem-based management and models in sustainable management of coastal aquaculture
from measurements taken in Jiaozhou Bay in 1996

and in the experiments, phytoplankton and（Collaudin, 1996）. The scallop rafts consist of vertical

zooplankton were measured in units of carbon

lines of lantern nets. Based on the average number（C）and nutrients by units of phosphorus （P）.

per lantern net, the standing stock parameter was

A constant C/P ratio of 100 was used to convert

set at 12 individuals m−3 that is the equivalent tocarbon to phosphorus. A 60C/Chl−1

0 012 individuals L . The scallop filtration ratevaries in a range of 30 to 200L d−

individual−1

to convert chlorophyll

ratio was used

to carbon.

ataround 25℃. This may overestimate the filtrationc. Effects of Aquaculture

rates since the food availability was not taken

Simulation experiments were made with two

into account（Winter, 1978）. So, a filtration rate ofscallop stocking densities of 12 individuals m −3（0 012

100L d−1 individual−1 was used in the model. The

individuals L −1）in the first case and 24 individuals

excretion fraction of the filtered food was assumed

m −3 in the second case. In both cases, scallops were

to be 0 3 or 30%.

grazing dramatically and decreased concentrations

Jiaozhou Bay is a phosphorus-limited ecosystem,of phytoplankton in the culture areas labeled A1 to

Fig. 6. Locations of the shellfish aquaculture sites（shaded area）and selected regions forthe flux estimation of nutrient and phytoplankton（areas enclosed by dashed line）.（Theheavy solid lines indicate two sections used to represent our model results on cross-bay
section（section A）and flux calculation into of out of the Bay（section B）.

Mac Rawson, Changsheng Chen, DaoRu Wang, Charles Yarish, Jim Sullivan, Lu Wang, and MingYuan Zhu
A3（Figure 6, Chen., 1999）. The experiments

μg ChlL −1 in A1, 0 38μg Chl

L−1 in A2, and 0 67

suggested that the scallops would sharply reduce

μg Chlthe concentration of phytoplankton to 0 99μg Chl

51 1%, 50 8% and 55 6% lower than the case without

L−1

in A1, 0 52μg Chl

L−1

in A2, and 1 0μg Chl

L−1 in A3, about 31 8%, 33 3% and 37 3% lower
than those in the case without shellfish（Plate 2,
Chen

L

−1

in A3. These concentrations were 〜

shellfish, but only 19%, 18% and 22% lower than thefirst case with shellfish（Figure 7, Chen., 1999）.

The impact of scallop culture on the concentration., 1999）. The response of phytoplanktonof nutrients was very small, even at the higher

to increased shellfish stocking densities was notstocking density. This is in contrast to previous

linear. When the stocking density was doubled to 24

studies which indicated that shellfish have an

individuals m−3

the concentrations decreased to 0 71

important role in nutrient cycling and distribution（Dame, 1993）. One explanation is that Chen s model
did not consider the impact of the biodeposition
process of shellfish. The biodeposition process could
result in shellfish taking up small particulate organic
matter and producing feces and pseudo-feces that
decompose into inorganic nutrients. Our model
did include shellfish excretion, which was directly
converted to phosphates. If the above explanationis correct, there should be significant modificationof nutrient concentrations when the excretion rateor stocking density is increased. However, that was
not the case in simulation experiments. Anotherpossible explanation is that most of the phosphates
in Jiaozhou Bay were the result of loading fromthe land and rivers. The recycling of nutrients byshellfish may directly influence the concentrationof nitrogen but not phosphates, or the nutrient
regeneration rate may be orders of magnitude
smaller than the nutrient loading rate from othersources.
d. Nutrient Uptake and Regeneration
To understand the roles of biological processes,
the nutrient uptake and regeneration processes
in the coupled model must be examined. Nutrient
uptake in this modified NPZ model was controlled
by the phytoplankton growth rate, incident radiance,
the half-saturation constant, phytoplankton biomass
and nutrient concentration. Nutrient regeneration
was estimated by the sum of zooplankton excretion,
death of phytoplankton and zooplankton, andFig. 7. Tidal-cycle averaged surface distributionof phytoplankton at the 20 model days for the casewith the shellfish culture densities of（a）12 and（b）24 individuals m−3. Physical forcings are tide,
freshwater discharge and a southeasterly wind（5ms −1）.

shellfish excretion.
In the case with only tides and freshwater
discharges, the model indicated that surface
distributions of the uptake and regeneration
rates were similar to nutrient distribution, which
decreased from the inner to outer bay with theEcosystem-based management and models in sustainable management of coastal aquaculture
highest values on the northwestern and northernof the study period. Sensitivity analysis of thecoasts. The maximum regeneration rate in thephytoplankton revealed that the spatial distribution−1

inner bay was 〜 2μmol C L−1

d , which was 〜 5of phytoplankton remained unchanged, although thetimes smaller than the maximum uptake rate. This

concentration varied remarkably with changes insuggests that the physical process associated withparameters. This suggests that the model results forriver discharge was a major source of nutrients for

phytoplankton were robust.

phytoplankton in the inner bay. Adding a southerly

The model results revealed that physicalwind did not significantly change the distributions

processes had a direct impact on temporal andof nutrient uptake or regeneration. The uptake

spatial distributions of nutrients and phytoplankton

rate was relatively large in the inner bay along

as well as on shellfish aquaculture. Tidal mixing

the coast as a result of nutrient accumulation bycaused physical and biological variables to be well

the wind-induced northwestward advection. This

mixed vertically. The concentrations of nutrients

phenomenon may explain why a phytoplankton

and phytoplankton were high near the northwestern

bloom occurs in the innermost bay during aand northern coasts near river sources but

southeasterly wind.

decreased from the inner bay to the outer bay.

When consumption of phytoplankton by shellfish

The model results suggested that prevailing river

was included, distribution of nutrient uptake anddischarges and tidal mixing, and the southeasterly

regeneration was modified, particularly in thewind in the summer may cause unusual nutrient

aquaculture areas. Nutrient uptake rates in theaccumulation and lead to phytoplankton blooms inaquaculture sites dramatically decreased because

the innermost bay. The fact that a phytoplankton

the phytoplankton decreased. Yet, the nutrient

bloom can occur under a condition of southeasterly

regeneration rate in these sites increased as awind implies that physical processes may have a

result of shellfish metabolism. As a result, thedirect impact on the occurrence of red tide along

distribution of phosphates was similar in the casethe northern coast of Jiaozhou Bay. The overloadingwith and without shellfish aquaculture, suggestingof nutrients from inland shrimp aquaculture,that the decrease in nutrient uptake rates due toindustries and other urban human activities caused

phytoplankton consumption was almost compensateda high nutrient concentration in the inner bay thatfor by the physical processes of advection andprovided favorable conditions for eutrophication.

diffusion.

Accumulation of nutrients due to the southeasterly

One of the main interests in this study was to
identify, qualify and quantify the roles of physicalwind speeds up the eutrophication process andcauses the red tide .

and biological processes in maintaining ecosystem

The estimation of nutrient and phytoplankton

health. In the simple NPZ food web, the physicalfluxes in the five identified sites suggested

processes included advection and diffusion,that the nutrients were maintained by physicalM 2 tide, river discharge and wind. Biologicalprocesses, while the phytoplankton was controlled

processes related to phytoplankton included

predominantly by biological processes. Shellfish

nutrient uptake and regeneration, phytoplankton

aquaculture tended to alter the entire Jiaozhou Bay

grazing and mortality, and shellfish consumption.

ecosystem. The loss of phytoplankton in shellfish

To examine effects of freshwater discharge andaquaculture sites was compensated by nutrientsshellfish aquaculture, the net flux of nutrients andthat advected and diffused from surrounding

phytoplankton in five closed regions and across thewaters. High levels of phytoplankton consumption

outer strait were estimated. The flux was calculated

also caused a net flux of phytoplankton into thebased on tidally averaged values over the 10 tidal

bay from the Yellow Sea, even though nutrients

cycles. When we say equilibrium state, that means

were advected out of the bay. In addition to

the flux is balanced for a first-order approximation

eutrophication caused by human activities, highin which the biological field changes slowly but

densities of suspended feeding shellfish will alter theno steady state could be reached over the course

lower trophic food web by grazing phytoplankton,

Mac Rawson, Changsheng Chen, DaoRu Wang, Charles Yarish, Jim Sullivan, Lu Wang, and MingYuan Zhu
excretion and biodeposition. Aquaculture populations

Marine Ecology Progress Series 23(1): 45-55.

of bivalves tended to transfer large quantities ofChen, C., H. Liu and R. C. Beardsley, 2003. An

materials from the water column to the sediment,

unstructured grid, finite-volume, threewhich can dramatically change the content ofdimensional, primitive equation ocean model:

the organic matter in the benthic layer（Kautsky

application to coastal ocean and estuaries. J.

and Evans, 1987; Kasper

Atmospheric&Oceanic Tech., 20, 159-186., 1985）. The benthic

processes, in turn, may alter nutrient cycling in

Chen, C., R. Ji, L. Zheng, M. Zhu and M. Rawson.

the bay（Barg, 1992; Dame, 1993; Jorgensen, 1990）.

1999. Influences of physical processes on the

It also should be noted that this model did notecosystem in Jiaozhou Bay: A coupled physicalinclude the intertidal zone. The direct impact ofand biological model experiment. Journal of

the intertidal process remains unclear, but a large

Geophysical Research. 104（C12）;29, 925-29, 949.

quantity of nutrients potentially can be advected

Collaudin, B. A. 1996. A first approach of aquaculture

back to the bay during ebb tide.

development in Jiaozhou Bay（P. R. China）.
Investigation Report, IFREMER, France

Ⅲ. Conclusion

Dame, R. F. 1993. The role of bivalve filter-feeder
material fluxes in estuarine ecosystems,: R.F.

Management of aquaculture in semi-enclosed

Dame（Ed.）. Bivalve filter-feeders in estuarine

embayments is influenced by numerous physical,

and coastal ecosystem processes. NATOchemical and biological processes. Resource

Advanced Study Institute Series G, Ecologicalmanagers who are tasked with maintaining andSciences, 33: 235-258.

improving environmental quality must balance the

Di Toro, D. M., D. J. O Conor, and R. V. Thomann.

multiple uses of bays. Three-dimensional models

1971. A dynamic model of the phytoplankton

provide tools that can help determine carrying

population in the Sacramento-San Joaquin Delta.

capacity for aquaculture by integrating knowledge: Nonequilibrium Systems in Natural Waterof physical, chemical and biological processes

Chemistry, edited by J. D. Hem, pp.131-180,

and accounting for multiple sources of pollutants.

American Chemistry Association, Washington, D.

The models also will provide credibility to theC.

decisions of managers and allow the development of

Fisher, T. R., P. R. Carlson and R. T. Barber. 1982.

sustainable aquaculture in locations throughout the

Sediment nutrient regeneration in three North

world.

Carolina estuaries. Estuarine, Coast and Shelf
Science 14(1): 101-106.
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production in tidal fronts: A model of Georges

Ambrose Jr., R. B., T. A. Wool, and J. L. Martin. 1993.
The water quality analysis simulation program,

Bank in summer. Journal of Marine Research 54:
631-651

WASP5, Part A.: Model documentation. U. S.

Hickey, Christopher W., 1986. Chamber studies ofEnvironmental Protection Agency, Athens,

benthic oxygen uptake kinetic in the Waioyapu

Georgia, 202 pp.

River, New Zealand,: Sediment oxygen

Blumberg, A. F. and G. L. Mellor. 1987. A

demand-processes, modeling, and measurement,

description of a three-dimensional coastal

K. Hatcher,（Ed）,Institute of Natural Resources,: N.S. Heaps

University of Georgia, Athens, Georgia, pp. 37-62.

（Ed.）. Three-dimensional coastal ocean, Coastal

ocean circulation model. pp. 1-16,

Jorgensen, C. B. 1990. Bivalve filter feeding:

Estuarine Science. American Geophysical Union,

Hydrodynamics, bioenergetics, physiology,

Vol. 4, pp.1-16, Washington, D. C.

and ecology. Olsen and Olsen, Fredensborg,

Boynton, W. R. and W. M. Kemp. 1985. Nutrient

Denmark, 140 pp.

regeneration and oxygen consumption by

Kasper, H. F., P. A. Gillespie, I. C. Boyer, and L.

sediments along an estuarine salinity gradient.

Mckenzie. 1985. Effects of mussel aquaculture onEcosystem-based management and models in sustainable management of coastal aquaculture
the nitrogen cycle and benthic communities in

K. Hatcher,（Ed.）,Institute of Natural Resources,

Kenepru Sounds. New Zealand Marine Biology,

University of Georgia, Athens, Georgia, pp.

85: 127-136.

343-366.

Kautsky, N. and S. Evans. 1987. Role of biodepositionbyin circulation of matter andnutrients in Baltic coastal ecosystem. Marine
Ecology Progress Series, 38: 201-212.

Stumm, W. 1973. The acceleration of biogeochemical
cycles in phosphorus. Progress Water
Technology, 2: 133-144.
Whittemore, R. C. 1984. Implementation of in-situ andLiu, F. and K. Wang. 1992. The rivers along Jiaozhou

laboratory SOD measurements in water quality

Bay coast line and their geological effects.

modeling. Water Pollution Control Federation

Marine Science（in Chinese）1: 25-28.

56th Annual Conference, Altanta, GA, USA,

Smith, Leslie K. and Thomas R. Fisher, 1986.

pp.2-6 October 1983.

Nutrient fluxes and sediment oxygen demand

Winter, J. E. 1978. A review on the knowledge ofassociated with the sediment-water interface

suspension-seeding in lamellibrachiate bivalves,of two aquatic system.

with special reference to artificial aquaculture: Sediment oxygen

demand-processes, modeling, and measurement,

systems. Aquaculture 13: 1-33.

水研センター研報，第19号，113−129，平成19年
Bull. Fish. Res. Agen. No. 19, 113‑129, 2007

博士号論文

Offshore finfish mariculture in the Strait of Juan de Fuca
J.E. Jack Rensel＊1, Dale A. Kiefer＊2John R.M. Forster＊3, Dana L. Woodruff＊4

and Nathan R. Evans

Abstract Finfish mariculture has existed in the U.S. Pacific Northwest for over thirty
years, but for the past 15 years most effort has focused on culture of Atlantic salmon in protected, inshore cage sites. The Strait of Juan de Fuca（the Strait ）is a large area with relatively sparse shoreline development and several apparent advantages for mariculture using
offshore technology.
This study provides an overview of pertinent hydrographic conditions and possible water quality effects of marine or salmonid finfish culture in the Strait for commercial harvest
or stock rehabilitation. Circulation studies, current and wave meter deployments, acoustic
Doppler current profiles and phytoplankton assessments were conducted in three different
regions distributed throughout the Strait near the southern, U.S. shore. Results were compared to existing inshore fish farms and analyzed with a simulation model（AquaModel）
that accounts for growth and metabolic oxygen demands of caged fish and the response ofphytoplankton to nutrients and grazing. An available benthic submodel was not used as
current velocities throughout the water column and near the sea bottom far exceed known
threshold rates for salmon farm waste resuspension. Such strong currents allow for dispersal of the organic wastes and their aerobic assimilation into the food web.
The field study results and modeling indicate no probable adverse effect of large scale
fish mariculture in the Strait with regard to sedimentation or water column effects. Phytoplankton growth stimulation as a result of fish culture will not occur because nutrients do
not limit microalgal growth. The area is naturally replete with dissolved inorganic nitrogenand sunlight is the primary factor limiting phytoplankton growth. Similarly, backgroundnitrogen levels exceed half-saturation rates of seaweeds and farm plume dispersal is mostly
parallel to shore in deep water so no effect on seaweeds is anticipated. Fish-killing harmful
algae were rarely observed and then only in sparse numbers, although harmful Heterosigma
akashiwo are known to occur throughout the waters of the Strait, Puget Sound and adjacentwaters of the Pacific Ocean. Growing season phytoplankton abundance is much lower in theStrait than in nearby bays or Puget Sound.
Previously undetected and persistently lower sea surface temperatures were observed insatellite imagery for the central Strait region, especially during the summer and early fall.
Surface-layer water temperature was positively correlated with dissolved oxygen concentration during the same seasons. Accordingly, there could be significantly reduced dissolved
oxygen content of surface waters of the central Strait during this period, but this finding
requires field verification. Eastern and western areas of the Strait may be marginally betterfor fish culture on this account, depending on fish species cultured.
We conclude that effects of marine fish mariculture on water quality or benthic conditions
would be insignificant and that fish culture is technically feasible in the Strait. However, thehigh energy environment and challenging conditions will necessitate revised and novel management techniques to insure successful operations.
2006年 月26日受理（Received. June 26, 2006）＊1
Rensel Associates Aquatic Sciences, Arlington, WA 98223 jackrensel@att.net＊2
University of Southern California, Los Angeles, CA 90089＊3
Forster Consulting Inc., Port Angeles, WA 98362＊4
Battelle Marine Sciences Laboratory, Sequim WA 98382＊4

J.E. Jack Rensel, Dale A. Kiefer, John R.M. Forster, Dana L. Woodruff and Nathan R. Evans
will have to be used if it is to be done successfully.
Introduction

Potential exists especially for the commercial
culture and/or restoration of stocks of marine fishThough more than half the world s salmon
and shrimp sold annually are now produced bysuch as rockfish（spp.）, lingcod（）or sablefish （aquaculture, very little of the marine white fish is）, culture techniques for which have now

farmed. As technical obstacles are overcome, many

been developed（Ikehara and Nagahara 1980, Whyte

now believe that farming or stock enhancement of1994, Clark

1999, Rust

2006）.

marine fish is a developing opportunity. It may be

The results of our study are reported in detailmore than just a business opportunity; it potentiallyin a literature review and annual reports preparedis the solution to a chronic problem of over-harvestingfor the U.S. NOAA Sea Grant Office that are all

and resource depletion in many of the world s wild

available via internet link in references（Rensel andcapture fisheries. But done improperly, mariculture

Forster 2002, 2003, 2004）. The literature review

could damage marine ecosystems and to deprive

indicated that few multi-year hydrographic studies

us of the seafood on which humans have comehad been published for the western and central

to depend. Modern, environmentally-sensitive

Strait and most were single year studies withaquaculture using low or no adverse environmental

monthly data collection. Studies conducted many

impact methods has been achieved at nearshore fish

decades ago, although done to high standards at themariculture sites in Washington State（NOAA 2001,

time, did not account for interannual and shorter

Rensel 2001）after environmental guidelines were

temporal variation, which is known to be significant,adopted 20 years ago（SAIC 1986）. A goal for theas discussed below.

future of all mariculture is one in which our seafood

monitoring of the eastern Strait began in 1999 andharvests and the environment that supports themhas shown some of this variability, such as occurred

are in natural balance.

during a severe drought in 2000 and 2001（Newton

Routine hydrographic

In recent years there has been increasing private

2003）. Our sampling of the Strait began inand government interest in aquaculture offshore

the late summer of 2001, but as explained below,

or in the open ocean in the nation s coastal waters.

the system had apparently not returned to normal

In some cases in the U.S. this could mean operating

conditions by then. At that time we documented

beyond the three mile State jurisdiction, in theunusually low dissolved oxygen concentrations for

Exclusive Economic Zone（EEZ）but in many cases,

surface and near surface waters in several locations.

due to siting limitations of water depth, it would be

As a result, the subsequent years work included anearer shore but in exposed locations. Advocatesfocus on dissolved oxygen conditions or surrogate

suggest that the only remaining opportunity formeasures, as discussed below.

mariculture siting is offshore, due to space limitations

Our study considered the siting of fish

and conflicting uses nearshore. Opponents raise

mariculture projects in the Strait in relation to key

several issues including nutrient enrichment andphysical（water depth, tidal velocity and near-field

possible adverse benthic effects.

circulation）,biological（phytoplankton）and chemical

Already a few such offshore projects are operating

factors（dissolved oxygen, water temperature andin the U.S. as research or commercial businesses,

dissolved nutrient）conditions. Other biological issues

mostly in Hawaii and Puerto Rico but more are being

such as effects of escapes, use of limited fish meal

located overseas. Although not truly offshore in

and oil or possible disease consequences are notterms of distance from the coast, or being outside

discussed here. Socio-political aspects of mariculture

state or province jurisdiction, the Strait of Juan desiting such as competition with existing fisheries,

Fuca（The Strait ）between Washington State andavoidance of navigation lanes and concentrated

British Columbia is being considered for marine fish

fishing areas, maintenance of visual and auditory

mariculture. The exposed, high energy nature of its

aesthetics for nearby shoreline owners, etc. arewaters means that offshore equipment and methods

important too. However, they are not discussed inOffshore finfish mariculture in the Strait of Juan de Fuca

Fig. 1. Study area locations in western Strait（offshore of Neah Bay）, central Strait（offshore of
Whiskey Creek）, Eastern Strait（offshore of Green Point to Morse Creek）and reference station at
Cypress Island in North Puget Sound. Base figure from Thomson 1981, used with permission.

this paper except to the extent that our study areas

have current velocity in the range of 10 to 60 cm

were selected with prior knowledge that such areass−1 but varies within this range depending on size

were likely to be suitable with regards to theseand species of fish, stocking density and pen design

other considerations.

or configuration. Regular resuspension and dispersal

Fish mariculture is technically possible in manyof salmon farm wastes occurs at near-seabed current

locations in the Strait but we selected three study

velocities in the range of 〜10 to 26 cm s−1 Cromey

areas, one each in the western, central and eastern2002）. Such dispersal allows the aerobic

Strait. These are referred to as 1）Offshore of Neah

decomposition of wastes and avoids the extirpation

Bay, 2）Offshore of Whiskey Creek and 3）Offshoreof benthic infauna beneath of near net pens underof Green Point（actually between Morse Creek andoptimum conditions.

