Preface
The United States and Japanese counterpart Panels on Aquaculture were formed in 1969 under theUnited States-Japan Cooperative Program in Natural Resources (UJNR). The UJNR Aquaculture
Panel currently includes specialists drawn from the government and academic departments most concerned with aquaculture. Charged with exploring and developing bilateral cooperation, the Panels
have focused its efforts on exchanging information related to aquaculture that could be of benefit toboth countries.
The UJNR was begun during the Third Cabinet-Level Meeting of the Joint United States-Japan
Committee on Trade and Economic Affairs in January 1964. In addition to the aquaculture Panel,current subjects in the program include destination of seawater, toxic microorganisms, air pollution,energy, forage crops, national park management, mycoplasmosis, wind and seismic effects, protein
resources, forestry, and several joint Panels and committees in marine resources research, development, and utilization.
Accomplishments of Aquaculture Panel include: increased communication and cooperation among
technical specialists; exchanges of scientists and students; focus of efforts to issues of major international concerns such as disease transmission and stock enhancement; exchanging of information,
data, and research findings; annual meetings of the Panel; administrative staff meetings; exchangesof equipment, materials, and samples; several major technical conferences; and beneficial effects on
international relations.
The 31st UJNR Aquaculture Panel Business Meeting and Symposium was held from October 16 to
October 17, 2002 at National Research Institute of Fisheries Science in Yokohama, Japan. The first
topic of the sixth five-year plan of the UJNR Aquaculture Panel from 2003 to 2007, "Aquaculture andStock Enhancement of Algae and Filter Feeders", provided the basis and focus for the Symposium.
Following the meeting and symposium, field trips and satellite symposium were held in Shizuoka
Prefecture, central Japan and Miyagi Prefecture, northern Japan to visit prefectural fisheries research organizations, culture sites of seaweeds and bivalves from October 18 to 24, 2002.
The symposium was organized by representative coordinator Dr. Tetsuo Seki and other UJNR
Aquaculture Panel staff members of the Japanese side. Twenty specific papers were presented in the
symposium. Eighteen full papers of them have been accepted for this Proceedings as a Supplementof Bulletin of Fisheries Research Agency. Two abstracts were included in this Proceedings. Editorial
work has been assisted by the staffs of National Research Institute of Aquaculture. We would liketo acknowledge Dr. Hisashi Kurokura, Dr. Ken Furuya, Dr. Charles Yarish and Dr. Roger I. E.
Newell to preparing keynote and identifying speakers, and Dr. Masao Ohno, Kochi University forpresiding the general discussion. On behalf of Japanese authors, we would like to express sincere
gratitude to Dr. Paul Kilho Park for revising English with great dedication. Finally we wish thankMs. Maya Kurihara to greatly support a editorial task for this Proceedings.
Chairman:Yasuji Sakai, Japan
James P. McVey, United States水研センター研報，別冊第 1 号，1 − 4 , 平成16年
Bull. Fish. Res. Agen. Supplement No. 1, 1-4, 2004

1

The importance of seaweeds and shellfishes in Japan:
Present status and history
Hisashi KUROKURA*

Abstract Though many manufactured goods are produced from aquatic resources,
people living in Japan consume them mainly as food. Among such sea foods, seaweeds
and shellfishes have special religious meaning. Kombu (Laminaria), wakame (Undaria)
and abalone or other shellfishes are commonly included in offerings to Shinto shrine. It
was supposed from this fact that these foods were important for Japanese ancestor. In
fact, many remains of seaweeds and shells were dug out from ruins of prehistoric age.
In the 8th century, Yakamochi Ohtomo, a famous poet in Nara Period, transplanted ashell species from Kishyu to Ecchyu. This is the oldest record of propagation of shellfish.
Nori (Porphyra) is now indispensable for sushi. Its culture started from the 17th century.
Aquaculture of wakeme, oyster, peal oyster, and many other seaweeds and shellfishes
had begun by the end of 19th century. Aquaculture technology has been improved and the
production has increased rapidly in the latter half of last century. Now seaweeds andshellfishes aquaculture encounter various difficult problems such as changes in coastal
environment by pollution and land reclamation. On the other hand, the function of theseaquaculture for water purification attracts attentions of people together with the increase of interest to environment issues.
Key words: shellfishes, seaweeds, Aquaculture, history

Importance of Seaweeds and Shellfishes inJapanese Daily LifeIn 2000, the average family income and expenditure for consumption were 6,371,000 yen/year and 3,806,000 yen/year in Japan (Ministryof Public Management, Home Affairs, Posts
and Telecomminucations, Japan, 2001). Within
the expenditure for consumption, 972,000 yen/year was consumed for foods including 174,000
yen/year for dining out (Fig. 1). Total amountof the expenditure for livestock products, suchas beef, pork, chicken, including hum, sausage,milk, and egg was 119,000 yen/year, and samemoney (118,000 yen/year) was paid for fresh
aquatic food. Besides the expenditure for fresh
aquatic foods, 49,000 yen was consumed forprocessed aquatic food, such as dried fish and"surimi" products. From these data, it can besupposed that an average Japanese family pays
1.5 times larger amount of money for aquatic
foods than livestock products, and that the expenditure for aquatic foods reaches 21％ of
total expenditure for foods excluding diningout (Fig. 2).
In expenditure for fresh aquatic foods, morethan half of it was occupied by fin fish (67,000
yen/year) and major parts of the remainder
were expenditures for crustacean and cephalopod. Only one tenth of the expenditure for
finfishes was paid for shellfishes (6,400 yen/
year). "Asari" (Manila clam, Ruditapes
philippinarum), Pacific giant oyster (Crassostrea
gigas) and scallop (Patinopecten yessoensis) are

2003年 6 月12日受理（Received on June 12, 2003）* Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, 113-8657, Japan

2

Hisashi KUROKURA

main shellfishes consumed in Japan. Nori
(Porphyra spp.), konbu(Lminaria spp.) andwakame (Undaria pinnatifida.) are major
seaweeds eaten in Japan. They are consumed asprocessed aquatic food (dried, salted, or boiledetc.) and the total amount of expenditure forseaweeds (6,200 yen/year) was same as that forshellfishes (Fig. 3).
In protein base, daily protein intake by Japanese was 86.8g/day/individual in 2000 (Minister's Secretariat, Ministry of Agriculture,
Forestry and Fisheries, Japan, 2001). Within
86.8g of daily protein intake, 20.9g and 7.5g
were from cereals and beans. Live stock products provided 28.4g of protein. Within that,
14.4g, 5.7g and 8.3g were by meats, eggs andmilk and milk products, respectively. Total volume of protein supplied by aquatic animal including fish, molluscs, crustaceans andechinoderms was 19.4g. Only 1.1g was supplied
from seaweeds (Fig. 4).
Though the contributions in the family expenditure and protein supply are not so highwhen compared with fishes and squids, shellfishes and seaweeds are very important foodmaterials for Japanese cuisine. They provide
delicate taste, flavor and trace nutrients to the
cuisine. For example, "sushi" can not be completed without these materials. The notable importance of shellfishes and seaweeds aresupported by Japanese environment and history.

Fig. 2. Expenditure for each food item in 2000

Fig. 3. Expenditure for fisheries products in 2000

Fig. 4. Protein intake of average Japanese( g/individuals /day) in 2000

History of Aquaculture of Shellfishes andSeaweeds

Fig. 1. Average family income, expenditure and expenditure for foods in Japan in 2000

Shinto is basically ancestor worship inJapan, and the offerings in Shinto shrines
originally were dinner of the ancestors. The
other side of the offering is promotion of local
industries and they have been modernized andstandardized twice in modern era. However,
several old shrines such as Kamo Shrine and Ise
Shrine keep old style in their offerings. We canThe importance of seaweeds and shellfishes in Japanfind abalone, hard clam and other shellfishes
and various kind of seaweeds in those offerings. This fact shows Japanese have been eating shellfishes and seaweed as daily food fromprehistoric age.
In 764, Yakamochi Ohotomo, a poet in the
Nara period, the last editor of Manyohshu,
transplanted a species of bivalve from Kishyu(Pacific coast of Honshu island) to Ecchyu (Seaof Japan side). This is the oldest record oftransplantation of bivalve and attempt for
propagation of aquatic animal. First record ofartificial propagation of seaweed was alsotransplantation. In 1081, a kind of seaweed wastransplanted from Kouzu-shima, an island in
Izu archipelago, to Izu peninsula. Nori and oyster culture were supposed to be started in
1670s. In 1892 Koukichi Mikimoto started pearl
oyster culture. Oyster culturists began to use
rafts for hanging culture in 1925. Floating net
culture of nori started in 1934 in Tokyo bay
and other modern "nori" culture techniques,
such as artificial spat collection, andcryopreservation of nori seeds, were established in the 1950s and early 1960s. These modern techniques enabled expansion of area andseason of nori culture. As the result, production of nori in Japan increased 40 times from
1940s to 1990s (Fig. 5) (Ministry of Agriculture,
Forestry and Fisheries, 2001). On the other
hand, pollution of costal environment became
considerable from 1950s on because of rapid
economic growth in Japan, and coastal
aquacultures often sustained heavy damages(e.g. oil pollution in Tokyo bay in 1954, inFig. 5. Changes in production of Nori3

Wakayama in 1955). In 1997, Ishaya Bay, an accessory bay of Ariake Bay, was closed by water
gates for land reclamation. Nori production in
Ariake Bay prominently decreased in the culture season of 2000. Several fishermens'
cooperations in Ariake Bay claimed that thepoor harvest of nori had been caused by alteration of environment of Ariake Bay which was
brought on by the close of Isahaya Bay. After
that, sustainability of coastal aquaculture has
been thought to be an indicator of health ofcoastal environment (Table 1 ).
Contemporary Importance of Shellfish
and Seaweed Culture in Japan
Through the discussions about the relationship between the alteration of coastal environment and fisheries production, people
understand the importance of aquaculture as amonitoring system of coastal environment andfunctions of shellfish and seaweed culture on
the conservation of coastal environment.
Fuyou Kaiyou Kaihatsu Co. Ltd. estimated thefunction of fisheries of asari on the environment in Hamana Lake, a brackish lake on the
Pacific coast of Honshu Island. Total influx ofcarbon, nitrogen and phosphate to Hamana
Lake, were 2,411, 1809 and 899 t/year respectively, and total catch of asari was 2,200 t/year
in 1990. When we calculate the magnitude of
the catch to the values based on carbon nitrogen and phosphate, they are 572, 132, 8.8t/year. These magnitude mean that 26, 7.9, 1.3％ of carbon, nitrogen and phosphate introduced to Hamana Lake were removed by catchof asari. Similar effect can be expected to shellfish and seaweed culture. Now Japanese people
has begun to notice the function of shellfish
and seaweed culture on the conservation ofcoastal environment and they expect systematic approaches to utilize aquaculture for conservation of coastal environment.

4

Hisashi KUROKURA

Table 1. History of shellfish and seaweeds culture in Japan
year
764

Transplantation of bivalve by Yakamochi Ohtomo

1081

First record of transplantation of seaweeds

1596

Name of Asakusanori
vested in Tokyo-bay.

1615

Transplantation of oyster from Wakayama to Hirosima

1674

Beginning of oyster culture

began to be used for Nori har-

1673-81 Beginning of nori culture
1781

Transplantation of abalone from Bousou to Shrahama

1853

Use of bamboo stick as structure for nori culture

1870

Beginning of nori culture in Kanagawa

1878

Transplantation of konbu from Hokkaido to Aomori

1881

Beginning of asari culture in Chiba

1882

Beginning of nori culture in Aichi

1890

Koukichi Mikimoto began pearl oyster culture

1900

Damage of pearl oyster by toxic algal bloom Gonyaulax
in Ago Bay

1912

Cleaning of rocky shore for the propagation of seaweeds

1920

Nets were firstly used as the substrata for nori attachment

1925

Start of hanging oyster culture

1926

Success in using net as the substrata of nori

1934

Floating culture of nori using floating net started inTokyo Bay1936

Beginning of spat collection of scallop in Lake Saroma

1942

Asari poisoned in Hamana Lake

1942

Success in artificial seed collection of wakame

1949

Discover of conochocelis
Success in artificial seed collection of konbu

1954

Success in artificial seed collection of nori
Leakage of heavy oil in Tokyo bay. ( Nori culture wasdamaged)

1955

Nori culture in Wakayama was damaged by waste oil

1960

Mass mortality of cultured oyster in Hirosima bay

1963

Invention of freezing preservation method of nori seed

1964

Invention of spat collection method of scallop

1974

Success in artificial inducement of spawning of abalone
by UV radiation

1997

Isahaya Bay, an accessory bay of Ariake Bay, was closed
by water gate for land reclamation.

2000

Production of nori in Ariake Bay prominently decreased.
The relationship between aquaculture production and alteration of costal environment became a national dispute

Cited from Ohshima, Y. (1994) with several modification byauthor

References
Ministry of Agriculture, Forestry and Fisheries, Minister's Secretariat 2001: Table offoods supply and consumption.
Ministry of Agriculture and Forestry, Statistics and Survey Division, 1941-2001: Annual report of catch statistics on fisheries
and Aquaculture.
Ohshima Y., 1994: Suisan zouyoushoku
gizyutsu Hattatsushi (History of development in aquaculture and propagation techniques) , Midorishobo, Tokyo, 476pp.
Ministry of Public Management, Home Affairs, Posts and Telecomminucations, Statistic Bureau and Statistic Center, 2001:
Annual report on the Family Income andExpenditure Survey.

水研センター研報，別冊第 1 号， 5 −12, 平成16年
Bull. Fish. Res. Agen. Supplement No. 1, 5-12, 2004

5

The present situation and problems of oyster culture in Hiroshima Bay
Yasushi HIRATA＊ and Satoru AKASHIGE＊

Abstract Hiroshima Bay including its adjacent area is one of the most important oysters farming areas in Japan. During 1980s, the oyster production in Hiroshima Bay was
about 30,000 metric tons (t) scale by fresh meat weight (FMW) a year. In the early 1990s,
the oyster production began to decrease and was about 20,000t in 2000. We analyzed thepresent situation and problems of oyster culture in Hiroshima Bay to show the problem
solution. This decrease in oyster production in the 1990s was caused directly by typhoon
damages; shellfish poisoning by Alexandrium spp.; and mortality by harmful
dinoflagellate Heterocapsa circularisquama: and was caused by dense cultivation indirectly. The postponing of harvesting the oyster caused by shellfish poisoning prolonged
the oyster culture period. The prolongation of the culture period in a limited culture
ground caused eventually dense cultivation of oyster. Aged and large-sized oysters tookmuch feed, therefore growth of all oysters in culture grounds were slowed down under
low feed level. The low growth rate accelerated prolongation of a culture period. Thesevicious spirals promoted dense cultivation, and changed the environment of the culture
ground into favorable environment for H. circularisquama. To analyze these situations,an oyster culture process model was built. This model showed that the reduction in oyster biomass in the culture grounds is needed to escape from the vicious spiral, and shortening of the culture period was the most effective method for this reduction without
reducing harvest magnitude.
Key words: oysters, Hiroshima Bay, culture process

Introduction
We present a model to describe the difficultythat oyster culture in Hiroshima Bay including
its adjacent area is facing currently. We haveexamined possible improvement of the culture
process by this model.
Hiroshima Bay is located in the western partof the Seto Inland Sea (Fig.1). Oyster culture in
the bay had begun at a tidal flat of estuary before 450 years ago. About 60％ of a Japaneseoyster are produced currently in Hiroshima
Bay. The oyster hanging culture method byrafts of bamboo spread over the Hiroshima Bay
after 1960. Kusuki (1991) had reviewed thehistory and technology of oyster culture in
Japan.
The changes in annual oyster production by
fresh meat weight (FMW) in Hiroshima prefecture after 1965 is shown in Fig. 2. The
Hiroshima Fisheries Experimental Station(2001a) reported the relationship between thechanges in oyster production and oyster culture technology as follows. In 1960s, the oyster
production increased to 30,000t by spread of thehanging raft culture. However, in 1969 and
1970, the oyster production decreased by outbreak of red tide and dense settlement ofserpulid worm (Arakawa, 1971). In 1970s, thevolume of production increased to 30,000t

2003年 6 月12日受理（Received on June 12, 2003）* Hiroshima Prefectural Fisheries Experimental Station, Ondo, Aki, Hiroshima, 737-1207, Japan

6

Yasushi HIRATA and Satoru AKASHIGE

again. The recovery of production was achieved
by development of a culture technique: hanging
down deeply and migration of a raft seasonally, to avoid the red tide and the settlement of
the other periphyton. In 1980s, improvement of
the culture technology provided both reliable
production of 30,000 t scale and the extensionof a culture period. In 1990s, the oyster production began to decrease. In September 1991, a severe typhoon damaged 40％ of the rafts, andthe harvest was about 1 month late. In theearly spring of the next year, harvest was
stopped because a shellfish poisoning had ex-

Fig. 1. Location of oyster culture areas in HiroshimaBayceeded safety regulation. The harvest suspension by shellfish poisoning in early spring occurred afterwards for several years. In
addition, red tide of H. circularisquama occurred in autumn 1995 (Matsuyama et al.,1997), and it delayed the oyster to gain weight.
In summer 1998, mass mortality occurred by
the red tide of H. circularisquama. In the next
harvest season the oyster production was decreased to about 16,000 t. However, the oyster
survived grew well. The Hiroshima Fsheries
Experimental Station (2001a) estimated thatthe decreasing of oyster production after 1990
was caused by shortening of a harvest period
by a shellfish poisoning and delay of growth or
mortality by H. circularisquama directly.
However, they thought that there were problems of production structure as arranging a lotof rafts in a limited culture ground and extending a culture period.
In late years, studies of shellfish poisoning,
red tide plankton, and that about evaluation ofcontribution degree of oyster culture in material circulation of Hiroshima Bay are pushedforward (Songsangjinda et al., 1999). However,there are no concrete measures to elucidate
their effects on oyster culture. In this study, we
describe an approach to analyze the oyster culture methods in Hiroshima Bay by an oyster
culture process model.
Materials and Methods

Fig. 2. Changes in cultured oyster annual production
by fresh meat weight (FMW) in Hiroshima
Prefecture. The data listed here can found in the"Annual Report of Production on Fishery and
Aquaculture, Statistics and Survey Division",
Ministry of Agriculture, Forestry, and Fishery,
Japan.

Oyster culture process model
1. Basic structure of the modelThis oyster culture process model consists ofphysiological changes of an oyster and culture
process of a raft unit in one culture ground.
For modeling of feed competition among oyster, the structure that the quantity of feed in
the culture ground decreases according to thebiomass increases was built in this model. The
calculation was carried out by one-day unit
during one year from 1 October to 30
September. The relationship of increase inweight of an oyster and a quantity of chlorophyll in the culture ground, the relation of a

The present situation and problems of oyster culture in Hiroshima Bay

size of oyster and a quantity of spawning eggs
or death rate are determined by the findings ofHiroshima Fisheries Experimental Station(2001b).
2. Individual scale
Oyster repeats physiological change of
gametogenesis and growth seasonally. In winter, oyster grows well. In summer; however,
spawning reduces the weight. On 30 September,
FMW for individual starts from 1g. The weightof oyster in this paper is expressed by FMW.
The weight gain a day (WG) of an oyster from
October to May was expressed by following
equation:
WG＝0.0512QC−0.0130,
where QC is the quantity of chlorophyll( μ g/L). The QC decreases by an oyster
biomass(OB)
inacultureground.
Environmental factors as water temperature,salinity and dissolved oxygen are not considered. The weight does not change in June and
September, and decreases according to weightof June by spawning in August from July.
Starting weight of September (Ws) is given by
Ws＝−0.02 Wjun2＋Wjun(Wjun≦30g),
Ws＝0.4 Wjun
(Wjun＞30g),
where Wjun is the weight of June.
3. Raft scale
Initial population is 250,000 oysters a raft.
Some oysters die in July and August. Numberof September (Ns) is given by
Ns＝Njun(Wjun＜10g),
Ns＝Njun {1−(Wjun/90)} (10g≦Wjun＜90),
where Njun and Wjun are number of June
and weight of June, respectively.
4. Culture ground scale
Quantity of chlorophyll (QC μg/L) in culture ground is constant, however, whenbiomass of oyster (OB) exceeds a fixed quantity, it decreases by competition. QC is given by
QC＝2.7(OB＜14,000t),
QC＝37,800/OB(OB≧14,000t).
5. Harvest
Oysters more than 5 g (FMW) are harvested.
The raft that contains the heaviest oyster inculture ground is harvested sequentially. Totalof 6,300 rafts are harvested in one year, with7

the speed of 28 rafts a day during 16 October to
28 May in this model. The oyster biomass (OB)is a total of weight of all individual of a culture
ground. Gross production of the year is provided by summing daily harvest.
6. Production economy
Money earned in a day is calculated fromgross weight of the oyster that harvested on
one day and unit prices of the day. The Unit
price of Hiroshima oyster is generally highuntil December, but tend to gradually fall fromJanuary. The change of unit price set it as follows. The price of oyster is 1,200 yen a kg from
October to December. The unit price decreases
by a rate of 5 yen/kg/day from 1,200 yen/kg
during January to February, and 1 yen/kg/
day from March to May. A gross production
amount of money of the year is provided by atotal of daily production sales.
Estimation of oyster production under different
culture patterns
The basic pattern of oyster culture in
Hiroshima Bay is classified into 3 patterns according to the length of the culture period. In
the 1-year-culture method called "Waka", oyster spats are collected in the summer, grown in
the winter, and harvested before the following
summer (less than 12 months old). In the
2-year-culture methods called "Yokusei" and"Ikisu", oyster spats are hardened on intertidal
racks for 2 to 3 months and 6 to 10 months, respectively, after spat collection in summer,
grown under rafts over the next summer, andharvested during the following harvest season(13-23 months old). In the 3-year-culture
method called "Nokoshi", oyster spats are hardened by the same method as in the "Yokusei"
method, grown over two summers, and harvested during the following harvest season (2535 months old). The combination of theseculture methods in Hiroshima Bay hadchanged as follows: In the 1960s, oysters were
produced by a combination of the 1 and 2-yearculture methods. Only a 2-year-culture method
was used from the 1970s to the beginning of the
1980s. In the latter half of the 1980s, the 3-year-

8

Yasushi HIRATA and Satoru AKASHIGE

culture method has been introduced in addition
to the 2-year-culture method, and its ratio has
increased after the consecutive outbreak ofshellfish poisoning (Fig. 3). We estimated oyster production by the number of rafts needed,
the gross production, the total amount ofmoney earned, oyster growth and oyster
biomass in five patterns of a combination ofculture methods. In patterns 1, 2, 3, 4 and 5, theoysters were cultured only by a 1-year-culture
method, a 1-year-culture and 2-year-culture
method, a 2-year- culture, a 2-year-culture and3-year-culture, and by only a 3-year-culture,
respectively.

harvest caused by shellfish poisoning on oyster
production by using this oyster culture processmodel, as follows: In the initial year, 90 ％ of
the 2-year-cultured oysters and 10 ％ of the 3year-cultured oysters would be harvested (year0). In every spring during next five years, theharvest would be suspended during the final 20
days of the harvest period due to shellfish poisoning occurred (years 1-5). In the summer ofthe fifth year (year 5), the H. circularisquama
red tide occurred and oyster mortality would
be assumed 100 ％ and 50 ％ in case of the 3year-cultured and the 2-year-cultured oysters,
respectively.

Estimation of impact of shellfish poisoning on
the oyster production
When the quantity of shellfish poison in oysters would exceed safety regulation, the oyster
harvest in Hiroshima Bay would be halted.
Oysters that aren't harvested would be left in
the culture ground until the next harvest season beginning in October. Shellfish poisoningof oysters had occurred in Hiroshima Bay
every spring from 1992 to 1998, except in theyear 1994. The mass mortality of oysters
caused by the H. circularisquama red tide occurred subsequently in summer, 1998 (Fig. 4).
We evaluated the impact of the suspension of

Results
Estimation of oyster production under different
culture patterns
Fig. 5 shows the simulated result on thenumber of raft needed, gross production, andtotal amount of money earned under each oyster culture pattern. These five culture patterns
correspond to the historic changes in the culture methods used in Hiroshima Bay. The culture methods in the 1960s, and from the 1970s
to 1980s and 1990s, are almost equivalent topatterns 1 or 2, 3, and 4, respectively. The shift
in culture methods from pattern 1 to pattern 3

Fig. 3. Transition of oyster culture methods in Hiroshima Bay

The present situation and problems of oyster culture in Hiroshima Bay

9

Fig. 4. Changes in annual cultured oyster production
by fresh meat weight (FMW), and events whichcaused a production decrease in Hiroshima prefecture.

caused an increase of 12,600 in the number ofrafts needed, which was twice the number used
(6,300) in pattern 1. In pattern 3, both the grossproduction and the total amount of money
earned was at its maximum. The shift in culture methods from pattern 3 to pattern 5caused a further increase in the number ofrafts needed, to 18,900 from 12,600. In patterns
4 or 5, the gross production and the total
amount of money both decreased. Fig. 6ashows the changes of in the individual weightof harvested oysters in each harvest pattern.
The shifts from pattern 1 to pattern 3 raised
the oyster size of the harvest at the beginning,
but reduced the oyster size of the harvest by
the end of the exchange. The shifts from pattern 3 to pattern 4 raised the oyster size of the
beginning harvest inconsiderably. However,the shifts from pattern 4 to pattern 5 reduced
the oyster harvest size of all periods comparedwith pattern 3. A change of biomass under each
culture pattern is shown in Fig. 6b. Fig. 6cshows the ratios of oyster age in each biomassof patterns 1, 3 and 5. The shift from pattern 1
to pattern 5 raised maximum biomass about 3
times.
Estimation of impact of shellfish poisoning on
the oyster production
Fig. 7 illustrates the annual changes in thenumber of rafts and gross production on thecondition that the mass mortality occurred
after shortening of the harvest period by 20
days continued for 5 years. One year later, thegross production of oysters decreased because

Fig. 5. The variation of: a) raft composition at theharvest of 6,300 rafts, b) estimated gross oyster production during each year, c) estimated total production of money in each culture pattern.

Fig. 6. Changes in the estimated: a) individual weightof oysters in each culture pattern, b) oyster biomassin each culture pattern, c) age composition of oysters
in the biomass of patterns 1,3 and 5. The numbers inthis figure correspond to each pattern in Fig. 5.

10

Yasushi HIRATA and Satoru AKASHIGE

the harvest had been halted for 20 days, and the
production decreased gradually thereafter.
This gradual decrease in production was due tothe postponement of the harvest schedule,
which caused the increase in the ratio of the 3year-culture, the change of the harvest size
(Fig. 8a) and the increase in oyster biomass inthe culture ground (Fig. 8b). Five years later,
the harvest size in 1 December increased to 15.9
g from 14.9 g, but the harvest size in 1 May decreased to 19.8 g from 23.0 g (Fig. 8a). The increase of biomass for 5 years was remarkablein June, just before spawning. The biomass
reached 1.34 times of the initial year (Fig. 8b).
Due to the mass mortality which occurred in
the summer of the 5th year, gross productionin the 6th year decreased to about 16,000 t.
However, individual oysters survived, showed
high growth rate due to the decrease in thebiomass (Fig. 8b).
Discussion
This oyster culture process model simulated
the oyster culture production structure ofHiroshima Bay, reproducing each changes of
the harvest size, gross production, and theFig. 7. The simulation of the shortening of the harvest period caused by shellfish poisoning and massmortality by H. circularisquama. a): changes in thenumber of rafts, and b): changes in gross oyster
production in that year.

total amount of money earned. This model enabled to obtain a long-term guide for selecting
a culture method.
In the 1980s, oyster had been cultured mainlyby the 2-year-culture method and the production had been constant approximately 30,000 t
in Hiroshima Bay. But in this period, the 3year-culture method was introduced to a small
percentage and was effective because large size
individuals were available to be harvested in
the early period of harvest seasons, when theunit price was high. However, the induction of
the 3-year-culture method caused an increase in
the oyster biomass in the culture ground, delayed individual growth, and then prolonged
the culture period, which led to a vicious spiral(Fig. 9). In the 1980s, we thought that the vicious spiral illustrated in Fig. 9 already existed. The progress of this vicious spiral was
not rapid, but after the 1990s. The outbreak ofshellfish poisoning caused a sharp increase inoysters cultured by the 3-year-culture method
because the harvest had to be postponed to thenext harvest season, and that caused an acceleration of the spiral. It can be considered that

Fig. 8. Changes in the estimated: a) individual weightof oysters, b) oyster biomass under shortening of
harvest period caused by shellfish poisoning andmass mortality by H. circularisquama. The numbersin this figure correspond to each year in Fig. 7.

The present situation and problems of oyster culture in Hiroshima Bay

dense cultivated grounds, where there is nocompetition with other plankton and the flowof water is stagnant are favorable environmentfor H. circularisquama to increase (Fig. 9).
Oyster biomass in culture grounds has to be
decreased in order to halt this vicious spiral.
The most effective method for this purpose is
to shorten a culture period. In other words, itwould be optimal to culture oyster only by the2-year culture method rather than combinate
with the 3-year one. To confirm this efficacy,
we are currently analyzing the carbon flow in
an individual scale and in a raft scale. We alsoplan to combine our analyses, and build an oyster culture model of a culture ground scale in
the future.
Acknowledgements
We are grateful to Dr. Paul Kilho Park and
Dr. Tetsuo Seki for their comments and suggestion on the manuscript.
References
Arakawa K. T., 1971: Notes on a serious dam-

11

age to cultured oyster crops in Hiroshimacaused by a unique and unprecedented outbreak of a serpulid worm, Hydroides
norvegica (Gunnerus) in 1969., Jap. J.
Malacol., 30(2), 75-82.
Hiroshima Prefectural Experimental Station,
2001a: An enterprise of engineering development for restructuring of an oyster culture system, final report, pp. 1-12.
Hiroshima Prefectural Experimental Station,
2001b: An enterprise of engineering development for restructuring of an oyster culture system, final report, pp. 13-19.
Kusuki Y., 1991: Oyster culture in Japan andadjacent countries: Crassostrea gigas(Thunberg) in "Estuarine and Marine
Bivalve Mollusk Culture" (ed. by MenzelW.), CRC Press, Boston, pp. 227-243.
Matsuyama Y., Kimura A., Fujii H.,
Takayama H., and Uchida T., 1997:
Occurrence of Heterocapsa circularisquama
red tide and subsequent damages to shellfish in western Hiroshima Bay, Seto
Inland Sea, Japan in 1995. Bull. Nansei
Natl. Fish. Res. Inst., 30, 189-207.
Songsangjimda P., Matsuda O., Yamamoto T.,

Fig. 9. The vicious spiral of oyster culture in Hiroshima Bay

12

Yasushi HIRATA and Satoru AKASHIGE

Rajendran N., and Maeda H., 1999:
Application of water quality data to estimate the cultured oyster biomass in

Hiroshima Bay: Estimation of the cultured
oyster biomass. Fisheries Science, 65(5),673-678.

水研センター研報，別冊第 1 号，13−18, 平成16年
Bull. Fish. Res. Agen. Supplement No. 1, 13-18, 2004

13

The decline of Manila clam stock in Tokyo Bay
Mitsuharu TOBA* 1

Abstract The fisheries production of Manila clam in Chiba Prefecture, which amounts
to more than 90 ％ of the total clam production in Tokyo Bay, markedly declined to
below 20,000 metric tons (mt) in 1979, after reaching 70,000 mt at its maximum in thelate 1960s. This is mainly because of the large-scale reclamation of the shallow tidal
areas where clam fisheries were intensively operated. However, the clam production
keeps gradual decreasing even after the cessation of the series of reclamation in 1979.
The periodical monitoring of clam stocking density shows decreasing of clam production
since 1985 seems to be associated with the poor occurrence of wild juvenile clam. In
Kisarazu Area, which is the largest Manila clam producer in Tokyo Bay, production isstably maintained between 5,000 and 6,000 mt since late 1980s, in spite of the stocking
density of juvenile clam (4-11 mm in shell length) declining from 68 to 12 inds/m2 during
this period. It is probably due to 2,000-3,000 mt of the transplantation of the seed clam(>20 mm) from other area in Tokyo Bay and other prefecture. On the contrary, inNorthern Chiba Area, where the clam fisheries relies only upon wild clam stocks without
any transplantation, the clam production has sharply declined from around 10,000 mt inlate 1970s to 800 mt in 1999 reflecting directly the poor occurrence of wild juvenile clam.
The cause of the substantial decline of the wild juvenile clam is still not known.
Key words: Manila clam, Tokyo Bay, stock decline, early life cycle, coastal development

Along the coast of Tokyo Bay, the clam fisheries and culture have been operating in the
tidal and shallow water area since before theWorld War II. Before 1960s, harvested species
were mainly hard clam, Manila clam, surfclam, blood cockle, Pacific oyster, and others.
However, at the present, only Manila clam andsurf clam dominate the bivalve fisheries production.
The annual production of Manila clam in
Chiba Prefecture, which occupies most part ofthe production in Tokyo Bay, reached its peakin late 1960s over 70,000 mt (Fig. 1)* 2. Then the
production declined markedly to below 20,000
mt mainly because of large-scale reclamation ofcoastal area, where the clam fisheries intensively operated. However, the clam production
is only about 8,000 mt in 1999 as a result of continuous and gradual decline even after the cessation of the coastal development. This recent
decline in Manila clam production is the major
problem of the clam fisheries in Tokyo Bay;
however, the exact mechanism responsible forthe decline is still not well understood. In thismanuscript, I show the details of this problem
and several probable factors responsible forthis decline.

2003年 6 月12日受理（Received on June 12, 2003）* 1 Futtsu Laboratory, Chiba Prefectural Fisheries Research Center, Kokubo 3091, Futtsu, Chiba 293-0042, Japan. 0439-65-3071,
E-mail: cbfb@tokyo-bay.ne.jp.
* 2 Statistics of fisheries and culture production of manila clam are quoted from Annual Statistic Report of Agriculture, Forestry and Fisheries
in Chiba.

14

Mitsuharu TOBA

through decades under their natural environment and reproductive characteristics of theclam.
Recent variations of Manila clam productionin these two areas show quite different patterns; drastic declining in Northern Chiba andrelative stability in Kisarazu.
Northern Chiba

Fig. 1. Annual production of Manila clam in Chiba
Prefecture after 1965.

Fig. 2. Culture and fisheries area of Mania clam inTokyo Bay.

Northern Chiba is located in the bottom inside of Tokyo Bay. West, east and North of thearea are surrounded by reclaimed land, andIchikawa Sea Route divides the area into west
and east. The bottom level of this area is almost 0 to−2 m in tidal level; the bottom surface is not completely exposed to air even while
ebb tide.
As the production in this area relies only
upon naturally occurring clams, the clam production has relatively large fluctuation (Fig. 3).
With fluctuation, the clam production tends todecline in these years, especially in 1990s. The
production in 1999 is only about 800 mt.
Despite recent poor production, fishermen do
not transplant any seed clams except during
small-scale experimental culture trials. This isbecause that the naturally occurring clams
were so abundant in this area that they did nothave to use any stock enhancement for a longtime. And also because, this may be the pri-

Culture and fisheries areas in Tokyo Bay
Three major areas of clam culture and fisheries in Tokyo Bay, Northern Chiba, Kisarazu,
and Futtsu, are located east coast of the bay in
Chiba Prefecture (Fig. 2). Each of them has
somewhat different operating patterns fromthe other. For instance, the production in
Kisarazu is mainly based on the transplanted
clam from outside of the area, while inNorthern Chiba production relies only upon its
domestic clams that naturally occur. This isdue to their historical customs of fisheries asmentioned later, probably being formed

Fig. 3. Annual local production of Manila clam in
Chiba

The decline of Manila clam stock in Tokyo Bay.

15

mary reason, the transplantation is highly
risky for them economically, as the frequentmortality will collapse the plans of the clam
growing and harvesting in this area.
In this area, unpredictable accidental mortality often have occurred. Some of them werecaused by Aoshio (blue tide), upwelling of theoxygen-deficient seawater from the bottom of
the subtidal zone. When the strong wind blows
in the direction from the land to off shore during spring and fall, bottom seawater comes up
as the counterbalance of the surface seawaterthat moves away to offshore (Kakino et al.,1987).
Ichikawa Sea Route, which runs through the
middle of the area, is connecting to Edogawa
Flood Control Channel. When the water level of
Edogawa River rises beyond a certain level dueto the heavy rain, such as the case in the typhoon, the floodgate is opened and a great dealof muddy fresh water flows out. Then the salinity of seawater reduces extremely for days,
and the mud deposits more than 10 cm in thickness in certain cases and covers the bottom surface for weeks or months. During 15 years
from 1985 to 1999, any mass mortality was absent only 6 years in this area (Kakino, 2000). In
addition to the mortality of the adult clam bysmothering and burying, the mud deposition
may inhibit the new recruitment of clam larvae.
Furthermore, population density sharply de-clines in winter every year (Fig. 4). In 19941998, the clam density reached annual peak insummer season, more than hundreds ofinds/
m2, and decreased to below 100 inds/m2 in winter. Winter mortality is considered to be causedby complex interaction among several factors(Chiba Pref. Fish. Exp. Stn. and Chiba Pref.
Fed. Fish. Co-op. Union, 1998). Firstly, the reduction of clam viability by the low temperature and low food condition in winter.
Secondly, disturbance of the bottom surface by
the stronger wave action in this part of the season. This is related to the subsidence of theland level due to drawing up large volume ofground water during coastal development. By
the reduction of the land level, large wave directly reaches deep inside the shallow area.
Besides these factors, the predation by somekinds of mallard, which migrate to this area
during winter, is also an important factor(Chiba Pref. Engineering Dept. and Chiba Pref.
Enterprise Dept., 1999).
Until mid 1990s, the population density ofthe total clam was constantly above 400 inds/
m2 in spite of the mortalities. That was due tothe quick recovery of clam stock after the massmortality. However, the clam density began to
decline rapidly after late 1990s, and it still continues. In particular, the low density of juvenileclam after 1990s is characteristic feature of thisarea (Fig. 5).

Fig. 4. Seasonal change of the stock density of
Manila clam in Northern Chiba.

Fig. 5. Changes in the stock density of Manila clamin Northern Chiba.

16

Mitsuharu TOBA

Kisarazu
The culture and fisheries ground in Kisarazu, which is located in the east coast of thecentral Tokyo Bay, is the tidal area of bottom
level −2 to ＋1 m in height. The clam production in this area is the largest in Tokyo Bay.
The major production of clam in this area relies
upon transplanted seed clams. As the densityof naturally occurring juvenile clams is relatively low, there remains large tidal area thatis used for culture.
The clam production from the transplanted
plot from 1986 to 2000 is about 4,000 to 6,000 mt
and that from naturally occurring plot is 200
to 1,100 mt. Thus, production from naturally
occurring plot is only 6 to 25 ％ of that oftransplanted plot. After 1986, the annual
amount of transplanted seed clam, which is introduced from other clam-producing district insouthwestern Japan, is 2,200 to 5,000 mt. The
shell size of transplanted clam was about 20
mm in length. Recently, the clam size of 25 to
30 mm, which is the minimum size of the clams
circulating the commercial market for thehuman consumption, is used as the seed. This
reflects the decline of naturally occurring juvenile clams all over Japan.
The density of naturally occurring juvenile
clams in Kisarazu decreased from about 70 to
10inds/m2 during 1989 and 2000 (Fig. 6). Despite
that, the stable total clam production in thisarea is supposed to be owing to large amount of
the seed transplantation. The period of consistent decline of juvenile clam is common to thatof Northern Chiba.
Factors common to Northern Chiba andKisarazu
I think I can indicate some of the probablefactors responsible for the decline of clam stock
as local and common factors (Table 1). As mentioned above, the poor occurrence of wild juvenile clam is common characteristics to these
two areas. Therefore, I am paying attention to
the early stage of the life cycle of the Manila

Table 1. Probable factors responsible for the declineof clam
1 Local factors (Northern Chiba)・ Accidental mortality by blue tide
(upwelling of oxygendeficient seawater)・Accidental mortality by river flood
・Winter mortality
2 Common factors to the areas
・Reduction of entire habitat by the coastal
reclamation
・Contraction of the effective spawning period
・Larval mortality due to oxygen deficientseawaterFig. 6. Changes in the stock density of Manila clamin Kisarazu.

clam in Tokyo Bay.
One of the most important factors influencing the decline of clam stock may be reductionof the habitat area (Fig. 7). Results of the investigation in 1945 and 1985 show that nearly 90％ of the tidal area was lost.
Manila clam has the spawning period inwarm water season; May to October in Tokyo
Bay. Newly hatched larvae have a strong negative geotaxis, and 2 to 4 weeks of swimming period until settlement. From the results of thestudies on the seawater current, the larvae,
which are spawned at the coastal area, may bedispersed and transported throughout the bay,
and mixed during the swimming period. The
bay area may play an important role as the
habitat of the larval stage for the Manila clam

The decline of Manila clam stock in Tokyo Bay.

population in Tokyo Bay. While the shallow or
tidal coastal area has reduced greatly in thepast few decades, the bay area is almost constant. The reproductive potentiality of theManila clam in Tokyo Bay is reduced by declineof the total fecundity of the adult clam.
Furthermore, the larvae dispersed all over thebay have much less chance to get back to thescattered shallow areas where they can settle.
Manila clam has two peak periods of gonadal
maturation in a year; spring and autumn inNorthern Chiba. While the fecundity of clam
seems greater in spring spawning (Toba et al.,1993), adult density in spring is very low because of the winter mortality. The clam population in Northern Chiba may not spawn
effectively in spring season.
The peak spawning period of Manila clam in
Kisarazu is suspected to be once in a year during summer months from the observation of
the seasonal changes in condition factor. And
the transplanted clams that have different seasonal reproductive patterns from native clams
may influence the low peak values of condition
factor in the clam population in Kisarazu.
Three peaks of the larval density were recorded in post summer months, August,
September, and November at the adjacentpoints of Northern Chiba from May to
December in 2001. The peaks of postlarval den-17sity, smaller than 0.4 mm in shell length, wereobserved 2 to 4 weeks after the peaks of larval
abundance. In Kisarazu as well, the peaks ofthe larval and postlarval density were observedin post summer months during 2000 and 2001.
Substantial spawning and postlarval recruitment for the clam population may contract topost summer in Tokyo Bay in these years.
During the warm water season from May to
October, the bottom layer of the large part inbay area is covered by oxygen-deficientseawater (Ishii, 2003). The thickness of oxygendeficient layer often grows more than several
meters especially in north bottom side of thebay. Although the thickness of oxygendeficient bottom layer gets lowered temporally
by the stormy weather, it builds up quickly
again under the calm weather within few days.
Thus, oxygen-deficient seawater lies intermittently during whole warm water season. As thelarval swimming activity is markedly reducedin oxygen-deficient seawater, continual appearance of oxygen-deficient layer may affect thesurvival of larval population in Tokyo Bay formonths.
Conclusion
I suspect that not only the sharp decline of
Manila clam production before late 1970s in

Fig. 7. Reduction of the clam habitat in Tokyo Bay during 1959-1984.

18

Mitsuharu TOBATokyo Bay but also the gradual decline afterwards may be affected by the series of thecoastal reclamation that ceased in 1979. One of
the marked and common characteristics of theclam populations in local areas during latter
period is continual decline of the recruitment of
natural juvenile clams. Reduction of adult
population, contraction of reproductive period,
larval mortality caused by oxygen-deficientseawater, and reduction of shallow or tidal
area for larval settlement may involve poor recruitment of juvenile clam. Temporal massmortality including adult population caused by
the blue tide, river flood, low temperature andwave action, predation by the birds seems to accelerate the decline of clam stock.
The ecological impact on the clam populationby the artificial modification of their habitatand hypertrophication of the bay area may
appeare through certain period as long as morethan 20 years. Unfortunately, however, as
mentioned before, the exact mechanism responsible for the decline is still not well understood.
References
Chiba Prefectural Fisheries Experiment
Station and Chiba Prefectural Federationof Fishermans Co-operative Union, 1998 :Report of the investigation on the causative factors of Manila clam winter mortality in Northern Chiba, 59pp.
Chiba Prefectural Engineering Department
and
Chiba
Prefectural
Enterprise
Department, 1999 : Variations of the environmental conditions in Sanbanse, 86pp.
Ishii, M., 2003 : Estimative method of oxygendeficient water mass scale in Tokyo Bay.
Bulletin of Chiba Prefectural Fisheries
Research Center, 2, 29-37.
Kakino, J., Matsumura, S., Sato, Y., and Kase,N., 1987 : Relationship between Aoshio,
blue-green turbid water, and wind-driven
current. Nippon Suisan Gakkaishi, 53(8),1475-1481.
Kakino, J., 2000 : Studies for the Japanese littleneck clam Ruditapes philippinarum
mortality due to wave action on the Banzu
tidal flats, Tokyo Bay. Doctoral thesis,
Tokyo University of Fisheries, 140pp.
Toba, M., Natsume, Y., and Yamakawa H.,
1993 : Reproductive cycles of Manila clam
Ruditapes philippinarum collected from
Funabashi waters, Tokyo Bay. Nippon
Suisan Gakkaishi, 59(1), 15-22.

