Participants in 45th UJNR Aquaculture Panel Symposium, held in International Conference Center Hiroshima,
Hiroshima, Japan, October 16 ‒ 17, 2017

Preface
The UJNR (The U.S.-Japan Cooperative Program in Natural Resources) Aquaculture Panel wasestablished in 1968, and the business meeting and symposium have been held every year since1971. Through the long history of UJNR, Aquaculture Panel has contributed to the developmentof aquaculture researches of both countries by means of various cooperative activities, suchas the exchange of scientists and literatures, and the promotion of joint research projects. The
Aquaculture Panel is highly appraised as one of the most active UJNR panels in both countries.
The 45th Business Meeting of the UJNR Aquaculture Panel was conducted at Conference Center
Hiroshima, Hiroshima Prefecture, Japan on October 16, 2017, and the Scientific Mini-Symposium washeld at the same venue from October 17 to 18. The symposium theme was "Potential of aquaculture
to mitigate impacts of environmental change", which was under the 10th Three-Year Plan, "Marine
Aquaculture in a Changing Environment", commenced in 2017. Fifteen oral presentations weremade on topics such as environmental change, environmental remediation, biological response toenvironmental change and ecosystem approach to aquaculture, and seven poster presentations
were also made on broader topics related to aquaculture during the two-day symposium.
The proceedings of the 45th UJNR Aquaculture Panel Scientific Mini Symposium "Potentialof aquaculture to mitigate impacts of environmental change" is published as the special issueof the Bulletin of Japan Fisheries Research and Education Agency. With great pleasure, thisUJNR proceedings containing high quality papers authored by selected American and Japaneseaquaculture scientists will hopefully help improve the aquaculture environment programs, whichis expected to contribute to the development of the aquaculture industry in both the United States
and Japan.
Finally, I would like to express my sincere gratitude to the colleagues involved in the UJNR
Aquaculture Panel for their efforts in the preparation and organization of the symposium. I would
also like to deeply thank the editorial board members for publishing the proceedings.

Fuminari Ito, Ph.D.
Chair of UJNR Aquaculture Panel
Executive Director
Japan Fisheries Research and Education Agency

CONTENTS
Preface ……………………………………………………………………………………………………………… 1
Group Photo ………………………………………………………………………………………………………… 2Contents ……………………………………………………………………………………………………………… 3
Program for The 45th Scientiﬁc Symposium of UJNR Aquaculture Panel ………………………… 5

Contributed Papers and Abstracts
1.

New direction of management policies in the Seto Inland Sea, Japan, in a changing environment(Osamu Matsuda) ……………………………………………………………………………………………

2.

9

Marine aquacultureʼs role in providing nutritional security in a changing environment (Michael B.
Rust) ………………………………………………………………………………………………………… 17

3.

An overview of NOAA grants on aquaculture and the environment (Shiyu Rachel Wang) ……

19

4.

Oligotrophication and its measures in the Seto Inland Sea, Japan (Katsuyuki Abo, Tamiji
Yamamoto) ………………………………………………………………………………………………… 21

5.

Assessment and future prediction of climate change impacts on the macroalgal bed ecosystem andcultivation in the Seto Inland Sea (Goro Yoshida, Hiromori Shimabukuro, Setsuo Kiyomoto, Tatsuru
Kadota, Taku Yoshimura, Noboru Murase, Mikio Noda, Shoichi Takenaka, Yoshimi Kono,
Toshiharu Tamura, Norio Tanada, Xiaojie Yu, Naoki Yoshie, Xinyu Guo) ………………………… 27

6.

Coastal management using oyster-seagrass interactions for sustainable aquaculture, ﬁsheries andenvironment (Masakazu Hori, Franck Lagarde, Marion Richard, Valerie Derolez, Masami
Hamaguchi, Mitsutaku Makino) ………………………………………………………………………… 35

7.

Marine sediment conservation using benthic organisms (Katsutoshi Ito, Mana Ito, Takeshi Hano,
Toshimitsu Onduka, Kazuhiko Mochida, Nobuaki Shono, Ryuhei Nakamura) …………………… 45

8.

Monitoring coastal acidiﬁcation along the U.S. East coast: concerns for shellﬁsh production (Matthew
Poach, Daphne Munroe, James Vasslides, Ian Abrahamsen, Nicole Coﬀey) ……………………… 53

9.

Growth variation in long blade kelp

in eastern Hokkaido, Japan (Natsuki

Hasegawa, Toshihiro Onitsuka, Sayaka Ito, Tomonori Azumaya)…………………………………… 65
10.

Harmful algal blooms and shellﬁsh aquaculture in changing environment (Leila Basti, Kiyohito
Nagai, Susumu Segawa, Yuji Tanaka, Toshiyuki Suzuki, Satoshi Nagai) ………………………… 73

11.

Deﬁning an ecosystem approach to aquaculture (EAA) for federal waters of the United States(Katherine A. McGraw, Michael B. Rust) ………………………………………………………………

81

12.

Spatial planning for shellﬁsh aquaculture and seagrasses in US West Coast estuaries: considerations
for adapting to an uncertain climate (Brett R. Dumbauld, Jennifer L. Ruesink, George G.
Waldbusser) …………………………………………………………………………………………………

13.

97

Oﬀshore mussel aquaculture: strategies for farming in the changing environment of the Northeast
U.S. shelf EEZ (Darien D. Mizuta, Mark S. Dixon, Edward J. Maney Jr., Mark Fregeau, Gary H.
Wikfors) ……………………………………………………………………………………………………… 111

14.

Eﬀects of ﬁsh aquaculture on inorganic nutrient levels in Gokasho Bay (Satoshi Watanabe,
Masayuki Minakawa, Yuka Ishihi, Natsuki Hasegawa, Toshie Matsumoto) ……………………… 121

15.

Challenges and opportunities of IMTA in Hawaii and beyond (Cheng Sheng Lee) ……………… 129

Abstracts of Poster Presentations
List of Presentations ……………………………………………………………………………………………… 135
Abstracts of Poster Presentations ……………………………………………………………………………… 137

Program
The 45th Scientiﬁc Symposium of UJNR Aquaculture Panel
Potential of aquaculture to mitigate impacts ofenvironmental change

Date:
October 16

13：30‑17：30

Oral Session, Poster Session

October 17

９：00‑16：00

Oral Session during lunch break

Venue:
International Conference Center Hiroshima, 1‑5 Nakajima‑cho, Naka-ku, Hiroshima‑shi,Hiroshima, 730‑0811, Japan

Aim of the Symposium
Environmental change impacts ﬁsheries and aquaculture in many ways. Nutrient pollution
is driving eutrophication and dead zones; ocean acidiﬁcation is changing water chemistry,
and climate change is already inﬂuencing our food supply, fresh water availability, weather
and way of life. Aquaculture will be impacted by, and can also impact, these environmental
changes over various time and spatial scales.

Aquaculture of ﬁnﬁsh, shellﬁsh and seaweed

have different threats, benefits and opportunities related to environmental change.
Understanding the global and regional trend of climate change, effects of environmental
change on ecosystem and aquaculture, technical improvement of aquaculture, andaquaculture industrial adaptation to climate change are all research priorities of the National
Ocean and Atmospheric Administration (NOAA), the United States Department ofAgriculture (USDA) and the Japan Fisheries Research and Education Agency (FRA). The
primary focus of this symposium will be on the potential of aquaculture to mitigate impactsof environmental change, such as sequestering carbon, bio-extraction of nutrients and CO2,
and ocean acidiﬁcation. We hope to exchange ideas and discussion which will be beneﬁcial in
exploring science and technology that will enable aquaculture to sustain in a changing
environment and be used to mitigate the anthropogenic impacts on environment. We also
hope the exchanged ideas will be developed into our collaborative research eﬀorts to resolve
key issues and assist strengthening of aquaculture industry in the United States and Japan.

Monday, October 16, 2017
Registration: 13：00‑13：30
Opening Session
Welcome Remarks
Fuminari Ito (Japan Panel Chair, Executive Director, Headquarters, FRA)…………………………………………………………………………………… 13：00‑13：40
Aim of the Symposium
Takuro Shibuno (Director,National Research Institute of Aquaculture, FRA)…………………………………………………………………………………… 13：40‑13：50
Session I. Keynote Presentation and Introduction of NOAA grants(Moderators: Paul Olin and Junya Higano)
1. New direction of management policies in the Seto Inland Sea, Japan in the changing
environment
Osamu Matsuda (Professor Emeritus, Hiroshima University) ………… 13：50‑14：30
Break ………………………………………………………………………………… 14：30‑14：50
2. Marine aquacultureʼs role in providing nutritional security in a changing environment
Mike Rust (US Panel Chair, NOAA Fisheries Oﬃce of Aquaculture) … 14：50‑15：30
3. An overview of NOAA grants on aquaculture and the environment
Shiyu Rachel Wang (Knauss Fellow, NOAA Headquarters, Oﬃce of Aquaculture)…………………………………………………………………………………… 15：30‑15：55
Session II. Environmental Change(Moderators: Takuro Shibuno and Mathew Poach)
4. Oligotrophication and its measures in the Seto Inland Sea, Japan
Katsuyuki Abo (National Research Institute of Fisheries and Environment of InlandSea, FRA) ……………………………………………………………………… 15：55‑16：20
5. Assessment and future prediction of climate shift impacts on the macroalgal ecosystemand cultivation in the Seto Inland Sea
Jeﬀrey Silverstein (USDA Agricultural Research Service)…………… 16：20‑16：45

Poster Session
Poster presentation …………………………………………………………………… 16：45‑17：30

Tuesday, October 17, 2017
Session III. Environmental Remediation(Moderators: Natsuki Hasegawa and Darien Mizuta)
6. Coastal management using oyster-seagrass interactions for sustainable aquaculture,ﬁsheries and environment
Masakazu Hori (National Research Institute of Fisheries and Environment of InlandSea, FRA) ……………………………………………………………………… ９：00‑ ９：25
7. Marine sediment conservation using benthic organisms
Katsutoshi Ito (National Research Institute of Fisheries and Environment of InlandSea, FRA) ……………………………………………………………………… ９：25‑ ９：50
Break ………………………………………………………………………………… ９：50‑10：10
Session IV. Biological Response to Environmental Change(Moderators: Satoshi Watanabe and Brett Dumbauld)
8. Coastal acidiﬁcation ampliﬁers along the US East coast: concerns for shellﬁsh production
Matt Poach (NOAA, Northeast Fisheries Science Center) ……………… 10：10‑10：35
9. Growth variation in long blades kelp

in eastern Hokkaido, Japan

Natsuki Hasegawa (National Research Institute of Aquaculture, FRA)…………………………………………………………………………………… 10：35‑11：00
10. Harmful algal blooms and shellﬁsh aquaculture in a changing environment
Leila Basti (Tokyo University of Marine Science and Technology) …… 11：00‑11：25
Lunch Break ………………………………………………………………………… 11：25‑13：00
Session V. Ecosystem Approach to Aquaculture Part 1(Moderators: Masakazu Hori and Cheng Sheng Lee)
11. Ecosystem approach to marine aquaculture
Kay McGraw (NOAA, Oﬃce of Habitat Conservation) ………………… 13：00‑13：25
12. Spatial Planning for Shellﬁsh Aquaculture and Seagrasses in US West Coast Estuaries:
Considerations for Adapting to an Uncertain Climate
Brett Dumbauld (U.S. Department of Agriculture, Agricultural Research Service)…………………………………………………………………………………… 13：25‑13：50
13. Oﬀshore mussel aquaculture: strategies for farming in the changing environment of NE
Atlantic EEZ
Darien Mizuta (NOAA, Northeast Fisheries Science Center) ………… 13：50‑14：15

Session VI. Ecosystem Approach to Aquaculture Part 2(Moderators: Katsuyuki Abo and Kay McGraw)
14. Nutrient environment in Gokasho Bay, eﬀects of ﬁsh aquaculture on inorganic nutrient
levelsSatoshi Watanabe (National Research Institute of Aquaculture, FRA)…………………………………………………………………………………… 14：15‑14：40
15. Challenges and opportunities of IMTA in Hawaii and beyond
Cheng Sheng Lee (Director, Center for Tropical and Subtropical Aquaculture, U.S.
Department of Agriculture) ………………………………………………… 14：40‑15：05
Break ………………………………………………………………………………… 15：05‑15：25

Open Discussion: Development of collaborative research projects … 15：25‑15：50(Moderators: Fuminari Ito and Mike Rust)
Science Symposium Closing …………………………………………………… 15：50‑16：00
Mike Rust (US Panel Chair, NOAA Fisheries Oﬃce of Aquaculture)水 研 機 構 研 報， 第 49 号，9 − 15， 平 成 31 年
Bull. Jap. Fish. Res. Edu. Agen. No. 49，9−15，20199

New direction of management policies in the Seto Inland Sea, Japan,
in a changing environment
Osamu MATSUDA＊

Abstract: The Seto Inland Sea, the largest enclosed coastal sea in Japan, covers an area of 23,000
km2 and was originally renowned as a productive fishing and aquaculture ground with scenic
beauty. However, since the coastal basin in the watershed around the sea is home to 30 million
people, and impact of human activities on the sea has been very strong. During Japanʼs period of
rapid economic growth in the mid-1960s to mid-1970s, industrialization of the coastal area, increasein the number of factories and expansion of landfills in waterfront areas caused a rapid increase inwater pollution with a reduction in shallow water area and destruction of the marine environment.
In order to conserve the environment of the region, the Law on Temporary Measures for theEnvironment Conservation of the Seto Inland Sea was enacted in 1973. This law was madepermanent in 1978 as the Law on Special Measures for the Environment Conservation of the Seto
Inland Sea (“The Seto Inland Sea Law”). More than 40 years have now passed since the enactmentof the legal system. During the time, changes of both the natural and socio-economic environments
around the sea were remarkable. And, recently, 2015 became the year for a particularly importantchange of direction for management because major revisions of both “The Seto Inland Sea Law” andthe governmental Basic Program based on the Law were made. In the newly revised Basic Program,two major aims of the previous Basic Program (conservation of water quality and conservation ofnatural landscape) were reformed into four new major aims, including conservation and restorationof coastal environment, conservation and appropriate management of water quality, conservation ofnatural and cultural landscapes, and sustainable utilization of fish resources. These recent changes
indicate that not only passive conservation but also positive conservation, such as restoration ofcoastal environment, became very important targets. The new direction of the management reflects
the changing environment of the Seto Inland Sea. After WWII, the first major target was waterpollution control, including toxic substances. Then, the target turned to red tides due toeutrophication. Recently, major targets are changing to lowered biological productivity and diversity
due to oligotrophication and deteriorated habitat. Therefore, the main approaches of management
also changed from water quality control by restrictive measures to restoration of habitat, such as
tidal flats and sea grass beds, by promotion of participatory creative activities. New direction is also
supported by the concept of, which includes restoration of biodiversity, biologicalproductivity, habitat and well balanced nutrient cycle by the intervention of positive humanactivities. These recent shifts of the management policies are expected to contribute to recovering
productive fishing and aquaculture grounds in the Seto Inland Sea in the future.
Key words: coastal management, environmental conservation, Seto Inland Sea,

2018年８月31日受理（Accepted on August 31, 2018）
Hiroshima University (Professor Emeritus), Higashi-Hiroshima, 739-8528, Japan
E-mail: matsuda036@go3.enjoy.ne.jp＊

10Osamu MATSUDA
Introduction

In reality,

is a traditional Japanese coastal

ecosystem and landscape management system that
Brief History of the Seto Inland Sea

was found in many coastal areas throughout JapanThe Seto Inland Sea, the largest enclosed coastal

in days gone by Sustainable community-based

sea in Japan (Fig.1), has long history in which plenty

management of the local sea areas has a long historyof ecosystem services have been provided. However,in Japanese tradition.

serious environmental changes due to land-based

However, during the nationʼs high economic

human activities occurred during the postwar

growth, this type of traditional coastal management

reconstruction age after WWII. Rapid economic

has gradually deteriorated due to changes in thegrowth during 1960s to 70s was accompanied

local community and life style of the people. As aby serious water pollution, eutrophication andresult, social demand to create a new type ofdestruction of habitat, such as tidal flats and sea

defined as high biological productivity and highgrass beds, in the shallow coastal areas. Among many

biological diversity in the coastal seas with positive

countermeasures, the Seto Inland Sea Law (Lawhuman intervention has arisen and grown strong. In

Concerning Special Measures for Conservation of theJapan, community-based habitat restoration activities

Environment of the Seto Inland Sea), which was firsthave been gaining ground in recent years partly

enacted in 1973 and applied only to the Seto Inland

because the concept ofSea, played an important role. Major functions of

into official institutional systems of national policy.

“the special law” were area wide total pollution load

Since

control (TPLC) and suppression of land reclamation.

said to have grown up in the Seto Inland Sea,

was incorporated

originated in Japan and is sometimes
exemplifies the close relationship between

Brief Introduction to

the deterioration of the sea and active conservation

What doesmean? Why is so muchattention paid to

nowadays? In Japanese,“” means local village or community where

people live their life and “” means the sea.

Therefore, the simple literal meaning ofisthe sea associated with local village or community.

of the area by local people (Fig.2).
Recently, a new concept for coastal sea
management called

has been noticed

not only in its original place of Japan but also inmany other countries, including both western andAsian. Multilingual editions of books on

Biodiversity

SUBSTANCECIRCULATION
Appropriate nutrients
Healthy material circulation
Water and sediment quality

Biii

ECOSYSTEM
Diversity and productivity
Resource management
Fishing operation

Three elements that
support conservation
and restoration
CONTACT

Coexistence with nature
Regional cooperative effort

SATOUMIACTIVITYSPHERESFishing village and cities
Watershed(mountains,rivers, fields and ocean)

Fig. 1. Outline of the Seto Inland Sea, its watershed
and location of 13 prefectures around the Sea. The
applied area of “The Seto Inland Sea Law” is almost
equal to the watershed area of all rivers flowing into
the Sea, where ca. 30 million people live. (Source: The
Association for the Environmental Conservation of
the Seto Inland Sea)

ENTITIES THATPERFORM ACTIVITY
Fisher and other coastal residents
Urban residents that use the ocean
Residents of watershed

Sustainability
Two elements that support hands-on action

Fig. 2. Five important elements ofconcept.
Three objectives to be improved (upper) and two
indicators on activities (lower). (Source: Sato-Umi net)

New management policies in the Seto Inland Sea

11

published by such international organizations aschanges in water quality in the Seto Inland Sea due

the United Nations University and the Secretariat

to the TPLC system is very clear. The load of COD,of the Convention on Biological Diversity (CBD) also

TN and TP decreased during the years of 1979 tocontribute to expanding

2014. Generally, concentration of TN and TP in sea

activities in theworld.

water is proportional to the TN and TP load perunit area of the sea. This means that water quality

Change of the Environment and Ecosystems

in terms of TN and TP has been much improved ingeneral. However, decreased nutrient concentrations

The TPLC system has significantly improvedin sea water has led to the new issue of artificial

water quality in terms of COD, Total Nitrogen

oligotrophication, which caused insufficient growth in(TN) and Total Phosphorus (TP). For example, the(laver) culture.

number of the occurrences of red tide decreased

Meanwhile, changes in biodiversity in the Seto

from about 300 a year at the peak to about 100 aInland Sea have not been systematically monitored.

year recently. Concentration of TN and TP in sea

However, biodiversity seems to have decreased

water also decreased, and recently, it has cleared the

judging from the evidence that the number oflegal environmental standard of Japan in many areas

observed sea shore animals of at various stationsof the Seto Inland Sea. However, since suppression

around Kure area that are members of long monitoredof land reclamation does not mean total ban of land

species has decreased drastically from the mid-1960s.

reclamation, the effect of the policy was restricted. As

Tidal flats and sea grass beds around the Seto Inlanda result, shallow areas -- in particular tidal flats and

Sea decreased mainly due to land reclamation and,sea grass beds -- have been drastically lost during thetherefore, natural coastlines disappeared (Fig.3).

last 50 years.

These events indicate that the habitat condition has

Changes in the pollutant load from land anddeteriorated. Fish catch data indicate that fisheries

Fig. 3. Result of historical land reclamation in Osaka Bay. Natural shorelines and shallow areas, such as sea grass beds
and tidal flats, disappeared. (Source: The Association for the Environmental Conservation of the Seto Inland Sea)

12

Osamu MATSUDA

production is decreasing after a peak in the mid-conservation, such as

1980s. From these results, it can be said that therestoration of biodiversity, biological productivity,

which includes

ecosystem services available are decreasing in the

habitat and a well-balanced nutrient cycle between

Seto Inland Sea, although water quality has beenland and sea. Holistic approaches, such as ecosystem-

improved to some extent.

based management (EBM) and integrated coastal

Major environmental and related problems in the

management (ICM), are also being incorporated in

Seto Inland Sea in recent years can be summarized

new policy. In the recently revised governmental

as following.