Green Point）, respectively（Fig. 1）. Also included

At higher current velocity, fish may have to be

for comparison was a reference area at Deepwater

sized appropriately and cage systems reinforced. At

Bay, Cypress Island in north Puget Sound where fishmean velocities lower than 5 to 10 cm s−1（depending

mariculture has been practiced and environmentallyon the fish species and feed size）significant adverse

monitored for several decades.

sedimentation effects on the benthos are possible

Additional details and literature reviews arebeneath or adjacent to the cages, although some

reported in the underlying technical papers available

sites in other areas may be episodically flushed byfrom the primary author or from NOAA or atstorm events. The minimal recommended average

http://www.wfga.net/sjdf/index.html. Here we only

current velocity for near surface and midwater

include a partial overview of some of the results

depths combined in Washington State is 5 cm s−1

from our study in the 20 to 40 m depth zone of the（SAIC 1986）. Other physical factors besides current

subject area.

velocity factors have a bearing on site suitability
too, such as depth beneath pens, but in the Pacific

Current Velocities and Circulation

Northwest and in Maine it is believed that current
velocity is relatively more important than depth

Current velocity is a primary consideration

beneath cages to minimize benthic impacts（Cross

for fish culture in net pens both in regard to its

1993）. Current and wave meters were deployed at

effect on cultured fish and to potential impacts on

all sites and acoustic Doppler current profilers withthe benthos and water column. Presently, sites

bottom tracking were used on vessels to survey

considered optimal for fish mariculture in pensduring varying types of tidal amplitude cycles.

J.E. Jack Rensel, Dale A. Kiefer, John R.M. Forster, Dana L. Woodruff and Nathan R. Evans
Drogue tracking was also used; see Rensel and1991 to 1993, as did the Atlantic salmon cultured

Forster（2003, 2004）.

within them （Loverich and Croker 1997）. The

Current velocity distributions for surface cagestrength and persistence of currents in the study

mean depth of 5 m in the western and central Strait

areas are more than sufficient to prevent adverse

locations were skewed with maximum velocity nearbenthic sedimentation effects, i.e., reduced benthic−1

100 cm sec （Fig. 2）. Mean current velocity was〜32 cm sec−1

diversity and species composition changes. But suchat both locations. At the locationstrong currents present challenges for mariculture

offshore Neah Bay, direction of flow was parallel

operation and maintenance. Pacific Northwest fish

to shore and equally distributed in both seaward

farmers typically move cages, adjust anchoring（westerly）and easterly directions（50% each of total

systems and perform diving inspections outside of

the 2,590 observations, directions within 180 degreepens during slow currents or slack tides, conditions

arc of perpendicular bearing from shore）suggestingthat are relatively infrequent in the Strait. The

no net outflow during the winter time period.

observed currents at our study sites, adjusted for

Net outflow at the nearshore locations sampleddeflection of currents（Inoue 1972）, are also suitable

would be expected to increase in spring and earlyfor culture of appropriately-sized salmonids, but it issummer coincident with increasing river flow fromunknown how various sizes and species of marine

the Georgia Strait-Puget Sound Basins. Periodic

fish species would respond to them. Effect of strong

winter main channel and summer nearshore current

current velocity on marine fish culture is a topic

reversals that last for several days are also not

requiring further research and experimentation.

uncommon（Cannon 1978, Thomson et al. 2004）.
Wave Exposure

A major difference between the Strait andinshore waters of Puget Sound is the temporalextent of slack tide between tidal phases periods,

Wind waves and oceanic swell are major

herein defined as periods of current velocity < 2considerations for any form of mariculture. Oceanic

cm sec−1. Offshore of Neah Bay slack tidal periods

swell is periodically encountered in the Strait,

averaged only about one minute per day versus

especially the west end, but large wind waves may

an estimated hour or more at a typical Puget

be encountered anywhere in the Strait, depending

Sound net pen site. In commercial fish mariculture,

on season and weather. Wind waves are particularly

extended slack tide periods may result in depressedcommon in the afternoons from late spring throughdissolved oxygen concentrations within the pens,

early autumn when westerly or sometimes easterly

sometimes causing damaging physiological stresssea breezes funnel through the Strait（Renner 1993,

on cultured fish. Offshore spar cages performed

Thomson 1994）. Wave amplitude and frequency

well in early trials offshore of Whiskey Creek indata offshore of Neah Bay were collected from
December 2001 through January 2002 （Fig. 3）.
Significant wave height ranged from 0 2 to 2 2 m
and was dominated by long period（〜15 s）waves.
These conditions do not exceed design criteria forseveral types of offshore cages. Moreover, wave
frequency was not positively correlated with wave
height（r2 = 0 02）, which means that large waves
were not usually of short period that may be more
destructive to mariculture facilities. Oceanic swellheight estimates in the field were much less toward
shore at 25 m depth, compared to further offshore at

Fig. 2. Velocity distribution for 5 m depth（MLLW）
current meter data offshore of Whiskey Creek andoffshore of Neah Bay.

50 m depth. This may be due to protection provided
by Waadah Island, located immediately west of thestudy site.

Offshore finfish mariculture in the Strait of Juan de Fuca

Fig. 3. Wave frequency（Tp, left）and significant wave height（Hs, right）offshore of Neah Bay
during a two month period in the winter 2002-03.

Oceanic swell was also observed in the central

at many times no consistent pattern is observable

Strait during our summer and fall field work but not（Rensel and Forster 2002, 2003）. We examined allin the eastern Strait on the same days. Significant

available past surveys, studies and data reports,

wave height offshore of Whiskey Creek in a priorand could find no consistent trends within the

study in 1993 reached 3.6 m, but did not harm acentral and western zones of the Strait at these

prototype spar style offshore cage（Loverich andtimes. Most prior studies were based on one year,

Croker 1997, Loverich and Forster 2000）. Shortonce-per-month, multiple-day cruises or two year

frequency, choppy wind waves were relatively

studies with less frequent cruises. Such monitoring

common during our field studies at all locations,is insufficient to describe the substantial change ofparticularly during afternoon hours. Modern offshore

dissolved oxygen that occurs in a few hours or acage and anchoring systems should be able tosingle tidal phase, as first noted by Herlinveaux andsurvive all probable weather extremes at our study

Tully（1961）. Moreover, all prior published studies

areas.

focused on deepwater areas, not in depths of 20 to
40 m as we did in our field studies.

Water Temperature and Dissolved Oxygen
Dynamics

A preferred approach to describe variability ofdissolved oxygen in the Strait would have been
to install moored instrument packages at several

The historical annual range of near-surface waterlocations. But given the difficulties and cost of

temperatures in the Strait is approximately 7 to 12 C

numerous such moorings, and the need to make（e.g., Collias et al. 1974）, more moderate than similar

repeated field observations of other factors, we

depths of north or central Puget Sound presently

chose two surrogate methods.

used for fish mariculture. The range is well suitedcollection of vertical profiles of water quality during

to salmon and several other candidate marine fish

the potentially critical period of late summer andspecies and is among the most moderate range offall period in 2001 and 2002. The second utilized

temperatures for all of temperate coastal waters ofsatellite sea surface temperature（SST）images,

North America.

since it was shown that there is a strong positive

The first was

Dissolved oxygen concentrations in surface

correlation between near surface temperature andwaters of the Strait follow previously documented

dissolved oxygen as described below. The former

seasonal and spatial cycles, peaking in late winteris reported in Rensel and Forster（2002, 2003）andand declining during summer and early fall. In

indicated no significant differences among sampling

general, surface waters of the eastern Strait tend

locations. But the satellite SST approach yielded

to have higher dissolved oxygen concentrations insome interesting finds.

the summer and fall than waters to the west, but

SST data was extracted from a transect locatedJ.E. Jack Rensel, Dale A. Kiefer, John R.M. Forster, Dana L. Woodruff and Nathan R. Evansalong the central longitudinal axis of the Strait

Based on the SST satellite imagery analyzed,

between Neah Bay at the entrance to the Straita persistent central Strait surface temperature

and Dungeness Bay at the eastern end of the Strait

reduction was noted for all months examined from

（Fig. 4d）
. In addition, the Strait was divided into 3

May through October during 2001 and 2002. A

geographic regions（Western, Central, and Eastern

persistent central Strait surface temperature

Strait）for analysis purposes, and average transect

reduction was noted for all months examined,

temperatures for each region calculated fromwhen compared to the eastern and especially themonthly composite satellite imagery.

western Strait（Figs, 4a and 4b）. The feature isFig. 4. AVHRR sea surface temperature imagery from the Strait of Juan de Fuca
showing a lower temperature feature mid-Strait for a）2001 and b）2002 with c）
bathymetry and d）transect sampled.

Offshore finfish mariculture in the Strait of Juan de Fuca
prominent in SST satellite imagery of the Strait andprimarily estuarine, with cooler more saline oceanic

persistent to the extent of being visible in many

water flowing inshore and eastward at depth, anddaily and most weekly and monthly composites of

warmer freshwater flowing seaward closer to thethe imagery（images not shown here due to color

surface （Godinpublication limitations）. As much as a 1 5 to 3 ℃

Thomson 1981）. Supercritical turbulent flow overtemperature differential was observed in individuala shallow sill will cause deep water intrusions

images, exceeding the 0 3 to 3 ℃ AVHRR SST error

toward the surface during spring tides, particularly

estimates noted above. In comparison, the eastern

if density differences are minimal （Thomson

Strait had generally the highest SST results and the1994）. Such phenomenon may be expected to vary

western Strait results were intermediate（Figs, 4a

on timescales similar or greater to a fortnightly

and 4b）.

schedule.

1980, Holbrook1980,

We compared temperature data from our field

In addition to bathymetry, tidal cycle variation

surveys using CTDs, previously discussed, to data

may influence the observed condition. Estuary tofrom individual satellite images on the same days

ocean exchange in the Strait is also thought to be

and same locations. There was an apparent lack

modulated by tidal mixing and wind forcing thatof correlation between these data sources. There

increases during neap versus spring tidal periods

are several possible explanations for this. Satellitewith greatest freshwater export during the neap

imagery provides an average temperature basedtides （Griffin and LeBlond 1990）. Monthly oron the pixel size of the imagery（1 1 km）. A directbimonthly pulses of relatively warm fresh watercomparison between point data collected with thehave been documented traveling seaward from the

CTD and the average over a considerably larger

western entry of the Strait（Hickey

area is necessarily going to yield differing results.

although that particularly analysis was focused on

In addition, the time differential between CTD data

the western entry to the Strait and adjacent oceanic

collection and satellite overpass was in some cases

waters off Vancouver Island. When we collated ourseveral hours, adding to the differential. Also, ourdata into neap vs. spring tide periods we did observe

field sampling locations were relatively close toenhancement of the anomaly during spring tides

shore where satellite imagery is less accurate due toand reduced intensity during neap tides, particularlyinterference from land. We would expect nearshore

during 2002（the year with increased river flow）
.

1991）

waters to be more variable and less vertically

Whatever the cause of the anomaly, apparent

stratified due to more abrupt changes of bathymetry

reduced water temperature in the central Strait may

and the shoreline ruggedness that may enhance

be biologically significant because as pointed out

vertical mixing.

above, even a small temperature variation equates

To our knowledge, there have been no prior

to a significant variation in dissolved oxygen. For

published studies that have examined SST patterns

example, using the 2001 regression（y = 1 5186x -in the Strait or mapped the extent of the surface

8 3368 where y = dissolved oxygen in mg/L and x

temperature reduction we observed in the central

is water temperatures in degrees C and r = 0 92）

Strait of Juan de Fuca persistently through thea decline of only one degree C water temperaturesummer and fall months of our study in 2001 andfrom 10 to 9 ℃ results in a reduction of dissolved

2002. The cause（s）of the temperature differential

oxygen of 1 5 mg/L from 6 8 to 5 3 mg/L. For wild

are unknown; however the bathymetry and crossand particularly cultured fishes, these are significant

channel profile of the central region may provide

changes.

some insight.

The single major bathymetric

Dissolved oxygen cycles have been observed atobstruction to deep flow in the Strait of Juan deour reference station at Cypress Island, generally,

Fuca is the Victoria-Green Point sill （Thomson

but not exactly, correlated with the spring-neap

1994）. The sill is located to the east of Ediz Hookcycles（Rensel and Forster 2003）. In the case of

in a region of slightly elevated surface-water

the mid Strait anomaly, westward, estuarine flow

temperatures（Fig. 4c）. Circulation in the Strait isof the surface layer may result in the shift of theJ.E. Jack Rensel, Dale A. Kiefer, John R.M. Forster, Dana L. Woodruff and Nathan R. Evanssurface water temperature anomaly to the west offish losses of mariculture fish and also wild fish in

the Green Point-Victoria Sill into the central Strait.

shallow bays. Blooms of

Displacement of the feature so far to the west ofpredictable in north Puget Sound on a time scale ofthe sill by tidal excursion may not be the onlydays, typically occurring during especially warm,

factor involved. Narrowing of the cross channel

sunny periods marked by neap tides and calm

profile to the west of the sill and turbulence ofwinds（Rensel 1995, Anderson

are somewhat2001）. Second,high velocity flow near the south end of Vancouverlarge-bodied diatoms of the genus

Island may contribute by elevating the degree of（subgenus

vertical mixing. Occasional reversals of flow patternandallowing eastern transport of surface waters occur

cultured fish at relatively low concentrations（Bellin winter and even summer（Thomson

1961, Kennedy2004）,）are capable of killing wild and1976, Rensel

1989）
. In

although no low SST zone is persistently located toacute exposures, fish death is due to clogging thethe east of the sill in the images we reviewed during

gill secondary lamellae with cells and excessive gill

the study periods of 2001 and 2002.

mucus production that interferes with respiration

The low temperature anomaly we have observed（Rensel 1993）.

and measured in the central Strait warrants further

For the present study we collected 1 andinvestigation. Other studies in the past（Herlinveaux

10 m water sample composites from all three

and Tully 1961, Collias

1974）have measured

offshore stations during our 2001 field studies. For

vertical diversion of deepwater toward the surface

comparison, samples at the same depths were also

by the Victoria-Greenpoint sill particularly on thecollected in the approximate centers of adjacentebb tide, however such results are typically sectional

bays included Neah Bay, Port Angeles Harbor

views and do not indicate regular breaching of theand Inner Dungeness Bay（1 and 5 m composite）.

surface layer. The feature is highlighted in satellite

Samples were preserved to 1% final concentration ofimagery because of the greater temporal and spatial

formalin and later identified and enumerated using

coverage of a feature in context to the surrounding

settled subsamples and an inverted microscopewater masses and topography. The seasonal and（Hasle 1978）.

interannual nature of this feature and linkages toOverall, diatoms were represented by 55 species

other parameters such as dissolved oxygen andor taxonomic groups, dinoflagellates by 27 species

salinity should be investigated to further understandand taxonomic groups, and microflagellates by 15

basic water quality conditions and effects on marine

species, taxonomic groups or size classes. At theresources.

offshore stations, total cell counts were relatively
low compared to the bays. Total diatom counts

Phytoplankton and Harmful Algae

offshore averaged 1 2 x 105 cells L−1, about an orderof magnitude less than in the nearby bays thatFew studies have documented the spatial or

averaged 1.3 x 10 6 cells L −1. A few

temporal occurrence of phytoplankton in the Strait.

cells were seen in October 2001 at very low

Fish mariculture interests have a special interest inconcentrations at offshore stations（mean 0 5 x 103

phytoplankton and harmful algae as the former is acells L−1, fish death sometimes occurs at 75 x 103

primary source of fish-sustaining dissolved oxygen incells L−1）. No cells were seen in Neah Bay or Portsurface waters while the latter may cause occasional

Angeles Harbor but 5 x 103 cells L−1 were observedfish mortality（see Anderson

2001 for casefrom samples inside Dungeness Bay. A large bloom

histories, Rensel and Whyte 2003 for overview

occurred in Puget Sound in late June 2006 afterof harmful algae and mariculture）. In the Pacificthe completion of this study and the bloom was

Northwest, two genera of harmful algae have been

observed in the Strait out to the Pacific Ocean. In

involved in kills of wild or cultured fish.

the eastern Strait the bloom was visible from an

Large blooms of the raphidophyte microflagellate
have caused occasional

airplane survey very near the south shore, but notas prevalent offshore（K. Bright, pers. comm.）.