水研センター研報，別冊第 1 号，19−31, 平成16年
Bull. Fish. Res. Agen. supplement No. 1, 19-31, 2004

19

Environmental conditions relevant to aggregative distribution ofmacrobenthos below coho salmon culture cageRyo SASAKI* and Akio OSHINO*

Abstract Actual changes in environmental conditions relevant to aggregative distribution of the macrobenthos below coho salmon culture cage were examined by diving observation at Onagawa Bay in 1990s. Organic sediment derived from leftovers of moisture
food pellets and fish feces were 15 cm in height at the center below culture cage.
Dominant species of macrobenthos were identified Nebalia bipes, Schistomeringos japonica, Melita sp. and Capitella spp. Highest density of Nebalia bipes was found ca. 40,000
inds./m 2 and that of Schistomeringos japonica was ca. 5,000 inds./m 2 from enriched sediment on the bottom surface. Aggregative distribution of Nebalia bipes andSchistomeringos japonica were monitored at 10-m distance zone from the center point insummer, and that of Nebalia bipes and Melita sp. were monitored within 5-m distancefrom the center in winter. From the ecological viewpoint for these external distributions, aggregative position of macrobenthos was correlated to the marginal zone of enriched sediment. Biological activities so-called bioturbation were recognized inconjunction with synchronous patterns of the distribution between macrobenthos andorganic sediment below culture cage.
Key words: coho salmon, macrobenthos, environmental condition

The work described here has the aim of obtaining information on the ecological relationship between decomposition of organic
sediment and distribution of macrobenthos
below coho salmon culture cage. To assess theimpacts of fish farming and to prevent selfinduced deterioration, several criteria for theprotection of the environment aroundaquaculture farms have been proposed andsummarized (Yokoyama, 2000). In order to establish the most prudential plan to prevent environmental deterioration around fish farmsite, we need to understand the following ecological basis. Firstly, promotion of circulated
nutrient linkage converted by mineralizationfrom the loaded organic sediment decomposed
through bacteria and macrobenthos toward

ongrowing of sedentary fish, which is regarded
as a part role of the cyclic processes in natural
ecosystem. Secondary, retrieval of economicalmaterials such as a sedentary fish which converted by macrobenthos with enriched sediment in the course of fishing is a removal stepfor discharging the organic loads to outside of
ecosystem through food chain in the benthic
community (Tamai, 1990).
Ohmori et al. (1995) has already estimated on
the organic loads derived from coho salmon
culture by analyzing culture records of fisherman's annual diary, and pointed out that low
oxygen levels were yearly correspondent to theincreasing production of coho salmon at
Onagawa Bay during early 1990s. Key problem
to study actual changes in environmental

2003年 6 月12日受理 (Received on June 12, 2003)* Kesennuma Miyagi Prefectural Fisheries Experimental Station, 119 Hajikami, Kesennuma, Miyagi 988-0247 Japan.
Email: Kssuisi@pref.miyagi.jp

20

Ryo SASAKI and Akio OSHINO

conditions below fish culture cage lies in improving the methods for monitoring organic
sediment and macrobenthos, which sample wasindirectly obtained with Ekman-Birge grab
conducted by surrounding researcher on theboat. This lack of understanding is mainly due
to underwater research activity and also due todifficulty in sampling methods for macrobenthos below culture cage where environmental conditions are dark, dirty anddangerous for research diver.
In addition to the finding on the nitrogenloads to the environmental water caused by thefeeding (Ohmori et al., 1995), we tried to findoutthecorrelationshipbetweentheaggregative distribution of macrobenthos andloaded organic sediment that needed to establish the actual contribution for preventing thedeterioration. Furthermore, effects of shellcollector as a habitat for macrobenthos were
investigated to promote the decomposition oforganic sediment and artificial improvement
for a bio-monitoring function of environmental
condition on the bottom surface below culture
cage.
Materials and Methods

Fig. 1. Location of northern part of Japan and coast
map of Miyagi Prefecture showing the study site

Fig. 2. Monthly changes in water temperature ofsurface and 20-m depth layer in Onagawa bay

Onagawa Bay (38°24'N, 141°29'E), which has
an area of 12 km 2 and a mean depth of 19 m, isa typical embayment where mariculture farms,
e.g. oyster, scallop, and coho salmon, aredensely distributed（Fig. 1）. Water temperature of surface ranged from 21 ℃ in August
and to 7 ℃ in February, and that of 20-m depth
ranged from 19 ℃ in September to 8 ℃ in
March, respectively. Depth of the study sitewas 20 m and bottom water temperature between August and October during post harvest
time were more than 18 ℃ (Fig. 2).
Coho salmon culture is generally started
from November with 150 g of body weight fora juvenile and continued until following July
with 3 kg body weight for a harvest size, sothat absent periods for culture attains 3
months from August through October. Initial
density of juveniles in a cage was approximately 15,000 and harvest time 10,000 individuals. The size of culture cage was a regularsquare of 13-m long with 10-m depth net.
Comparing the correspondence between
trend of coho salmon production and environmental conditions in bay-wide, macroscopicchange of dissolved oxygen as a bottom watercondition and total sulfide value as a sedimentcondition were reexamined by the monthly recording data-book on environmental survey of
Onagawa Bay (Miyagi Prefecture, 1982〜2000).
Dissolved oxygen at surface and bottom
water was measured monthly from June
through November 1996 in the vicinity of
studying culture cage. Bottom sediments werecollected by the core-tube of 6-cm diameterwith a cap. Core samples were carefullyMacrobenthos below culture cagecollected by diver's hands at each 5-m intervals
from the center point toward out-skirt with 30m-long distance by 5-m intervals.
In order to estimate the influence of fish culture, the scale-bar marked 5-cm interval recognizing for the degree of sedimentation was set
by diver at the center point of the bottom surface below culture cage in May 1996. Height oforganic sediments before and after harvest derived from leftovers of moisture food pellets
and fish-feces were recorded by underwater
camera once in a month until following years.
Monthly fluctuations of total sulfides (TS),chemical oxygen demand (COD) and ignition
loss (IL) values of bottom sediments regarded
as the organic indicator were monitored to define a boundary of the enriched area at each 5m intervals from the center point below culture
cage.
In addition to the measurement of environmental conditions, spatial and temporal distribution patterns of macrobenthos werecompared below culture cage. Bottom sediments in a 0.2 m 2 was dragged for collecting
macrobenthos with 1-mm mesh net by diver's
hands from the center point toward out-skirtof 30-m-long distance by 5-m intervals in July,
September, December, 1996 and February 1997.
In the course of research activities, feeding ofmoisture food pellets for the culture cage wasdiscontinued at this study site after July 1996
by the cessation of culture operation with costdisadvantage. After then, distribution ofmacrobenthos and TS, COD and IL value of
sediment were traced at the same center area
below culture cage until August 1997 to compare with those of the environmental conditions in July 1996 of the harvest time.
In order to examine the dependency of
Nebalia bipes, a dominant species of macrobenthos in the study site, shell-collector bag as
a habitat for shelter substratum was set on thebottom surface at each 5-m intervals from thecenter point. Shell-collector bag was composedby 10 pieces of oyster shells. The control sample
against shell-collector bag was collected at thedirect vicinity of each area by the same square.

21

Besides outdoor observations for the distribution pattern of macrobenthos, feeding responses between sedentary fishes distributed
around culture cage against macrobenthos
were confirmed by the indoor rearing experiment, which frozen Nebalia bipes andSchistomeringos japonica were put into theFig. 3. Trends in production and growers of coho
salmon culture in Onagawa bay, Miyagi Prefecture
1982 - 2000

Fig. 4. Yearly changes in dissolved oxygen value ofthe bottom water in July and total sulfide value ofthe bottom sediment at August in coho salmon culture ground, 1982-2000

22

Ryo SASAKI and Akio OSHINO

tank fed for several species of fishes.
Results and Discussion
1. Environmental conditions at coho salmon culture area
Production of coho salmon culture in
Onagawa Bay has developed increasingly from1980s, then matured in early 1990s and decreased in subsequent several years including
cessation of operations due to cost disadvantage. The total production reached a peak in
1992 when 10,769 ton were landed with 148
growers, and bottomed in 1998 when 5,021 ton
were landed with 62 growers (Fig. 3).
Changes in dissolved oxygen saturation as abottom water condition in summer of early
1980s ranged between 120 ％ and 80 ％, after
then oxygen value decreased abruptly and attained lowest in 1990 with 26 ％, and recovered
yearly until 2000 with 85 ％ (Fig. 4). Changes intotal sulfide value as a sediment condition ofcoho salmon culture ground also attained ahighest value in 1994 with 0.9 mg/g･dry･sediment, which tend to follow the deterioration ofwater condition and recovered yearly until 2000
with 0.2 mg/g ･ dry ･ sediment. Both oxygen
concentration and total sulfide value were subsequently appeared in corresponding to thosepeak years by over-production of coho salmon
culture. In recent years, the relationship between the production of coho salmon and decreasing value of dissolved oxygen and total
sulfide were regarded as a balanced load between organic deposit by culture production
and decomposition by natural environment. In
relation to this tendency, Yokoyama (1995) described that large biomass at the innermost
part of Ohmura Bay suggest that a relatively
high concentration of sulfide (0.45-0.75 mg/g･
dry sediment) never prevents distributions ofanimals, and that organic enrichment of thesediments is sufficient to provide a rich foodsource but is not yet high enough to cause serious oxygen depletion .
Organic loads in bay-wide derived from coho
salmon culture with feeding moisture pellets

Fig. 5. Annual amount of organic loads and equivalent nitrogen discharge for a grower of coho salmon
culture (after Ohmori et al. 1995)

has already estimated at the same area in early
1990s by analyzing culture records of fisherman's diary (Ohmori et al, 1995). According to
the estimation of each parameter, annual
amount of organic loads as equivalent to nitrogen discharge was calculated 6,767 kg a grower
from total amount of food supply. This amountof nitrogen divided into 1,640 kg as 25 ％ forlanding of culture production and 5,127 kg as
75 ％ for discharging to the environmental waters (Fig. 5). Nitrogen load against the environmental waters was corresponded to 9 ％ of total
landing of cultured coho salmon, so that annual nitrogen load was estimated approximately 2 ton/day in Onagawa Bay (Ohmori etal., 1995).
2. Environmental conditions below culture cage
Saturation of dissolved oxygen at surface
water in the study site was 96 ％ in average,
ranging 137 ％ at highest in June and 76 ％ at
lowest in October, and that of bottom water
was 73 ％ in average, ranging 53 ％ at lowest in
September and 84 ％ at highest in November.

Macrobenthos below culture cage

Monthly changes in the height of sediment
derived from leftovers of moisture food pellets
and fish feces was directly measured by scalebar set below the center of culture cage (Fig. 6).
Maximum sedimentation was monitored 15 cm
in height at the harvest time in July 1996, andthen decreased month by month until following
February 1997 when original ground was again
exposed through the decomposition processesof organic sediment (Fig. 7). Feeding was ended
by culture cessation in July 1996. Therefore, it
was evident that the time for decomposition oforganic sediment derived from food supply requires nearly 7 months under natural environmental conditions. The volume of organic
sediment at harvest time was estimated approximately 37 m3 below culture cage, which
was calculated from the distributed range of
sedimentation within 25-m diameter measured
by diver.

23

The TS, COD and IL values of bottom surface
were monitored to define a boundary of the enriched sediments collected at each 5-m intervals
from the center point toward outer area below
culture cage, which expressed the marginalzone decomposed organic sediments by benthic
communities（Fig. 8）. A peak of TS values was
1.22 mg/g ･ dry sediment at 10-m distance inJuly, 1.98 mg/g･dry sediment at 5-m distancein September and 1.65mg/g･dry sediment at 5m in December 1996. A peak of COD values was
270mg/g･dry sediment at the center in July,
255 mg/g ･ dry sediment at 5-m distance in
September, 182 mg/g･dry sediment at the center in December 1996 and 104 mg/g･dry sediment at the center in February 1997. A peak of
IL values was 59 ％ at the center in July, 42 ％at 5-m distance in September, 35 ％ at the center in December 1996, and 26 ％ in February
1997.

Fig. 6. 1：Scale-bar in the bottom sediment at harvest time (photographed in July 1996). 2：Con
tents of core tube samplers viewing from lateral side. 3 ： Aggregative distribution of
Schistomeringos japonica on the bottom sediment. 4：Scale-bar in the bottom restored original
condition (photographed in Feb. 1997)

24

Ryo SASAKI and Akio OSHINO

According to the change in a peak position of
COD and IL values below culture cage, simultaneous fluctuations corresponded to each monthindicate removable contraction of organic sediment from outer marginal zone toward the cen-Fig. 7. Monthly changes in the height of sediment
derived from leftovers and fish feces below culture
cage monitored by scale-bar

ter area through the decomposition processesof organic sediment. The TS, COD and IL values as a chemical indicator of the bottom conditions suggest in general that the influences oforganic sediments were limited within 10 to 15m distance area from the center point in summer and within 5-m distance in winter throughthe synchronous contraction. In relation tothese findings, azoic conditions and high TS
value (over 1.3mg/g･dry sediment) were foundat the fish farm in Gokasho Bay during thesummer, which suggested a key factor in eliminating the macrofauna in organic enriched
habitat and significant negative correlation between the sulfide content and the density of themacrofauna (Yokoyama et al., 1997).
3. Distribution of macrobenthos below culture
cage
Dominant species of macrobenthos collectedby dragging with hands-net through bottom

Fig. 8. Changes in total sulfide, chemical oxygen demand and ignition loss values of bottom sedimentcollected from each 5-m intervals within 30-m distance from the center point below culture cage

Fig. 9. Photographs of Nebalia bipes (A) andSchistomeringos japonica (B)Macrobenthos below culture cage

sediment below culture cage were identified as
Nebalia bipes and Schistomeringos japonica(Fig. 9).
From the indoor observations under rearing
conditions, the response of Nebalia bipes to thelight is strongly photonegative, hiding andburrowing underneath bottom sediment in thedaytime and swarming up and crawling aroundbottom surface in the dark. Nebalia bipes behaves as carnivorous feeder, which tends tocause economical damage for coastal fishing by
aggregating and feeding the fishes left, caught
within gill-net (Nishimura and Hamabe, 1964).
The habitat of Nebalia bipes seems to be widelyadopted to low oxygen conditions under chemically reduced environment. Maturing adults
holding larvae within brood-pouch were collected in summer and subsequent juveniles wereappeared in autumn. Average body length
measured between carapace and telson were 6.9mm in April, 5.7 mm in August, 4.9 mm inNovember 1996 and 4.2 mm in January 1997.
Yokoyama et al. (1997) pointed out that
Nebalia bipes had its maximum density (700inds./m 2) at fish farm site of Gokasho Bay inMay, probably due to the deoxygenation of thebottom water accompanied by increasing temperatures and increasing activities of fish
farming.
From the field observations, Schistomeringos
japonicas aggregates to the leftovers, fish fecesand empty shells of fouling animals etc., which
distributed on the surface of sediments covered
ordinarily by sulfur bacteria Beggiatoa spp.
The habitat and behavior of Schistomeringos
japonicas seems to be similar to that of Nebalia
bipes, which originally adopted to chemicallyreduced environment. Maturing adults ofSchistomeringos japonicas were recognized by
its visible gonad through the translucent skinwith body length ca. 10 mm in summer, andsubsequent juveniles were appeared in autumn.
Schistomeringos japonicas adapted for a tolerance to azoic conditions and distributed frequently in the byssus of Mytilid communities
under polluted waters. It is supposed that thisspecies performs important role for decomposi-

25

Fig. 10. Changes in the aggregative distribution of
the macrobenthos (■: Nebalia bipes, ▲: Melita sp.,●: Schistomeringos japonica and×: Capitella spp.)
collected in 0.2 m2 from each 5-m intervals within
30-m distance from the center point below culture
cagetion of organic sediments by grazing the substratum with its developed jaws under azoic
conditions (Miura, personal communication).
Seasonal changes in the aggregative distribution of dominant macrobenthos collected by
0.2-m2 sediment at each 5-m intervals within 30m distance from the center point below culture
cage were shown in Fig. 10.

26

Ryo SASAKI and Akio OSHINO

In the distribution of macrobenthos collected
In July, highest density of Schistomeringos japonica was found 5,240 inds./m 2 at 10-m distance from the center, that of Nebalia bipes
was found 3,760 inds./m2 at 10-m distance andthat of Capitella spp. was found 1,600 inds./
m2 at 15-m distance. Schistomeringos japonica
and Nebalia bipes dominated from 5-m to 15-mwith a peak at 10-m distance from the center
point. Fouling organisms including oyster,mussel, barnacle etc. fell down to the bottom
from culture facilities, which materials exposedon the bottom surface seem to be suitable habitats as shelters for Schistomeringos japonica
and Nebalia bipes.
Distribution of macrobenthos collected in
September, highest density of Nebalia bipes
was found 23,340 inds./m2 at 10-m distancefrom the center, that of Schistomeringos japonica was found 4,500 inds./m2 at 10-m distance,that of Melita sp. was found 3,360 inds./m2 at
10-m distance and that of Capitella spp. wasfound 400 inds./m2 at 20-m distance. Nebalia
bipes, Schistomeringos japonica and Melita sp.
were dominant in order at 10-m distance fromthe center point. Comparing with the densityof July, the number of matured individuals of
Schistomeringos japonica was decreased by assuming mortality due to spawning. It was evident that those macrobenthos tend toaggregate around the immediate vicinity besides organic sediments and impoverish in acenter area where organic sediments wereabundant.
In the distribution of macrobenthos collected
in December, highest density of Nebalia bipes
was found 42,480 inds./m2 at 5-m distance fromthe center, that of Schistomeringos japonica
was found 4,160 inds./m2 at 5-m distance, thatof Melita sp. was found 4,350 inds./m2 at 10-m
distance and that of Capitella spp. was found
240 inds./m2 at 20-m distance. In December, distribution pattern of macrobenthos were synchronously removed toward the center fromout-skirt area and concentrically limited
within 10-m distance around the center point.
Matured individuals of Schistomeringos

japonica were already disappeared and only juveniles dominated within 10-m distance zone.
High abundance of juveniles of Nebalia bipes
was characteristically found within 5-m distance zone from the center point. Fouling
empty shells and particle fish-bones derived
from raw fish in moisture pellets were exposed
again on the natural ground, which corresponded to the decomposition of organic sediment below culture cage.
Distribution of macrobenthos collected in
February, highest density of Nebalia bipes wasfound 16,800 inds./m2 at the center, that of
Melita sp. was found 10,400 inds./m2 at the center and that of Capitella spp. was found 520
inds./m2 at the center. In February, distribution pattern of Nebalia bipes and Melita sp.
were concentrated within 5-m distance fromthe center point, which organic sediment enriched macrobenthos for the nutrient consumption as a terminal area below culture cage.
Considering the distribution pattern in respect of each species, highest density of Nebalia
bipes was 42,480 inds./m2 at 5-m distance fromthe center in December 1996, that of Melita sp.
was 10,400 inds./m2 at the center in February
1997, that of Schistomeringos japonica was5,240 inds./m2 at 10-m distance in July and thatof Capitella spp. was 1,600 inds./m2 at-15m distance in July, respectively .
According to synchronous patterns of the
distribution between macrobenthos and organic sediment properties which was concerning the environmental viewpoint with thechemical indicator by TS, COD and IL values at
each season, aggregating sites of eachmacrobenthos were closely correlated to themarginal zone of enriched sediment below culture cage.
At the time of 1-year discontinuance after
culture cessation in July 1996, chemical indicesof organic sediments collected at the centerarea in July 1997 were changed from 0.79 mg/
g ･ dry sediment to 0.65 mg/g ･ dry sedimentwith TS value, from 257 mg/g･dry sediment to
151 mg/ mg/g･dry sediment with COD value
and from 54 ％ to 26 ％ with IL value,Macrobenthos below culture cage

respectively. Highest density of macrobenthos
at the same area was changed from 3,760 inds./
m2 to 110 inds./m2 with Nebalia bipes, from5,240 inds./m2 to 260 inds./m2 with
Schistomeringos japonica, from 50 inds./m2 to215 inds./m2 with Melita sp. and from 1,600
inds./m2 to 5,125 inds./m2 with Capitella spp.
Comparing with the data between 1996 and1997, it was supposed that the habitat evaluation below culture cage of Nebalia bipes andSchistomeringos was decreased and that of
Melita sp. and Capitella spp. was increased inaccordance with those nutrient conditions indicated chemical indices mentioned above.
From the indoor rearing observation by feeding
responseof
Hexagrammos otakii(greenling), Sebastes inermis (black rockfish),
Limanda yokohamae (marbled sole) andKareius bicoloratus (stone flounder), Nebalia
bipes and Schistomeringos japonica were almost fed with a desirable reaction. Comparing
the reaction time for feeding by these sedentary fishes between Nebalia bipes andSchistomeringos japonica, those fishes tended
to prefer Nebalia bipes. It was suggested that
Nebalia bipes and Schistomeringos japonica
were treated for suitable bait against adjacentsedentary fishes distributed around the enrichedsediment
below
culturecage.
Furthermore, dispersion by ongrowing and retrieval by fishing of these sedentary fishes are
regarded as a removal step for macrobenthos
propagated by enriched sediment, which has a
responsibility for promoting discharge of organic loads to outside of ecosystem throughfood chain in the benthic community at the fish
farm site.
4. Evaluation of shell-collector
Considering
thedistributionofmacrobenthos below culture cage, Nebalia
bipes dominated in a year-around and recognized as effective species for decomposition ofloaded organic sediment. Spatial and temporal
distribution patterns of Nebalia bipes were reexamined by the comparative observation conducted within and without shell-collector set

27

Fig. 11. Spatial and temporal distribution of Nebalia
bipes below coho salmon culture cage. A: seasonalchanges in the density in 0.2 m 2 and aggregative position on bottom surface , B: seasonal changes in theaggregative position distributed within shellcollector bag, C: comparison of monthly density between shell-collector bag and bottom surface in 0.2
m2

for a monitoring of shelter substratum (Fig.
11). Distribution of Nebalia bipes was delineated with aggregative pattern in a certain position, which location was seasonally shiftingfrom outer area toward the center point corresponded to the marginal zone of enriched sediment under natural conditions (Fig. 11A). The
reason for shifting distribution was supposedthat the behavior of Nebalia bipes depended
highly on the habitat with shelter materials including empty shells and so on that were exposed subsequently on the bottom surface bysediment decomposition with passing of theseason.

28

Ryo SASAKI and Akio OSHINO

The average number of Nebalia bipes distributed within shell-collector in summer (Augustand September) attained 2,335 individuals at
the center and 1,075 individuals at 5-m distancezone. Furthermore, that of Nebalia bipes distributed within shell-collector in autumn(October and December) attained 590 individuals at the center and 817 individuals at 5-m distance zone, respectively (Fig. 11B). It wasevident by the indoor rearing observation that
Nebalia bipes expressed a photonegative response and a high dependency with substratum
such as shell-collectors like a shelter for habitatin daytime. On the other hand, the number of
Nebalia bipes without shell-collector distributed in natural bottom condition was almost
nil at the center area during summer andautumn, the aggregative distribution of
Nebalia bipes was limited outer area than 5-m
distance zone without in winter as shown in
Fig. 11A.
On the monthly changes in the density of
Nebalia bipes from May through October 1996
collected at the center area below culture cage,
the average number of Nebalia bipes distributed within shell-collector was 2,684 individuals
and that without shell-collector was 97 individuals, respectively, density variance of 28
times (Fig. 11C). Comparing the efficiency ofshell-collector between oyster and scallop
shells, the average number of Nebalia bipes
was 2,940 individuals with oyster and was 2,330
individuals with scallop. On the other hand,that of control sample collected direct vicinity

Fig. 12. Shematic diagram showing seasonal changes in sedimentation and aggregative distribution of themacrobenthos below coho salmon culture cage

Macrobenthos below culture cageof shell-collector was 13 individuals. At thesame time, the number of Nebalia bipes collected oyster shell-collector suspended 10-cm
distance above the bottom was 528 individuals.
It was supposed that the suitable position ofshell-collector was partially moated onto thebottom surface with enriched sediments. Fromthe ecological viewpoint, the center area below
culture cage was originally impoverished for
macrobenthos by its environmental conditionof bottom surface covered with enriched sediment, which was improved to the aggregativesite for artificial habitat of Nebalia bipes set byshell-collector.
Concerning another species of macrobenthos,
the average number of Melita sp. distributed
within shell-collector at the center area was 59
individuals in summer and 453 individuals in
winter. On the other hand, that without shellcollector in natural bottom sediment was almost nil at the same area below culture cage.
From monthly changes in the density of
Schistomeringos japonica from May throughJuly collected at the center area below culture
cage, the average number of Schistomeringos
japonica distributed within shell-collector was
1,503 individuals and that without shellcollector was 216 individuals, respectively, withmean density variance of 7 times. The adult
number of Schistomeringos japonica was disappearing after August due to mortality attributed to reproduction.
Therefore, spreading shell-collectors regarded as a habitat for macrobenthos seems to
be much more effective to promote the carrying
capacity of macrobenthos below culture cage,
which improve the decomposition processes oforganic sediment.
Conclusion
According to direct diving observation below
culture cage, it was evident that the organic
sediments derived from food supply were deposited 10 to 20 cm in height and 20 to 30 m indiameter through harvest time, in which sediments were decomposing until following spring29

under natural environmental conditions (Fig.
12). Aggregative distribution of thosemacrobenthos was corresponded to the marginal zone of enriched sediments, which location was seasonally removed before and after
harvest. High density of Schistomeringos japonica and Nebalia bipes were supported in accordance with organic sediments distributed
around removing marginal zone below culture
cage from spring to summer, and that of
Nebalia bipes, Melita sp. and Capitella spp.
were supported there from autumn to winter.
On the contrary, very few macrobenthos appeared at the center of bottom surface below
culture cage where enriched sediments wereabundant. These faunal zones might be generally constructed by the bottom substratum for
habitat based on the gradients of environmental conditions of organic loads that cause
the differentiation in the concentration of oxygen in the bottom water and nature of the sediment. Ecologically these distributions of eachmacrobenthos, close correlation between
aggregative site and organic sediments were
supposed by nutrient linkage. From these findings observed in each seasons, temporal andspatial distribution pattern were recognized asa change of environmental conditions of bottom surface below culture cage. Distribution
patterns of macrobenthos were concentricallyremoved from outer area toward the center
point according to the synchronous contractionof decomposed organic sediments in marginalzone by benthic communities.
Considering to synchronous patterns of removal distribution mentioned above, biologicalactivities of so-called bioturbation such as feeding, burrowing and gardening conducted bythese macrobenthos were recognized importantin preventing self-induced deterioration of fishfarming. In coastal and estuarine areas,
infauna is known to affect physical, chemicaland biological properties of sediment by
bioturbation, namely its feeding, burrowing,tube building, defecation and ventilation activities (Kikuchi and Mukai, 1994). Tsutsumi andMontani (1993) has already pointed out that the

30

Ryo SASAKI and Akio OSHINO

Capitella colonies increased rapidly and biological activities such as feeding, reworking
etc. efficiently decomposed the organic matter
added on the sediment. Besides these findingsof Capitella spp., rearing experiment of
Nebalia bipes, Schistomeringos japonica andMelita sp. would be needed to analyze the quantitative capacity of assimilation through decomposition processes of organic sediment.
A part role of decomposition andmineralization of the loaded organic matter
was confirmed by bacteria and macrobenthos
through cyclic processes under natural environmental conditions. Sulfate-reducing bacteria, Beggiatoa spp., was investigated in thebottom of coho salmon culture area and considered that occurrence and distribution of
Beggiatoa spp. was regarded as a indicator ofenvironmental conditions derived from the organic loads by food supply (Takekawa et al.,1989). The significance in distribution of relationshipbetweensulfur bacteria
andmacrobenthos would be furthermore needed toanalyze the efficiency of decomposition processes of organic sediment.
In addition to natural decomposition carriedout by those bacteria, it might be available that
artificial habitat such as shell-collector set on
the bottom surface promote the decompositionof enriched sediment through the activity ofbioturbation
with
those
speciesofmacrobenthos. It is supposed that spreadingshell-collectors as a habitat for macrobenthos
on the bottom surface below culture cage seems
to be effective for not only to promote the carrying capacity for decomposition of organic
sediments but also to control eutrophicatedconditions for improving the productivity of
aquaculture biomass. From the ecological relationship between macrobenthos and sedentary
fishes below culture cage, retrieval by sedentary fish propagated by macrobenthos with enriched sediment is a removal step for
discharging the organic loads toward outsideof natural ecosystem through food chain in thebenthic community.
Future work should be focused on the goalwith ecological basis for decomposition of organic sediment contributed by macrobenthos
and on the relationship between sustainablecarrying capacity and environmental conservation. The goal would be established by a biocontrol technology for planning mixed
aquaculture that organized with algae as mineral assimilator, bivalvia as filter-feeder andfishes as organic loader in respect to the circulated eco-system through nutrient linkage.
Acknowledgments
We sincerely thank Prof. T. Ohmori (Tohoku
University) for permission to use the data in
Figure 3.
We are grateful to Dr. T. Miura (Kagoshima
Univ.) for identification and information of
Schistomeringos japonica and Capitella spp.,
Dr. Y. Kamihira (Hakodate Univ.) for that of
Melita sp., Dr. T. Kikuchi (Yokohama Univ.)and Dr. R. Kado (Kitasato Univ.) for valuable
information on Nebalia bipes. Thanks also to
Dr. P. K. Park for improvements to the manuscript.
References
Kikuchi E. and Mukai H., 1994: Bioturbation :Changes produced by benthos in sedimentenvironments. Benthos Research, 46, 59-79.
(In Japanese with English abstract)
Miyagi Prefecture, 1982-2000: Data-book on environmental survey of Onagawa Bay.
Miyagi Prefectural Fisheries Experimental
Station. (In Japanese)
Nishimura S. and Hamabe M., 1964: A case of
economical damage done by Nebalia. Publ.
Seto Mar. Biol. Lab., 12, 173-175.
Ohmori M., Takeuchi M., and Arai E., 1995:
Nitrogen loads to the environmental water
caused by the feeding of coho salmon culture in Onagawa Bay. Suisan no kenkyu,
14(6), 57-66. (In Japanese)
Takekawa H., Ohta H., and Igarashi T., 1989:
Environmental conditions of occurrence
and distribution of sulfate-reducing

Macrobenthos below culture cagebacteria, Beggiatoa spp., at coho salmon
culture area. Bull. Kesennuma Miyagi Pref
. Fish. Exp. St., 8, 82-94. (In Japanese)
Tamai K., 1990: Tolerance of benthic animals tooxygen deficiency, in "Coastal fish farms
and the environment,"(ed. by WatanabeT.), Koseisha-koseikaku, Tokyo, pp.69-78.
(In Japanese)
Tsutsumi H. and Montani S., 1993: Utilizationof biological activities of Capitellid
polychaetefortreatmentofhedoro(organically enriched sediment) deposited on the marine bottom below fish
net pen culture. Nippon Suisan Gakkaishi,
59(8), 1343-1347. (In Japanese with English
abstract)
Yokoyama H., 1995: Macrobenthic assemblages

31

in Omura Bay-Ⅰ Community parameters
versus bottom environmental factors. Bull.
Natl. Res. Inst. Aquaculture, 24,43-53. (InJapanese with English abstract)
Yokoyama H., Abo K., Toyokawa M., Toda S.,
and Yamamoto S., 1997: Impact ofmariculture on the spatial and temporal
patterns of the macrobenthos in Gokasho
Bay. Bull. Natl. Res. Inst. Aquacult.,
Suppl., 3, 7-16.
Yokoyama H., 2000: Environmental quality criteria for aquaculture farms in Japanese
coastal areas -a new policy and its potential problems-. Bull. Natl. Res. Inst.
Aquacult., 29, 123-134. (In Japanese withEnglish abstract)

水研センター研報，別冊第 1 号，33−40, 平成16年
Bull. Fish. Res. Agen. Supplement No. 1, 33-40, 2004

33

Influence of environmental changes in the tidal flats on the filtration
and respiration of bivalve mollusks
Junya HIGANO*

Abstract Manila clam Ruditapes philippinarum and the other filter feeding bivalves intidal flat are not only commercially important as seafood, but also ecologically significant because of their filtration activity. The volume of water filtration by bivalves in
Ariake Sound is estimated to be equivalent to daily water exchange on the tidal flat in
1970s. However, the annual catch of Japanese littleneck has been decreased during thepast 20 years in Japan. Especially, rapid decrease in the clam population in Ariake
Sound since 1980s forced to depress the nationwide production. Recent coastal changes
such as land reclamation, dike, port, barrage, and dam construction presumably
brought about the environmental impact for filter feeding bivalves through water andsediment movement. Higher intertidal zone and supralittoral zone are intercepted by artificial structure such as dike and breakwater. Consequently suspended sediments areprevented from depositing at the higher intertidal zone and are drifted in littoral zone.
High concentration of mud particles suppresses the water clearance of the clams. On theother hand, reduction of water current by barrages encourages the stratification.
Hypoxia and anoxia often occur in subtidal zone of eutrophied sheltered coast under the
stratified layer in summer. Complex effects of mud increase and oxygen shortage areconsidered to be physiologically harmful to filter feeding bivalves. The ecological function of tidal flat has been destroying and it disturbs the recovery of the bivalve resources.
Key words: bivalves, coastal change, filtration, Manila clam, reclamation

Transition on production of filter feedingbivalves in tidal flats
Many kinds of filter feeding bivalve mollusks
inhabit in the tidal flat buried. Some of these
are not only commercially important, but also
ecologically important as a nutrient recycling.
In fact, Manila clam, Ruditapes philippinarum
Adams & Leeve, is the most abundant infaunal
bivalve in tidal flat of Japan. Major production
localities of Manila clam and the other commercially important filter feeding bivalves on
sheltered inlets in Japan are listed as; Tokyobay, Mikawa Bay, Ise Bay, Seto Inland Sea and
Ariake Sound crossing southern half ofJapan(Fig. 1). Fig. 2 shows the annual production of Manila clam in main prefectures and localities (Ministry of Agriculture, Forestry and
Fisheries, Japan, Statistics and Survey
Division, 1954-2001). There are three chronological stages in the clam production. The production from Tokyo Bay had occupied morethan half of national production at the firststage in 1960s. At the second stage, the depletion of Manila clams in Tokyo bay was attributed to land reclamation in 1960s to 1970s, and2003年 6 月12日受理 (Received on June 12, 2003)* National Research Institute of Aquaculture, Fisheries Research Agency 422-1 Nakatsuhamaura, Nansei, Watarai, Mie 516-0193 Japan
Email: higa@fra.affrc.go.jp

34

Junya HIGANO

Fig. 1. Main bays and estuaries where Ruditapes philippinarum and otherfilter feeding bivalves inhabiting in their tidal flats

it was compensated by increase of the clam production in Ariake Sound that had the largest
tidal flat in Japan. The annual catch had been
maintained more than 100 thousand tons until
mid 1987 since 1960. However, constant decrease of the clam in Ariake Sound since 1980s
forced to depress even national production at
the third stage. Only the production in Aichi
Prefecture has been maintained through about
50 years. The other commercially important
species of filter feeding bivalves has also decreased their production. Poker-chipped venus,
Meretrix lusoria, is one of the most valuable
clams in Japan, but decreased its production
earlier (Fig. 3) than on Manila clam. National
production of Poker-chipped venus has exceeded 10 thousand tons a year until 1966. It decreased very rapidly in 1970s by losing theirhabitat especially in Tokyo Bay. The clam wasconsidered to be predominant before increasing
the modern human activities because it is founddominantly in shell middens. It is difficult to
explain the reason why M. lusoria had decreased so rapidly by environmental changes
because there are few references (Kawamoto,
1967; Sagara, 1981) of environmental toleranceof M. lusoria than R. philippinarum. However,Fig.
2.
Annualproductionof
Ruditapes
philippinarum in Japan; Aichi-Pref., Chiba-Pref.
and total of four Prefs. in Ariake Soundthe fact that M. lusoria had started decreasingprior to Manila clam indicates this species prefers more natural habitat to have a dynamic
estuarine circulation connecting the rivermouth to tidal flat nearby.
There are several causes for explaining the
rapid decrease of bivalve resources in tidal flat
(Table 1). Over-catching is a commonly recognized cause on most of commercially important
species inhabiting in the bottom sediment.
Actually, the fluctuation of annual productionof R. philippinarum and M. lusoria reflect theInfluence of environmental changes in tidal flats for bivalves

35

influence of over fishing and recovering byregulation of catch. The other causes are deeply
concerned with environmental impacts byhuman activities. Physical alteration of coastal
area may affect physical properties of habitats
and chemical uses in watershed and sea area
may cause the incompetence in their reproduction. Decrease of filter feeding bivalves must
affect the coastal ecosystem by reducing theirfiltration.

Table 1. Causes of rapid decrease in filter feeding bivalves in tidal flats and its effects on the ecosystem

Depression of filtration by bivalve mollusks･Combining effects of hydrodynamics and organic load

What are possible causes?
･Over catching･Decrease of habitats
Land reclamation･Change of food supply･Change of bottom substrata･Anoxic or hypoxic water･Toxic chemical substances･Disease and parasites

What are main effects to the ecosystem?

Manila clams and the other filter-feeding bivalves play an important role in purification ofwater through their filtering activity.
Outbreak of exotic bivalves reportedly affected
the phytoplankton density in the sheltered sea
area such as San Francisco Bay (Alpine andCloern, 1992). In Ariake Sound, frequency of
red tide increased in 1990s whereas Tokyo Bay
and Mikawa Bay have had the increase in
1970s-1980s. This is caused by not only
eutrophication being connected to urbanization
around the bays but also depression of grazingpressure by filter feeders.
Based on the fisheries statistics (Statistics
and Survey Division, Ministry of Agriculture,
Forestry and Fisheries, 1954-2001) and clearance rate of Manila clam estimated by
Akiyama et al. (1986), I tried to estimate theFig. 3. Annual production of Meretrix lusoria inJapan; Mie-Pref., Chiba-Pref. and total of fourPrefs. in Ariake Sound･Decline of filtration capacity･Change of nutrient cycle･Increase of red tide･Increase of oxygen deficiency in the substrata

daily clearance rate by filter feeding bivalves in
Ariake Sound. In the calculation, it is assumed
that the average harvested size was 35-40 mm
in shell length which have specific clearance
rates of 0.83 L/hr/g WW at 24 ℃ and 0.23
L/hr/g WW at 10 ℃, where WW is flesh wetweight. Ratio of flesh wet weight to total wet
weight of Manila clam was averagely 0.4, thus
total catch could be converted to the flesh wetweight by multiplying 0.4. For the bloody cockles and the other bivalves, 1.676 L/hr/g DW at
24 ℃ and 0.635 L/hr/g DW at 10 ℃ derived
from the clearance rate of ark shell, Scapharcabroughtonii (Fujiwara, 1986 and Yamamoto etal., 1996), where DW is flesh dry weight. The
duration of filtration by Manila calm assumed
to be 22 hr a day as the average drying period
at low tide was two hr. For the other bivalves,
no drying period was considered.
Fig. 4 shows the annual change of daily
clearance rate of bivalves inhabiting in Ariake
Sound calculated under the condition that described above. This calculation contains many
assumptions, but it is considered to approximate real situation. It fluctuates year by year
and more than 300 million kL/day before 1990.
But in recent decade it has decreased continuously and reached one tenth of the highest

36

Junya HIGANO

value in 1970s. Although total clearance rate by
all bivalves was equivalent to daily water exchange rate on the tidal flat in spring tide (tidalrage is ca. 5 m) before 1990, that in 1996 to 2000
reached to only less than daily water exchange
rate in neap tide (tidal rage is ca. 3 m) (Table 2).
It is estimated that the clearance rate in winteris much less than daily water exchange rate inneap tide and nearly equal to daily river water
discharge. Depression of clearance rate means
the depression of all kinds of purifying andproducing process by bivalves around tidal flat.
It is connected to elimination of phytoplankton
or other suspended matter, feces andFig. 4. Daily clearance rate of filter feeding bivalvesin Ariake Sound calculated from statistical data of
their annual productions（see text for calculation）

pseudofeces production providing food for deposit feeders, retaining the nutrient to the bodies of bivalves and releasing inorganic
nutrients to the water column enhancing primary production. The very low level of clearance rate in recent years presumably
accelerates environmental deterioration in
Ariake Sound.
Coastal changes of sheltered sea area in Japan
Tidal flats in sheltered inlets or bays areformed by the relation between tidal current
and sediment movement. As, in general, floodtide currents are usually stronger than the ebbtide currents, sediment moved into the innerestuary on the flood being left behind on theebb (Little, 2000). Especially, at the upper partof the tidal flats tidal currents velocities arevery low and finer sediments are deposited,
then sediment in flats usually are sorted as
finer at the higher than the lower parts (Little,
2000). Bloody cockles, Anadara spp. and theother filter feeding bivalves inhabiting higher
intertidal zone may trap fine sediments
through their biodeposition and contribute toforming tidal flats (Fig. 5).
In Japan, coastal line has been artificiallychanged for many years. Especially in sheltered bays, reclaimed lands and artificial struc-

Table 2. Comparison among total volume of Ariake Sound, water exchange, water discharge from rivers and clearance rate of bivalves（Unit：
×106kL）
Total water volume

34,000Daily water exchange ontibal flat
50 years ago
Present

Spring tide

Neap tide

1,015

189

761

142

Daily discharge from rivers (average)
Clearance rate by R. philippinarum

21.9
24℃

10℃

Mid 1970s-mid 1980s

400-600

100-200

1996-2000

23-51

6 -14

24℃

10℃

Before 1990

400-1,000

100-370

1996-2000

61-177

21-63

Clearance rate by Total bivalves

Influence of environmental changes in tidal flats for bivalvestures such as dikes, breakwaters and jetties
have replaced natural coastal line. Reclaiming
tidal flats is the easiest way in order to extend
farmland, industrial zone and residential areas.
Ariake Sound has been gradually reclaimed fora long time since the sixth century in accordance with natural land forming. After Meiji
era (from 1868), huge undertaking of reclamation was started and the shoreline moved forward up to 5 km (Satoh, 2000). Tokyo bay wasreclaimed at the very rapid rate after 1945
(Koike, 1990) and natural coastal line remains
only 9.7 ％ whereas 19.6 ％ in Ariake Sound in1984 according to Coastline Survey, 3rd National
Survey on the Natural Environment (see: www.
biodic. go. jp / reports / 3-2 / hyo/ w064_001.
html). In other words, the pace of recent coastalchanges such as reclamation in tidal flat, construction of dike, port, dam and barrage is very
rapid and exceed the natural processes. It presumably brought about negative ecological impact for filter feeding bivalves throughhydrodynamic changes of water and sediment
movement. Higher intertidal zone andsupralittoral zone are intercepted by artificial
structure such as dike and break water.
Consequently decreasing area of tidal flatcaused the habitat decrease and increasing suspended mud by prevention of their depositingat the higher intertidal zone (Fig. 5). Dams andbarrages often store the sand at the water reservoirs. It sometimes causes not only the decrease of reservoir capacity but also coastal
erosion. Very fine sediment particles like silt
and clay do not easily settle even in calm water
as far as they are still in fresh water. In downstream region of dams and barrages, thus, finesediments allow to discharge higher ratio incomparison with sand particles.
Both USA and Japan have a peak of dam
construction around 1960 to exploit the energy
and water supply (see: www. wec. or. jp/ center/ shiryou/ image/ download/ B-24.pdf).
Japan still continued dam construction until
1990s mainly for water utilization despite USA
put the brake on it after 1960s. This may havea possibility to make sediments in sheltered37

bays muddy and to change sediment property
not suitable for originally inhabited bivalves.
Environmental Impact for filtration andrespiration
How does coastal changes affect filter feeding bivalves? As I described above, coastalchanges bring about the loss of habitat, depression of tidal current and accumulation of finesediments. Fig. 6 indicates that these factors
eventually affect the bivalves on both oxygen
deficiency and high suspended load. Hypoxia
and anoxia often occur in subtidal zone ofeutrophied sheltered coast under the stratified
layer in summer. Most of the bivalves can
switch to anaerobicbiosis to maintain theirlives and survive several days in anoxic condition (Hochachka, 1984; Nakamura et al., 1997).