Basic Program for the Environmental Conservation of
the Seto Inland Sea (2015), based on the revised Seto・Deterioration of the ecosystem, natural resources

Inland Sea Law (2015), 2 major aims of the previous
Basic Program (1. conservation of water quality,and ecosystem services
・Decrease of biological diversity and biological

2. conservation of natural landscape) are reformed
into 4 major aims (1. conservation and restoration of

productivity (fish catch)
・Weakened relationship between humans and thecoastal environment, 2. conservation and appropriate
management of water quality, 3. conservation ofsea

natural and cultural landscapes, 4. sustainableutilization of fish resources) (Fig.4). Therefore, the・Occurrence of red tides and oxygen depletion in

simplified major change of the aim is from a focus onwater quality control to more holistic restoration ofbottom waters・Deterioration of the benthic environment andenvironmental and fish resources, which can lead toabundant and bountiful coastal seas.

sediment quality
・Disappearance of biological habitat for spawning

Present Status ofand as nursery grounds
・Insufficient nutrients for laver

cultureground in winterHistorically,

has evolved as the traditional

Japanese way of coastal management in which local
Recent Shift of Management Policyin the Seto Inland Sea

communities co-existed with nature. In theconcept, peopleʼs livelihoods and their culture are
deeply involved, biological productivity is sustained,

Environmental conservation and management

and biological diversity is protected and conserved,

policy firstly made emphasis on water pollution

while ecosystems are able to be sustained and material

control. However, this kind of passive conservation

cycling is maintained. These community efforts werepolicy is gradually being shifted to active

undertaken in a comprehensive and integrated

Fig. 4. Outline of recent revision of the governmental Basic Program, based on the revision of “The Seto Inland
Sea Law” (2015). (Source: Ministry of the Environment)

13

New management policies in the Seto Inland Sea<

manner from upland forest and rivers to coastal seas.
Therefore, the concept ofprimarily provides

㼓㼛㼛㼐

6DWRXPL
5HVWRUDWLRQ

holistic management of watersheds, including forests,, focuses on forest andagricultural land, withis also expected toW
Q

Presentstatus(IIHFWRI
73/&HWF

help develop a Japanese model of integrated coastal
In many-like coastal seas in Japan,

sea has historically been conducted in a traditional'HWHULRUDWLRQGXULQJKLJKHFRQRPLF
JURZWKDJH

Worst
condition
inmid70s

management (ICM).
sustainable community-based management of the

Beforehigheconomicgrowth

Shiftrivers, local communities and coastal environments.
Combining

Smoothmaterial
circulationand
richecosystem)XWXUHGLUHFWLRQ㼎㼍㼐;HabitatCondition

㼎㼍㼐

NATURALENVIRONMENT㼓㼛㼛㼐

manner. However, during the nationʼs high economic
growth after World War II and due to social changes
associated with the economic development of thenation, this type of traditional coastal management
gradually declined because of the changes in local

Fig. 5. Conceptual view of future directions andnecessary shifts of environmental management in
the Seto Inland Sea. (Reformed figure by the author
based on Ministry of the Environment)

communities and life styles of the people. During thesame period, coastal environments, habitats and livingof Seto Inland Sea area also introduced theresources were also seriously damaged by water

concept as official policy. For example, Kagawa

pollution, eutrophication and land development, as aprefecture has always promoted

result of urbanization and industrialization of coastal

official policy. And, recently, based on the revised

areas. Instead of obtaining efficiency and convenience

special Law and revised governmental Basic Program

due to industrial development, valuable capital, suchon the Seto Inland Sea, every local government ofas the natural environment, natural resources andprefectures around the Seto Inland Sea revised thenatural landscape was lost. As a result, social demandenvironmental management plan at the prefecture

to create and establish a new type of, defined

level by the end of 2016. This new management planas high biological productivity and high biologicalat each prefecture level reflected the shift toward thediversity in the coastal seas with positive humanas anconcept directly and will promoteintervention, has arisen and gradually gained ground.

activities. The above mentioned

In other words, a “

Renaissance” is taking

Kagawa prefecture was incorporated into the revised

place in order to restore once lost rich and healthy

prefecture plan. This kind of enhanced policy will

coastal seas by community-based participatory

promote local activities for the creation ofactivities. In seas where

elsewhere in the near future.

activity ispolicy ofnecessary, natural environmental conditions and theecosystems are so deteriorated they cannot recover

Future Direction under New Policy

naturally without support by human behavior.
In Japan, community-based habitat restoration

The conceptual view on future directions ofactivities have also been gaining ground in recent

environmental management in the Seto Inland Sea

years. This is partly because the concept ofis presented in Fig.5. In this figure, past, present

was incorporated into official institutional systems ofand future environmental conditions are indicatednational policy, such as the Basic Ocean Plan (2008),

on an X-Y axis. The horizontal axis shows natural

based on Basic Ocean Act (2007), and some national

environmental conditions, such as habitat condition,

environmental strategies.

and the vertical axis shows water quality. Recent

The Governorʼs and Mayorʼs Conference forshifts mean that not only is improvement of water

Environmental Conservation of the Seto Inland Sea

quality needed but also more active conservation,

has been seeking new policy, based on the concept

such as restoration of deteriorated habitat andofpromotion ofsince 2004. Some local governments out

activities, are necessary.

14

Osamu MATSUDAThis shift of management policy may help local sea

Consequence: The Case of the Seto Inland Sea, inareas to realize smooth material circulation and rich“Asia-Pacific Coasts and Their Management” (ed. by

ecosystems.

Mimura N.), Springer, The Netherlands, pp. 78-92.

In close relation to, ecosystem-based

management (EBM), community-based management

This is a case study on the management of theeutrophic Seto Inland Sea.

(CBM) and ICM are also very important concepts
for coastal management in the near future. Sincemeans community and(2) Secretariat of the Convention on Biologicalalso focuses

Diversity (CBD) (2011), Biological and Culturalon the relationship between humans and nature,

Diversity in Coastal Communities ‒ Exploring thecan be a type of diversified CBM.

Potential offor Implementing the Ecosystem

is also focusing on biological diversity and biologicalApproach in the Japanese Archipelago, CBD

productivity. Therefore,

Technical Series No. 61, Montreal, 118pp.

can be a part of

EBM. Besides, combination ofandThis volume provides relevance oftocan be a type of ICM, including both land and sea.

biodiversity issue and case studies ofSimilarities and differences among

activities from Hokkaido northernmost area to, CBM,

EBM and ICM should be made clearer and easier to

Okinawa southernmost area of Japan.

understand in the near future.
The next possible step of coastal management(3) Okaichi T. and Yanagi T. (ed.) ,1997: Sustainable

under the new policy might be as follows. Integration

Development in the Seto Inland Sea Japan-From theof science into management decisions and managing

Viewpoint of Fisheries, Tera Scientific Publishinghabitats through application of biological information

Company, Tokyo, 329pp.

from all available data sources is necessary.
Recognizing the importance of ecological networks

This book provides valuable information on the
Seto Inland Sea until 1990s.

from forests and rivers to the sea, including thehuman dimension, is also necessary. A comprehensive(4) Stickney R. R. and McVey, J. P. (ed.) ,2002:

management of the material flow from hilltop to

Responsible Marine Aquaculture, CABI Publishing,

the coastal environment is essential for successful

Maryland, 391pp.

costal management. Managing coastal habitats byparticipatory activities of people, based on increasingThis is a milestone work on the development ofsustainable and responsible marine aquaculture.

public awareness, adopting appropriate legislationand enforcement, is also essential. Coordination(5) Okaichi, T. (ed.) ,2003: Red Tides, Tera Scientificacross sectors to improve governance and efficiency

Publishing Company, Tokyo, 439pp.

and addressing trans-boundary issues are mostThis book provides comprehensive aspects ofimportant in the future of coastal management. In

red tides such as phenomena, organism, ecologicalorder to restore once lost rich and healthy coastal

problems, environmental relevance and mechanism

seas in deteriorated areas,of outbreaks.

can play a role inactive conservation measures to restore deteriorated
ecosystems. Valuable coastal areas, such as tidal flats(6) Yanagi T., 2007: Sato-Umi: A New Concept forand sea grass beds, which were already lost by land

Coastal Sea Management, Terra Scientific Publishingdevelopment, were historically a kind of commons or

Company, Tokyo, 94pp.

shared space for people. And, therefore, to take backthese kinds of common spaces for people is also an
important role ofThis book was written by the first proposer of theconcept of Sato-Umi ().

in the future.
(7) Matsuda O., 2012: Western Japan cluster: Seto

Annotated bibliography

Inland Sea as, in “Ecosystems and Human Well-Beings” (ed. by(1) Matsuda O., 2008: Eutrophication and its Cause/

Duraiappah A. K., Nakamura K., Takeuchi K.,

15

New management policies in the Seto Inland Sea
Watanabe M., and Nishi M.), United Nations(9) Berque J. and Matsuda O., 2013: Coastal

University Press, Tokyo, pp. 381-402.

Biodiversity Management in JapaneseThis is a comprehensive reference of the Seto
Inland Sea and also a part of the result of Sub-Global
Assessment on Japanese Satoyama and.

, 39, 191-200.
This paper refers to relevance oftobiodiversity management.

(8) Matsuda O., 2012: Combining Activities ofand.

(10) Matsuda O., 2014: Predicting and promoting thein Japan: Towards a New Typefuture state of coastal seas with special emphasis

of Integrated Coastal and Watershed Management, inon“The Dilemma of Boundaries-Toward a New Concept

Oceans, Challenge to Improvement of Watershed andof Catchment” (ed. by Taniguchi M. and Shiraiwa T.),

Coastal Environments” (ed. by Shimizu N., Tateno

Springer, The Netherland, pp. 221-234.

R., Kasai A., Mukai H., and Yamashita H.), Kyoto

This paper describes the possibility of integrated
coastal management by connecting.

and, in “Connectivity of Hills, Humans andUniversity Press, Kyoto, pp.209-221.
Some aspects of future perspective of
were described in this paper.

水 研 機 構 研 報， 第 49 号，17 − 17， 平 成 31 年
Bull. Jap. Fish. Res. Edu. Agen. No. 49，17−17，201917

Marine aquacultureʼs role in providing nutritional security in achanging environment
Michael B. RUST＊

Abstract: The world produces less than 2 % of its food, fiber and biofuel from the sea despite thefact that oceans cover 70 % of the earth and receive 70 % of its solar energy. Instead we use 70 %of available freshwater and 40 % of our land through agriculture to feed and clothe ourselves. Futureworld food security plans developed by governments and international agencies often focus mainlyon improving agriculture with an occasional nod toward fisheries, but rarely consider what
aquaculture, especially marine aquaculture could provide. Marine aquaculture represents a foodproduction approach that uses less freshwater, feed and land resources than agriculture, is moreenergy efficient and emits fewer greenhouse gasses than agriculture. In addition, marine aquaculture
is relatively buffered from some aspects of climate change. For example, marine aquaculture does
not suffer from droughts or floods, and is buffered from extreme storm events and temperaturechanges. Properly sited and managed, marine aquaculture can provide ecosystem services that help
wild stocks persist under changing environmental conditions. Finally, the nutritional quality of
aquaculture products is high relative to terrestrial products, increasing the nutritional quality of thediet for society. Marine aquaculture needs to articulate the advantages it represents to world
nutritional security so discussions and planning for future food security under a changing climate
can be informed.
Key words: N/A

Annotated bibliography(2) Forster J. and Radulovich R., 2015: Chapter
11 - Seaweed and food security, in “Seaweed(1) U.S. Department of Health and Human Services

Sustainability” (ed. by Tiwari B. K. and Declan J. T.),and U.S. Department of Agriculture, 2015 ‒ 2020

Academic Press, San Diego, pp. 289-313.

Dietary Guidelines for Americans, 8th Edition,

Makes the case for a marine agronomy based on

December 2015. Available at https://health.gov/

seaweeds analogous to terrestrial agronomy that

dietaryguidelines/2015/guidelines/.

currently provides the majority of our food and fiber.

Every five years the US government reviews
current nutritional research and analyzes US food(3) Hall S. J., Delaporte A., Phillips M. J., Beveridge M.,

consumption patterns to develop guidelines. Seafoodand OʼKeefe M., 2011: Blue Frontiers: Managing theis chronically under consumed by all age groups andEnvironmental Costs of Aquaculture, The WorldFish

both sexes. This has real impacts on human healthCenter, Penang, Malaysia.

and results in increased heart disease, stroke andProvides a comparison between aquaculture

dementia in the US population. Americans consume

and terrestrial production from an environmental

about half of what is recommended for optimal

perspective.

human health.

2018年８月31日受理（Accepted on August 31, 2018）NOAA Office of Aquaculture, 1315 East-West Highway, Silver Spring MD. 20910, U. S. A.
E-mail: mike.rust@noaa.gov＊

水 研 機 構 研 報， 第 49 号，19 − 19， 平 成 31 年
Bull. Jap. Fish. Res. Edu. Agen. No. 49，19−19，201919

An overview of NOAA grants on aquaculture and the environment
Shiyu Rachel WANG＊

Abstract: NOAA funds extramural research on aquaculture and environmental change throughthree major competitive grants: Small Business Innovation Research (SBIR) Program, SaltonstallKennedy (SK) Grant Program and Sea Grant Program. From 2002 to 2016, NOAA has spent $9.2
million U.S. dollars on research projects focus on the interactions between aquaculture and theenvironment, with $6.5 million federal funds and $2.7 million matching funds. Annual spending
fluctuated with a maximum of $1.3 million in 2005 and a minimum of $0.14 million USD in 2002 andzero spending in 2009. Out of the three major funding programs, Sea Grant funded 75 % of the entire
spending. A total of 43 projects on aquaculture and related topics including nutrient removal, carbon
fixation, ocean acidification, waste treatment and related topics were completed. Analysis of the
impact of these projects is planned. An understanding of NOAAʼs spending can help identify
research gaps, evaluate impact, inform policy and allocate budget related to aquaculture in achanging environment.
Key words: N/A

Annotated bibliography

in aquaculture, followed by aquatic animal healthand disease (17 %). Environment related aquaculture(1) Love D. C., Gorski I., and Fry J. P., 2017: An

topics including water and waste management andAnalysis of Nearly One Billion Dollars of Aquaculture

environmental interactions received 7 % of theGrants Made by the US Federal Government fromtotal federal funding across all related agencies.

1990 to 2015.

Comparing the U.S. domestic aquaculture production., 48(5), 689-710.

The authors conducted a study on U.S. federal

with the federal spending, the authors concluded aspending for aquaculture by tracking 2957 federal

37-fold return in federal government investments inresearch grants awarded through different agencies

aquaculture since 2000. This study can be used asfrom 1990 to 2015. For the past quarter century, 1.04

a framework to track and assess federal agenciesʼ

billion US dollars were spent on aquaculture research

spending on different topics of aquaculture, identify

with about 90 % of federal funds and 10 % matchingresearch gaps and inform policy making and grant

funds. Aquaculture production sciences received

allocation.

the most funding (27 %) out of 13 major disciplines

2018年８月31日受理（Accepted on August 31, 2018）NOAA Headquarters, Office of Aquaculture,1315 East-West Highway, Silver Spring MD. U. S. A. 20910
E-mail: shiyu.wang@noaa.gov＊

水 研 機 構 研 報， 第 49 号，21 − 26， 平 成 31 年
Bull. Jap. Fish. Res. Edu. Agen. No. 49，21−26，201921

Oligotrophication and its measures in the Seto Inland Sea, Japan
Katsuyuki ABO＊1 and Tamiji YAMAMOTO＊2

Abstract: The Seto Inland Sea experienced eutrophication during the period of high economic
growth and then subsequent oligotrophication due to reduction of inflow load. The nutrient
concentration in the seawater peaked in the beginning of 1970ʼs, and thereafter, it has been
decreasing. Dissolved inorganic nitrogen (DIN) has remarkably decreased in recent years following
the decrease in dissolved inorganic phosphorus (DIP). As a result, Nori () production has

decreased in recent years due to bleaching of leaves caused by DIN deficiency. Recent slack infisheries production was also likely influenced by the nutrient depletion as evidenced by the fish
catch using a compact trawl. The process of both eutrophication and oligotrophication that occurredin the Seto Inland Sea can be explained by hysteresis. We introduce several countermeasures to theoligotrophication in the Seto Inland Sea. In particular, to improve Nori production, local nutrient
supply was experimentally augmented, such as by application of fertilizer, temporary discharge ofdam water, sediment plowing, and ad hoc operations of relaxing sewage treatment water.
Key words: fisheries production, nutrient, oligotrophication, Seto Inland Sea

Introductionchanges in and current situation of water quality
in the Seto Inland Sea and discuss the influence of

The Seto Inland Sea had been known as aload reduction on the lower trophic ecosystem andbeautiful and bountiful sea with a rich ecosystem.

fishery production. We also introduce nutrient supply

However, during the period of high economic growth,methods, which were experimentally conducted as

eutrophication progressed, and fishery damage

countermeasures for bleaching Nori.

caused by harmful algal blooms became frequent.
Since the Interim Measures Law concerning

Variation of water quality

Conservation of the Environment of the Seto Inland
Sea (later the Special Measures Law) was enacted

Fisheries research institutions surrounding thein 1973, the water quality of the Seto Inland Sea has

Seto Inland Sea have been monitoring the monthly

improved by a series of measures such as reduction

water quality since 1973. The monitoring has beenof inflow load. On the other hand, oligotrophication

carried out using similar methods over time, and it

has become a problem in recent years (Yamamoto,can elucidate the process of cultural oligotrophication

2003), and it caused a decrease in Nori ()

in the Seto Inland Sea. Fig.1 shows the variations of

production due to bleaching of leaves because ofannual averaged concentrations of dissolved inorganic

nutrient depletion (Murayama

nitrogen (DIN) and dissolved inorganic phosphorus., 2015; Tada., 2010). In addition, it is also pointed out that the(DIP) in the surface layer of the Seto Inland Sea. The

decrease in fisheries production, such as small pelagic

DIN concentration was extremely high in the 1970s,

fish and demersal fish, is related to nutrient reduction

decreased sharply in the 1980s, and then remained(Tanda and Harada, 2012). Here, we describe theflat. After that, it decreased again in the latter half of2018年８月31日受理（Accepted on August 31, 2018）
National Research Institute of Fisheries and Environment of Inland Sea, Fisheries Research and Education Agency, 2-17-5 Maruishi,
Hatsukaichi, Hiroshima 739-0452, Japan＊2
Hiroshima University, Higashi-Hiroshima, Hiroshima 739-8528, Japanabo@fra.affrc.go.jp＊1

22

Katsuyuki ABO and Tamiji YAMAMOTO

the 1990s and remains at low levels in recent years.
According to the pollutant discharge loads in the
Seto Inland Sea (Fig.2), the load of chemical oxygen
demand (COD) sharply decreased in the latter halfof the 1970s, and the load of total nitrogen (TN)decreased after the latter half of the 1990s, whichis in good agreement with the decreasing periodof the DIN concentration. On the other hand, the
DIP concentration remained flat after decreasing
until the early 1980s. The load of total phosphorus(TP) has sharply decreased in the first half of the
1980s following reduction of the load of COD in thelatter half of the 1970s, which is consistent with thedecreasing DIP concentration. However, there wasno decrease in DIP concentration corresponding to
the TP load reduction in the early 2000s.
Regarding water quality in each sub-area (Fig.3),
DIN started to decrease in the 1980s in the westernpart, then it tended to decrease in the 1990s in theeastern and central parts of the Seto Inland Sea. The
decreasing rate of DIN concentration in the surface
layer of each sub-area was 0.16 to 0.26 μM per year,
but it was largest in the eastern part, Osaka Bay andHarima Nada (Abo., 2018). On the other hand,Fig. 1. Temporal variations in annual averaged
concentration of dissolved inorganic nitrogen (DIN)
and phosphorus (DIP) in the surface layer of the Seto
Inland Sea, Japan.

the DIP concentration had no large variation overthe entire Seto Inland Sea, but the molar ratio of DIN
and DIP has changed from 16 - 17 to 8 - 10 in thepast 30 years, i.e., it has changed from a value close
to the Redfield ratio to nitrogen deficiency (Tanda., 2014).
Variation of fisheries production
Recently, fisheries production in the Seto Inland
Sea has been stagnant. Especially for Nori ()

culture, the influence of nutrient deficiency due tocultural oligotrophication is crucial to production.
The annual production of Nori in the Seto InlandFig. 2. Five-year changes in the generated loads
of chemical oxygen demand (COD), total nitrogen(TN) and total phosphorus (TP) flowing into the Seto
Inland Sea, Japan.

Sea increased in 1970s due to the maturation of theaquaculture technology and reached 4 billion sheetsin the 1980s. In the 1990s, it remained at more than
3.5 billion sheets. However, it decreased sharply inthe 2000s and has been around 2 billion sheets inrecent years (Fig.4). The sharp decrease in the Nori
production after 2000 coincided with the decrease in
DIN concentration mentioned above. Since the late
1990s, bleaching of Nori leaves caused by nitrogen

Fig. 3. Map of the Seto Inland Sea and sub-areas.

Oligotrophication and its measures in the Seto Inland Sea

23

depletion occurred frequently. The bleaching of Nori
leaves is said to occur at DIN concentrations of 3
μM or less in the eastern part of the Seto Inland Sea(Murayama., 2015). DIN deficiency is the maincause of the recent decrease of Nori production, but
global warming may also cause a decrease in Nori
production because water temperature rise could
have shortened the culture period.
The fish catch of the Seto Inland Sea peaked in
the beginning of the 1980s, but the catch in 2014 wasless than 160,000 tons, which is one third of the peak
production (Fig.5). The cause of the catch decline is
not clear. Although land reclamation during the rapid
economic growth period in Japan and overfishing
could be responsible for the decrease in fish catch,

Fig. 4. Annual variation of Nori (in the Seto Inland Sea, Japan.

) production

oligotrophication is pointed out as a decisive factor
in the decrease in fishery production. Tanda andHarada (2012) revealed that fluctuations in catch ofsand lancein Harima-Nada in

the eastern part of Seto Inland Sea synchronized withfluctuations in the DIN concentration, with 2-3 years
lag. There was also a tight relationship between
0-year-old sand lance and DIN concentration.
From these analyses, they concluded that nutrient
depletion affected early survival and growth of sandlance larva. Tarutani and Nakajima (2011) showed
the correlation between pollutant discharge load andthe catch of demersal fish and shellfish in Osaka Bay.
They also suggested bottom-up material flow may
play a role in recent decreases in fisheries productionin Harima-Nada.
As for Nori, which requires nutrients for growth,
reduction of nutrient load directly contributes tothe decrease in production. As coastal ecosystems
are largely affected by various human disturbances(Jackson, 2001), it is important to clarify theFig. 5. Annual variations of fish catch (upper) andshellfish production (lower) in the Seto Inland Sea,
Japan.

processes occurring in the ecosystem scientifically.
Processes of eutrophication and oligotrophication
Along with the eutrophication and oligotrophication

process, as mentioned theoretically by Scheffer (1989),

that occurred in the Seto Inland Sea, hysteresis was

fisheries production in the Seto Inland Sea did notobserved (Yamamoto, 2015). The pattern of increased

return to the original position; it decreased to a much

fisheries production during eutrophication was

lower level (Fig.6). Ecosystem structure might havedifferent from that during oligotrophication (Fig.6).

changed or overfishing may be a cause. The cause

Although fisheries production should return toof this issue is still under debate and remains to be

the original position at the end of oligotrophication

solved.

24

Katsuyuki ABO and Tamiji YAMAMOTO
activity, and other social backgrounds. Even in the
Practical measures against oligotrophication

totally oligotrophic state it is in, oxygen depletion in
the bottom water and/or harmful algal blooms occur

In the Seto Inland Sea, experimental attempts

in some sub-areas. Therefore, different measures

to supply nutrients to fishing grounds have been

applicable to each different sub-area are required.

made as a measure against the oligotrophication.