Offshore finfish mariculture in the Strait of Juan de Fuca
were

submodel that provides a description of the response

dominant at the offshore stations composing 60 4%

Non-harmful species of

to nutrient and oxygen perturbations caused by theof the diatoms, withmore abundant thanfarm and a 3 dimensional circulation submodel. The

other diatoms. Inshore in the bays, non-harmful

simplified version of the model is available on line

composed 79 7% of the diatoms,

for demonstration at http://netviewer.usc.edu/maric

followed by 7 species of（9 9%）andulture/mariculture.htm

Skeletonema costatum （5 3%）. Approximately

The metabolic submodel of AquaModel is

2 000 cells L−1 of the harmful species Chaetoceros

budgeted for the fate of carbon ingested by the fish;convolutus were counted from offshore of Neahthese include calculations of the rates of ingestion,

Bay in early September but none were seen in

egestion, respiration, and growth. Specifically, these

additional samples from offshore of Clallam Bay atrates are functions of the average weight of fish,

the same time. Such patchiness may be common

the feed ration, the ambient temperature, oxygenwith the harmful Chaetoceros in most cases. In

concentration within the farm, and advective flow

vivo chlorophyll a measurements and laboratory

speed. The system of equations that describe rates

extractions for offshore stations ranged from 1 to 4

of metabolism were obtained by fitting functions

μg L−1.

to the data found in the extensive literature on theOverall, we expect the offshore waters of thegrowth and respiration of（Atlantic

Strait to be more suited for fish mariculture insalmon）and（sockeye）

regard to less frequency of fish-killing harmful algae.

dealing with metabolic scope for activity including

Increased phytoplankton in the bays does afford

Fry（1947）, Brett（1964, 1976）, Brettsomewhat higher dissolved oxygen concentrations

Brett and Zala（1975）and Smith, 1982.

1969,

during the summer and fall, but if certain species
of marine fish are selected this may not be a

Key features of the model are:primary consideration due to their lower respiratory

The growth rate of the fish is determined by dif-requirements for oxygen.

ference in the rate of assimilation of organic carbon（food）and the rate of respiration.

Water Column Effects Modeling

The rate of carbon ingestion and assimilation isdetermined by a single most limiting factor: either

We have developed a simulation model of marine

the size of the fish, the temperature of the water,fish farms to assess water column and benthic

the food ration, the concentration of dissolved oxy-effects, as summarized at http://netviewer.usc.edu/agen, or the swimming speed required of the fish

quamodel/index.html.

within the farm.

The model was imported into a marine,

Because water temperature of Strait is slightly be-

geographical information system called EASy

low the optimal temperature range for growth, the（Environmental Analysis System www.runeasy.com

maximum growth rate of a 0 5 kg Atlantic salmon

developed by one of us, DAK）
, which provides

is calculated to be 0 01/ day, similar to that actu-

a 4 dimensional framework （latitude, longitude,

ally achieved in Puget Sound net pens for similar-

depth, and time）to run simulation models as well

sized Atlantic salmon and significantly below theas to analyze field measurements as graphical andmaximum rate of 0 021 reported by Brett et al.

statistical outputs. Although several species of（1969）for smaller sockeye salmon. In our model,

marine fish are candidates for future culture in thethe growth rate of the fish is reduced as condi-

Strait, salmon were selected for this simulation since

tions vary from near optimum.

their physiology has been well studied, and they

Respiration rates increase with swimming speed.

may be more sensitive to low dissolved oxygen.

Such increases in respiration cause decreases inThis salmon farm model is conveniently described

growth rate when swimming speed exceeds thein terms of 3 components: a growth and metabolic

optimum range of 〜 1 to 2 body lengths per sec-

submodel of salmon within the farm, a plankton

ond.

J.E. Jack Rensel, Dale A. Kiefer, John R.M. Forster, Dana L. Woodruff and Nathan R. Evans
The supply of oxygen to the fish is described

ture light levels, DIN concentration, and dissolved

mathematically as the product of the rate of flow

oxygen concentrationof water across the gills（respiratory pumping at

grazing by zooplankton on phytoplankton which

low speeds and ram ventilation at high speeds）

is a function of temperature and concentrations ofand the ambient concentration of dissolved oxy-

dissolve oxygen concentration, zooplankton, andgen.

phytoplankton

The rate of oxygen consumption by the fish is

excretion of DIN by zooplankton, which is solely alinked to the rate of carbon dioxide production byfunction of the concentration of zooplankton

a constant flux ratio of 1 mole O2/mole CO2, andthe rate of nitrogen excretion by the fish is linked

It is assumed that all three compartments areto the rate of carbon dioxide production by a con-transported by advective and turbulent flow as

stant flux ratio of 1 gm-at N/7 moles CO2.

described above. The model displays predator-prey
oscillations which dampen over time and reach

The ideal rate of flow for culturing Atlantica steady state. The default simulations for DIN,

salmon is not known precisely, but is probably about

phytoplankton, and zooplankton stabilize at roughly

1 to 1 5 body lengths per second. In a literature

12 mg-at N-at m−3, 2 mg-at N m−3, and 3 mg-at N m−3,

review, Davison（1997）concluded that training at 1 5

respectively. In order to calculate the concentrations−1

body lengths per second（bl s ）or less improved

and rates of loss by respiration and production by

growth rate and food conversion for many teleostphotosynthesis, we have assumed a constant flux

species, but cited some exceptions in the literature

ratio of oxygen to nitrogen of 7 moles O2 per gm-at N,

showing conflicting information for Atlantic salmon

consistent with the Redfield ratio. As indicated in theand other species. It can also be concluded withaccompanying table, the inputs to this model consist

certainty that above optimum swimming speeds doof the time series of exchange coefficients produced

not result in better food conversion and growth andby the circulation model, surface irradiance, andwe would estimate that this means above 2 bl s−1 forwater temperature as well as concentrations oflarger（> 500 g）Atlantic salmon. Salmonids do notdissolved oxygen, dissolved inorganic nitrogen,require a rest period for optimum growth, survival

cellular nitrogen in phytoplankton and zooplankton.

and food conversion, continual exercise results in

Outputs of this model consist of a time series of thebetter growth than intermittent swimming（e.g.,concentrations of dissolved inorganic nitrogen andAzuma 2001）.

oxygen, phytoplankton, and zooplankton.

A plankton submodel describes the cycling

The inputs to the fish farm model are theby plankton of nitrogen and oxygen within eachdimensions and location of the farm in the array,element of the array, both within the farm and thedaily feed ration, the initial average weight andsurrounding waters. This model is similar to thedensity of the fish, as well as the water temperature,

PZN models that have been published by Kiefer

and the time series of outputs from the circulation

and Atkinson（1984）and Wroblewski, Sarmiento,and plankton models.

and Flierl（1988）. The master cycle describes thetime series of the average rates of growth, nitrogentransforms of nitrogen between three compartments,

excretion, and respiration.

inorganic nitrogen （consisting of the sum of

BOD of egested, solid material（fish feces）is notconcentrations for nitrate, nitrite and ammonia

considered since, as discussed above, the study areas

as well as urea as oxidized to nitrate）, organic

are not depositional zone and the BOD is distributed

nitrogen in phytoplankton, and organic nitrogen in

widely in the deep layer or on the bottom.

zooplankton.

The outputs consist of a
The dispersion and

The physical dimensions of the model are set
by the user, and in our simulations the transport

The three biological transforms consist of:and transformations of variables was calculated forphotosynthetic assimilation of inorganic nitrogenrectangular region or array that is aligned parallelby phytoplankton which is a function of tempera-

to the coastline. The modeling domain is 10 000

Offshore finfish mariculture in the Strait of Juan de Fuca
meters in length, 2 500 meters in width, and 30

surface mixed layer was 10 times greater that its

meters in depth. Figure 5 shows only the center ofvalue in deeper waters, and the horizontal exchange

this domain. This region consists of a 3 dimensional

velocity was 5 times greater than the verticalarray of rectangular elements each of which is 50

exchange velocity within the mixed layer.

meters in length, 25 meters in width, and 5 meters

have run simulations for winter conditions whenin depth. The farm itself with dimensions of 50m

the mixed layer extends to 30 meters, and summer

x 25m x 10m occupies 2 of the elements, both inconditions when the mixed layer extends only to 5

the center of the array with one at the surface

meters. The vertical exchange coefficients at theand one immediately below. Water as well as thesurface and the bottom of the water column are

chemical and biological variables of the model are

zero.

We

transported between adjacent elements of the array

AquaModel provides several types of graphic

by advection and turbulent dispersion. The region

displays of the dynamic 3-dimensional fields

is bounded by the air-water interface at its surface,

produced by the simulation model.

by the 30 meter bottom, and by ambient waters

include plane 2-dimensional views of the waste

along its 4 sides.

plume produced by the farm at selected depths,

These

The circulation model is a simple finite element

2-dimensional vertical transects or slices throughdescription of the movement of water and suspended

the plume, 1-dimensional depth profiles at a given

and dissolved materials caused by advection andlocation, and time series plots of current speed, theturbulent dispersion. Such circulation is describedmean growth rate of fish, and the concentration of

in terms of a box model in which flow occurs acrossany variable of within the farm.

5 sides of those elements found at the surface andFig. 5 is a representative screen of selectedbottom and across all 6 sides of all other elements

outputs for the farm simulation model with oxygen

at intermediate depths deeper elements. Advective

selected as one of several available main screen

flow in the Strait is largely driven by semidiurnalviews. It is a computational array for a virtual fishtides that are oriented along the central axis of the

farm placed in surface waters offshore of Neah Bay

array. Advection is constant with depth and occurs

at our study location.

principally in the horizontal direction. We are able to

The location of a virtual farm, which initiallyrun two types of simulation, one in which the time

contains a concentration of 90 fish m−3 whose

series of advective velocity was determined by theaverage weight is 0.5 kg, is marked by a central

current meter records discussed above and anotherorange-colored rectangle. The resulting density ofin which velocity was described by a sine function

45 kg m−3 is approximately triple the maximumof 6-hour periodicity. Inputs to this model consist

loading achieved for S. salar in the past, but is usedof the time series for advective flow, the depth

here intentionally to illustrate worst-case possibleof the surface mixed layer, and the dimensions ofeffects. Total biomass is set at about 0.6 metric

the region and location within the Strait. Outputs

tons for this single large pen simulation. Larger

consist of exchange coefficients for advective andamounts of fish may be cultivated in an area, but

turbulent flow for all elements of the array.

presently offshore pens such as the Ocean Spar

Turbulent dispersion was parameterized assystem are placed and moored separately, not in aan exchange velocity whose value was someseries as with some nearshore pens. We show here

fraction of the speed of advective flow. Horizontala snapshot of the time series for a summer-timedispersion was assumed isotropic, thus the exchange

simulation during which the mixed layer is shallow,

coefficients of the 4 vertical sides of element were

irradiance is sufficiently high to drive drivingof the same value, 1/10th the advective velocity.

optimal rates of photosynthesis and grazing within

However, vertical dispersion varied depending uponnear surface waters. The orange to green plumewhether the element lies within the surface mixed

shows the horizontal distribution of waters withlayer or within the underlying water column. The

concentrations of dissolved oxygen that are below

vertical turbulent exchange velocity within theambient concentrations. Such a plume is caused

J.E. Jack Rensel, Dale A. Kiefer, John R.M. Forster, Dana L. Woodruff and Nathan R. Evansby the passage of water through the farm andcenter of the farm（at the red dot, also moveable）,

subsequent mixing with surrounding waters. During

the time series of the rate of advection（current

a simulation the plume will spread toward the east

velocity）, and the instantaneous rate of growth ofduring the flood tide and then recede and spreadthe fish over time.

to the west during ebb tide. The magnitude of the

Similar dynamic 3-dimensional views of theoxygen reduction within the plumes will vary withfarm s waste plumetidal flow; highest during slack flow and lowest

concurrently for other variables of interest suchduring peak tidal flow. These changes are complex

as nitrogen, phytoplankton and zooplankton. Since

and not only depend upon cumulative effects ofthe excretion of dissolved inorganic nitrogen andthe near-term history of advective and turbulent

urea by the fish in the farm is proportional to thetransport within the array but also depend upon therate of consumption of oxygen, the waste plumecumulative effects of the near-term response of theis enriched in nitrogen, and its spatial distribution

fish to the changing conditions.

closely resembles that of the oxygen-deficit waters.

The longitudinal red line is a transect placed（andeasily moved）to measure conditions through the

may also be displayed

The distribution of phytoplankton and zooplankton
are unaffected by the farm as discussed below.

centerline of the plume; it yields a vertical transectof oxygen vs. depth that is shown in the lower left.

Analyses of Model Simulations

At this time in the simulation the graph shows theconcentration of oxygen is lowest within the pen

We have run the fish mariculture model forwhich extends to a depth of 10 m. The other X-Ysummer and winter conditions, and examined theplots display a vertical profile of oxygen within the

results in terms of three key questions.

Fig. 5. Screen view of outputs from the simulation model showing just a few of thepossible plots or profiles available for display and output to file. See text for explanation.

Offshore finfish mariculture in the Strait of Juan de Fuca
First, will the operation of a single farm stimulate

growth rates decline as ambient current velocities

algal blooms within the farm s nutrient enriched

exceed 〜60 cm s−3 for fish of the size modeled

waste plume?

Our simulations produced nohere. The metabolic cost of swimming against thephytoplankton enrichment much less a bloom.

increased current diminishes the reserves that

This result is easily explained by the fact that the

support growth. Furthermore, growth rates decline

ambient concentration of the limiting nutrient in thewhen oxygen concentration declines within theStrait, dissolved inorganic nitrogen, is much higher

farm falls. This occurs during slack water whenthan the concentrations that are know to limit

water exchange within the farm is diminished, andphytoplankton growth（Bowie et al. 1985, Rensel

the condition is exacerbated when the tidal flow

Associates and PTI Environmental 1991, Mackas

reverses direction, thereby sweeping water fromand Harrison 1997）. Even though the concentration

the oxygen-depleted waste plume through theof dissolved inorganic nitrogen is higher in thefarm. It is also exacerbated by decreases in thewaste plume than in the surrounding waters, there

low concentrations of oxygen of ambient waters

is no increase in the growth rate of phytoplankton,that occur during summer and early fall when cold,

because their growth rate is already nutrient

oxygen-depleted water is upwelled or advected tosaturated. In addition, because rates of turbulent

the surface of the Strait.

dispersion in the Strait are high, the residence timeof the phytoplankton within the waste plume is

Discussion and Conclusions

relatively short, a few minutes to less than a day.
The second question is: will the operation of aThis study indicates that the high energy study

single farm form an oxygen-depleted waste plumezone near the south shore of the Strait of Juanthat is of significant ecological concern?

Ourde Fuca is suitable for finfish mariculture withsimulations showed that during times in the tidal

minimal or even no measurable adverse effects on

cycle when flow is slow the concentrations ofbenthic or plankton components. Dissolved nitrogen

oxygen within the farm are much reduced, sufficientconcentrations are constantly high, while standing

to temporarily reduce the metabolic rate of thestock of phytoplankton is relatively low.

fish. However, the simulation also revealed that

limitation and some grazing are the factors that limit

the oxygen-deficit plume extended less than 50m

phytoplankton growth in the Strait. Benthic impacts

downstream. Both the short duration of slack waterfrom fish mariculture facilities will be transientand horizontal dispersion once flow accelerates limits

and limited in extent, as resuspension and fast

the spatial extent of the plume. Many measurements

transport rates will rapidly spread fish fecal matterup and downstream of commercial salmon farms

for long distances downstream of the pens where

by Rensel（1989）and more extensively by Heinig

it can be decomposed and biologically assimilated.

（1998, summarized by Normandeau Associates andAquaModel simulations provided a useful tool toBattelle 2003）indicate that reduction of downstream

examine probable effects.

Light

dissolved oxygen is extremely infrequent beyond

Although environmental impacts discussed above

about 5 m downstream, usually less than 0.1

should be very limited, rigorous conditions found in

mg/L at 30 m distance and non-existent at 100 m

the Strait during storms will challenge fish culturists

downstream. Such oxygen and nitrogen production

and demand use of offshore technology and methods.

data and horizontal dispersion measurements fromOperation, maintenance, grading and harvesting

drift objects are used for model validation, alongprocedures in the cold waters of the Strait willwith other types of data.

demand innovation and careful consideration. The

Third, is the growth rate of salmon within

species of fish likely to be reared in such cages may

the farm significantly affected by environmental

include marine fish that have not been cultivatedconditions?

Our simulations indicate that thein offshore cages in the past. They may have an

growth rate of the fish in the farm is sensitive toadvantage over salmonids with regards to oxygen

both ambient and operating conditions. Specifically,requirements（e.g., Sullivan and Smith 1982）, but

J.E. Jack Rensel, Dale A. Kiefer, John R.M. Forster, Dana L. Woodruff and Nathan R. Evans
their physiological performance and stamina inmlhigh current conditions is not known in some cases.

Azuma, T. 2001. Can water-flow induce an excellent

Creative configuration and arrays of pens to reduce

growth of fish; effects of water flow on thesurface currents or stocking of relatively large fish

growth of juvenile masu salmon,

may be means to deal with elevated current velocity
effects.

World Mariculture 32: 26-29.
Bell, G.R. 1961. Penetration of spines from a marine

There are other factors besides those considereddiatom into the gill tissue of lingcod（

here in siting of fish mariculture in the coastal）Nature（Lond.）192:279-280.

zone of the Strait. For example, the south shore ofBowie, G. L., Mills, W. B., Porcella, D. B., Campbell,

the central Strait has very prolific kelp beds that

C. L., Pagenkopt, J. R., Rupp, G. L., Johnson, K.

generate large rafts of floating, senescent material in

M., Chan, P. W. H., and S.A. Gherini. 1985. Rates,

the late summer and fall. Test versions of offshore

Constants and Kinetics Formulations in Surface

cages placed offshore of Whiskey Creek in 1991

Water Quality Modeling. 2nd Ed., US EPA,

where able to withstand forces generated by thisAthens, Georgia, EPA 600/3-85/040.

material impinging on the nets for long periods.

Brett, J.R. 1964. The respiratory metabolism andOther regions of the south shore have much lessswimming performance of young sockeye

kelp and resulting flotsam. Mariculture siting must

salmon. J. Fish. Res. Bd. Can. 21:1183-1226.

also consider native Tribal fishing, sport fishing andBrett, J.R. 1976. Scope for metabolism and growth ofcommercial fish and shellfish areas, recreationalsockeye salmon, Oncorhynchus nerka, and someand commercial navigation use, habitats of special

related energetics. J. Fish. Res. Bd. Can. 33:

significance, marine bird and marine mammal habitat

307-313.

and shoreline residents view and aesthetic concerns.

Brett, J.R., Shelbourne, J.E. and C.T. Shoope. 1969.

There is precedence for dealing with site-specific

Growth rate and body composition of fingerling

topics such as these. Washington State government

sockeye salmon,

has promulgated monitoring requirements, operation

to temperature and ration size. J. Fish. Res. Bd.

guidelines, a programmatic impact statement andCan.26:2363-2394, in relation

2 sets of NPDES permits（SAIC 1986, WDF 1990,

Brett. J.R. and C.A. Zala. 1975. Daily patterns of

WDOE 1996, WDOE 2002）to document impacts

nitrogen excretion and oxygen consumption of

based on ten years of annual impact monitoring thatsockeye salmon（

led to strict impact limits and rules. This regulatory

controlled conditions. J. Fish. Res. Board Can.

experience and set of rules can be applied to fish

32:2479-2486.