Fig. 5. Conceptional illustrations of land formation
on upper level of tidal flat, and the impact of land
reclamation and construction of artificial structurearound high water level

38

Junya HIGANO

However, elongation of anaerobicbiosis requires consumption of reserve substances like
aspartic acid and glycogen. The accumulationof metabolites will indicate the limit to tolerate
anoxia (Hochachka, 1984). Hydrogen sulfide is
generated in anoxic layer of sediment and affects bivalves to inhibit aerobic respiration.
Bivalves can also survive in relatively high concentration of hydrogen sulfide, but bivalves
have to respond as same as under anoxia.
Combined effects of hypoxia and hydrogen sulfide may act as anoxia, thus oxygen deficiency
is extremely dangerous and should be noticed
its effect on bivalve physiology.
High concentration of suspended particle
suppresses the water clearance of the bivalves
and increases pseudofeces ejection (Bayne,1993). The increase of several tens mg/L of sus-pended mud mixed with food algae brings
down the clearance rate and ingestion rate offood algae (Bricelj & Malouf, 1984). Increase ofsuspended particles may cause the excess energy expenditure for pseudofeces ejection andowe deficit on energy budget. The bivalves
under the high turbidity should show low
growth rate. Highly concentrated muddy
water may clog the gill of bivalves and force toclose the valves. The bivalves have to wait until
the overlaying water replaced sufficiently clear
for resuming respiration. So, high concentration of turbid water presumably affects the bivalves in almost same manner as anoxia.
Conclusions and further studies
Environmental changes in tidal flat in recent

Fig. 6. Conceptual flow of coastal changes affecting to the depression of Manila clam resources

Influence of environmental changes in tidal flats for bivalves

years probably affect the depression of thestanding stock of filter feeding bivalves byhigh sediment load and oxygen deficiency.
Consequently, the decrease of bivalve stocks
may affect the surrounding environment. Oncethe ecological function of tidal flat has been degraded, it is very difficult to recover the proper
bivalve resources. Under this situation, thenatural recovery of ecosystem cannot be expected, and then the problem must be solved byhuman efforts. Quantitative assessments ofcauses and effects between environmental
changes and bivalve's depression are strongly
needed. Responses of the bivalves to single andcompound environmental factors have to beclarified associating with their reproductive cycles. We also need to find out the suitable species for bioremediation. For example, thephysiological and ecological evaluation of moretolerable species to turbid and anoxic condition
will help design the habitat disposition.
Availability of mechanical devices for improvement of water circulation and oxidation has tobe considered at the same time. For example,
the introduction of natural energy like windand solar power to these devices and estimationof their cost-benefit should be inquired.
Basically, efforts for eliminating negative factors and propagating the bivalve's stocks are
essential to maintain coastal ecosystems.
References
Akiyama A., 1985: Teisei seibutsu no kyodou to
shokumotsu rensa (behaviour of benthos
and food web). in "Choukantai shuuhen
kaiiki ni okeru joukakinou to seibutsuseisan ni kansuru kenkyuu (Studies on purification and production in intertidal sea
areas) report on 1984" (eds. by TokaiRegional Fisheries Research Institute andNansei Regional Fisheries ResearchInstitute) pp.99-104. (in Japanese)
Alpine A. E., and Cloern J. E., 1992: Trophic interactions and direct physical effects control
phytoplankton
biomass
andproduction in an estuary. Limnol.

39

Oceanogr., 37(5), 946-955.
Bayne B. L., 1993: Feeding physiology of bivalves: time-dependence and compensation
for changes in food availability, in "Bivalve
filter feeders in estuarine and coastal ecosystem processes" (ed. by Dame F. R.),
Springer-Verlag, Berlin Heiderberg, pp.124.
Bricelj V. M., and Malouf R. E., 1984: Influenceof algal and suspended sediment concentrations on the feeding physiology of the hardclam Mercenaria mercenaria. Mar. Biol.,84, 155-165.
Fujiwara M., 1986: Influence of temperature on
filtration rate of young cockle and ark
shell. Bull. Kyoto Ocea. Fish. Sci., 10, 19-24.
(in Japanese)
Hochachka P. W., 1984: Biochemistry of adaptation of hypoxia-strategy of theoraganisms to survive without oxygen,
Kouseishakouseikaku, Tokyo, 194pp.
Kawamoto N., 1967: Report on the cause ofmass mortality of Meretrix lusoria in the
coast of Chiba preferture, Nourin Toukei
Kyoukai, Tokyo (in Japanese)
Koike K., 1990: Artificial beach construction on
the shore of Tokyo Bay. Japan. Jour.
Coastal Res., SI No.6, 45-54.
Little C., 2000: The biology of soft shores andestuaries, Oxford University Press, New
York, 252 pp.
Ministry of Agriculture, Forestry and
Fisheries, Statistics and Survey Division,
1954-2001: Annual report of catch statistics
on fisheries and Aquaculture in 1953-2000,
Nourin Toukei Kyoukai, Tokyo
Nakamura M., Shinagawa A., Toda K., andShigeru N., 1997: Tolerance of 4 bivalvesfrom lake Shinji and Nakaumi to environmental factors. Suisanzoshoku, 45(2), 179185. (in Japanese)
Navarro E., and Iglesias J. I. P., 1993: Infaunalfilter-feeding bivalves and the physiological response to short-term fluctuations infood, in "Bivalve filter feeders in estuarine
and coastal ecosystem processes" (ed. by
Dame F. R.), Springer-Verlag, Berlin40

Junya HIGANOHeiderberg, pp.25-56.
Newell R. I. E., and B. L. Bayne., 1980: Seasonalchanges in the physiology, reproductive
condition and carbohydrate content of the
cockle Cardium (＝Cerastoderma) edule(Bivalvia: Cardiidae). Mar. Biol., 56, 11-19.
Sagara J., 1981: Ecology, and physiology of
Tapes (Ruditapes) philippinarum and
Meretrix lusoria. Aquabiology, 3(2), 102105. (in Japanese)

Satoh M. (Ed.), 2000: Life in Ariake Sea:
Biodiversity in tidal flats and estuaries,
Kaiyusha, Tokyo, 396pp. (in Japanese)
Yamamoto K., Tamura I., and Tochino M.,
1996: Effects of water temperature on filtration volume and ciliary movement ofgills in the Japanese ark shell, Scapharcabroughtonii. Journal of National Fisheries
University, 45(2), 95-101. (in Japanese)水研センター研報，別冊第 1 号，41−50, 平成16年
Bull. Fish. Res. Agen. Supplement No. 1, 41-50, 2004

The microbial loop and its contribution to bivalve aquaculture

41

The microbial loop in a eutrophic bay and its contribution
to bivalve aquaculture
Takashi KAMIYAMA*

Abstract Information on planktonic food webs around bivalve farms is important, because bivalves utilize natural suspended matter as food. Not only phytoplankton but
also other heterotrophic protists are occasionally essential to bivalves. Oysters cannot
use bacterioplankton, but they can ingest protists that feed on bacterioplankton, thus
using microbial energy indirectly through this microbial loop. To evaluate the importance of the microbial loop in planktonic food webs, occurrences of bacteria andheterotrophic protists were studied in the eutrophic Hiroshima Bay, where oyster
aquaculture is economically important. Temporal changes in microbial loop components
suggested that energy flow within the microbial loop was enhanced at the end of aphytoplankton bloom. The distribution of microbes and other protists implies thattransfer efficiencies within planktonic food webs including the microbial loop differedamong regions of the bay. Thus, the microbial loop may play an important role inplanktonic food webs in Hiroshima Bay. In some oyster ponds in France, the importanceof microbial energy flow to oyster production was actually evaluated. Possibly, energy
flow within the microbial loop is also important to oyster production in Japan.
Key words: microbial loop, bacteria, flagellate, ciliate, oyster

In various oceanic regions, significant energy flows from bacteria to higher trophic levels and return flows from such organisms todissolved organic matter pool, that is an original sense of the microbial loop (Azam et al.,1983), have been clarified (eg. Sieburth, 1984;
Pierce and Turner, 1992). In eutrophic bays,
where the bacterial biomass and production arevery high, possibly the bacterial production
strongly influences planktonic food webs,
which may enhance the productivity of higher
trophic levels (Sherr et al., 1986; Sherr andSherr, 1988; Fukami et al., 1999).
Hiroshima Bay is one of the eutrophic areasin the Seto Inland Sea of Japan. The northern,
inner region of the bay is strongly influenced
by riverine inputs and has a very low seawaterexchange rate with the outer region. Also, likechlorophyll- a concentrations, the biomass andproduction of bacteria are high in the Seto
Inland Sea (Yamaguchi et al., 1995; Imai andYamaguchi, 1996; Tada et al., 1998), implyingthat microbial food webs play important rolesin the ecosystem of the bay. There are manyrafts for aquaculture of oysters throughout
the whole bay and adjacent areas, and oyster
production in these areas constitutes 50-60 ％of the total Japanese production. To utilize theoyster productivity effectively and sustainably,
it is necessary to clarify the food web components and the energy flow between them, including the microbial loop system.
In the present study, firstly, the temporalchange of the microbial loop components in thecoarse of a phytoplankton bloom was elucidated. Secondly, the characteristics of the

2003年 6 月12日受理（Received on June 12, 2003）* Tohoku National Fisheries Research Institute, Fisheries Research Agency, Shinhama, Shiogama, Miyagi, 985-0001, Japan

42

Takashi KAMIYAMA

distributions of the main microbial loop components[bacteria,
heterotrophic
nanoflagellates (HNF) and ciliates] as well as theenvironmental conditions in Hiroshima Bay insummer were evaluated. Thirdly, the functionof the microbial loop to oyster production was
reviewed and then the importance of the energy
flow from ciliates to oyster was discussed.
Temporal changes in the microbial loop components in the coarse of a phytoplankton bloom
The investigation was conducted in a harbor(ca. 5-m water depth) in the northern part ofHiroshima Bay, the Seto Inland Sea of Japan(Fig. 1), to clarify the temporal changes in the
microbial loop components in the coarse of theharmful alga Heterosigma akashiwo. Seawater
sampling was carried out at surface and 1 m
above the bottom every one to four days in themornings from 6 June to 17 July in 1995.
Heterosigma akashiwo cells were counted in
fresh seawater from each depth. A seawatersubsample was fixed with Lugol's iodine solution (final concentration : 2 ％), and then concentrated by settling. Microzooplankton(zooplankton with body widths less than 200μm) of each subsample were counted in 1-2 mLof concentrated samples with a phase contrast
microscope using a Sedgwick-Rafter chamber.
Another seawater in each sample was fixed byglutaraldehyde (final concentration: 1 %), andfixed bacteria and HNF were stained withDAPI (Porter and Feig, 1980) and DAPI and
FITC (Sherr and Sherr, 1983a; 1983b), respectively, and then counted with epifluorescencemicroscopy.
Decay of tintinnid-ciliate population
A H. akashiwo bloom with a cell density ofover 104 cells mL−1 in the surface water occurred from 23 June to 1 July 1995 (Fig. 2). A
typical negative effect of the H. akashiwo
bloom on the microzooplankton community
was the decay of tintinnid ciliate population.
During the bloom period, the abundance oftintinnid ciliates in the surface layer markedly
decreased by one order of magnitude, comparedto the abundance before the bloom (Fig. 2). The
species diversity (Shannon-Wiener's H') of
tintinnids in the surface layer also decreased
during the bloom. Similar phenomena during
H. akashiwo blooms have been reported in previous studies (Verity and Stoecker, 1982;
Kamiyama, 1995).
Response of the microbial loop components

Fig. 1. Sampling station for investigating thechange in the microbial loop components in a harborin Hiroshima Bay, the Seto Inland Sea of JapanThe microbial loop components fluctuated in
response to the formation and decay of thebloom. Two abundance peaks of bacteria in surface water were recorded just after the beginning and just after the end of the bloom (Fig.
3). Also, the fluctuations in HNF abundancewere found to be tightly coupled with those ofbacterial abundance; there were two abundance
peaks detected after 1 - 3 days of the bacterial
abundance peaks. Although conspicuouschange of aloricate ciliates was not observed

The microbial loop and its contribution to bivalve aquaculture

during the process of bloom formation, theabundance increased drastically at the end of
the bloom, and temporarily became two orders
higher in magnitude than before the bloom.
These fluctuations of the microbial loop components reveals a drastic change in the foodweb system during the course of the H.
akashiwo bloom. In particular, it is clear thatthe decay of the bloom enhanced the flow of energy within the microbial loop from the bacteria through the HNF to the aloricate ciliates.
This process is interpreted as follows. The
decay of the H. akashiwo bloom probably
caused increase in dissolved organic matter(DOM) because of cell lysis of H. akashiwo.
Increased DOM possibly stimulated the production of heterotrophic bacteria (Cole et al., 1988).
Consequently, bacterivorous organisms such as

Fig. 2. Temporal changes in abundance ofHeterosigma akashiwo, and abundance and species
diversity of tintinnid ciliates during the course of
the bloom. Shaded areas indicate the bloom period(23 June to 1 July 1995) when the density of H.
akashiwo exceeded 104 cells mL−1

43

HNF and small aloricate ciliates increased in
response to the food supply. Partly, productionof aloricate ciliates may be also promoted by
the increase of HNF. It is interesting that it
took only a few days for the process from decayof the bloom to the increase of aloricate ciliates.
The microbial loop system probably responds
the change of the plankton community quickly.
Characteristics of the distributions of bacteria,
HNF and ciliates in Hiroshima Bay in summer
Investigation was performed in 4 - 6 layers in
the water column at 6 sites in Hiroshima Bay(Fig. 4) from a research vessel in summer, (1315 June and 20-22 August 1996, and 1 - 3 July1997). Environmental parameters were measured and analyzed (temperature, salinity, chlo-Fig. 3. Temporal changes in the abundance of microbial loop components of bacteria, heterotrophic
nanoflagellate (HNF) and aloricate ciliates during
the course of a Heterosigma akashiwo bloom.
Shaded areas indicate the bloom period (23 June to 1
July 1995) when the density of H. akashiwo exceeded
104 cells mL−1

44

Takashi KAMIYAMA

rophyll-aandnutrients).
Basedonunfractionated seawater (total faction) and theseawater filtered through a 20-μm mesh screen(＜20-μm fraction), the chlorophyll-a concentration in each fraction was measured with aTurner Designs fluorometer according toSuzuki and Ishimaru (1990). From another filtered seawater sample, the concentrations of
dissolved organic nitrogen (DIN) that consistsof NO2-N, NO3-N, NH4-N, and PO4-P and SiO2-Si
were determined using a TrAAcs 800
autoanalyzer (Bran-Luebbe Co.)
The main microbial loop components (bacteria, HNF and ciliates) were also investigated at
3 of the 6 sites: the inner (Stn. 1), central (Stn.
3) and outer (Stn. 5) regions of the bay (Fig. 4).
Abundances of them were generally measured
with the same method as the above.
Simultaneously the cell dimensions of eachtaxon for HNF and aloricate ciliates and thelorica dimension of each tintinnid-ciliate species were measured, and the cell volume of themwas calculated by approximating the shape ofeach taxon to a standard geometric configuration. Bacterial carbon biomass was estimatedbased on the average cell volume (0.098μm3
cell−1 ) from annual Hiroshima Bay data (Imaiand Yamaguchi, 1996) and an allometric conversion equation (29.6 f gC cell−1; Loferer-Krößbacher et al., 1998). The carbon biomass of HNF
and aloricate ciliates were estimated based on
the cell volume data and the carbon-volume
conversion factors for HNF (0.22 pgC cell−1; Børsheim and Bratbak, 1987) and for aloricate
ciliates (0.19 pgC μm−3 ; Putt and Stoecker,1989), and that of tintinnid ciliates were calculated based on the volume of the lorica according to Verity and Langdon (1984).

the surface layer at the innermost site (Stn. 1;
distribution of only DIN concentration shownin Fig. 5). However, high concentrations of DIN
in the surface layer were limited to the innermost site where chlorophyll-a concentrations
were high (Stn. 1, 2), suggesting that riverinenutrient inputs may rapidly be taken up byphytoplankton in the vicinity of the rivermouth areas in Hiroshima Bay. Generally,
higher concentrations of chlorophyll-a were recorded in the surface and near-surface layers in
the inner regions of the bay (Stn. 1 and 2; Fig.
6). The contribution of the ＜20-μm fraction tototal chlorophyll-a concentration mostly exceeded 60 ％ in June 1996 and in July 1997. In
August 1996, also more than 60 ％ of the contribution of the ＜20-μm fraction was recordedin the almost all layers at Stn. 1 and 2 althoughless than 40 ％ of the contribution was partly

20 'Environmental conditions
The strong influence of riverine inputs on theseawater environment in the inner region of
the bay was recognized by the low salinity inthe surface on all occasions. Similarly, in July
1997, the concentrations of nutrients (DIN,
PO4-P and SiO2-Si) were comparatively high in

Fig. 4. Study sites in Hiroshima Bay for investigating the distribution of the microbial loop components. Environmental conditions were surveyed at
all sites, while abundance and biomass of the microbial loop components (bacteria, heterotrophic
nanoflagellates and ciliates) were investigated atStn. 1, 3 and 5 only ( )The microbial loop and its contribution to bivalve aquaculture

observed in the central and outer regions of thebay.
This result
indicatesthatthephytoplankton assemblage is generally dominated by nano- and picoplankton in the inner
region of the bay in summer.
Abundance of the main microbial loop components
In the inner region of the bay, abundances ofthe main microbial loop components werehigher than in the other regions. Abundancesof bacteria and HNF ranged from 1.10 × 106
cells ml−1 to 5.75×106 cells ml−1 and from 0.52
×103 cells L−1 to 11.06×103 cells L−1 , respectively. The highest abundances of both organisms on each occasion were recorded in thesurface, 2-m or 5-m layers at Stn. 1 (Fig. 7). The
abundance of total ciliates ranged from 0.6×
102 ind. L−1 to 20.5 ×103 ind. L−1 during the45

study, and distributed abundantly in the surface and 2-m layers at Stn. 1 in all months.
Ciliate assemblages were generally dominatedby aloricate forms except for samples collectedin August 1996 at Stn. 1 and 5 (Fig. 8). In July
1997, the maximum abundance of ciliates, especially the tintinnid forms at Stn. 1, was considerably lower than in June and August 1996
(Fig. 8).
Transfer efficiency from primary producers totheir grazers
Among Stn. 1, 3 and 5 in the present study,
Stn. 1 was characterized by high chlorophyll-aconcentrations and high abundance of the microbial loop components. High biomass of primary producers may sustain the highproduction of the grazer plankton. Further, toevaluate the transfer efficiency of energy fromthe primary producers to their grazers, the relationships of the carbon biomass between eachciliate assemblage (tintinnid or aloricate ciliate)
and the prey organisms (bacteria, HNF, and＜20-μm chlorophyll-a) were analyzed, assuming that the carbon conversion factor of the＜20-μm chlorophyll-a was 30 (Riley, 1965;
Parsons, 1984). For this analysis, stable preypredator conditions are necessary but at Stn. 1
in July 1997, environmental conditions indicat-

Fig. 5. Horizontal and vertical distributions of salinity and dissolved inorganic nitrogen (DIN) concentration.

Fig. 6. Horizontal and vertical distributions of thechlorophyll-a concentration and the percentage ofthe chlorophyll-a concentration accounted for by the＜20-μm fraction

Fig. 7. Vertical distributions of the abundances ofbacteria and heterotrophic nanoflagellates (HNF) at
Stn. 1, 3 and 5 in Hiroshima Bay

46

Takashi KAMIYAMA

ing extremely low salinity from riverine inputs
imply that the stable prey-predator conditions
was not applicable for the ciliate assemblage.
Hence, data from Stn. 1 in July was not used
for the analysis.
Regardingtherelationships
betweenaloricates and the total prey organisms, thesignificant positive linear correlations (r2＝0.45- 0.73, p＜0.05) were observed at all sites (Fig.
9). The slope of the linear regression at Stn. 3
was significantly higher than those at Stn. 1
and 5 (p＜0.01). Further, the X-axis intercept at
Stn. 1 in Fig. 9 was significantly higher thanthose at Stn. 3 and 5 (p＜0.01), implying thatthe biomass of primary producers and microbes not utilized by aloricate ciliates washigher at Stn. 1 than at the other sites. These
interpretations demonstrate that the energy
transfer efficiency from primary production
and microbes to aloricate ciliates may be low in
the inner region of the bay (Stn. 1) compared tothe central region of the bay (Stn. 3).
To consider the energy transfer efficiency, it
is necessary to practically measure the primary
production and subsequent grazing impact, because information on biomass only represents
a scene of dynamic relationships between preyFig. 8. Vertical distributions of the abundance of ciliates at Stn. 1, 3 and 5 in Hiroshima Bay

and predator. In spite of such limitations,biomass relationships between prey and predators in this study were clear and characteristics
differed among areas in the bay, suggestingthat the biomass relationship may be one of thefactors to evaluate the efficiency of energy flowin planktonic food webs.
Contribution of the microbial loop to production of bivalve aquaculture
The size of prey that bivalves can feed upon
depends on the bivalve species. Some mussels
can retain the particles of bacterial size
(Kreeger and Newell, 1996) but oysters cannot
efficiently utilize the picoplankters (Langdon
and Newell, 1990). However, the oysters havethe ability to efficiently retain the particles
larger than 6μm (Palmer and Williams, 1980),
which included the size of bacterivorous
protists. Hence, it is a possibility that oysters
can utilize the picoplanktonic energy source byingesting bacterivorous protists. Le Gall et al.
(1997) proved this scenario. The cyanobacteria
Synechococcus sp. retaining specific yellow-gold
autofluorescence was supplied for the ciliate
Uronema sp. as food source. This protist that

Fig. 9. Relationships between the carbon biomass ofaloricate ciliates and all prey organisms that consistof bacteria, heterotrophic nanoflagellates (HNF) and＜20-μm fraction of chlorophyll-a. ○ (data at Stn. 1
in July 1996) was omitted from the calculation of theregression line

The microbial loop and its contribution to bivalve aquaculture

fed on Synechococcus was labeled by many
spots of the yellow-gold autofluorescence observed by epifluorescence microscopy underblue-light excitation. Then, the labeled
Uronema was supplied to oysters, large
amount of autofluorescent particles clumped
on residual membranes of labeled ciliates wasobserved in the stomach of oysters, although
few parcels could be found in the stomach ofoysters which were provided with only
Synechoccus suspension. The results suggestthat the ciliates play a role as a trophic
intermediation between picoplankton and oysters. This result is evidence that oysters can receive from not only phytoplankton energy
source but also from the microbial loop energy
flow.
Actually, the effects of oyster feeding on
protists and picoplankton were compared
under laboratory experiments (Dupuy et al.,2000b).
Whiletheabundanceofpicophytoplankton was constant under bothconditions with a filtering oyster and without
oyster, in the case of ciliates as prey, the abundance decreased under the conditions with a filtering oyster for the first 15 minutes (Fig. 10).
Also, the feeding activity of oysters was compared between food sources. The clearance rateof oysters on ciliates was in the same level asthat on diatoms as shown in Fig. 11 (Dupuy etal., 2000b). Furthermore, based on the feeding

47

activities of the oyster Crassostrea gigas on theciliates, the carbon specific feeding impacts ofoysters on ciliate assemblages in some oyster
ponds in France were estimated and comparedwith the impact on phytoplankton assemblages(Table 1). The results indicated that the ratio ofremoved carbon contents from ciliate assemblage to that from phytoplankton assemblage
ranged from 0.30 to 4.5, implying that importance of ciliates for oyster probably depends onthe environmental conditions and the food-web
systems in the oyster farming area. Ciliate
may not be always important food source foroysters, but there is a possibility that they play
an important role as a food source if the microbial loop activity was high and thephytoplankton biomass is insufficient for oyster food.
The role of the heterotrophic protists as foodsource for oysters has been pointed out in thesome ponds where the oyster was cultured on
the bottom (Dupuy et al., 1999; 2000a; 2000b). In
Japan, generally cultured oysters are suspended into the seawater from the specific rafts
or line to get higher production of oyster in aunit area. Hence, probably the oyster production more strongly depends on the planktonic
food webs in the oyster farming areas. In someareas in Japan, unknown death in summer, decreasing production in a unit area and damage
due to red tides have caused many problems forFig. 10. Change in abundances (mean±SD, n=3) of picophytoplankton and ciliates under the conditions with a filtering oyster (●) and without oyster (◇)(Modified from Dupuy et al., 2000b)

48

Takashi KAMIYAMA

Table 1. Feeding impact by Crassostrea gigas on ciliates and phytoplankton
Ciliates
Biomass Removed（Ａ）−1(μgC L ) (μgC h−1g−1)

Prey

Phytoplankton
Biomass Removed
（B）
−1
−1 −1
(μgC L ) (μgC h g )

Area

Prey

A/B

French Atlantic coastal
ponds*1

FA

63.5

126

CD

−

27.5

4.5

French Atlantic coastal
ponds*2FA

7-32

48-218FA

161-648641-2652

0.07-0.21

Mediterranean Thau
Lagoon*3

FA

3

38.6

FD

161.5

1307

0.03

* 1: Dupuy et al. 1999, * 2: Dupuy et al. 2000a, * 3: Dupuy et al. 2000b.
FA: field assemblage, FD: field diatoms, CD: cultured diatom (Phaedactylum tricornatum 1 ×106 cells L−1)

Thanks are also extended to Mr. Arima and
Ms. Tsujino, FEIS, and the captain and all thecrew of the R/V Shirafuji-Maru, for theirassistances of field investigation of Hiroshima
Bay.
References

Fig. 11. Standardized clearance rates (mean ± SD,n=3) of the oyster Crassostrea gigas on the various
taxonomic groups. Data taken from Dupuy et al.
(2000b)oyster aquaculture. One of the reasons is toohigh density of oyster in the farming area,
which probably exceeded the carrying capacity
for oyster cultivation suitable for the particular environmental conditions. To use the bivalve farming area efficiently and lastingly, it
is essential to estimate the carrying capacity
for oyster aquaculture. For that, it is necessary
to quantitatively clarify the food-web system(biomass of each planktonic group, its production and the trophic interaction) and to monitor environmental characteristics in oyster
farming area as well.
Acknowledgements
The author thanks Drs. Itakura andNagasaki, National Research Insitutute ofFisheries and Environment of Inland Sea(FEIS), for their cooperation during the field
investigation for the H. akashiwo bloom.

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49planktonic ciliates in marine food webs.
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irradians and the oyster Crassostrea
virginica. Ophelia, 19, 163-174.
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DAPI for identifying and counting aquatic
microflora. Limnol. Oceanogr., 25, 943-948.
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for marine "oligotrichous" ciliates fromestuarine and coastal waters. Limnol.
Oceanogr., 34, 1097-1103.
Riley GA., 1965: A mathematical model of regional variations in plankton. Limnol.
Oceanogr. Suppl., 10, R202-215.
Sherr B. and Sherr E., 1983a: Enumeration ofheterotrophic
microprotozoa
byepifluorescence microscopy. Estuar. Coast.
Shelf. Sci., 16, 1-7.
Sherr B. F. and Sherr E. B., 1988: Role of microbes in pelagic food webs: a revised concept. Limnol. Oceanogr., 33, 1225-1227.
Sherr E. B. and Sherr B. F., 1983b: Doublestaining epifluorescence technique to assess frequency of dividing cells andbacterivory in natural populations ofheterotrophic
microprotozoa.
Appl.
Environ. Microbiol., 46, 1388-1393.
Sherr E. B., Sherr B. F., and Paffenhöfer G.A.,
1986: Phagotrophic protozoa as food formetazoans: a "missing" trophic link in marine pelagic food webs? Mar. Microb. FoodWebs, 1, 61-80.
Sieburth J. McN., 1984: Protozoan bacterivory
in pelagic marine waters, in "Heterotrophic
activity in the sea" (ed. by Hobbie, J. E. andWilliams, P. J. LeB.), Plenum Press, New
York., pp. 405-444.
Suzuki R. and Ishimaru T., 1990: An improved
method forthedetermination ofphytoplankton chlorophyll using N, Ndimethylformamide. J. Oceanogr. Soc.
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Tada K., Monaka K., Morishita M., and50

Takashi KAMIYAMA

Hashimoto T., 1998: Standing stocks andproduction rates of phytoplankton andabundance of bacteria in the Seto InlandSea, Japan. J. Oceanogr., 54, 285-295.
Verity P. G. and Langdon C., 1984:
Relationships between lorica volume, carbon, nitrogen, and ATP content oftintinnids in Narragansett Bay. J.
Plankton Res., 6, 859-868.

Verity P. G. and Stoecker D., 1982: Effects ofOlisthodiscus luteus on the growth andabundance of tintinnids. Mar. Biol., 72, 7987.
Yamaguchi M., Imai I., and Matsuo Y., 1995:
Seasonal changes in biomass and photosynthetic rate of phytoplankton in
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水研センター研報，別冊第 1 号，51−58, 平成16年
Bull. Fish. Res. Agen. Supplement No. 1, 51-58, 2004

51

Balancing marine aquaculture inputs and extraction:
Combined culture of finfish and bivalve molluscs in the open ocean
Richard LANGAN*

Abstract Enrichment of the water column with dissolved nutrients and of bottom sediments with organic matter as a result of culturing finfish in sea cages have been identified as real and potential environmental impacts of fish culture. While severe impacts
have been documented in shallow, poorly flushed waters, proper siting of sea cage operations generally results in only minor localized impacts to the benthic community on thesea floor directly beneath the cages. None the less, the perception of environmentalgroups and regulatory agencies in the U.S.A. that fish waste and uneaten feed will impact the marine environment regardless of siting has affected the expansion of existingsites and the establishment of new sites. In order for the industry to expand to meet thegrowing demand for seafood, measures to mitigate these impacts must be taken. One
possible solution is to balance inputs of feed with extraction of biomass of organisms
such as marine plants and bivalve molluscs that do not require external feed application.
In 1999, the University of New Hampshire established the Open Ocean Aquaculture
Demonstration Project. Funded by the National Oceanic and Atmospheric
Administration, the project was designed to provide a commercial scale demonstration
and research site for open ocean aquaculture in the northeast U.S.A. The project is an integrated, multi-disciplinary, regional effort that includes biology, oceanography, engineering, sociology, economics, technology transfer, and education. While thedevelopment of technologies for finfish and shellfish production in offshore environments is central to the mission of the project, demonstration of the environmental
sustainability of open sea culture is critical to the social acceptance of industry development.
Since 1999, the project has produced harvests of several species of finfish using submersible sea cages and six crops of molluscan shellfish (primarily blue mussels) using
submerged longlines in close proximity to the sea cages. While not considered true
polyculture, the harvest of the filter feeding bivalve molluscs represents a net removal of
nitrogen, carbon and phosphorus that can be used in mass balance to offset the additionof these nutrients from finfish feeding. In this paper, data the potential for balancing inputs associated with feed application and fish wastes with extraction of fish and bivalve
biomass will be examined.
Key words: bivalve mollusc culture, finfish culture, sea cages, waste feed, nitrogen

2003年 6 月12日受理（Received on June 12, 2003）* 1 Cooperative Institute for New England Mariculture and Fisheries, University of New Hampshire, Environmental Technology Building,
35 Colovos Road, Durham, NH 03824, USA, Email: rlangan@cisunix.unh.edu

52Richard LANGANAs the world's human population continues
to grow, the demand for food, and especially
protein, increases correspondingly. The protein
derived from seafood accounts for 13 ％ to 16 ％of the human diet worldwide. In other words,
in order for high quality protein production tokeep pace with population growth, seafood production must increase. Addressing this shortage of seafood requires more production fromeither capture fisheries or aquaculture. By
most accounts production from capture fisheries is unlikely to increase from the current levels (FAO, 1998), therefore aquaculture will
become an increasingly important source of
seafood production.
Marine aquaculture systems are quite diverse, ranging from highly controlled landbased systems that recycle water and remove
and treat wastes to open water cages that release wastes directly to the environment.
Species produced in the marine environment
are also very diverse, and include seaweeds, bivalve molluscs, echinoderms, crustaceans, andfinfish. As with all concentrated food production systems, aquaculture can potentially havenegative impacts on the environment, however,the severity of impacts depends on the culture
system employed, the location, the species
under cultivation, and husbandry practices. In
the marine environment, negative impacts havebeen attributed to all forms of aquaculture,
though finfish aquaculture has been the primary target of most of the critics of theaquaculture industry (Goldberg and Tripplett,1997). One of the negative effects attributed to
finfish culture is enrichment of the water column with dissolved nutrients, resulting fromthe decomposition of uneaten feed, and frommetabolic wastes produced by the fish (Fig. 1).
While the amount of dissolved nitrogen discharged from fish farms may be locally significant and could potentially impact poorly
flushed shallow embayments by increasing
phytoplankton production, the volume of thedischarge relative to other human sources ofnitrogen to coastal waters is negligible (McVey
et al., 2002). In well flushed areas, it is unlikely

thatnitrogenadditionfromfinfishaquaculture would have any impact on trophic
conditions of the receiving waters (Sowles andChurchill, 2002). None the less, the perceptionof environmental groups and regulatory agencies in the U.S.A. that fish waste and uneaten
feed will impact the marine environment regardless of siting has affected the expansion ofexisting sites and the establishment of newsites. In order for the industry to expand tomeet the growing demand for seafood, measures must be taken to address these environmental concerns.
The salmon industry worldwide has greatly
reduced nitrogen discharge by developing better feed formulations, reducing the amount"fines" or small feed particles by improved feed
handling and delivery methods, and by monitoring the feeding behavior of the fish withvideo systems and ceasing feed delivery when
the fish stop feeding (Sowles and Churchill,2002). Another possible solution is to balance
inputs associated with fish feeding with extraction of biomass of organisms such as marine
plants and bivalve molluscs that do not require
external feed application. This approach has
been referred to as integrated aquaculture andis attracting increasing attention as a way tomitigate the real and perceived impact of
finfish culture (McVey et al., 2002； Chopin etal., 2002).
The concept and conduct of polyculture or integrated aquaculture is not new, and has beenFig. 1. Pathway of nitrogen wastes generated by theaddition of fish feed in open water systems

Balancing Marine Aquaculture Inputs and Extraction

practiced for centuries in Asian countries(Chopin et. al. 2002). While the rationale forconsidering integrated aquaculture today concerns mitigation of nitrogen additions from fed
aquaculture, the result is similar, in that one
species benefits from the waste products of another. With dissolved nitrogenous wastes,
plants such as seaweeds benefit with enhanced
growth from the increase in essential nutrients. Harvesting plant biomass for food or for
pharmaceutical or industrial extracts constitutes mitigation of the nitrogen added throughfeed addition. Bivalve molluscs can also incorporate the waste nitrogen, however the pathway is indirect, relying on an increase inphytoplankton production resulting from thenitrogen additions (Yarish et al., 2002).
Integrating seaweed or bivalve culture with
finfish culture provides a mechanism for removing some of the added nitrogen resulting
from feed introduction through harvest. The
pathway of waste nitrogen in integrated systems is illustrated in Fig. 2.
The effectiveness of extractive aquaculture
species in mitigating nitrogenous wastes produced by finfish culture has been demonstrated
for closed-system, intensive land based culture(Shpigel et. al., 1993). Obtaining accurate,quantitative mass balances for waste addition
and removal are much more difficult in open
water systems since hydrographic conditions,natural and analytical variability, and seasonalchanges in fish physiology make it difficult toisolate changes in water quality due toaquaculture. A more simplistic a approach
would be to calculate the amount of nitrogen
discharged to system from finfish operations,and the amount of nitrogen extracted by plants
or bivalves in harvested biomass. In 1999, theUniversity of New Hampshire established a 30acre aquaculture demonstration site 8 km fromshore in the open waters of the Gulf of Maine(Fig. 3). The site located in 52 m of water and isfully exposed to wind and tides from all directions. Wave heights can reach 9 m in severe
storms.
Aquaculture installations at the site include

53

Fig. 2. Pathway of nitrogen wastes in integrated
aquaculture systems

Fig. 3. Map of the New Hampshire and SouthernMaine coast showing the location of the open ocean
aquaculture demonstration site. The rectangle represents the area in which the fish cages are mooredand the adjacent line represents the longlines used
for bivalve mollusc culture.

two submersible fish cages and two submerged
longlines for bivalve mollusc culture. While theproject was not intentionally established todemonstrate integrated aquaculture, the presence of finfish and bivalve molluscs provided an
opportunity to investigate the capacity of themolluscs to mitigate nitrogen wastes resulting
from finfish production.
Materials and Methods
Fish and shellfish were cultured in adjacentinstallations consisting of two submerged sea

54Richard LANGAN

cages and two submerged longlines. The sea
cages were Ocean Spar Technologies, Inc, 600
m3 Sea Stations, one of which was modified for
flatfish culture (Fig. 4). The sea cages occupy arectangular area of seafloor 24 acres in size,with the length of the rectangle oriented northto south (Fig. 3). The shellfish longlines are located approximately 200 m to the east of thesea cages, and together are 360 m in length. In
the current operations, the cages are stockedwith 1,500 Atlantic halibut (Hippoglossoides
platessoides)
and
4,000
haddock(Melanogrammus aeglifinis) respectively. A
proposed expansion of finfish production includes the addition of a third larger cage (3,000m3 ) in 2003 that will be stocked with 37,500
Atlantic cod (Gadus morhua). The increased
production plan also includes increasing thestocking density of the smaller cages to 25 kg/
m3, which would bring the numbers of halibut
and haddock up to 3,750 and 7,500 respectively.
The growout perid for halibut from a 100 gm
stocking size to 4 kg is 36 months. Under current stocking density, this would result in total
production at harvest of 6,000 kg for the cage.
Haddock are grown to 2 kg each in 24 months,
yielding a harvest of 8,000 kg.
The amount of nitrogen discharged from
finfish operations has been estimated in a number of studies, and most of these have focusedon salmon production. The vast majority (87％) of discharged nitrogen is in the dissolved inorganic form consisting of ammonium (80 ％)and nitrate-nitrite (20 ％) (Sowles andChurchill, 2002). The estimates range from alow of 30 kg annually per ton of fish, to a highof 78 kg (Sowles and Churchill, 2002). The
higher figures were calculated in the early
1990's (Enell and Ackfors, 1991) and the lower
discharge estimates in subsequent studies
likely reflect improved efficiencies in feed formulation and husbandry practices (Sowles andChurchill, 2002). For this study, an annual
value of 50 kg N per ton of fish was used.
The amount of nitrogen removed annually
via bivalve harvest was calculated by multiplying the total annual production in meat weighttimes the percent nitrogen of mussel flesh. At
full capacity, each longline can yield 6,000 kg
live weight of mussels in a 12 month growout
period, resulting in annual production of 12,000
kg whole live weight. Meat yields of mussels
cultured at the site have ranged seasonallyfrom 42 ％ to 60 ％ with an average of 50 ％throughout the year. Estimates of nitrogencontent of bivalve flesh range from 1.3 ％ to 1.8％ (Rice, 2001). A figure of 1.6 ％ was used inthis study.
Since the growout period for halibut is three
years, a three-year cycle was used in calculating discharge and extraction. Fish weights andtotal tonnage from each cage per year was
based on observed growth rates for this project(Howell, unpublished data). For halibut, average individual weights of 0.5 kg, 2 kg, and 4 kg
were used for years 1, 2 and 3 respectively. For
haddock, average annual weights of 0.5 kg and
2 kg were used for years 1 and 2. Year 1 of asecond haddock growout cycle was used to calculate the total production weight for year 3.
No mortality for either halibut or haddock was
assumed in calculating nitrogen discharge.
Total weight of mussel meat (and nitrogen removed) was based on observed production andmeat yield data from this project (Langan,2001). Meat yields range throughout the annual growout cycle from a low of 42 ％ to ahigh of 60 ％. An average meat yield of 50 ％was applied to the annual production of 12,000

Fig. 4. A schematic of the 600 m3 OST Sea Station
cages used for finfish growout. The cage in this diagram was modified for flatfish culture.