Furthermore, ideal water quality could be different

Especially to prevent the bleaching of Nori laver,among various stakeholders; some might desire

fertilizer application, temporary discharge of dam

higher water transparency, while others mightwater, relaxing discharge of sewage treatment

desire high fisheries production. We, therefore, needwater, etc., were carried out. A fundamental issue

an organization or council with various stakeholders

that is common to these techniques is the diffusion

representing different standpoints in each sub-area.

feature of seawater in the sea. Once we apply one ofthese techniques, added nutrient is diluted in a short

Referencestime. For example, relaxing the discharge of sewage
treatment water has been conducted to increase

Abo K., Akiyama S., Harada K., Nakaji Y., Hayashi

DIN concentration in the treated water to the

H., Murata K., Wanishi A., Ishikawa Y., Masui

allowable levels by suppressing denitrification and/T., Nishikawa S., Yamada K., Noda M., andor nitrification processes, with restriction during theTokumitsu S., 2018: Long-term variations in

winter Nori growing season. Evaluation by numericalwater quality and causal factors in the Seto

simulation reproduced the dispersion pattern of aInland Sea, Japan.

high nutrient water mass to the Nori cultivation area,

111. (in Japanese with English abstract)which was monitored by field observations (Abo., 2012; Harada., 2018).

In order to sustain fisheries production in theoligotrophic Seto Inland Sea, effective measures may

Abo K., Tarutani K., Harada K., Miyahara K.,
Nakayama A., and Yagi H., 2012: Effects ofnutrient discharge on Nori aquaculture areain Kako River estuary.

be different in each sub-area because of differencesin terms of geography, oceanography, fisheries, 55, 101-

, 68 (2), Ⅰ̲1116-Ⅰ̲1120.
Harada K., Abo K., Kawasaki S., Takesako F., andMiyahara K., 2018: Influence of DIN derived
from ports and treated sewage effluent on nori(

) farms of the northeastern part ofHarima Nada.

., 82,

26. (in Japanese with English abstract)
Jackson J. B. C., Kirby M. X., Berger W. H., Bjorndal
K. A., Botsford L. W., Bourque B. J., Bradbury R.
H., Cooke R., Erlandson J., Estes J. A., Hughes T.
P., Kidwell S., Lange C. B., Lenihan H. S., Pandolfi
J. M., Peterson C. H., Steneck R. S., Tegner M. J.,
and Warner R. R., 2001: Historical Overfishingand the Recent Collapse of Coastal Ecosystems.
, 293(5530), 629-637.
Murayama F., Shimizu Y., and Takagi S., 2015: The
relationships between nutrient concentration in
the coastal area of Okayama prefecture, the color
tone of fresh thalli (Fig. 6. The theoretical path and the actual pathobserved in the Seto Inland Sea as an example ofhysteresis.

) and the unit price ofdried nori.

81, 107-114.

(in Japanese with English abstract)
Scheffer M., 1989: Alternative stable states in25

Oligotrophication and its measures in the Seto Inland Sea
eutrophic, shallow fresh water systems: A

discharge on Nori aquaculture area in Kako River

minimal model.

estuary.

., 23, 73-83.

Tada K., Fujiwara M., and Honjo T., 2010: Water
quality and nori (., 68 (2), Ⅰ̲1116-

Ⅰ̲1120.

) culture in the Seto

Effects of nutrient discharge on Nori aquaculture

59, 945-955. (inarea were investigated. The Nori production in the

Inland Sea.
Japanese with English abstract)

winter season were sustained by nutrient discharge

Tanda M., Akashige S., Ariyama H., Yamanoi H.,

from the river, sewage treatment plant and industrial

Kimura H., Dan H., Sakamoto H., Saiki Y., Ishidaeffluent. A numerical simulation evaluated theY., Kotobuki H., and Yamada T., 2014: Nutrient

effects of nutrient control operation of the sewage

environment and fisheries in the Seto Inland

treatment plant on the nutrient environments of theSea.

aquaculture area.

, 7, 37-46. (inJapanese with English abstract)
Tanda M. and Harada K., 2012: Nutrient environment
and Fishery Production in Harima-nada, Eastern
Seto Inland Sea, Japan.

, 34, 132-141.

(in Japanese with English abstract)(3) Yamamoto T., 2002: The Seto Inland Sea‒eutrophic
or oligotrophic?.

., 47, 37-42.

This was the first study showing the Seto Inland
Sea was in the state of ʻcultural oligotrophicationʼ

Tarutani K. and Nakajima M., 2011: Effect of nutrient

caused by the reduction of nutrient loading. This

reduction on fisheries resources in enclosed sea

study indicated that the measures to reducewaters.

phosphorus had caused a change in phytoplankton., 34(A), 47-50. (inJapanese)

species composition, thereby altering the food web

Yamamoto T., 2003: The Seto Inland Sea- Eutrophic
or oligotrophic?.

., 47, 37-42.

structure, suggesting that this might be the major
cause of the reduction of fishery production.

Yamamoto T., 2015: Cultural oligotrophication in
the Seto Inland Sea, in “Oligotrophication in(4) Yamamoto T. and Hatta G., 2004: Pulsed nutrient

inland and sea waters” (ed. by Yamamoto T. andsupply as a factor inducing phytoplankton diversity.

Hanazato T.), Chijinshokan, Tokyo, pp. 55-87. (inJapanese)., 171, 247-270.
A numerical model was constructed to elucidate
whether phytoplankton species diversity could be

Annotated Bibliography

increased by an environmental fluctuation suchas a pulsed nutrient supply. Diatom showed large(1) Abo K., Akiyama S., Harada K., Nakaji Y., Hayashi

fluctuations in cell density in response to pulses ofH., Murata K., Wanishi A., Ishikawa Y., Masui T.,

nutrients, while dinoflagellate showed preference for

Nishikawa S., Yamada K., Noda M., and Tokumitsu

continuous nutrient supply mode. Dam construction,S., (accepted): Long-term variations in water quality

which is one of the causes of oligotrophication, usuallyand causal factors in the Seto Inland Sea, Japan.

flattens variability in the freshwater discharge, hence., 55.

lead to dinoflagellate dominancy.

The long-term variations in water quality in
the Seto Inland Sea were investigated based on(5) Yamamoto T., Tateno S., Hata K., Mizushima K.,

the routine observation data of the local fisheries

Goda Y., Takahashi S., Tarutani K., Saito H., andexperimental stations. The water temperature

Tanimoto T., 2017: Designing an effective action

increased due to the global warming and the nutrient

plan for sustainable local resources and the coastal

decreased due to oligotrophication. The reduction ofenvironment: A case study of Mitsu Bay, Hiroshima,

DIN and DIP concentrations were largely affected by

Japan. Proceedings of International Conference

land load reduction.

"Managing risks to coastal regions and communities
in a changing world" (EMECS'11 - SeaCoasts(2) Abo K., Tarutani K., Harada K., Miyahara K.,

XXVI, St. Petersburg, 22-27.08.2016). Moscow,

Nakayama A., and Yagi H., 2012: Effects of nutrient

RIOR Publ., ISBN978-5-369-01628-2, DOI: 10.21610/

26

Katsuyuki ABO and Tamiji YAMAMOTO

conferencearticle̲58b43157871ef

necessary. As oyster cultivation was popular inThis study proposed measures for sustainable

this bay, improvement of sediment quality using

fishery production in an oligotrophic bay (Mitsu Bay).

oyster shells could contribute to the formation of a

Water quality was extremely good (oligotrophic),

recycling-oriented society.

therefore improvement of sediment quality was水 研 機 構 研 報， 第 49 号，27 − 34， 平 成 31 年
Bull. Jap. Fish. Res. Edu. Agen. No. 49，27−34，201927

Assessment and future prediction of climate change impacts on themacroalgal bed ecosystem and cultivation in the Seto Inland Sea
Goro YOSHIDA＊1, Hiromori SHIMABUKURO＊1, Setuo KIYOMOTO＊2, Tatsuru KADOTA＊2,
Taku YOSHIMURA＊2, Noboru MURASE＊3, Mikio NODA＊3, Shoichi TAKENAKA＊4,
Yoshimi KONO＊4, Toshiharu TAMURA＊5, Norio TANADA＊6, Xiaojie YU＊7, Naoki YOSHIE＊7,
and Xinyu GUO＊7

Abstract: Macroalgal bed ecosystems are an important platform for coastal biological production
and fisheries. After the late 1990s, rapid decline or disappearance of macroalgal beds, generally
called, has been spreading along the coast of western Japan where there is an influence ofwarm ocean currents. This phenomenon has been occurring with an increasing trend in watertemperature in recent decades and is considered to be an impact of the climate change.
The Seto Inland Sea is the largest semi-enclosed sea area in Japan, and macroalgal beds in thearea are still intact with no prominent sign of. However, water temperature in the Seto

Inland Sea has also been increasing for a few decades, and according to climate change scenarios,
negative impacts to macroalgal beds and their ecological functions are possible in the future in thearea. Against this background of concern, we conducted research on the assessment and future
prediction of climate change impacts on the macroalgal bed ecosystem in the Seto Inland Sea andassociated sea areas. The research consisted of 1) field monitoring of macroalgal beds and associatedspatio-temporal variation in water temperature, including along the coast of Kyushu (Nagasaki)
where loss or changes of macroalgal beds has created a large social problem; 2) experiments on
physiology and behavior of key species in macroalgal bed ecosystems (macroalgae and herbivorousfish) with respect to temperature and other conditions to understand the mechanisms of theecosystem shift; 3) construction of an original physical model to reproduce past temperatures in theenvironment and predict future ones in the applicable ocean areas; and 4) interpreting the impact of
future water temperature conditions predicted by the model on macroalgal beds. In addition,
impacts on macroalgal cultivation, which is an important industry in the Seto Inland Sea, were also
assessed. In this paper, some of the main results and conclusions are introduced.
Key words: macroalgal bed, macroalgal cultivation, climate change, Seto Inland Sea

2018年８月31日受理（Accepted on August 31, 2018）
National Research Institute of Fisheries and Environment of Inland Sea, Japan Fisheries Research and Education Agency, 2-17-5 Maruisihi,
Hatsukaichi, Hiroshima 739-0452, Japan＊2
Seikai National Fisheries Research Institute, Japan Fisheries Research and Education Agency, Taira-machi, Nagasaki, Nagasaki 851-2213, Japan＊3
National Fisheries University, Japan Fisheries Research and Education Agency, Nagata-honmachi, Shimonoseki, Yamaguchi 759-6595, Japan＊4
Fisheries Research Center, Ehime Research Institute of Agriculture, Forestry and Fisheries, Shitaba, Uwajima, Ehime 798-0104, Japan＊5
Ehime Prefectural Government, Ichibancho, Matsuyama, Ehime 790-8570, Japan＊6
Fisheries Research Division, Tokushima Prefectural Agriculture, Forestry and Fisheries Technology Support Center, Minami-cho, Kaifu-gun,
Tokushima 779-2304, Japan＊7
Center for Marine Environmental Studies, Ehime University, Bunkyo-cho, Matsuyama, Ehime 790-8577, Japan
E-mail: gorogoro@affrc.go.jp＊1

YOSHIDA, Hiromori SHIMABUKURO, Setuo KIYOMOTO, Tatsuru KADOTA, Taku YOSHIMURA, Noboru MURASE, Mikio
28 GoroNODA, Shoichi TAKENAKA, Yoshimi KONO, Toshiharu TAMURA, Norio TANADA, Xiaojie YU, Naoki YOSHIE, and Xinyu GUO
Introduction

sea area in Japan, situated between western Honshu
and Shikoku Islands and connected with the PacificMacroalgal bed ecosystems offer various

Ocean via the Bungo and Kii Channels. In contrast

ecosystem services, which substantially contributewith the drastic change in the macroalgal beds along

to human welfare. Among the services provided by

the Shikoku and Kyushyu areas being affected by thethe macroalgal beds, their contributions as nursery

warm currents, macroalgal beds in the Seto Inland

grounds, habitats and actual fishery grounds of

Sea have remained productive and still contribute tocommercially important fishes and shellfishes are

the coastal fisheries, which are important industries insignificantly important in Japan.

this region (Yoshida., 2011). This is attributable to

However, rapid disappearance of macroalgal

the special environmental characteristics of the Seto

beds and subsequent desertification of the seafloor,

Inland Sea, which experiences little direct effects ofwhich is a phenomenon generally called 'the Kuroshio and maintains lower water temperature', hasbeen spreading along the Japanese coast (Fisheries

conditions than those of the Pacific coastal regions.

Agency, 2007). In particular, along the coast of

However, water temperature in the Seto Inlandwestern Japan (that is, central Honshu, Shikoku

Sea is also showing an increasing trend (+0.11 ~and Kyushu coastal areas facing the Pacific Ocean

0.33 ℃/ 10 y at surface, National Research Instituteand East China Sea), where the warm currentsof Fisheries and Environment of Inland Sea, 2015).

flow offshore, nearly

If it continues to increase according to the present

20 % of the macroalgal beds have already been lostandscenarios of climate change, macroalgal beds insince the early 1990s when a nationwide research

the Seto Inland Sea are also feared to be greatlyof macroalgal bed distribution was conducted

diminished and fisheries relying on these macroalgal(Akimoto and Matsumura, 2010). Most of the lost

beds will be seriously damaged (Yoshida, 2018).

beds were constituted by warm-temperate kelp,
mainly macroalgae belonging to the genus,

In addition to the importance of fisheries,
macroalgal cultivation, such as for(laver,and macroalgae belonging to Family Sargassaceae,spp.) and

which were the most important foundation species

is also an important industry in the Seto Inland Sea.

along temperate rocky shores in Japan. As a result,

Macroalgal cultivation occupies over 20 % of the total

production of fisheries resources that rely on

production value (131 billion yens in 2012) of fisheries

these beds (such as abalones) has been decreasing

and aquaculture of the Seto Inland Sea. However,tremendously in those regions (Serisawa., 2004).

increases in water temperature can also have a great

Increasing coastal water temperatures over

impact on the cultivation because these macroalgae

several recent decades and an increase in browsing(sea mustard,),

are so sensitive to higher temperature conditions.

of herbivorous animals (fishes and invertebrates

United against these future fears, we joined thelike sea urchins) on macroalgae associated with theresearch project by Ministry of Agriculture, Forestry

temperature rise are considered direct factors inand Fisheries named “Technology development fortheoccurrence (Fisheries Agency, 2007). In

circulatory food production systems responsive toaddition, in some areas in western Japan, sub-tropicalclimate change” (2013-2017) and conducted researchmacroalgae and corals expand their distribution as

on predicting climate change impacts on macroalgalthe ʻoriginalʼ macroalgal beds decline (Tanaka.,

bed ecosystems and cultivation in the Seto Inland2012). Ocean area along Kuroshio is one of the hot-Sea and its connecting waters. The research

spots showing a much larger increase in surface

consisted of 1) field monitoring of macroalgal beds

seawater temperature than the global mean, andand associated spatio-temporal variation in watertemperate coastal ecosystems in the ʻhot-spotsʼ, which

temperature, including along the coast of Kyushu

also includes the Australian coasts, eastern coastal(Nagasaki) where loss or changes of macroalgal beds

area of South America, etc., have been suffering fromhas created a large social problem; 2) experiments on

̀tropicalizationʼ (Vergés

physiology and behavior of key species in macroalgal., 2014).

The Seto Inland Sea is the largest semi-enclosed

bed ecosystems (macroalgae and herbivorous fish)

29

Climate change impacts on the macroalgal bed ecosystemwith respect to temperature and other conditions

places in Nagasaki Prefecture, but expansion of

to understand the mechanisms of the ecosystemcorals and tropicalshift; 3) construction of an original physical model toin some places after kelp and temperate

reproduce past temperatures in the environment andbeds disappeared (Kiyomoto

species were observed., 2018).

predict future ones in the applicable ocean areas; 4)

The other area of the survey was the westerninterpreting the impact of future water temperature

Seto Inland Sea and Bungo Channel, which connects

conditions predicted by the model on macroalgal

the western Seto Inland Sea and Pacific Ocean.

beds; and 5) macroalgal cultivation. In this paper, we

We set many survey stations along a geographicalintroduce the outline of our research and show somenorth to south transect from Hiroshima Bay in theof the main results and conclusions.

Seto Inland Sea to southern Uwa Sea, which is aneastern part of the Bungo Channel, and conducted

Outline of the research

surveys on the macroalgal bed vegetation in 2013-14.
Within this relatively small geographical area (ca. <Field monitoring and surveys of macroalgal beds

200 km in distance), there is a large surface wateralong spatio-temporal environmental gradients intemperature gradient, especially during winter, inwestern Japan

which the annual minimum temperature drops below

To find any specific relationship between change

10 ℃ in Hiroshima Bay but never drops below 15 ℃

of macroalgal beds and the environment, includingin the southern Uwa Sea (Yoshidawater temperature conditions, we have beenfound clear shifts in macroalgal vegetation along

conducting field monitoring and surveys in two areas

the temperature gradient in beds 1) composed ofin western Japan.

kelp +

One area is along the coast of Nagasaki Prefecture(north-western Kyushu) where

has been., 2011). We, 2) composed of only,3) with no large brown algae but small undergrowthalgae, and 4) with tropicaland somea serious social problem since the late 1990s. The

corals in themonitoring was begun in 1998 when drastic changes

crustose coralline algae) (Shimabukuro

in macroalgal beds were first observed. Beds ofInterestingly, this geographical shift in the vegetation

a warm temperate kelp

was analogous to the temporal shift in vegetation

were

greatly damaged by browsing of herbivorous fish,
such as,landscape (barren seafloor with., 2018).

observed in Nagasaki after the late 1990s.

andThese results indicated that there were discrete, along the coast of Nomo-Zaki,

steps in the vegetative changes as macroalgal beds

Nagasaki Peninsula. Extremely high summer water

declined or turned into an

temperatures seriously damaged the kelp in 2004

water temperature increase was a strong driving

and 2008, and in combination with heavy browsing,factor of the change. The field monitoring andkelp beds completely disappeared in Nomo-Zaki untilsurveys also indicated that warm-temperate kelp

2013. Sargassaceous plants, the other major member

was the most vulnerable to increasing seawaterof rocky macroalgal beds, seemed to be more tolerant

temperature.

situation, andto high temperature than the kelp, but heavybrowsing concentrated onafter the kelp

In-house experiments on the effects of water

species intemperature rise on key organisms in macroalgal

disappearance. The number ofthe beds has gradually decreased, andbecame the dominant species until 2011. However,bed ecosystems
Physiological vulnerability of kelp andthis species also disappeared due to browsing and theto high temperature conditions and behavioral

effects of a typhoon soon after kelp had disappeared.

characteristics of rabbit fish (After those large brown algae disappeared, only

which is one the major herbivorous fish, wassmall undergrowth macroalgae, such as

examined by indoor experiments in our research

and

),

spp., constituted the macroalgal(Murase and Noda, 2018). The experiments werebeds. Similar situations were observed in many

also aimed at finding some threshold temperature

YOSHIDA, Hiromori SHIMABUKURO, Setuo KIYOMOTO, Tatsuru KADOTA, Taku YOSHIMURA, Noboru MURASE, Mikio
30 GoroNODA, Shoichi TAKENAKA, Yoshimi KONO, Toshiharu TAMURA, Norio TANADA, Xiaojie YU, Naoki YOSHIE, and Xinyu GUO
conditions relating to the macroalgal bed ecosystem

concentrates on the remaining beds, which means thechanges caused by physiological limits or the effects

size of fish school attacking each bed becomes larger.

of browsing behavior.

The loss of macroalgae by browsing accelerates and,the beds disappear rapidly. And, if damage is so large

which is a main kelp species in the Seto Inland Sea

High-temperature tolerance inas to restrain macroalgal reproduction, the change

and Kyushu, was tested. Young sporophytes ofproceeds irreversibly.

exhibited slight growth under 28 ℃, but
under 29 ℃, the growth rate was negative and they

Construction of a physical model for numerical-

were dead within 9 days of culture. It was reported

simulation of the temperature environment inthat upper temperature limits for survival of the kelp

the Seto Inland Sea and, one of the main temperate kelps incoastal area

‒ Reproduction of past temperature history andJapan, was also 29 ℃, so it is difficult for kelp beds

collation with current macroalgal bed distribution

in western Japan to be persistent when summer

To understand how current macroalgal bed

water temperatures exceed 29 ℃ for a relatively long

distributions were determined by water temperature

period, a situation that has recently come to occur

conditions and how they will change according tofrequently. Sargassaceous plants are more tolerant

future climate change, we constructed an original

to high temperature conditions, and upper limits of- Seto Inland Sea hydrodynamic model intemperature for survival of main temperate species

our project. The objective of the model is to reproduce

such asare aboutand understand past interannual variations in water

30-31 ℃. We also found that photosynthetic activity

temperature, salinity and currents in the Seto Inlandofnever declined under 30 ℃,

Sea and Kuroshio region, as well as to develop a tool

declined soon after being

for future prediction of these physical conditions in

andwhereas that oftransferred to the experimental condition of 30 ℃.

response to climate change.

Rabbitfish showed a preference of macroalgal

The main characteristic of the model was a highspecies for browsing, but both kelp and Sargassaceous

resolution 1 km grid because macroalgal beds

plants could be grazed by rabbitfish. However, thedistributes very locally as a narrow belt along theability of grazed plants to regenerate was larger

coast, in general, and outputs of the model shouldfor Sargassaceous plants than kelps because someexhibit the physical conditions corresponding to thespecies of

distribution. Also, parameters corresponding to theare able to regenerate the basal

part (holdfast or stem) of the plant (Yatsuya.,2012).

effects of tide and river discharge were incorporated
in the model as well as general ocean model

Rabbitfish grazed more under higher temperature.

parameters like heat fluxes and wind stress, etc.,

They grazed little under 20 ℃, and browsing almost

because these parameters can substantially affect the

stopped at 15 ℃. Browsing behavior was affected not

physical conditions of coastal areas, especially those

only by temperature, but also the size of its school.

in the Seto Inland Sea.

More macroalgal tissue was grazed by an individual

On the other hand, we illustrated current

fish as the size of the school of the fish grew, althoughmacroalgal bed distribution in the Seto Inland Sea

actual intake by the fish was getting smaller. Thatand Kuroshio coastal region in western Japan onmeans a large amount of macroalgal tissue wasa GIS map. Nationwide research on macroalgal

wasted without being assimilated by fish and more

bed distribution in Japan was conducted in thegrazed tissues were scattered on the seafloor whenearly 1990s under the initiative of the Ministry of

the school of the fish was large.

the Environment, but after that, no research on

These results described recent drastic changes
in macroalgal beds. Extremely high summer watertemperature can cause large-scale decline of kelp
beds. Though some kelp or

beds get overthe catastrophic event, browsing of herbivorous fisha nationwide scale has been conducted. However,loss of macroalgal beds due to spreading ofhas become prominent in various places
since the late 1990ʼs, and many local governments(prefectures) troubled withexpansion have

31

Climate change impacts on the macroalgal bed ecosystem
conducted their own original research on the status

model referred to the output of the atmosphericof macroalgal beds in their local areas (Akimoto andocean coupled model MIROC 5 corresponding toMatsumura, 2010). We referred to their reports for

AR 5 (by National Research Institute of Fisheries

constructing the map of the current distribution

Science). Predictions were made for the decades offrom late 1990ʼs to 2014. For some areas, we usedthe 2050s and 2090s, respectively.

the results of our field surveys described above (forUnder both RCP scenarios, surface water

Uwa Sea area of Ehime Prefecture) and the results

temperature increase is larger in the Seto Inlandof interviews.