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Cannon, G.A.（Ed.）. 1978. Circulation in the Strait

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marine fish mariculture.

observations. NOAA Technical Report EFL
399-PMEL 29. Pacific Marine Environmental

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水研センター研報，第19号，131−141，平成19年
Bull. Fish. Res. Agen. No. 19, 131‑141, 2007

博士号論文

Direct payment system to promote the appropriate managementof aquaculture grounds
Yasuji TAMAKI＊Abstract: Aquaculture occupies an important role in Japanese fisheries; it also plays various
social, cultural and economic roles and functions other than food supply, but is becoming aproblem in that leftover feed and excrement causes coastal environmental pollution. A subsidy system is already in place in the EU and USA to compensate for the decreased revenue
and increased costs incurred by reducing environmental damage by agriculture. In thisstudy, I consider a plan to apply a similar subsidy system to Japanese aquaculture.
Key words: direct payment system, aquaculture, multifunctionality
respectively, of marine fisheries output and 45% andMaterials and methods

42%, respectively, of freshwater fisheries output（Fig.
1）. According to the national census of fisheries,

Aquaculture is one of Japan s key industries: it

the number of marine aquaculture businesses inprovides a steady supply of various types of fish

2003 was 23 068, 17% of the total number of fishing

all nationwide. Aquaculture also has various social

businesses. The number of freshwater aquaculturists

and cultural roles and functions. The financial

was 4 495 in 2003.

state of aquaculture businesses, however, has been

For the production of major fish species inworsening for a number of reasons, including falling

2002 in marine aquaculture, the output of marine

prices. The number of businesses is shrinking andaquaculture was 162 000 tons for yellowtail andtheir operators are aging. In this paper, I describe

72 000 tons for red sea bream; that of shellfish

the current state of the Japanese aquaculture

aquaculture was 272 000 tons for the common scallop

business through analysis of statistical data andand 221 000 tons for oysters; and that of seaweedcase studies. Another point I discuss in the paper

aquaculture was 436 000 tons for laver, 54 000 tons

is pollution problems, including the damage causedfor

to wild fishing grounds by uneaten fish food used2）. The output of laver andin aquaculture and excrement of fish. I focus on thedecreasing in the last few years. In inland water

direct payment method applied in the agricultural

aquaculture, major fish species cultured include

field in some other countries and analyze it for its

eel with an output of 21 000 tons, trout with 14 000

applicability to the Japanese aquaculture industry.

tons, carp with 9 000 tons, and sweetfish（ayu）withand 51 000 tons for（Fig.
has been

7 000 tons（Fig. 3）. The production of each of these
Results

is decreasing, with that of eels showing the steepest
decline.

（1）The current state of Japanese aquaculture

Concerning the financial condition of

In 2002, Japanese marine aquaculture yieldedaquaculturists, the annual average fishery profits in

1 333 000 tons, worth 478 3 billion yen, and2002 was 7 745 000 yen for oysters, 7 654 000 yen for

freshwater culture yielded 51 000 tons worth

laver, 6 873 000 yen for common scallops, 4 725 000

43 8 billion yen. These account for 23% and 23%,

yen for pearls, and 3 840 000 yen for

2006年 月26日受理（Received. June 26, 2006）＊
National Research Institute of Fisheries Science, Fukuura, Kanazawa, Yokohama 236-8648, Japan

These

Yasuji TAMAKI

Fig. 1. Aquaculture proportion of the whole fisheries

Fig. 2. Change of Marine Aquaculture Productuin

culturists earn more than the average profits for all（Fig. 4）. Of 21 129 individual marine aquaculturists,fishing businesses. However, culturists of yellowtail

27%, or a little more than one-fourth, know who will

（2 799 000 yen）
, sea bream（1 770 000 yen）, andtake over the business when they retire. Of 3 457

pearl oyster（792 000 yen）
, earn below the average

individual freshwater aquaculturists, only 15% haveof 2 871 000, evidence of their poor financial state

successors（Fig. 5）. Inland water aquaculturists

Direct payment system to promote the appropriate management of aquaculture grounds

Fig. 3. Annual variation of Freshwater Aquaculture Production

Fig. 4. Annual Average Profits of Aquaculture in 2002

are aging: 43% of male operators of inland water

due to growing imports and the stagnant domestic

aquaculture are aged over 60. The majority of

economy. However hard each aquaculturist tries toJapanese aquaculturists are small-scale operators

improve their financial condition, it is not enough todependent on family labor. The major cause ofbring about any significant improvement.

their financial deterioration is a drop in fish prices

A comparison of the age constitution of male

Yasuji TAMAKI

Fig. 5. Successors of Aquaculturist in 2003

FIg. 6. A comparison of age construction of male fishery workers in 1998

fishery workers in 1998 between coastal fishing boat

below.

fisheries and aquaculture businesses, according to1）Food security

the census, shows 59% in fishing boat fisheries to be

Unlike ordinary fishing, where fish are caught asover 60 years of age, whereas fewer aquaculturists

a natural resource, aquaculture can reliably supply（43%）are over 60（Fig. 6）.

selected fish species with the help of appropriatetechnology. Some aquaculture seeds, such as（2）The various roles and functions of aquaculture

yellowtail, oyster, or common scallop, may have to

Aquaculture has multifaceted functions in addition

be taken from natural resources, but others, suchto the supply of fish. Each such function is explained

as red sea beam, prawn, or laver, can be artificiallyDirect payment system to promote the appropriate management of aquaculture grounds

Fig. 7. Production Ration of Aquaculture in 2003

produced. Even when culturing natural seeds, taking

are eluted into the water. Seaweed also provides

special care of life stages at which fish seeds have ashelter to young fish and the larvae of many otherhigher natural mortality rate can reduce the death

creatures, contributing to biodiversity. In addition

ratio and minimize loss of resources.

to the benefits obtained from seaweeds themselves,

In addition, aquaculture produces the types of fish

there are cases where the bamboo poles used inthat are particularly in demand. In fact, certain fish

aquaculture for attachment of laver in the water can

species are characterized by high production ratios,

serve as substrates for the larvae of short-neckedsuch as 100% for laver, oysters, and pearls; 95% forclams, promoting favorable growth of shellfish, 82% for red sea beam, 76% for yellowtail,grounds. In waters where aquaculture facilities are

67% for prawn, 47% for common scallop, 46% for

set up, rafts and net pens used to aquaculture canflatfish, 38% for globefish, and 33% foralso provide shelter for wild fish. It is impossible toas well as, in freshwater culture, 97% for eel, 73%

carry out seine fishing or trawl netting in the samefor carp, 51% for trout, and 40% for sweetfish（ayu）

waters, thus promoting the preservation of marine（2003）. There are many fish species that would

resources. When filter-feeding marine species,

disappear from the market or be in very shortsuch as bivalves and sea squirts, are cultured,supply if it were not for aquaculture（Fig. 7）. Giventhey filter seawater and simultaneously reduce thethese circumstances, it is logical to conclude thatorganics in the water. Silver carp and white crucianaquaculture plays a major role in food security.

carp produced in freshwater culture grow on2）Environmental improvement（Table 1）

phytoplankton and do not need to be fed, therefore

Seaweeds convert carbon dioxide in the seawater

reducing the pollution load on lakes. One kilogram of

into oxygen through photosynthesis. They

silver carp filter a cubic meter of water and eat 20

also prevent eutrophication of the seawater bygrams of phytoplankton daily（Ibaraki Prefecture,immobilizing dissolved nitrogen and phosphorus. In

1996）.

cultured seaweed grounds, unlike natural seaweed3 ）E x c h a n g e b e t w e e n u r b a n a n d f i s h i n ggrounds, we can recover most of the immobilized

communities

nitrogen and phosphor before these elements

Aquaculture promotes exchange between urban

Yasuji TAMAKI
Table 1. Environmental improvements by aquaculture
Aquaculture species
Seaweeds

ExampleConvert carbon dioxide in the seawater into oxygen
Immobilizing nitrogen and phosphor
Provide shelter to young creatures

Bivalves and Sea squirts Filter sea water and reduce organics in the water
Silver carp and White
crucian carp

Filter sea water and reduce organics in the water

Aquaculture facilities（rafts and net pens）

Provide shelter for natural ﬁsh
Stop the ﬁsheries operation of natural resources andprovide nursary groundand fishing communities. For instance, a fisheries

and learned how to use it in cooking. There are also

cooperative in Kagawa Prefecture has a cultured

exchange promotion programs in which elementary

oyster ownership system in which consumers buy

and junior high school students visit a fishing village

oysters at the seeding stage. Later, they are entitledas one of their school excursion destinations andto experience the harvesting of the grown oysters

take part in various events alongside the people

or have them directly delivered by delivery service.

of the village to gain a closer and more personal

In this system, an aquaculture rope with someunderstanding of how they live. Since the culture

70 oysters attached is sold at 2 200 yen. Orders

grounds are close to the port and located in calmer

for some 1000 ropes are received per year. They

waters than in the case of offshore fishing, programs

even come from outside the prefecture, such asthat feature actual experience of aquaculture arefrom Okayama or Tokyo. This cooperative has also

very popular with city people as safe and accessible

discovered that many consumers prefer to come toopportunities to experience this type of fishery. It is

get the oysters themselves to having them delivered.

a valuable experience for young people to actually

Another fisheries cooperative is advertising forfeed cultured fish species and see how shellfish

purchasers of oyster culture ropes, at 2 500 yen

species and seaweeds are cultured. They caneach, but only accept orders from consumers within

actually see for themselves what the sea has to givethe same prefecture. In 2000, they received somethem. Another example is fishing ponds using the

500 orders. In Kagawa Prefecture, some culturists,

sea surface in Mie and Hyogo Prefectures, or fresh

including the said cooperative, have their own

water in other prefectures. These fishing ponds

small restaurants that serve grilled oysters during

are very popular among angling fans, not to mention

the winter. A different cooperative offers all the

beginners and children who tend to be seasick inoysters you can eat at 2500 yen per person and, inopen waters, because they can experience fishing in

1999, achieved sales of 10 million yen. In Kanagawa

a safe and unthreatening environment. Many of thePrefecture, a hands-on experience program thatfish caught from these ponds are cultured species.

offers a course inculture was provided for

Aquaculturists facilitate exchanges between cities

100 groups at a fee of 3000 yen per group. Visitors

and fishing villages by stocking these ponds withtook part in seeding ofand studied thefish and opening them to the public. Aquaculturists

details of seaweed aquaculture and its environmental

can also obtain a profit by selling fish for stocking

advantages, including how it purifies water. In

the ponds. Oyster culture rafts are ideal nests for

November, they learned how to culture seaweed

black sea bream, a popular fish with anglers, forand in February experienced harvesting of thetheir shade and the plants and animals that cling

seaweed, took classes on the nutrients into them. In Ishikawa Prefecture, these rafts areDirect payment system to promote the appropriate management of aquaculture grounds
Table 2. Example of exhange between urban and ﬁshing communities
Area

ExampleKagawa Prefecture

Cultured oyster ownership system

Kagawa Prefecture

Small restaurants that serve grilled cultured oyster

Kanagawa Prefecture

Experience of

Mie Prefecture andHyougo Prefecture

Provide cultured ﬁshes to Fish ponds

Ishikawa Prefecture

Oyster culture rafts are provided for sport ﬁshing

Shimane Prefecture

Takes anglers aboard recreational ﬁshing boats to thewater near their aquaculture grounds

Freshwater

Fishrman s cooperative release cultured seeds for sportﬁshingFishing Village

School excursion

cultureTable 3. Maintenance of traditions
CultureMaintain Japaneseculinary traditions

ExampleEnjoy eel on speciﬁc days in summer
Laver for Rice ball（Onigiri）and Rice roll（Norimaki）
Sushi

Japanese garden

Fancy carp

Local festivals

Goldﬁsh scooping

provided by some culturists for sport fishing. Aof aquaculture that it provides types of fish thatfisheries cooperative in the Oki Islands, Shimane

would run short if we relied exclusively on natural

Pref., who know that large wild fish are attracted

resources. Providing these fish also helps to keep

to their fish culture grounds to eat the fodder that

alive Japanese culinary traditions. For example, itleaks out, take anglers aboard recreational fishingis a custom to eat eel on certain days in summer.

boats to the waters near their aquaculture grounds.

Without aquaculture, however, the lack of eels

These anglers pay 10,000 yen per person for thiswould lead to this custom s disappearance. Red

experience and are allowed to take home up tosea bream is very popular to the Japanese style

three red sea bream. The cooperative had somewedding reception. Laver, indispensable for rice

250 customers in five months in 2002. Freshwaterball and sushi, is 100% supplied by aquaculture.

fishermanʼs cooperative often release cultured

Yellowtail, red sea bream, and common scallop areseeds for sport fishing. According to the census,

also essential materials for sushi and are supplied

the total number of sport fishers in fresh waterby aquaculture. Fancy carp（nishiki-goi）are anin 2003 was 7,770,000（excluding those for bass）.

invaluable part of many Japanese gardens. Without

Thus, aquaculture plays numerous roles, including

aquaculture,exchange between urban and fishing communities

entertaining part of local festivals and a traditional

and provision of recreational opportunities to urban

festive pastime for children, would disappear. Thesedwellers（Table 2）.

aquarium fish species are also the products of4）Maintenance of traditions（Table 3）

aquaculture.

I have already pointed out as one of the features

goldfish scooping,an essential and5）Formation and maintenance of local communities

Yasuji TAMAKI
Aquaculture needs calm waters and clear fresh

feeding, it is reported that feces and pseudofeces

water and is thus often conducted in places far from（rejected food particles embedded in mucus）

major cities. The economy of many such places

tend to accumulate on the sea floor. Katsuhiko Itorelies entirely on fisheries and related industries.

（1994）compared the sediment in the water at the

Aquaculture helps dilute the otherwise concentrated

mouths of bays not used for aquaculture with those

population in cities and settle people in remote areas

employed for shellfish（pearl）culture grounds andby providing economic security. At the same time,those with fish（red sea bream and yellowtail）. The

it plays other associated roles, such as monitoring of

sediments were analyzed for total amount of sulfides,

national borders, preservation of national land andoxidation-reduction potential, total amount of organic

protection of the landscape.

carbon, total amount of nitrogen, and the content
of pheo-pigment. The results showed sediments（3）Pollution of fishing grounds by aquaculture

to be worst near fish culture grounds, followed by

So far I have dealt with the bright side ofshellfish culture grounds and then non-cultured bays

aquaculture by discussing the originally intended and（Table 4）. Red tides often occur in the waters withvarious roles and functions of aquaculture. However,

the most serious pollution, with the negative impact

it is also true that aquaculture causes problems.

of such pollution affecting both cultured products

In aquaculture which involves feeding, residual

and natural resources. Ito reported that toxic red

fodder and feces are swept out of the grounds andtides, such as those comprisingcause pollution of neighboring waters and the sea
floor. Even with shellfish culture, which requires noor, occur over wider areas in waters wherefish culture is more common and extensive.

Table 4. Comparison of Bottom environment with Aquaculture grounds to non
aquaculture grounds in Gokasyo-bay（average 1984-1985）
Aquaculture

Non aquaculture ground

Pearl

Fish

Bay-entrance

Total amount of sulﬁdes（mg/g dried mud）

0 16

1 96

0 004

Eh（mV）

＋172

−11

＋323

Content of pheopigment（μg/g dried mud）

45 3

98 2

49

Total amount of organic carbon（mg/g dried mud）

20 4

23 4

21

Total amount of Nitrogen（mg/g dried mud）

2 51

3 53

0 37

Katsuhiko Ito（1994）

Table 5. The Environmental Benefit Index of The
Conservation Reserve Program（CRP）of USA● Water quality（maximum 20 points）● Wildlife（20）● Land erosion（20）● Reforestation（10）● Desired rent
Eiichiro Nishizawa（2001）

Direct payment system to promote the appropriate management of aquaculture grounds（4）Direct payment methods used to support

and for recreational use（Table 6）（Keiichi Ishii,

agriculture in some countries

2001）. One example is the system of environment

Schemes based on the direct payment method

payments introduced in France. The overall

assume that existing modes of agriculture impose

programs in this system generally include reduction

loads on the environment, and are designed toof input, conversion of farmland to grassland,compensate for the increased costs or loss of income

long-term suspension of production, and reduction ofthat result from efforts to make agriculture morerearing density, and, as local projects, preservation

kind to the environment.

of biotopes and prevention of farmland decay.