55

Balancing Marine Aquaculture Inputs and Extraction

kg whole live weight. Discharge and extraction
for the current fish and mussel production (described above) and for the proposed finfish expansion were calculated.

three-year period, production of 6,000 kg of
halibut resulted in a discharge of 488 kg of nitrogen. Haddock production, which was estimated at an 8,000 kg harvest in year 2, followed
by a restocking with 4,000 juvenile fish in year
3, resulted in an estimated discharge of 600 kg
of nitrogen, bringing the three year total forboth species to 1,088 kg of nitrogen.
Nitrogen extraction via mussel harvest as-

Results
Total estimated nitrogen discharge for thetwo sea cages is presented in Table 1. For the

Table 1. Calculation of total nitrogen discharge for a three year period for two
cages. Wt/fish＝the average weight of individual fish at the end of the production
year, Biomass＝total biomass in the cage at the end of the production year
Species
Halibut

Halibut total
Haddock

Year
1
2
3

No.
1500
1500
1500

wt/fish
0.5kg
2.0kg
4.0kg

Biomass
750kg
3,000kg
6,000kg

N/ton
50kg
50kg
50kg

1
2
3

4000
4000
4000

0.5kg
2.0kg
0.5kg

2,000kg
8,000kg
2,000kg

50kg
50kg
50kg

Haddock total
Two cage total nitrogen discharge

N dis
38kg
150kg
300kg
488kg
100kg
400kg
100kg
600kg
1,088kg

Table 2. Calculation of the amount of nitrogen extracted via mussel harvest over athree-year period. Total wt＝total live weight of mussels and shell, MY＝meat
yield, MW＝meat weight
Year
1
2
3

Total wt
12,000kg
12,000kg
12,000kg

MY
50%
50%
50%

MW
6,000kg
6,000kg
6,000kg

%N
1.6
1.6
1.6

Total nitrogen extracted

kg N
96kg
96kg
96kg
288kg

Table 3. Calculation of total nitrogen discharge for a three year period from threefully stocked cages
Species
Halibut

Year No.
1
2
3

wt/fish
3750
3750
3750

biomass
0.5kg
2.0kg
4.0kg

N/ton
1,875kg
7,500kg
15.000kg

N dis
50kg
50kg
50kg

1
2
3

7500
7500
7500

0.5kg
2.0kg
0.5kg

3,750kg
15,000kg
3,750kg

50kg
50kg
50kg

1
2
3

37500
37500
37500

0.5kg
2.0kg
0.5kg

18,750kg
75,000kg
18,750kg

50kg
50kg
50kg

Halibut total
Haddock

Haddock total
Cod

Cod total
Three cage total nitrogen discharge

94kg
375kg
750kg
1,219kg
188kg
750kg
188kg
1,126kg
938kg
3,750kg
938kg
5,626kg
7,971kg

56

Richard LANGAN

sumed three complete growout cycles at the fullproduction capacity of 12,000 kg/year. These
calculations are presented in Table 2. For thecurrent operations at the site, which consists oflow stocking densities for the two cages, total
nitrogen discharge exceeds nitrogen extraction
via mussel harvest by 800 kg over a three-year
period. Therefore, in order to remove all the nitrogen discharged from finfish production,mussel production would have to be increased
by a factor of 2.7, or to 32,400 kg/year.
Increasing production to this level would require the installation of six additional
longlines.
Similar calculations for nitrogen discharge
were applied to the proposed expansion of
finfish production and are presented in Table 3.
The expansion includes fully stocking the 600
m3 Sea Station cages to a 25 kg/m3 density withhaddock and halibut, and the addition of a
3,000 m3 cage with Atlantic cod at the same
stocking density. Cod have a two-year growout
cycle and annual biomass for year 3 wastreated similarly to haddock production in theprevious example.
If three cages are fully stocked for growout,
the total nitrogen discharged to the environment over a three-year period would be 7,971
kg, or 2,657 kg per year. Based on the calculations presented in Table 2,125 kg of mussels(live weight) need to be harvested to extract 1
kg of nitrogen. Therefore, if a goal for the proposed expansion of finfish production was no
net addition of nitrogen, 332,125kg of mussels
would need to harvested each year to extract all
the nitrogen added by finfish culture.
Discussion
Based on the results of presented here, balancing the total nitrogen discharge from
finfish culture operations by integrating extractive species such as bivalves would require
the scale of operations for the extractive species
to be far larger than the finfish operations.
Certainly from an industry perspective, thiswouldcreateoperational
management

complexity as well as a significant challenge
for marketing the large volume of extractive
product. The exercise of making these calculations was undertaken to investigate the capacity for mitigating nitrogen addition by
culturing an extractive species such as mussels,
and is by no means to be construed as advocacy
for no net addition of nitrogen for all culture
operations. The location of the culture site, thetrophic condition and assimilative capacity of
the receiving waters, and marketing landscapemust all be taken into consideration in order todetermine the most effective approach to integrated aquaculture. In locations such as theGulf of Maine where this project is being conducted, the coastal waters are naturally high innitrogen due to upwelling of deep nutrient richwaters. It is highly unlikely that operations inoffshore environments with high ambient nitrogen concentrations and large dilution capacity would be impacted by discharge from
finfish culture. Sowles and Churchill (2002) investigated the potential exposure and effect ofnutrient enrichment by salmon culture in
Cobscook Bay, Maine, U.S.A. They found that
despite the significant loading associated withannual production of 6,000,000 kg of salmon,
there was little change in water column nitrogen concentration and no discernable increasein primary production. Similarly, Wildish etal. (1992) reported difficulty measuring differences in nitrogen concentration from ambientconditions beyond a few meters from the cages
in an intensely farmed area of the Bay of
Fundy. Whether or not nitrogen plumes above
ambient conditions can be measured should not
be the only criteria for determining whether
finfish operations should be permitted, or mitigation by extractive species should be required.
Determining the assimilative capacity and nutrient sensitivity of the surrounding waters isextremely important (Chopin et al., 2001). In
some cases, an increase in nutrient loading may
result in beneficial increases in secondary production without any associated negative impacts. Nixon and Buckley (2002) examined
nutrient loading in relation to fisheries growthBalancing Marine Aquaculture Inputs and Extraction

and biomass data from the Baltic Sea. They
found that fish growth and biomass were significantly greater with increased nitrogenloading in the latter throughout the 20th century. Concerns over nutrient additions tocoastal waters are in many cases valid, however, it should be recognized that nutrients are
essential for producing biomass, and may potentially result in greater fisheries yields.
Certainly, if aquaculture operations are to besited in waters that are already eutrophic or
have been scientifically determined to be nitrogen sensitive, they should be of the extractive
type or at minimum strive to balance inputs
with removal.
As illustrated by the exercise undertaken inthis study, if no net increase in nitrogen is agoal for aquaculture development, it would be
difficult to achieve without shifting the emphasis from finfish to extractive species such as bivalves and seaweeds, or by vastly reducing
discharge by improving feed formulations andnitrogen assimilation by the fish. Nutrient issues aside, there may be other reasons for amore integrated approach to aquaculture development. Among these are to counter the negative perception of aquaculture by theenvironmental and regulatory communities, toincrease profit margins with revenue from secondary crops and to reduce the financial risk ofrelying on a single species.
Acknowledgements
The research presented in this paper was
made possible by a grant from the U.S.
Department of Commerce, National Oceanicand Atmospheric Administration to the
University of New Hampshire's Cooperative
Institute for New England Mariculture andFisheries (CINEMAR).
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58

Richard LANGAN

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水研センター研報，別冊第 1 号，65−69, 平成16年
Bull. Fish. Res. Agen. Supplement No. 1, 65-69, 2004

Carrying capacity in an aquaculture ground of seaweed and shellfish

65

Environmental carrying capacity in an aquaculture ground ofseaweeds and shellfish in Sanriku coast
Ken FURUYA*

Abstract In non-feeding aquaculture of seaweeds and shellfish the culture organisms
compete with natural populations for resources, viz. nutrient salts and food particles.
Therefore evaluation of carrying capacity of coastal waters is crucial for sustainable exploitation of biological productivity. For this two major criteria are proposed: accurate
estimation of phytoplankton primary production which governs the magnitude of total
biological productivity, and understanding of oxygen dynamics based on a preliminary
study in a bay on the northeastern coast of Japan.
Key words: carrying capacity, shellfish culture, seaweed culture, Sanriku coastNon-feeding aquaculture of seaweeds andshellfish recovers nutrient loadings from theland. Since there is no other industrial way ofrecovery, this function is very important incontrolling nutrient cycling between land andcoastal waters. The amount of the recovery byshort-neck clam fisheries is estimated to beabout a sixth of the total input of nitrate in
Hamana Bay in central Japan (A. Hino, personal communication). Knowledge of material
cycling in the natural ecosystem is prerequisite
to utilize coastal productivity in a sustainable
manner, as the cultured organisms are dependent on the natural ecosystem. Nutrients, thekey factor that fuels primary production, aresupplied by advection, riverine input and regeneration, and utilized by phytoplankton andmacroalgae competitively. Then, organic matter produced by phytoplankton, naturally occurring and cultured macroalgae is consumed
not only by zooplankton and benthic organisms, but also by cultured scallops and oysters.
Thus it is important to quantify the production
at different trophic levels for evaluation of thecarrying capacity of coastal waters.
Tatara (1992) partitioned the distribution oforganic matter produced by primary producers
to heterotrophs and traced a grazing foodchain. In this work, several factors were considered that determine the carrying capacity ofcoastal waters for fisheries production. One of
the major hurdles recognized was the poor
availability of biological data. In coastal areas,
primary production of phytoplankton markedly fluctuates in the time scales of hours toweeks. Although the bottle incubation technique has been traditional and standard in themeasurement of primary production, its
spatio-temporal coverage is strictly limiting.
A study on material cycling in an
aquaculture ground for seaweeds and shellfish
is in progress in Otsuchi Bay. The bay locatedat 39°20'N, 141°56'E is 8 km long and 2 km
wide, and opens into the western North Pacific
Ocean. Owing to the freshwater flow into theinnermost part, and the long and narrow topography of the bay, exchange of water in thebay is expected to be brought about as, a seaward outflow of the surface water overlandward-moving inflow of denser, more saline
subsurface water from outside the bay(Shikama, 1990). This circulation occurs fre-

2003年 6 月12日受理（Received on June 12, 2003）* Graduate School of Agricultural and Life Sciences, The University of Tokyo Bunkyo, Tokyo 113-8657, Japan

66

Ken FURUYA

quently during winter and spring when thewesterly seasonal wind prevails. Conversely, an
inflow of surface water over outflow of deeper
water is also observed during the summer. This
circulation pattern may alter from the former
to the latter, and vice versa in summer, depending on the difference in water density between
inside and outside the bay. The formation ofspring bloom depends on the wind-driven circulation. The outward flow of the surface waterinterrupts formation of the spring bloom, andtransports phytoplankton population seaward(Fig. 1, Furuya et al., 1993). By such water
movements, a significant amount of nutrientsin the bay is brought out, or replenished into
the bay in the subsurface layer, depending onwater masses located outside the bay.
Therefore, the water movement governs in- andoutward flux of materials in the bay. Owing tothis physical condition, high temporal resolution of observation is of particular importancein the study of material cycling in the bay.
Preliminary results of the study are summarized in Furuya (2004) and briefly outlined here.
Primary production and dissolved oxygen on
the bottom
A bio-optical approach was used for rapid
monitoring of chlorophyll a and primary production with high temporal resolution. The

Fig. 1. Chlorophyll a at a station in Otsuchi Bay
during the spring of 1990 (Furuya et al., 1993)

natural fluorescence technique (Chamberlinand Marra, 1992) was improved for use incoastal waters (Yoshikawa and Furuya, inpress) and applied for estimating chlorophyll aand phytoplankton primary production in thebay. Both calculated chlorophyll a and primary
productivity from natural fluorescence showedsignificant correlations with the directly measured values during four seasons.
The integrated primary production throughout the water column was estimated from dataobtained by a moored fluorometer, and extrapolated to the production of the whole bay.
The primary production of the entire bay wasestimated to be 1.7×103 ton C during a period
from mid January to late April.
The cultured kelp Undaria. pinnatifida (locally called wakame) showed steady growth
until March, while growth was much reducedin April (Yoshikawa et al., 2001). Maximum
biomass of 840 ton in wet weight (28.3 ton C,
and 2.54 ton N) was recorded in early March,just prior to the harvest, and these figures decreased as the harvest continued. During Aprila major portion of the primary production was
lost by removal of aged part of the thallus.
Production of cultured U. pinnatifida throughout Otsuchi Bay increased steadily in January
and February, and reaching maximums of 1055
kg C d−1 and 99.0 kg N d−1 in March. Erosion of
the alga began in early March, and peaked at a
rate of 469 kg C d−1 and 43.1 kg N d−1 in mid
March. Erosion declined gradually as harvesting continued, and was comparable to production rates during the month of April.
The biomass harvested was 38.7 ton C (81 ％of total) while that lost due to erosion was 10.8
ton C corresponding to 19 ％ of the total
biomass produced.
Phytoplankton primary production consistently exceeded that of U. pinnatifida by morethan 20 times and was 38 times higher on average (Fig. 2). Variations in phytoplankton primary production was ascribed primarily to thechange in phytoplankton biomass, which waslargely controlled by water circulation (Furuya
et al., 1993).

Carrying capacity in an aquaculture ground of seaweed and shellfish

Fig. 2. Primary production of phytoplankton as
measured by natural fluorescence and that ofwakame (Furuya, 2003)

Organic matter loadings and dissolved oxygen concentration in bottom waters were examined near the shellfish culture areas underculture rafts of a scallop Patinopecten
yessoensis and the Japanese oyster Crassostrea
gigas. Sinking flux of organic matter, mainlycomposed of fecal matter was significantly
higher under the culture rafts of the oyster
than under those of the scallop. The flux under
the oyster rafts was 21.6 mg C m−2 d−1 on average in spring and summer, while that under thescallop rafts was 7.75 mg C m−2 d−1 . The mean
flux outside the raft area as control was 5.75
mg C m−2 d−1. Oxygen consumption rate of bottom seawater taken under the scallop rafts asdetermined by dark bottle incubation ranged
from 0.26 to 3.07 mg L−1 d−1 with a mean of 1.49
mg L−1 d−1 . The mean in vitro rate implied
rapid depletion of dissolved oxygen near thebottom in 5 days. However, in situ dissolved
oxygen was never exhausted in summer varying between 4.34 and 7.19 mg L−1 d−1 . In situ
continuous monitoring showed steady but slow
decrease in dissolved oxygen during the summer at a mean rate of 0.041 mg L−1 d−1. This apparent rate indicates that it should have taken
160 days to produce anoxic water. These observations show continuous supply of dissolved
oxygen through water flow along the bottom
is large and maintain the favorable oxygenfield near the bottom in summer. Wind-induced
circulation, density current and, in particular,

67internal tide are responsible for the inflow of
the outside water along the bottom (H. Otobe,
in preparation).
In Sanriku coast there is an array of bays
with similar topography to that of Otsuchi
Bay. Therefore, an active inflow of subsurface
water can be expected from outside which prevents depletion of dissolved oxygen. On thecontrary, anoxic water mass is formed near thebottom of Ofunato Bay which located in thesouthern part of the Sanriku coast. There is asill in the mouth part of the bay that reduces
water exchange considerably, being responsible
the formation of anoxic water together with
the intensive culture of the Japanese oyster.
With comparison of the water circulation andassociated oxygen field near the bottom sediment between Otsuchi Bay and Ofunato Bay, it
is clear that dissolved oxygen is important forsustainable exploitation of biological productivity in aquaculture areas. Other bays on the
Sanriku coast, water exchange is likely active
according to bottom topography. Therefore,
the Sanriku area is in general suitable foraquacultures in a point of view of oxygen supply.
Shellfish culture
Cultures of scallop and oyster occupy morethan 95 ％ of total annual production of shellfish in Japan (Fig. 3). The annual production
has been rather constant over recent ten years.

Fig. 3. Annual production of shellfish culture in
Japan (Ministry of Agriculture, Forestry and
Fisheries Japan, 2001)

68

Ken FURUYA

Almost all of the production is consumed as
foods for human with a small portion for pet
foods. Among the major reasons for the constant production over years, saturation of market and maturation of culturing technique areconsidered to be most responsible (H. Kurokura, personal communication). Considering
the significance of shellfish culture as recovering means of nutrient loadings, utilization of
unexploited potentials of shellfish culture
should be challenged intensively. For development of the market, one possibility is use ofshellfish as materials of forage production.
Since there is increasing demand of foods of
livestock and fish culture in Japan, selfsupport ratio of food is under the influence inJapan. Potential importance of shellfish as protein source may be acknowledged by selectionof suitable species for culture, and technical development of food processing for forage production. Nevertheless, there should be various
uncertainties how compatible a new species is
introduced with current culture of scallop andoyster. Therefore, optimized utilization of biological production is emphasized for the introduction of new species as well as sustainable
development of scallop and oyster culture.
Conclusion
The observation during the study serves development of numerical physical-biological coupled models (Kawamiya et al., 1995; Kishi et al.,
2003; Kishi et al., in prep.). Kishi et al. (2003) incorporates the aquaculture of both wakame
and shellfish into the model. The continuous
monitoring of flow field, chlorophyll a, primary production and dissolved oxygen withhigh temporal resolution serve robust validation of the model performance and improvement of the model. Evaluation of carrying
capacity of the bay is in progress using themodel to understand the importance ofphytoplankton primary production and dissolved oxygen and to identify other key factors. The model is intensively used to optimize
aquaculture production of seaweeds andshellfish with least environmental impacts inthe bay.
Acknowledgements
I thank M. J. Kishi, H. Otobe, T. Yoshikawa,M. Takagi, S. Kaga and K. Sekiguchi for theircooperation throughout the study.
References
Chamberlin S. and Marra J., 1992: Estimationof photosynthetic rate from measurementsof natural fluorescence: analysis of the effects of light and temperature. Deep-Sea
Research, 39, 1695-1706.
Furuya K., 2003： Environmental carrying capacity in an aquaculture ground of seaweed and shellfish in northern Japan. in"Determining Environmental Carrying
Capacity of Coastal and Marine Areas:
Progress, Constraints and Future Options"(ed. H. Yu and N. Bermas), PEMSEAWorkshop Proceedings 11, 52-59.
Furuya K., Takahashi K. and Iizumi H., 1993:
Wind-dependent
formationofphytoplankton spring bloom in Otsuchi
Bay, a ria in Sanriku, Japan. Journal of
Oceanography, 49, 459-475.
Kawamiya M., Kishi M. J., Ahmed M. D., and
Sugimoto T., 1995: Causes and consequences of spring phytoplankton blooms in
Otsuchi Bay, Japan. Continental Shelf
Research, 16, 1688-1695.
Kishi M.J., Higashi N., Takagi M., Sekiguchi
K., Otobe H., Furuya K., and Aiki T., 2003:
Effect of aquaculture on material cycles in
Otsuchi Bay, Japan. Otsuchi Marine
Science, 28, 65-70.
Ministry of Agriculture, Forestry and
Fisheries Japan, 2001: National Statistics
of Agricultural Production in 2000.
Ministry of Agriculture, Forestry and
Fisheries Japan.
Shikama N., 1990: Characteristics in flow fieldof water in Otsuchi Bay. Otsuchi Marine
Research Center Report, 16, 75pp.

Carrying capacity in an aquaculture ground of seaweed and shellfish

Tatara K., 1992: General consideration anddefinitions: Biological aspects, in "Fishing
Ground Capacity for Artificial Impacts"(ed. by Hirano, T.), Koseisha Koseikaku,
Tokyo, pp. 20-36.
Yoshikawa T. and Furuya K., 2004: Long-termmonitoring of primary production incoastal waters by natural fluorescencemethod. Marine Ecology Progress Series, in69

press.
Yoshikawa T., Takeuchi I., and Furuya K.,
2001:
Activeerosionof
Undaria
pinnatifida
Suringar(Laminariales,
Phaeophyceae) mass-cultured in Otsuchi
Bay in northeastern Japan. Journal of
Experimental Marine Biology and Ecology,
266, 51-65.

水研センター研報，別冊第 1 号，71−76, 平成16年
Bull. Fish. Res. Agen. Supplement No. 1, 71-76, 2004

71

Review: Production of Gracilaria parvispora in two-phasepolyculture systems in relation to nutrient requirements and uptake
Erin RYDER*1 , Stephen NELSON*2, Edward GLENN*2, Pamela NAGLER*2,
Sherman NAPOLEAN*3 and Kevin FITZSIMMONS*3

Abstract Gracilaria parvispora Abbott is highly valued in Hawaiian seafood markets.
Due to the over-harvesting of natural beds. G. parvispora is scarce on the open reef ; andharvesting is strictly regulated. On Molokai, Hawaii, a community-based operation wasestablished to develop a sustainable, integrated culture system for this species. Previous
research suggested that ammonium was the limiting factor for sufficient growth on thereef. Therefore, on Molokai, a polyculture system was developed using fish/shrimp effluent to load thalli with nitrogen before placement in a low-nutrient lagoon for growout. The research described here demonstrates how small-scale, commercial culture ofseaweed can be successfully integrated with the production of fish and shrimp. Twobenefits of a two-phase polyculture system are: 1) a waste product from the first phase(i.e. ammonia nitrogen) becomes a resource for the second phase and 2) integrated systems are financially more stable because of improved cash-flow and product diversification. A modest biomass of fish can support a substantial production of seaweed. The
type of cage-based, polyculture system developed on Molokai could be applicable to otherrural coastal areas.
Key words: Gracilaria parvispora, polyculture, tank culture, effluent, nitrogen

Introduction
Intensive tank and pond culture of freefloating seaweeds has been developed over thelast two decades in Israel (Friedlander andLevy, 1995), Taiwan, Chile, the United States,
Canada (Buschmann, 2001) and other areas.
Advantages of these methods include a high potential yield, the possibility to control andmechanize operations and the possibility ofusing seawater ponds as biological filters forfish culture and other effluents (Friedlander
and Levy, 1995). A disadvantage is the highcost compared to less intensive culture methods. However, on the island of Molokai,

Hawaii, we have developed a two-phasepolyculture system for production of seaweedsthat has the advantages of more intensive culture systems but can be operated at low cost.
The integrated aquaculture system describedhere was designed as a model for sustainable,
small-scale crop production in rural areas of
the tropical Pacific. The research was initiatedpartly in response to declines in local seaweed
resources in Hawaii, where seaweeds such as
Gracilaria parvispora are valued, traditional
foods. In Hawaii, over-harvesting of G.
parvispora from the fringing reefs started in
the 1970s, and this led to a severe decline innatural stocks. As a result, conservation laws

2003年 6 月12日受理（Received on June 12, 2003）* 1 University of Maryland, Center for Environmental Science, P.O.Box 775, Cambridge, MD 21613 USA Email: Erin_Ryder@hotmail.com* 2 University of Arizona Dept. of Soil, Water, and Environmental Science, 2601 East Airport Drive, Tucson, AZ 85706, USA* 3 Ke Kua'aina Hanauna Hou, HC01 Box 741, Molokai, HI 96748-0741, USA

72Erin RYDER , Stephen NELSON, Edward GLENN, Pamela NAGLER,
Sherman NAPOLEAN and Kevin FITZSIMMONS

have been enacted that limit wild-crop harvesting; and commercial harvesters cannot takemore than 4 kg per day. In addition, it is forbidden to remove cystocarpic thalli from thewater. The initial restoration project, whose
purpose is to develop a cultivation system to reestablish Gracilaria on the reef, was instituted
as a result of declining wild stocks.
The project was developed in conjunction
with a non-profit, community-development organization on Molokai. The group, Ke Kua'aina
Hanauna Hou (KKHH), was established in 1991
to develop ways to help the local community by
developing means for individuals or groups toearn an income while maintaining the local
land-use traditions. Although they participate
in the modern economy, many Molokai families still derive a substantial percent of theirlivelihoods from fishing, gardening, and othersubsistence activities that help them maintain aconnection with their traditional value system,
including a sense of stewardship towards theirisland's natural resources. Marketing seaweeds
is one way for native Hawaiians to achieve this.
In Hawaiian seafood markets, an edible, redseaweed G. parvispora known locally as "longogo" is highly valued (Glenn et al., 1998). Total
sales of G. parvispora by KKHH in 1999 were
10,670kg with a wholesale market value of approximately $75,000. By combining ogo culture
with shrimp and fish culture, production has
increased substantially. Molokai long ogo sells
for $7 per kg (a $2.20 per kg premium overother seaweeds on the market), and sales of
Molokai ogo was approximately $250,000 overthe last 12 months.
In previous work, Glenn et al. (1998, 1999)
demonstrated that G. parvispora is limited bynitrogen on the south reef of Molokai, HI. This
led to the development of a labor-intensive culture system where the seaweeds were producedin cages in the nutrient-poor coastal area andthen brought in each week to be fertilized intanks. More recently, the production system
was modified to reduce labor and increase
yields by integrating the cage grow-out systemwith the local production of fish and shrimp,

which are examples of other small-scale commercial aquaculture enterprise that have developed on Molokai.
The environmental benefits of integrating
the production of aquatic plants with the production of fish or shrimp to recapture nutrients are well known (e.g., Buschmann et al.,
1994; Neori et al., 1996; Shpigel and Neori, 1996;
Chopin and Yarish, 1998; Mathias et al., 1998;
Troell et al., 1997, Petrell et al., 1992.). Most of
the research on integrated plant-animal
aquaculture systems has involved intensive,land-based culture methods (Buschmann, et al.,
1994; Neori et al., 1996; Shpigel and Neori,
1996). Growing multiple cash crops such as
shrimp, fish, bivalves, and seaweeds in extensive systems is common in Asian aquaculture
systems (Chen, 1990), but this has not been
widely adopted in western aquaculture.
The focus of this paper is to describe the application of this concept to the development of
a two-phase polyculture system that has beensuccessful on Molokai and could therefore serve
as a model for similar small-scale commercial
development in other tropical areas.
The Molokai two-phase polyculture system
Since 1992, the University of Arizona together with Ke Kua'aina Hanauna Hou worked
at developing and refining a community-based
system for culturing Gracilaria. The system
now incorporates: a hatchery (Nelson and
Glenn, 2000), which produces spore-coated substrates for distribution to outside growers;
outplants of sporelings on the reef or inpolyculture with fish and shrimp; a cageculture farm for multiplication of the harvest;
and a processing facility. The two-phases ofseaweed culture in this system are an enrichment phase and a grow-out phase (Fig. 1). The
overall method involves all the life stages of theseaweed crop and enhances wild stocks on thereef. The system incorporates the major strategies of ecological design: conservation, regeneration, and stewardship (Van der Ryn and
Cowan, 1996).

Two-phase production systems for Gracilaria

From research in outplanting of spore-ladenmaterials it was found that the success of
sporeling development was related to dissolved
ammonia levels in the immediate vicinity(Glenn et al, 1999). This led us to look at growing the seaweeds in conjunction with fish or
shrimp, since the primary excretory product ofaquatic animals is dissolved ammonia. Our
first trials involved marine shrimp culture, because one of the local shrimp farms was foundto have dense populations of G. parvispora
growing in its effluent ditch. We transferrednutrient-depleted, tagged thalli to the ditch
and monitored their growth and nutrient content along with levels in the effluent (Nelson etal., 2001). Because of the periodic draining of
shrimp ponds into the ditch, nutrient levels
fluctuated widely from day to day, but meanammonia levels in the ditch (approximately 62
mmol m−3 ) were many times higher than in
nearby coastal waters. In this environment thethalli nitrogen content was increased from approximately 1 ％ to 3 ％ within about 5 days.
We also found that when these thalli wereplaced in the lagoon for grow-out they grew at

73

rates of 8 ％ to 10％ per day for the first week.
Growth and thalli nitrogen content declined
over the 4-week growth period so that by the
fourth week, growth was approximately 2 ％per day and the nitrogen content was back to 1％. Growth rates of thalli that were enriched in
the ditch are shown in Fig. 2. This method ofenriching the thalli requires much less laborthan the weekly use of chemical fertilizers intanks as was previously practiced.
Seaweed produced in the shrimp effluent
channel became an important source of newmaterial for stocking grow-out cages in the lagoon. Harvested seaweed from the ditch was
not directly marketable because of heavy loads
of sediment and epiphytes. However, after a period of grow-out in which seaweed biomass wasincreased in clean water, the product was ofhigh quality and easily sold in local markets.
Success with the use of shrimp effluent led us
to establish a tank culture system for production of local fishes at the seaweed production
site (Nagler et al., 2003). This allows more control of the production cycle and further decreases labor, by eliminating the need toFig. 1. Schematic of Ke Kua'aina Hanauna Hou's polyculture system for production of Gracilaria parvispora.
Seaweed is supplied by outside growers or hatchery then fertilized in shrimp/fish effluent channels (1a, 1b).
After enrichment with nitrogen, the seaweed is placed in floating cages (2) and floated in Puko'o lagoon for
growout (3). After 10 days in the lagoon, the seaweed is cleaned and sold to market.

74Erin RYDER , Stephen NELSON, Edward GLENN, Pamela NAGLER,
Sherman NAPOLEAN and Kevin FITZSIMMONS

in 55-L, aerated tanks that were filled withseawater from the grow-out site on Molokai.
Water samples from the tanks were taken immediately after the fish were added and at
2-hour intervals thereafter. We used afluorometric method for determining the concentrations of dissolved ammonia (Holmes
et al., 1999). Data for the first 2-hour period areshown in Fig．3, which shows the relationshipbetween fish mass and the ammonia excretion
rate in a log-log plot. Mean excretion rates
were 7.03, 2.17, and 1.81μg g−1 per hour formean fish weights of 200 g, 800 g, and 1200
grams, respectively.
Projections
Data from these studies was used to calculate
the fish biomass required to support the seaweed production levels usually achieved at the
Molokai grow-out site. This is a small-scale
cage culture operation that typically has about
80 cages in production throughout most of theyear. The optimal stocking density for the
cages, in terms of the percent increase of seaweed biomass, was determined to be approximately 2 kg per cage (Nagler et al., 2003). Table
1 shows the requirements of the biomass andnumber of fish needed to support a variety ofseaweed production projections. As shown,even at high stocking densities, the amount offish needed to support G. parvispora growth isrelatively small. Considering KKHH is a small,RGR (％day−1)

harvest seaweed from the effluent ditch andtransport of the harvest to the grow-out facilities. Milkfish (Chanos chanos) and mullet(Mugil cephalus) juveniles were obtained fromthe Oceanic Institute on Oahu and were cultured in tanks onshore immediately adjacent tothe seaweed grow-area. Milkfish grew muchbetter in the tanks than mullet and is now theprimary species being cultured.
Nagler et al. (2003) were able to densely stock
the fish tanks with nutrient-poor seaweed for
periods of 7 days in order to enrich the thalli.
Over the enrichment period the thallus nitrogen content increased up to 5 ％ on a dry
weight basis. The growth rate of enrichedthalli was up to 10 ％ per day and production in
the cages ranged from 39-57 g dry mass per
m2 per day over a 21-day production cycle. In
these trials with fish, we estimated the nitrogen requirements of Gracilaria and calculated
the amounts of fish feed needed to provide
these amounts, without calculating the actual
excretion rates of the fish. Subsequently, however, in order to provide data useful in designing a similar integrated farm, we measured theexcretion rates of fed milkfish as the amount of
nitrogen excreted per gram of fish.
For the excretion studies (unpublished),
milkfish of various sizes were held individually

Fig. 2. Gracilaria parvispora relative growth rates(RGR) after enrichment in a shrimp effluent channel. Day 7 growth rates occurred during the enrichment process. Week 1 depicts growth after
placement in lagoon. Seaweed experienced initial
rapid growth during the first week, then lower
growth on subsequent days. Data are from Nelson etal. (2001).

Fig. 3. Relation between wet fish biomass and excretion of ammonium (μg/L).

75

Two-phase production systems for Gracilaria
Table 1. Number and biomass of milkfish required to support (to increase nitrogen content of thalli from 1 to 4 ％) the production of Gracilaria parvispora in a two-phasepolyculture system in Hawaii
Total algal biomass

0.2-kg fish

0.8-kg fish

1.2-kg fish

(kg wet weight)

kg fish# fishkg fish# fishkg fish# fish

40

17

85

55

70

7

57

80

34

170

110

140

133

115

160

68

340

220

275

265

230

320

140

680

440

553

530

460

640

270

1,365

885

1,106

1,060

917

community-based operation, they can sufficiently support their ogo production using fish
effluent as a nutrient source. Their current operation consists of several tanks containing
enough milkfish to enrich the seaweed that isin the production system.
Conclusions
The production of Gracilaria in cage culture
can be successfully integrated with small-scale
production of fish and shrimp. Seaweed stockedin shrimp culture effluent ditches can thrivewith little management and can serve as stocks
for grow-out in clean, low-nutrient water. We
were able to achieve similar enrichment ofGracilaria thalli by holding stocks for 5 to 7
days in fish tanks. We found that a even a modest biomass of fish can support a substantial
production of seaweed in this culture system.
This was also the case in studies of Gracilaria
cultivated with salmon grown in cages (Troellet al., 1997; Buschmann et al., 2001), where increased productivity of 1 hectare of Gracilaria
could be supported with 5 ％ of the fish dissolved nitrogenous waste. In the culture operation on Molokai the main benefits of nutrientsare to support seaweed production rather thanto scrub nutrients for effluent. However, if
seaweeds are cultured on a larger scale, such as
for the phycocolloid industry, they can be efficient at removal of nutrients from effluent ofintensive land-based fish farms (Troell et al.,
1997; Chopin et al, 2001).
Disregarding the environmental benefits ofintegrated seaweed and fish or shrimp production, seaweed culture can also benefit smallscale aquaculture farms by increasing theireconomic viability. Small aquaculture enterprises for shrimp or fish, such as those on
Molokai, tend to be financially unstable, because they have continuous, fixed expenses but
intermittent income because their harvests
come in batches that are spaced weeks ormonths apart. Integration of seaweed production with these systems greatly improves cashflow, as seaweeds can be harvested weekly
throughout the year. The seaweed component
in our system is worth approximately $7 per
kg and revenues from seaweed sales could significantly enhance the profitability of an integrated system. On Molokai, the use of fish or
shrimp effluent increased production ofGracilaria and also resulted in reduced labor
requirements, an additional economic benefit.
In addition, diversification of farms in the community can aid in reducing competition andstimulate the formation of cooperative relationships among producers. This type of cagebased, polyculture system developed on
Molokai could also be successfully employed inother rural areas of the Pacific.
References
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Bottger M., Buitana S., Retamales C.,
Vergara P. A., and Guitteriz A., 1994:
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76

Erin RYDER , Stephen NELSON, Edward GLENN, Pamela NAGLER,
Sherman NAPOLEAN and Kevin FITZSIMMONS

Aquaculture Engineering, 13, 283-300.
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Chopin T. and Yarish C., 1998: Nutrients or not
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Phycology, 37, 975-986.
Friedlander M. and Levy I., 1995: Cultivation ofGracilaria in outdoor tanks and ponds.
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Glenn E., Moore D., Akutigawa M., Himler A.,
Walsh T., and Nelson S., 1999: Correlation
between
Gracilaria
parvispora(Rhodophyta) biomass production andwater quality factors on a tropical reef in
Hawaii. Aquaculture, 178, 323-331.
Glenn E., Moore D., Brow J., Tanner, R.,
Fitzsimmons K., Akutigawa M., andNapolean S., 1998: A sustainable culture
systemfor
Gracilaria
parvispora(Rhodophyta) using sporelings, reef
growout and floating cages in Hawaii.
Aquaculture, 165, 221-232.
Holmes R., Aminot A., Kerouel R., Hooker B.,
and Peterson B., 1999: A simple and precise
method for measuring ammonium in marine and freshwater ecosystems. Canadian
Journal of Fisheries and Aquatic Sciences,56, 1801-1808.
Mathias J., Charles A., and Baotong H. (eds.),
1998: Integrated fish farming, CRC Press,
Boca Raton, Florida, 420pp.
Nagler P., Glenn E., Nelson S., and NapoleanS., 2003: Effects of fertilization treatment
and stocking density on the growth andproduction of the economic seaweed

Gracilaria parvispora (Rhodophyta) incage culture at Molokai, Hawaii.
Aquaculture, 219, 379-391.
Nelson S. G. and Glenn E. P., 2000: Spore andsporeling production in the development ofaquaculture systems for species ofGracilaria and related seaweeds, in "Recent
AdvancesinMarine Biotechnology
Volume 4: Aquaculture, Part A Seaweeds
and Invertebrates" (eds. by Fingerman M.
andNagabhushanam
R.),
SciencePublishers, New Hampshiere, pp.1-21.
Nelson S. G., Glenn E. P., Conn J., Moore D.,
Walsh T., and Akutagawa M., 2001:
Cultivation of Gracilaria parvispora(Rhodophyta) in shrimp-farm effluent andfloating cages in Hawaii: a two-phasepolyculture system. Aquaculture, 193, 239248.
Neori A., Krom M., Ellner S., Boyd C., Popper
D., Rabinovich R., Davidson P., Divr. O.,
Zuber D., Ucko M., Angel D., and Gordin
H., 1996: Seaweed biofilters as regulatorsof water quality in integrated fish-seaweed
culture units. Aquaculture, 141, 183-199.
Petrell R. and Mazahari K., 1992: Integrated
salmon netpen and laminaria culture,
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A. H., Kautsky N., and Kautsky L., 1997:
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201pp.

水研センター研報，別冊第 1 号，77−82, 平成16年
Bull. Fish. Res. Agen. Supplement No. 1, 77-82, 2004

77

Preliminary examination of the bioremediation and mariculture
potential of a Northeast U.S.A. and an Asian species of Porphyra
George P. KRAEMER* 1, Raquel CARMONA* 2,3, Christopher NEEFUS* 4,
Thierry CHOPIN* 5, Sheryl MILLER* 3, Xiaogeng TANG* 3,6 and Charles YARISH* 3

Abstract Finfish and shrimp mariculture operations produce nutrient-rich effluentthat can threaten the health of coastal ecosystems if not properly managed. As part ofan effort to develop an economically viable system of integrated polyculture, we havebegun to evaluate the bioremediation and mariculture potential of Northeast U.S.A. andAsian species of Porphyra. We present here preliminary results based on short- andlong-term experiments. Short-term nitrogen (N) uptake measurements were conducted
over ca. 20 min in 50 mL tubes at 5-15 ℃ and at high (10 g FW L−1 ) stocking density.
During long-term (28-d) experiments at 15 ℃ and at 0.4 g FW L−1 , we examined thegrowth, N assimilation into Porphyra tissue, and phycobiliprotein contents at three- toseven-day intervals as a function of N concentration (25, 75, 150, 300μM). Performance(growth rate and bioremediation) was maximal at 150-300μM inorganic N. Induction ofarchaeospore production reduced growth rates. Porphyra purpurea removed 96-100 ％ of
N within 3.5 days at 150μM NH4＋. Overall, Porphyra appears to be an excellent choice
for bioremediation of moderately eutrophic effluents, with the added benefit that tissue
may be harvested for sale.
Key words: Porphyra, eutrophication, aquaculture, mariculture, nitrogen, phosphorus,
bioremediation, seaweed

Introduction
Finfish and shrimp mariculture produces effluent that is rich in inorganic nitrogen (N) andphosphorus (P). These nutrients derive fromthe bacterial release of inorganic N and P from
non-consumed animal food, and from excretory
waste products of the cultured animals(Beveridge, 1987). These additions of N and P
can threaten ecosystem health by degrading
critical functions of coastal ecosystems (McVey
et al., 2002). The detrimental effects ofeutrophication include blooms of harmful

phytoplankton and unwanted macroalgae(Cuomo et al., 1993), as well as development of
hypoxia and anoxia (Sfriso et al., 1987). The
ecological incentive for remediating eutrophic
effluents is clear. Moreover, there are also economic incentives to reduce the poss of nutrients. The N and P that are flushed from thesystem represent a loss of opportunity for theaquaculturist, since these nutrients could bechanneled into the production of valuable products. In addition, governmental agencies
charged with reducing coastal eutrophication
are developing regulations limiting the release2003年 6 月12日受理（Received on June 12, 2003）* 1 Department of Environmental Sciences, State University of New York, Purchase College, Purchase, NY 10577 USA* 2 Department of Ecology and Evolutionary Biology, University of Connecticut, Stamford, CT 06901 USA* 3 Faculdade de Ci＾
encias do Mar e do Ambiente, Universidade do Algarve, PORTUGAL* 4 Department of Plant Biology, University of New Hampshire, University of New Hampshire, Durham, NH 03824
5* Centre for Coastal Studies and Aquaculture, University of New Brunswick, Saint John, New Brunswick E2L 4L5 CANADA* 6 College of Marine Life Sciences, Ocean University of Qingdao, PRC

78

George P. KRAEMER, Raquel CARMONA, Christopher NEEFUS
Thierry CHOPIN, Sheryl MILLER, Xiaogeng TANG,6 and Charles YARISH

of N and P (c.f. U.S.A. Environmental
Protection
AgencyProposed
Effluent
Guidelines Program Plan, Federal Register(June 18, 2002, Volume 67, Number 117);
Jordan, 2002). In the future, aquaculturists
can expect to incur financial penalties if theycannot regulate the release of their waste effluent.
One solution to the problem of eutrophic effluent that addresses both ecological and economic issues is the development of integrated
aquaculture, in which seaweeds are growndownstream from animals. Systems of integrated aquaculture are ideal because the N and
P in the animal effluent are necessary requirements for the growth of the seaweeds. This is
not a new idea (for review see Chopin et al.,2001). What distinguishes this project frommany of the prior studies is the selection of thealgal component. Obviously, the best seaweed
to integrate into an animal aquaculture operation is one characterized by rapid growth, theaccumulation of N and P to high levels in tissue, and some added value. We are investigating the genus Porphyra as the seaweed partner
for a number of reasons (Yarish et al., 1998;
Chopin et al., 1999). All species of Porphyra
produce gametophytes that are flat sheets one
or two cell layers thick. This combination ensures an extremely high surface area-tovolume ratio, with all cells involved in the
uptake of nutrients and production of new tissue. In part for these reasons, Porphyra is capableof
rapid
growth;preliminary
measurements show this genus capable of atleast 20 ％ d−1 (Kraemer, pers. obs.). Species ofPorphyra also are efficient nutrient concentrators. In situations where nutrients are readily
available, N can constitute up to 7.4 ％ of thedry tissue biomass (Chopin and Yarish, 1998,
1999). Finally, several species of Porphyra form
the basis for a multi-billion dollar (U.S.) global
business in the production of nori for humanconsumption. A recent added value under development is the use of R-phycoerythrin as thefluorescent conjugate for immunologicaldectection of target molecules in molecularbiological research (Mumford and Miura, 1988).
Previous studies have focused on the integration of other macroalgal species into finfish
culture (e.g., Ulva lactuca; Cohen and Neori,1991). While other species may be efficient nutrient filters, the biomass that is produced has
limited application after harvest (e.g., organic
composting). Consequently, Porphyra not only
has potential for bioremediation of aquaculture
effluents, but also production of a crop that
may have economic value.
Growth, accumulation of N and P, and highvalue by-products in tissue are dependent on
the environmental factors that regulate production: temperature, nutrient availability,
irradiance, water motion. As part of an effort
to develop an economically viable system of integrated aquaculture, we have been evaluating
the bioremediation and mariculture potentialof Northeast U.S.A. and Asian species ofPorphyra. We have included Asian species in
the comparison since they represent in many
ways the industrial benchmarks. However, we
do not advocate the use of non-native species ofPorphyra in open culture in New Englandcoastal waters. We present here preliminary
results that describe the influence of temperature and nutrient availability on N uptake, tissue production, phycoerythrin and N tissue
content, and nutrient removal efficiency.
Materials and Methods
We have been working with aquaculturists
from GreatBay Aquaculture, LLC. (GBA;
Portsmouth, New Hampshire, U.S.A.) in thedevelopment of the integrated system. GBA
raisessummerflounder(Paralichthysdentatus) and cod (Gadus morhua) in a landbased system. Effluent from the grow-out
tanks has an average NH4 concentration of 150
μM, and temperatures that range from 10 to
19℃ over the course of the year. These values
were used to determine the conditions for thelaboratory experiments.
All blade (gametophyte) tissue used for theseexperiments
wasgenerated
from
the

79

Bioremediation of eutrophic effluents by Porphyra

conchocelis stage. The experimental work was
conducted under controlled environmental conditions of irradiance, temperature, andphotoperiod in walk-in growth chambers at the
University of Connecticut, Stamford. We present here data from the Northeast U.S.A. species P. purpurea (New York strain for longterm experiment and Maine strain for shortterm N uptake measurements) and P. yezoensis(an Asian cultivar). Short-term measurementsof NH4＋ uptake rate were performed on tissuegrown at 5 , 10 , or 15 ℃. Samples (ca. 0.3 g FW)
were placed in 50 mL transparent plastic screwtop tubes containing 30 mL of artificial
seawater ("MBL" formula, Cavanaugh 1975).
Ammonium levels were adjusted to 10, 20, 40,
75, or 150μM while inorganic phosphorus wasadded to a constant N:P molar ratio of 10:1.
Tissue was incubated at the growth temperature. At 7 and 17min after the introduction oftissue into the tubes, samples of incubation medium were collected and analyzed for NH4＋ concentration (Liddicoat et al., 1976). Five to seven
replicates were used per N concentration.
Long-term (28-d) experiments were also carried out at the University of Connecticut facility in 1-L flasks. Porphyra gametophytic tissue(ca. 0.4 g FW L−1 ), grown at 10 ℃ and acclimated at 15 ℃ for seven days, was placed in 800
mL of von Stosch-enriched culture medium.
The N level in the incubation medium was adjusted to either 25, 75, 150, or 300μM, with P
added to constant 10:1 N:P molar ratio. Threereplicates at each N concentration were used.
At 3-4 d intervals the culture medium waschanged, with a sample from each flask retained for N and P analysis (via Technicon
autoanalyzer). At 7-d intervals, the tissue ineach flask was weighed (FW). Newly produced
tissue was removed so that each 7-d growth period began with the same stocking density (0.4g FW L−1 ). From the excised tissue, samples
were conserved for CHN (by means of a PerkinElmer CNS analyzer) and phycobiliprotein
analyses (Beer and Eshel, 1985).

Results
Porphyra purpurea demonstrated differencesin the rate of NH4＋ uptake that were a functionof temperature (Fig. 1). The highest rates of
NH＋
4 uptake by P. purpurea occurred at 10 ℃.
Porphyra yezoensis took up NH＋
4 roughly twice
as fast at 15 ℃ than did P. purpurea.
Over the 28-d long-term experiments, growth
was not constant for either species (Fig. 2).
Porphyra yezoensis grew well during the firstweek (18 ％ d−1 ), but archaeospore production
ensued and the tissue began to disintegrate. By
the experiment's end, the P. yezoensis growthrate was negative as losses due to reproduction
exceeded new growth. Porphyra purpurea appeared to enter a brief period of archaeospore
production but growth rebounded by the experiment's end.
By the experiment's end, phycobiliprotein
concentration in P. purpurea blade tissue
showed approaching saturation (Fig. 3). Halfsaturation values at occurred at ca. 120 μM
NH4＋. Unlike phycobiliprotein content, tissue N
content did not appear to be close to an asymptote, even when grown at 300μM (Fig. 4).
Preliminary results for P. purpurea demonstrate its efficacy as a bioremediator of
eutrophic effluent (Fig. 5). During 3.5 d batch
cultures, P. purpurea removed on average 96-98％ of the NH4 in the incubation medium. This

Fig. 1. Short-term NH4＋ uptake rates measured as afunction of temperature. All measurements conducted at 150μM ammonium. Errors bars are standard deviations.