Sea area than in the coastal area facing the PacificComparisons of macroalgal bed distribution in early

Ocean and in Bungo and Kii Channels. Also, water

1990ʼs and current distributions on the map indicatedtemperature increase from the current (2010s) was

great losses of temperate macroalgal beds of kelp andlarger in winter than in summer in the Seto Inland

in areas directly exposed to the PacificSea. In summary, under the RCP 8.5, a scenario ofOcean (e.g., Kochi and Miyazaki Prefecture). Alongcomparatively high greenhouse gas emissions, water

the coast of the Bungo and Kii Channels (Oita, Ehime

temperature increases + 2 ~ 4 ℃ in the 2050s (meanand Tokushima Prefectures), the southern boundaryof the 10 years, the same hereafter) and + 4 ~ 6 ℃

of kelp bed distribution has shifted northward a few

in the 2090s compared to the current temperaturestens of kilometers during these approximately 20

both in winter and summer, though the degree ofyears.

temperature increase is quite different locally among

The current macroalgal bed distribution wassea areas. Under RCP 2.6, in which measures against

overlayed with the outputs of surface water

greenhouse gas emissions are the most effective,

temperature (SST) conditions reproduced bywater temperature increases + 1 ~ 3 ℃ in thethe

2050s from current levels but its rise thereafter was(Shimabukuro-Seto Inland Sea Physical Model., 2018), and it was determined

predicted to be little up to the 2090s.

what kind of SST outputs best fitted and mostAccording to the prediction of future water

explained the macroalgal bed distribution. One clear

temperature environment, the distribution of kelp

result was shown in the distribution of kelp beds. The

beds in the Seto Inland Sea was also predictedcurrent distribution of kelp beds in the Seto Inland(Shimabukuro

Sea and Bungo Channel was clearly within the area

the prediction, including a warm condition criterion

where the total days of SST < 15 ℃ (daily mean) was

and a cool condition, which regulates the kelp

over 70 days / year (mean of 1993 - 2014). Under 15

distribution. For the cool condition criterion, kelp℃, activities of herbivorous fish almost stop evenbeds can be maintained at the places where the total

though kelp maintains its high productivity underdays of SST < 15 ℃ (daily mean) is over 70 days /that temperature condition (Yatsuya., 2014).

year, which was mentioned in the former section. For

Therefore, a duration of 70 days without herbivory is

the warm condition criterion, kelp beds cannot be

considered to be needed for persistent establishment

maintained when ambient daily mean SST reaches

of kelp beds.

29 ℃ over 6 consecutive days. This was the survival., 2018). Two criteria were used forlimit of the kelp
Prediction of future water temperature conditions
and macroalgal bed distributions in the Seto Inland
Sea
Using thedetermined in theindoor experiment.
Applying these criteria on the predicted SST outputof the model, future kelp bed distribution in the Seto

- Seto Inland Sea hydrodynamic

Inland Sea was predicted. Kelp beds will remain only

model we constructed the future water temperature

in Iyo-Nada and Aki-Nada sea areas in the 2050s

environment and macroalgal bed distributions

and will completely disappear in the Seto Inland Sea

reflecting that environment for the relevant sea areas.

by the 2090s under the RCP 8.5 scenario. On the

The prediction was based on the scenarios RCP 2.6

contrary, under the RCP 2.6 scenario, in which futureand RCP 8.5 in IPCC AR 5. The boundary condition

temperature rise will be moderate, most of the currentof the outer region of the corresponding area of thekelp beds were predicted to remain into the 2090s.

YOSHIDA, Hiromori SHIMABUKURO, Setuo KIYOMOTO, Tatsuru KADOTA, Taku YOSHIMURA, Noboru MURASE, Mikio
32 GoroNODA, Shoichi TAKENAKA, Yoshimi KONO, Toshiharu TAMURA, Norio TANADA, Xiaojie YU, Naoki YOSHIE, and Xinyu GUO
Effect of climate change on macroalgal cultivation

will be impossible in the current first half of the

As mentioned in Introduction, macroalgal

production season. The duration in which water

cultivation, such as for(laver) andtemperature drops below 15 ℃ is also predicted to(sea mustard), is an important regional industry

be shortened, and thus, cultured

in the Seto Inland Sea, but water temperature is

will be exposed to more heavy herbivory of fish.

andextremely important as it is for natural macroalgal
beds. “Seedlings” ofandare cultured inConclusions and future prospect for adaptations

artificial tanks on land during the summer as a minutegeneration of conchocelis (() or gametophytes

We predict temperate macroalgal beds composed). As ambient water temperature decreasesof kelp in the Seto Inland Sea will disappear by thein autumn, juvenile thalli ofor

begin toend of this century under the RCP 8.5 scenario in

be cultured in the cultivation field. Ambient water

which an extreme water temperature increase wastemperature of 23 ℃ is recommended at the start ofpredicted by the model simulation. As most of the beds

the culture, but the water temperature in autumn

were predicted to remain under the RCP 2.6 scenario,

has been increasing in the last several decades in theit will be a great value for the coastal ecosystem andSeto Inland Sea. As a result, suitable seasonal timing

fisheries or human lives relying on these ecosystems

for the start of cultivation has been delayed by 10 toto make maximum efforts to reduce greenhouse gas

20 days since the 1980s.

emissions. In addition, macroalgal beds in some areas

Recently, production incultivation has

were more likely to remain than those in other areas,

been affected by the changes in water temperature

possibly due to physical characteristics, such as tidal(Tanada, 2016), though production ofcultivation

currents or upwellings, specific to these areas. These

has been more affected by nutrient depletion, whichareas should be preferentially subject to conservationis also a recent serious problem in the Seto Inland Sea

of macroalgal beds. Combined with existing(Abo., 2015). In

cultivation, seedlings arecountermeasures protecting macroalgal beds

produced in an ambient condition in outdoor tanks, sofrom browsing pressures by herbivorous animals,

its production is easily affected by abnormal weather

productivity and ecological functions of these(e.g., extremely high air temperature in summer). In

macroalgal beds will be preserved effectively.

addition, many producers tend to begin cultivation

As these macroalgae are originally cold-waterin autumn according to the old-fashioned cultivation

species, it will become more difficult to cultivate

schedule without waiting for the appropriate waterandtemperature drops. All of these events lead to

For immediate measures, breeding of varieties

significant loss of seedlings due to physiologicaltolerant to higher water temperatures and their

damage or herbivory under high temperatureapplication will be effective, but they are still in theconditions. As a result, in the Naruto district, where

early stage of development. In thethe largest production area ofindustry, seedling production is still performed inexists,with increasing seawater temperatures.

cultivation

shortages and quality deterioration of seedlings haveits traditional and extensive way by the

been causing sharp declines in recent production,

farmers. Artificial seedling technology has proved

which is now less than 40 % of the peak in early 1990s

to be effective for a stable mass supply of seedlings,(Tanada, 2016).

avoiding the influence of weather conditions (Tanada

Further, the seasonal duration in which bothandcan be produced was predicted to be., 2015). Practical spreading of this technology
among the farmers will be important for maintaining

shortened in the future. In 2090s, the seasonal timing

production. However, when future waterat which ambient seawater temperature drops below

temperature increases exceed the adaptable range

23 ℃ will be delayed by about 4 weeks and 5.5 weeksof this macroalgal cultivation, introduction of newfrom the current under the RCP 2.6 and 8.5 scenarios,

cultured macroalgae, which are tolerant to warmer

respectively. Under these conditions, cultivation has

condition and with high economic values, will be

to be begun in mid-winter (January) and cultivationneeded.

(

) and

33

Climate change impacts on the macroalgal bed ecosystem() are candidates, and there are

an increasing number of producers who have started

with increased seawater temperatures in Tosa
Bay, southern Japan.

., 70, 189-191.

cultivating them. Even in macroalgal cultivation,

Shimabukuro H., Yoshida G., Kato A., and Guo X., 2018:

it will be necessary to develop countermeasures

Prediction of changing seawater temperature

against browsing of herbivorous animals, similar toand transition of seaweed bed distribution in themacroalgal bed conservation countermeasures.

next 100 years.

, 236, 233-242.

Tanada N., 2016: Development of a practical method
Acknowledgement

for mass seedling production using free-living
gametophytes and a new cultivar tolerant to

The research introduced in this paper was

warm waters for early harvesting of

supported by the research project of Ministry of(Harvey) Suringar.

, 225,

Agriculture, Forestry and Fisheries “Technology

464-471. (in Japanese with English abstract)development for circulatory food production systems

Tanada N., Dan A., Kusaka K., Oka N., and Hamano T.,

responsive to climate change”.

2015: A new practical method for mass seedling
production ofReferences(Harvey)

Suringer using free-living gametophytesthat originated from single zoospores and its

Abo K., Nakagawa N., Abe K., and Tarutani K.,

application for commercial cultivation.

2015: Nutrient dynamics and nutrient level
management for., 8, 23-36.

() culture in the

Tanaka K., Taino S., Haraguchi H., Prendergast G.,

eastern Seto Inland Sea.

, 218, 274-

and Hiraoka M., 2012: Warming off southwestern

279. (in Japanese with English abstract)
Akimoto Y. and Matsumura T., 2010: Available past
information on seaweed bed distribution andJapan linked to distributional shifts of subtidal
canopy-forming seaweeds.

.

., 2, 2854-

2865．

changes in seaweed bed area in Japanese coastal

Vergés A., Steinberg S. D., Hay M. E., Poore A. G. B.,

waters, in “Monitoring and maintenance ofCampbell A. H., Ballesteros E., Heck K. L., Booth

seaweed beds” (ed. by Fujita D, Murase N., and

D. J., Coleman M. A., Feary D. A., Figueira W.,

Kuwahara H.), Seizando-Shoten, Tokyo, pp. 17-24.

Langlois T., Marzinelli E. M., Mizerek T., Mumby(in Japanese)

P. J., Nakamura Y., Roughan M., van Sebille E.,

Fisheries Agency, 2007: Isoyake Taisaku Guidelines,
208pp. (in Japanese)

Gupta A. S., Smale D. A., Tomas F., Wernberg
T., and Wilson S. K., 2014: The tropicalization of

Kiyomoto S., Kadota T., Taneda T., and Yoshimura

temperate marine ecosystems: climate-mediatedT., 2018: Transition of seaweed bed along thechanges in herbivory and community phasewestern coast of Kyushu.

, 236, 210-

219. (in Japanese with English abstract)
Murase N. and Noda M., 2018: Influence of change

shifts.

, 281, 20140846.

Yatsuya K., Kiyomoto S., Yoshida G., and YoshimuraT., 2012: Regeneration of the holdfast in 13

in temperature on the growth of macroalgae

species of the genus

and browsing pattern by herbivorous fish.

the western coast of Kyushu, south-western, 236, 226-232. (in Japanese withEnglish abstract)

Japan.

grown along, 60, 41-45. (in Japanese with English

Abstract)

National Research Institute of Fisheries andYatsuya K., Kiyomoto S., and Yoshimura T., 2014:

Environment of Inland Sea, 2015: Results of

Seasonal changes in biomass and net production

past 40 years of fisheries monitoring programofin the Seto Inland Sea ‒ long-term variation of

Gounoura, Iki Island, northern Kyushyu, Japan.

oceanographic conditions, 256pp. (in Japanese)
Serisawa Y., Imoto Z., Ishikawa T., and Ohno M., 2004:
Decline of

population associatedOkamura community off., 7, 67-77. (in Japanese with English

Abstract)
Yoshida G., Terawaki T., Yamashita A., Arai S.,

YOSHIDA, Hiromori SHIMABUKURO, Setuo KIYOMOTO, Tatsuru KADOTA, Taku YOSHIMURA, Noboru MURASE, Mikio
34 GoroNODA, Shoichi TAKENAKA, Yoshimi KONO, Toshiharu TAMURA, Norio TANADA, Xiaojie YU, Naoki YOSHIE, and Xinyu GUO
and Tarutani K., 2011: Variation in

G. and Hiraoka M., 2012: Warming off southwesternforest characteristics along the coastal water

Japan linked to distributional shifts of subtidal

temperature gradient from the Seto Inland Sea

canopy-forming seaweeds.

to the Bungo Channel sea area.

2865.

, 195,

337-343. (in Japanese with English abstract)., 2(11), 2854-

Along the coast of Kochi Prefecture, southwestern

Yoshida G., 2018: Climate change impact on macroalgal
bed ecosystem-Threatening environmental shift
approaching to the Seto Inland Sea-.

.

,

236, 203-209. (in Japanese with English abstract)

Japan, macroalgal bed of temperate kelp () has been tremendously decreasing and it hasserious impact on abalone fishery. In addition, theauthors clarified by field surveys that temperate
species which are also important

Annotated bibliography

constitutes of macroalgal beds have been replaced bytropical species,. Behind these events,(1) Yoshida G., Terawaki T., Yamashita A., Arai S.,

the coastal water temperature has been increasing

and Tarutani K., 2011: Variation inforestsince the 1970s at the rate of 0.3 ℃/decade in thecharacteristics along the coastal water temperature

annual mean. In addition to the trend, the authors

gradient from the Seto Inland Sea to the Bungo

considered that those events became prominent in

Channel sea area.

1998 when the largest ENSO occurred and extremely, 195, 337-343. (inJapanese with English abstract)high water temperature observed in the year

Authors surveyed characteristics of fiveaccelerated the change.

forests along the geograohical temperature gradientsfrom the western Seto Inland Sea to the Bungo(3) Tanada N., 2016: Development of a practical

Channel area. Luxuriant forests with many temperate

method for mass seedling production using free-living

species and a kelp () weregametophytes and a new cultivar tolerant to warm

observed at the two stations in the Seto Inland Sea

waters for early harvesting of(Hiroshima Bay and Iyo-nada sea). Analogous flora(Harvey) Suringar.

and luxuriance was also observed in the northern part

Japanese with English abstract)(the Sata-Misaki Pen.) and central part (the coast of

The production of, 225, 464-471. (in,Uwajima-City) of the Bungo-Channel though increasein cultivation in Tokushima, which is one of theof coralline algae and sea urchins which symbolizes

largest producing area in Japan, has been decreasing

ʻmarine desertʼ () was also observed. At theseriously after the 1990s. The decrease is supposed

southern part (the coast of Ainan-cho), sub-tropicalto be due to water temperature increase, especiallyand corals appeared and replaced thetemperateof the shift ofandduring autumn when seedlings ofare started. Relationshipto be cultured in the sea, because the seedlings areforests observed and thesensitive to high temperature conditions at that

notable gradient in coastal water temperature alongstage. Authors developed new techniques in mass

the two sea areas was discussed.

seedling production and its control, and it can enable
to make new cultivars of(2) Tanaka K., Taino S., Haraguchi H., Prendergast

tolerance to high temperatures.

which can have

水 研 機 構 研 報， 第 49 号，35 − 43， 平 成 31 年
Bull. Jap. Fish. Res. Edu. Agen. No. 49，35−43，201935

Coastal management using oyster-seagrass interactions for sustainableaquaculture, fisheries and environment
Masakazu HORI＊1, Franck LAGARDE＊2, Marion RICHARD＊2, Valerie DEROLEZ＊2,
Masami HAMAGUCHI＊1, and Mitsutaku MAKINO＊3

Abstract: Coastal environments of the world have been exposed to eutrophication for several
decades. Recently, the quality of coastal waters has been gradually and successfully improved;
however, this improvement has caused another issue in coastal ecosystem services: oligotrophication.
While oligotrophication, with higher water transparency, has recovered benthic macrophyte
vegetation, which have been depressed by phytoplankton derived from eutrophication, local
stakeholders have suggested that oligotrophication reduces pelagic productivity and, therefore,
fishery production in coastal ecosystems. In contrast, oligotrophication with high transparency has
recovered benthic primary productivity, including seagrass vegetation. Seagrasses are quite
important for climate change mitigation and adaptation, such as through carbon storage, acidification
mitigation, and protection from sea-level rise and storm surges, affects which have been welcomedby other stakeholders. Therefore, harmonizing coastal fishery with environmental conservation
goals is now essential for the sustainable use of ecosystem services. Here, we present the scope of
our study based on an interdisciplinary approach, including ecological actions, socio-economicalactions and psychological actions. We chose to focus on the interaction between oyster aquaculture
and seagrass vegetation as a typical ecological action. Coastal organisms have adapted their traits
to the environment over a long period of time, so restoration of mixed coastal habitats represents
reconstruction of the original process of coastal production. Subtidal seagrass vegetation withintertidal oyster reefs is the original mixed habitats in Japan, which would be expected to enhancecoastal production by improving the production efficiency without adding nutrients. A simple field
experiment with carbon and nitrogen contents and stable isotope analyses revealed that oyster
spats cultivated on a tidal flat adjacent to seagrass beds had higher nitrogen contents and higher
δ13C ratios than spats cultivated in an offshore area using only pelagic production. This result
suggests that utilization of the traditional mixed habitats, which enables oysters to use both pelagicand various benthic production, has potential to sustain food provisioning services for humans evenin an oligotrophic environment.
Key words: Oyster aquaculture,, blue carbon, Indigenous and local knowledge,

Integrated coastal management

Introduction

exposed to eutrophication with red tides for several
decade (Selman and Greenhalgh, 2009; Yanagi,

Coastal environments of the world have been2015). Also, in the Inland Seas of the Japanese

2018年８月31日受理（Accepted on August 31, 2018）
National Research Institute of Fisheries and Environment of Inland Sea, Fisheries Research and Education Agency, 2-17-5 Maruishi,
Hatsukaichi, Hiroshima 739-0452, Japan＊2
Station de Sete, IFREMER, Sete 34203, France＊3
National Research Institute of Fisheries Science, Fisheries Research and Education Agency, 2-12-4 Fukuura, Kanazawa, Yokohama, Kanagawa
236-8648, Japan
E-mail: mhori@affrc.go.jp＊1

36

Masakazu HORI, Franck LAGARDE, Marion RICHARD, Valerie DEROLEZ, Masami HAMAGUCHI,
and Mitsutaku MAKINO

coast, eutrophication in 1970 to1980s had becomeand demonstrations for establishing both sustainable

very serious, and red tide blooms, hypoxia andfishery and water-quality improvement, with aother biological/chemical problems have appeared

special focus on the interaction between oyster

frequently. The eutrophication has promoted the shift

aquaculture and seagrass vegetation as a typicalfrom inshore boat fishing toward oyster and seaweedcase. First, we introduce the scope of our study based

aquaculture due to massive pelagic phytoplankton

on an interdisciplinary approach, including ecologicalabundances and nutrient loads. As a result, oyster

actions, socio-economical actions and psychologicalaquaculture has become an important producer ofactions. Second, we explain the result from our global

seafood in coastal areas (Tsurita

manipulative experiment with nutrient loading into., 2017).

Recently, as public awareness of marine pollution

seagrass beds, suggesting the possibility that nutrient

has become higher, the quality of coastal waters has

reloading would cause the decline of seagrassbeen gradually and successfully improved in some

distribution again. The last is the result from a fieldregions (Matsuda, 2015). In the Seto Inland Sea, legal

experiment to clarify the effect of oyster-seagrass

control of nutrient loading has successfully reduced

interaction on the trophic aspect of cultured oysters,

nutrients and toxic materials input from factories

including how the nitrogen and carbon composition

and rivers to coastal areas. However, some coastalof cultivated oyster spats tissues can reflect the

stakeholders suggest that the improvement, which

difference in potential food resources with andis called oligotrophication, is now causing anotherwithout eelgrass vegetation under oligotrophication.

issue in coastal ecosystem services (Collos., 2009;

Yamamoto and Hanazato, 2015). It is suggested that

Short Materials and Methods

oligotrophication has reduced pelagic productivity
in coastal ecosystems, sometimes resulting in

The Seto Inland Sea (coordinates at its centre:

the decrease of fishery catch because the coastal

34.1667°
N, 133.3333°
E) in Japan and the Thau Lagoon

fishery system in some regions has adapted to the(coordinates at its centre: 43.41°
N, 3.6241°
E) in France

eutrophic environment. In Seto Inland Sea, most ofwere chosen as study sites for this research (Fig.1).

the recent fishery-target species are derived fromThe Seto Inland Sea is located in the southwestern

pelagic production (Hori and Tarutani, 2015), whichpart of the main island of the Japanese archipelago.

is now decreasing year by year. In addition, oyster

Rafted aquaculture using natural spats of the native

aquaculture, especially Pacific oyster culturing, isPacific oystera typical fishery that has been prospering withareas of the Seto Inland Sea. The annual production

eutrophication, but it has been recently exposed toin the Seto Inland Sea accounts for more than 60

serious shortage of natural spats, resulting in the% of the national production of Japan. Along withis flourishing in many

decline of the harvest.
In contrast, oligotrophication with high transparency
has recovered benthic primary productivity, including
seagrass vegetation. Seagrasses are quite importantfor climate change mitigation and adaptation, such as
through carbon storage and protection from sea-level
rise and storm surges (Arkema., 2013; Duarte., 2013). These effects are welcomed by otherstakeholders concerned with environmental issues.
Therefore, harmonizing sustainable coastal fisheries
and aquaculture with environmental conservation
is now essential for the sustainable provision of
ecosystem services. This would not be achieved
simply by additional nutrient reloading.
In this paper, we will introduce some of our ideas

Fig. 1. Study sites, the Seto Inland Sea, Japan (leftfigure) and Thau Lagoon, France (right figure). Thesefigures were revised from Hori
. (2018).