1）Agriculture in the USA

Grassland promotion grants are provided nationwide

The Conservation Reserve Program（CRP）is a

in France. The highest grant per contract is for

scheme created as part of the Food Security Act of

reduction in rearing density, at about 27,000 francs

1985 to remove fragile and easily eroded farmland（about 565,000 yen）
（Table 7）. In 1997, 1.9 billion

from production for 10 to 15 years. Instead, thefrancs were spent on the agricultural environment

United States Department of Agriculture（USDA）

program. Of this amount, 1.63 billion francs werepays rent on the retired land and 50% of the cost

spent on the promotion of conversion to grassland.

incurred in maintaining the land s vegetation

By type of operation, 69% of operators covered bycover. As of October 2000, 13 million hectares ofthe program were sheep and goat farmers and 55%

farmland, 8% of total farmland, was retired, with

were for beef farmers（Keiichi Ishii, 2001）.

more than 80% of this retired land turned into
grassland. A total of 290 000 farmers participated in

Discussion -Application of the direct payment

the program. Rental payments made per year are

method to Japanese aquaculture$111 5 per hectare, and $4 800 per farm on average.
Annual spending by the USDA on the CRP totaled

Assuming that control of aquacultural activity$1 7 billion, accounting for half of environmental

based on a system using the direct payment method,preservation spending. The rental payment andas practiced outside Japan, would be effective incost-share payment to be made by the USDA are

improving the fishing environment, I reviewed adetermined based on a environmental benefit index

potential form of direct payment system applicablecalculated from the total sum of points for water

to the Japanese case. If this method were introduced,

quality（maximum 20 points）, wildlife（20）, landit would run the risk of sending a clear message

erosion（20）, reforestation（10）and desired rent

officially stating that aquaculture without control is（Table 5）（Eiichirou Nishizawa, 2001）.

an environmental threat. It is also important to set

2）Agriculture in the EUa certain standard that does not violate the polluter

EU agricultural environment programs provide
subsidies to programs to limit the input amount ofs responsibility principle and to make payments toaquaculturists who satisfy the standard.

fertilizers and agricultural chemicals, maintenance of

Actions or efforts to reduce environmental loads

already reduced input, introduction and maintenanceinclude, for fish culture by feeding, reduction inof organic farming, introduction of extensive

rearing density, amount of fodder, and amount of

production of plants, conversion of cultivated landchemicals; for shellfish culture without feeding,to extensive grassland, reduction of rearing density

reduction in rearing density; and for aquacultureof cows and sheep, introduction of farming methods

operated inland, installation of wastewater treatment

necessary for preservation of the environment andfacilities. Changing to fish species that have lesspreservation of the rural atmosphere and landscape,environmental load is also a strategy for reducing

protection of rare or threatened breeds, maintenanceenvironmental load. Reduction in CO2 of vessels andand management of abandoned farmland or forests,

processing machine such as laver molder. Changing

retiring of farmland for over 20 years for protection

floats of plastics and foam polystyrene to aluminumof the biotope and water quality, and management

floats. Direct payment for doing this may be logicallyof farmland for easier access by the general public

equivalent to the direct payment method used forYasuji TAMAKI
Table 6. EU Agricultural Environment Program①Limit the input amount of fertilizers and agricultural chemicals, maintenance of already
reduced input, introdudtion and maintenance of organic farming②Introduction of extensive production of plants, conversion of cultivated land to extensive
grassland③Reduction of rearing

density of cows and sheep④Introduction of farming methods necessary for preservation of the environment andpreser-vation of the rural atmosphere and landscape, protection of rare or threatened
breeds⑤Maintenance and management of abandoned farmland or forests⑥Retiring of farmland for over 20 years for protection of the biotope and water quality⑦Management of farmland for easier access by the generalpublic and for recreational use

Table 7. The system of environment payments introduced in France①Overall programs
・Reduction of input（422）
・Conversion of farmland to grassland（236）・Long-term suspension of production（Biotopes（302）,Water maintenance（247））
・Reduction of rearing density（565）
・Protection of rare or threatened breeds（52）・Switch to organic farming（485）②Local projects
・Preservation of biotopes（242）
・Prevention of farmland decay（226）
・Prevent a risk of a fire
（427）
・Water maintenance（349）③Provided nationwide in France
・Grassland promotion grants（283）（）means average grant per one contract（Thousand yen）

Keiichi Ishi（2001）
Table 8. Actions or efforts to reduce environmental loads
Type

ExampleFish aquaculture byfeeding

Reduction in rearing density, amount of fodder, amount ofchemicals
Change to seaweed aquaculture

Shellﬁsh aquaculture
without feeding

Reduction in rearing density
Change to seaweed aquaculture

Inland water aquaculture

Installation of wastewater treatment facilities

Aquaculture

Reduction in CO2 of vessels and processing machine
Changing ﬂoats of plastics and foam polystyrene toaluminumDirect payment system to promote the appropriate management of aquaculture grounds

Fig. 8. The Schematic Diagram Showing the Relationship between
the Environmental benchmark and Aquaculture Income
agriculture in some other countries. For example, it
References

is considered worthwhile to plan coordination withfishing ground improvement plans in the Law toEnsure Sustainable Aquacultural Production（Table
8）.
According to the schematic diagram showing therelationship between the environmental benchmark

Ibaraki Prefecture Inland Water Fisheries
Experiment Station, 1996: Biology of the Fish ofLakes Kitaura and Kasumigaura, Ibaraki, p 10
（in Japanese）

and aquaculture income shown here, for R1, theIto Katsuhiko, 1994: Environmentally Friendly

production curve of ordinary aquaculture, production

Propagation and Aquaculture, in Fisheries andincreases with the rise of the environmental

the Environment （ed. by Shimizu Makoto）,

benchmark until reaching a certain point E1. But

Koseisha-Koseikaku Publishing Co., Tokyo, pp.

after E1, it is necessary to reduce production to

20-21（in Japanese）

maintain the environmental benchmark. For C1,

Ishii Keiichi, 2001: Development of Environmental

the cost curve of ordinary aquaculture, past E1,

Payments in France, in

Direct Payments tocosts are reduced due to production control, but theand Environmental Preservation in Mountainous

balance turns negative due to a large reduction in

Areas （ed. by Goda Yasuyuki）, Ie-no-Hikari

income. R2 is production curve of environmentally

Association, Tokyo, p. 117（in Japanese）

frindly aquaculturists, increase of production does

Ishii Keiichi, 2001: Development of Environmental

not give big influence to environmental benchmark.

Payments in France, in

Direct Payments to

C2 is the cost curve of environmentally friendly

and Environmental Preservation in Mountainous

aquaculturists, who have a minus balance, since

Areas （ed. by Goda Yasuyuki）, Ie-no-Hikari

the cost is greater than for ordinary aquaculturists.

A s s o c i a t i o n , T o k y o , p p 1 2 0 - 1 2 1 , 1 2 5 （i n

On the other hand, C3 is the cost curve of an

Japanese）

environmentally friendly aquaculturist who received

Nishizawa Eiichirou, 2001: US Preservationa grant for cost reduction efforts. They make a

Retiring Program, in Direct Payments to andprofit until the break-even point at E2. E2 is a higher

Environmental Preservation in Mountainous

environmental benchmark than E1（Fig. 8）.

Areas （ed. by Goda Yasuyuki）, Ie-no-Hikari
A s s o c i a t i o n , T o k y o , p p 1 5 4 , 1 6 7 - 1 6 8 （i nJapanese）

水研センター研報，第19号，143−147，平成19年
Bull. Fish. Res. Agen. No. 19, 143‑147, 2007

Nutrient uptake by(Yendo) Okamura andapplication as an algal partner of fish-alga integrated culture
Hajime KIMURA※1, Masahiro NOYOYA※2

and Daisuke FUJITA※2

Abstract : Nitrogen (N) and phosphorus (P) budgets in a fish-alga integrated culture werestudied using an edible kelp，
and the red sea breaminTanabe Bay, Japan. The kelp was cultured on one rope (16 m in length) surrounding a fishculture cage (3 x 3 x 3 m) to reduce the loads of fish discharge. From 2002 December to2003 March, 260 young red sea breams (172.7 g in average), were cultured in the cage by
feeding 18.4 kg of artificial compounds containing 1435 g nitrogen and 282 g of phosphorus.
At the end, 8.3 kg of fish growth was obtained; 243 g (16.9 % of the given feed) of N and 71
g (25.2 %) of P were stored in the fish bodies. During the culture, kelp absorbed N and P atestimated rates of 3.11μg atm/wet g/hr and 0.16μg atm/wet g/hr, yielding 161 kg of commercial size on the rope. The total amounts of N and P absorbed by kelp corresponded to40.5 % and 25.9 % of those in given food, respectively. This is the first report of the total N
and P budgets in a fish-alga integrated culture in Japan.

Introduction

includingparticularly in the formof fish-alga integrated culture. Although integrated
An edible kelp,(Laminariales,

cultures are worldwide concerns (ex. Troell

Alariaceae), which is close to a widely distributed

2003, Neori2004), the combination of red sea

and utilized species,

bream andspecies is limited to Kitadai &, is localized

in southern parts of warm temperate in Japan

Kadowaki (2004 b), in which nutrient uptake by(Okamura 1915). As the unique kelp is commercially

was determined. In the present study,

important as a local high-priced food, culture has

the authors reported the nitrogen and phosphorus

been attempted in southern coasts of Wakayama

budget in a red sea bream-

Prefecture (Kimura & Notoya 1996). On the otherculture.

hand, cultures of red sea bream,

integrated

havebeen popular in these areas (Uede & Takeuchi2004). As the fish cultures are localized in innerbays, where seawater exchanges are limited, lords

Materials and Methods
Culture of red sea bream:of nitrogen and phosphorus discharged from fish

Red sea bream was cultured in the Mera Cove of

cultures, including excretion and defecation from

Tanabe City in Wakayama Prefecture (Fig.1) fromfish, dissolution from residual feeds or re-suspension

2002 Dec. 14 to 2003 Mar. 12. A total of 260 fish offrom the bottom sediments, are becominga mean body weight of 172.7 g were kept in a cageproblematic (Uede ＆ Takeuchi 2004). These nitrogen(3x3x3m) fixed at the sea surface and satiated byand phosphorus, however, are essential nutrientsfeeding soft-dry pellet (SP)(See Table 1) 4 days (infor the growth of seaweed. Therefore, enrichedevenings) a week. This type of feed was used toseawater stagnating around fish culture is highly

minimize the load to the ambient water. The total

expectant for cultures of commercial seaweeds

weights of fish were determined at the beginning

2006年 月26日受理（Received. June 26, 2006）※1
Fish Farming Laboratory Fisheries Experimental Station, Wakayama Research Center of Agriculture, Forestry and Fisheries, Mera, Tanabe,
Wakayama, 646-0058, Japan.
※2
Laboratory of Applied Phycology, Tokyo University of Marine Science and Technology, Konan-4-5-7, Minato-ku, Tokyo, 108-8477, Japan.

Hajime KIMURA, Masahiro NOYOYA and Daisuke FUJITA
and the end after 89 days culture. The seawaterloads discharged from cultured fish were estimatedtemperature ranged between 12.2 and 19.2 ℃ during

by subtracting the value of each component obtained

the culture.

from the harvested fish bodies from that obtained

Estimations of nitrogen and phosphorus from redsea bream:from the total weight of given feed. Nitrogen was
assumed to be 16 % of proteins contained in the feed

In analysis of fish body composition, 5 fish samples

and the fish bodies.

were taken at the beginning of the experiment, andCulture of kelp:

whole fish bodies were used after slicing. Water,

Juveniles of, produced in Fishprotein, lipid, ash and phosphorus contents were

Farming Laboratory Fisheries Experimental

determined using methods of the normative thermal

Station, Wakayama Research Center of Agriculture,desiccation, quantitative nitrogen desiccation, Soxhlet

Forestry and Fisheries on 2002 Nov. 28, were kept

extraction, direct ashing and vanado-molybdic acidin the form of square (4 × 4 m) at a depth of 1 m

absorbance, respectively. Nitrogen or phosphorus

around the cage ofcultures using a ropeof 16 m long. The strings of 30 mm long, on which
juveniles attached, were stuck into the rope (18 mm
in diameter) at 20 cm intervals, resulting in sticking
out of each string end by 6 mm long on both sidesof the rope. Namely, a total of 80 strings with two
ends were set around the cage. As the growth ofvaried, all of the thalli growing on
one end of a string (called unit string hereafter)
were collected from 5 sites of the rope. The mean
weight and number of kelp per half-side string
was estimated after removing excess water. The
samplings were conducted on 2002 Dec 28, 2003 Jan.
6, 20, 30, Feb. 10, 21 and Mar. 14. On the last day,Fig. 1. Map showing the location for cultivation of
red sea bream and(Yendo) at
Shimohaya Bay in Wakayama Prefecture.（★）The
place which examined.

although some of thalli were matured, matured ones
were eliminated.
Estimations of nitrogen and phosphorus
absorbance by cultured kelp:
Nitrogen and phosphorus levels incorporated
into the kelp from sea water were estimated from

Table 1. Composition of the experimental a diet
Ingredients
Jack mackerel meal
50％
Defatted soybean meal
5
Corn gluten meal
5
Wheat flour
17
Pregelatinized starch
5
Pollock liver oil
15
P-free mineral mix
1
Vitamin premixture
2
Diet of nutrient content

Moisture
Crude protein
Crude fat
Crude ash
Phosphorus

weight gain of the thalli and their ratios of water,
total nitrogen and total phosphorus contents. Total
nitrogen and total phosphorus were determinedby Kjeldhal method and vanado-molybdenum
absorbance method, respectively.
RESULTS
Estimated nitrogen and phosphorus contents in
red sea bream culture: The growth and analytical

2.1
49.0
20.4
9.2
1.54

％

data (including data of feed) of red sea bream areshown in Table 2 and Table 3, respectively. The
total weight of given feed was as low as 18.3 kg for
89-day period, yielding weight gain of 8.3 kg in fish
bodies. The nitrogen and phosphorus contained inNutrient uptake by

and fish-alga integrated culture

Table 2. Results of red sea bream feeding with the EP-pellet in the 3×3×3m net cage from Dec.14 to Mar.12
No. offish
260

Average body fish(g)Initial

Final

172.7

205.3

Daily feedintake(%)

Weightgain(g)A

Growthrate(%)

Amount ofdiets(g) B

Feedefficiency

Mortality
(%)

0.42

8,297

1.19

18,30045.3

1.15

Table 3. Composition of the Whole body of red sea
bream
Diet

Body

Moisture

％

2.1

67.3

Crude protein

％

49.0

18.3

Crude fat

％

20.4

9.6

Crude ash

％

9.2

4.7

Phosphorus

％

1.54

0.85

the given feed were 1,435 g and 282 g, respectively.
Nitrogen and phosphorus pooled in the harvested
fish bodies were 243 g (cumulative rate: 16.9 %) and

Fig. 2. Changes in the weight（─●─）per culture
unit string and number （□）of blade.

71 g (cumulative rate: 25.2 %), respectively. Using
these data, the nitrogen and phosphorus loads to theambient water were calculated as 1,192 g (83.1 %)and 212 g (74.8 %), respectively.
Estimated nitrogen and phosphorus absorbance

μg atm/wet g/hr and 0.26 μg atm/wet g/hr，
respectively.

by the cultured kelp:
Changes in weight, height and number of the kelp

Discussion

per unit string were shown in Fig. 2. The kelp grew
rapidly between Jan. 6 and Mar. 14 after a lag phase

In the present study, we could obtain commercial-lasting 40 days, recording final biomass of 1,007 g

sized edible kelp

by utilizing

per unit string or 37.3 g per thallus. As 5 strings

the nitrogen and phosphorus discharged from awere stuck into 1 m of rope and each sample was

red sea bream culture, although the experiment iscollected from one end of each string, the yield waslimited in winter, when growth of the kelp is highestimated as 10 kg/m ( ≒ 1,007 kg × ２ ｘ 5) or a

(Kimura & Notoya 1996) but that of red sea bream

total of 161 kg on the rope (16 m) around the cage ofis low because of low feeding activity in
low temperatures (Fukusho 1986). For the warmer

fish culture.
Composition of the kelp blade was shown inseasons,

andTable 4. The nitrogen and phosphorus incorporated(Kimura & Tanaka 2004) are now on trial as thethrough cultivation were 483 g and 54.7 g,candidates for the algal partners.

respectively. Therefore, 40.5 % and 25.9 % of thenitrogen and phosphorus loads the ambient water(1,192 g and 211 g, see above) were assimilated by
the cultured kelp, respectively. The budgets ofIn the previous studies on red sea bream andseaweed integrated culture,(Hirata. 1993，Kitadai ＆ Kadowaki 2004a),(Kitadai & Kadowaki 2003) or

nitrogen and phosphorus in the present integrated(Kitadai & Kadowaki 2004b) was used as algal

culture were summarized in Fig. 3. Using thepartners. In these studies, however, only absorption

growth data, theuptake rates of nitrogenof nutrients by algae was paid attention without

and phosphorus by the kelps were calculated as 2.34

demonstrating any data on nutritional input andHajime KIMURA, Masahiro NOYOYA and Daisuke FUJITA

Fig. 3. Circulation of nitrogen and phosphorus at the red sea bream with
culture.

Table 4. Composition of the blade of(>16 ℃) for its browsing (Kimura 1995). Thus theculture depth ofis well coincidence

Moistureg/100g90.3

with that of the red sea bream culture usually

Total amount of nitrogeng/100g0.3

practiced near sea surface (Fukusho 1986).

Total amount of phosphorus

mg/100g

34

The present integrated system could reduce
equipments for

culture such as

anchors and floats by using a framework of the
red sea bream culture, resulting in the decrease
output from red sea bream culture. Therefore, thisof cost of equipment by ca 90 % (ca 200,000 yen)is the first report that showed the total nutrient

comparing with the case of non-integrated culture

budgets in the red sea bream-alga integrated culture.

of the kelp. Additional income (ca 40,000 yen in the

Furthermore, we could provide several benefits ofpresent case) was also available for the culturists

the integrated system other than the above moral

by selling the kelp at the price of 350 yen/wet kg.

benefit as followings.

These economical benefits substantially support theFirst of all is the depth merit. The depth ofculture in the present integrated

introduction of integrated cultures by raising the
motivation of fishermen.

system (1 m) was shallower than depths (2 to 8 m)of its natural habitats (Okamura 1915; Kimura 1995).

Acknowledgement

However, Kimura and Notoya (1996) revealed thatthe growth of the cultured kelp was faster at depths

This study was supported by a grant from theof 0.5 and 1.5m than at a depth of 2.5m. In addition,

Wakayama Prefecture Collaboration of Regional

the subsurface culture of the kelp also gives spatial

Entities for the Advancement of Technologicalrefuge to juvenile kelps because browsing by

Excellence of the JST.

the herbivorous fish,

is the mostsignificant factor causing the reduction of the kelp at
depths from 2.5 to 7 m from November to February,
in which the water temperatures are enough highReferences
Fukusho, K. (1986) Red sea bream. p.219-245. In: (ed)

Nutrient uptake by

and fish-alga integrated culture, 51, 15-23.

Shigen Kyokai, Aquaculture in shallow waters,
Tokyo.

Kitadai Y. and Kadowaki S. (2004a) The growth

Hirata H., E. Kohirata, F. Guo, Bo-Toa Xu and E.
Danakusumah (1993) Culture of the sterile. (Chlorophyceae) in a mariculture farm.
, 41, 541-545.

process and N, P uptake rates ofculture in coastal fish farm.

, 52,

65-72.
Kitadai Y. and Kadowaki S. (2004b) The growth

Kimura H. (1995)

andprocess and N, P uptake rates of

Okamura along the coasts ofculture in coastal fish farm.
, 52, 365-374.

Wakayama Prefecture. Nippon Suisan Gakkaishi,
61, 109-110.

Neori, A., Chopin,T., Troell, M., Buschmann A.H.,

Kimura H. (1995)

andKraemer, G.P., Halling, C., Shipgel,M and Yarish,

Okamura along the coasts of

C. 2004．Integrated aquaculture: rationale,

Wakayama Prefecture. Nippon Suisan Gakkaishi,

evolution and state of the art mphasizing

61, 109-110.

seaweed biofiltration in modern mariculture.

Kimura H. and Notoya M. (1996) Suitable timeand depth of outplant seedling for cultivation(Yendo) Okamura
at Tanabe Bay in Wakayama Prefecture,, 62⑸, 723-726.
Kimura H. and Tanaka T. (2004) Development ofpolyculture system. Reports of Fish Farming

Aquaculture, 231, 361-391.
Okamura, K. (1915)

and its species. Bot.Mag.,

29: 266- 278.
Troell, M., Halling, C., Neori, A., Chopin, T.,
Buschmann, A.H., Kautsky, N. & Yarish, C.
(2003) Integrated mariculture: asking the rightquestions. Aquaculture, 226, 69-90.

Laboratory Fisheries Experimental Station,

Uede T. and Takeuchi T. (2004) Report of project

Wakayama Research Center of Agriculture,in conservation of environment in aquaculture

Forestry and Fisheries. 35, 37-50.

ground. Fish Farming Laboratory Fisheries

Kitadai Y. and Kadowaki S. (2003) The growth
process and N, P uptake rates ofculture in coastal fish farm.

Experimental Station, Wakayama ResearchCenter of Agriculture, Forestry and Fisheries.
24pp.