80

George P. KRAEMER, Raquel CARMONA, Christopher NEEFUS
Thierry CHOPIN, Sheryl MILLER, Xiaogeng TANG,6 and Charles YARISH

removal declined to 77 ％ at 300 μ M.
Interestingly, the efficiency with which P.
purpurea removed inorganic P declined as N
concentrations increased (molar N:P ratios constant at 10: 1). At 150μ M NH4 and 15 μM
PO43− P. purpurea removed 46 ％ of the inorganic P.
Discussion
The short-term measurements of NH4 uptake
rate demonstrated interspecific differences in
performance. Clearly, not all Porphyra species
are equally efficient in the uptake of NH4 , anargument for the evaluation of a range of pos-sible species before selecting the bestbioremediator.
Porphyra
yezoensis
outperformed P. purpurea, at least at 15 ℃, but we
do not yet know whether other local species
will compare with the Asian species. Some haveargued that short-term uptake measurements
are to some extent artifactual due to "surge"
uptake (e.g., Dy and Yap, 2001). However, previous work with P. yezoensis suggests that thisphenomenon is not common to all macroalgal
species (Yamamoto, 1992). The fact that a definite temperature optimum was identified for
one Porphyra species suggests that further ex-

Fig. 4. Relationship between N availability (as NH4concentration at start of each 3-4 d growth period)
and tissue N content at the end of the 28-d experiment (n＝3; error bars are standard deviations)Fig. 2. Average growth rates (n＝3) during longterm experiments (150μM NH4 ). Negative growth
rates occur when tissue becomes reproductive andfragments

Fig. 3. Ammonium concentration vs. Porphyra
purpurea r-phycoerythrin concentration at end of
28-d experiment (n＝3; error bars are standard deviations)Fig. 5. Efficiency of nutrient removal from incubation media. Values are averages over entire 28-d experiment (n＝12; error bars are standard deviations)Bioremediation of eutrophic effluents by Porphyra

panding the pool might provide a high- or low
temperature tolerant species. This would enable seasonal crop rotation to take advantageof temperature optima for each particular species. Alternatively, project engineering could be
employed to moderate the differences between
the operating and optimal temperatures forbioremediation of nutrient-rich aquaculture effluent.
When grown during the long-term experiments (effectively 3.5 d batch culture at 15 ℃,
150μmol photons m−2 s−1, and a stocking density of 0.4 g FW L−1 ,) the performance indicators indicated that different physiological
functions respond differently to the availability of inorganic nitrogen. Data for P. purpurea
regarding phycobiliprotein concentration indicates that production of pigments is not restricted under our experimental conditions inthe same way that growth is limited. That pigments continue to accumulate under nutrientreplete conditions suggests that thesecompounds can act both as light absorbers andas nitrogen stores, something reported forother red macroalgae under N-sufficient conditions (Bird et al. 1982; Vergara et al., 1995).
Presumably, as growth causes an increase inbiomass density the extra pigments are advantageous in light of the diminution of theirradiance regime. Second, tissue nitrogen accumulates in an apparently linear function of
nitrogen availability, with no indication ofsaturation even at 300μM NH4 . This argues
that nitrogenous compounds other than pigments are important in the storage of nitrogen.
Amino acids are a candidate. Our unpublisheddata demonstrate such a response to nitrogen
availability, though the increases in aminoacids concentrations may not account for all of
the increase in tissue nitrogen.
Our short-term data indicates that P.
purpurea (Maine isolate) is capable of removing
ca. 120μmols NH4 g−1 FW d−1 (assuming 10: 1
FW: DW ratio and uptake during 12 lighted
hours of a day). The long-term experimentusing P. purpurea (New York isolate) indicatesan average uptake rate during a 3.5 d period of

81

66μmols NH4 g−1 FW d−1. This difference may
be due to true differences in performance between strains. However, the average uptake
rates during the long-term experiments reflect
an integration of the effects of changing NH4
concentration during the 3.5 d period. The uptake rates in a functioning, flow-through system will be much higher, since theconcentration will be correspondingly higher.
The actual bioremediation (i.e., ％ N and P removed) will depend on Porphyra stocking density and effluent residence time, in addition toconcentration-specific uptake rates. These arevariables to be investigated at larger scales.
Acknowledgements
Support for this project was provided byfunding to C. Y., C. N., and G. P. K. by the Sea
Grant Programs of Connecticut, New
Hampshire, and New York, respectively and by
NOAA'sNational
MarineAquaculture
Initiative, U.S.A.; to C. Y from the State ofConnecticut Critical Technology Program; andto X. T. by the National Natural Science
Foundation of China for Science.
References
Beer S. and Eshel A., 1985 ： Determining
phycoerythrin and phycocyanin concentrations in aqueous crude extracts of red
algae. Aust. J. Mar. Fresh. Res., 36, 785792.
Beveridge M. C. L., 1987: Cage aquaculture,
Fishing News Books Ltd., Farnham, 352pp.
Bird K. T., Habig C., and DeBusk T., 1982:
Nitrogen allocation and storage patterns
in Gracilaria tikvahiae (Rhodophyta). J.
Phycol., 18, 344-348.
Cavanaugh G. M., 1975: Formulae and Methods
VI, The Marine Biological Laboratory,
Woods Hole, MA.
Chopin T. and Yarish C., 1998: Nutrients or not
nutrients? That is the question in seaweed
aquaculture ... and the answer depends on
the type and purpose of the aquaculture

82

George P. KRAEMER, Raquel CARMONA, Christopher NEEFUS
Thierry CHOPIN, Sheryl MILLER, Xiaogeng TANG,6 and Charles YARISH

system. World Aquaculture , 29(4), 31-33,
continued 60-61.
Chopin T. and Yarish C., 1999: Seaweeds must
be a significant component of aquaculture
for an integrated ecosystem approach.
Bull. Aquacul. Assoc. Canada., 99, 35-37.
Chopin T., Yarish C., Wilkes R., Belyea E., Lu
S., and Mathieson A., 1999: Developing
Porphyra/salmon integrated aquaculture
for bioremediation and diversification of
the aquaculture industry. J. Appl. Phycol.,11, 463-472.
Chopin T., Buschmann A. H., Halling C., TroellM., Kautshy N., Neori A., Kraemer G. P.,
Zertuche-Gonzalez J. A., Yarish C., andNeefus C., 2001: Integrating seaweeds into
mariculture systems: a key towards
sustainability. J. Phycol., 37, 975-986.
Cuomo V., Merrill J., Palomba I., and PerrettiA., 1993: Systematic collection of Ulva andmariculture of Porphyra: Biotechnology
against eutrophication in the Venice
Lagoon. Int. J. Environ. Stud., 43, 141-149.
Dy T. and Yap H. T., 2001: Surge ammonium
uptakeofthecultured
seaweedKappaphycus alvarezii (Doty). J. Exp.
Mar. Biol. Ecol., 265, 89-100.
Jordan M. E., 2002: US. EPA's Aquatic Animal
Production
Effluent
Limitations
Guidelines and Standards, Book of
Abstracts,
Northeast
Aquaculture
Conference and Expo 2002, 12pp.
Liddicoat J. C., Tibbets S., and Butler E. I.,
1976: The determination of ammonium innatural waters. Wat. Res., 10, 567-568.
McVey J. P., Stickney R., Yarish C., andChopin T., 2002: Aquatic Polyculture andBalanced Ecosystem Management: New
Paradigms for Seafood Production, in"Responsible Marine Aquaculture" (eds. by
Stickney R. R. and McVey J. P.), CABI,
Oxon, UK., pp. 91-104.
Mumford T. F. and Miura A., 1988: Porphyra
as food: cultivation and economics. in"Algae and Human Affairs" (eds. by Lembi
C. A. and Waaland J. R.), Cambridge
University Press, Cambridge, pp. 87-117.
Sfriso A., Marcomini A., and Pavoni B., 1987:
Relationships between macroalgal biomass
and nutrient concentrations inahypertrophic area of the Venice lagoon.
Mar. Environ. Res., 22, 297-312.
Vergara J. J., Bird K. T., and Niell F. X., 1995:
Nitrogen assimilation following NH4＋
pulses in the red alga Gracilariopsis
lemaneiformis: Effect on C metabolism.
Mar. Ecol. Prog. Ser., 122, 253-263.
Yamamoto T., 1992: Constant uptake ofammonium-N and nitrate-N by Porphyra
yezoensis thalli. J. Fac. Appl. Biol. Sci.
Hiroshima Univ., 31, 155-159.
Yarish C., Wilkes R., Chopin T., Fei X. G.,
Mathieson A. C., Klein A. S., Friel D.,
Neefus C. D., Mitman G. C., and Levine I.,
1998: Domesticating indigenous Porphyra(nori) species for commercial cultivation in
Northeast America. World Aquaculture, 29(4), 26-29.

水研センター研報，別冊第 1 号，83−90, 平成16年
Bull. Fish. Res. Agen. Supplement No. 1, 83-90, 2004

83

An assessment of the beneficial roles of Nannochloropsis oculata
in larval rearing of marine finfish
Masanori OKAUCHI*

Abstract From points of both water quality management by algal nutrient absorption
and a good live food of rotifer, the role of Nannochloropsis oculata supplied to larvalrearing water was examined by a larval rearing experiment in this study. Larvae ofJapanese red sea bream, Pagrus major, were reared being fed rotifers and subsequently
an artificial diet during the thirty-day experimental period. In the four test tanks (100-L
capacity) each with 1,000 Japanese red sea bream larvae in addition to the rotifers, N.
oculata was maintained at a density of 5-10×105 cells/mL while in the four control
tanks, no N. oculata supplemented, but all the other experimental conditions were thesame as the test tanks.
At the end of the experiment, the concentrations of inorganic nitrogen (NH4-N, NO2-N,
and NO3 -N) and inorganic phosphate (PO4 -P) in the control tanks were 1.5-2.0 times
higher than those in the test tanks. While, the number of rotifers with eggs in the testtanks was remarkably higher in comparison with that in the control tanks. Moreover,rotifers in the test tanks contained much more eicosapentaenoic acid (EPA) and n-3
highly unsaturated fatty acid (n-3 HUFA), so that their nutrient value is concluded as
higher than that in the control tanks. From the results of this experiment, supplementation with N. oculata into the rearing water is concluded to produce beneficial effects
on maintaining water quality and also enhancing the nutrient quality of the rotifers.
Key words: Nannochloropsis oculata, larval rearing, water quality management,
Pagrus major, rotifer, Brachionus, food organism

Recently, the condensed freshwater Chlorella
has been popularly used as a food organism for
L-type and S-type rotifers, Brachionus
plicatilis and B. rotundiformis, in Japanese
hatcheries of marine fishes (Hirayama et al.,
1989; Maruyama et al., 1989). Because condensed freshwater Chlorella is readily available
from several private companies, it has contributed to much laborsaving and allowed the realization of the stable production of rotifers(Yoshimura et al., 1997). While, the number ofhatcheries which culture the microalga
Nannochloropsis oculata, which has been usedas the main food for rotifers for more than 20

years, has gradually reduced in Japan.
However, the freshwater Chlorella has mainly
three demerits as a live food. (1) Chlorella contains little n-3 highly unsaturated fatty acids(n-3 HUFA) (Maruyama et al., 1986), which areessential fatty acids for marine fishes(Watanabe et al., 1983), so its nutritive value
has been considered as lower than that of N.
oculata. (2) The alga does not survive long-termin sea water and readily decays within several
days. The dead cells then induce water pollution. (3) The alga has a hard cell wall, so that it
cannot be used as a food organism for almost
all important aquacultured invertebrates.

2003年 6 月12日受理 (Received on June 12, 2003)* National Research Institute of Aquaculture, Fisheries Research Agency, Nansei, Mie 516-0193, Japan

84

Masanori OKAUCHI

From these reasons, small quantities of N.
oculata are cultured in many hatcheries andused to enrich the HUFA content of rotifers,
which are predominantly cultured with
Chlorella, before feeding the rotifers to finfish
larvae. Moreover, it is recognized empiricallythat the addition of N. oculata into the rearing
water is useful to increase the activity and survival of larval fish (Eda et al., 1990; Murashige
et al., 1991; Tamaru et al., 1994). In this study,
the effect of N. oculata additions to the rearing
water was investigated from the point of viewof both the quality of the food organisms rotifers and for water quality management in thelarval rearing tanks.
Materials and Methods
Materials
Japanese red sea bream, Pagrus major, wasselected as the material of this study, because
the larval rearing method is fully establishedand larval production is carried out regularly
in Japan. Eggs were obtained from a matured
female, and were fertilized artificially. Prior to
the experiment, the larvae were reared for 10
days after hatching in a 500-L polycarbonate
tank with a continuous air-supply and waterexchange system. The larvae were fed with sufficient S-type rotifer during this period.
Nannochloropsis oculata collected from
Gokasho Bay in 1986, and cultured in liquid
Guillard F medium (Guillard and Ryther, 1962)
was used in this experiment. This strain has
been cultured using 100-mL flasks with periodic changes of medium under 20℃ and 50 μmol/m2/s for more than ten years. During theexperiment, the alga was produced using some
10-L glass carboys in batch style under conditions of 25 ℃ and 80 μmol/m2 /s. When thealgal growth reached the stationary phase, it
was added to the larval rearing water.
S-type and L-type rotifers were obtained
from Mie Prefecture Fish Farming Center,
Hamajima City. They could make few restingeggs in mass production. They mainly reproduced by parthenogenesis and produced few

resting eggs in mass production. They were
produced using some 500-L polycarbonate
tanks fed with freshwater Chlorella at 25 ℃.
The artificial diet for red sea bream larvae usedin this study was purchased from a Japanese
private company.
Larval rearing experiment
The experiment was conducted using eight
100-L transparent polycarbonate tanks eachwith 90-L filtered seawater. Four tanks wereused as test trials and others were used as control. One thousand larvae at age 10 days wereintroduced into each tank. In the test tanks,
both N. oculata and rotifers were put into therearing water at densities of 106 cells/mL and
10N/mL, respectively, at the beginning of theexperiment. They were kept at 5 -10 × 105
cells/mL and 10-20/mL, respectively, during
the experiment. In the control tanks, the density of rotifers was kept almost the same asthat in the test tanks, however, N.oculata was
not supplied. S-type and L-type rotifers were
fed from day 10 to day 20 and from day 20 today 30, respectively. Before being supplied to
the larvae, the rotifers were fed with N. oculata
sufficiently for one day to enhance the eicosapentaenoic acid (EPA) levels. From day 30 tothe end of experiment (day 40), the appropriatequantity of artificial diet was fed in each tank.
The densities of N. oculata and rotifers in alltanks were estimated twice daily using acoulter counter and a stereoscopic microscope,
respectively. Moreover, the densities were adjusted to the fixed densities by further additions or by draining and adding filteredseawater. The rearing water temperature was
kept at 20-22 ℃ and aeration was continuously
supplied at a rate of 400-500 mL/min per atank. To maintain the water quality in eachtank, about 30-L rearing water was exchanged
once a day before feeding using thin vinyl
tubes.
Counting of dead larvae and female rotifers
carrying eggs
Dead larvae, which sank to the bottom of85

Beneficial roles of N. oculata in fish larval rearing

each tank, were collected each day into a whitebeaker using thin glass tubes with a siphon effect. The average and standard deviation (±S.
D.) were calculated from the number of deadlarvae in the four test tanks and four control
tanks, respectively. Moreover, four 10-mL samples were taken from each tank in order to cal
culate the amictic (undergoing parthenogenesis)
female ratio (％); (the number of rotifers carrying eggs/the number of rotifers) × 100.
Because no resting eggs were observed in themass culture tanks of S-type and L-type rotifers, all rotifers carrying eggs were regarded
as amictic females in this experiment.
Water quality analysis
In this experiment, the contents of inorganic
nitrogen (total ammonia; NH4-N, nitrite nitrogen; NO2-N, nitrate nitrogen; NO3-N) and inorganic phosphate (PO4 -P) were selected asindicators of water quality. Water samples(about 500-mL) for their analysis were collectedfrom each tank every day before changing thewater. The samples were filtered using GF/C
(Whatman). The filtered samples were put in
500-mL polyethylene bottle and preserved at−30 ℃ for later analysis. The total ammonia
was measured using an ammonia electrodewith digital ion analyzer (Orion Research,model 701A). Other nutrients were measured
according to the methods of Strickland andParsons (1972).
Measurement of the survival rate of larvae
At the end of the 30-day rearing experiment,
the number of surviving larvae and the total
body length of 100 randomly sampled larvae
from each tank, were measured and their averages±S.D. in the test tanks and control tanks
were calculated and analyzed by one-way
ANOVA.
Fatty acid analysis of rotifers
On day 30, at the start of feeding the artificial diet, rotifers in the test and control tanks
were sampled using a plankton net. They were
washed with fresh water for about ten minutes,

and were stored at − 80 ℃ until analysis.
Furthermore, rotifers enriched with N. oculata
after being produced with freshwater Chlorella
were also analyzed. Total lipids were extracted
by chloroform-methanol method according toFolch et al., (1957). The fatty acids of the total
lipids were methyl-esterified and analyzed by
gas-liquid chromatography.
Results
Survival and growth of larvae
Daily changes of the average number of deadlarvae in the test and control tanks are shownin Fig. 1. The number of dead larvae per day inthe control tanks was significantly higher thanthat in the test tanks after day 28 (P＜0.01).
The average total number of the conformed
dead larvae in test tanks during this experiment was about 100, while that in the control
tanks was about 198. The averages±S.D. of thetotal body length (mm) in the test and control
tanks were 9.5±0.9 and 8.8±1.2, respectively.
Thus, larvae in the test tanks were significantly larger (P＜0.05) than those in the control
tanks.
Rate of rotifers with eggs
Daily changes of the percentage of rotifers
with eggs in the test and control tanks areshown in Fig. 2. Regardless of the rotifer type,the number of rotifers with eggs in the testtanks was clearly higher than that of the control tanks. More than 20 ％ of rotifers in thetest tanks carried one or two eggs under theirloricas, while rotifers with eggs in the control
tanks were less than 10 ％. During the experiment, no mictic reproduction was observed in
any tank.
Fatty acid components of the rotifers
Percentage composition of the fatty acids ofrotifers is shown in Table 1. The crude protein
and crude lipid contents of them are also
shown. The rotifers collected from the testtanks contained much EPA comparison withthe rotifer from the control tanks.

86

Masanori OKAUCHI

Fig. 1. Daily changes of the average number of dead larval Japanese red sea bream, Pagrus major, in the testtanks (Dotted bars ; ) and the control tanks (Shaded bars ; ). Vertical lines indicate the standard deviations.
X-axis shows the larval age, which is indicated by days after hatching.

Fig. 2. Daily changes of percentage of rotifers with eggs in the test tanks (Dotted bars ; ) and the control tanks(Shaded bars ; ). Vertical lines indicate the standard deviations. X-axis shows the elapsed time from the larval
hatching out. In order to calculate the ratio of females carrying eggs, four 10-mL samples were taken from eachtank and the number of rotifers with eggs was counted using a stereoscopic microscope.

Consequently, the content of n-3 HUFA contained in rotifers from the test tanks was significantly higher than that in rotifers from thecontrol tanks. While, the fatty acid componentof rotifers, which were secondarily enrichedwith N. oculata after production using

freshwater Chlorella, was almost the same asthat of rotifer from the test tanks. On theother hand, the protein content of rotifers fromthe control tanks was lower in comparison
with those of rotifers from the test tanks.

Beneficial roles of N. oculata in fish larval rearing

87

Table 1. Percentage composition of the fatty acid components, percent total lipid and crude protein of rotifers
collected from the test tanks and the control tanks are shown in the first and second rows. Moreover, these components of rotifers, which were secondarily enriched with N. oculata after production using freshwater
Chlorella, are shown in the third row for comparison.
(％)
Rotifers in the test tanks Rotifers in the control tanks Rotifer cultured with Chlorella
Fatty acid(with Nannochloropsis)(without Nannochloropsis)(secondary enriched with Nannochloropsis)
14 : 0
5.5
5.2
5.8
16 : 0
15.2
15.6
16.4
16 : 1
18.8
11.1
19.8
16 : 4 n-3
0.6
1.2
0.8
18 : 02.6
2.2
2.8
18 : 1
8.2
9.6
10.5
18 : 2 n-6
4.5
5.6
4.7
18 : 3 n-6
0.5
0.7
0.4
18 : 3 n-3
0.5
0.2
0.8
18 : 4 n-3
0.9
0.8
0.1
20 : 1
3.7
2.7
4.7
20 : 2 n-9
0.2
0.2
0.3
20 : 3 n-6
0.4
1.1
1.0
20 : 4 n-6
3.2
2.7
4.7
20 : 4 n-3
0.5
0.6
0.5
20 : 5 n-3
18.9
5.8
20.8
22 : 11.2
2.0
1.1
22 : 3 n-6
0.1
0.3
0.1
22 : 5 n-6
1.6
Tr*2
0.1
22 : 5 n-3
2.6
1.2
5.6
22 : 6 n-3
0.4
0.2
0.4
24 : 1
0.3
0.2
0.4
∑n-6
10.3
10.4
11.0
∑n-3
24.0
10.0
29.0
∑n-3HUFA
28.7
12.5
33.0
Lipid (%) *1
2.5
2.1
2.9
Protein (%) *1
7.2
5.6
7.8
*1 Wet matter basis; *2 Tr indicates trale level

Results of water quality analysis
Daily changes of NH4 -N, NO2 -N and NO3 -N
concentrations are shown in Fig. 3. After day
21, the concentration of NH4-N in the test tanks
was significantly lower than that in the control
tanks (P＜0.01), except on days 31 and 32. The
average concentration of NH4-N after day 32 in
the test tanks was 1.6 mg/L, while that in thecontrol tanks was 2.2 mg/L. In the case of
NO2-N, its concentration in the test tanks was
significantly lower than that in the control
tanks after day 30 (P＜0.01), except on day 33.
The average rate of increase per day from day
29 to day 40 in the test tanks was 0.064 mg/L,
while that in the control tanks was 0.095 mg/L.
The concentration of NO3-N was about 10 times
higher than that of NH4 -N and NO2 -N during
the experiment in both test and control tanks.

The difference between the concentration of
NO3 -N in test tanks and that in the control
tanks was significantly different after day 18(P＜0.01), except day 21. The average rate ofincrease per day after day 18 to day 40 was
0.545 mg/L in the test tanks and was 1.002
mg/L in the control tanks.
On the other hand, daily changes of PO4 -P
concentration are shown in Fig. 3. No difference between its concentrations in the testtanks and those in the control tanks was
detected from day 10 to day 29. However, thedifference between them gradually became
clear after day 30 (P＜0.01). At the end of theexperiment, the concentration of PO4 -P in thecontrol tanks was about two times higher thanthat in the test tanks.

88

Masanori OKAUCHI

Fig. 3. Daily changes of the average contents of NH4-N, NO2-N, NO3-N and PO4-P in the test tanks(●) and the control tanks(▲). Vertical lines indicate the standard deviations. S-type rotifers were
fed from day 10 to day 20, L-type rotifers were fed from day 20 to day 30, and an artificial dietwere supplied from day 30 to the end of the experiment.

Beneficial roles of N. oculata in fish larval rearing

Discussion
Efficiency of N. oculata to enrich rotifers inlarval rearing tanks
Regardless of the rotifer type, the nutritive
value of rotifers collected from the test tanks
was high comparison with that of rotifers fromthe control tanks. Especially, the EPA and n-3
HUFA contents of rotifers were reduced clearlyin the control tanks. This is concluded to becaused by the deficiency of N. oculata in thecontrol tanks. Both types of rotifer put in thecontrol tanks and their newly hatched offspring were not supplied with alga and as such
had minimal available food materials so that
their n-3 HUFA and protein contents werereduced compared the test tank rotifers. Even
if the larvae are fed such rotifers enough, theirsurvival and growth rates will undoubtedly belower. While, the rotifers in the test tank fed N.
oculata enough, so that it's nutritive value wasenhanced. Thus, the larvae in the test tanks
grew well and their survival rate was high.
Moreover, the rotifers in the test tanks had ahigher rate of egg carrying than that in thecontrol tanks. The amictic reproduction of rotifers would be induced more frequently in thetest tanks, because of the higher food availability in the tanks. Therefore, the addition of N.
oculata seemed to be effective to produce bothnutritive and reproductively active rotifers in
the larval rearing water.
Water quality management by N. oculata
After day 30, the number of dead larvae inthe control tanks became conspicuously higher
than that in the test tanks. However, the same
quantity of artificial diet was supplied to boththe test and control tanks from day 30.
Therefore, there was no difference in the foodsupplied to the test and control tanks. As thecause of larval death in the control tanks, twopossible causes are apparent.
One is the sudden diminution of rotifers in
the rearing water. No rotifers were supplied
into both the test and control tanks after day
30. However, the number of rotifers only89

reduced gradually in the test tanks, because
active reproduction occurred continuously.
Thus, the larvae in the test tanks could eat not
only the artificial diets, but also the rotifers.
While, the larvae in the control tanks after consuming the remaining rotifer ate the artificial
diet only. Therefore, the effect of the additionof N. oculata into the rearing water seemed tocontinue after even changing to the artificial
diet.
Moreover, water pollution was a probablefactor inducing larval mortality. After changing from rotifers to the artificial diet, inorganic nitrogen (NH4-N, NO2-N, and NO3-N) andphosphate (PO4 -P) concentrations increased
both in the test and control tanks. Especially,
they increased rapidly in the control tanks.
One of the reasons for the differences in concentrations of nitrogen and phosphate in therearing water between in the test tanks and in
the control tanks seemed to algal nutrient
absorption. Nannochloropsis oculata absorbed
dissoluble nitrogen and phosphate as nutrientsin the test tanks. Additionally, many larvae
died in control tanks, and their bodies, prior tobeing removed each day would also deteriorate
the quality of the rearing water. Thus, waterpollution seemed to be accelerating in a shot
term. From this point of view, additive N.
oculata was effective.
In an almost similar rearing experimentusing mullet larvae, Tamaru et al., (1994) reported that the NH4-N content in the test tanks
was significantly higher than the control
tanks. They considered that the reason was
contamination from the algal medium, because
they used ammonium sulfate as a nutrient in
the medium. In this experiment, sodium nitrate
was used instead of ammonium sulfate, so thatthe toxicity of unionized ammonia was concluded as negligible. Moreover, N. oculata wasput into the rearing water after the algal
growth reached the stationary phase. At thestationary phase, almost all the nutrients inthe medium were used for the algal growth.
Thus, contamination from the algal medium
would not raise the nitrate nitrogen level in the90

Masanori OKAUCHI

larval rearing water.
A new role of N. oculata for larval rearing
From the results of this experiment, it was
shown that N. oculata has main two roles in
the larval rearing water. The addition of N.
oculata into the rearing water was indispensable to enhance the fatty acid component of rotifers to a level suitable for the fish larvae.
Moreover, the addition of the alga was effective
to reduce the concentrations of the soluble
nitrogen and phosphate. Especially, after feeding with the artificial diet, the concentrationsof NO3 -N and PO4 -P increased remarkably.
However, because the larvae still only had aweak swimming ability, we could not adopt a
continuous flowing system with a high flow
rate. When a semi-continuous changing water
system was adopted, the alga seemed to be useful as absorbing potentially harmful excess
nutrients and contribute to maintain the water
quality management.
In the near future, various kinds of artificial
diets will be used commonly in larval rearing.
Moreover, freshwater Chlorella is now usuallyused in rotifer production. The characteristics
of N. oculata have significant potential to enhance and stabilize production in finfish larval
culture and as such for the effective utilizationof this useful link in the food chain in hatcheryproduction, further detailed research is required.
References
Eda H., Murashige R., Oozeki Y., Hagiwara A.,
Eastham B., Bass P., Tamaru C. S., andLee, C.S., 1990: Factors affecting intensive
larval of striped mullet, Mugil cephalus.
Aquaculture, 91, 281-294.
Folch J., Lees M., and Sloane Stanley G.H.,
1957: A simple method for the isolation andpurification of total lipids from animal
tissues. J. Biol. Chem., 226, 497-509.

Guillard R. R. L., and Ryther J. H., 1962:
Studies of marine planktonic diatoms. I.
Cyclotella nana Hustedt and Detonula
confervaceae (Cleve) Gran. Can. J.
Microbiol., 8, 229-239.
Hirayama K., Maruyama I., and Maeda T.,
1989: Nutritional effect of freshwater
Chlorella on growth of the rotifer
Brachionus plicatilis. Hydrobiologia, 186/
187, 39-42.
Maruyama I., Ando Y., Maeda T., andHirayama K., 1989: Uptake of vitamin B12by various strains of unicellular alga
Chlorella. Nippon Suisan Gakkaishi, 55,
1785-1790.
Maruyama I., Nakamura T., Matsubayashi T.,
Ando Y., and Maeda T., 1986: Identificationof the alga known an marine Chlorella
as a member of the Eustigmatophyceae.
Jap. J. Phycol. (Sorui ), 34, 319-325.
Murashige R., Bass P., Wallace L., Molnar A.,
Eastham B., Sato V., Tamaru C. S., and
Lee C. S., 1991: The effect of salinity on thesurvival and growth of striped mullet,
Mugil cephalus, Larvae in the hatchery.
Aquaculture, 96, 249-254.
Strickland J. D. H., and Parsons T. R., 1972: A
practical handbook of seawater analysis.
Bull. Fish. Res. Bd Can., 167, 310pp.
Tamaru C. S., Murashige R., and Lee C. S.,
1994: The paradox of using background
phytoplankton during the larval culture of
striped mullet, Mugil cephalus L.
Aquaculture, 119, 167-174.
Yoshimura K., Usuki K., Yoshimatsu T.,
Kitajima C., and Hagiwara A., 1997:
Recent development of a high density massculture system for the rotifer Brachionus
rotundiformis Tschugunoff. Hydrobiologia,
358, 139-144.
Watanabe T., Kitajima C., and Fujita S., 1983:
Nutritional value of live food organisms
used in Japan for mass propagation offish: a review. Aquaculture, 34, 115-143.

水研センター研報，別冊第 1 号，91−100, 平成16年
Bull. Fish. Res. Agen. Supplement No. 1, 91-100, 2004

91

Integrating Intensive Aquaculture of the Red Seaweed
Chondracanthus exasperatus
J. Robert WAALAND*

Abstract Washington State has a significant history of experimental seaweed
aquaculture. Early experiments involved the carrageenophytes Mazzaella splendens andChondracanthus exasperatus in both open water net culture and semi-closed tank systems on land. Later, net culture of Porphyra for nori and long line culture of the edible
kelps Nereocystis and Macrocystis were tested successfully. Further development of theseculture systems was halted due to combinations of market, regulatory, political and social considerations. When a Seattle company developed a high value product from theTurkish Towel Seaweed, Chondracanthus exasperatus, there was renewed interest in intensive tank and pond based aquaculture because Washington has a long term moratorium on commercial seaweed harvesting from wild seaweed populations. The initial
phase of this research was conducted at Mukilteo, Washington, where strategies forlong term cultivation in tanks were tested, and a new custom cultivation tank design
was developed for pilot scale cultivation research at a larger site on the shore of Clam
Bay near Manchester, Washington. Long term cultivation is now being tested in tanks
of up to 5,000L volume supplied with natural seawater, nutrient supplemented seawater,and seawater effluent from nearby fish culture tanks. Seawater from Clam Bay is naturally rich in nutrients from tidal driven upwelling and nearby commercial salmon
aquaculture operations. Supplemental nutrients (commercially available "f/2" enrichment and agricultural fertilizers) and halibut culture tank effluent have both been tested
for their ability to support C. exasperatus growth with relatively low seawater turnoverrates. Compared to seawater at the Clam Bay site, halibut tank effluent differs in bothnutrient composition and quantities. Initial results indicate that halibut tank effluent isa satisfactory source of nutrients for C. exasperatus in intensive culture and that thisseaweed scrubs significant quantities of nutrients from halibut tank effluent, especiallyammonium. Recent experiments with several bioreactor designs have investigated theculturing of C. exasperatus at very high loading densities in recirculated natural and artificial seawater in both submerged and spray culture.
Key words: seaweed, red algae, Chondracanthus, aquaculture

Introduction
Washington State has a history of experimental seaweed aquaculture. In the 1970s net
and tank cultures of the carrageenan producing red seaweeds Mazzaella (then known as

Iridaea) and Chondracanthus (then known as
Gigartina) were tested. In the 1980s, the emphasis shifted to Porphyra species, both
Japanese and Washington species which were
cultivated on raft nets to produce edible nori
(Mumford et al., 1985; Merrill & Olson, 1988).

2003年 6 月12日受理（Received on June 12, 2003）* Department of Biology, University of Washington, Seattle, Washington 98195, USA Email: jrw@u.washington.edu

92

J. Robert WAALAND

Late in the 1980s, long line cultivation of thekelps Nereocystis (as a wakame substitute) andMacrocystis (for the herring roe on kelp fishery) were tested on long lines (Merrill, 1989).
Recentlyinterest
incultivationofChondracanthus exasperatus was renewed
when a Seattle company discovered and developed a high value cosmetic product from thisseaweed. Since Washington State has a moratorium on commercial seaweed harvestingfrom natural populations and harvest limits
elsewhere in this species' range limit harvests
from the wild, aquaculture was viewed as thebest option for obtaining raw material to support this developing industry. As the earlier
open water aquaculture activities had elicitedconsiderable opposition from shoreline property owners, open water cultivation was notconsidered a viable option. Therefore, intensive
tank or pond cultivation was viewed as the best
option for obtaining a sustained raw material
supply to support this new industry.
Furthermore, intensive aquaculture offers opportunities for optimizing product yieldthrough strain selection, genetic manipulation,
control of certain growth parameters and protection from pests and competition. A joint university, industry and agency project was
initiated to develop this option.
In earlier research, both open water net cultivation and tank culture of Chondracanthus
exasperatus had been tested on a limited basis
as Mazzaella splendens (as Iridaea cordata) was
the species which received the most attention in
the 1970s research (Waaland, 1973, 1976). Whatwas known was that C. exasperatus exhibited
dependable growth in tank culture and could becloned and propagated perennially from vegetative fragments. Additional data were available about loading densities, seawater turnoverand mixing required for sustainable growth inintensive tank culture (Waaland 1977).
This report includes both field and laboratory aspects of recent research which has progressed through three phases. The first phaseinvestigated strategies for long term maintenance of seaweed stocks and exploredexperimental and pilot scale tank designs forcultivation of C. exasperatus. The second phasefocused on increasing stock quantity and quality by selection and management of growth parameters and integrating water from fish
(Pacific Halibut) culture tanks. The third andmost recent phase has emphasized reducing
water use and pumping through recycling andspray culture.
Methods
The Chondracanthus exasperatus (Turner &Bailey) J. Hughey plants used to initiate theseexperiments were obtained from natural populations at Clam Bay near Manchester,
Washington in Sept. 1999. After the initial collection, most material used in large-scale experiments came from the tank cultures withoccasional use of freshly collected wild plants.
In certain smaller scale laboratory and field
experiments, plants from uni-algal laboratory
experiments were sometimes used. These weretypically maintained in natural seawater enriched with commercially available Guillard's
f/2 enrichment (Kent Co. marketed by AquaticEcosystems), grown in controlled environment
chambers at 15℃ with irradiance of 〜50μE･
m−2 ･ s−1 from cool white fluorescent lamps(Merrill & Waaland 1979). In many experiments, artificial seawater (Instant Ocean R ,Aquarium Systems Inc., Mentor, OH) madewith reverse osmosis water to salinity 30o/oo(typical of Puget Sound) and supplemented
with Guillard's f/2 enrichment (Kent Co.
chemicals as above) was used successfully.
Outdoor Experiments
Several types of tanks were used dependingon the experiment. The tanks at the first outdoor site, Mukilteo, Washington were cylindrical fiberglass fish culture tanks 1.2m diameter,
1.0m deep, volume 1500L, with a center drain(Fig. 1). Water motion was provided by a central aerator.
At the Manchester, Washington site, mosttanks were horizontal half cylinders with

Intensive Chondracanthus Aquaculture

hemispherical ends (4.7m long, 1 m deep, 1.5m
wide, 5500L volume) with a well screen equippeddrain near each end (only one drain was active,
the other was used for instruments, cross connecting tanks and other purposes) (Fig. 2). A
longitudinal aeration pipe circulated theseawater and seaweeds. Smaller versions ofthese tanks were used in a few experiments. An
array of ten 75L semi-square polyethylenetanks was used for small scale field experiments; they were equipped with well screen center drains and central aeration (Fig. 3).
Seawater was pumped from an intake on a
nearby pier (visible in background in Fig. 3). At
the Manchester site, effluent seawater from
Pacific Halibut culture tanks was also available. Typical salinity is 28-30o/oo at these sites.
Typical tank culture conditions involved ambient daylight and ambient temperatures of thepumped seawater. At this latitude (〜47 °N),
winter days are short (〜8.5 hr light) and often
cloudy and summer days long (16 hr light).
Pumped seawater temperatures ranged from 46 ℃ in winter to 14-15℃ in summer. Solar heating may raise water temperatures one or two
degrees in large tanks depending on flow rate.
Light and temperature in or near the largetanks were monitored with data loggers (Onset
Computer Corp.). Other experimental details
will be given with each type of experiment.
Nutrient analyses (nitrate, nitrite, ammonium,
phosphate) were performed by the Marine
Chemistry
Laboratory,
Department
ofOceanography.
Greenhouse Experiments
In the greenhouse, plants were housed in an
hexagonal plexiglass (0.50m long×0.45m wide,
100L volume aquarium) turned on its side andfitted with a plastic mesh platform to support
the plants and equipped with drain openings
and a removable panel for sealing the opening
and providing for sea water supply and drain
pipes (Fig. 4).
Plastic spray nozzles were connected to an
external polyethylene reservoir recirculating
80L of UV sterilized (QL-25, Rainbow

93

Fig. 1. Vertical cylindrical tanks used at Mukilteo
field station

Fig. 2. Horizontal half cylinder tanks used at
Manchester field station

Fig. 3. Semi-square tanks used for outdoor culture at
Manchester and indoor spray culture in controlledenvironment room

94

J. Robert WAALAND

Aquarium Systems), 35 μm filtered (Aquatic
Ecosystems VF-125), and chilled sea water. The
chiller (Aqualogic 0.23Kw) was equipped with atitanium heat exchanger. The seawater medium
was
pumpedat
approximately
12-15L･min−1 through the spray nozzles. The
chiller maintained the seawater at temperatures between 10-15℃depending on the experiment. From late spring through mid autumn,
the greenhouse was covered with 30％ shade
cloth to reduce the solar heat load. In addition
to the greenhouse shade cloth, plastic window
screen often was used as a neutral density filteron the tank. The ambient light is supplemented
on cloudy days and daylength extended in winter with 600W high pressure sodium greenhouse lamps. Data loggers (Onset Computer
Corp.) were used to track temperature andlight in this system. This culture unit has arelatively low density of seaweed per seawater
volume because of the volume needed to cover
the chiller probe in the reservoir. The large volume of chilled medium also adds a brief periodof buffer time to react to failure of the coolingsystem in the high ambient heat of the greenhouse environment. The unit has operated satisfactorily for months at a time with weekly
shut offs to remove the plants for weighing.
Typical Operating Conditions:Light: ambient greenhouse, shading in summer, 〜150μE･m-2･s-1

Temp: 10-12℃
Nutrients: 0.1×f/2 (low biomass/medium volume)
Seawater: replaced 〜7-8weeks
Pumping rate: 〜12-15L･min-1 (for spray)
Growth rate: 〜4-5％ d-1

Fig. 4. Hexagonal chamber used for spray culture ingreenhouse environment

Fig. 5. Rectangular plastic tanks used in controlled

Controlled Environment Rooms
In controlled environment rooms, two typesof tanks were used for most experiments: 320L
rectangular polyethylene tanks (1.0m ×0.67m
× 0.65m) (Fig. 5) and 0.6m × 0.6m, 75L
semisquare tanks (described above) equippedwith a plastic screen platform to support theplants and using a recirculating pump (20L in
circulation), 25 watt UV sterilizer (25 watt) and
35μm particle filter and plastic lawn sprinkler
spray nozzles attached to a distribution manifold (Fig. 6). In the controlled environment
rooms, the temperature of the circulatingwater was maintained in a range (10-15℃) encountered by C. exasperatus in natural communities in the Puget Sound region during spring,summer and early autumn.
The 320L rectangular polyethylene tanks
were used primarily as holding tanks forplants to be used in other experiments.
Nevertheless, they demonstrated that highdensities of plants may be maintained for up to
16 months in batch culture with little seawater

environment room

95

Intensive Chondracanthus Aquaculture

turnover (once every 3-6 months) provided thatmineral nutrients are replenished and salinity
controlled (by addition of reverse osmosis
water) as required. For faster growth, additionof carbon dioxide (via a pH controller andsparger) resulted in higher growth rates.
Particle filtration (35μm) and UV sterilization
(25
watt)
were
essential
tocontrolphytoplankton species in such a system and to
reduce the survival of spores of competing
seaweeds (e.g., Ulva and Enteromorpha, etc.)
which might be circulating in the system, introduced with the C. exasperatus from natural
populations. Growth rates up to 5 ％ d-1 day
were observed in this system. It would be relatively simple to integrate this type of culture
system with a finfish or shell culture system.
Laboratory Benchtop Bioreactor
Cytolift R Bioreactor (Kontes Glass Co.) vessels were used for the most intensely monitored
experiments (Fig. 7). These are cylindrical, water-jacketed bioreactors with an internal vol-Fig. 7. Cytolift R bioreactor used in laboratory

ume of 〜500mL. Water circulation was provided by a multi-channel peristaltic pump(Cole-Parmer/MasterFlex
Model
7553-70).
Seawater was chilled in a countercurrent heatexchanger chilled by a 0.12Kw Lauda K-2/R
chiller
circulating
chilledtap
water.
Circulating seawater was UV treated by circulating the water through quartz tubing in a cylindrical aluminum chimney housing a 25 WattUV lamp. A computer interfaced data logger(pH, dissolved oxygen, temperature and light)
and controller (Remote Measurement Systems,
Inc., "EnviroMac" unit) was used to monitor experimental conditions and to add CO2 as theplants consumed it via photosynthesis.
An Olympus 620L digital camera was used torecord the appearance of individual tagged
plants at weekly intervals. Fresh weights were
measured after plants were drained and blotted.
Results
The results presented here are representativeof the performance, as measured by relative
growth rate, of plants raised under the conditions specified for each series. These represent
the potential performance of such systems but
do not detail experiments that were not productive.