37

Coastal management using oyster-seagrass interactions
oligotrophication, eelgrass recovery in the Seto

actions (HoriInland Sea has become apparent over the last decade

aimed to improve or maintain the ecosystem

due to legal restrictions on nutrient input from thefunctioning and ecosystem services of a target

watersheds. It has been estimated that the area of

ecosystem consists of two processes: investigations

sea grass meadows had increased from 6000 ha toto understand the ecological condition of theabout 10,000 ha by 2011 (Hori and Tarutani, 2015).

ecosystem functioning and the ecosystem services., 2018). First, the ecological actions

The Thau Lagoon is the largest lagoon located onin the target ecosystem and then management forthe southern French coast in the Mediterranean Sea.

the sustainable supply of ecosystem services based

The lagoon is famous for oyster farming using non-on the knowledge acquired by the investigation. The

native Pacific oyster spats cemented on longlines.

socio-economic aspect is important to convey the

The longlines with the spats are hung on oysterchange of an ecosystem state and ecosystem services

tables established in the nearshore zone. About

to the recipient human community. The socio-

10% of the French national production of oysters is

economic actions also consist of investigations andcultivated there; it is the largest oyster farming area

management, which are firstly aimed at clarifying

in the Mediterranean Sea. It has been suggested thatthe commodities and value chains to the humanthe recovery of eelgrass beds is still proceeding, andcommunity from oyster and recreational businesses,

now the area of sea grass distribution extends up toas well as the interface between ecosystem services

800 ha (Hori, personal communication with Syndicat

and socio-economic activities in the target ecosystem,

mixte du bassin de Thau). The expansion of eelgrass

which is regarded as a Social-ecological systemmeadows was observed even within oyster farming

approach (Makino

areas in June 2016.

aim to identify the effect of the changes in ecosystem., 2018). Second, the actions

The Thau lagoon (coordinates at its centre:

functioning and ecosystem services on the structure

43.41°
N, 3.6241°
E) is the largest lagoon located onof these chains and to draft adaptive tactics for thethe southern French coast in the Mediterranean Sea.

changes in the target ecosystem. The fundamental

The lagoon is famous for oyster farming using non-purpose of socio-psychological actions was to identify

native Pacific oyster spats attached on longlines by athe potential stakeholders and their well-being in thespecific cement to the spats. The longlines with therecipient community and to influence their view onspats are hung on oyster tables established in thenatureʼs values. Some of the ecosystem functioningnearshore zone. About 10 % of the French nationaland services cannot be appreciated based purely on

production of oysters is cultivated there: the largest

financial aspects, and therefore, we need to develop aoyster farming area in the Mediterranean Sea. It has

psychological method to directly identify well-being.

been suggested that the recovery of eelgrass beds isstill proceeding, and that now the area of sea grass

Nutrient loading manipulation in seagrass beds as a

distribution extends up to 800 ha (Hori, personalpossible ecological action

communication with Syndicat mixte du bassin de

Nutrient reloading would be a simple action toThau). The expansion of eelgrass meadows was

mitigate the effect of oligotrophication. However,observed even within oyster farming areas in June

there is a possibility that the nutrient reloading

2016.

may cause the decline of seagrass vegetation again
like previous eutrophication in the 1970s.

We

Schematic of an interdisciplinary approach adopted

participated in a global experiment spanning thein this study

northern hemisphere to demonstrate the relationshipAs a first step to establish harmony between

among eelgrass ecosystem functioning, the associatedsustainable oyster aquaculture and seagrass

epifaunal diversity and nutrient loading (Duffy

conservation under oligotrophication in both study., 2015). In the experiment, we established ansites, we devised a management strategy based

experimental site of seagrass bed in western Setoon an interdisciplinary approach, which consists ofInland Sea and then conducted nutrient loading by

ecological, socio-economic and socio psychologicalfertilization and epifaunal diversity manipulation

38

Masakazu HORI, Franck LAGARDE, Marion RICHARD, Valerie DEROLEZ, Masami HAMAGUCHI,
and Mitsutaku MAKINO

during the same period using the same equipment as

in this study

other sites of the world. Although the fundamental

Based on this approach, we are now proceeding

aim of the world experiment was to clarify thewith the research on clarifying the interactions

indirect effect of epifaunal diversity on eelgrass

between oyster farming and eelgrass beds to estimate

growth via epiphyte removal on leaves by meso-

the possibility of the oyster farming using seagrass

grazers in hemisphere scale, the result of fertilization

beds as an ecological action in our managementfrom the Seto Inland Sea can suggest whether the(Fig.2). We have three working hypotheses at thenutrient loading decrease eelgrass vegetation or not.

moment. First, oyster farming using seagrass beds
can maintain or improve coastal productivity even

Oyster spats cultivation in seagrass beds as ain healthy environmental conditions undergoingpossible ecological action

oligotrophication. To our knowledge, there is no caseWe established a field experiment in the Seto

study directly demonstrating the effect of oyster-Inland Sea to clarify trophic contribution of eelgrass

seagrass interactions on ecosystem functioning

beds to the growth of oyster spats as a feasibilityof target ecosystems, although there are somestudy of the oyster-seagrass interactions (Hori.,modelling studies on the material cycling in a coastal

2018). We established an experimental area (5 m × 5

ecosystems, including oyster and seagrass bedsm) in the lower intertidal zone on the tidal flat with

(Kishi and Oshima, 2008). Further studies are needed

seagrass vegetation, set a raft floating on the sea

to demonstrate this hypothesis.

surface 200 m offshore from the tidal flat, and hungThe second hypothesis is that seagrass beds

a replicate of three cages at a depth of 2 m frommaintain or improve conditions for oysters to reduce

the sea surface using vinylon ropes. Thirty spats ofpotential pathogens, enabling more hygienic culture

each of three species (practices, and to mitigate ocean acidification. This) hatched from the same lot wererequires a study of the effect of the change in

put into the cages on the tidal flat, and the otherenvironmental condition by seagrass beds on thehalf of the spats of each species were put into thequality of oysters, which will potentially enhance

cages hanging from the raft. The experiment was

the value of oyster products. In other regions, it

conducted for two months from November 2016 to

was reported that there was a 50% reduction in theJanuary 2017. The fundamental motive of this field

relative abundance of potential bacterial pathogens

experiment was also derived from the social concern

capable of causing disease in humans and marine

in the local community of stakeholders. In both theorganisms when seagrass beds are present (Lamb

Seto Inland Sea and the Thau Lagoon, it has been a., 2017).

concern of local oyster fishermen and oyster farmers

The third hypothesis is that seagrass beds canwhether the increased seagrass meadows have any

support oyster production and improve its quality

positive or negative effects on oyster production

and sustainability. This requires studies on theand sustainability in the near future. We especiallytrophic effect of the change in ecosystem functioning

analysed the carbon and nitrogen concentrationinduced by seagrass beds on oyster production as aand the stable isotope ratios of the oyster spats todominant ecosystem service in our study sites (seedemonstrate the effect of different food resources

the section on the oyster spats experiment below).

on their nutritional condition. Such differences
are derived from the different sources of primary

Nutrient loading manipulation in seagrass beds as a

production in both the pelagic ecosystem (using

possible ecological action

raft culture) and the benthic ecosystem utilized byground culture in the tidal flat.

Duffy. (2015) suggested the global experiment

revealed that higher epifaunal diversity significantly
affected higher eelgrass ecosystem functioning, while

Results and Discussion

any significant effect of experimental fertilization
was not detected on a global scale. However, in

Schematic of an interdisciplinary approach adopted

the individual result from Seto Inland Sea underCoastal management using oyster-seagrass interactions

39

Fig. 2. The hypothetical pathways that the oyster-eelgrass interaction positively affect the recipient community
via the change in ecosystem goods and services. This figure is revised from Hori
. (2018).

oligotrophication, fertilization had a significant
interactive effect on the ecosystem functioning
and epifaunal diversity (Fig.3). The fertilization
significantly decreased the eelgrass growth when
epifaunal diversity was low (Two-way ANOVA: F= 4.627, p = 0.038), suggesting a context dependent
possibility that nutrient reloading decreased
macrophyte vegetation, resulting in a failure
to harmonize sustainable coastal fisheries withenvironmental conservation.
Oyster spats cultivation in seagrass beds as apossible ecological action
The feasibility experiment of oyster spat
cultivation exhibited some results that support thethird hypothesis in our interdisciplinary approach tooyster-seagrass interactions. Among three
species we cultivated, especiallyexhibited

Fig. 3. The result of 2-way factorial experiment withgrazer exclusion and fertilization in the Seto Inland
Sea. The grazer exclusion significantly decreased
epifaunal diversity and indirectly increased
epiphyte biomass on eelgrass leaves, resulting in asignificant difference in eelgrass leaf growth between
fertilization and control plots.

significant differences in the N/C ratio (Fig.4) andsoft tissue part ratio (Fig.5) between the spats on thewhile the oyster spats on the tidal flat can use both

tidal flat and those from the offshore raft after two

pelagic and benthic production (Benthic POM on tidal

months, but there was no significant difference in theflat: - 17.00 ‰, seagrass: - 10.50‰, Hamaoka unpubl.

shell growth. In addition, there was a clear differencedata, 2017). These results suggest that utilization ofin the stable carbon isotope ratio between the spatsbenthic production can facilitate the nitrogen content

on the tidal flat and those from the offshore raft in allof cultivated oysters, which would provide a higher

three species after two months. This was presumably

quality food provision service for human beings.

because the oyster spats from the offshore rafts used

In oligotrophic environmental conditions, our first

only pelagic production (pelagic POM: - 22.00 ‰,ecological action aims to facilitate total productivity

Hamaoka, unpubl. data, 2017, from this study site),based not only on pelagic production by increasing

40

Masakazu HORI, Franck LAGARDE, Marion RICHARD, Valerie DEROLEZ, Masami HAMAGUCHI,
and Mitsutaku MAKINO

the nutrient level, but also various benthic products,

for oysters and nutrients and POM as resources

including seagrass beds. Interactive resourcefor eelgrass and eelgrass-associated organisms.

subsidies between eelgrass and oysters can include

Seagrass-oyster interactions would become a key

supplying epiphytes and detritus as food resources

factor to improve bio-resource cycling and increase

Fig. 4. The results of N/C ratio of (a), (b), and (c)and the result of therelationship between carbon and nitrogen stable isotope composition of (d), (e), and (f)at the beginning (initial) and the end of the experiment (raft and tidal flat). The assumption of variancehomogeneity was kept in each statistical test for the difference in N/C ratio of (c)(P = 0.154) and thecarbon stable isotope composition of (d)(P = 0.551), (e)(P = 0.731), and (f)(P = 0.793).
These figures were revised from Hori
. (2018).

Fig. 5. The difference in the ratio of soft tissue weight (gDW) to total weight (gDW) of each oyster species (leftfigure) and longest part of shell length (right figure) between the spats cultivated on the tidal flat and those fromthe offshore raft. Significant p-values are represented by asterisks: *p < 0.05; **p < 0.01; ***p < 0.001. These figures
were revised from Hori
. (2018).

41

Coastal management using oyster-seagrass interactions
the turnover efficiency of ecosystem functioning in

M., Hovel K., Iken K., Lefcheck J. S., Moksnes

the study area. If the above three hypotheses are

P.-O., Nakaoka M., O'Connor M. I., Olsen J. L.,

successfully verified, the recipient human community

Richardson J. P., Ruesink J. L., Sotka E. E.,in the socio-economical section of our approach canThormar J., Whalen M. A., and Stachowicz J.

get both valuable products and a better environment.

J., 2015: Biodiversity mediates top-down control

The change in the community by the ripple effectin eelgrass ecosystems: a global comparative-of the ecological action would cause the change
in the well-being of the stakeholders of the target
ecosystem.

experimental approach.

, 18, 696-705.

Hori M. and Tarutani K., 2015: Changes in the
distribution of seagrass vegetation with relation

For example, oyster-eelgrass interactions would

to the possible regime shift from pelagic-

keep high water-transparency and better sanitary

dominant to benthic-dominant system in Seto

conditions, which is also beneficial for recreational

Inland Sea, in “Issues of oligotrophication inuse. Larger distribution of eelgrass beds canocean and lakes” (ed. by Yamamoto T. andabsorb more carbon dioxide from the atmosphereHanazato T.), Chijinshokan press, Tokyo, pp. 129-and store it as organic carbon, which can mitigate

148. (in Japanese)ocean acidification and, moreover, offset the carbon

Hori M., Hamaoka H., Hirota M., Lagarde F., Vaz S.,

emissions from oyster aquaculture and recreational

Hamaguchi M., Hori J., and Makino M., 2018:activities. This kind of local offset system of carbon

Application of the coastal ecosystem complex

emission can contribute to the promotion of theconcept toward i ntegrated managem e n t

Paris Agreement adopted at UNFCC-COP21. Ourfor sustainable coastal fisheries understudy has only just been initiated, so we have tooligotrophication.

., 84, 283-292.

make steady progress to identify wise-use and better

Kishi M. J. and Oshima Y., 2008: The role of benthos

management for oligotrophic coastal ecosystems

and epiphyte on the material cycle in Akkeshi

through these ecological, socio-economical and socio-

lake, Japan, in “Monitoring and Modeling Lakes

psychological actions in the future.

and Coastal Environments” (ed. by Mohanty P.
K.), Springer, Netherlands, pp. 151-158.

References

Lamb J. B., van de Water J. A. J. M., Bourne D.
G., Altier C., Hein M. Y., Florenze E. A., Abu

Arkema K. K., Guannel G., Verutes G., Wood S. A.,

N., Jompa J., and Harvell C. D., 2017: Seagrass

Guerry A., Ruckelshaus M., Kareiva P., Lacayo

ecosystems reduce exposure to bacterialM., and Silver J. M., 2013: Coastal habitats shieldpathogens of humans, fishes, and invertebrates.

people and property from sea-level rise andstorms.

, 3, 913-918.

, 355, 731-733.
Makino M., Hori M., Hori J., Nanami A., Tojo Y., andCollos Y., Bec B., Jauzein C., Abadie E., Laugier T.,

Tajima H., 2018: Understanding the integrated

Lautier J., Pastoureaud A., Souchu P., and Vaquer

policy for harmonizing the marine ecosystem

A., 2009: Oligotrophication and emergence ofconservation and sustainable uses: a casepicocyanobacteria and a toxic dinoflagellate inof Sekisei lagoon, Japan. Selected papers inThau Lagoon, southern France.

Oceansʼ18 MTS/IEEE Kobe/Techno-ocean 2018.

., 61,

68-75.

Matsuda O., 2015: Towards rich Seto Inland Sea,

Duarte C. M., Losada I. J., Hendriks I. E., Mazarrasa
I., and Marba N., 2013: The role of coastal plantcommunities for climate change mitigation andadaptation.

, 3, 961-968.

considerable change of the basic plan on Seto
Inland Sea approved by the cabinet.
, 36, 7-12. (in Japanese)
Selman M. and Greenhalgh S., 2009: Eutrophication:

Duffy J. E., Reynolds P. L., Boström C., Coyer J. A.,

policies, actions, and strategies to address

Cusson M., Donadi S., Douglass J. G., Eklöf J.

nutrient pollution, WRI Policy Note 3, World

S., Engelen A. H., Eriksson B. K., Fredriksen

Resources Institute, Washington, D. C., 16pp.

S., Gamfeldt L., Gustafsson C., Hoarau G., Hori

Tsurita I., Hori M., and Makino M., 2017: Fishermen

42

Masakazu HORI, Franck LAGARDE, Marion RICHARD, Valerie DEROLEZ, Masami HAMAGUCHI,
and Mitsutaku MAKINO
and conservation: sharing the case study ofprovisioning service for humans, even in oligotrophic

Hinase, Japan, in “Marine Protected Areas:

conditions.

Interactions with Fishery Livelihoods and Food
Security” (ed. by Westlund L., Charles A., Garcia(2) Pernet, F., Malet N., Pastoureaud A., Vaquer

S. M., and Sanders J.), FAO-FA Technical Paper

A., Quere C., and Dubrica L., 2012: Marine diatoms

603, FAO, Rome, pp. 43-50.

sustain growth of bivalves in a Mediterranean lagoon.

Yamamoto T. and Hanazato T., 2015: Issues ofoligotrophication in ocean and lakes, Chijinshokanpress, Tokyo ,195pp. (in Japanese).

., 68, 20-32.
Carbon stable isotopes and fatty acids were
measured in the suspended particulate organic matterYanagi T., 2015: Eutrophication and oligotrophication(POM) of the Thau lagoon to study its qualitativein Japanese estuaries: the present status andtemporal changes in relation to environmental factors

future tasks, Springer, Dorderecht, 97pp.

and to identify the food sources of bivalves over a
one-yr-cycle in relation to their growth. Reciprocally,

Annotated bibliography

the impact of shellfish farming on POM was alsostudied. Oysters and mussels were sampled and(1) Hori M., Hamaoka H., Hirota M., Lagarde F., Vazmeasured for biometry, stable isotopes and fatty

S., Hamaguchi M., Hori J., and Makino M., 2018:acid composition. Water samples were collected at

Application of the coastal ecosystem complex concept

two sites, both inside and outside of the shellfish

toward integrated management for sustainable

farming area, to determine concentrations in POM,

coastal fisheries under oligotrophication.

chlorophyll a (Chl.,84, 283-292.

) and stable isotopes. Carbon

isotopes and fatty acids in bivalves reflected seasonal

Harmonizing coastal fisheries with water-qualitychanges in food sources, which varied consistently

improvement has become an essential factor forwith the environment. Seasonal changes in δ13C andthe sustainable use of coastal ecosystem services.

fatty acids in the bivalves suggested that dietary

Here, we present the scope of our study based on

phytoplankton contribution varied according toan interdisciplinary approach including ecologicalseason. Terrestrial organic matter and bacteria canactions, socio-economic actions and socio-psychologicalcontribute to the diet of bivalves during non bloom

actions. We chose to focus on the interaction between

periods. Mussels seemed to rely more on diatoms andoyster aquaculture and seagrass vegetation as aless on terrestrial organic matter and bacteria thantypical ecological action using the coastal ecosystemoysters did, particularly when phytoplankton biomass

complex (CEC) concept. Coastal organisms have

was low during the summer. Although one- and two-

adapted their traits to the environment over a

yr-old oysters showed similar δ13C, their fatty acidlong period of time, so that restoration of the CEC

dynamics differed slightly. Periods of high growth

represents reconstruction of the original processrate in bivalves were mainly fuel led by diatoms,of coastal production. Subtidal seagrass vegetation

thus highlighting the importance of seasonal blooms

with intertidal oyster reefs is the original CEC inof micro phytoplankton during the critical period ofJapan, which would be expected to enhance coastal

bivalve growth and gamete production. Althoughproduction by improving the production efficiency

there was no significant effect of shellfish farms on

without adding nutrients. A simple field experimentChlexamining carbon and nitrogen contents and stablethat stable isotopes could be used successfully to

isotope ratios revealed that oyster spats cultivatedinvestigate the effects of bivalve aquaculture.

and POM δ13C, consistent differences indicate

on a tidal flat adjacent to seagrass beds had higher
nitrogen contents and higher δ13C ratios than spats(3) Morimoto N., Umezawa Y., San Diego-McGlone M.

cultivated in an offshore area using only pelagicL., Watanabe A., Slringan F. P., Tanaka Y., Regino

production. This result suggests that utilization of

G. L., and Miyajima T., 2017: Spatial dietary shift

the CEC, which enables oysters to use both pelagic

in bivalves from embayment with river discharge

and benthic production, has potential to sustain a foodand mariculture activities to outer seagrass beds in43

Coastal management using oyster-seagrass interactions
northwestern Philippines.

., 164, 84.

weak benthic-pelagic coupling for bivalves. These

To investigate the spatial variation in bivalve

cycles would need to be taken into account whenfood sources along a pollution gradient and assess

estimating the biogeochemical cycles in eutrophicatedbivalve contribution to biogeochemical cycles incoastal areas.

tropical coastal ecosystems, the δ13C and δ15N valuesof bivalves and their potential food sources were

(4) Duarte C. M., Losada I. J., Hendriks I. E.,

studied in northwestern Philippines. In a semi-

Mazarrasa I., and Marba N., 2013: The role of coastal

enclosed embayment affected by river discharge andplant communities for climate change mitigation andmariculture activities, bivalves depended primarily

adaptation.

, 3, 961-968.

on 13C-depleted suspended particulate organic matter

Marine vegetated habitats (seagrasses, salt-

such as phytoplankton and/or fish feeds. However,marshes, macroalgae and mangroves) occupy 0.2 %toward the relatively oligotrophic seagrass beds,of the ocean surface, but contribute 50 % of carbon

the bivalve food source gradually shifted to moreburial in marine sediments. Their canopies dissipate

13

C-enriched resuspended and/or settled particles.

wave energy and high burial rates raise the seafloor,

Furthermore, in the outer seagrass beds exposed tobuffering the impacts of rising sea level and wave

the open ocean, bivalves mainly relied on similar foodaction that are associated with climate change. The

sources, such as detritus of microalgae, regardlessloss of a third of the global cover of these ecosystemsof the distance from the embayment. These trends

involves a loss of CO2 sinks and the emission of 1

appear to reflect the ready availability of the foodPg CO2 annually. The conservation, restoration andsources. Especially in the outer seagrass beds, ause of vegetated coastal habitats in eco-engineering

semiclosed material cycle within the vicinity of thesolutions for coastal protection provide a promisingsea bottom likely emerged between bivalves andstrategy, delivering significant capacity for climate

algae, but not between the phytoplankton in thechange mitigation and adaption.

overlying water column. This resulted in a relatively

水 研 機 構 研 報， 第 49 号，45 − 51， 平 成 31 年
Bull. Jap. Fish. Res. Edu. Agen. No. 49，45−51，201945

Marine sediment conservation using benthic organisms
Katsutoshi ITO＊1, Mana ITO＊1, Takeshi HANO＊1, Toshimitsu ONDUKA＊1, Kazuhiko MOCHIDA＊1,
Nobuaki SHONO＊2, and Ryuhei NAKAMURA＊2

Abstract: Estuaries and coastal zones used for fish aquaculture are often polluted by organic
contaminants and anthropogenic chemicals. Bioremediation has been recognized as an efficienttechnology to clear environmental pollutants. The authors therefore studied environmental
remediation using benthic organisms and have shown that some annelids are adaptable to polluted
environments. For example,cf.

, a polychaete inhabiting the sediment beneath a fish

farm, displayed high protease activity, whereas, a polychaete inhabiting anestuary, displayed high cellulase activity. Additionally, the oligochaetecf.

was found to survive highly hypoxic and sulfidic sediments contaminated with various pollutants
and was shown to biotransform 1-nitronaphthalene, a toxic and carcinogenic chemical, into
substances that are nontoxic to fish.
In another experiment in which these three benthic species were maintained in polluted
sediments, the polychaetes

and

cf.

markedly increased redox potential (Eh) anddecreased the level of acid volatile sulfides relative to the oligochaetecf.

. Furthermore, theconcentration of polycyclic aromatic hydrocarbons (PAHs) in the sediment with all three species was
significantly lower than the initial level.

cf.