水研センター研報，第19号，149−154，平成19年
Bull. Fish. Res. Agen. No. 19, 149‑154, 2007

Growth, nitrogen and phosphorous uptake rates and O2
production rate of seaweeds cultured on coastal fish farms
Yuuki KITADAI* and Shusaku KADOWAKI*
Abstract

To improve the water quality in coastal fish farms throughout year, we cultured
at 12-19℃ ,at 13-26℃ , andat 17-28℃ in
the Yatsushiro Sea. The growth, N and P uptake rates and O2 production rate of seaweeds
were estimated. The growth of the seaweeds cultured were identified and measured. Eachof the seaweeds cultured was collected monthly and analyzed for N and P contents. The observed N and P uptake rates per the blade and thallus area ( N,P, mg N,P/ms2/day) of eachseaweed were calculated by the following formula: N,P = ( N,Pt - N,P0) ･α / ，where N,P0 is
the N and P contents at the start of the experiment (mg N,P/g dry), N,Pt is the N and P contents day (mg N,P/g dry), α is the dry weight per the blade and thallus area, and is thecultivation days. The calculated N and P uptake rates of the seaweeds cultured were estimated from the dissolved inorganic nutrients concentrations, irradiance, and water temperature characteristics found at the fish farms. The O2 production rates of the seaweeds were
measured by the Winkler s method used light and dark oxygen bottles on fine day in thefish farm. The allowable volumes of seaweeds cultured for N uptake to N load in fish farming area, and for O2 production to O2 consumption by a fish cultured in cage were estimatedby using the maximum N uptake rate and the maximum O2 production values, respectively.
Key words : seaweeds, coastal fish farm, N and P uptake rates, O2 production rate, growth

Introduction
Today, biological water purification strategies
are required to solve anoxic water and prevent
eutrophication, aiming to establish sustainableaquaculture that can be produced on coastal fish
farms (Kadowaki, 2001). Seaweed cultivation results

minimum cultivation scales of seaweed to reduce
the N load and improve the O2 environment were
estimated by the results of the N uptake rate andthe O2 production rate of seaweeds.
Materials and Methods

in dissolved nitrogen and phosphorus that can be

Seaweeds cultivation were carried out at stations

uptaken to supply oxygen for cultivation on coastal

A-E in coastal fish farms in the Yatsushiro Sea

fish farms. For an entire year we cultured seaweed(Fig.1). During the investigation period the wateron coastal fish farms, and the nitrogen (N) andtemperature (WT) and the dissolved oxygen (DO)the phosphorus (P) uptake rates of seaweed wereconcentration of each station were recorded atfixed by the environmental factors of the dissolved

3 meter under the surface every three hours.

inorganic nutrients, the irradiance, and the water

Dissolved inorganic nitrogen (DIN) and dissolved

temperature. The oxygen (O2) production rate of the

inorganic phosphorus (DIP) concentrations were

seaweed was fixed by the environmental factors ofanalyzed once a week (Strickland and Parsons, 1972).

the dissolved inorganic nutrients. Furthermore, theDuring the experiment period, downward irradiance2006年 月26日受理（Received. June 26, 2006）*Graduate School of Agricultural Science, Kagoshima University, Shimoarata 4-50-20, Kagoshima, 890-0056, Japan
E-mail: kadowaki@fish.kagoshima-u.ac.jp

Yuuki KITADAI and Shusaku KADOWAKI
was automatically recorded under the surface at the) and consumption (1.3 meter and 2.0 meter depths every hour with athe seaweed were measured between 10 a.m. and 2

photon meter (LI-COR model 190SA). We cultured

p.m for 4 hours on a fish farm. The suspended depth

from December 2000 to July
2001,

from November 2002 to

May 2003, andfrom August 2002 to

November 2002.

and

were

of light and dark bottles was 2 meter atandwas cultivated under the surface atthe 0.5-8 meter layer.
of blade length (BL), and theand, and 0.5 m depth at

DO concentration was analyzed by Winkler s
method.

cultivated under the surface at the 1-4 meter layer,and) rates per chlorophyll-a of

The relationship between N and P uptake
rates (

N,P

) per seaweed area and the, DIN,and DIP concentrations were elucidated byof the thallus

Michaelis-Menten s formula. Maximum N and P

area (TA) which were identified, were measured

uptake rates (twice a month. The area, the weight, and the N and(

P contents in the seaweed were measured every

DIN and DIP concentration were calculated (Kitadai

month, and the analyzed N and P uptake rates wereand Kadowaki, 2003; 2004a; 2004b). The relationshipalso measured. On fine days, the O2 production (betweenN,P), maximum O2 production rate), and Michaelis-Menten s constants (

N,P

) of

and downward irradiance was analyzed

Fig. 1．Map showing the cultured sites of seaweeds at stations A-E of Goshoura
coastal fish farms in the Yatsushiro Sea

N,PGrowth, nitrogen and phosphorous uptake rates and O2 production rate of seaweeds cultured on coastal fish farms
by the Steel formula (Steel, 1962) to calculate the1.076, and theirsaturation irradiance (respectively (Table.2).

between

N,P) to. The relationshipN, P

and water temperature was analyzed

were 1.062，1.081, and 1.084,

O2 production and consumption rates of seaweeds

by the Allometry formula (Kadowaki and Tanaka,1994) to calculate the temperature coefficient (at

The water temperature of the).

The densities of seaweeds cultured per fish farm

and
, and

the cultivation weights of seaweeds necessaryofwere 2.6, 2.7, and 2.8

mg O2/mg chl.a/h, and theirwere 0.29, 0.24, and0.35 mg O2/mg chl.a/h, respectively. The

for oxygen consumption per aofcultured and the cultivation densities of seaweedsof

was 23, 20,

and 28 ℃ , respectively. The

area necessary to uptake the N load by theculture were calculated. In addition,

and

and

/
were

calculated at 8.9, 11.2, and 8.0, respectively (Table.3).

to oxygen consumption per cage volume ofcultured were provisionallycalculated.

Discussion
Density of seaweeds cultured to N load of fish farmarea

Results

It was reported that N load rates per fish farm

Cultivation environmentarea of

The WT and DO concentration during thein theandcultivation periods

cultivation period were 12-28 ℃ and 5.7-10.7

were 290, 115, and 520 mg N/mf2/day, respectively

mg/l at stations A-E, respectively. DIN and DIP(Kouchi Fisheries Experimental Station, 1989).

concentrations ranged between 31-150 μ g N/l and

The minimum densities of

7.0-27 μ g P/l, respectively. DIN/DIP ranged fromandper fish farm area of S.

3.1 to 8.4. The mean downward irradiance value ( ±quinqueradiata were analyzed by PmN, resulting inSD) in the 2 meter depth for the investigation period

2.9, 3.1, and 3.6 mg N/ms2/day, respectively. Thus,2f

was 650 ± 74 μ mol/m /s.

the minimum cultivation densities ofand U. pertusa per fish farm area of

Growth of seaweeds

cultured were 105, 27, and 7.6 kg/mf2,

The maximum BL ofandrespectively (Table.4).

reached 250 cm and 182 cm at the 2
meter depth, and their maximum growth rates

Weight and density of seaweeds cultured to O 2

were 3.0 cm/day and 4.2 cm/day, respectively. The

consumption of fish culture2

maximum TA ofreached 640 cm at the

The oxygen consumption rate per an

0.5 meter depth, and the maximum growth rate wascultured in the2

41 cm /day (Table.1).

andcultivation periods were879, 695, and 1392 mg O 2/a fish/h, respectively
N and P uptake rates of seaweeds
The(Kadowaki, 1990; 1994). The minimum cultivation

of

and
2

were 2.9, 3.1, and 3.6 mg N/m s /day, andtheweights ofperwere 0.43, 0.54, and 0.19 mg P/m s2/day,

respectively. Furthermore, the

of

, and
cultured were analyzed by, resulting in 0.75, 0.83, and 6.39 mg O2/g wet/h,
respectively. Thus, the minimum cultivation weights

andwere 29, 17, and 26ofμ g N/l, and theirwere 8.7, 6.2, and 8.0 μ g P/l,arespectively. Theof

0.21 kg wet/a fish, respectively. Moreover, theandwere 720, 670, and 730 μ mol/mf2/s,

respectively. The
, and

at

of
were 1.071, 1.090, and, andminimum densities of
and

per

cultured were 1.70, 0.83, and,per cage volume ofc u l t u r e d w e r e 5 . 6 , 4 . 0 , a n d 1 . 3 k g w e t / m 3,

Yuuki KITADAI and Shusaku KADOWAKI

Table 1．Maximum growth and growth rate of blade length (BL) ofand, and thallus area (TA) of

Table 2．Maximum N and P uptake rates (N,P), the maximum irradianceto), Michaelis-Menten constants ( ), and the water temperature
N,P (coefficients ( 01) of, and

Table 3．Maximim O2 production rates (rates (
) of, and

) and O2 consumption

Growth, nitrogen and phosphorous uptake rates and O2 production rate of seaweeds cultured on coastal fish farms

Table 4．Comparison of minimum density of seaweeds cultured per fish farm area for nitrogen load of
in
, and

Table 5．Comparison of minimum amount of seaweeds cultured per a fish, and minimum density of seaweed
cultured per fish cage volume for O2 consumption of, andYuuki KITADAI and Shusaku KADOWAKI
respectively (Table.5).
The/bacteria in sea water．

of

, and

，42，

267-272．(In Japanese)were 8.9, 11.2, and 8.0, respectively, proving

Kadowaki S.，2001:

Creations of sea, fishes andthat the O2 production rate of seaweed is eight tohuman in 21th century for environmental

eleven times more than the O2 consumption rate.

conservation of mariculture．The Society

Therefore, seaweed cultivation is effective on the O2of Naval Architects of Japan，16，1-6．(Insupply of fish farms.

Japanese)

The present study clarified the estimated water
purification methodology by seaweed that N and

Kitadai Y．and Kadowaki S．，2003:

process and N, P uptake rates of

P uptake rates, and the O 2 production rate were

cultured in coastal fish farms．

fixed by the environmental factors of the dissolved
inorganic nutrients, irradiance, and the watertemperature on coastal fish farms.

The growth，51, 15‑23．(In Japanese)
Kitadai Y. and Kadowaki S., 2004a: The growth and
N, P uptake rates ofcultured incoastal fish farms．

，52，65‑72．

(In Japanese)

References

Kitadai Y. and Kadowaki S., 2004b: The growth
Kadowaki S.，1990:

Production ecological studies onprocess and N, P uptake rates ofallowable capacity of aquaculture in yellowtail,cultured in coastal fish farms.

．Doctoral thesis of
Hokkaido university, 123 pp．(In Japanese)
Kadowaki S.，1994:．

．

Kouchi Fisheries Experimental Station，1989:

Energy budget for a yellowtail,in pen culture．
．

, 52, 365‑374．(In Japanese)

．

，

．1，

Kadowaki S．and Tanaka Y.，1994:

Oxygen45-59．

Loadvolume of nitrogen.
., 85, 34‑41．(In Japanese)
Strickland, J. D. H. and Parsons, T. R., 1972: A
practical handbook of seawater analysis．

consumption rates by phytoplankton and., Ottawa, pp. 45‑90．
S t e e l , J . H . , 1 9 6 2 : E n v i r o n m e n t a l c o n t rol ofphotosynthesis in the sea．
137‑150．

．

.，7，

水研センター研報，第19号，155−166，平成19年
Bull. Fish. Res. Agen. No. 19, 155‑166, 2007

博士号論文

Model management plan to optimize production of marine tropical systems
James P. McVey＊1

and Dallas E. Alston＊2, Alexis Cabarcas＊2and Edgardo Ojeda＊3

Abstract NOAA, the University of Puerto Rico Sea Grant College Program, and other federal, state, and private partners are proposing to develop model management plans suitable
for tropical marine ecosystems. In this paper we offer a new ecosystem-based management
scenario using aquaculture to optimize value and function of tropical island ecosystems.
Experience in Puerto Rico offers an excellent opportunity to combine several management
plans while maintaining the flexibility to work with user groups to manage and optimize
sustainable production from marine tropical systems. Puerto Rico has several tropical ecosystems available for study ranging from the high energy coastlines found on the northcoast to low energy, mangrove shorelines on the southwest coast. Coral reefs are prevalent
in the east, south, and west. All Puerto Rico coastal communities have seen a decline in fishery resources and habitats with subsequent decline in monetary value. A new approach forcoastal resource management is needed.
The key element in coral reef management is that large scale commercial removal of reef
resources has proven basically unachievable on island coral reef systems and larger coral
reef systems. There are many species but not a lot of any one species. Commercial operators travel farther to find commercial levels of catch until the reef is exhausted and out ofbalance. Our premise is that the reef should be maintained with minimum impact to foster
tourism and some subsistence fisheries to keep populations intact to maintain ecological balance of the reef and possibly provide broodstock for offshore aquaculture. Proper placementof offshore aquaculture in water over 30 m and 2-5 km offshore, away from coral reef structures has minimal environmental impact. With guidance from coral reef experts and aquaculturists, island communities can decide to combine marine protected areas, habitat protection, tourist scenic reefs, rigorous fisheries management and enforcement, and innovative
marketing to optimize the value of coral reef systems. Technology exists to implement thesemanagement tools. Culebra Island, Puerto Rico, offers an excellent location to demonstrate
this assumption.
Culebra has attracted international attention by petitioning the government to establish a
no-take marine reserve. The subsequent increase of reef fish is a clear demonstration of agrassroots effort to manage local fisheries resources. By combining the knowledge of recognized coral reef experts with innovative offshore aquaculture techniques, Culebra community leaders have the opportunity to optimize the value from their coral reef systems and toprotect their marine resources. Recent advances in the development of offshore, submerged,
marine aquaculture technology for island locations provides a new tool to optimize production of marine tropical systems. A panel of reef specialists, enforcement agents, aquaculturists, and environmentalists would advise the community and develop a management plan to
optimize scenic reefs, promote rigorous fisheries management and enforcement, and propose
innovative marketing strategies.
2006年 月26日受理（Received. June 26, 2006）＊1
National Sea Grant College Program 1315 SSMB Complex Ⅲ Silver Spring, MD 20910 USA＊2
Department of Marine Sciences, PO Box 9013 University of Puerto Rico, Mayagüez Campus Mayagüez, PR 00681-9013 USA
Email: Dalston@uprm.edu＊3
Sea Grant College Program, PO Box 9011 University of Puerto Rico, Mayagüez Campus Mayagüez, PR 00681-9013 USA

James P. McVey and Dallas E. Alston, Alexis Cabarcas and Edgardo Ojeda
public and private institutions. This approach
Introduction

will include industry partners and community
involvement, combined with strong research andManagement of tropical marine systems has hadcollaboration related to coastal ecosystem modeling.

varying degrees of success. These systems have

The addition of aquaculture to these strategies could

been impacted heavily, resulting in detrimental

help alleviate the impact on the fisheries habitat

impacts in many areas. Many approaches arewhile still providing healthy seafood products for thesuggested: closed fisheries, seasonal closing, or

public. In this respect, US and Japanese aquaculture

maintenance of the status quo. In most coastal

and fisheries in both the public and private sectors

communities, environmentalists, non-government

can work together to combine fisheries andagencies, fishermen, and recreational users

aquaculture to improve marketing, exports, andare concerned about their marine resources.

value of fishery products in both countries.

Community-based decisions, guided by professional

One caveat of this paper is that we use theadvice, provide a grass-roots approach to optimize

popular term

offshoreaquaculture to indicate

production from marine systems. In this paper, we

open ocean conditions. Thus the term offshore insuggest offshore aquaculture as an additional tool forthis paper does not have a legal context involving

optimizing marine production.

economic zones or legal boundaries. The popular

During the Thirtieth Joint Meeting of the United

term mariculture is a specialized word for marine

States-Japan Cooperative Program in Natural

aquaculture ; we generally prefer to use the phrase

Resources（UJNR）Aquaculture Panel Meeting inmarine aquaculture .

Sarasota, Florida, discussions entailed joint efforts to

Since 2001, Puerto Rico （PR）has maintainedchange the perception of aquaculture by developing

an offshore, submerged-cage aquaculture projectenvironmentally sound aquaculture practices using（Fig. 1）similar to Hawaii s recent efforts. Basedbroad-based ecosystem management that includes

on cutting-edge technology developed in the US,

aquaculture and fisheries. Three priority areasa New York based company, Snapperfarm, Inc.,

should include on-shore recirculating systems,

has successfully grown two fish species in cages

offshore aquaculture, and marine stock enhancement.

located 3 km southwest of Culebra, Puerto Rico.

Increasingly complex aquaculture management

Snapperfarm worked for four years to write astrategies require a multifaceted approach involving

business plan, obtain experimental permits frommany subject disciplines, human resources, and

the PR Department of Natural and Environmental

Fig. 1. Location of Snapperfarm offshore aquaculture cage site, Culebra, Puerto Rico.

Management plan to optimize marine tropical systems
Resources, assemble two submerged Ocean Spar Seaof recognized coral reef experts with innovative

Station cages, and deploy them in 90-feet of water at

offshore aquaculture techniques, Culebra community

the Culebra site. Snapperfarm s success has sparked

leaders will have the opportunity to optimize

the initiation of two other farms planning to installthe value of their coral reef systems to protect

16 more cages in Puerto Rico within two years.

their marine resources. Simultaneously, marine

Growth of R. canadum（cobia）to 6 kg in one year

aquaculture provides a new tool for managing island

has been the primary success factor driving thiscoastal resources to optimize production of marine

new industry with little environmental impact.

tropical systems. A panel to advise the community

In addition to the marine aquaculture project,would include reef specialists, enforcement

the island of Culebra has attracted international

agents, aquaculturists, economists, sociologists,

attention by petitioning the government to establish

and environmentalists to develop a managementam a r i n e r e s e r v e （C a u s e y 2 0 0 2 ）.

plan to optimize scenic reefs, promote rigorous

The subsequent increase of reef fish is a clear

no-takefisheries management and enforcement, and propose

demonstration of a grassroots effort to manage local

innovative marketing strategies.

fisheries resources. By combining the knowledgeof recognized coral reef experts with innovative

Deterioration of coral reefs

offshore aquaculture techniques, we expect topersuade Culebra community leaders to continue to

On a world-wide basis, coral reefs are at a fork

optimize the value from their coral reef systems byin the road （Wilkinson 2002）. Either reefs willdeveloping other marine protected areas（MPAs）

continue to decline due to increasing direct humanto ensure habitat protection. For instance, thestresses and indirect pressures of global climate

plan should include scenic reefs, rigorous fisherieschange; or there could be major improvements inmanagement and enforcement, and innovative

coral reef health in specific areas as a result of themarketing.

conservation and management projects; or more

The resulting increase of reef fish is a clear

likely coral reefs will travel down

both roads,

demonstration of a grassroots effort to manage local

with some reefs showing major improvements withfisheries resources. By combining the knowledge

increased coral cover, fish populations, and better

Fig. 2. Location of major reefs in Puerto Rico（from: http://www.nodc.noaa.gov/col/projects/coral/coralreef/CoralPR.html）.