Fig. 6. Semi-square tank with recirculating pump,
UV sterilizer and particulate filter as used for spray
culture in controlled environment room

Outdoor tanks
At present,

the

large

outdoor

tanks

96

J. Robert WAALAND

Fig. 8. Summary graph for Mukilteo tank array

Fig. 9. Summary graph for Manchester tank array

Intensive Chondracanthus Aquaculture

represent the most realistic option for pilot or
small commercial scale production. Several
years of experience have been obtained encompassing all seasons and a variety of weather
conditions (from September 1999 through lateAugust 2000 at Mukilteo and late August 2000
through mid-June 2001 at Manchester for our
experiments and subsequently to the present
by Söliv personnel at Manchester).
A summary of production in the Mukilteo
tanks is seen in Fig. 8. A similar summary for
the Manchester large tank array is seen in Fig.
9.
For some experiments some or all of theManchester tanks were supplied with effluent
water from adjacent halibut rearing tanks.
Fig. 10 shows the ammonium supplementationthat occurred as a result of the halibut in thewater and the reduction in ammonium that occurred as a result of C. exasperatus growing in
the water.
Greenhouse experiments
Several tank and container designs were
tested in greenhouse conditions, but only one isshown here, the hexagonal enclosure used forspray culture (Fig. 4). Early experiments did
not use particle filtration or UV sterilization of
the medium. Such filtration (to prevent nozzle

97

clogging) and sterilization (to inhibit epiphyteand phytoplankton growth) proved essential
for long term operation (months) of culture
units using recirculated medium. Without suchtreatment, diatoms, green flagellates andulvoids were recurring problems. Typical operating conditions for the recirculating hexagonal enclosure system were:Light: 150 μ E ･ m-2 ･ s-1 (ambient greenhouselight, shaded and/or supplemented
with sodium vapor lamps)
Temp: 12℃
Nutrients: 0.15×f/2/week
Seawater: replaced 〜every 8-20 weeks
Pumping rate: 12L ･min-1 for circulation andspray operation
Growth rate: 〜1-2％ d-1
A representative plant growing in this system
is shown in Fig. 11.
Controlled Environment Room Experiments
Controlled environment rooms provide a convenient way of maintaining seaweed cultures attemperatures similar to those of their naturalenvironment. UV sterilization of the seawater
medium pumped using an airlift system,
proved essential to prevent growth of competing algae (e.g., diatoms, green flagellates andulvoids). With a pH controller to add carbon di-

Fig. 10. Seawater and halibut tank inflowing and effluent water. Samples were taken near mid-day. Loading
density was as shown. Note the preferential use of ammonium over nitrate. Plants were actively growing although the plants in Tank 1 were at a very high density and may have been light limited compared to those in
Tank 3

98

J. Robert WAALAND

Fig. 11. Representative plant grown in spray culturein hexagonal enclosure in greenhouseoxide as the pH rose above 8.2 and mineral nutrient supplementation by periodic additions of
f/2, it was possible to maintain plants in an actively growing state at very high densities forseveral months in the same batch of seawater.
Typical operating conditions for the 320L tanks
follows:
Light: 150μE･ m−2 s−1 (metal halide and coolwhite fluorescent lamps; 16 hr L: 8 hr D)
Temp: 12℃
Nutrients: 0.15×f/2/week
Seawater: replaced 〜every 8-20 weeks
Pumping rate: aeration for circulation, air lift
pump for UV sterilizer
Growth rate: 〜1-2％ d-1
Semisquare Spray Culture System
This system has a very small volume ofwater (〜20L) circulating in a chamberequipped with a plastic mesh rack to support
plants and plastic spray nozzles to keep theplants damp and supply mineral nutrients.
This system circulates the seawater medium
through a UV sterilizer to inhibit competingalgae and a particle filter which prevents fouling of the spray nozzles and also removes competing algae. This system has proved quite
successful.
Typical Operating Conditions:Light: 150μE･ m−2 s−1 (metal halide and coolwhite fluorescent lamps; 16 hr L: 8 hr D)
Temp: 12℃
Nutrients: 1.5×f/2/week
Seawater: replaced 〜every 4-10 weeks

Fig. 12. (Top): Representative plant ER-3 grown inspray culture in controlled environment room
(Bottom): Representative plant 02-05-31 growing inbenchtop Cytolift Bioreactor

Pumping rate: 〜12L/min for spray
Growth rate: 〜4-5％/dA representative plant is shown in Fig. 12 (top).
Cytolift Bioreactor
The Cytolift R Bioreactor units have a very
high plant density per volume of circulating
medium. The temperature and light monitors
mainly reported on the functioning of the lamp
timer and circulating chiller. The pH monitor
could add CO2 to the closed system via a low
volume pumping system. The oxygen monitor
was useful only when plants were entirely submerged with no air space to provide an oxygen
reservoir and sink. Most useful for these experiments was the pH monitor and regulator as
it provided rapid feedback and also compensated for carbon dioxide uptake by rapidly
growing plants. Mineral nutrient additions
were done manually with the frequency andamount depending on the experiment being
conducted. Similar growth rates are obtainedfor immersed or emersed plants. A representative plant is shown in Fig. 12 (Bottom).
Typical Operating Conditions:Light: 150μE･m−2s−1 16L: 8D & 20L: 4D (fluorescent)Temp: 15-20℃
Nutrients: pH maintained at 8.0-8.2; f/2 enrichment 1.2×per week (proportional to biomass)
Seawater: replaced 〜every 4 weeks
Pumping rate: 〜0.2L/min
Growth rate: 〜4-5％/d99Intensive Chondracanthus Aquaculture

Discussion and Conclusions
This report describes several scales of culture
method for use with the red seaweed
Chondracanthus exasperatus. Many otherseaweeds are likely to flourish in such systems
as well. The larger scale flow through outdoor
systems are presently used as a pilot scale research system for commercial production associated with a high value product extracted
from Chondracanthus. The smaller scale experimental systems can be modified for immersed or emersed culture of this seaweed andprobably other seaweeds. All the tested systems offer opportunities for reducing the volume of seawater used. All the laboratory scale
systems have been successfully tested withboth natural and artificial seawater medium.
Recirculation offers significant economies in
reduced pumping and materials handling costs.
All tested systems benefit from nutrient supplementation, particularly at low seawater
turnover rates. Mineral nutrient supplementation is essential in low volume and/or turnoversystems to maintain plant growth. Carbon dioxide supplementation improves growth rate
where CO2 limits growth as it does in all thesesystems as shown by pH monitoring and CO2
supplementation. These systems offer many
opportunities for integrating seaweed culture
with finfish or shellfish culture to use theseawater more efficiently and to benefit fromthe seaweed's extractive metabolism in removing nitrogenous compounds from the animal
culture effluent. With appropriate integration
with fossil fueled power plants, seaweeds may
also contribute to carbon dioxide scrubbing
from the flue gases. The effectiveness of suchintegration will likely depend on seasonal effects on growth in outdoor systems. One of thelarger challenges in such integration will likely
be obtaining rapid feedback on the mineral nutrient demands of the seaweeds. While pH provides rapid and convenient feedback on carbon
dioxide uptake, methods for similarly rapid
analysis (i.e., sufficiently rapid to supplement
the limiting nutrient[s] within a few hours) of

the numerous mineral nutrients that might
limit seaweed growth in a closed or semi-closed
system are either non-existent or very expensive.
Acknowledgements
Financial support and facilities access forthis research was provided by NOAA/NMFS,
Washington
Sea
Grant,
Washington
Technology Center, Söliv International Corp.,
and the University of Washington. The research benefited greatly from the ingenuity
and sustained effort, often under cold and wet
conditions from the sustained efforts ofE.W.("Pete") Duffield, E.C.S.("Ellie") Duffield,
M. Costanza, K. Cooley, M. Brockington, D.
Boratyn, C.T. Jensen, and E. Mahler.
References
Merrill J. E., 1989: Cultivation of bull kelp inWashington State, USA. Appl. Phycol.
Forum, 6(3), 6-7.
Merrill J. E. and Olson J. R., 1988: The firstcommercial-scale nori sea vegetable farmin North America, Aquaculture International
CongressandExposition,
Vancouver, B. C., Canada, Sept. 6-9, 1988,
34pp.
Merrill J. E. and Waaland J. R., 1979:
Photosynthesis and respiration in a fast
growing strain of Gigartina exasperata
Harvey & Bailey. J. Exp. Mar. Biol. Ecol.,39, 281-290.
Mumford T. F., Jr., Waaland J. R., Dickson L.
G., and Melvin D. J., 1985: Porphyra
aquaculture in the Pacific Northwest. J.
Phycol. 21(suppl.), 7
Waaland J. R., 1973: Experimental studies on
the marine algae Iridaea and Gigartina. J.
Exp. Mar. Biol. Ecol., 11, 71-80.
Waaland J. R., 1976: Growth of the red alga
Iridaea cordata (Turner) Bory in semiclosed culture. J. Exp. Mar. Biol. Ecol., 23,
45-53.
Waaland J. R., 1977: Growth of Pacific

100

J. Robert WAALAND

Northwest marine algae in semi-closed culture, in "The Marine Plant Biomass of the
Pacific Northwest Coast" (ed. by KraussR.), Oregon State University
Corvallis, Oregon, pp. 117-137.

Press,

水研センター研報，別冊第 1 号，101−109, 平成16年
Bull. Fish. Res. Agen. Supplement No. 1, 101-109, 2004

101

Economic value of tideland as place for recreational clam digging,a case study at Kajishima Island
Yasuji TAMAKI*

Abstract Clam digging produces large revenue for fishery cooperative associations andproduces a large additional income to fishermen. Although many urban residents enjoy
clam digging, an evaluation of the economic value has not been carried out until now.
Therefore, I estimated the recreational benefits of clam digging by the travel cost
method by using the embarkation lists of the ferryboats for recreational clam digging
visitors at Kajishima Island, Kira Town. The results totaling 35.65 million yen were calculated as the recreational benefits of Kajishima Island's surroundings of about 6 hafrom the clam digging bed. This amount with Manila clam fishing amount of the Kira
Fishery Cooperative Association of 38 million yen. It is evident that urban residents
gained a large benefit from recreational clam digging. Mitigation by artificial tidal landis necessary for the tidal land lost by land reclamation as a future policy.
Key words: clam digging, recreational benefits, travel cost method

Among various important uses of tidelandsuch as purification of water and nursery ofaquatic animals, the function as a place for recreation and tourism should not be disregarded.
Clam digging has been traditionally major recreation performed on tideland in Japan. Manila
clam is dominant species caught by recreational clam digging. However, the catch of
Manila clam in Japan by commercial fisheries
has been decreasing recently and recreational
clam digging is no longer carried out in many
areas depending on only local resources. Many
fishermen's cooperative associations are releasing recently seeds of Manila clam along theircoast to compensate the decrease, and to continue clam digging habit. Under this situation,
estimation of economic value is becoming important though there is no research on the economic value of clam digging except the report
by Aoyama et al. (1996), which considers thevalue from the view point of water purification

function. In this study, I estimate the economic
value of clam digging in Kajishima Island as acase study.
1. Present status of clam digging in KajishimaIsland.
Kajishima is located in Mikawa Bay facing toMiyazaki Port, Kira City, Aichi, Japan. The
shore line of the Kajishima Island is 1.8 km andthe distance between Miyazaki port andKajishima Island is 1.5 km. The nearest largecity is Nagoya City and distance between
Miya-zaki Port and Nagoya is 50 km and 1.5
hours by car. The shore where clam digging ispossible is about 2/3 of the circumference of theisland. An area of the clam digging ground isestimated at about 6 hectares. Most of clam
digging grounds of this island are shores whichhave many stones instead of a tideland of asandy area. Manila clams live in the sand which
occurs between these stones (Fig. 1). Clam

2003年 6 月12日受理（Received on June 12, 2003）* National Research Institute of Fisheries Science, Fukuura, Kanazawa, Yokohama 236-8648, Japan

102

Yasuji TAMAKI

digging in Kajishima Island is administrated
by Kira Fishermen's Cooperative Association(KFCA). KFCA operates 14 small trawl net
fishing boat as transportation between Miyazaki Port and Kajishima Island during the season. The price of round ticket by boat between
Miyazaki port and Kajishima is 1,100 yen andtourist for clam digging in Kajishima Island
pay 1,200 yen as a charge for clam digging to
KFCA. The passenger on the boat has obligation to fill up the passenger list with theirname and address. A net is handed to a tourist
as the payment of clam digging charge and a
tourist can catch the clam up to the limit of thevolume of the net. A net can accommodate
about 10kg of clam.
Aside the income of clam digging charge,
KFCA collect 8 ％ of the boat charge, 5 ％ ascatch commission and 3 ％ as Manila clam seed
price from the captains of trawl net fishingboats.
2. Present status of Manila clam fishery and recreational clam digging
Aichi prefecture had recorded the highest
catch among prefectures in Japan for 14 years
until 2000 except 1995 (Fig.2). The amount of
the catch by Manila clam fisheries in Aichi
Prefecture decreased after the peak in 1989
(Fig.3). Table 1 shows the number of people
who visited shore of prefectures for recreational clam digging from fisheries census in
1998. Nine hundred and ninety five thousand

Fig. 1. Kajishima-island clam digging spot

people visited the shore of Kanagawa
Prefecture and this was the highest record ofvisitors in 1998. Less than half of the highest
record visited to coast of Aichi Prefecture(424,000). This number attributes to 10 ％ of
total number in Japan. Recreational clam digging in Aichi is supported by fishermen's cooperative
associations. There are many
fishermen's cooperative associations that havethe section for recreational clam digging service. They release 18×10 8 Manila clam seeds (57％ of total released seed in Japan) for stock enhancement and more than 80 ％ of tourist whocame to shore of Aichi for clam digging used
the guidance by fishermen's cooperative associations (Table 2).
Table 3 comes from investigation of fishermen's cooperative associations. Table 3 is showing management rules and present status ofclam digging controlled by 13 fishermen's cooperative associations in central part of Mikawa
Bay, from Gamagouri City to Isshiki Town.
The seasons for recreational clam digging andnumber of visitor differ among fishermen's cooperative associations. The lowest number ofvisitors is 679, and highest number of visitors
is 70,000. The quantity of released seed ranged
Table 1. Number of clam digging visitors
Prefecture
Name

Numberofclam Number of clam digging
visitors who used guiddigging
ance of fishermens' coopvisitors
erative associations(total)Kanagawa

995,000

5,000

Mie

734,800

260,500

Chiba

652,800

480,800

Aichi

424,100

395,200

Ibaraki

396,600

0

Okinawa

178,000

1,600

Hyogo

167,300

138,700

Hiroshima

117,900

26,100

Shizuoka

117,000

74,300Kagoshima

103,200

0

Wakayama

86,70082,800Oita

79,60021,000Osaka

64,3000

Kumamoto

54,7009,100

Source: Fishery Census (1998)

Economic value of tidelands as place for recreational clam digging

from 1 to 126 ton. The coefficient of correlation
between the number of visitors and the quantity of seed released was high with 0.888. Inother words places with many visitors correlate with high seed release. The charge for103

adult varies from 900 to 1,400 yen. The highest
price is 2,300 yen when the ferryboat charge isadded. The upper limit of catch allowed to visitor is from 2 to 10kg, and some places are allowed to catch clams without limit.
MethodFig. 2. The change of total catch by Manila clam
fishery in Japan
Source: Fishery Statistics

Fig. 3. The change of total catch by Manila clam
Fishery in Aichi
Source: Fishery Statistics

Table 2. Number of Manila clam seed released
Prefecture Name

1998 (billion)

Aichi

18.08

Mie

2.9

Chiba

2.43

Yamaguchi

1.88

Kumamoto

1.48

Fukuoka

1.24

Oita

1.07

Shizuoka

0.9

Nagasaki

0.68

Miyagi

0.55

Fukushima

0.21

Hiroshima

0.08

Hyogo

0.06

Ehime

0.03

Others0.09

Source: Fishery Census (1998),

I estimate economic value of recreational
clam digging for KFCA and fishermen whocarry visitor by fishing boat. I estimate recreational benefits of recreational clam digging for
visitors by using travel cost method. The passenger list of boat transportation between
Miyazaki Port and Kajishima Island was usedin the estimation of number of visitor andspecification of address of each visitor. I estimate travel cost (TC ) of each visitor by summing up their monetary expenses and time
expenditure. In the estimation of travel cost,
necessary time and distance were calculated byassuming that each visitor came from theirmunicipality office and they used toll way
when the distance exceed 100 km. In the estimation of traffic expenses, rate of fuel consumption is 15 yen a km. Monetary expenses include
a traffic expenses, a toll, the price of roundticket by boat between Miyazaki Port andKajishima and a charge for clam digging to
KFCA. In the estimation of time expenses, opportunity expenses of round trip and clam digging were calculated by using of average wages
rate. I estimate visit rate (V ) by using each
population of municipality and visitor's number of each municipality. I estimate relational
expression between TC and V. I estimate visitor's number of each municipality by using thisrelational expression and TC. I sum up by 500
yen to the TC of each municipality until visit
rate down to 0. I sum up visitor's number of
each municipality by an additional expenses(TC' ). I calculate acceptable rate (V' ) of eachTC'. I estimate relational expression between
TC' and V'. I can find the visitor's average recreational benefit by integrating this equation.

104

Yasuji TAMAKI

Table 3. Aichi clam digging enforcement situation comparison
LimitaCharge
ChargeLimiFerryPeriod fortionoffor adult
for child tation of boat
clam digcatch for
(yen/
(yen/
catch for charge
ging
in
adult
indiv.
indiv.
child (kg/ (yen/
2002
(kg/
/day)
/day)
indiv.)
indiv.)
indiv.)

AmountAccommoNumberof Manila
Chargedationof visitor
clam seed
for parknumberayear
releaseding
of a park(2000 or(ton/(yen/car)
ing
2001)
year)

A 2/28〜6/27

1,200

5

600

2.5

-

B 2/28〜6/27

2,000

5

1,000

2.5

800

3.2

C 3/28〜6/16

900

2

900

2

-

60.8

D 3/1〜5/30

1,200

4

700

2

-

13.0

80

0

2,602

E 3/17〜7/29

1,400

4

700

2

-

126.0

2,000

0

70,000F 3/17〜7/29

2,100

4

1,400

2

700

18.0

-

-

10,000G 3/1〜7/28

1,400

4

700

2

-

28.0

300

0

9,482

H 2/28〜6/25

1,400

10

700

5

-

46.0

500

0

3,300

I

2/28〜6/23

2,300

10

1,500

5

1,100

50.0

-

-

11,000J

3/14〜6/16

1,300 unlimited

700 unlimited

-

60.3

500

0

15,263

K 3/1〜6/29

1,000 unlimited

500 unlimited

-

8.5

1,000

0

10,335

L 4/beg.〜6/beg.

1,000 unlimited

500 unlimited

-

2.0

1,000

0

2,000

M 3/16〜5/31

1,200

600

40.0

-

-

4,700

5

3

1,600

1.0

150

0

679

-

-

1,096

400 400〜500

25,000Source: Information from fishery cooperative associations

Results
1. Economic value of recreational clam digging
for KFCA
The fiscal year of the KFCA begins in May
and is over in April, the season of clam digging
is divided into two financial years. The incomeof the KFCA in 2001 was 14.66 million yen fromthe recreational clam digging visitors and 1.43
million yen from the fees from the ferryboat
fishermen. As for the outgoing of the KFCA,
the Manila clam seed price for release was thebiggest expenditure with 6.25 million yen, andwages were 490 thousand yen, and the enterprise profit that subtracted the outgoings fromthe incomings was 9.36 million yen (KFCA,
2001)(Table 4). In addition, a subsidy of about 3
million yen is expended to the seed price from
Kira Town.
2. Economic value of recreational clam digging
for fishermen who ferry visitor by fishing boat
Clam digging was carried out for 32 days
from 24 March to 24 June in 2001 in KajishimaIsland. The number of embarkation persons
last year (2001) was 7,276, there was about 8

Table 4. An enterprise effect by recreational clam
digging in the Kira Fishermens' Cooperative
Association from 1 May 2000 to 30 April 2001
(units: million yen)
Income
The income from recreational digging

14.66

The income from the ferryboat fishermen

1.44

Expenses
Seed release expenses

6.25

Wages for watchmen

0.49

Profit9.36

Sources: KFCA, 2001 and hearing investigation from KFCA

million yen income for fishermen from adultrecreational diggers. Fishermen paid 8 ％ of income to the KFCA. And it was 525,971 yen income for a vessel a season.
3. Economic evaluation of the recreational benefits for visitor from recreational clam digging inKajishima Island by travel cost method
Clam digging visitors came from 17 prefectures, but 88 ％ were from Aichi Prefecture(Table 5). Nagano and Gifu accounted foraround 4 ％. In Aichi Prefecture, Kira Town occupy 11 ％, and Okazaki City 10 ％, Nagoya

105

Economic value of tidelands as place for recreational clam digging
Table 5. Clam digging visitors from various prefectures

Table 6. Clam digging visitors by municipality of
Aichi Prefecture

Prefecture
People
Total
7,276
Aichi
6,432
Nagano
312
Gifu
261
Mie
62
Shizuoka
50
Yamanashi
28
Kanagawa
22
Ishikawa
15
Tokyo
14
Osaka
5
Saitama
4
Niigata
4
Shiga
3
Fukui
3
Kyoto
2
Gunma
2
Chiba
2
Unknown
55
Source: Embarkation list of 2001

Municipality
PeopleTotal for Aichi Prefecture
6,432
Kira Town
710
Okazaki City
645
Nagoya City Minato Ku
459
Nishio City
453
Gamagoori City
342
Toyota City
310
Anzyou City
278
Hekinan City
177
Tiryu City
167
Hazu Town
163
Handa City
152
Kasugai City
147
Kariya City
144
Nagoya City Midori Ku
132
Toyohashi City
126
Nagoya City Nakagawa Ku
119
Nagoya City Minami Ku
99
Kisogawa Town
87
Toyoake City
84
Ohbu City
80
Nagoya City Kita Ku
72
Tohkai City
69
Kohta Town
64
Isshiki Town
63
Chita City
60
Ichinomiya City
59
Nagoya City Tenpaku Ku
59
Taketoyo Town
57
Nagoya City Moriyama Ku
56
NagoyaCity Mizuho Ku
56
Komaki City
53
Miyoshi Town
51
Others of Nagoya City
266
Others of Aichi Prefecture573
Source: Embarkation list of 2001

Percent
100.0
88.4
4.3
3.6
0.9
0.7
0.4
0.3
0.2
0.2
0.1
0.1
0.1
0.0
0.0
0.0
0.0
0.0
0.8

City Minato Ku 7 ％, Nishio City 7 ％,Gamagoori City 5 ％, Toyota City 5 ％ rank
high (Table 6).
(1) Monetary expenses
I include the clam digging charge of 1,200
yen, ferryboat charge of 1,100 yen and traffic
expenses for monetary expenses. I could specify
7,221 addresses that came from 187 municipalities from the embarkation list. The measurement of distance from each municipality's
government office to the Miyazaki Fishing
Port was taken from the motoring distancewith commercial map software. The measurement of money of road toll uses the map software, too. Because I used adult charge, it iscalculated to raise it slightly because there
were some children diggers. In addition, because for the embarkation person from Kira
Town, as many visitors from Miyazaki District
traveled on foot no charge for transportation
was assumed and I assumed that visitors fromother districts came by car and used the distance from a Kira Town Government Office toMiyazaki Fishing Port. Family groups were assumed to travel together and the expenses

Percent
100.0
11.0
10.0
7.1
7.0
5.3
4.8
4.3
2.8
2.6
2.5
2.4
2.3
2.2
2.1
2.0
1.9
1.5
1.4
1.3
1.2
1.1
1.1
1.0
1.0
0.9
0.9
0.9
0.9
0.9
0.9
0.8
0.8
4.1
8.9

averaged for the number of people and, about
all the municipalities, calculated the amount of
average one person and weighted average ofthem and calculated the average transportation
expenses for each municipality. By the travel
cost method, it does not exclude a person having other purpose of trip, and thus it may overestimate. However, the outskirt of KajishimaIsland and Miyazaki Fishing Port do not haveany other big recreation facilities elsewhere. I
judged the purpose of embarkation visitors
only for clam digging so that it was necessary

106

Yasuji TAMAKIfor visitors who gathered clam at low tide to
take home live clams with them because mostvisitors return home after clam digging immediately.
(2) Time expenses
I measured tour time to the Miyazaki
Fishing Port from the municipality office ofresidence of each embarkation person by map
software. Furthermore, I applied tour times tohave made use of an expressway in case thatthey exceed 100 km one way. The necessary
time for clam digging is 3 hours and 30 minutes. I multiplied for the expenses rate in an
opportunity of a tour time for the total in the
aforementioned necessary times. I used an average wages rate R in the following equation as
an expenses rate in an opportunity of a tour
time (Fujimoto, 1996).
R＝(w×( 1−T )/Hw )×(E/M )(1)

Where w is average monthly cash earnings
for regular employee by prefecture ( establishments with 30 employees or more ) (Statistics
and Information Department, Ministers'
Secretariat, Ministry of Health, Labor andWelfare, Japan, 2002). The term T is tax ratio
against each prefecture inhabitant of a prefecture income (Government Cabinet Prefecture,
1998, Local Public Finance Investigation
Research Society, 1999 and National Tax
Agency, 1999). The term Hw is averagemonthly hours worked by a regular employee
at prefecture (establishments with 30 employees or more) (Statistics and Information
Depart-ment, Ministers' Secretariat, Ministryof Health, Labor and Welfare, Japan, 2002).
The term E is the number of persons who workin one household with each prefecture office location city (Statistics Bureau, Ministry of
Public Management, Home Affairs, Posts andTelecommunications, Japan, 2001)
The term M is the number of persons in one
household with each prefecture office locationcity (Statistics bureau Ministry of Public management,
Home
Affairs,Posts
andtelecommunications, Japan, 2001)
I summed up aforementioned monetary expenses and time expenses and calculated thetravel cost (TC ) for one person for each municipality.
(3) Visit rate (V )I estimate V (percentage) from the following
formula. Divide visitor's number of each municipality by each population of municipality(thousand persons).
(4) Calculation of equation of V and TC
Because I applied function style by the leastsquares method in respect of scattering of V−
TC, applying to it indeed for natural logarithm
equation was good. The relation between V andTC can be expressed by the following equation.
(Fig. 4)
V＝−181.496logTC＋1808.978(2)

The P value was 0.000113 and meaningful
though the decision coefficient is low with 0.08.
(5) Estimation of visitor number of each municipality.
I calculated the estimated V of aforementioned equation based on TC for each municipality. Then I found the estimation number ofvisitor for each municipality.
(6) Measurement of the additional expenses(TC' ) and accept rate (V' )I added additional expenses until an estimation visitor number became 0 by 500 yen for TC
every municipality. Because I applied function

V＝−181.496logTC＋1808.978

Fig.4. The relation between V and TC

107

Economic value of tidelands as place for recreational clam digging

style by the least-squares method in respect of
scattering of V'−TC', applying to it indeed fornatural logarithm equation was good. Relation
between the additional expenses ( TC ' ) and theaccept rate ( V' ) can be expressed by the following equation.(Table 7 and Fig.5)
V'＝−0.33809logTC'＋3.239559(3)

The value P was 1.21×10−19 and meaningful
with a 0.954 decision coefficient.
(7) Calculation of the average WTP (willingness
to pay)If I decide demand curve of equation (3), integrate it, I can calculate the average WTP.
bcarried out in a lot of fishermen's cooperative
associations in Mikawa Bay, and an enterpriseprofit of a fishermen's cooperative association
plays an important role.
At Kira Town, fishermen carry clam digging
visitors after their trawling operation, so the
pickup income is added to a fishing income.
Because the unloading of a small trawl net of2001 was about an average of 7.5 million yen,
the pickup income comprises around 7 ％.
However, as for the fishery income, pickup income (525,971 yen) amount to the 23 ％ for 2.3
million yen by unloading 7.5 million yen. It became clear that clam digging brings large additional income to fishermen who carry visitors.
Recreational benefits of clam digging for

WTP＝ 殺a (−0.33809log TC'＋3.239559) dTC'

Table 7. Measurement of the additional expenses(TC' ) and accept rate (V' )a: 0
b: 14,077 yen (accepting 1 percent)
The average WTP for a person was 4,900 yen
by this equation.

Estimated numTC' (Additionalber of accepted
expenses
V' (Accept rate)
person of all(yen/indiv.))
municipalities(8)Estimation of the recreation benefits
Average WTP 4,900 yen × 7,276 person ＝35,650,000 yen
Recreation benefits of visitor at KajishimaIsland estimated 35.65 million yen.
Discussion
Because of the enterprise, general profit of
the KFCA in 2001 was about 42 million yen,and the profit from recreational clam digging
accounts for 22 ％ of general profit, and its
benefit in the KFCA is high. Clam digging is

Fig.5. The relation between V' and TC'

0
500
1,000
1,500
2,000
2,500
3,000
3,500
4,000
4,500
5,000
5,500
6,000
6,500
7,000
7,500
8,000
8,500
9,000
9,500
10,00010,50011,00011,50012,00012,50013,00013,50014,00014,50013,53012,55011,616
10,733
9,906
9,114
8,359
7,638
6,958
6,309
5,694
5,122
4,580
4,069
3,576
3,102
2,642
2,222
1,821
1,455
1,103
802
561
368
226
123
54
23
9
2

1.0
0.927590.85856
0.79332
0.732160.673610.61779
0.564540.51426
0.46633
0.42086
0.37856
0.338530.300730.26433
0.22925
0.195280.164220.13457
0.10751
0.08152
0.05927
0.04147
0.02718
0.01667
0.00909
0.003970.00172
0.000700.00016

108

Yasuji TAMAKI

visitors are estimated 35.65 million yen at
Kajishima Island. This amount of money is almost equal to 38 million yen of quantity of
Manila clam fishery of 151 tons a year in the
KFCA. It is obvious that urban residents give ahigh evaluation against recreational benefits ofclam digging.
A lot of city inhabitants enjoy clam digging
as natural scene or object which adds to poetic
charm to the season, but, on the other hand, atendency to decrease Manila clam population,
and an expense of seed discharge rises, too. In
addition, landfill goes ahead through a tidelandof the coast, and fishing grounds of clam digging are being lost. For example, large quantities of Manila clam died by high watertemperature and an outbreak of blue tide in
Mikawa Bay in 1994. And a red tide by
Heterocapsa occurred on the coast that reached
Gamagoori City from Issiki-town in summer,
2000, and Manila clam died in large quantities(Sonda and Kimura ., 2001). Clam digging wascanceled due to shellfish poisoning which occurred in spring, 2001, until a declaration ofsafety came out on 19 March, and, it is a grave
concern.
I estimated the recreational benefits of clam
digging at 35.65 million yen as the recreation
benefits of about 6 hectares Kajishima Islands'clam digging ground. It became clear that therecreational benefits of clam digging for city
inhabitants were equivalent to the fisheryamount of money and the scale.
Maintenance of the water quality is important, but in fact the water purification abilityof a tideland where clam digging is possible isthe most effective for the improvement of thewater quality, and enhancement of artificial
tidal land is necessary for the tidal land lost byland reclamation as a future policy so that we
can continue clam digging in future. I would
like to do such an economic assessment of tideland to judge whether the budget expenditureis right or not when a country and a local selfgoverning body enforces mitigation and supports clam digging. In addition, producer of theartificial tideland must not make the newenvironmental disruption by collection of sandto make the tideland.
The number of people digging clam according to prefecture by a fishery census,
Kanagawa Prefecture was the first place, but
most people are the people who came to thePark of the sea which is an artificial tideland
made in reclaimed land of Kanazawa-ku,
Yokohama City, Kanagawa Prefecture. But
there is not management by fishermen's cooperative associations, and indiscriminate gathering becomes a problem because there is notfishery right in the Park of the sea (Kudou,
2000). It is thought that the role of management by the fishermen's cooperative associations in a clam digging fishing ground is very
important.
References
Aoyama H., Imao K., and Suzuki T., 1996:
Function that a tidal land purifies a quality of water−As doing Issiki tidal land foran example−. Kaiyo Monthly, 28(3 ), 178188.(In Japanese)
Fujimoto T., 1996: Economic evaluation of agricultural externalities−An Application ofContingent Valuation Method−. Bulletinof the Nara Prefectural Agricultural
Experiment Station, Special research, 5962. (In Japanese)
Government
CabinetPrefecture,
1998:
Prefectural economy calculation annual report. (In Japanese)
Kira Fisheries Cooperative Association., 2001:
Heisei Year 12 Business Report, 17pp. (InJapanese)
Kudou T., 2000: Manila clam digging problem
at a beach where resource manager is absent, Coastal Zone, 13(1 ), 53-57. (InJapanese)
Local Public Finance Investigation ResearchSociety, 1999: Prefectural settlement of accounts situation survey. (In Japanese)
National Tax Agency, 1999: Statistical annual
report on the national taxes. (In Japanese)
Sonda Y. and Kimura H., 2001: Occurrence ofEconomic value of tidelands as place for recreational clam digging

Heterocapsa circularisquama red tide in
Mikawa Bay, 2000. Bulletin of the Aichi
Fisheries Research Institute, 8, 1-6. (InJapanese with English abstract)
Statistics and Information Department,
Ministers' Secretariat, Ministry of Health,
Labor and Welfare, Japan, 2002: Annual
report on the monthly labor survey

109

Prefectural Survey, 22pp. and 42pp. (InJapanese)
Statistics
BureauMinistryof
PublicManagement, Home Affairs, Posts andTelecommunications, Japan, 2001: Annual
report on the family income and expenditure survey, 304pp. (In Japanese)水研センター研報，別冊第 1 号，111−121, 平成16年
Bull. Fish. Res. Agen. Supplement No. 1, 111-121, 2004

111

Large-scale restoration of tidal flats and shallows to suppress thedevelopment of oxygen deficient water masses in Mikawa Bay
Teruaki SUZUKI*

Abstract Development of hypoxia has been confirmed in the inner-part of almost every
major bay of Japan on the Pacific coast from Tokyo southward. Mikawa Bay, where
Japan's most serious hypoxia occurs, is used to this report to present the effects andcauses of hypoxia, such as impact upon fisheries, historical development and nutrient
budget between sediment and water. Although hypoxia basically results from an increase in nutrient load input, intense reclamation in Mikawa Bay of about 1,200 ha ofshallows in the 1970s, including tidal flats, has drastically accelerated a deficiency in dissolved oxygen. This is mostly due to losses in the rich filter-feeding macrobenthic community that largely control the high water-purification capacity of those areas.
Currently, oxygen deficient water masses in Mikawa Bay are large enough to strip the
precious water purification capacity of the remaining shallows by killing the remaining
filter feeders. Consequently, the considerable shallows have turned from being a purifierof water quality to a source of excess nutrients, thus sending the Bay into a spiral of deterioration. In order to break this vicious cycle, the dissolved oxygen deficiency of the
Bay must be contained to the extent that the purification capacity of the shallows canbe brought into full play. To this end, the first thing to do is to restore the tidal flats
and the shallows having the effective depth so designed as not to be affected by oxygen
deficient water masses, over an extensive area. This may be a more urgent imperative
than reducing the nutrient load input. Since 1998 to 2001, about 350 ha of artificial shallows, including tidal flats, have been restored in Mikawa Bay using sand dredged fromthe Nakayama sea channel. Recovery of abundant benthic organisms, such as bivalves,
has been confirmed already by monitoring. Additional tidal flat restoration is now inprogress.
Key words: hypoxia, tidal flat, restoration, Ruditapes philippinarum

Effects of a dissolved oxygen deficiency on fisheries in Mikawa Bay
Mikawa Bay is a typical, partially mixed estuary located in the central part of Japan asshown in Fig. 1. The Bay consists of two inlets:
The northwest part is Chita Bay into which theRiver Yahagi-gawa flows. The eastern part isAtsumi Bay into which the River Toyo-gawaflows. In its entirety, Mikawa Bay measuresabout 600 km2 and is very shallow with an average depth of 10m.
Oxygen deficient water masses occur in
Mikawa Bay on a large scale as seen in the example shown in Fig. 2 (Ishida and Hara, 1996)
since about 1970. Oxygen deficiencies can last
as long as four months, or more, from midJune to mid-October.
Mikawa Bay was one of the best fishinggrounds for commercial crustaceans (such as

2003年 6 月12日受理（Received on June 12, 2003）* Aichi Fisheries Research Institute, 97, Wakamiya, Miya-cho, Gamagori, Japan, 443-0021

112

Teruaki SUZUKI

Fig. 1. Map of Mikawa Bay

kuruma-prawns, swimming-crabs), bivalves(such as short-necked clams, cockles) andbenthic fishes (such as stone flounders) inJapan. For example, the catch of the shortnecked clam (Ruditapes philippinarum) has
been the best in Japan until today, contributing the largest share of about 36 ％ to the total
yield. However, the total catch in Aichi
Prefecture decreased from 20,000 ton year−1 to
11,000 ton year−1 from the latter half of the
1960s to 2001.
Since 1970, when dissolved oxygen deficiencies began to develop, the major fishinggrounds of small-trawl fisheries of these species shifted from the middle of the bay towards
the mouth. At present, the Mikawa Bay trawl
fishery yield is rapidly declining.

between the benthic sediment and seawater isaffected, using a benthic ecosystem model(Suzuki et al., 1998b) that was developed toquantify the nitrogen cycle of tidal flats in
Mikawa Bay (Suzuki et al., 1997). Those results
are outlined below.
Fig. 3 shows the temporal changes in watertemperature, salinity, and dissolved oxygen
saturation percentage immediately above thebottom sediment in shallow areas (4 m depth
expressed by chart) that were recorded in the
inner part of Mikawa Bay, from June to theend of July 1996, and compared to changes inthe benthic community (bacteria, benthic micro
algae, meiobenthos, and macrobenthos).
A deficiency in dissolved oxygen was observed
on 25-26 June, 28-29 June, and 10 July , buteach time the occurrence was brief and thesaturation level stayed at about 50 ％ until atleast 20 July. Then, a deficiency in dissolved
oxygen lasted through the period from July 20-

Effects of dissolved oxygen deficiencies on the
Mikawa Bay nutrient budget
A deficiency of dissolved oxygen not only affects the structure of a benthic community, butalso its functionality. We have studied the temporal development of waters deficient in dissolved oxygen and the resulting benthic
community changes (Suzuki et al., 1998a). We
have also studied how the nitrogen balance

Fig. 2. Example of the distribution of dissolved oxygen deficient water masses in Mikawa Bay. Fourlegends denote the level of dissolved oxygen saturation percentage

Large-scale restoration of tidal flats in Mikawa Bay

29 and the frequency of anoxic conditions increased.
Different species reacted in different ways to
low oxygen concentrations according to theirtolerance limits, but eventually on July 29 thebiomass of every species dropped sharply.
Fig. 4 shows a time-series chart of the nutrient
flux between seawater and sediment calculated
by a benthic ecosystem model. On the verticalaxis, the flux from seawater to sediment is indicated as negative quantities.
Before 16 July, particulate organic nitrogen(PON) was being removed from the water at−561 to −962 mgN m−2 day−1 (−785 mgN m−2
day−1 , on average). Dissolved inorganic nitrogen (DIN) was eluting at 159 to 757 mgN m−2

Fig. 3. Time-series changes in water temperature, salinity and degree of dissolved oxygen saturation percentage immediately above the bottom sediment inshallow areas of Mikawa Bay and changes in thebenthic community (bacteria, benthic micro algae,
meiobenthos, and macrobenthos) from June to endof July in 1996 (Suzuki et al., 1998a)

113

Fig. 4. Change of the nitrogen budget between sea
water and sediment on the shallow area of the inner
Mikawa Bay from 1 June to 29 July, 1996 (Suzuki etal.,1998b)

day−1 (535 mgN m−2 day−1, on average). On balance, Total nitrogen (TN) was removed fromthe water at − 43 to − 401 mgN m−2 day−1(−250 mgN m−2 day−1, on average). Then, from
16 to 22 July, both the PON removal rate andthe DIN elution rate dropped rapidly, and on 29
July PON removal had almost ceased. Thus,
after 22 July, the TN budget turned from negative to positive to about 240 mgN m−2 day−1.
The analytical results from the benthic ecosystem model indicate that the shallows usually have the capacity to reduce particulateorganic matter at a higher rate of efficiency
than the rate of elution of inorganic nutrient
salts. However, this so-called "water purification capability" functions only if ambient oxygen conditions are normal. If a large oxygendeficient water mass develops in the offshore
sea bottom to a scale that can affect the shallows under certain wind and tide conditions,the situation changes completely.
First, the macrobenthic biomass of suspension-feeders decreases, resulting in a lower rateof removal of particulate organic matter fromthe water. Then, the rate of removal of organic
sediment matter by macrobenthic depositfeeders, which balances with the rate of sedimentation of PON, also drops. Subsequent
deterioration in water transparency near thesea bottom hinders the growth of benthic
microalgae and seaweeds, which slows down
the absorption rate of inorganic nutrient salts.
Then, the amount of oxygen generated by

114

Teruaki SUZUKI

photosynthesis also falls, accelerating the development of the anaerobic condition near thesea bottom.
Circulation of nutrient salts within the bottom sediment becomes heavily dependent onbacteria, although this system is also hindered
by a reduction in bacterial biomass. Although
this means a reduction in nutrient elution fromsediment to seawater, the TN budget of PON
and DIN shifts from a sink (−) to a source (＋).
Consequently, the shallows that were a highly
efficient water column purifier become a sourceof nutrients, and this further exacerbates thedissolved oxygen deficiency.
It is estimated that benthic organisms usually abundant in shallow sea areas above 5 m indepth are wiped out by the deficiency of dissolved oxygen in about one third of the total
shallow area under the worst circumstances.
This results in nitrogen elution of 11 tons
day−1, which amounts to about 27 ％ of the nutrient load input to Mikawa Bay. This meansthat countermeasures to reduce the nutrient
input, such as construction of sewage treatment plants, would make little difference unless the hypoxic condition is improved first.
Historic record and causes of dissolved oxygen
deficiencies
An oxygen deficient water mass is formed
when oxygen demand exceeds oxygen supply.
The main cause of high oxygen demand is theincrease in the amount of particulate organic
matter in the water or organic sediments on
the bottom.
Fig. 5 shows the transition in transparency
and the nitrogen load through time.
Transparency rapidly decreased from 1955 to
1970, corresponding to annual fluctuations in
the nitrogen load. During that period, the nitrogen load doubled and phosphorus tripled.
However, from about 1970 to 1983 as shown in
Fig. 6, red tides became a notable feature afterthat period. The development of dissolved oxygen deficiencies also increased steeply fromabout 1970. Red tides and associated hypoxia

rarely occurred before 1970.
Thus, historically, eutrophication in Mikawa
Bay can be divided into Phase I (1955-1970) in
which transparency decreased considerably asa result of the increased nutrient load; andPhase II (1970 and after) in which fisheries wereseverely damaged by red tides and oxygendeficient water masses. The question now is,apart from the increase in nutrient inputs,
whatcausedtheintensificationofeutrophication between Phase I and Phase II?
One likely cause is the intense reclamation
throughout the extensive shallow areas.
During the 1970s in Atsumi Bay, in the eastern-part of Mikawa Bay, about 1,200 ha ofshallows, including tidal flats, were reclaimed
to prepare for constructing a harbor (see Fig.
7). The appearance of red tides, accompanied byoxygen deficient water masses, coincides exactly with that reclamation of the shallows.
This fact is very important in regard to
hypoxia in the estuary. Tidal flats and shallows have a high water-purification capability
due to filtering by macrobenthic suspensionfeeders. Incidentally, benthic suspension feeders (mainly bivalves) living on the Isshiki tidal
flat of Mikawa Bay, are estimated to filter
seawater at a rate of 3.4 (Aoyama and Suzuki,1997) to 5.0 m3 m−2 day−1 (Sasaki, 1994). From
the reclaimed 1,200 ha, this totals to about 500
m3 sec−1. This value is calculated by assumingthat the standing stock of the benthic suspension feeders in the reclaimed area in 1970s is
equal to that of the present Isshiki tidal flatarea. However, it is possible that this value isunderestimated because the reclaimed area was
the richest clam fishing ground in Mikawa
Bay. The standing stock of short-necked clams
in the reclaimed area was estimated at 3.4 times
as much as that in the present Isshiki tidal flat,according to the past catch statistics of Aichi
Prefecture. Using this revised value, the reclaimed 1,200 ha of shallows are estimated tofilter seawater at a rate of 1,700 m3 sec−1. Since
the rate of exchange of seawater at the mouthof Mikawa Bay is 1,169 m3 sec−1 (Unoki, 2000) to
2,600 m3 sec−1 in the summer (Sasaki, 1989), theLarge-scale restoration of tidal flats in Mikawa Bay

lost seawater filtration rate equals 19 ％ to 43％ of the exchange rate of seawater in the caseof 500 m3 sec−1 and 65 ％ to 145 ％ in the case of
1,700m3sec−1.
It seems likely that the reduced capability ofseawater filtration drastically reduced the capacity to remove suspended organic matterfrom the water and consequently, accelerated
the development of water masses with a dissolved oxygen deficiency, followed by severe
red tides.
There is another possibility besides intensive
reclamation. It is the development of water resources in the catchment basin. In Mikawa
Bay, the River Toyo-gawa is the most important river in regard to density flow andseawater exchange of the Bay.
In 1968, Toyo-gawa canal was completed,which diverts about 20 ％ (in an average year)
to 40 ％ (in a dry year) of the total flow of theRiver Toyo-gawa. The chief purpose of thecanal is irrigation of farmlands on the Atsumi
Peninsula, for which 72 ％ of the diversion isused. There is speculation that this large reduction in the river flow, due to the canal diversion, reduces the density flow in the bay andexchange of seawater proportionally by 20 ％to 40 ％. However, this subject needs further
study, since a lower estimation of the decline
rate of exchange of seawater has been made inan analysis using a numerical model (Suzuki etal., 1986). Nevertheless, it is certain that thehindrance to seawater exchange slows the ejection of suspended organic matter to the exterior of the Bay; and reduces the supply of
dissolved oxygen from the mouth of the Bay.
We surmise that the reduction in the filtration rate of seawater, caused by reclamation of
the shallows around 1970s, was what mainly
accelerated the occurrence of red tides and dissolved oxygen deficient water masses. As mentioned above, Oxygen-deficient water masses in
Mikawa Bay have become large enough to strip
the precious water purification capability of
the remaining shallows. Unfortunately, theshallows have turned from being a water purifier to a source of nutrients sending the Bay

115

into a spiral of deterioration. This phenomenon, triggered by hypoxia, is very similar tothe catastrophic degradation of lake ecosystems caused by several external forces.
Takamura (2002) reports in order to maintain a healthy lake ecosystem, it is necessary to
distinguish between acceptable change andchanges to avoid. The most important factor
affecting this distinction is the concept of "re-Fig. 5. Transparency and nitrogen load in Mikawa
Bay

Fig. 6. Total number of days of red tides observed
and the areal proportion of oxygen deficient waterwith less than 30 ％ saturation in Mikawa Bay

Fig. 7. Total number of days red tides observed andthe area of reclaimed land in Mikawa Bay

116

Teruaki SUZUKI

silience". Takamura (2002) defines lake ecosystem "resilience" as the ability to sustain certain
structures and functions of the lake ecosystemagainst several external forces, and changes
that can damage this resilience (catastrophic
change) must be avoided.
There are reports in the literature that,through their feeding activities, the macrobenthic
community controls the structure of theplanktonic community and nutrient concentrations of seawater. They also exert a strong influence on nutrient circulation in the bay(Cloern, 1982; Cohen et al., 1984; Carlson et al.,1984). Thus, in Mikawa Bay, it may be said
that abundant bivalves that lived in the reclaimed area provided the Bay with its "resilience". Ironically, the drastic environmental
deterioration caused by intensive reclamation
projects in Mikawa Bay proved the importanceof the benthic community in providing that resilience function.