, especially, showed a marked ability to degrade

the PAHs in the sediment. These results indicate that benthic organisms have species-specificremediation properties and ecological functions in organically polluted sediments.
We are also working on the development of a real-time measuring device for determining the Ehin the sediment under fish farms as Eh is a comprehensive parameter to monitor the degree ofcontamination of these sediments.
Key words: annelid, bioremediation, environmental pollutants, Polychaeta,, polycyclicaromatic hydrocarbons

Introduction

This eutrophication causes anoxic conditions and anincrease in sulfides (Pawar. 2002; Tanigawa

Estuaries and coasts are crucial for the life histories, 2007), leading to serious problems, such as algalof many aquatic organisms. The estuarine and coastal

blooms and the elimination of the benthic community

sediments accumulate organic matter from bothand seagrass (Holmer

marine and terrestrial sources (Jorcin, 2000; Hu.,

Polycyclic aromatic hydrocarbons (PAHs), which

2009; Zhang., 2008; Leon., 2010).

., 2009). In the sediments of coastal

are products of the incomplete combustion of fossil

areas where aquaculture is conducted, considerable

fuels, contaminate estuarine and coastal sediments

organic enrichment is caused by the input of large

in areas associated with human activity (WHO,amounts of unconsumed fish food and fish feces.

1998). Therefore, remediation of organically polluted

2018年８月31日受理（Accepted on August 31, 2018）
National Research Institute of Fisheries and Environment of Inland Sea, Fisheries Research and Education Agency, 2-17-5 Maruishi,
Hatsukaichi, Hiroshima 739-0452, Japan＊2
Biofunctional Catalyst Research Team, RIKEN Center for Sustainable Resource Science (CSRS), 2-1 Hirosawa, Wako, Saitama 351-0198, Japan
E-mail: katsuit@affrc.go.jp＊1Katsutoshi ITO, Mana ITO, Takeshi HANO, Toshimitsu ONDUKA, Kazuhiko MOCHIDA,
Nobuaki SHONO, and Ryuhei NAKAMURA

46

sediment is necessary for maintaining ecological

the remediation of polluted sediment using annelids.

balance, biological diversity, and the sustainable
development of aquaculture.

Materials and Methods

One pollutant of interest is 1-nitronaphthalene(1NN), a nitrated polycyclic aromatic hydrocarbon(nitro-PAH) that is formed during the incomplete
combustion of organic compounds (Nielsen, 1984).
Such compounds are formed mainly by the reaction

Animals
The benthic organisms used in this study (Fig.1)
are as follows: the nereidid polychaete, opportunistic

cf.

,of PAHs with nitrogen oxides in polluted air

and oligochaete(Atkinson and Arey, 1994). Nitro-PAH products are

worms, including

more toxic to many organisms than are the parent

and shallow marine waters and are widely distributed

PAHs (Yaffe

off the coasts of Asia and in the southern hemisphere., 2001). Yaffe. (2001), using anenvironmental model, reported that 1NN had thehighest concentration potential among nitro-PAHs in
the Los Angeles Basin in Southern California, USA.

cf.

. Nereidid, are common in intertidal(Wilson and Glasby, 1993; Muir and Hossain, 2014).
is a large-sized species, very common in Japan,
and is often found burrowing in sand under stones

Macrofauna, especially sediment-dwellingin estuaries and on sheltered beaches, sometimes inpolychaete and oligochaete worms, are known

near-anaerobic conditions. This species is used as ato affect sediment characteristics biologically,model species for pollutants and has the potential

chemically, and physically through feeding activity,

to be used for wastewater treatment through its

bioturbation, ventilation, and irrigation, resulting

ability to reduce organic matter (Palmer, 2010).

in mineralization and organic degradation in thesediments (Banta
Giere, 2006; Heilskov., 1999; Volkenborn., 2007;

fish farms in Japan and is a small- to medium-sized., 2006; Quintana., 2011).

species.

The activities of some polychaetes are closely related
to the remediation of contaminated sediments andwater (Licciano. cf.

is frequently observed in the sediment under
species are opportunistic and cantolerate hypoxia and sediment toxicants (Gamenick., 1998; Bach., 2005; OʼBrien and Keough, 2013).

., 2005; Palmer, 2010).

Organic matter in the environment is decomposed
chemically by many enzymes (e.g., proteases,
cellulase phosphatases, and carbohydrases). Someenzymes have been utilized to estimate organic
matter decomposition in water and sediment inestuarine and coastal environments (Hiroki
2003; Arnosti(formerly.

. 2009). The polychaete
sp. I; Blake., 2009) has

been reported to remediate organically contaminatedsediment by enhancing the decomposition rate of
the organic matter of the sediment under fish farms(Tsutsumi and Montani, 1993; Kinoshita., 2008).

Moreover, some benthic organisms, including
and, can degrade oil, acyclichydrocarbons, and the PAHs, such as fluorantheneand pyrene in sediment (Gilbert., 2002; Madsen., 1994; Grossi., 1997; Christensen., 2002),

indicating that they can contribute to the remediationof sediments polluted by PAHs.
In this proceeding, we introduce research results
targeting organic pollutants, chemical pollutants, andFig. 1. Nereidid polychaete
opportunistic polychaete
oligochaete
cf.

(a),
(b), and

cf.
(c).

47

Sediment conservation using benthos
are distributed in the sediments of many

replicate columns were prepared for each treatment.

areas including China, North America, and Western. cf.

The benthic worms were fed a commercial fish diet

Australia (Erséus, 1990; Milligan, 1996).

(N400; Kyowa Hakko, Tokyo, Japan) once every 3 days
(5 % of total biomass per day; approximately 22.5 mg).

Enzyme activities of the benthos
The whole body of each

The columns were closed and kept in an incubator
and

. cf.

at 20 °C for 50 days. For the initial sediment sample,

worm, was homogenized in 10 mM sodium phosphatea column was prepared as described above and kept

buffer (PBS; pH 7.5) using a pestle on ice. The

overnight to allow the mud to settle. After removing

homogenate was centrifuged for 30 min at 10,000 rpm

the overlying water, the oxidation-reduction potential

at 4 °C, and then the supernatant was used for the(ORP), acid volatile sulfides (AVS), loss on ignition

determination of enzyme activities. Protease activity(LOI measured as organic matter), and concentration

was measured using milk casein as a substrateof PAHs in the sediment were measured.

according to the procedure of Kashiwagi (2004).

After 50 days, the overlying water was removed

Cellulase activity was measured at 37 °C for 24 h in 10

from all test microcosms, and the ORP (mV) of themM PBS (pH 7.5) with 0.8 % carboxymethyl cellulose

sediment was measured at 2 cm depth using an

as the substrate. Reducing sugars produced by the

ORP meter (D-55, Horiba, Kyoto, Japan). AVS wasreaction were determined by the dinitrosalicylic

measured using a Hedorotech-S gas detection tube

reagent method (Miller 1959). Glucose was used as(GASTEC, Kanagawa, Japan). Benthic organisms

the standard.

were sorted from a subsample of the wholesediment sample. The living infauna were cleaned in

Chemical pollutants catabolism tests with annelids

seawater and their biomass measured; total column

The residual 1NN in seawater following metabolism

biomass was estimated from this measurement. The

by both of the annelids was examined. Each replicate

concentrations of 16 PAHs were measured in theused 300

whole sediment samples.

. cf.

g), 5

individuals (total weight: 0.1
individuals (average weight: 90 mg/

individual; total weight 0.42 g). 1NN test solutions

Results and Discussion

were made by adding the necessary amount ofstock solution to pre-filtered (GFC filter, Whatman,

Enzyme activities of the benthos

Maidstone, UK) seawater. Animals were exposed to

The protease activity ofcf.

(89.7 µg/

1NN at 170 μg/L for 5 days in the dark at 20 °C inmg) was about 10 times those of

aquaria containing seawater and quartz sand. The(8.0 µg/mg). High cellulase (endo-β-1,4-glucanase)residual 1NN concentration in seawater was analyzed

activity was detected inby GC-MS at 0, 2, and 5 days.

µg/mg), whereas the activity was scarcely detectedincf.

Remediation of polluted sediment using annelids.

cf.

(3.2

. The high protease activity ofenabled it to survive in the sediment

Artificial microcosms, consisting of clear glass

under a fish farm, where it degrades organic matter.

columns (diameter 9.0 cm, height 12.2 cm) filled with

In contrast, the high cellulase activity of the estuary-

150 g of sediment (Sediment was collected fromdwelling

Hatsukaichi Marina of Hiroshima, Japan, an active

organic matter originating from terrestrial areas.

allowed it to degrade

harbor in which many fishing boats travel) and 300
mL seawater filtered through sand and activatedChemical pollutants catabolism tests with annelids

carbon, were prepared. Approximately 150 mg

In the 1NN metabolism tests with annelids, thebiomass of one benthic worm species−P. nuntia

1NN concentration in seawater did not decrease(mean ± standard deviation) (n = 5 ± 0),(nsignificantly from the initial concentration of 170= 59 ± 5), or

. cf.

. cf.

(n = 160 ± 6)−was added to

μg/L without animals present. However, in all animaleach of three microcosms. A fourth column, without

treatments, the concentrations in the seawater

benthic organisms, was prepared as a control. Threedecreased significantly ( . cf.

: 23.3 %;:Katsutoshi ITO, Mana ITO, Takeshi HANO, Toshimitsu ONDUKA, Kazuhiko MOCHIDA,
Nobuaki SHONO, and Ryuhei NAKAMURA

48

32.6 %) after 2 days. After 5 days, the concentrations

sediment. To observe the progress of the remediation,in the seawater were 3.0 ± 0.2 μg/L in the. cf.

we plan to use real-time measuring to trace the Eh.

tank, and 14.3 ± 2.1 μg/L in thetank.

If sediment pollution progresses, we will implement

to biotransform 1NN

countermeasures, such as increasing the number of

The ability of the. cf.

was significantly greater than that of thebenthic organisms or decreasing the feed volume.

(p < 0.01). Furthermore,

can survive inThis allows not only for evaluating the healthy

highly hypoxic and sulfidic sediments contaminatedconditions of benthic systems, but even facilitatingwith various pollutants, and have been shown to

the remediation potential of benthic organisms tobiotransform 1NN, a toxic and carcinogenic chemical,

improve the toluene of sediment ecosystems against

into substances that are nontoxic to fish.

over feeding on fish farms.

. cf.

Remediation of polluted sediment using annelids

Acknowledgments

The annelidʼs effects on physicochemical
properties, such as organic matter (LOI), Eh, AVS,This work was supported by JSPS KAKENHI

and the degradation of PAHs, were assessed. EhGrant Numbers 17K20075, 15K16144, 22710083, andlevels were significantly higher, and AVS levels

26712017.

lower, in the sediments of the polychaetes
and

. cf.

the oligochaetethan they were in those of. cf.

Referencesor the control (without

benthic organisms). Total PAH concentration

Arnosti C., Ziervogel K., Ocampo L., and Ghobrial

significantly decreased from the initial level inS., 2009: Enzyme activities in the water column

all three groups;

and in shallow permeable sediments from the. cf.

displayed a marked

ability to reduce PAHs in sediment. These results
indicate that benthic organisms have species-specificremediation properties and ecological functions inorganically polluted sediments.

northeastern Gulf of Mexico.
., 84, 202-208.
Atkinson R. and Arey J., 1994: Atmospheric chemistryof gas-phase polycyclic aromatic hydrocarbons:formation of atmospheric mutagens.

Real-time device for measuring Eh in sediment., 102, 117-126.

In our group, sediment remediation tests using

Bach L., Palmqvist A., Rasmussen L. J., and Forbes V.

benthos were carried out in the field, such as atE., 2005: Differences in PAH tolerance between

fish farms. Periodic surveys conducted by sediment
sampling and diving were necessary to verify the

species: Underlying biochemicalmechanisms.

., 74, 307-319.

effects of the annelids. The Eh is a comprehensive

Banta G. T., Holmer M., Jensen M. H., and Kristensen

parameter, which can be used to monitor the degreeE., 1999: Effects of two polychaete worms,of contamination of the sediment under a fish farm.
Currently, we are working on the development of areal-time device for measuring Eh in the sediment
under fish farms.

and, on aerobic

and anaerobic decomposition in a sandy marine
sediment.

., 19, 189-204.

Blake J. A., Grassle J. P., and Eckelbarger K. J., 2009:

In fact, we are operating a real-time measurement, a new species designation forin a 3-ton water tan and confirmed that the processes

the opportunistic and experimental

by which the organic matter in the sediments wasI, with a review of the literature for confirmed

being removed by remediation with annelids wererecords.

sp.

, 2, 25-53.

successfully monitored, demonstrating that it is

Christensen M., Andersen O., and Banta G. T., 2002:

possible to measure redox potential in real time even

Metabolism of pyrene by the polychaetes N

in the field. In future, in the case of a fish farm whereandorganic pollution has advanced, we plan to use an., 58, 15-25.

appropriate benthic species to restore the bottom

Erséus C., 1990: The marine Tubificidae (Oligochaeta)

49

Sediment conservation using benthosof the barrier reef ecosystems at Carrie Bowof the sediment in the estuarine region of Canan´

Cay, Belize, and other parts of the Caribbean Sea,eia (SP), Brazil.

with descriptions of twenty-seven new species
and revision of, 431, 59-67.

Kashiwagi Y., 2004: Enzymes of filamentous fungiin fermentation. MAFF Microorganism Genetic

and., 19, 243-303.

Resources Manual No. 16, 1-16.

Gamenick I., Vismann B., Grieshaber M. K., andKinoshita K., Tamaki S., Yoshioka M., Srithonguthai

Giere O., 1998: Ecophysiological differentiation

S., Kunihiro T., Hama D., Ohwada K., andofTsutsumi H., 2008: Bioremediation of organically(Polychaeta). Sibling species

from different sulfidic habitats.

enriched sediment deposited below fish farms., 175, 155-166.

with artificially mass-cultured colonies of a

Giere O., 2006: Ecology and biology of marine
Oligochaeta - An inventory rather than anotherreview.

, 564, 103-116.

deposit-feeding polychaete

sp. I.

, 74, 77-87.
Leon S. D., Mae S., Diego-McGlone S., Lourdes M., andGilbert F., Rivet L., and Bertrand J. C., 1994: The

Reichardt W., 2010: Impact of polychaete infaunain vitro influence of the burrowing polychaeteon enzymatic protein degradation in marine

on the fate of petroleum

sediments affected by intensive milkfish farming.

hydrocarbons in marine sediments.

,

29, 1-12.

., 41, 11.
Licciano M., Stabili L., and Giangrande A., 2005:

Grossi V., Massias D., Stora G., and Bertrand J. C.,

Clearance rates of

2002: Burial, exportation and degradation of(Annelida: Polychaeta)

acyclic petroleum hydrocarbons following a

on a pure culture ofsimulated oil spill in bioturbated Mediterranean, 39, 4375-4384.

coastal sediments.

, 48, 947-954.

Heilskov A. C., Alperin M., and Holmer M., 2006:

and.

Madsen S. D., Forbes T. L., and Forbes V. E., 1997:
Particle mixing by the polychaete

Benthic fauna bio-irrigation effects on nutrient

species 1: Coupling fate and effect of a particle-

regeneration in fish farm sediments.

bound organic contaminant (fluoranthene) in, 339, 204-225.

a marine sediment.

Hiroki M., Yabe T., Nohara S., Utagawa H., Satake
K., Koga T., Ueno R., Kawachi M., and WatanabeM., 2003: Evaluation of an organic matterdecomposing function from hydrolytic enzyme
activities of tidal flat sediments in Japan.

., 147,129-142.
Miller G. L. 1959. Use of dinitrosalicylic acid reagent
for determination of reducing sugar.
31, 426-428.
Milligan M., 1996: Identification manual for the., 64, 113-120. (in Japanese with English
abstract).

aquatic Oligochaeta of Florida. Vol. II. Estuarine
and nearshore marine oligochaetes. Florida

Holmer, M., Argyrou M., Dalsgaard T., DanovaroR., Diaz-Almela E., Duarte C. M., Frederiksen

Department of environmental Protection,
Tallahassee, Florida, 239pp.

M., Grau A., Karakassis I., Marbà N., Mirto S.,

Muir A. I. and Hossain M. M. M., 2014: The intertidal

Pérez M., Pusceddu A., and Tsapakis M., 2008:

polychaete (Annelida) fauna of the Sitakunda

Effects of fish farm waste on Posidonia oceanica

coast (Chittagong, Bangladesh), with notes on

meadows: Synthesis and provision of monitoring

the Capitellidae, Glyceridae, Lumbrineridae,

and management tools.

Nephtyidae, Nereididae and Phyllodocidae of the., 56,

1618-1629.

“Northern Bay of Bengal Ecoregion”.

Hu L., Guo Z., Feng J., Yang Z., and Fang M., 2009:,27, 1-27.

Distributions and sources of bulk organic matter

Nielsen T., 1984: Reactivity of polycyclic aromaticand aliphatic hydrocarbons in surface sediments

hydrocarbons towards nitrating species.

of the Bohai Sea.

.

.

., 113, 197-211.

Jorcin A., 2000: Physical and chemical characteristics., 18, 157-163.
OʼBrien A. L. and Keough M. J., 2013: Detecting

Katsutoshi ITO, Mana ITO, Takeshi HANO, Toshimitsu ONDUKA, Kazuhiko MOCHIDA,
Nobuaki SHONO, and Ryuhei NAKAMURA

50

benthic community responses to pollution in

Annotated bibliography

estuaries: A field mesocosm approach.
., 175, 45-55.

(1) Ito K., Nozaki M., Ohta T., Miura C., Tozawa Y.,

Palmer P. J., 2010: Polychaete-assisted sand filters.
, 306, 369-377.

and Miura T., 2011: Differences of two polychaete
species reflected in enzyme activities.

Pawar V., Matsuda O., and Fujisaki N., 2002:

158(6), 1211-1221.

Relationship between feed input and sedimentquality of the fish cage farms.

, 68, 894-

903.

.,

Polychaetes constitute most of the benthic
macroinvertebrates in estuarine and coastal
environments. We investigated the utilization of

Quintana C. O., Hansen T., Delefosse M., Banta G.,

organic matter in two polychaete species,

and Kristensen E., 2011: Burrow ventilation

sp I andand associated porewater irrigation by thedifferent coastal habitats. The protease activity ofpolychaete, living in

sp I (89.7 µg/mg) was about 10 times that., 397, 179-187.

of

Tanigawa T., Tamashita A., and Koizumi Y., 2007:(8.0 µg/mg). High cellulase(endo-β-1,4-glucanase) activity was detected in

Effect of effluents from a new fish farming siteon the benthic environment.

(3.2 µg/mg), whereas scarcely any
was detected in., 19, 69-77.

sp. I. We isolated cDNA

clones of protease mRNA fromsp. I and

Tsutsumi H. and Montani S., 1993: Utilization ofof cellulase mRNA from. The

biological activities of capitellid polychaete forhigh protease activity of

sp. I enabled ittreatment of “hedoro” (organically enrichedto survive in the sediment under a fish farm, wheresediment) deposited on the marine bottom below

it degrades organic matter. In contrast, the highfish net pen culture.

cellulase activity of the estuary-dwelling

59, 1343-1347.

allowed it to degrade organic matter

Volkenborn N., Hedtkamp S. I. C., van Beusekom J. E.

originating from terrestrial areas.

E., and Reise K., 2007: Effects of bioturbation andbioirrigation by lugworms ()(2) Ito K., Ito M., Onduka T., Ohta K., Torii T., Hano

on physical and chemical sediment properties

T., Mochida K., Ohkubo N., Miura T., and Fujii K.,

and implications for intertidal habitat succession.

2016: Differences in the ability of two marine annelid., 74, 331-343.

species,WHO, 1998: Selected non-heterocyclic polycyclicaromatic hydrocarbons. Environmental Healthsp. and,to detoxify 1-nitronaphthalene.

, 151,

339-344.

Criteria 202. World Health Organization, Geneva.

Bioremediation is a promising method for

Wilson R. S. and Glasby C. J., 1993: A revision of theremediating environmentally polluted water. We

species group (Polychaeta:

investigated the abilities of two benthic annelid

Nereididae).

, 45, 253-277.

Yaffe D., Cohen Y., Arey J., and Grosovsky A. J., 2001:

species to biotransform 1-nitronaphthalene, anitrated polycyclic aromatic hydrocarbon. We used

Multimedia analysis of PAHs and nitro-PAH

an oligochaete,

daughter products in the Los Angeles Basin.

collected from the sediment beneath a fish farm and a., 21, 275-294.

polychaete,sp. (Naididae),, which was obtained from

Zhang L., Yin K., Wang L., Chen F., Zhang D., anda commercial source. Populations of both organisms

Yang Y., 2009: The sources and accumulation

were exposed to 1400 μg/L of 1-nitronaphthalene

rate of sedimentary organic matter in thein seawater for 3 days in the dark at 20 °C. ThePearl River Estuary and adjacent coastal area,

concentration of the pollutant decreased to 12 μg/L

Southern China.

in the seawater containing the

190-196.

., 85,

sp. and to 560 μg/L in the seawater containing. The 1-nitronaphthalene concentration in the

51

Sediment conservation using benthos
bodies of the animals increased from 12 to 94 μg/kg

This study aimed to evaluate the possible

insp. and from 0.90 μg/kg to 38,000

remedial effects of three marine benthic annelids

μg/kg in

After 3 days, 99 % and 40 % ofon organically polluted sediments from the waters

the 1-nitronaphthalene had been biotransformed inof Hatsukaichi Marina, Hiroshima, Japan. Twothepolychaetes,

sp. andexperimentalgroups, respectively. We then tested the acute

and

cf.

, and an oligochaete,sp.,

toxicity of residual 1-nitronaphthalene from the same

were incubated in sediments for 50 days. Theirwater using mummichog (fish) larvae. After theeffects on physicochemical properties, such aslarvae had been exposed for 96 h, the percentage

organic matter (loss on ignition), redox potentialof apparently unaffected larvae remaining was 83.3

(Eh), acid volatile sulfides (AVS), and degradation% in

sp. group but only 16.7 % inof polycyclic aromatic hydrocarbons (PAHs), werethegroup. Clearly, of the two species westudied,sp. had a superior ability

assessed. The polychaetes

and

cf.

significantly increased Eh level and decreased AVS

to convert 1-nitronaphthalene into substances thatlevel compared with the oligochaete

were nontoxic to mummichog larvae. Therefore, we

sp. and control (without benthic organisms). Total

recommend the use of this species for bioremediation

PAH concentration significantly decreased from theof chemically polluted sediments.

initial level in all three groups;

sp.

had a marked ability to reduce PAHs in sediment.
(3) Ito M., Ito K., Ohta K., Hano T., Onduka T., Mochida

These results indicate that benthic organisms haveK., and Fujii K., 2016: Evaluation of bioremediation

species-specific remediation properties and ecologicalpotential of three benthic annelids in organicallyfunctions in organically polluted sediments.

polluted marine sediment.