James P. McVey and Dallas E. Alston, Alexis Cabarcas and Edgardo Ojeda
water quality, while many others will continue tofishery resources and the marine environment arelose corals and result in smaller fish populations andavoided. The terms over fishing and overfishedpoor water quality.

mean a rate or level of fishing mortality jeopardizing

Caribbean corals have been impacted. On Curacao,

the capacity of a fishery to produce the maximum

Netherlands Antilles, settlement of corals onto

sustainable yield on a continuing basis. The term

2experimental plates has dropped from 22 8/m in2fishing community means a community which is1981 to 3 0/m in 2001（Wilkinson 2002）. Many of

substantially dependent on or substantially engaged

the causes of coral reef decline have been identified

in the harvest or processing of fishery resources

and management techniques can be used to reduce

to meet social and economic needs. The termpressures degrading coral reefs. It is imperative to

optimum , with respect to the yield from a fishery,

apply this knowledge and demonstrate to coral reefmeans the amount of fish which will provide theuser communities and their governments that coral

greatest overall benefit, taking into account thereef conservation pays off in the long run.

protection of marine ecosystems and prescribing

In addition to the main island of Puerto Rico,

for maximum sustainable yield from the fishery,

there are 2 inhabited small islands off the east coast

as reduced by any relevant economic, social, or（Culebra and Vieques）and 3 uninhabited islands

ecological factor. In the case of an overfished fishery,（Mona, Monito, Desecheo）off the west coast. Most

the plan should provide for rebuilding to a level

coral reefs are located on the east, south, and west

consistent with producing the maximum sustainable

coasts（Fig. 2）, with fringing reefs being the mostyield in such fishery.

common type. The western two-thirds of the north

These definitions allow considerable leeway tocoast consists of mainly hard ground and reefdevelop management plans to provide sustainablerock with low to very low coral cover and someproducts with little environmental impact. However,small, sparse, low coral colonies. The main islands

many environmentalists want to close the resourceof Puerto Rico, including Culebra and Vieques, areto any human activity. While this may be suitable inalmost completely encircled by reefs, although coralsome instances, most laws are designed to promote

reef abundance is highly variable, depending on local

the best use of a resource.

conditions（http://www.aims.gov.au/pages/ research/coral-bleaching）.

The Department of Natural and Environmental
Resources of PR（DNER）is responsible for the
management of marine components（http://mpa.g

Puerto Rico and related management plans

ov/mpa̲programs/states/puerto̲rico.html）. The
Natural and Marine Reserves are managed by

The Magnuson-Stevens （M-S）Act Fishery

the Natural Reserves and Commonwealth Forests

C on se rv at io n and Management Act set t he

Divisions of the Bureau of Reserves, Refuges, andstandards for managing fisheries, so any plans must

Coastal Resources. Additional sites are administeredfollow these guidelines. For instance, a fishery is

and managed by the PR Conservation Trust. All

defined as one or more stocks of fish which can beof the sites included in the Marine Managed Areas

treated as a unit for purposes of conservation andInventory have been designated by the Puerto

management and which are identified on the basis

Rico Planning Board, except Isla Desecheo Marineof geographical, scientific, technical, recreational,

Reserve and Seven Seas Natural Reserve which wasand economic characteristics. Any plan mustdesignated by the PR Legislature. Most sites haveinclude the best scientific information available

year-round protection, excluding three red hindand be responsive to the needs of citizens. The（Epinephelus guttatus）spawning aggregation sites,

term

refers towhich have a temporary fishing ban（December

measures to rebuild, restore, or maintain any fishery

to February）, designated by a joint effort between

resource and the marine environment to assure

DNER and the Caribbean Fisheries Managementthat the food or products taken is continuous, andCouncil. Many sites include critical habitat andthat irreversible or long-term adverse effects onessential fish habitat for endangered and threatenedconservation and management

Management plan to optimize marine tropical systems
species including coral reefs, seagrass meadows,

Government to designate alagoons, mangroves, estuaries, wetlands, offshore

the west side of the island in 1999. The Biology

no-takezone onkeys, sandy beaches, and rocky shores. The sites

Department of the University of Puerto Rico-Rio

protect a great diversity of endemic, endangered,

Piedras conducted scientific monitoring, both before

and keystone species, both terrestrial and marine.

and after the establishment of the reserve, andFishermen are notoriously vociferous as a group.

their results show that fish abundance increased

Because PR has a tradition of fishing, albeit at an

dramatically and species numbers increased byartisanal level, they are generally supported by the

38%. Dramatic increases in the abundance（2 539%）

government. Our suggestion is to include the major

and in the biomass （26 618%）of the yellowtail

players in the decision-making process, including

snapper（Ocyurus chrysurus）were noted, as well

fishermen, environmentalists, non-government

as significant increases in the abundance（414%）

organizations, and representatives from the generaland biomass（868%）of the schoolmaster（Lutjanus

community. Communities should have the choice

apodus）. Thus, the designation of the Luis Peña

of deciding the fate of fishery activities in their

Channel No-Take Marine Reserve in Culebra, Puertoarea. This grass-roots approach should make it

Rico is a clear demonstration of a grass-roots effort

easier for fishermen to accept new strategies.

to manage local fisheries resources. Please refer toEfforts should be made to include the fishermen in

Hernández-Delgado and Sabat（2000）or Hernández

proposed aquaculture activities. After all, they arefamiliar with marine operations and should continue（2000）for additional details referring to theno-take marine reserve.

to contribute their skills within their respective

Dr. Sarah Keene Meltzoff, University of Miami,

communities. A major problem is enforcement. By

and Dr. Janet Bonilla, UPRM contributed to ahaving the communities join in the decision-making

socio-economic study of Culebra in relation to theprocess, we would hope the locals would provide

new offshore aquaculture project by Snapperfarm.

self-enforcement, especially if MPAs would benefit

Most comments concerning the new cage culture

the community as a whole.

industry were positive or neutral with a let s wait

We also suggest avoiding managing specificand see

attitude. Several respondents indicatedspecies; instead focus would be on maintaining

they would like to know more about the industry.

the reef in optimum condition. This should greatly

Questions arose concerning the competition of theminimize expensive studies for each target species;

cages with the local subsistence fishing industry.

instead effort could be re-directed toward optimizing

Snapperfarm has repeatedly stated its goal to work

the health of reefs.

closely with the Culebra Fishermen s Associationand has voluntarily agreed to hire locals first to

Culebra Island as an example of community

fill vacant positions; however, realities in education

involvementa n d w o r k e x p e r i e n c e （p r o f e s s i o n a l d i v i n g ,aquaculture experience）severely limit employment

The Island of Culebra is 27 km east of Puerto

opportunities. This is an area that could be theRico and is 11 by 5 km. The surrounding waters

focus for future projects, especially to train locals insustain an extensive and varied coral reef that isoffshore aquaculture techniques.

healthier than most others in Puerto Rico. The
Culebra Fishermen s Association recognized that

Community involvement and education

over fishing was a problem in their area withserious consequences for their artisanal fishing

Any management process should include

livelihood. Through their own initiative and with

community involvement. All too often

top

the assistance of a volunteer fisheries scientist,to bottom

the association catalyzed the conservation effort

management policies for the natural resourceby petitioning the Department of Natural andwithout incorporating community ideas. Phillips

Environmental Resources of the Puerto Rico

（1998）used the term social sustainability whichplans impose new strategies andJames P. McVey and Dallas E. Alston, Alexis Cabarcas and Edgardo Ojeda
incorporates systematic community participation

based management schemes could be the basis forwhich will only be socially sustainable if it conforms

these plans.

to social norms or does not stretch them beyond a

Whatever the management strategy developed,

community s tolerance for change. If the community

education needs to be included in the plan. The

is not involved from the initiation of the project,public will be more apt to accept new strategies

imprecise or erroneous perceptions emerge.

when they understand the consequences of the

These perceptions become reality. Therefore

status quo

the community must participate in the initial

will learn to appreciate the accrued benefits

situation that benefits no one anddecision-making phase. Education becomes an

by incorporating suitable management plans toessential component in these interactions and should

optimize the productivity of their marine resource.

be continued throughout each phase of the project.

In addition, they will be able to make valuable

Fong（1999）reported enhanced environmentalsuggestions to adapt the plans to their respective

responsibility and participatory self-governancecommunity. By playing a role in the decision-making

by fishermen. The previous model utilized

process, community participants will be muchcentralized governmental control and input that

more disposed to accept management plans thatwas distant in time, space, and purpose in relation

benefit the environment and the community. It

to the local fisheries industry, which resulted in low

is important to include the major players in the

productivity by the fisheries. Although centralized

discussions, including fishermen, environmentalists,

controls were set in place to cover a variety of

non-government organizations, and representatives

environmental conditions, they were not appropriate

from the general community. The discussion groupfor all local conditions. Such distant governmental

should be advised by experts.

control promoted neglect or outright damage tothe environmental conditions, to the detriment

Offshore aquaculture as an additional management

the fishery in question. Taiwan tried a different

tool

approach to involve the communities by dividing
theircounties

into individual units to develop

The key element in coral reef management is thatpolicies unique to their area. This has the advantage

managed removal of reef resources has shown to be

of being site specific so plans can be adapted tobasically unachievable on island coral reef systems

varying hydrological and terrestrial habitats. Whenand even larger coral reef systems. Wilkinson（2002）

the local government worked with local fisheries

reported the following:associations and communities, productivity increased

All regions of the world report that human factors

with increasing participation of fishermen andare behind the declining health of coral reefs. The

officials. Thus, Taiwanese fisheries cooperative

major stresses are increased sediments and pollution

practices were developed to involve the interaction

by nutrients and toxic compounds, and reef damageof the community and the fishermen with technicalfrom exploitation of fishes, invertebrates, algae, rock

input from the government（Fong, 1999）.

and sand, and constructions. The most extreme

Many legislators traditionally consider the ocean

example from the 2002 Reefs at Risk analysis is

as a common property resource to be managed

that 88% of all reefs in Southeast and East Asia arefor all the people, assuring free and equal accessunder moderate to very high human pressures.

（Corbin and Young 1997）. Others have feared

For Southeast and East Asia, Wilkinson（2002）

that leasing could lead to widespread subdivision

reported that most reefs continue to decline underof ocean space by large, financially well endowed

increasing human impacts, except where there

companies, thus taking away the use and enjoyment

has been strong community involvement in MPA

of ocean resources by the general public. Legislators

design and management. Unstressed and protected

are now considering the best use of the oceanic

reefs are recovering from losses in 1998, but there

environment; however, care should be continued

was further bleaching in Japan in 2001, with 50%

to provide for sustainable development. Ecosystemmortality on some reefs. By far the most serious

Management plan to optimize marine tropical systems
threats are destructive and over-fishing, followed byPuerto Rico and the fishery is heavily impacted.

coastal development, increased sedimentation, andEach of these factors will continue to impact coastal

pollution. Monitoring and management capacity isaquaculture; even land based operations utilize

relatively strong, but not sufficient for adequate reef

coastal waters to culture species such as marine

assessment and conservation.

shrimp and tropical aquarium fish.

Caribbean activities have been boosted with

The term sustainability is controversial and hassome new funding, but many the problems remain

several related factors that should also be considered（Wilkinson 2002）. The corals in Florida, US Virginwith its usage. The concept of sustainability

Islands and Puerto Rico are either declining or

should include not only the ongoing operation andhave not recovered after decades of losses. No-takeits long-term impacts on the environment andreserves in Florida have larger fish populations thansociety, but also the infrastructure, materials, andin fished areas, and public support for management

regenerative capacity of the natural system whichis increasing.

generates these latter items（Phillips 1998）. Thus

Healthy coral reefs have many species, but notsustainability entails prolonged socially acceptable,

many of a particular species. Commercial operators

economically viable, and technologically appropriate

travel more to find commercial levels of catchproduction without degrading the environment.

until the reef is exhausted and out of balance.

Simultaneously, additional resources supporting

Our premise is that it is better to maintain thethe industry（i.e., feeds, wild juveniles）should be

reef with minimum impact to be used as a source

renewable, or if not renewable（i.e., hatchery rearedof enjoyment for tourists and some subsistence

juveniles）, these resources should be replaced withactivities, but to keep populations intact to maintainsuitable substitutes on a timely basis.

the reef in balance and possibly provide broodstock

Environmentalists are justifiably disturbed thatfor offshore aquaculture. Proper placement ofoffshore aquaculture depends on feeds containing aoffshore aquaculture in water over 30 m and 2-5high percentage of fishmeal. However, only a portion

km offshore, away from coral reef structures hasof fishmeal and fishmeal derived oils are used inminimal environmental impact. With guidancefish culture operations. The rest is used in feedfrom coral reef experts and aquaculturists, island

for food animals such as poultry, cattle, or swine

communities can decide to combine protected areas,

and a portion is incorporated into pet foods. Feedhabitat protection, tourist scenic reefs, rigorous

suppliers are willing to incorporate other ingredients

fisheries management and enforcement, andinto high quality, high protein feeds, but farmers

innovative marketing to optimize the value from

report inferior growth. Perhaps environmental costs

coral reef systems. Technology exists to implements

are too high to continue using fishmeal in animalthese management tools.

feeds. An international ban on fishmeal use will

FAO（1997）identifies environmental deterioration

be complicated, however, because incorporating

and land availability as important constraints for

bycatch from fisheries operations or offal frommarine aquaculture. Over 70% of the total worldprocessing procedures（like tuna, catfish, etc.）is

population lives in Asian coastal areas（Phillips

considered a legitimate use of an otherwise wasted

1998）; about 60% of the world s population currently

resource. Nevertheless, a fishmeal ban should notlives within 60 km of the sea（Phillips 1998）. Puerto

discriminate among various aquaculture sectors

Rico, with 3 9 million inhabitants occupying 9100

or by country. This complicated topic should be

2

km , has a central mountainous region, thus forcing

subject to multi-lateral deliberation with input fromthe majority of the population to live near the coast.

scientists, governments, and the fisheries industry.

Puerto Rico s coastal pollution is typical of manyIn the meantime, the marine aquaculturists should

industrialized regions（eutrophication, sediments,

purchase feeds which minimize the incorporation ofand other contaminants）, but deterioration is also

fishmeal. Recent studies indicate excellent growth

exacerbated by intense recreational and artisanalfrom feeds containing a minimum of fishmeal.

fishery activities. Reef decline is widespread in

Offshore aquaculture has been hindered because

James P. McVey and Dallas E. Alston, Alexis Cabarcas and Edgardo Ojedaof the energetic oceanic environment, lack of

Virgin Islands（USVI）averaged 3,360 MT（FAO,

suitable equipment, fingerling fish, and unclear

2004）for the years 1993-2002（Fig. 3）. In 1996, there

policies and regulations concerning this nascentwere 1758 fishermen with a total of 1501 vessels.

industry. Reviews of monitoring strategies andUsing conservative estimates（survival of 85%, mean

methods revealed the need for standardized

weight of 6 kg）of Snapperfarm s actual stocking

approaches flexible enough to cover the wideand fish mean weight after 12 mo, each cage should

range of environments in which fish farms areproduce about 61 MT/per year（4 fish stocked/m3＊

located（Cochrane

1995;

3 000 m3/cage ＊ 0 85 survival ＊ 6 kg/fish ＊ 0 001 to

2004）. Future challenges toconvert kg to MT = 61 MT）.Rachycentron canadum

offshore aquaculture include clarification of policies

are stocked at 4-6 fish/m 3 and harvested at 6-10

and regulations, strengthening marketing and

kg/fish in Taiwan（Sudistribution channels, coping with rapid growths stocking rates are similar to those used in Taiwan.

of biofouling organisms, improving harvesting

Even though all the fish were not harvested at 10

techniques, and establishing a source of marine fish

months, we are assuming a survival of 85% after

juveniles to achieve a viable, sustainable industry.

12 months. Using these conservative numbers, only

A dynamic, flexible strategic plan is essential for

55 cages of fish would produce tonnage equaling

incorporating the needs of the private industry,the entire Puerto Rico and USVI fishery production

optimizing support from the government, and（3360 MT divided by 61 MT = 55 cages）. Taiwan

providing for adequate research support from

reported that 1,500 cages were in operation in 1999

Puerto Rico universities. Evaluation of the industry

with volumes ranging from 216 to 1,884 m3. Thus ifshould utilize assessment methodologies, including

Puerto Rico and the USVI operated 55 cages, theysocio-economic considerations and comparisons withcould alleviate fishing pressure on reefs and still

domestic and foreign offshore industries.

maintain present fishery production levels.

and Alston

1994; Codling

2000）, so Snapperfarm

Marine aquaculture operations may have positive

Alternatively, the Snapperfarm cages served asor negative effects on the environment（Phillips

fish aggregation devices（FADs）. Most subsistence

1998）. The environment may have positive or

fishermen in Puerto Rico focus their efforts innegative effects on aquaculture, especially if external

inshore areas, so are dependent on reef species. Thisfactors continue to degrade the environment.

causes a high pressure on coral reef species（Weiler

Eutrophication may provide nutrients beneficial

and Suarez-Caabro 1980）. Hence, FADs to attract

for aquaculture production, especially for oysters,

pelagic fishes are integrated into management

clams, and mussels. However, toxic pollutants canstrategies to enhance local fisheries. FADs servedamage aquaculture investments（Phillips 1998）.

as additional substrate, shade, and refuge from

Aquaculture operations may affect each other,predators（De Silva 1982）; as an additional foodespecially where the carrying capacity is exceeded

source; and offer a break in the monotonousby rapid expansion of many farms within a limited

offshore environment. Friedlander（1986）compared

area. Each of the suppositions mentioned generally

small-scale fishing-gear techniques at six FADs

refer to land-based or inshore mariculture operations.

deployed off northeast Puerto Rico and found

Offshore aquaculture avoids many of these factors.

differences in species diversity between FADs

Thus far, studies by the University of Puerto Ricoand control areas, indicating FADs may enhanceand the University of Miami of the Snapperfarm

recreational fishing catch rates. Beets（1989）foundsubmerged cage operation have indicated negligiblethat FADs not only aggregate fishes but also havenegative environmental effects. As expected, thethe potential to enhance the recruitment of benthic

footprint of the effects was limited to directly

artificial reefs. Offshore cages offer protection andbeneath the cage and attributed to a combination

substrate similar to other FADs and also supplementof nutrient release（uneaten feed, fish feces）andthe nutrient supply in the area through feeding theshading by the cage itself.

cages which could serve as direct or indirect sources

Fisheries production for Puerto Rico and the USof food for opportunistic feeders（Koslow

1988;

Management plan to optimize marine tropical systems

Fig. 3. Fishery landings for Puerto Rico and the US Virgin Islands, 1993-2002.
Source FAO, 2004 （http://www.fao.org）

Humann 1994）.