Restoration of tidal flats and shallows
In order to break the vicious cycle ofeutrophication, the dissolved oxygen deficiencyof water masses in Mikawa Bay must be contained to the extent that the purification capability of the shallows can be restored to a
sufficient level. To this end, the first thing to
do is to restore tidal flats and shallows having
the effective depth so designed as not to be affected by oxygen deficient water masses, overan extensive area. This may be a more urgent
imperative than reducing the nutrient load
input.
The Aichi Prefectural Federation of Fisheries
Co-operative Associations (APFFCA) organized a technical society to study environmental
improvement methods for Mikawa Bay from1995 to 1997. APFFCA published a proposal titled "The necessity to artificially develop tidal
flats and shallows for the improvement ofAichi prefectural sea areas" in 1997. The proposal stated that aggressive restoration of thewater purification capability in the Bay would

Fig. 8. Locations of the sites restored by 2001

Large-scale restoration of tidal flats in Mikawa Bay

be the most effective way to improve thehypoxic conditions, and then it would be necessary to enhance biological diversity and the
productivity of fisheries.
At first, it was thought that realization ofthis proposal would be very difficult because of
the high cost and the large sand volume, giventhat the APFFCA proposal stated that it would
be necessary to restore a large area of over
1,000 ha to significantly suppress hypoxic conditions.
The Nakayama sea channel, located at theentrance of Mikawa Bay, is important to marine traffic accessing the ports in Mikawa Bay.
However, the navigation of vessels in the area
is limited, because of patchy shoals (the mostshallow point is −8.6m) and sunken rocks thatinterfere with the economical operation of vessels. To improve navigability of the channel,
the Ministry of Land, Infrastructure andTransport (MLIT), Chubu Bureau, made the"Nakayama Channel Line improvement plan"in 1980. APFFCA has consistently objected tothis plan because this area has been a goodfishing ground. As a result of many negotiations between APFFCA and MLIT, it wasagreed that all dredged sand (6.2×106 m3) would
be used to restore tidal flats and shallows in
Mikawa Bay. After this agreement, artificial
development of tidal flats and shallows to improve Mikawa Bay accelerated drasticallyunder a joint effort between MLIT and Aichi
Prefecture. Fig. 8 shows the locations of the restored sites, in which 11 sites were created by
MLIT and 16 sites by Aichi Prefecture. In total,
tidal flats and shallows of 350 ha have been restored already using the sand of 3.4×106 m3
from 1998 to 2001. The use of the remaining
2.8×106 m3 is scheduled to restore tidal flatsand shallows by 2004.
Effect of the restoration
At some of the restored tidal flats and shallows, monitoring surveys have been conductedon environmental conditions such as water
quality, sediment quality, benthic community

117

diversity and abundance of fishery organisms
by MLIT and Aichi Prefecture. As the investigations are still going on, we cannot show theresults in detail yet. However, parts of the interim results are given in the following:
At the Nishiura site (12 ha) where a tidal flat
was created in 1999, many bivalves have been
observed-even immediately after construction.
In an investigation using a small trawl shellnet (0.59 m width) conducted about 3 years
after the tidal flat creation, many megabenthic
species, including commercial species, were observed as shown in Table 1. These values arecomparable to those of natural tidal flats in
Mikawa Bay. Before the creation of the artificial tidal flat, these megabenthic species were
not found in this area in summer.
Fig. 9 shows the transition in the numbers ofbenthic species at the Mito site (10 ha).
Initially, the biota consisted mainly ofpolychaetes (unpublished data by MLIT). As
time passed, many additional bivalves appearedsuch that the biota has become diversified.
Improvement of the water purification capacity
is expected due to the increase of bivalves because they have a high water filtration capability. At present, the most dominant species, ona wet weigh basis, is Mactra chinensis as is
likely at the Nishiura site. The particulate organic nitrogen purification capability of thissite has been estimated at 136 mgN m２ day−1 ,based on the monitoring results of June 2000
(unpublished data by MLIT). This value, estimated 21 months after the artificial creation, is
equivalent to about 60％ of the nitrogen purification ability of Isshiki tidal flat, which was estimated at 227 mgN m2 day−1 by Aoyama andSuzuki (1997).
At the Isshiki site (26 ha), a lot of juvenile
flounders were caught using a standard sledge
net (Koshiishi et al., 1999). The most dominant
species was the stone flounder (Platichthys
bicolorantus), which appeared mainly fromMarch to May. A sledge net was towed along
three transects on the tidal flat and one
transect off the tidal flat at high water.
Observed individuals ranged between 3,278-

118

Teruaki SUZUKI

13,489 inds ha−1 (7,156 inds ha−1 on average) in
March, 2,647-7,037 inds ha−1 (5,571 inds ha−1 onaverage) in April and 216-3,315 inds ha−1 (1,390
inds ha−1 on average) in June, respectively assuming that the efficiency of catch is 0.4-0.7 estimated from the body size (Koshiishi et al.,1999). The values on the restored tidal flat arelarger than that of the outside of site.
Although the Isshiki site was created inAugust 2000 and less than one year had passed,
these values are almost equal to, or larger
than, the density (1,620-8,192 inds ha−1 ) observed in the natural estuary, of Gamou of
Sendai Bay in mid April from 1992 to 1996
(Yamashita et al., 1999). However, there aresome sites of artificial shallows where good results that were expected have not been obtained. In summer, at the innerpart of Mikawa
Bay, serious hypoxia is frequently observed
near the bottom, even in shallows above 4 m indepth. Therefore, the aim of developing a newshallow area should be to avoid hypoxia.
Imao et al. (2001) proposed a method to determine the depth necessary to avoid hypoxia at a
new artificial shallow area. They proposed thatthe depth of the artificial shallow should be
where the survival rate for the short-neckedclam will be over 70 ％ under the severest
hypoxic conditions (hereafter called the "survival depth"). Imao et al. (2001) sampled themacrobenthos, water temperature and dissolved oxygen concentration successively innine coastal areas of Mikawa Bay. Then they
estimated each survival depth using a numerical model to forecast the survival rate of shortnecked clams against hypoxia (Suzuki et al.,1998c). The results showed that the survival
depth is different for each area within a rangeof D.L. −1.3 m to D.L. −4.0 m. Unfortunately,
however, in the actual tidal flat creation, civilengineers, who tend to plan uniformly without
reflecting the local hypoxic features, have not
yet acknowledged the importance of thismethod.
We suggest that the depth of the artificial
tidal flat creation was slightly lower than theFig. 9. Numbers of the benthic species at the Mitosite (unpublished data by MLIT)

Table 1. Megabenthos caught by a small trawl shell-net (0.59m width)in summer 2002 (21 June; 13 August; 26 August) at Nishiura artificial
tidal flat (12 ha) created in June 1999
Species nameinds. m−2

wet. g. m−2(Pelecypoda)
Mactra chinensis(bakagai)

2.3-17.2

73-614Mactra quadrangularis(shiohukigai)

0.7-22.7

9-194

Ruditapes philippinarum(asari)

3.4-72.9

21-678

Scapharca subcrenata(sarubou)

1.2-4.2

6-42

Neverita didyma(tsumetagai)

0.3-1.5

14-68

Rapana venosa(akanishi)

0-0.1

0-11

Portunus trituberculatus(gazami)

0-1.0

0-14

Charybdis japonica(ishigani)

0-0.1

0-1

(Gastropoda)(Crustacea)

Large-scale restoration of tidal flats in Mikawa Bay

survival depth at some unsuccessful sites.
There are some problems to solve in addition
to the acknowledgement of survival depth. The
first is the supply of the sand. As mentioned,
we must restore at least 1,200 ha to supress the
hypoxic condition in Mikawa Bay effectively,
but we can restore only half of 1,200 ha by 2004.
After 2004, we shall not be able to get the119

enough sand to restore. So, we are now studying the alternative materials including the artificial sand such as granulated blast furnaceslag, urgently.
The second is the proper selection of the site
location. It is important to choose areas thatwill be the most effective for the recruitment or
supply of bivalve's pelagic larvae. To that end,
we selected the short-necked clam (Ruditapes
philippinarum) as a target species, and observed the vertical distribution pattern of thelarvae. Then, using a receptor mode model, we
are trying to predict trajectories of the pelagic
larvae (Suzuki et al., 2002). Receptor mode
model is the simulation technique to trace thedrift particles in the inverse time mode. Fig. 10
is one of the examples of the calculations (thecase calculated at the period from 27 May to 14
May, 1998). Isshiki area where the initial distribution of pelagic larvae was given, is the mostimportant fishing ground of short-necked clamin Mikawa Bay. Pelagic larvae supplied to thisarea was estimated by receptor mode model,
supposing that the drift period is two weeks
from the water temperature and the larvae distribute around the mid-depth from the observation. As the model result, it was suggested
that the inner part of Atsumi Bay is the mostimportant origin and perhaps it may be theproper site location in future.
Although there are some problems to solve,
we will be able to confirm the suppression of
hypoxic conditions in future by an increase of
the water purification capability, as long as therestoration of tidal flats and shallows progresses smoothly and the existing reclamationplans are abandoned.
Acknowledgements

Fig. 10. The example of the final horizontal distribution pattern of pelagic larvae calculated by receptor
mode model. Upper figure shows the initial distribution (Suzuki et al., 2002)

I wish to thank the staffs of Kinuura Branchof Mikawa Port Construction Office, Chubu
Bureau of the Ministry of Land, Infrastructure
and Transport for the use of figures and also
thank Dr. J. Higano and Dr. T. Seki, National
Rsearch Institute of Aquaculture, for their encouragement and helpful suggestions.

120

Teruaki SUZUKI

References
Aoyama H. and Suzuki T., 1997: In situ measurement of particulate organic matter removal rates by a tidal flat macrobenthic
community. Bulletin of the JapaneseSociety of Fisheries Oceanography, 61, 256274 (in Japanese with English abstract).
Carlson D. J., Townsend D. W., Hilyard A. L.,
and Eaton J. F., 1984: Effect of intertidal
mudflat on plankton of the overlying
water column. Can. J. Fish. Aquat. Sci.,
41, 1523-1528.
Cloern J. E., 1982: Does the benthos control
phytoplankton biomass in South San
Franciso Bay? Mar. Ecol. Prog. Ser., 9, 191202.
Cohen, R. R., Dresler P. V., Phillips E. J. P.,
and Cory R. L., 1984: The effect of the
Asiatic clam Corbicula fluminea on
phytoplankton of the Potomac River,
Maryland. Limnol. Oceanogr., 29, 170-180.
Imao K., Suzuki T., Aoyama H., Kai M., Ito N.,
and Watanabe J., 2001: Investigation of
conditions required to construct an artificial shallow area to recover the water purification function of a hypoxic sea.
Fisheries Engineering, 38, 25-34 (inJapanese with English abstract).
Ishida M. and Hara T., 1996: Changes in water
quality and eutrophication in Ise and
Mikawa Bays. Bulletin of The Aichi
Fisheries Research Institute, 3, 20-42 (inJapanese with English abstract).
Koshiishi U., Kiyomoto S., Osaka Y., Sawano
K., and . Kimoto K., 1999: The situation ofsampling efficiency for juvenile plaice(Paralichthys olivaceus) and samplingtechnique concerning heterosomate fishes
by Seisuiken-V type beam trawl net, in "A
guide of sampling technique for juvenile
heterosomate fishes. The report of standardization section concerning ecologicalinvestigation for aquaculture" (eds. by
Yamazawa M. and Shiraishi M.), National
Research Institute of Fisheries Science,
Yokohama, pp. 53-59 (in Japanese).

Sasaki K., 1994: Material circulation and production in estuary and tidal flat-12.
Aquabiology, 16, 487-492 (in Japanese withEnglish abstract).
Sasaki K., 1989: Mechanism of oxygen-deficientwater formation in Mikawa Bay. Bulletin
on Coastal Oceanography, 26, 109-118 (inJapanese with English abstract).
Suzuki T., Hirasawa Y., and Seko Y., 1986: The
1985 technical report of red tide countermeasure,
Aichi
Fishries
Research
Institute, 32pp (in Japanese).
Suzuki T., Aoyama H., and Hata K., 1997: The
quantification of Nitrogen cycle on tidal
flat by ecosystem model-in the case ofIsshiki tidal flat in Mikawa bay-. J. Adv.
Mar. Sci. Tech. Soc., 3, 63-80 (in Japanesewith English abstract).
Suzuki T., Aoyama H., Kai M., and Imao K.,
1998a: Effect of dissolved oxygen deficiency
on a shallow benthic community in an
Embayment. Umi no Kenkyu, 7, 223-236 (inJapanese with English abstract).
Suzuki T., Aoyama H., Kai M., and Hata K.,
1998b: The effect of change in the benthic
community due to the development of dissolved oxygen deficiency on the nitrogenbudget between the sediment and overlying water. J. Adv. Mar. Sci. Tech. Soc., 4,65-80 (in Japanese with English abstract).
Suzuki T., Aoyama H., and Kai M., 1998c: The
formulation of the mortality of Japaneselittle clam (Ruditapes phillipinarum) caused
by a deficiency of dissolved oxygen in
Mikawa Bay. J. Adv. Mar. Sci. Tech. Soc.,
4, 35-40 (in Japanese with English abstract).
Suzuki T., Ichikawa T., and Momoi M., 2002:
The approach to predict sources of pelagic
bivalve larvae supplied to tidal flat areas
by receptor mode model: A modeling study
conducted in Mikawa Bay. Bull. Jpn.
Soc. Fish. Oceanogr., 66, 88-101 (inJapanese with English abstract).
Takamura N., 2002: Biodiversity and lake conservation, Aquabiology, 24(3), 197-202 (inJapanese with English abstract).
Unoki. S., 2000: Relation between the transportLarge-scale restoration of tidal flats in Mikawa Bayof gravitational circulation and the riverdischarge in bays. Umi no Kenkyu, 7, 283292 (in Japanese with English abstract).
Yamashita Y., Yamada H., Takami H.,
Kawamura T., and Tsuruta Y., 1999:

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Occurrence, distribution and utilization ofnursery grounds of settling and newly settledstoneflounder,Platichthys
biocoloratus, in Sendai Bay. Bull. Tohoku
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水研センター研報，別冊第 1 号，123−132, 平成16年
Bull. Fish. Res. Agen. Supplement No. 1, 123-132, 2004

123

Linking watershed loading and basin-level carrying capacity models
to evaluate the effects of land use on primary production andshellfish aquaculture
Mark W. LUCKENBACH* and Harry V. WANG*

Abstract Aquaculture production of hard clams, Mercenaria mercenaria, in the lower
Chesapeake Bay, Virginia, U.S.A., has increased dramatically within the last decade. In
recent years concern has been raised that some growing areas may be approaching the
exploitation carrying capacity for clam production. Preliminary calculations indicatethat large-scale intensive clam aquaculture may be controlling nutrient andphytoplankton dynamics in this system. To date, carrying capacity models have notbeen applied to this system, but we are in the process of building models for that purpose. Moreover changing land use in the watersheds surrounding the clam-producing
areas raises the need for an improved understanding of how these changes will affectwater quality, primary production and shellfish production. We describe an ongoingproject linking a watershed-based loading model with a physical transport-based water
quality model to simulate primary production and predict carrying capacity for clam
aquaculture. Extensive calibration and verification of the water quality model has demonstrated its utility for simulating primary production and water quality parameters in
the Chesapeake Bay. In our present efforts, watershed loading models have been developed and tested for predicting both surface and groundwater inputs into the coastal waters. We are currently coupling the water quality and watershed loading models, anddeveloping clam physiology and population-level sub-models. Also, under development is
a sediment deposition/resuspension sub-model. Each of these components will be linked
to estimate exploitation carrying capacity for clam production in this system. Our goal
is to use the coupled models to predict how varying land use scenarios impact water
quality, primary production and shellfish carrying capacity of coastal waters.
Key words: Mercenaria mercenaria, aquaculture, carrying capacity, water qualitymodel

In many coastal ecosystems phytoplankton
and suspension feeding bivalve production aretightly coupled (Dame, 1996). That suspensionfeeding bivalves can play an important role incontrolling phytoplankton abundance incoastal systems is well established (e.g., Officer
et al., 1982; Cloern, 1982; Nichols, 1985; Alpine

and Cloern, 1992). Through their feeding activity bivalves can alter nutrient dynamics (Dameet al., 1984; Dame and Libes, 1993), affect sediment composition and nitrogen cycling (Kaspar
et al., 1985), strongly affect carbon budgets(Rodhouse and Roden, 1987) and alter the composition of both benthic and planktonic

2003年 6 月12日受理（Received on June 12, 2003）* Virginia Institute of Marine Science, College of William and Mary. P. O. Box 350, Wachapreague, VA, USA, 23480
Email: luck@vims.edu Contribution number 2584 from the Virginia Institute of Marine Science124Mark W. LUCKENBACH and Harry V. WANG

assemblages (Tenore et al., 1982). Wild populations of bivalves have been implicated in someinstances (Officer et al., 1982, Cloern, 1982;
Newell, 1988; Dame, 1996), but much evidence
has come from bivalve aquaculture operations,
including mussel culture in the Rias of northwest Spain (Tenore et al., 1982) and New
Zealand (Kaspar et al., 1985) and oyster culturein Killary Harbor, Ireland (Rodhouse andRoden, 1987) and the Marennes-Oléron Bay inFrance (Bacher, 1989), that suspension-feedingbivalves affect phytoplankton dynamics onlarge scales.
The reciprocal is, of course, also true;
phytoplankton production strongly affects bivalve production. In a review of trophic dynamics in temperate estuaries Heip et al. (1995)
concluded that the ecological carrying capacityof bivalve populations in estuaries and coastal
bays is often constrained by phytoplankton
production. For bivalve aquaculture, whichseeks to maximize shellfish production,
phytoplankton production may determine theexploitation carrying capacity-the maximum
yield of market-size individuals within a particular environment. Carver and Mallet (1990)
showed that the exploitation carrying capacityof a coastal embayment in Nova Scotia formussel production varied with temporal variations in food supply. A series of models developed to predict the exploitation carrying
capacity for oyster aquaculture production in
Marennes-Oléron Bay in France (Bacher, 1989;
Héral, 1993; Bacher et al., 1997) have been used
to predict optimum stock size for maximizing
production in this estuary. Similarly, Ferreira
et al. (1998) developed a carrying capacity
model for oyster cultivation in Carlingford
Lough, Scotland. In the Oosterschelde estuary
in the Netherlands, Smaal et al. (2001) foundthat mussel production was limited byphytoplankton production. They estimated thecarrying capacity of the estuary for mussel culture before and after large-scale hydrographic
modifications and discussed how adapting
aquaculture practices in the context of food
limitations helped the industry to maximize

production.
Hard
clam
(Mercenaria
mercenaria)
aquaculture has expanded dramatically overthe past decade along much of the UnitedStates' Atlantic coast and the northeast Gulf of
Mexico. In Virginia, growth in this industry
has been especially dramatic. A conservative estimate places the total standing stock of cultured clams in Virginia in excess of 500 million
clams (estimate based upon federal crop insurance program statistics). Most of thisaquaculture occurs in small tidal creeks thatempty into the Chesapeake Bay and shallow
embayments behind coastal barrier islands(Fig. 1). In many of these areas clam
aquaculture has grown to a scale at which it
may be reasonable to ask if clam production isclose to the limit set by phytoplankton production, i.e., it may be at, near or even exceeding
exploitation carrying capacity.
Additionally, the clam aquaculture industry
faces threats from changing land use practices
in the adjacent watersheds. Rapidly changing
demographic trends in the region are leading to
the replacement of farmland by residential andindustrial uses. The potential impacts of thischanging use on water quality and clam
aquaculture are presently unknown.
In this paper we will (1) give a brief descrip-

Fig. 1. Region of study. Clam aquaculture is taking
place in the tributaries of the lower Chesapeake Bay
and the coastal embayments on the Atlantic coast.
C.I. denotes the location of Cherrystone Inlet.

Modeling water quality and carrying capacity for clam aquaculturetion of the farming practices for hard clams, (2)detail some preliminary calculations that reveal the potential strength of the interactions
between phytoplankton production and clam
production in one tributary, and (3) describe amodeling effort that is currently underway tolink watershed loading, water quality and clam
production models to provide a tool for predicting effects of changing land-use practices onwater quality, phytoplankton production andclam aquaculture production.

125

clam farm may include several hundred suchnets (Fig. 2). The grow-out period ranges from18 to 30 months with most clams harvested
within 24 months of planting.
In some of the most densely planted tributaries and embayments clam farmers have begun
to observe declining growth rates over the past
few years. One possible explanation for this observation is that these areas may have exceeded
the exploitation carrying capacity and clam
production may be limited by primary production in these systems.

Hard clam aquaculture
Detailed descriptions of the production practices for farming hard clams are given in Manzi
and Castagna (1989) and Castagna (2001).
Briefly, larvae are spawned and reared inhatcheries in seawater ranging from 20 to 35
ppt. Post-set juveniles are generally raised inland-based, flow-through nursery systems
until they reach a size of 3-4mm in shell height.
At that time they are placed into one of several
types of field nursery systems-either fine meshbags, sand-filled trays or floating upweller systems-and grown to a size range of 10-15mm.
Clams are then planted in the low intertidal
and subtidal zone in sand and sand-mud mix
bottoms for grow-out to market size. Generally
clams are planted in rows approximately 4 m
×18m at densities ranging from 550 to 1650
clams m-2 and covered by polyethylene nettingthat serves as predator protection. A typicalFig. 2. Aerial view of a clam farm in Chesapeake
Bay, U.S.A. Each rectangular net is approx. 4 m×
18m and covers 50,000 clams.

Estimating links between clam production andwater quality
To provide a first approximation of the effects of clam culture on water quality and of
the possibility that clam production may belimited by phytoplankton production in thesesystems, we performed some simple calculations for Cherrystone Inlet, a small tidal
embayment on the eastern margin of the
Chesapeake Bay (see Fig. 1). From theaquaculture industry we have an estimatedstanding stock of cultured clams in system of
45×10６ . The volume of Cherrystone Inlet athigh tide is 15.4×10６m3 and the volume of thetime averaged tidal prism is 5.8×10６m3 (Kuo etal., 1998). We used the filtration rate formula
reported by Hibbert (1977a, b) for Mercenaria
mercenaria at 25 ℃ (typical summertime watertemperatures in this area): FR＝0.063 ･ L0.834 ,where L＝shell length and FR has units of L
indiv−1 hr−1 . Multiplying by the total numberof clams and dividing into the total and tidal
prism volume estimates then provides roughestimates of the clams filtration volume relative to volumes in the embayment (Table 1).
Data from the clam industry indicates that annual harvest of clams from this region is approximately 20 × 10６ with an average shellheight of 60mm. Using a shell height to dry
weight regression from Walne (1972) and value
for tissue nitrogen＝0.1 ･ dry tissue weight(Hawkins et al., 1985), we estimate the amountof nitrogen removed annually from the system

126

Mark W. LUCKENBACH and Harry V. WANG
Table 1. Preliminary estimates of some of the effects of clam aquaculture on filtration on water
quality in Cherrystone Inlet. (NH＝nitrogen removal from harvest, NATM＝nitrogen loss as N2 to theatmosphere, NEX＝nitrogen excretion rate, primarily as ammonia.
Summertime filtration rate

Nitrogen uptake and releaseTotal
filtration rate

％ oftidal exchangeTime to filter
creek volume

NH

NATM

NEX

1.6 x 106 m3
day−1

28％

10 days

18,000kg
yr−1

36,000kg
yr−1

900kg
day−1

by harvesting (Table 1). Estimates by Hibbert(1977a) on the production of feces andpseudofeces by clams and measurements reported by Newell et al. (2002) for rates of nitrification and denitrification of bivalve
biodeposits were used to compute the amountof nitrogen lost as N2 to the atmosphere as a result of clam feeding (Table 1). Finally, we estimate nitrogen excretion rates from these clams
based on Hibbert (1977a) (Table 1).
We emphasize that all of the estimates inTable 1 are preliminary. Our intention in making these estimates was to provide an initial
evaluation of whether clam aquaculture in thissystem might have reached a scale at which it
was reasonable to hypothesize that it is nearcarrying capacity or that clams are having asignificant effect on water quality andphytoplankton dynamics. Evaluating these hypotheses will require an integrated modelingapproach. As noted above, land use in the watersheds around these small tidal creeks andembayments in which clam aquaculture is occurring is changing. It is likely that thischange will affect the inputs of nutrients, sediments and freshwater into these water bodies,
which in turn will have consequences for clam
production. In the sections below we provide an
overview of a modeling approach that we aretaking to address these issues.
Model Description
Carrying capacity models
Smaal et al. (1998) reviewed the requirements
for modeling bivalve carrying capacity incoastal ecosystems. In doing so, they outline a

number of sub-models that are required to provide input to an ecosystem-level model that estimates maximum production level. In short,hydrodynamic and sediment sub-models areused to characterize movement of materials in
the water column and between the sediment/water interface, respectively. A physiologicalsub-model incorporates bivalve feeding andenergetics on a size-specific basis, while thepopulation sub-model builds in the planting
densities and harvest schedules along with cohort growth and mortality. Output from thesesub-models together with data on physicalcharacteristics (e.g., light, T & S) and nutrient
loadings are then used in a system-level model
to estimate production capacity. Below we discuss in greater detail how each of these submodels are being developed for Cherrystone
Inlet.
Hydrodynamic submodel
A hydrodynamic sub-model called HEM3D(Hydrodynamic Eutrophication Model 3D) has
been developed at Virginia Institute of Marine
Science as part of a dynamic water quality
model. This model has been calibrated and verified in a number of systems such as YorkRiver, James River, Mobile Bay and Florida
Bay with relative success and has been selectedby the U.S. Environmental Protection Agency
as one of the standard model codes for water
quality application. The hydrodynamic submodel requires a number of inputs. The geometry (shape) and bathymetry of the system isrequired to construct grid configuration andbathymetry (each model cell is given an average
depth value). Boundary condition specifications

Modeling water quality and carrying capacity for clam aquacultureof forcing function(s) (e.g., tidal elevation, velocity, and usually salinity) at the open boundary, as well as discharge at the upstream
boundary must be specified. Runs of the model
are facilitated by proper initialization values ofmodel parameters, especially those that requirea relatively long time to equilibrate, such as salinity. Finally, specification of other inputs facilitates the calibration process (e.g., bottom
friction adjustment). For Cherrystone Inlet thegeometry and bathymetry data have alreadybeen collected and the grid system developed(Kuo et al., 1998). Boundary conditions for all
forcing functions have been established andproper initialization and calibration terms incorporated. Simulation with a precursor to thismodel, a tidal prism water quality model conducted by Kuo et al. (1998), was the first attempt using coupled hydrodynamic, water
quality and watershed models in theCherrystone Inlet. The simulated results of salinity, chlorophyll, DO, total carbon, total nitrogen and phosphorus provided reasonablepredictions compared to bi-monthly measured
field data (Kuo et al., 1998).
The state variables in this sub-model include
tidal elevation at each cell in the horizontal andvelocity, salinity, and temperature at cells inboth the horizontal and the vertical directions.
Process variables are derived from these, andinclude transport processes such as density
driven circulation. Advection and dispersion influence the flow field as well. Pending further
field verification and calibration this sub-model
will be used to generate the transport featuresthat drive the system-level model.
Resuspension/sedimentation modelThis sub-model, which is currently under development, will simulate fluxes of sediments
and other materials between the water column
and the bottom. In order to calculate suspended
sediment concentration in each cell of the model
domain, flow velocities are provided to the sediment sub-model by the hydrodynamic submodel. In addition, sediment settling velocities
are specified for each size class of the sediment.

127

Time series of sediment concentrations at the
upstream and open boundaries are used as the
input sediment fluxes to the model domain. The
erosion and deposition rate, representing vertical sediment fluxes between the water column
and the bottom, are calculated based on bottom
shear stress and the critical shear stress.
The sediment sub-model is being calibrated
to simulate the temporal and spatial variationsof sediment concentrations within the model
domain. The calculated sediment concentrationin each cell will be used to determine food quality and light attenuation factors for thegrowth of algae. A benthic compartment ingeneral and a clam sub-model in particular areimportant to include as both sink and sourcefor nutrients and particulate matter.
Clam feeding and physiological sub-model
The purpose of the clam feeding and physiology sub-model is to link the feeding, growth,energetics and excretion by clams to the general system-level model. Data are available on
the feeding, growth and energetics of wild M.
mercernaria throughout its range (reviewed by
Grizzle et al., 2001). Feeding rates vary withbody size, temperature and salinity; univariate
relationships with each of these factors havebeen reported in a large number of studies (e.g.,
Loosanoff, 1939; Coughlan and Ansell, 1964;
Hamwi, 1969; Hibbert, 1977a,b; Doering andOviatt, 1986; Bricelj, 1984; Walne, 1972).
Feeding rate also varies as a function of foodconcentration (Tenore and Dunstan, 1973), silt
content of the seston (Hamwi, 1969; Bricelj andMalouf, 1984) and phytoplankton species composition (Rice and Smith, 1958; Walne, 1972).
Relationships between respiration rate andbody size (Loveland and Chu, 1969) and respiration rate and temperature (Hamwi, 1969;
Hibbert, 1977b) have been published for M.
mercenaria. Hibbert (1977a,b) developed an energy budget for this species growing on
mudflats in Southampton, England.
In their extensive review of hard clamphysiological ecology, Grizzle et al. (2001) report growth rates for M. mercernaria that

128

Mark W. LUCKENBACH and Harry V. WANG

range from 0.42-1.11mm (growth in shellheight) week−1 and average time to market size
(25.4mm shell thickness) ranging from 2.1 to
13.0 years over a geographical range from
Prince Edward Island, Canada, to the Florida
Gulf coast. While they observed a latitudinal
gradient in growth rate, they noted that over abroad geographical range (New York to
Florida) variation in growth rate within an estuary generally exceed that attributable tolatitude (Grizzle et al., 2001).
The basic construct of the physiology
submodel is straightforward:
Growth＝Consumption−Respiration−Egestion−Excretion.
Consumption is a function of filtration rate
and food availability. Filtration rate and respiration vary as a function of temperature andbody size as discussed above. Because the cultured clams have been artificially selected forhigh growth for several decades by aquacultureindustry, it will be necessary to measure eachof these variables for cultured animals in
Cherrystone Inlet, rather than relying on published values for wild clams. When completed
this sub-model will output growth rates fromone size class to another that will serve as input
to the population sub-model.
Clam population sub-model
For wild populations of bivalves obtaining
reliable parameter estimates for the population
sub-model can often be the most difficult partof developing carrying capacity model.
Uncertainties surrounding estimates of reproductive output, larval survival and postsettlement mortality for field populations all
make it difficult to obtain accurate predictions.
For aquaculture, however, the parameter estimates are straightforward. The number andsize of clams planted by the industry, thegrowth rate between size classes and the harvest of clams by the industry, along with asmall, but defined, non-harvest related mortality are the primary parameters of interest.
These values will serve as inputs to the population sub-model and the measured growth rates

will be compared to predicted values based upon
the linked sub-models.
System-level model
Output from the various sub-models serves
as input for the system-level model that computes several state variables including primary
production and bivalve biomass for each cell at
the specified time step. The role of the hydrodynamic sub-model is to provide the transportquantities induced by the physical process,such as fluxes between the boxes and the mixing within a box. The sediment resuspension/
deposition model calculates the suspended matter concentration, which in turn determines thefood quality and light attenuation. The physiology sub-model drives the growth of clams
that feeds into the clam population sub-model
to drive cohort production estimates.
Because primary production varies temporally and spatially within estuaries, a dynamic
modeling approach as described above is required to estimate the exploitation carrying capacity for bivalve aquaculture (Smaal et al.,1998). Thus, once developed and calibrated, we
will run the model under varying conditions of
nutrient loading to investigate how clam production is affected by nutrient loading (either
from the Bay or the watershed) and undervarying clam stocking densities to evaluateaquaculture practices. Additionally, we will explore the effects of clam aquaculture on water
quality within the system by running themodel under various stocking densities (including no clam aquaculture) and estimating chlorophyll and light attenuation levels.
Watershed loading sub-model
A unique feature of our project to estimate
carrying capacity for clam aquaculture is an
ongoing effort to link a watershed loading
model to the system-level water quality model.
In order to understand and quantify the effects
of changing basin scale land-use patterns, awatershed model is needed. The HSPC
(Hydrologic Simulation Program C language)
will be used for simulating the watershedModeling water quality and carrying capacity for clam aquaculturehydrology and associated water quality parameters on pervious and impervious land surface and in streams and well-mixed
impoundments.
Sediment
andnutrientloadings in the model are transported fromland to the receiving coastal waters. Inputs tothis model include precipitation, soil type andland-use within the watershed. Outputs will include freshwater discharge, nutrient inputs
and sediment loading, each of which serves as
input into the system-level water quality
model. Data collected from within the watershed over the next two years will serve as initial input to the model for the purpose ofmodeling current conditions. Subsequently, we
will vary these inputs to explore how changing
conditions within the watershed affect water
quality and clam production.
Discussion
Clam aquaculture is an important and growing industry in the U.S. that is replacing fisheries on over exploited wild stocks andproviding economic development in traditional
coastal fishing communities. Sustaining clam
aquaculture in the coastal waters of the U.S.
will require an improved understanding of theinter-relationships between coastal land-use,water quality, primary production and clam
production. The modeling approach describedhere will provide an important suite of tools foradvancing our understanding of these linkages.
Initial estimates from a single embayment in
Virginia suggest that clam aquaculture has developed to a scale at which system-level impacts
on water quality and phytoplankton dynamics
may be evident (Table 1). Understanding thoseeffects, as well as how watershed inputs andwater column dynamics affect the growth andproduction of hard clams, requires an integrated modeling effort such as the one we described here. This effort is still underway witheach of the sub-models currently being refined
and
field
data
being
collected
forparameterization, calibration and verification.
When complete, the model output under129

current conditions will provide an understanding of the relationship between current clam
production levels and primary production
within Cherrystone Inlet. If the model results
indicate that the Cherrystone Inlet system isnear or has exceeded exploitation carrying capacity, then the explanation for the reported
decrease in clam growth will lie in the relationship between basin-wide phytoplankton production
andclamstocking
densities.
Conversely, if clam production is not limited byprimary production, then either local growing
conditions (e.g., sediment changes) or genetic
condition of the stocks may be the cause of thispattern.
The utility of this model goes beyond explaining the current growing situation in
Cherrystone Inlet. It will permit us to explore
various scenarios of stocking density, seasonaland inter-annual variations in primary production, and altered nutrient loading to assess
their impacts on clam production in the system. Furthermore, although the specific formulation of the model in this instance will be
for Cherrystone Inlet, once developed and calibrated, it should provide a useful starting point
for describing the relationship between primary production and clam aquaculture in othertidal creeks and embayments throughout themid-Atlantic region of the U.S. With the addition of basin-specific inputs on geometry,bathymetry, tidal elevations and currents, salinity and boundary conditions the model willserve to estimate exploitation carrying capacity for clam aquaculture in any system in the
mid-Atlantic region.
By coupling the clam physiology and population sub-models with the hydrodynamic-based
water quality model and linking it to a watershed loading model, we will achieve a powerfultool for use by natural resource managers andlocal governments that goes beyond traditional
carrying capacity models. For instance, this region is experiencing growing development
pressure, especially along the waterfronts adjacent to clam growing areas. The coupled models described here will permit us to run various

130Mark W. LUCKENBACH and Harry V. WANG

hypothetical watershed development scenariosand predict the impacts on water quality andclam production. This information will be valuable in permitting informed decisions about
coastal development and its impacts on a valuable aquaculture industry.
Acknowledgments
Development of various components of thewater quality and watershed loading models
have been funded by the Maryland Departmentof the Environment and Virginia Departmentof the Environmental Quality. Development of
the carrying capacity model is being supported
by NOAA Sea Grant Program.
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水研センター研報，別冊第 1 号，133−142, 平成16年
Bull. Fish. Res. Agen. Supplement No. 1, 133-142, 2004

133

Environmental change in the coastal environment: challenges forthe selection and propagation of filter feeding species in aquaculture,stock enhancement and environmental rehabilitation.
Roger MANN*
Abstract Selection of species for aquaculture, fishery stock enhancement and environmental rehabilitation or restoration in the coastal zone requires consideration of the factthat species have evolved over geological time whereas changes in the coastal environment have occurred predominantly over recent historical time, often with the largest
changes occurring within the past decades of human activity. The evolutionary issue isparticularly noted with filter feeding molluscs, where extant species supporting bothmajor natural fisheries and aquaculture have ancient lineages and evolved in environments that may have differed considerably from the locally turbid, nutrient enriched,disturbed (through watershed change and local activity) waters in which they now survive. We cannot presume that native species are strongly selected to survive in the environments in which they currently reside. Neither can we presume that they will be
successful candidates for aquaculture, fishery stock enhancement, environmental rehabilitation (the restoration of ecological services in community structure), or environmental restoration (restoration of native community structure with associatedecological services). Watershed and coastal use impacts have, over recent human history,altered community structure in coastal waters, and diminished the ability of surviving
community members to perform the ecological services that are one end product of theirevolution. A challenge is therefore presented to students of intensive species culture, extensive fishery enhancement, and ecological rehabilitation or restoration: how to best
use the tools of husbandry in concert with large and small scale environmental manipulation to promote progress in the designated area of interest? Ecological rehabilitation
or restoration centered on cornerstone filter feeding species must employ local environmental rehabilitation, but this will only be successful if it is accompanied by a wider
commitment to watershed management protocols that protect all life history stages, including the delicate early stages. A numerical argument for this approach, based on
Paulik life history models, will be presented. Intensive aquaculture, by comparison, may
be able to progress in marginal environments where delicate early life history stages arecultured in controlled situations, thus limiting mortality, before transfer to open systems. Fishery enhancement resides between these options, where a dual role of supplementing local reproduction is balanced against increased exploitation of commercial
product.
Key words: bivalve molluscs, aquaculture, stock enhancement, environmental rehabilitation

2003年 6 月12日受理（Received on June 12, 2003）* 1 Virginia Institute of Marine Science, Gloucester Point, VA 23062 USA, phone: 804/684-7360, FAX: 804/684-7045,
Email: rmann@vims.edu

134

Roger MANN

Selection of species for aquaculture, fisherystock enhancement and environmental rehabilitation or restoration in the coastal zone requires consideration of the fact that species
have evolved over geological time whereaschanges in the coastal environment have occurred predominantly over recent historicaltime, often with the largest changes occurring
within the past decades of human activity. A
history of the traits driving selection of
aquaculture species is given by Mann (1984a),and emphasizes the roles of species low in thefood chain with physiologically tolerant adultstages and reproductive cycles that are easily
subject to control and manipulation. Filter
feeding bivalve molluscs fit these requirements.
The evolutionary time frame is particularly
important with filter feeding molluscs, where
extant species supporting both major natural
fisheries and aquaculture have ancient lineages
and evolved in environments that may have differed considerably from the locally turbid, nutrient enriched, disturbed (through watershedchange and local activity) waters in which they
now survive. This grouping includes extant
oysters, mussels and clam species of commercial interest, especially those under active
aquaculture. Oysters are a notably primitive
form, exemplified by the loss of the second adductor to the monomyarian form. They havesurvived by migrating over geological time into
geologically ephemeral estuarine environments, being served in this purpose by theircomplex life history employing pelagic larval
forms. Recent commentaries on the evolutionof the larval form summarized in McEdward(1995) and Hall and Wake (1999) emphasize why
the combination of these "dual" evolutionary
paths of the adult and larval forms in responseto stage specific selection pressures has left the"primitive" bivalves so well equipped to respondto rapid (in the evolutionary time frame)changes in local environments that would typically lead to local extinction. Oyster populations in the Chesapeake Bay provide an
excellent example of successful invasion in geologically ephemeral environments. The current

bay is a product of 8,000 years of Holocene sea
level rise (Haven and Whitcomb, 1983; Hargis1999). Recent fossil deposits including oyster
shells can be found many kilometers offshoreof the current shoreline in depths corresponding to earlier sea level stanzas. These illustrate
both the changing environment with sea level
rise over recent geological time and the accompanying "migration" of the oyster populations.
Substantial changes have occurred in both
the watershed biology and physical environment of the Chesapeake Bay since the arrival of
European colonists. The past four centuries
have been marked by deforestation for agriculture, urban development on the shoreline of thebay or its tributaries, and increasing, andmostly uncontrolled exploitation of the fisheryresources for much of the period. The humanpopulation in the Chesapeake Bay watershed
has reached approximately 15 million with projected growth rates at double the national average for the next twenty years. The record ofwatershed change is abundant from both directpublic records and indirect evidence fromsources such as pollen records of land usechange. Extensive records of recent and current
land use patterns are available from the U.S.
Environmental Protection Agency world wide
web site at http://www. chesapeakebay.
net/bayprogram with summary information
changes in land use practices such as no till
farming and shoreline buffer zones designed toreduce non point source sediment and nutrient
runoff into the bay. In addition, changes in thebay and tributary morphologies have resulted
from river dredging and shoreline development. Fundamental changes in the biology of
the aquatic system have been caused by overfishing and critical environmental degradation.
Failure to return shell to the bottom after oyster harvest has resulted in once significant
three dimensional reef structure being reduced
to patchy monolayers of substrate for extant
oyster populations with accompanying change
in both the complexity of the associated communities and the ecological services they provide (compare data from Baylor 1894 with

Management of bivalve species in stock enhancement and environmental rehabilitation

Luckenbach, Mann and Wesson 1999). This
rapid, in an evolutionary time frame, change inlocal environment has clear implications forchanges in community structure in the local
community (Mann, 2001). We cannot presume
that target species are strongly selected to survive in the environments in which they currently reside, as opposed to those in which they
evolved. Neither can we presume that they will
be successful candidates for aquaculture, fishery stock enhancement, environmental rehabilitation (the restoration of ecological services
in community structure), or environmental restoration (restoration of native community
structure with associated ecological services) inthese rapidly changing environments. Indeed,this realization has been a driving force for theuse of non-native species in both intensive
aquaculture and fishery enhancement in recent
decades (see Mann 1979, 1984b; Rosenfield andMann, 1992).
A challenge is presented to students of intensive species culture, extensive fishery enhancement, and ecological rehabilitation or
restoration: how to best use the tools of husbandry in concert with large and small scale
environmental manipulation to promote progress in the designated area of interest?
Ecological rehabilitation or restoration centered on cornerstone filter feeding species must
employ local environmental rehabilitation, but
this will only be successful if it is accompanied
by a wider commitment to watershed management protocols that protect all life history
stages, including the delicate early stages. The
cost-benefits of each component of this restoration or rehabilitation strategy on the performance of a target species in culture or as afishery are of direct interest. Can specific management actions be targeted at improving the
response of the most susceptible life history
stages to specific stresses? A numerical approach to this question is offered by consideration of Paulik life history models.
Paulik (1973) provide a useful conceptual toolfor quantitative descriptions of the stock - recruit relationship in commercially exploited135

marine fish species. Examples are discussed inRothschild (1986). The graphical presentationof the concept, the Paulik diagram, consists ofa four-quadrant plot. Quadrant 1, proceeding
in a clockwise direction, is the desired stockrecruitment function. It is constructed fromthe end product of the other three quadrants.
The second quadrant relates stock size to egg
production and thus incorporates absolute
number of fertile individuals, demographics
through size specific fecundity, and the integrated effect of environment and prior feeding
history on fecundity. The third quadrant relates egg production to larval production andincorporates spawning synchrony, spawning
behavior where applicable, and density dependent fertilization success. The fourth quadrant
describes the relationship of larval production
to recruitment to the subsequent spawning
generation. In fish populations this does not involve a transition from pelagic to attached or
sessile benthic form, although a larval to adultmetamorphosis is included. Application ofPaulik models to benthic invertebrates withcomplex life histories dictates that this quadrant include larval growth and loss to
predation and dispersal to hostile environments, settlement and metamorphosis, andpost settlement growth to sexual maturity.
Applications of such models to cultured benthic
species are somewhat rare, yet the structure
provides a useful tool for integrating studies ofindividual life history stages. Of particular importance in the context of stresses acting oncoastal ecosystems is the ability to quantitatively describe the impact of a stress on one life
history stage on a separate but subsequent life
history stage. In the coastal zone where increasing eutrophication and other pressures
can disproportionately impact one life history
stage over another in isolated test challenges
the utility of this holistic approach is both obvious and powerful.
Mann and Evans (1998) adapted the approachof Paulik (1973) in estimation of oyster,
Crassostrea virginica, standing stock, larval
production and advective loss in relation to136