, 163, 392-399.

水 研 機 構 研 報， 第 49 号，53 − 64， 平 成 31 年
Bull. Jap. Fish. Res. Edu. Agen. No. 49，53−64，201953

Monitoring coastal acidification along the U.S. East coast: concerns forshellfish production
Matthew POACH＊1, Daphne MUNROE＊2, James VASSLIDES＊3, Ian ABRAHAMSEN＊4,
and Nicole COFFEY＊5

Abstract: In coastal systems endangered by acidified water, it becomes paramount to understandthe link between acidification and its environmental drivers. Embayments along the US Mid-Atlantic
coast are particularly vulnerable to local amplification of ocean acidification due to eutrophic
conditions, low alkalinity freshwater input, and episodic upwelling of acidified water. To better
understand these drivers, two research studies were conducted along the coast of New Jersey, U. S.
A. The first study was conducted during the summer of 2014 at the Aquaculture Innovation Center(AIC) of Rutgers University located in Cape May, NJ. The AIC is an important research hatcherythat currently supports the local oyster aquaculture industry through the production of disease
resistant and triploid seed oysters. The second study, which began in the summer of 2017, focusedon elucidating the range of pH and aragonite saturation (ΩAr) conditions experienced in Little Egg
Harbor Bay, NJ, an important shellfish farming and fishing location. At the AIC, temperature,salinity, dissolved oxygen (DO), turbidity and pH were continuously monitored at the intake pipe
located in the Cape May Canal. The pH at the intake showed diurnal variations that tended tomirror the DO signal. The largest drop in pH was measured in July of 2014. This pH drop was
decoupled from the DO signal. The occurrence of consistent Southwesterly winds and cooler surface
water temperatures along the coast before the pH decrease indicated that upwelling was occurring.
A strong shift in the winds likely pushed upwelled water inshore to the intake. The lowest pH
reading coincided with a decrease in salinity due to higher river discharge and strong winds. These
results show that hatcheries along the NJ coast need to be aware that upwelling and freshwater
input may bring reduced pH conditions that can negatively impact shellfish production, andhighlights the need for continued monitoring. Starting in May of 2017, temperature, salinity, DO,turbidity, pH and carbon dioxide partial pressure (pCO2) were continuously monitored at a stationin Little Egg Harbor off Beach Haven. Sensor temperature, salinity, pH and pCO2 data were used to
calculate ΩAr. Results indicated that DO and pH conditions are likely not detrimental to local shellfish
production. There was no indication that upwelling occurred during the monitoring period so noconclusions could be reached about the potential for summertime upwelling to impact shellfish
production in Little Egg Harbor.
Key words: coastal acidification, upwelling, shellfish aquaculture, hatchery2018年８月31日受理（Accepted on August 31, 2018）
NOAA/NMFS, James J Howard Marine Sciences Laboratory, Highlands, NJ 07732, U. S. A.
＊2Rutgers University, Haskin Shellfish Research Laboratory, Port Norris, NJ 08349, U. S. A
＊3
Barnegat Bay Partnership, Ocean County College, Toms River, NJ 08753, U. S. A.
＊4
University of Pittsburgh, Pittsburgh, PA 15260, U. S. A.
＊5
University of Delaware, Newark, DE 19716, U. S. A.
E-mail: matthew.poach@noaa.gov＊1

54

Matthew POACH, Daphne MUNROE, James VASSLIDES, Ian ABRAHAMSEN, and Nicole COFFEY
Introduction

populations. For example, coastal acidification has
caused hatchery larval production problems costing

Human carbon dioxide (CO2) emissions have raised

the oyster farming industry in the U.S. Pacificatmospheric CO2 levels from 180 ppmv in the 19th

Northwest over $100 million and threatening 1000ʼs

century to over 400 ppmv today (IPCC, 2014; Tansof jobs (Washington State, 2012).

and Keeling, 2018). Of that CO2 increase, ~ 1/3 hasbeen absorbed by the oceans (Sabine., 2004)

Global aquaculture production is expanding and
now accounts for half of world food fish and shellfish

and has impacted the oceanʼs carbonate chemistry

production (Naylor

in a process known as ocean acidification (OA). The

is particular a widely practiced way of producing

increase in surface water pCO2 leads to a decrease

food in coastal areas that helps meet the needs ofin pH and carbonate ion concentrations (Caldeiraa rapidly growing global human population (Foley., 2009). Shellfish aquacultureand Berner, 1999; Caldeira and Wickett, 2003). A., 2011; FAO, 2016). Most commercially andreduction in the carbonate ion concentration also

recreationally important fish and shellfish species

reduces carbonate ion saturation state (Ω), which candepend on estuarine ecosystem services at someresult in an undersaturated condition for carbonate

point in their life cycle. An assessment of theminerals. These changes in carbonate chemistry arevulnerability and adaptation of U.S. shellfisheries toparticularly detrimental to the early developmental

ocean acidification (OA) found that the most sociallystages of shellfish as the larvae tend to precipitate

vulnerable communities are spread along the U.S.

the more-soluble aragonite-form of calcium carbonate

East Coast and Gulf of Mexico (Ekstrom(Barton., 2012; Waldbusser., 2015).

., 2015). Aragonite

Their analysis also found that a number of socially

undersaturation has been shown in laboratory

vulnerable communities lie adjacent to water bodies

experiments to reduce survival and growth ofthat are exposed to a high rate of OA or at least one

shellfish larvae (Barton

local amplifier, indicating that these places could be., 2012; Gazeau.,

2013; Gobler., 2014; Talmage and Gobler, 2010;

Waldbusser., 2013; Waldbusser and Salisbury,2014).

at high overall vulnerability to OA.
Shellfish production was once vitally important to
the economy of the state of New Jersey (Ford, 1997).

While OA monitoring has historically been

From 1870 to 1930, the Barnegat Bay-Cape May area

focused on offshore regions, commercially important

produced about 20 % of all market oysters harvested

bivalve aquaculture and fisheries are located in thein the state. This production had declined significantly

coastal zone where the CO2-system is impacted byby the 1950ʼs due to overfishing, salinity changes, andthe additive effects of natural and anthropogenic

disease. The quahog fishery also saw a decline after

processes at both global and local scales (Feely

the 1950ʼs mainly due to pollution which caused bed., 2010; Cai, 2011; Bauer
2013; Breitburg., 2013; Duarte.,

closures. The decline of shellfish populations along., 2015). In productive estuarine

the New Jersey coast over the last century has

environments, the system is further driven toward

prompted significant efforts at their restoration. As aincreasing acidity from local generation of CO2 due toresult of coastal acidification processes, the shellfish

microbial decomposition of labile organic carbon andindustry in New Jersey is likely already experiencing

by injection of waters undersaturated with respect

acidification conditions stronger than the open ocean.

to carbonate via upwelling or storm events. With

Since modern shellfish aquaculture production relies

high rates of photosynthesis and respiration in theseentirely on reliable and consistent larval production insystems, they can be expected to experience greater

hatcheries, understanding coastal ocean acidification

fluctuations in pH and Ω compared to the open ocean.

(coastal OA) in the Northeast U.S. is a matter critical

Importantly, increased respiratory CO2-production

to the stability and sustainability of this industry. In

and upwelling events that lower Ω and adversely

coastal systems endangered by acidified water, it

impact estuarine chemistry may co-occur with the

becomes paramount to understand the link between

timing of the economically driven production ofacidification and its environmental drivers.

larval shellfish at hatcheries or spawning in wild

In order to understand the carbonate chemistry

55

Monitoring coastal acidification along the U.S. East coast
experienced by coastal estuaries and their shellfish

stored by a Campbell® Instruments CR-6 datalogger.

resources, two different monitoring studies were

Data sets were retrieved hourly through cellular

conducted, one at Rutgers Universityʼs Aquaculture

telemetry to a desktop computer. Downloaded dataInnovation Center (AIC) located in Cape May and thewere subjected to quality control analysis, which

other at a marina in the southernmost segment of theconsisted of the identification and removal of missing

Barnegat Bay - Little Egg Harbor Estuary complex,

or erroneous data due to sensor malfunction as

NJ, U.S.A. (Fig.1). The AIC is an important researchwell as identification and removal of outliers. The

hatchery that currently supports the New Jersey

sampling line for the pCO2 and SeaFET™ sensors

oyster aquaculture industry through the production

fouled often compromising the data and leading toof disease resistant and triploid seed oysters. The

their removal in mid-August. Data recorded during

Barnegat Bay - Little Egg Harbor estuary is currently

an 11 day period in June and a 12 day period in Julyundergoing eutrophication (Fertig

displayed a reasonable range of values for pCO2.

., 2014), which

may impact shellfish restoration in this estuary.

During those periods the pCO2 explained 89 % ofvariation in pH indicating that the data was likely

Materials and Methods

valid as the YSI pH and the pCO 2 sensors wereindependent of each other. In July the SeaFET™

: At the AIC, the carbonate chemistry of

pH was similar to YSI pH. As the SeaFET™ sensor

intake water was monitored during the summer ofshared the same sample intake as the pCO2 sensor

2014. From June 15 through July 20, temperature,

the similarity between the two independent pH

salinity, dissolved oxygen (DO), and pH werereadings provide additional support for the quality ofmeasured every 15 minutes at the AICʼs intake

the YSI pH data and pCO2 data (Fig.2). The valid YSIpipe located in the Cape May Canal. Parameters

pH and pCO2 data along with their corresponding

were monitored using a YSI EXO™2 water quality

depth, salinity, and temperature data were used tosonde that was installed 1 meter off the bottom next

calculate the aragonite saturation state (ΩAr) by theto the intake. Probes were calibrated according to

CO2SYS̲xls program (Pierrot. 2006).

manufacturer recommendations prior to deployment.
Probe calibration was also performed at the end of
the deployment. After sensor retrieval, data were
downloaded and subjected to quality control analysis.
Quality control consisted of the identification andremoval of missing or erroneous data due to sensor
malfunction as well as identification and removalof outliers. Correlations between pH and othermeasured parameters were examined throughregression analysis.
: During the Spring of
2017, the Little Egg Harbor estuary monitoring station
was installed at a bay side pier located at MorrisonʼsMarina in Beach Haven, NJ. The installation consistedof a YSI EXO™2 water quality sonde to measuretemperature, salinity, DO, and pH and a Pro-Oceanus
CO 2Pro-CV™ sensor to measure pCO2. In July, aSeaFET™ pH sensor was attached to the pCO 2
sensor. Sensors were installed ~ 1 meter off the bay
bottom. YSI sensor readings were collected every 15
minutes while the pCO2 and SeaFET™ pH sensors
took a reading every 30 minutes. Sensor data wasFig. 1. Map showing the coast of New Jersey withthe two monitoring sites indicated.

56

Matthew POACH, Daphne MUNROE, James VASSLIDES, Ian ABRAHAMSEN, and Nicole COFFEY
and DO exhibited similar patterns, DO accounted for
only 35 % of the variation in pH. The relationshipbetween pH and DO noticeably diverged during
July 3rd through the 5th (Fig.3). During this period
the decreases in pH were not associated with similar
decreases in DO. The lowest pH values of the study
were measured during this period with the lowest
value of 7.45 measured on the morning of July 5th.
Low correlation between pH and DO can result
from factors in the coastal environment that canaffect pH without a change in DO such as the inputof low pH water from either coastal upwelling or

Fig. 2. Regression relationship between pCO2 andYSI pH measured in the LEH estuary during June
and July.

freshwater inflow. Upwelled water tends to have a
pH lower than the average surface ocean pH due tohigher net respiration rates in bottom water. Once
this water reaches the surface it will equilibraterather quickly with atmospheric O 2, while pCO 2
remains relatively unchanged due the slow rate of
CO2 degassing. Likewise, most rivers in New Jersey
have low alkalinity which would lead to a different
relationship between pH and O2 in river water thanin ocean water.
An examination of other environmental data
indicated that the drop in pH observed from July 3rd
through the 5th likely resulted from a combination ofboth coastal upwelling and freshwater input. From
July 1st through the 3rd there were strong south /southwest winds (Fig.4), which are necessary to drive

Fig. 3. The pH as measured on the NBS scale anddissolved oxygen in mg/L recorded during the study
period by a YSI water quality sonde installed one
meter off the bottom and next to the intake pipe for
the Aquaculture Innovation Center.

upwelling along the New Jersey coast. The premisethat upwelling was occurring during this period was
supported by colder sea surface temperatures along
the coast on July 2nd (Fig.5a). Cold water along thecoast on July 5th (Fig.5b), indicated that upwelling
was still occurring even though the winds were
blowing strongly out of the northeast on July 4 ththen out of the northwest on July 5th. This change

Results and Discussion

in wind direction along with its strength is likely thereason why low pH water made it to the AICʼs intake.

thst: From June 15 to July 20 of 2014, pH ranged

Similar pH drops were not recorded at other dates

from 7.45 to 7.99 while DO ranged from 4.95 to 8.60

when there were strong upwelling favorable winds.

mg/L (Fig.3). The coarse scale trend for pH tended

Strong southerly winds occurred between July 13th

to mimic that for DO. Both tended to show a generaland 15th; yet during or immediately after this period,

diurnal trend of increasing values during the day

pH did not drop below 7.6. The difference between

and decreasing values at night. These trends were

this period of southerly winds and the previous was

expected because during the day net photosynthesis

the lack of strong northerly winds immediately after

will increase both DO and pH, while net respiration

July 15th. The distinction between these two events

during the night will decrease both. Even though pH

strongly suggests that an abrupt shift to strong

Monitoring coastal acidification along the U.S. East coast

57

a)Fig. 4. Wind stick vector plot for winds during thestudy period as measured by the weather station
located at the Cape May - Lewes ferry terminal
which is adjacent to the Aquaculture Innovation
Center. Arrows point in the compass direction
toward which the wind is blowing (a northward
pointing arrow indicates a south wind). Arrow heads
mark the magnitude of the winds.

b)

northerly winds following sustained southerly winds
helps to push upwelled water inshore along the New
Jersey coast.
While upwelling and strong northerly winds would
explain the decrease in pH on July 4th; the lowest pHof 7.45 on July 5th coincided with the lowest salinity
reading during the study period. Salinity dropped toa low of 21.3 ppt after an early morning high of 29.3
ppt (data not shown). This salinity decrease coincidedwith a high river discharge and outgoing tide. This

Fig. 5. Satellite AVHRR‐derived images of sea
surface temperature from NOAA-18 satellite for a)
July 2nd at 10:07 Z and b) July 5th at 09:33 Z. (Images
from Rutgers Coastal Ocean Observation Laboratory
at https://marine.rutgers.edu/cool/sat̲data/)

indicates that river water likely contributed to thelowest pH reading. Along with freshwater input,
upwelling and strong northerly winds were also likely

werenʼt exhibited until after more than three days

contributors as there was a higher river discharge onof constant exposure. The reduced pH event at theJune 15 , yet on that date salinity and pH did not

AIC lasted two days and was not constantly helddrop lower than 25.9 and 7.69, respectively.

low as intermittent increases occurred due to tidalth

These results indicate that both upwelling andchanges. Fluctuating pH has been shown to lessen

freshwater input can reduce the pH of source water

the negative effects of constantly low pH on survival

for the AIC. To assess the potential for those driversof(Clark and Gobler, 2016; Keppel

to affect shellfish production it is necessary to., 2016). When only considering the pH data, theconsider the magnitude, duration, and timing of pH

previous research suggests that the short duration

decreases. During this study the pH decreased toof the reduced pH event along with the fluctuationlevels that have been shown to decrease survival andin pH levels would not be stressful enough to impact

to delay metamorphism ofoyster product in the facility (Shaw(Gobler., 2013). But

and Talmage, 2014; Talmage and Gobler, 2009). It

the decrease in pH wasnʼt the only change thatshould be noted, however, that these negative effects

would have been stressful for oyster production. The

58

Matthew POACH, Daphne MUNROE, James VASSLIDES, Ian ABRAHAMSEN, and Nicole COFFEY

decrease in pH on July 5th was also accompanied bya)an additional stress of a sudden decrease in salinity.
While no studies have looked at the effects of shortterm salinity decreases on larvae of;in studies of gastropod larvae, short term salinity
decreases resulted in increased mortality (Diederich., 2011; Montory., 2014; Montory., 2016).

Decreased salinity has also been shown to exacerbate
the negative effects of lower pH on
juveniles (Dickinson., 2012; Waldbusser.,

2011). Even if the reduction in salinity was temporary;
this additional stress may shorten the exposure timenecessary for reduced pH to affect oyster larvae.

b)

As for event timing, the AIC conducts the majorityof its oyster spawning during the late winter-spring
period. High river discharges accompanied by strong
northerly winds are more likely to occur duringthat time period (Hughes, 2011; Joesoef, 2015); while
upwelling is limited to the summer season. Thismeans that freshwater input has a higher potential
to impact AIC operations than upwelling. While
upwelling will likely not affect spring hatcheryoperations, it occurs during the most sensitive timeof year for natural coastal populations of shellfish. In
coastal New Jersey, oysters and clams spawn during
the summer. Summer is also when eutrophic systems
can develop hypoxic conditions with associatedacidification. These conditions can be exacerbated by

Fig. 6. Trends in pH (blue) and dissolved oxygen(red) measured at the intake to the AIC hatchery by
a YSI EXO™2 water quality sonde during a) Juneand b) July of 2017.

upwelling as it not only transports acidified water but
also nutrients that further drive eutrophication.
: For June and July of 2017, YSI pH ranged
from 7.71 to 8.15 while DO ranged from 4.4 to 9.57

during both days that helped to build up water levelsin the estuary.

mg/L (Fig.6). As with the AIC data, the coarse scale

These results are evidence of the dynamic

trend for pH mimicked that for DO, with increasing

environment to which estuarine organism mustvalues during the day and decreasing values at

adapt. It is this dynamic nature that makes it difficultnight. Conversely, pH trends in June and Julyto predict the effects of acidification on bivalves

mirror the trends in pCO2, which ranged from tocommon in Northeastern U.S. estuaries. While

438 to 1122 µatm (Fig.7). The fluctuations in pH andconstant exposure to pCO2 and pH levels similar to

pCO2 produced levels that ranged from present-day

the lowest recorded here have been shown to affectaverages for the open ocean to averages predicted

the survival, metamorphosis, growth, and physiology

stfor the open ocean at the end of the 21 century due
to ocean acidification (Bopp

of

, and
larvae (Gobler and Talmage,., 2013). The paired

values for YSI pH and pCO2 produced values for2014; Miller., 2009; Talmage and Gobler, 2009);

ΩAr ranging from 0.75 to 1.87 (Fig.8). Most ΩAr values

effects were not seen when exposure periods were

were between 1 and 1.5. The ΩAr dropped below 1

shorter (Boulais

for an extended period on June 6th and then again on

Such shorter exposure periods may occur underJune 7th. This likely resulted from a strong east windfluctuating pH conditions leading to the mitigation of., 2017; Talmage and Gobler, 2009).

59

Monitoring coastal acidification along the U.S. East coast
a)

a)

b)

b)

Fig. 7. Trends in pH measured by a YSI EXO™2
sonde (blue) and a SeaFET™ (green) and pCO 2
measured by a CO2Pro-CV™ sensor in LEH estuary
during a) June and b) July of 2017.

Fig. 8. Trends in aragonite saturation state, omega
aragonite, measured 1 meter off the bottom in LEH
estuary during a) June and b) July of 2017.

low pH impacts on bivalves (Frieder., 2014). Veryestuaries can experience extended periods of

few studies of acidification effects on local bivalve

hypoxic and anoxic conditions in summer that also

species have included a fluctuating pH treatment. In

lead to depressed pH (Gobler and Baumann, 2016).

studies that have included fluctuating treatments, pH

Hypoxic conditions and its associated acidification

was decrease to levels below the lowest pH levels

have negative effects on marine organisms that arerecorded here (Clark and Gobler, 2016; Gobler

both additive and synergistic (Wallace., 2017; Keppel., 2014).

., 2016). The levels of pH and

Even though LEH is considered mildly eutrophic, DO

pCO2 recorded here likely did not lead to negative

levels did not drop below 4 mg/L (Fig.6). The DO

impacts because ΩAr rarely dropped below 1. Still,values recorded here appear to be representativeeven fluctuating pH conditions can produce negativeof summertime values for the Barnegat Bay ‒ LEH

impacts in bivalves when compared to static levels

system (Glibertthat are similar to the average of the fluctuations. In

system is shallow and well mixed which deters theorder to understand the impacts of fluctuations in pH

occurrence of extremely low DO levels (Glibert

reported for LEH, more studies need to be conductedthat incorporate similar pH ranges.
The LEH is considered to be undergoing
eutrophication (Fertig., 2014). Eutrophic., 2010; NJDEP, 2014). This., 2010). The levels of both DO and pH measured
during the monitoring period indicate that thisarea of LEH is likely not experiencing oxygen or
carbonate conditions that are detrimental to shellfish

60

Matthew POACH, Daphne MUNROE, James VASSLIDES, Ian ABRAHAMSEN, and Nicole COFFEY

production.

S., Robison M. R., Roberts J. P., and Volety A.,

The LEH monitoring site was chosen because it

2017: Oyster reproduction is compromised byis near the mouth of Great Bay, which is a site ofacidification experienced seasonally in coastal

recurrent summertime upwelling (Glenn., 2004).

regions.

A decrease in pH indicative of upwelled water did not

13480-3., 7, 3276. doi:10.1038/s41598-017-

occur during the June and July monitoring periods

Breitburg D. L., Salisbury J., Bernhard J. M., Cai W.

highlighted here. While it is possible for upwellingJ., Dupont S., Doney S. C., Kroeker K. J., Levin L.

to occur and not be pushed far enough inshore to be

A., Long W. C., Milke L. M., Miller S. H., Phelan

captured at this sensor location; upwelling was not

B., Passow U., Seibel B. A., Todgham A. E., andindicated in the coastal sea surface temperature data

Tarrant A. M., 2015: And on top of all that…

during June or July. More monitoring is necessary

Coping with ocean acidification in the midst of

to determine if upwelled water has the potential to

many stressors.

, 28, 48-61.

impact the LEH ecosystem. Determining if upwelling

Cai W. J., 2011: Estuarine and coastal ocean carbon

can enter LEH is important because it not only

paradox: CO2 sinks or sites of terrestrial carbon

brings lower pH water but also additional nutrients
to fuel productivity during the warmer moreproductive time of the year. These excess nutrientscan exacerbate eutrophication.

incineration?.