The Snapperfarm cages attracted 40 fish

Because of the cage structures themselves andspecies from 23 families and 6 orders and mean

the constant food supply, we hypothesize thatfish abundance recorded near the cage site was

the offshore aquaculture industry could enhance

approximately 40 times higher than at the control

the local fishery by facilitating new pelagicsite（Bejarano

resources or serving as a source of recruitment tothe cage site was located in offshore conditions

replenish impacted reefs. This could occur by two

approximately 1 km from the nearest reef, 23 reefmechanisms. The fishermen could have access the

species, and 17 pelagic species were observed

aquaculture site to catch fish attracted to the cages.

aggregating near the cages. Twelve reef species

The cage site could serve as a mini-reserve where

included juvenile individuals in most of thethe cage site is restricted to fishermen. In the firstobservations. Thirty-one of the species found nearcase, fishermen could fish for pelagic species not

the cages are commercially important in Puerto

normally accessible, therefore offering an additionalRico, representing 43% of the total numbers ofincome and economic options. However, fishermen

individual recorded. Of the commercially important

would have to be careful to avoid damaging thefish, 94% are used for human consumption （10cages. Pelagic fish species are not frequently

pelagic species and 8 reef species）and 6% are used

captured by artisanal fishermen because of theby the aquarium industry. The majority of the fish

difficulty and effort needed to find and capture theseused for human consumption were pelagic fish

fishes. Fishing for pelagic species is more expensive.

swimming in schools with numerous individuals.

. final preparation）. Although

However, fishery activities understandably makes

Some species exhibited a solitary behavior suchcage aquaculturist nervous; so initially, Puerto

as Sphyraena barracuda, Scomberomorus cavalla,

Rican aquaculturists have decided to close their

Scomberomorus regalis, Ginglymostoma cirratum,site to fishing. The second mechanism to allow

Dasyatis americana, Aetobatis narinari, and Lutjanus

the site to serve as ajocu. Many were seen several times by the divers,mini-reserve

provides anopportunity for reef and pelagic species to use theusually moving away if closely approached.

cages as an artificial reef and spawning ground.

Our data indicate submerged aquaculture cages

Recruitment from the aquaculture site to area reefs

are suitable for juvenile fish, acting as artificial

could indirectly improve the fish catch on the reefs

habitats with additional substrate, refuge, and food.

themselves. Thus, the first step was to determine

Artificial habitats in tropical waters attract reef

the qualitative and quantitative composition, and thefishes and contribute to artisanal fishing activities

relative abundance of wild fish associated with the（Johannes 1997）. With appropriate management

offshore cage site.

strategies, fishermen could work with cage-cultureJames P. McVey and Dallas E. Alston, Alexis Cabarcas and Edgardo Ojeda
operations, possibly kindling a proprietary andand explore markets for sale of urchin roe.

protective interest in fishing grounds. Fish

Enhance BMPs（best management practices）.

collectors often become active stewards, guarding

Develop standardized monitoring techniques forthe resources against destructive uses and often

cages.

creating conservation areas（Galvez 1991）.

Automation of harvest system.

The rate of accumulation and coverage ofAutomation of feeding systems.

biofouling organisms attached to the surface of theAutomation of cleaning biofouling from cages.

cage netting were assessed because they obstruct

Improve cage technology（shape, resistancewater flow through the cages, add additional weight

to hurricanes/typhoons, maximize volume per

to the cage, and increase the net drag. Even thoughdollar spent）.

biofouling was apparently not a problem in Hawaii s

Share information concerning disease andsubmerged cages （Helsley 2002）, Snapperfarm

parasite infestations.

reportedly cleaned their cages biweekly, thus,

Develop feeds with little environmental costs

significantly increasing their operational costs.

（i.e., without using fishmeal）that support rapid

Because growth conditions apparently arefish growth.

optimum for biofouling growth, this provides an

Develop methodologies to measure genetic

interdisciplinary opportunity to look for suitable

dilution from fish escapes.

organisms which could be grown quickly andCompare carrying capacity per unit area（i.e.,

harvested within a short time.

kg/km2）of tropical versus temperate systems.

Although Puerto Rico historically has not cultured

Model nutrient flow（i.e., nitrogen into fish flesh,seaweed, the climate is suitable for tropical seaweed

uptake by biofouling or sediment, dissolved

culture. By contrast, the Philippines produces

nitrogen in water column）.

895 mt of aquatic plants（mostly marine algae）

Compare discharge permit regulations.

（http://www.fao.org/fi/statist/statist.asp）, including

Compare social perception of cage culture

Eucheuma alvarezii and E. denticulatum（Trono

operations.

1981）. A separate species of Eucheuma isiforme is

Study evidence of benign or beneficial

reported from Puerto Rico（Ballantine and Aponteinteractions with the environment rather than2002）
. Each has a tropical marine environment, so

solely concentrating on the devastation of

Puerto Rico should be suitable for seaweed culture.

accidental releases, eutrophication due to over

Ballantine and Aponte（1997）reported 473 benthic

feeding, or overproduction in a confined body ofmarine algae, some of which could be useful forwater（Helsley 2001）.

culture.
Conclusions
Areas for collaborative efforts
Offshore aquaculture needs to confront problems
Possible US and Japanese collaborative efforts

inherent to the industry, especially those that seem

related to optimizing production in the marine

unavoidable

environment:

acknowledgment that unforeseen disasters could:

Cultureuseful algae outside of cages

instead of letting

wild biofouling organisms

at the moment. These include theCause the escape of thousands of culture
animals with little genetic diversity thereby

dominate; in tropical conditions biofoulingpossibly diluting the gene pool of native fish.

growth is rapid and results in economic loss

Result in large-scale havoc by escapees on local

for the aquaculturists due to frequent cleaning

reef ecology（predation, competition, etc.）

procedures.

Spread of parasites and diseases to wild

Culture filter-feeding pearl oysters on or near

populations. The inherent crowding of cultured

the cages to minimize wastes.

fish provides ideal conditions for parasites andPlace urchins on cages to consume biofoulingdiseases.

Management plan to optimize marine tropical systems
Australia, pp. 251-276 in
The public has acknowledged and accepted that

FAO, （1997）The state of world fisheries andland agriculture perturbs the environment; the sameaquaculture, 1996:Fisheries Department, FAO,

will be true of offshore aquaculture.

Rome.

However, by integrating aquaculture as an

FAO, 2004:（http://www.fao.org）

additional tool to manage marine tropical systems,

Helsley, C. E., 2001:Open Ocean Aquaculture‑areefs can be protected while the community

Venue for Cooperative Research Between thecan benefit from aquaculture fish yields. In the

United States and Japan. U.S.‑Japan Cooperative

meantime, we need to continue to determine theProgram in Naural Resources Aquaculture

environmental effects of marine aquaculture. Except

Panel, Ecology of Aquaculture Species andfor unforeseen natural disasters, the potential

Enhancement of Stocks : Proceedings of thebenefits of marine aquaculture seem to outweigh theThirtieth UJNR Aquaculture Panel Symposium,

negative aspects.

Sarasota, Florida, December 2-3, 2001.
Helsley, C. E., 2002:Offshore aquaculture in Hawaii

Acknowledgementsfrom research to reality. First Korea-U.S.
Joint Coordination Meeting for Aquaculture

Information relating to this paper was supported
by two National Oceanic and Atmospheric
Administration（NOAA）projects:

Cooperation, April 15-16, 2002, Busan, Republicof Korea.

Offshore Cage

Hernández-Delgado, E. A. and Sabat A. M.,

Culture: Environmental Impact and Perceptions

2000:Ecological status of essential fish habitats

by Local Fishing Community by the National Sea

through an anthropogenic environmental stress

Grant Program（grant number NA16RG1611）and

gradient in Puerto Rican coral reefs. Proceedings

the Saltonstall Kennedy Program（SK）from（grantof the Gulf and Fisheries Institute, 51, 457-470.

number: NA17FD2370P）.

Hernández-Delgado, E. A., Alicea-Rodríguez L. A.,
Toledo C. G., and Sabat A. M., 2000:Baseline

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checklist of the benthic marine algae known toWorld Publications, Jacksonville, Florida, USA.

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Phillips, M. M., 1998:Tropical mariculture and coastal（3-4）, 150-179.
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checklist of the benthic marine algae known to
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York, USA, pp. 17-69.
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Causey, B., Delaney J., Diaz E., Dodge D., Garcia

C. Liao and C. K. Lin, editors. Proceedings ofJ., Higgins J., Keller B., Kelty R., Jaap W.,

the First International Symposium on Cage

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Tungkang, Pintung, Taiwan, pp. 97-106.

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Florida, Texas, Puerto Rico, Us Virgin Islands,

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水研センター研報，第19号，167−171，平成19年
Bull. Fish. Res. Agen. No. 19, 167‑171, 2007

博士号論文

New approach for the integrated aquaculture management from theview point of multi-functional role of fisheries and aquacultures
Osamu MATSUDA*
Abstract: Supply of food, in particular of protein has long been widely accepted as majorrole of fisheries and aquaculture for human society. However, recent growing concern on the
global environmental issue and sustainable development is now making clear that fisheries
and aquaculture also play important roles on material cycling between land and sea, monitoring of fishing environment and living resources, purification of pollutant through biological activities and food chain, environmental watching by fisherman, environmental education,
eco-tourism and etc. In this context, Science Council of Japan submitted a special report to
the Minister of Agriculture, Forestry and Fisheries recently (Aug. 2004) on multiple roles
and functions of fisheries and fishing communities, in which role on environmental conservation, role on formation of regional community, role on maintaining personal security, role onproviding fields of education and many kinds of amenity were highlighted as well as the roleof food supply. Responsible and sustainable aquaculture also can play important functionalroles. As an example of possible new approach for the integrated aquaculture managementfrom the view point of multi-functional role of aquaculture, present status and possible future
direction of large scale oyster culture in Hiroshima Bay, Japan are discussed. For the future
direction, integrated oyster culture management responsible for regional economy and community are proposed with particular reference to safe and clean oyster meat supply, benthic
living resource enhancement by raft oyster culture system, recovery of discharged N and
P from land, environmental and red tide monitoring system, many varieties of recreation,
seascape, eco-tourism and environmental education for especially younger generation. This
proposed management should be involved in the more holistic environmental and ecosystemmanagement by wide variety of stakeholders as a part of integrated coastal management ofHiroshima Bay including land use management of Ohta River watershed which has strong
influence on the biological productivity and diversity of Hiroshima Bay.
Key words: multi-functional role, integrated aquaculture management, oyster, Hiroshima
Bay

Introduction

global environmental crisis. In the symposium on“Role of Fisheries in Environmental Management

A major role of fisheries and aquaculture which

and Remediation

held in 2001, Matsuda (2002)

has long been widely accepted and is still primarily

pointed out another six possible functional roles

important is supply of food, in particular of protein,

described below in addition to food supply, which

for human society. However, new ideas on theare closely related to environmental conservation,

concept of multi-functional roles of fisheries andpurification of polluted environment and prevention

aquaculture are now growing public concerns inof eutrophication: 1) Conservation of habitatthe environmental conscious society under theenvironment, 2) Monitoring of environment and2006年 月26日受理（Received. June 26, 2006）*Professor Emeritus, Hiroshima University, 6-8-13 Hachihonmatsu-Minami, Higashi-Hiroshima 739-0144, Japan. E-mail: matsuda036@go3.enjoy.ne.jp

Osamu MATSUDA
living resources, 3) Recovery of inflowing nutrientsduring recent few years. In the present paper, under(nitrogen and phosphorus) through fish catch andthese circumstances, five selected multi-functional

harvesting, 4) Reduction of COD (chemical oxygenroles of fisheries and aquaculture below aredemand) value through biological activities, 5)highlighted and reviewed in order to clarify

Environmental watching by fisherman, and 6)

those functional roles with particular reference toEnvironmental education, eco-tourism.

environmental conservation, purification of polluted

In this context, fisheries and aquaculture which

environment and prevention of eutrophication: 1)

is to be discussed in the present paper indicate

Material cycling between land and sea, 2) Monitoring

primarily responsible fisheries and aquaculture,of environment and living resources, 3) Purificationand hence, do not include such destructive fisheriesof polluted environment through biological activities

or aquaculture as had ever given strong negativeand process of food chain, 4) Environmental watching

impact on the fisheries environment and living

by fisherman, and 5) Environmental education.

resources.

Therefore, main objective of the present paper is

Fundamental Law on Fisheries was enacted in

not to show experimental data but to propose newJapan in 2001, in which the term “multiple functions

concept and approach for the integrated aquacultureof fisheries and fishing community

management from the view point of multi-functional

officiallyappeared and the necessity of future investigationrole of fisheries and aquacultures.

on these functions was clearly stated.
In February, 2003, “International Symposium
on Multiple Roles and Functions of Fisheries andExemplified multi-functional roles of fisheries andaquaculture

Fisheries Communities was held in Aomori, Japan,
where Hiroyoshi (2003) made a key note lecture,

1. Material cycling between land and sea

in which he stated “There has not been awarenessLanding of fish catch by capture fisheries isamong people regarding multiple functions ofa valuable and rare process by which inflowing

fisheries communities. There is a need to renew ournutrients to the sea such as nitrogen andrecognition in this respect from the view point ofphosphorus are recycled to the land. Non-feeding

structural changes in fisheries as well as the earth s

aquaculture such as bivalve culture and algal culture

environment .

also contributes to the same type of processes.

The Ministry of Agriculture, Forestry andSince anadromas fishes such as salmon play a same

Fisheries of Japan made an announcement on therole on the material cycling between land and sea,

new policy from 2004, main concept of which is moreconservation of normal behavior of anadromas fish

environmental conservation concerned agriculture,

can contribute to this function.

forestry and fisheries through healthy water

The magnitude of the recovery of inflowing

circulation, healthy atmospheric circulation, healthy

nitrogen and phosphorus by fisheries is sometimes

material circulation and conservation of healthy local

not so small and that in the Seto Inland Sea iscommunities.

estimated as 5 to 8% for nitrogen and 15 to 22% for

In August, 2004 the Science Council of Japan

phosphorus.

submitted a special report to the Ministry ofAgriculture, Forestry and Fisheries of Japan on

2. Monitoring of environment and living resources

the multiple roles and functions of fisheries andFishing boats encounter many kinds offishing communities with particular reference tooceanographic and meteorological evidence orrole on food supply, environmental conservation,

phenomena and can collect huge amount of data

formation of regional community, people s security

which has high possibility to build up valuable dataand providing fields of education and many kinds ofbase. Fisheries statistics in particular of fish catchamenity.

data in terms of weight according to species areThus, public awareness and interest on thevaluable information of living resources particularly

multi-functional roles of fisheries is rapidly increasingin Japan. Although fish catch data do not directlyDistribution and physiological function of vitamin K
indicate fish resource data, no other similar biologicalFisherman on the boat also sometimes rescues anddata base are available covering such a long termsaves people in crisis.

and wide area of the sea as to many species. By the
careful analysis of fish catch data, evaluation of living
resource and estimation of the change in ecosystem
structure is possible.

5. Environmental education
Fisheries and aquaculture provide us withvaluable opportunity for environmental education
and recreation. Excellent fishing ground and fisheries

3. Purification of polluted environment throughcommunity are attractive site for eco-tourism.

biological activities

Not only that fish landing market is a part ofDuring a process of food chain, filter feeders

informative eco-museum on living resources but also

such as bivalves purify water through filtration

cooking fish at home can help the understandingsof particulate matter and detritus feeders purify

of children for introductory anatomy and zoology.

sediment through decomposition of organic matter.

In Japan, access to natural seashore has been

Not only detritus feeders but also aquatic animals

historically restricted by new land reclamation or

generally decompose organic matter throughport development, combined activities of recreation,

heterotrophic nutrition resulting in the reduction ofseascape, eco-tourism and environmental education

BOD, COD values of water and sediment. Anothersuch as shellfish gathering is recommended for

purification process regarding biological activities

better understanding of marine environment andis removal of pollutant. When any kind of organic

living resources, especially for younger generation.

matter in the area is carried out by some migration
or behavior of animals, this kind of removal of

New approach for possible integrated oyster cultureorganic matter from the area in question is alsoin Hiroshima Bay

evaluated as a kind of purification of the area inAmong a number of multi-functional roles ofthe broad sense. Filtering activities by bivalvesfisheries and aquaculture which has already been

estimated by some authors depends on conditions

exemplified in the previous section, oyster culture

but generally very significant. With use of those

has many positive aspects of functional roles ofeffects of filtering activities of bivalves as well as theaquaculture. Matsuda

removal of N and P through catch of the bivalves,on the new perspectives for oyster culture as aenvironmental restoration of tidal flats is made in

biofilter and biohabitat. According to Songsangjinda

some coastal area of Japan, for example, in Mikawa(1999, 2000), role of oyster culture in Hiroshima

Bay, to enhance the production of clam shells as

Bay on material cycling is valuable. However,

Manila clam.

production of oyster from Hiroshima Bay has been

(1999) already reported

decreased due to multiple reasons. Main objective
4. Environmental watching by fishermanof the present proposal is to maximize any kind of

Fisherman is a careful watch on marine

positive effect of oyster culture and to minimize

environment, who can find out any kind ofnegative effect at the same time. As positive

abnormal conditions such as red tide, oil spill

effects, in addition to supply of high quality oysteror accident. Therefore, when the legal right ofmeat which is primarily important, purification offishing of some area became null and void due toseawater by filtering activity of oyster, enhancement

some reason, environmental conditions of the areaof material circulation through harvesting, providing

often deteriorated historically because of the luck

variety of habitat for living organisms by cultureof watching and objection against deterioration.

gear, effect of oyster raft as floating algal bed,

Original information on abnormal conditions,effects on recreation, amenity and education are

occurrence of red tide for example, often comes frompointed out. Oyster culture of Hiroshima Bay has

fisherman. Therefore, networking of the information

valuable experience of monitoring and management

collected by fisherman potentially can play anof paralytic shellfish poisoning (PSP) in which

important role on environmental conservation.

monitoring of causative phytoplankton and toxicity

Osamu MATSUDAof shellfish were made. While, as negative effects,

food, future direction for integrated aquaculture

deterioration of sediment quality by deposition ofmanagement should be sustainable in its manner,feces and pseudofeces due to excessive culture,

responsible for human society and playing as muchinhibition to tidal movement by more than 10,000

multi-functional roles of aquaculture. Integrated

floating culture rafts, occurrence of PSP, effect ofaquaculture management to enhance regional

waste from oyster culture industries can be listed

economy and employment should also contributeup. Not a small amount of waste from culture system

to build up healthy material circulation and healthysuch as foam polystyrene from float and PVC pipe

ecosystem. In order to maximize multi-functionalfrom oyster hanging wire system have been everroles of fisheries and aquaculture, collaboration isreported in and around culture ground.

recommended with holistic regional environmental

Under these circumstances, future integrated

management as a part of integrated coastal zone

oyster culture management in Hiroshima Bay should

management which includes watershed area

be responsible for regional environment, economy

management. It is also proposed for integrated

and community. Hirata and Akashige (2004) analyzed

aquaculture management from the view point of

the present situation and problem of oyster culture

multi-functional role of aquaculture to minimize

in Hiroshima Bay and pointed out, as one of thewaste material, to reuse waste material, to reduce

problems, dense cultivation which prolonged theenergy consumption, to reduce new resource

culture period due to low phytoplankton level. They

consumption, to restore deteriorated environment

also showed with use of model that the reduction inand to collaborate with variety of stakeholders.

oyster biomass in the culture ground is needed tosolve the problem and that shortening of the culture

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Hiroyoshi K., 2003: Keynote speeches in “Proceedings

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