Roger MANN

observed recruitment in the James River,
Virginia. The present illustration simplifies
this approach using a virtual population to examine the effects of three parameters on recruitment in subsequent generations. These
parameters are (1) varying egg production byvarying age specific mortality of the parent
population as a proxy for disease impacts, (2)varying duration of larval period in response to
sub-optimal feeding conditions, and (3) varying
loss to advection related to estuarine tidal exchange. All three variants are examples of theeffect of possible environmental stresses on
critical life history stages. Others can be examined by the method described below as appropriate to the location under stress.
Methods
To summarize and simplify Mann and Evans(1998), recruitment to the 25mm size class is estimated from larval supply thus:(Ftot×Fq×Fs×Fd×Ff )×(1−exch)2d×(1−Lmort)d×
Psub×Pfoul×Pmet×(1− Jmort)dp
where:
Ftot is total egg production and estimatedfrom size specific fecundity. It is a cumulative
total for all individuals (Find) in all size classes
and typically estimated from length:dryweight estimators. In the current illustration
all sizes below 40mm are considered young of
the year (spat) and do not contribute to spawning, and fecundity is estimated from relationships given in Thompson et al (1996), and Mannand Evans (1998).
Fq is a sex ratio modifier. Cox and Mann
(1992) suggest parity in sex ratio. Given thelack of other data a single sex ratio modifier,Fq, with a value of 0.5 (50％ female in all sizeclasses) is used in this illustration.
Fs: Find and hence Ftot can be modified based on
salinity (S) effects. Mann and Evans (1998) suggested the following estimators for Fs:
if S＞13.5, Fs＝1.0
if S＜13.5, thenFs＝[(S−8.0)/(13.5−8.0)]×1.0＝(S−8.0)/5.5
Fd modifies fecundity for disease effects withvalues ranging from 1.0 to 0.0. In the present illustration it varies from 1.0 to 0.75 (a 25％ reduction based on disease impact).
Ff describes a density dependent multiplierfor fertilization efficiency with values from 1.0(100％ fertilization) to 0.0 (no fertilization). It isbased on Levitan (1991) where:log ％ fertilization＝[0.72 (log OD)＋0.49] or,％ fertilization＝[0.49×OD0.72]
where OD is oyster density in numbers m−2.
In the present illustration it is rewritten thus:
Ff＝0.0049×OD0.72
Production of larvae (strictly speaking embryos or fertilized eggs) m−2 is therefore estimated by (Ftot × Fq × Fs × Fd × Ff ) in units oflarvae m−2.
(1−exch)2d : Mann and Evans (1998) estimatedretention of the larvae within the James Riverduring planktonic development using the three
dimensional flow model of Hamrick (1992a,
1992b) to provide source and sink data at scales
within the estuary. For the present illustrationa simple dilution function is used that assumes
uniform dispersal within the estuary and proportional loss on each tidal cycle, that is larvae
are assumed to be neutrally buoyant and exertpassive swimming behavior in response to oriented stimuli. Thus larval numbers decreased
with days with the duration of planktonic development by the function (1 − exch)2d whereexch is proportional volumes exchanged on eachtide. The value of exch varies in the current
study between 0.1 and 0.2 (0.2 equals a 20％
exchange per tidal cycle) and d is the durationof the larval development (＝planktonic) period.
The correction 2d is used with a simple assumption of 2 tidal exchanges per day. In the current
study d varies from an optimum of 21 days,
based on values from Mann et al (1994), Mannand Evans (1998), Bochenek et al (2001) andPowell et al. (2002), to a sub-optimal value of 25days based on assumed reduction of feedingand hence growth in low salinity and/or highturbidity regions.
(1−Lmort )d estimates larval mortality in thewater column. Lmort is the daily larval mortality
rate (a proportional value between 1.0 (all died)Management of bivalve species in stock enhancement and environmental rehabilitationand 0.0 (no mortality)). Survival is (1−Lmort) fora period of one day or (1−Lmort )d for a d day
planktonic development period. For the current
illustration Lmort is set at 0.05, 0.06, 0.07. 0.1 andan extreme value of 0.25. The decreasing exponential relationship insures a gradual decreasingly sensitive response to increasing values ofd. Modification of the original number of larvae to account for dispersal loss and mortality
provides an estimate of larvae surviving to immediate pre-metamorphic size. The transition
to an attached benthic form requires successful
location of substrate, that the substrate not be
occluded by competing organisms, and that thelarvae have sufficient energy reserves to complete the metamorphosis to a juvenile feeding
form.
Psub, a dimensionless modifier with a value between 1.0 and 0.0, describes the probability offinding suitable substrate. The time scale andavailability of shell substrate is critical to successful recruitment (Morales-Alamo and Mann
1990). Consider that a shell layer one-cm thickcovering one-sq. m of bottom has a volume of
10L. For the current illustration a premise isadopted that a shell layer a minimum of one cm
thick is required to offer a suitable substrate.
Psub is estimated thus:
if shell volume＞10L m−2, Psub＝1.0
if shell volume＜10L m−2,
Psub＝0.1×Shell Vol. (in liters)
Pfoul describes proportional occupation of thesubstrate by competing organisms and varies
between 1.0 (no fouling) to 0.0 (complete preclusion of settlement). Rheinhardt and Mann
(1990) suggest a value of Pfoul ＝0.33 based onfield studies in the James River. For the current illustration a constant value of 1.0 is employed.
Pmet describes the probability of successful
completion of metamorphosis to the attachedform on a 1.0 (all survive) to 0.0 (no survival)
scale. For the present application the value isset at 0.20.
Recruitment to the benthos is therefore estimated from larval supply values by incorporating (1−exch)2d, (1−Lmort)d, Psub, Pfoul and Pmet thus:

137[(Ftot×Fq×Fs×Fd×Ff )×(1−exch)2d×(1−Lmort)d×Psub×Pfoul×Pmet](1−Jmort )dp modifies this estimator for post
settlement mortality and growth rates, both ofwhich are known to be size dependent (Roegnerand Mann, 1995). Mann and Evans (1998) describe daily juvenile mortality rate as Jmort (proportional with a value between 0.0 and 1.0).
Survival is (1−Jmort)dp where dp is the number ofdays to grow to a defined size. Based on valuesof Jmort in Roegner and Mann (1995), Mann andEvans (1998) suggest a cumulative mortality to
8 mm length of 93 ％ over a 28 days period, acalculated value for Jmort of 0.09. Thus (1−Jmort)dp
for the current study is set at 0.07 to 8 mm
length. Above this length Jmort is lower and set
at 0.05 for another 25 days until a size of 25 mm
when the surviving individuals are considered
recruits to the subsequent generation(Eggleston, 1990). For the current illustration(1 − Jmort )dp incorporates two mortality rates
with a cumulative mortality value for the premetamorphosis larvae to 25 mm size class, including a Pmet value of 0.20 is 99.84 ％, or a
proportional survival of 0.0016.
Demographics for a virtual population weregenerated from a data set describing Horse
Head Reef in the upper James River for the period 1993-1996 (National Oceanic Atmospheric
Administration
Chesapeake
Bay
Stock
Assessment funds to R. Mann and J. Wesson,
Virginia Marine Resources Commission). This
population was chosen because it was (a) stable
over that period with respect to recruitment,
total oyster density, and oyster demographics,and (b) suffered essentially no mortality due todisease. The size frequency distribution (in 5m
size classes) was converted to an age frequency
demographic using an a modified Von
Bertalanffy plot with growth oscillation corresponding to seasonal change in growth rate
(Evans and Mann, unpublished data based onfield data from Horse Head reef in the JamesRiver, Virginia, by Mann and Morales). Thistakes the form:
Lt＝Linf (1−e芋K拡廓t芋t 較茨A芋B郭),where: A＝C sin (2π(t−ts)) / (2π),
0138Roger MANN

and B＝C sin (2π(to−ts)) / (2π)
The parameters are: Lt is the length at timet, Linf is asymptotic length set at 120mm basedon field observations, K is the growth constant,
to is age at which length is zero, C is the amplitude of the growth oscillation, and ts is thestarting point of the oscillation with respect tot＝0. The parameters of this function were estimated by fitting a rearranged function to thesize increment data of a data set which records
serial increase in length over time so that wehave values of L1, L2, and so on. The rearranged
function is:
L2＝Linf (1−(1−L1/Linf) e芋K拡廓t 芋t 較茨A 芋B 郭)
where A'＝Csin (2π(t1−ts ))/(2π),
and B'＝Csin (2π(t2−ts ))/(2π)
The parameters were estimated as follows:
K＝0.204, to＝0.36, and ts＝0.608.
The virtual population demography is illustrated as population A in Fig. 1A, together
with a series of subsequent populations (B-E inclusive) generated by gradually increasing age
specific mortality (illustrated as cumulative
mortality in Fig. 1B) specifically chosen to
simulate the effects of increasing disease prevalence and intensity. It is notable that theextreme population, E, represents an approximation of current disease tolerance in the mostselected strains under typical disease challenge
in medium salinity waters. Each population
has the 25mm size class, here considered the
young of the year recruits or zero class, set at
100 oyster m−2 . This corresponds to the end
point of the above "recruitment to the benthos"
estimator. In all simulations, which are run asa sequential spreadsheet in Microsoft Excel thebarometer for successful recruitment of a subsequent generation is attaining a 25mm size
density of 100 oyster m−2.
袷

2

袷

1

options that can be run with the simulations
they illustrate the following important points:
Under low tidal exchange and optimum larval
development the recruitment values are very
high even with high larval mortality rates (Fig.
1C). Consider, however, that the employed scenario uses many optimal conditions including
no reduction in fecundity attributable to salinity, no shell limitation and only modest competition for substrate. This is very much an
optimal scenario.
(a) Increasing larval duration by only 4 days
reduces recruitment considerably (Fig. 1D).
(b) Increasing tidal loss to 20％ drives all recruitment values below the critical 100m−2
even with everything else at optimum (Fig.
1E).
(c) Reducing fecundity by 25％ as a proxy for
impact of disease and/or salinity has a
proportional effect (Fig. 1F).
(d) Reducing fecundity by 25％ and increasing tidal loss to 15％ provides options for
all population structure from A through E
to recruit at＜100m−2 depending on larvalmortality rate, even with all other factors
optimized (Fig. 1G, 1H).
These examples underscore the very nonlinear response of recruitment to various combinations of tidal exchange, reduced fecundity,
and larval duration as we move away from an
optimal combination. They also illustrate thateven the most stable population structure, A in
Fig. 1A, to produce marginal recruitment evenwith shell and competition (Psub and Pfoul) optimized and with no consideration of greater impact of post settlement mortality. In a large
number of slightly less than optimal scenarioseven a population with increased mortality
under sustained disease pressure−E in Fig. 1A−are prone to inadequate recruitment.

Results
Discussion
The simulation was run for a single generation time frame with each of A-E as the starting demographic under various scenarios andthe end points illustrated in Fig. 1C − 1H.
Although these are just a subset of the many

These limited simulations underscore theneed for holistic approaches to restoration or
response to multiple stresses. Approaches that
focus on only optimizing one life history stage

Management of bivalve species in stock enhancement and environmental rehabilitation

139

Fig. 1. Virtual oyster population year class structure (1A) and cumulative mortality (1B). Estimated recruitment(1C-1H) is shown under a variety of tidal loss, larval duration, and reduced fecundity scenarios

140

Roger MANN

response may be strongly compromised. For
example, even moderate disease tolerance alone
will not be effective under sustained diseasepressure, and restoration based only on thisimproved trait will fail. In practical terms, failure to effect restoration in the optimal location
will result in failure in recruitment. Optimal
location is a product of species traits that arearguably very conservative because of the evolution of the species (again see McEdwards
1995, Hall and Wake 1999) in combination withcirculation patterns of the host estuary-aunique feature. Critical oyster traits in thismix include, but are not limited to, adult egg
production, a trait for which we have not actively selected in breeding programs to date,and larval feeding ability and swimming behavior in turbid conditions. Fecundity is critical to driving the simulation as shown, yet weknow essentially nothing of size-fecundity relationships under challenging conditions inwhich we are attempting restoration. Both larval traits are arguably very highly conserved
because of limitations in the velar structure
and the clear selective pressure over time forlarval forms that recruit in optimal rather
than sub-optimal environments. Turbid conditions can be viewed as transitions in the ephemeral lives of estuaries on a geological timeframe, signals for oyster populations to moveas they have done over periods of sea level rise.
Larvae have no reason to evolve to survive inregions doomed to local extinction by rapidlychanging environments. Their conserved feeding abilities and behavioral strategies have
served them more than adequately without
such abilities. Restoration efforts thus match asuite of larval traits with conditions that westrongly suspect are very far from optimal, yet
we often proceed in the absence of knowledge as
to how debilitating this mismatch may be to
the desired end point. These troubling scenarios, well founded in both our current understanding of the evolution of complex life
history and simple numerical simulations of recruitment processes in virtual populations
under near optimized conditions, drive the needfor focused research to address these deficiencies. Without quantitative descriptors of the response of each life history stage to the local
stresses, their subsequent holistic synthesis ina practical model, and employment of sensitivity analyses, the options for adaptive management of long term, often very costly
restoration efforts, are limited, indeed soberingand probably doomed to failure. Intensive
aquaculture, by comparison, may be able toprogress in marginal environments where delicate early life history stages are cultured incontrolled situations, thus limiting mortality,
before transfer to open systems. Fishery enhancement resides between these options,where a dual role of supplementing local reproduction is balanced against increased exploitation of commercial product.
Acknowledgements
This manuscript represents the result of cumulative effort over many years from several
funding sources including National Oceanicand Atmospheric Administration (NOAA)
Oyster Disease Program Grant number
NA26FL0385-01, Chesapeake Bay
Stock
Assessment
Programgrant
number
NA07FU0539, Virginia Sea Grant number
115845-GL1 0003, National Science Foundation
grant number OCE-9810624, and EPA
Chesapeake Bay Program award number CB983649-01-0. Preparation of the manuscript was
supported by the Reves Center forInternational Studies at the College of William
and Mary. Partial travel support to attend the
31st United States-Japan Cooperative Programin Natural Resources (UJNR) Aquaculture
Panel Meeting was provided by NOAA. Thesesources of funds are gratefully acknowledged.
This manuscript is dedicated to my son,
Matthew Francis Mann, who also attended the
UJNR meeting, for his continuing intellectual
curiosity and reminding me that scienceshould, above all things, be fun. This isContribution Number 2590 from the Virginia
Institute of Marine Science.

Management of bivalve species in stock enhancement and environmental rehabilitation

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based model of the growth and development of Crassostrea gigas larvae. J.
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Cox C. and Mann R., 1992: Temporal andSpatial Changes in Fecundity of Oysters,
Crassostrea virginica (Gmelin) in theJames River, Virginia, U.S.A. J. Shellfish
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Eggleston D. B., 1990: Behavioral mechanisms
underlying variable functional response ofblue crabs, Callinectes sapidus, feeding on
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Hall B. K. and Wake M. H., 1999: The origin
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Hamrick J. M., 1992a: A Three-Dimensional
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Mann R., 1984a: On the selection of
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Mann R., Morales-Alamo R., and Rainer J. S.,
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Crassostrea virginica Gmelin, in the JamesRiver, Virginia, during 1987-1988. J.
Shellfish Res., 13(1), 157-164.
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Invertebrate Larvae, CRC Press, 464pp.
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Powell E. N., Bochenek E. A., Klinck J. M., andHofmann E. E., 2002: Influence of foodquality and quantity on the growth anddevelopment of Crassostrea gigas larvae: amodeling approach. Aquaculture, 210, 89117.
Rheinhardt R. D. and Mann R., 1990:
Development of Epibenthic Fouling
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Rothschild B. J., 1986: Dynamics of Marine
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Crassostrea virginica Gmelin with respect
to tidal zonation. Marine Ecology Progress
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Living Organisms Into Aquatic Systems,
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Thompson R. J., Newell R. I. E., Kennedy V. S.,
and Mann R., 1996: Reproductive processes
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A.F.), University of Maryland Sea Grant
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水研センター研報，別冊第 1 号，143−151, 平成16年
Bull. Fish. Res. Agen. Supplement No. 1, 143-151, 2004

143

Integrated aquaculture systems for nutrient reduction in agricultural
wastewater: potential and challenges*
Andrew M. LAZUR* 1 and Frank LETEUX* 2

Abstract The integration of aquaculture with agriculture, such and fish production
with poultry , has been practiced for hundreds of years and takes advantage of the nutrient output of one crop to increase pond primary productivity, subsequently, enhancing herbivorous fish production. Applying this integration concept for the purpose of
reducing the environmental impact of agriculture via the nutrient extraction ability ofvarious shellfish, plant and fish species, is however, a relatively new concept and is increasingly justified by nutrient discharge regulations and associated increasing effluent
treatment costs. Agricultural operations, such as animal feedlots, are specific nutrient
point sources in which integration with extraction aquaculture could reduce environmental impact. In addition to playing a key role in nutrient reduction, extraction
aquaculture species can be an important source of income, critical to offsetting increasing nutrient treatment costs and increasing farm profitability. This paper will review
current strategies to apply this concept in the field, present an overview of specific efforts in Florida and summarize the challenges of implementation of integrating production of various aquaculture species to reduce nutrients in agricultural wastewater.
Key words: Integration, aquaculture, agriculture, nutrient reduction

Agriculture has increasingly been identified
as a major source of nitrogen and phosphorus
contributing to eutrophication of numerous
bodies of water worldwide. Traditional grain
and vegetable row crop production with nitrogen and phosphorus based fertilizer applications, accounts for the majority of non-point
nutrient sources in many watersheds including
the Chesapeake Bay and Florida Everglades,
USA (Boesch et al., 2001; Sharpley, 2002;
SFWMD, 2002a). The vastness of land dedicatedto this type of agriculture presents a challenge
for specific nutrient discharge treatment.
However, progress in reducing nutrient runoff
has been achieved with adoption of specificchanges in production practices, or best

management practices, such as no till seedingor planting winter cover crops to minimize soil
erosion and enhance plant absorption of nutrients (Staver and Brinsfield, 1998; SFWMD,
2001a). Concentrated animal feeding operations(CAFO's) such as dairies, poultry houses, cattle
and swine feedlots, and aquaculture, however,are finite point sources of nutrients, and therefore, specific nutrient capture or treatment
systems could be more easily employed.
Numerous examples of aquaculture integrated with agricultural crop and animal production exist including fish culture with rice,
fruit, ducks, chicken production and have been
for hundreds of years in Asia (Beveridge andLittle, 2002; Little and Edwards, 1998; Little

2003年 6 月12日受理（Received on June 12, 2003）* 1 University of Maryland Center for Environmental Sciences, Horn Point Laboratory, P.O. Box 775, Cambridge, MD 21613 USA* 2 Florida Department of Agriculture and Consumer Services, Office of Agricultural Water Policy, 1203 Governor's Square Blvd., Suite 200
Tallahassee, FL 32301 USA* Presented in the Satellite Symposiun held in Shiogama on Oct. 21, 2002.

144

Andrew M. LAZUR and Frank LETEUXand Satapornvanit, 1996). In these cases, thegoal is to maximize food production by utilizing waste from one crop to enhance productionof another, in effect increasing nutrient utilization, and consequently, and until recently unintentionally, reducing nutrient impacts.
Aquaculture species such as clams, mussels,
oysters, algae and macrophytic plants are relatively efficient in assimilating or extracting nitrogenandphosphorus
from
their
environment. (Boyd, 1995; Jones et al., 2002;
Lasalle and Posadas, 1997; Newell, 1988;
Schwartz and Boyd, 1995). In addition, numerous studies have shown the benefits of applying
polyculture or culture of numerous species toreduce the nutrient and suspended solid loadingof aquaculture effluent (Drenner, et al.;Hopkins et al., 1993; Jones et al., 2002;
Schwartz and Boyd, 1998). The field of
aquaponics, integrating fish and plant production, whereby fish wastes are used as fertilizer
for vegetable crops has demonstrated successful method of increasing nutrient utilizationand improving farm income (Racocy, et al.,
1992; and Diver, 2000). Using this extraction attribute of aquatic species in conjunction with
agricultural crops specifically to reduce nitrogen and phosphorus discharges, or aquaculture
serving as environmental rededication, is stillin the development phase with limited field applications and research.
Current nutrient loading and reduction
strategies in Florida
In south Florida agriculture runoff has been
identified as the major contributor of theeutrophication of the Everglades and its watershed including Lake Okeechobee, Florida's largest lake. Phosphorus is the key limiting
nutrient in freshwater systems and increases inphosphorus loading play a major role toeutrophication of the Everglades. SFWMD(2002a) estimated the total phosphorus importto the Lake Okeechobee watershed is over 1,800
tons per year originating from the major usesof the watershed including: improved pasture(33 ％); truck crops (32 ％); dairy (27 ％); and citrus (11 ％).
Recent nutrient management strategies focusing on phosphorus reductions include establishment of total maximum daily loads(TMDL's) for industries and CAFOs including
an effluent standard of 40 ppb phosphorus forfarm discharges. The use of best management
practices (BMP's) and the employment of best
available technologies (BATs) for many of the
agricultural commodities including, beef cattle,
poultry, citrus, and dairy are being establishedto achieve the new discharge standard(SFWMD, 2002b). Attempts to reduce phosphorus loading on a large watershed scale in theLake Okeechobee region include: establishmentof artificial wetlands, large chemical treatment
ponds (which pump and inject untreated waterwith limestone, iron, humic acid, alum or polymers to bind P prior to discharging water), soil
treatments, limiting nutrient applications, confinement barn-based technology, on-farm storage or retention (permanent storage) ponds,
and governmental buy out of dairies (SFWMD,
2001b). These methods are very often costly toconstruct and maintain, have specific site limitations, and in the case of chemical treatment
ponds and wetlands, have only temporary benefits due to substrate saturation and siltation.
Dairies, which often concentrate several hundred to nearly two thousand animals per barn
or dairy facility, have been identified as major
phosphorus importers to Lake Okeechobee.

Fig. 1. Diagram of wastestream treatment and partial water re-use of a typical south Florida dairy

Integrated aquaculture systems for nutrient reduction in agricultural wastewater

Using daily nutrient excretion estimates of
Van Horn, et al. (1998) of 0.27-0.46 kg N and0.05-0.068 kg P per dairy cow, total daily nutrient loading of barns in the Lake Okeechobee
watershed are 81-828 kg and 15-122 kg of N and
P respectively. They further show that solids
collection, composting and crop irrigation of
pond treated manure can capture significant
levels of N and P and crops of bermudagrasshay and alfalfa periodically irrigated withdairy barn effluent resulted in 20-34 ％ and 2249 ％ absorption of N and P respectively for thetwo crops.
Since the 1980's, the predominant method fortreating CAFO wastes and effluent has been
the use of individual or a series of lagoons or
detention (temporary storage) ponds, both anaerobic and aerobic. The degree of nutrient reduction from ponds is highly variable anddepends on many factors such as pre-pond solids capture, pond depth, surface area, oxygen
concentrations, littoral area, plant species andhydraulic retention time. Increasing concern
and government regulation of dairy effluent
has prompted the necessity for additional or alternative nutrient reduction practices. Many
dairies have increased the scale of treatment
ponds and partially recycle water from the
aerobic ponds for use as barn wash down waterand for crop irrigation (Fig. 1). A waste treat-

Fig. 2. Conceptual diagram of a integrated dairy aquaculture operation with multi-stage water treatment and crop production. Shaded are in the aerobic
pond depicts aquatic plant littoral zone.

145

ment practice similar to the one depicted in Fig.
1 has resulted in reductions of 50 ％ and 76 ％for N and P respectively with the majority of
the remaining nitrogen being volatilized (Van
Horn , et al., 1998). The present challenge forthis treatment practice is dealing with storm
water discharge which is of special concern inthe area due to low elevation and periodic hurricanes. New discharge requirements with a
total maximum daily discharge (TDML) of 40
ppb phosphorus will mandate farms to treat
storm induced off-site discharges as well, requiring additional treatment innovation andinvestment.
The integrated dairy/aquaculture approach
One approach being developed for dairies inthe Lake Okeechobee area involves incorporating culture of aquatic species such as Tilapia,
paddlefish, baitfish (fish used as bait for recreational fishing), freshwater clams, and plants
to provide additional nutrient assimilation, andin addition produce secondary crop income(Fig. 2). In this scenario, modifications to thewater treatment ponds and ditches would benecessary as follows: 1) addition of more efficient solids removal equipment; 2) reshape pondbottom and slopes of anaerobic pond to facilitate removal of sludge accumulation in anaerobic pond; 3) renovate aerobic pond bottom toallow periodic fish harvesting; and 4) modify
ditches and to enable culture and periodic harvest of the freshwater clam Corbicula fluminea.
With the modifications in place several
phases of water treatment and nutrient reduction would occur:
Stage 1-Solids Collection:
Solids collection via use of a screen separator
can remove 20-30 ％ of the organic matter frommanure flushed with water that averages 72 ％moisture and is comprised of 1-1.6 ％ N and
0.12-0.15 ％ P on a dry matter basis (Van Hornet al., 1998). They also report an average of 45kg of feces is defecated per cow daily. Taking
into account the screen separator collection
rate and the moisture and phosphorus content

146

Andrew M. LAZUR and Frank LETEUX

of organic matter, a reduction of approximately 25 ％ of the phosphorus or 0.004 kg
P/cow is possible.
Stage 2-Anaerobic Pond:
Approximately 60 ％ of the nitrogen can bevolatilized from an anaerobic pond via
denitrification depending on hydraulic retention time. Phosphorus, however, is not removed
by any organic mechanism within the anaerobic pond, but will accumulate into the bottom
sludge. Phosphorus reduction estimated up to
50 ％ (Van Horn et al., 1998) can occur whensludge is periodically collected and removed
from the pond.
Stage 3-Aerobic Ponds:
Phosphorus absorption or removal can occur
by several mechanisms within the aerated
pond: fish harvest, macrophytic plant absorption, absorption by the pond sediment andphytoplankton. The aerobic ponds should receive intense mechanical aeration to enhanceoxidation processes and to ensure adequate
oxygen levels for the Tilapia stocked into thepond. The Tilapia serve as a forager on plankton and detritus, hence removing both nitrogenand phosphorus from the water. Harvesting
Tialpia 2-3 times per year is possible and can beprocessed into a fish meal source for animal
feeds. With a phosphorus and nitrogen content
of Tilapia of 1.6 ％ and 2.7 ％ live weight respectively (Lovell, 1989) and using mean annual
production of Tilapia of 1,600 kg/hectare/yr in
cow manure fed ponds (Racocy and McGinty,1989), an estimated 25.5 kg P and 43 kg N ha−1
y−1 removal is achieved.
In addition, the aerated pond has a littoralzone where aquatic plants can assimilate or extract additional phosphorus. Total export of P
will depend on plant species and plant area.
Common native emergent plant species which
are effective in assimilating nutrients and havevalue in mitigation markets include: duck potato
and arrowhead, Sagittaria spp.,
pickerelweed, Pontederia spp., and many shoreline grasses or rushes such as bulrush, Scirpus
spp., and Juncus spp. Mitsch and Gosselink(2000) presented potential nutrient retention

rates per area of marsh or wetland ranging
from 3 -66 g N m−2 y−1 and 0.36-5.6 g P m−2 y−1.
In existing dairy operations, most of the aerobic ponds range from 4 -14 hectares in size andutilize 4 : 1 pond levee slopes, thus providing
approximately 450 square meters of littoralzone per hectare of pond. Using nutrient retention rates suggested by Mitsch and Gooselink,
nutrient retention would amount to 0.5-5.6 kg
P ha−1 y−1 and 3-65 kg N ha−1 y−1 . Aquaticplants can also serve as an important secondary crop for sale in the restoration or mitigation markets.
Phosphorus readily binds with soil particles
and accumulates in aerobic pond bottom muds.
Pond sediment becomes saturated with phosphorus, which can be released into the water
when the bottom sediments become anaerobic(Newell, 2003). The long-term P removal by the
pond sediment will vary on several factors including degree of oxygenation, pH, soil type
and plant absorption, but would be insignificant compared to other sources of P removal
mechanisms in the aerobic pond.
Phytoplankton are efficient utilizers of phosphorus. Nurdogan and Oswald (1995) report 1030 ％ absorption of phosphorus by microalgae
in high-rate holding ponds and studies by
UNEP (1999) show a 30-50 ％ uptake of P by
microalgae in the aerobic pond portion of awaste stabilization pond system. The phosphorus uptake of microalgae is significant and appreciably greater than the potential from fish
harvesting and marcrophytic plants in the perimeter littoral zone.
Stage 4-Baitfish Ponds:
Within the baitfish production ponds, species
such as golden shiner, Notemigonus crysoleucas
and bull minnow, Fundulus spp. feed on
phytoplankton and zooplankton, and with harvesting further N and P assimilation and export from the system is achieved. Expectedannual production of golden shiners using thewild spawn method (low fish yield culture practice where broodfish and offspring are raised insame pond) and with no commercial feed added
is 110-330 kg ha−1 (Stone et al., 1997).

Integrated aquaculture systems for nutrient reduction in agricultural wastewater

Phosphorus removal rates from harvestingbaitifsh would be expected to range from 1.85.3 kg ha−1 y−1 . In addition, the baitfish ponds
proposed to be 4 hectares in size each would
have similar littoral zone area and nutrient absorption as the aerobic pond on a per hectare
basis. As in the aerated pond stage,
phtoplankton would be present in the baitfish
ponds and, therefore would be a major meansof P uptake. In addition, incorporating theminor stocking (1-20 fish/ha) of paddlefish,
Polydon spathula, an efficient zooplankton
consumer, contributes to nutrient reduction
benefit and also offers high value for its meatand roe. Paddlefish cultured in a 5 hectare
reservior within a 200 hectare cattle watershedhave been shown to survive for over 15 years
and reach up to 36 kg (Kahrs, J., personal communication, 2002).
Stage 5-Clam Culture:
The final phase of water treatment prior to
returning to the barn for wash down purposes,
is clam culture within modified ditches or
earthen raceways to facilitate periodic clam
harvest. The species considered to be a goodcandidate for the integrated system in Florida
is the Asian clam, Corbicula fluminea, due toits abundance throughout Florida freshwater
bodies, tolerance to various water quality, highstanding densities of up to 4,000 adults m−2 ,relative high shell growth rate and rapid population recovery (McMahon, 1999). In addition,
this species of clam has been observed to be amajor feeder of phytoplankton, reducing
plankton concentrations by 20-75 ％ in certain
areas of the Potomac River (Cohen et al., 1984).
Unlike the fish culture portion of this integrated dairy/aquaculture system, in which extensive production data exists, the effectivenessand applicability of Corbicula as the final phaseof water treatment within this integrated setting remains unproven. Current studies at the
University of Florida Department of Fisheries
and Aquatic Sciences are investigating somefundamental questions on Corbicula prior toincorporation into the dairy/aquaculture system. These include: substrate suitability,

147

growth and filtering rates in a raceway environment, phosphorous uptake, shell and tissue
P concentrations, and recommended water flow
and clam stocking rates. Preliminary results
show reasonable clam growth, but also a partial die off occurred which may be due to highwater temperatures as observed with Corbicula
in many natural environments (McMahon,1999).
Summary of opportunities and challenges ofintegrated systems
The nutrient assimilation or reduction capability and production potential of all components within the integrated concept except the
Corbicula stage have individually been demonstrated in the field. Using the mean P uptake
values reported for stages 1 - 4 : 25 ％, 50 ％ 20％, and 40 ％ respectively, a 99 ％ total uptake
may be possible without including the less significant removal by the Tilapia and baitfish
harvesting as well as the littoral zone contributions. The Corbicula culture component would
serve as the final P removal or polishing stage
providing additional P removal. Proper sizingof each stage to the total P input or loading,would be necessary to prevent phosphorus
being removed at high enough rates to starve
subsequent stages of either P or P induced
phytoplankton. Reviewing the uptake efficiencies, one could suggest that perhaps improvements on stages 1 , 2 and the contribution ofphytoplankton together can accomplish P reduction goals. However, the fish, macrophytic
plants and clams serve two important roles: 1)
consumption of phytoplankton and subsequent
removal of the P bound in the plankton via periodic harvesting; and 2) provide economic
value to potentially pay for the treatment system. Pilot field studies are a essential tool tovalidate nutrient removal contributions of eachstage and provide critical information in sizing
the system, identifying optimum combinationsof stages, and cost-benefit data.
The fundamental concept of sustainable animal production integration is maturing and148

Andrew M. LAZUR and Frank LETEUX

being considered in many areas to improvesustainability of intensive animal production.
Fedler and Parker (1994) present a similar multistage wastewater treatment scenario forswine or cattle production. In their system concept, fish, algae, duckweed, Lemma spp., andmacrophytic plants are used to filter nutrients
and, energy recovery, in the form of methane isincorporated. Parker and Fedler (1996) also
note the increased potential for energy production through use of advanced facultative pond
incorporated into an integrated wastewater
treatment system and further suggest the
many environmental and economic benefits ofan integrated feedlot system.
The integrated concept is relatively simple indesign, is applicable to a variety of type andscale of animal operations, and offers farmers
the potential for increased farm income
through sales of high value aquaculture crops.
Incorporating a phosphorus reduction approach within the existing dairy barn treatment operations in south Florida offers costsavings and is more attractive to farmers compared to either new treatment systems or"regulatory relief" technologies, such as chemical treatment, that offers P reduction without
any secondary crop income potential. Utilizing
an aquaculture production component, does
however, present challenges, especially the needfor aquaculture training and experience, anddetailed market information. In most cases, as
was indicated by dairy farmers in the Lake
Okeechobee area, demands on the farmers' time
is currently too great to take on the additionaltime for training or production management
responsibilities. Therefore, integrated operations would need to hire experienced individuals or contract with an aquaculture service
company to manage the aquaculture component. An additional, and essential consideration is identification of market opportunities
for the aquaculture products. The relatively
large volume of fish and aquatic plants potentially generated by this system would be best
accommodated through wholesale type markets rather than retail which require greater

time due to smaller volumes and distances between customers. Thorough research on market outlets and their needs such as species
preferences, product sizes, frequency of supply,
volumes, seasonality of demand and pricing information is critical to evaluating the economic
benefit of the aquaculture component and in
the decision making process of investment.
The advantage of application in areas likesouth Florida are: 1) a long growing season of
10−11 months enabling efficient filtration capability of aquatic species nearly year-round; 2)
the close proximity to high value markets andestablished distribution for baitfish (Adams etal., 1998; Lazur, 1995), and aquatic plants; and3) access to infrastructure and outlets using
farm biosoilids such as, manure for compost,organic fertilizer, or bio energy production,
and Tilapia and possibly clam shells for generation of animal feed products. Adapting thistechnology to cooler climates would result in
reduced filtration efficiencies of aquatic species
due to dormancy periods, which would increase
the need for manure storage during wintermonths. However, the nutrient reduction benefit of wastewater treatment of an integrated
system, despite the reduced growing season,
may be highly significant and be more environmentally and economically justifiable thanother options.
The culture of brackish water or marine
aquatic algal and shellfish species with a joint
goal of food production and nutrient reduction
is expanding rapidly and Costa-Pierce, (2002)
states many estuary based examples worldwide. Neori et al. (2000) studied a land-basedmarine recirculating polyculture system incorporating gilthead sea bream, Sparus aurata,
Japanese abalone, Halotis discus hannai, andtwo seaweed species (as biofilters), Ulva lactuca
and Gracilaria conferta. In their system, nutrients from the fish wastes were fed to the seaweed which was then fed to the abalone. They
found that Gracilaria performance was poor,
but the sea bream, Ulva, and abalone experienced good growth and the system converted 23％ of the nitrogen into fish and abalone flesh

Integrated aquaculture systems for nutrient reduction in agricultural wastewaterand an additional 10.3 ％ into seaweed exported
from system. Based on their study, a component ratio of 0.6: 1 : 2 m2 of abalone: fish: seaweed respectively is recommended. With thisratio, they estimate that 27％ of the nitrogen
would be converted to fish and abalone flesh
with much of the remaining nitrogen in theform of ammonia and DON and would be recycled into the seaweed biofilters.
Applying marine species in integrated
agriculture/aquaculture presents greater challenges given that CAFO's utilize freshwaterand many operations are located inland. Thoseoperations located near marine environments
would require mixing the freshwater effluent
with the marine water source in order to provide salinities required for the desired marineorganisms. Recycling the treated water containing high salinities may not be acceptable insome applications, but may fit the dairy modeland wash down use described within this paper.
The methods and potential combinations ofcomponents of integrating agricultural systems for nutrient reduction are numerous. The
one concept presented here bases the nutrient
reduction potential on a collection of observations and data for individual systems components. Field tests or demonstration projects are
essential next steps and would provide valuable
data in determining individual component andwhole system nutrient reduction efficiencies,
component compatibility, recommended nutrient input to component sizing, system costs
and economic viability.
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for the future of aquaculture, in " Ecologicalaquaculture" (ed. by Costa-Pierce B. A.),
Blackwell Publishing, Oxford, pp. 339-372.
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Hopkins J. S., Hamilton I. I. R. D., Sandifer, P.
A., and Browdy C. L., 1993: The productionof bivalve mollusks in intensive shrimp ponds
and their effect on shrimp production andwater quality. World Aquaculture, 24, 74-77.
Lasalle M. W. and Posadas B. C., 1997: Use of
constructed wetlands to improve water quality in finfish pond culture, Final report,
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153

Understanding the influence of bivalve suspension-feeder populations
on water quality in eutrophic coastal waters
Roger I.E. NEWELL*, Jeff C. CORNWELL*, Raleigh R. HOOD* and Evamaria KOCH*

Suspension feeding bivalve molluscs serve to couple pelagic and benthic processes because they filter particles with high efficiency from the water column and transfer undigested remains in their biodeposits to the sediment surface. This feeding activity,
combined with their often high abundance as natural stocks and in intensive
aquaculture farms, can make bivalves extremely important in regulating water column
processes in shallow coastal waters. Of all bivalve species worldwide, eastern oysters areamong the most powerful in this regard because of their unusually high weight specificfiltration rates ( 7 to 10 L h−1 g−1 dry tissue weight at typical summer water temperatures of 25 ℃.) The eastern oyster is well adapted to living in estuaries where inorganic
particles comprise a large fraction of the seston because it can sort filtered particles
prior to ingestion and reject less nutritious particles as pseudofeces. Currently in the nutrient enriched Chesapeake Bay, where phytoplankton are in high abundance, easternoysters maintain high filtration rates but now reject large amounts of undigested algal
cells in their pseudofeces. Newell (1988) initially drew attention to the possible ecosystembenefits of the original huge stocks of eastern oysters in Chesapeake Bay by comparing
water column turnover times before oysters were commercially exploited to the situation today when oysters are at an all time low abundance.
In contrast to Newell's (1988) proposition that oyster populations may once have exerted "top-down" control on phytoplankton stocks others claim that oysters may simply
recycle inorganic nutrients rapidly back to the water column and hence there would nothave been any long-lasting reduction in phytoplankton biomass. To help distinguish between these scenarios, Newell et al. (2002) explored in laboratory incubations changes innitrogen fluxes and denitrification under anoxic and oxic conditions in response to loading by different amounts of phytoplankton cells, representing an experimental analog ofoyster biodeposits. When organics were regenerated under aerobic conditions, typical of
those associated with shallow water oyster habitat, coupled nitrification-denitrification
was promoted, resulting in denitrification of 〜20 ％ of the total added nitrogen. In contrast under anoxic conditions, typical of current summertime conditions in main-stem
Chesapeake Bay where phytoplankton is microbially degraded beneath the pycnocline,
nitrogen was released solely as ammonium from the added organics. Such denitrificationof particulate nitrogen remaining in the biodeposits of benthic suspension feeders will
enhance nitrogen removal from eutrophied coastal waters (Newell, 2004).
It is likely that reduced oyster filtration by the much diminished oyster populations
has contributed, in part, to observed higher turbidites in Chesapeake Bay and the consequent reduction in light reaching the sediment surface. In aerobic incubations of sediment cores with even low light levels (70μmol−2 s−1 ), Newell et al. (2002) found that abenthic microalgal/cyanobacterial community grew that not only absorbed the inorganic nitrogen released from oyster biodeposits but also fixed N2. This suggests that an* Horn Point Laboratory, University of Maryland Center for Environmental Science, PO Box 775, Cambridge, MD 21631 USA
Email: newell@hpl.umces.edu

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Roger I.E. NEWELL, Jeff C. CORNWELL, Raleigh R. HOOD and Evamaria KOCH

ecosystem dominated by benthic primary production may develop in shallow waters
when reduced turbidity associated with bivalve feeding increases light penetration to alevel that can sustain benthic microalgal production.
Over the last four decades seagrass beds have either declined or have disappeared
throughout much of the Chesapeake Bay due to high water turbidity leading to reduced
light availability for these benthic plants. In order to explore the possible interactions
between oyster and seagrass declines we have developed a numerical model to simulate
the interaction between wave-induced sediment resuspension, bivalve filtration, andseagrass growth. This model, which is parameterized based upon direct measurementsof oyster filtration and seagrass wave dampening effects, shows that under high wave
height conditions the presence of oysters can reduce suspended sediment concentrations
by nearly an order of magnitude, which significantly increases water clarity and thedepth to which seagrasses can grow (Newell, 2004).
References
Newell R. I. E., 1988: Ecological Changes in Chesapeake Bay: Are they the result ofoverharvesting the Eastern oyster (Crassostrea virginica)?, in "Understanding theEstuary: Advances in Chesapeake Bay Research" (eds. by Lynch M.P. and Krome
E.C.), Chesapeake Research Consortium Publication 129 (CBP/TRS 24/88),
Gloucester Point, VA, pp.536-546. (Available for free download from http://www.
vims. edu/GreyLit/crc129. pdf)
Newell R. I. E., 2004: Ecosystem influences of natural and cultivated populations of suspension-feeding bivalve molluscs: a review. J. Shellfish Res., 23(1)Newell R. I. E, Cornwell J. C., and Owens M. S., 2002: Influence of simulated bivalve
biodeposition and microphytobenthos on sediment nitrogen dynamics: a laboratory
study. Limnol. Oceanogr., 47, 1367-1379. (Available for free download from the
Limnology Oceanography web site in the September 2002 issue. http://aslo.
org/index2. html)

水研センター研報，別冊第 1 号，155, 平成16年
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155

DEVELOPMENT OF A NOVEL GENE TRANSFER METHODIN PORPHYRA
Chum-Mean LIN* 1, Charles YARISH* 2 and Thomas CHEN* 1

Foreign genes have been successfully transferred into both animal and plant bytransgenesis, but introduction of foreign genes into many important algae species is stillin its infancy. Although nuclear and organelle transformations in Chlamydomonas
reinhardtii, a green microalgal species, have been well established, attempts to developtransformation methods for macroalgae, such as Volvox carteri and several diatom species have just begun. Currently, there is no report of success of genetic transformationin Porphyra species (seaweed).
To facilitate applications of seaweed in both basic research and integrated aquaculturebiotechnology, we have undertaken initiatives to develop gene transfer technology for
Porphyra, and made significant progress. A plasmid DNA with a selection marker wastransferred into archaeospores of P. leucosticta by electroporation. Total DNA was thenprepared from those electroporated samples at various times of incubation including 24
hrs, one week, two weeks and up to two years. PCR analysis showed the consistent presence of plasmid DNA in all samples tested, strongly suggesting the success of genetransfer in Porphyra. The thalli developed from those transformed archaeospores growwell under continuous presence of selection pressure over two years with serial transfers. Reverse transcription (RT)/PCR analysis of RNA samples isolated from transgenic
thalli showed expression of the transgene. These observations provide us with great confidence that genetic manipulation and production of transgenic Porphyra is feasible.

* 1 Department of Molecular and Cell Biology, and * 2 Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs,
CT 06269 USA *Corresponding author, Email: tchen@uconnvm.uconn.edu