, 3, 123-145.

Caldeira K. and Berner R., 1999: Seawater pH andatmospheric carbon dioxide.

, 286, 2043-

2043.
Caldeira K. and Wickett M. E., 2003: Anthropogenic

Acknowledgmentcarbon and ocean pH.

, 425, 365-365.

Clark H. R. and Gobler C. J., 2016: Diurnal fluctuations
The authors would like to acknowledge NOAAʼsin CO 2 and dissolved oxygen concentrations

Ocean Acidification Program and NOAAʼs Hollings

do not provide a refuge from hypoxia and

Scholarship program for the support that they

acidification for early-life-stage bivalves.

provided to this research. Thanks to Mike DeLuca., 558, 1-14. doi:10.3354/meps11852

and the AIC staff for their support with water

Dickinson G. H., Ivanina A. V., Matoo O. B., Pörtner

sampling at the AIC. Gregg Sakowicz provided

H.O., Lannig G., Bock C., Beniash E., and Sokolova

technical assistance and YSI calibration for which

I. M., 2012: Interactive effects of salinity and

we are grateful. Thanks also to Nicole Petersen forelevated CO2 levels on juvenile Eastern oysters,

her tireless work in troubleshooting and maintaining, 215, 29-43.

the LEH station. The LEH station was funded by a
US EPA Clean Water Act Section 320 Grant to theBarnegat Bay Partnership (CE982123-12-2).

doi:10.1242/jeb.061481
Diederich C. M., Jarrett J. N., Chaparro O. R., Segura
C. J., Arellano S. M., and Pechenik J. A., 2011: Low
salinity stress experienced by larvae does not

References

affect post-metamorphic growth or survival inthree calyptraeid gastropods.

Bauer J. E., Cai W. J., Raymond P. A., Bianchi T.

, 397, 94-105.

S., Hopkinson C. S., and Regnier P. A. G., 2013:

Duarte C.M., Hendriks I. E., Moore T. S., Olsen Y. S.,

The changing carbon cycle of the coastal ocean.

Steckbauer A., Ramajo L, Carstensen J., Trotter J.

, 504, 61-70.
Bopp L., Resplandy L., Orr J. C., Doney S. C., Dunne
J. P., Gehlen M., Halloran P., Heinze C., Ilyina
T., Séferian R., Tjiputra J., and Vichi M., 2013:

M., and McCulloh M., 2013: Is ocean acidification
an open-ocean syndrome? Understanding
anthropogenic impacts on seawater pH.
, 36, 221-236.

Multiple stressors of ocean ecosystems of the

Feely R. A., Alin S. R., Newton J., Sabine C. L., Warner

21st century: projections with CMIP5 models.

M., Devol A., Krembs C., and Maloy C., 2010: The, 10, 6225-6245.

combined effects of ocean acidification, mixing,

Boulais M., Chenevert K. J., Demey A. T., Darrow E.

and respiration on pH and carbonate saturation

61

Monitoring coastal acidification along the U.S. East coastin an urbanized estuary.

.

.,88, 442-449.

US EPA report 68-C-02-091 and EP-C-07-025,
United States Environmental Protection Agency,

Fertig B., Kennish M. J., Sakowicz G. P., and Reynolds

Washington, D.C., 188pp.

L. K., 2014: Mind the data gap: identifying andGobler C. J. and Talmage S. C., 2014: Physiologicalassessing drivers of changing eutrophication

response and resilience of early life-stage

condition.

Eastern oysters (, 37, S198-S221.

doi:10.1007/s1223701397465) to past,present and future ocean acidification.

Foley J. A., Ramankutty N., Brauman K. A., Cassidy, 2. doi:10.1093/conphys/cou004

E. S., Gerber J. S., Johnston M., Mueller N. D.,

Gobler C. J., DePasquale E. L., Griffith A. W., andOʼConnell C., Ray D. K., West P. C., Balzer C.,

Baumann H., 2014: Hypoxia and acidification

Bennett E. M., Carpenter S. R., Hill J., Monfreda

have additive and synergistic negative effects

C., Polasky S., Rockström J., Sheehan J., Siebert

on the growth, survival, and metamorphosis ofS., Tilman G. D., and Zaks D. P. M., 2011: Solutions

early life stage bivalves.

for a cultivated planet.

doi:10.1371/journal.pone.0083648, 478, 337-342.

, 9(1), e83648.

FAO, 2016: The State of World Fisheries andGobler C. J., Clark H. R., Griffith A. W., and Lusty M.

Aquaculture 2016. Contributing to food security

V., 2017: Diurnal fluctuation in acidification andand nutrition for all, Rome, 200pp.

hypoxia reduce growth and survival of larval

Ford S. E., 1997: History and present status ofmolluscan shellfisheries from Barnegat Bay
to Delaware Bay, in “The History, Present

and juvenile bay scallops ()

and hard clams ().

, 3, 282. doi:10.3389/fmars.2016.00282

Condition, and Future of the Molluscan Fisheries

Hughes C. P., 2011: The climatology of the Delawareof North and Central America and Europe, Vol.

Bay/sea breeze. M.S. thesis. School of Marine

1. Atlantic and Gulf Coasts” (ed. by MacKenzie Jr.

Science and Policy, University of Delaware,

C. L., Burrell Jr. V. G., Rosenfield A., and Hobart

129pp. [Available online at http://udspace.udel.

W. L.), NOAA Tech. Rept. NMFS 127, pp. 119-140.

edu/handle/19716/10659.]

Frieder C. A., Gonzalez J. P., Bockmon E. E., Navarro

IPCC, 2014: Climate Change 2014. Synthesis

M. O., and Levin L. A., 2014: Can variable pH

report, Contribution of working groups I, II

and low oxygen moderate ocean acidification

and III to the Fifth Assessment Report of theoutcomes for mussel larvae?.

Intergovernmental Panel on Climate Change,

20, 754-764.

(ed. by Pachauri R. K. and Meyer L. A.), IPCC,

Gazeau F., Parker L. M., Comeau S., Gattuso J. P.,

Geneva, Switzerland, 151pp.

O'Connor W. A., Martin S., Portner H. O., andJoesoef A., Huang W.-J., Gao Y., and Cai W.-J., 2015:

Ross P. M., 2013: Impacts of ocean acidificationAir‒water fluxes and sources of carbon dioxide

on marine shelled molluscs.

in the Delaware Estuary: spatial and seasonal, 160, 2207-

2245.

variability.

Glenn S., Arnone R., Bergmann T., Bissett W. P.,, 12, 6085‒6101.

doi:10.5194/bg-12-6085-2015

Crowley M., Cullen J., Gryzmski J., Haidvogel

Keppel A. G., Breitburg D. L., and Burrell R. B., 2016:

D., Kohut J., Moline M., Oliver M., Orrico C.,

Effects of co-varying diel-cycling hypoxia andSherrell R., Song T., Weidemann A., Chant R.,

pH on growth in the Juvenile Eastern Oyster,and Schofield O., 2004: Biogeochemical impact, 11, e0161088.

of summertime coastal upwelling on the New
Jersey Shelf.

, 109, C12S02.

doi:10.1029/2003JC002265
Glibert P. M., Madden C. J., Boynton W., Flemer
D., Heil C., and Sharp J. H., 2010: Nutrients inestuaries: a summary report of the National
Estuarine Experts Workgroup (2005‒2007).

doi:10.1371/journal.pone.0161088
Miller A. W., Reynolds A. C., Sobrino C., and Riedel
G. F., 2009: Shellfish face uncertain future in highCO2 world: influence of acidification on oyster
larvae calcification and growth in estuaries.
, 4, e5661. doi:10.1371/journal.pone.0005661
Montory J. A., Chaparro O. R., Pechenik J. A., Diederich

62

Matthew POACH, Daphne MUNROE, James VASSLIDES, Ian ABRAHAMSEN, and Nicole COFFEY
C. M., and Cubillos V. M., 2014: Impact of short-larval shellfish.

term salinity stress on larval development

17246-17251.

of the marine gastropod
(

). .

.

.

.

.

.

, 107,

Tans P. and Keeling R., 2018: Trends in atmospheric., 458, 39-45.

carbon dioxide, Mauna Loa, Hawaii, Earth

Montory J. A., Chaparro O. R., Navarro J. M., Pechenik.

.

System Research Laboratory Global Monitoring

J. A., and Cubillos V. M., 2016: Post-metamorphic

Division, NOAA. https://www.esrl.noaa.gov/

impact of brief hyposaline stress on recently
hatched veligers of the gastropod
(

).

.

gmd/ccgg/trends/data.html
Waldbusser G. G. and Salisbury J. E., 2014: Ocean., 163, 1-10.

acidification in the coastal zone from an

Naylor R. L., Hardy R. W., Bureau D. P., Chiu A.,

organismʼs perspective: multiple system

Elliott M., Farrell A. P., Forster I., Gatlin D. M.,

parameters, frequency domains, and habitats.

Goldburg R., Hua K., and Nichols P. D., 2009:
Feeding aquaculture in an era of finite resources.
.

.

, 6, 221-247.
Waldbusser G. G., Brunner E. L., Haley B. A., Hales, 106, 15103-15110.

B., Langdon C. J, and Prahl F. G., 2013: A

doi:10.1073/pnas.0905235106

developmental and energetic basis linking larval

New Jersey Dept. of Environmental Protection

oyster shell formation to acidification sensitivity.

(NJDEP), 2014: Dissolved Oxygen Levels in, 40, 2171-2176. doi:10.1002/

Estuarine & Near Shore Waters. Environmental
Trends Report, NJDEP, Office of Science.

grl.50449
Waldbusser G. G., Hales B., Langdon C., Haley B. A.,

https://www.nj.gov/dep/dsr/trends/

Schrader P., Brunner E. L., Gray M. W., Miller

Pierrot D., Lewis E., and Wallace D. W. R., 2006:

C. A., and Gimenez I., 2015: Saturation-state

MS Excel program developed for CO2 systemsensitivity of marine bivalve larvae to ocean

calculations, ORNL/CDIAC-105a. Carbon Dioxide

acidification.

, 5, 273-280.

Information Analysis Center, Oak Ridge National

Waldbusser G. C., Voigt E. P., Bergschneider H., Green

Laboratory, U.S. Department of Energy, Oak

M. A., and Newell R. I. E., 2011: Biocalcification in

Ridge, Tennessee. doi:10.3334/CDIAC/otg.

the Eastern Oyster (CO2SYS̲XLS̲CDIAC105a

relation to long-term trends in Chesapeake Bay

Sabine C. L., Feely R. A., Gruber N., Key R. M., LeepH.

K., Bullister J. L., Wanninkhof R., Wong C. S.,) in, 34, 221-231. doi:10.1007/

s12237-010-9307-0

Wallace D. W. R., Tilbrook B., Millero F. J., Peng

Washington State Blue Ribbon Panel on Ocean

T.-H., Kozyr A., Ono T., and Rios A. F., 2004: The

Acidification, 2012: Ocean acidification: fromoceanic sink for anthropogenic CO2.

knowledge to action, Washington Stateʼs strategic, 305,

367-371.

response (ed. by Adelsman H. and Binder L. W.),

Shaw E. C., Munday P. L., and McNeil B. I., 2013: The

Washington Department of Ecology, Olympia,

role of CO2 variability and exposure time forbiological impacts of ocean acidification.
.

Washington. Publication no. 12-01-015.

.

., 40, 4685-4688. doi:10.1002/grl.50883

Annotated bibliography

Talmage S. C. and Gobler C. J., 2009: The effects ofelevated carbon dioxide concentrations on the(1) Barton A., Hales B., Waldbusser G. G., Langdon C.,

metamorphosis, size, and survival of larval hardand Feely R. A., 2012: The Pacific oyster, Crassostrea

clams (), bay scallops

gigas, shows negative correlation to naturally), and Eastern oysters

elevated carbon dioxide levels: Implications for near-

(
(

).

.

., 54,

2072-2080. doi:10.4319/lo.2009.54.6.2072

term ocean acidification effects.

.,

57, 698-710.

Talmage S. C. and Gobler C. J., 2010: Effects of

The authors report results of a monitoring study

past, present, and future ocean carbon dioxide

designed to evaluate the response of Pacific oyster

concentrations on the growth and survival of() larvae, grown at a commercial

63

Monitoring coastal acidification along the U.S. East coast
hatchery on the Oregon coast, to natural changes

to ocean acidification. Their results highlight USin carbonate chemistry associated with periodic

regions most vulnerable to ocean acidification,seasonal upwelling during the summer of 2009.

reasons for that vulnerability, important knowledge

During the study the intake waters experienced

and information gaps, and opportunities to adapt

aragonite saturation states from 0.8 to 3.2 and pH

through local actions. Results indicated that 16 of thefrom 7.6 to 8.2. They observed significant negative

23 bioregions around the United States are exposed

relationships between aragonite saturation states at

to rapid OA (reaching ΩAr 1.5 by 2050) or at least

the time of spawning and subsequent growth andone amplifier; 10 regions are exposed to two or moreproduction of larvae over the size range of 120 tothreats of acidification. The marine ecosystems and150-mm shell length. This was one of the first studies

shelled molluscs around the Pacific Northwest andto link failures in seed oyster production to moreSouthern Alaska are expected to be exposed soonest

corrosive water from coastal upwelling.

to rising global OA, followed by the north-central
West Coast and the Gulf of Maine in the northeast(2) Booth J. A.T., McPhee-Shaw E. E., Chua P., Kingsley

United States. Communities highly reliant on shelledE., Denna M., Phillips R., Bograd S. J., Zeidberg L. D.,molluscs in these bioregions are at risk from OA

and Gilly W. F., 2012: Natural intrusions of hypoxic,

either now or in the coming decades. In addition,

low pH water into nearshore marine environments

pockets of marine ecosystems along the East andon the California coast.

Gulf Coasts will experience acidification earlier than., 45, 108-115.

The authors reviewed a decade-long data set to

global projections indicate, owing to the presence of

examine oxygen and pH variability on the inner

local amplifiers such as coastal eutrophication andshelf off of Central California. Results show regulardischarge of low-ΩAr river water. This analysis caninundation of cold, hypoxic and low pH water. The

be used to help prioritize societal responses to ocean

source-water for these periodic intrusions originates

acidification.

in the offshore, midwater environment above the local
OMZ, generally between 50‒100 m but occasionally(4) Gobler C. J. and Baumann H., 2016: Hypoxia anddeeper. Pulses of the greatest intensity arose at theacidification in ocean ecosystems: coupled dynamics

onset of the spring upwelling season, and fluctuations

and effects on marine life.

were strongly semidiurnal and diurnal. Arrival of

doi:10.1098/rsbl.2015.0976.

., 12, 20150976.

cold, hypoxic water on the inner shelf appears to be

As climate change progresses, the effects ofdriven by tidal-frequency internal waves pushingatmospheric CO2 on coastal acidification will intensify;

deep, upwelled water into nearshore habitats. These

and, while hypoxia is a much studied stressor for

observations are consistent with the interpretation

coastal organisms, the combined effect of hypoxia

that hypoxic water is advected shoreward from theand acidification has only recently become a focus

deep, offshore environment where water masses

for scientists. The authors conduct a meta-analysis

experience a general decline of temperature, oxygenof published research that studied the combined

and pH with depth.

effects of pH and dissolved oxygen variability on
marine organisms. The authors conclude that low(3) Ekstrom J. A., Suatoni L., Cooley S. R., Pendleton L.

DO is a greater stressor to most marine organisms

H., Waldbusser G. G., Cinner J. E., Ritter J., Langdon

than low pH conditions, although worse effects canC., van Hooidonk R., Gledhill D., Wellman K., Beck M.

occur through the synergistic interaction of the two.

W., Brander L. M., Rittschof D., Doherty C., Edwards

While most traits under concurrent low DO and low

P. E. T., and Portela R., 2015: Vulnerability andpH appeared to be additively affected, every study

adaptation of US shellfisheries to ocean acidification.

reviewed also found synergistic interactions in at.

.

., 5, 207-214. doi:10.1038/nclimate2508

least one instance. They also conclude that neither

Authors present a spatially explicit,

the occurrence nor the strength of these synergistic

multidisciplinary analysis of the vulnerability of

impacts is currently predictable, and therefore, thecoastal human communities in the United Statestrue threat of concurrent acidification and hypoxia

64

Matthew POACH, Daphne MUNROE, James VASSLIDES, Ian ABRAHAMSEN, and Nicole COFFEY

to marine food webs and fisheries is still not fully

across Narragansett Bay, Long Island Sound, andunderstood. Addressing this knowledge gap will

Jamaica Bay; and 3) Continuous, horizontal mapping

require an expansion of multi-stressor approaches inof conditions across Jamaica Bay and Hempstead

experimental and field studies.

Bay. Low pH conditions (< 7.4) were detected in all
systems during summer and fall months concurrent(5) Wallace R. B., Baumann H., Grear J. S., Aller R. C.,with the decline in DO concentrations. Whileand Gobler C. J., 2014: Coastal ocean acidification: The

hypoxic waters and/or regions in close proximity

other eutrophication problem.

to sewage discharge had extremely high levels of.

.

., 148, 1-13. doi:10.1016/j.ecss.2014.05.027

pCO2, (> 3000 µatm), were acidic pH (< 7.0), and were

To assess the potential for acidification in eutrophic

undersaturated with regard to aragonite (ΩAr < 1),estuaries, the authors characterized the spatial andeven near-normoxic but eutrophic regions of these

temporal patterns of DO, pH, pCO2, and ΩAr in four,

estuaries were often relatively acidified (pH < 7.7)

semi-enclosed estuarine system across the Northeast

during late summer and/or early fall. This study

US: Narragansett Bay, Long Island Sound, Jamaica

revealed that acidification is an annual feature ofBay, and Hempstead Bay. Multi-year monitoring

eutrophic estuaries across the Northeast US that co-datasets were assessed to define seasonal patterns

occurs with seasonally low oxygen. The spatial andin pH and DO while cruises were conducted totemporal dynamics of DO, pH, pCO2, and ΩAr suggest

vertically and horizontally resolve spatial patterns

that they are all ultimately driven by high rates ofof acidification during the seasonal onset, peak, andmicrobial respiration. The degree of acidification

decline of hypoxia in these estuaries. They utilized

observed in these systems during summer are within

three approaches for this study: 1) The analysis ofranges that have been shown to adversely impact amonthly monitoring data across Long Island Sound;wide range of marine life.

2) Vertical measurements of water column conditions

水 研 機 構 研 報， 第 49 号，65 − 72， 平 成 31 年
Bull. Jap. Fish. Res. Edu. Agen. No. 49，65−72，2019

65

Growth variation in long blade kelp
Hokkaido, Japanin eastern

Natsuki HASEGAWA＊1, Toshihiro ONITSUKA＊2, Sayaka ITO＊3, and Tomonori AZUMAYA＊2

Abstract:(Naga-konbu in Japanese) is distributed in shallow Pacific coastal

areas from eastern Hokkaido (Kushiro and Nemuro) to Chishima Island. It is a commercially
important Laminariacean kelp species in this area. The variations in the blade size of(age 1+) were analyzed in Habomai, eastern Hokkaido, Japan. The fisheries cooperative associationof Habomai in Nemuro monitored the blade size of the kelp in the harvest grounds along more than
15 km of coastline in May and June from 2000 to 2014. The monitoring data showed that the blade
weight varied among years, and the growth of blade weight was greater in 2002 and 2009 then theother years. The kelps had a poorer growth of the blade in 2001, 2011 and 2013. Correlation analysis
revealed that the coefficients between the blade weight in May and the monthly mean watertemperature in spring to autumn in the previous year were negative but positive in winter to springin the same year. Generalized linear regression model (GLM) analysis of the blade weight in May
also revealed that the growth models including only monthly mean water temperature (January,
April, July and October in the previous year, January, April during in the same year) and longitude
effectively estimated the variation of the annual mean weight. Correlation analysis also revealed thatthe mean wet weight ofin May represents the growth condition of the kelp of theyear, and it is useful for predicting the annual fisheries production in this area. These results
suggested that the weight growth ofis affected by the ambient water temperature

both in the previous and the same years. High temperature in the preceding autumn and extremely
low temperature in the preceding winter to spring reduce the blade weight in the summer harvest
season. Therefore, the increasing trends of water temperature in recent years may be one of thefactors decreasing the fisheries production of the kelp in eastern Hokkaido.
Key words:(Naga-konbu),

kelp, growth, water temperature,eastern Hokkaido

Introduction

culture of Laminariacean kelp species are important
for the fishing industry in the Pacific coastal areas,

Seaweeds, including kelps, are fundamental species

such as northern Japan (Mizuta, 2003).

of the coastal ecosystem, serving as a nursery, refuge,(Naga-konbu in Japanese) is one of thoseforage and spawning habitat for many organisms

kelp species, which grows up to more than 10 m

(Steneckin blade length (Fig.1a).

., 2002). In addition, kelp species haveespecially high growth rates, and wild harvest andclassified as

used to be(Miyabe), but

2018年８月31日受理（Accepted on August 31, 2018）
National Research Institute of Aquaculture, Japan Fisheries Research and Education Agency, 422-1, Nakatsuhamaura, Minamiise, Watarai, Mie,
516-0193, Japan＊2
Hokkaido National Fisheries Research Institute (Kushiro Laboratory), Japan Fisheries Research and Education Agency, 116 Katsurakoi,
Kushiro, Hokkaido, 085-0802, Japan＊3
Hokkaido National Fisheries Research Institute (Akkeshi Laboratory), Japan Fisheries Research and Education Agency, 2-1 Tsukushikoi,
Akkeshi-cho, Akkeshi-gun, Hokkaido, 088-1108, Japan
E-mail: hasena@fra.affrc.go.jp＊1

66

Natsuki HASEGAWA, Toshihiro ONITSUKA, Sayaka ITO, and Tomonori AZUMAYA

most

species including this species were

taxonomically reorganized into the genus
through a multi-gene molecular investigation (Lane., 2006; Yotsukura, 2010). The kelp is distributed
in shallow Pacific coastal areas (Fig.1b) from eastern
Hokkaido (Kushiro and Nemuro) to the ChishimaIslands. Its distribution area is under the influence ofthe cold Oyashio current, and the water temperature
varies seasonally from sub-zero to 20°
C. This kelp
is the main harvested species in eastern Hokkaido(Fig.1c, d), mostly used for tsukuda-ni (preserved
food cooked with sweetened soy sauce) and kelp
rolls, making use of its soft texture, whereas otherkelp species with harder blades are widely used
for broth. The annual total fishery production of
the kelp species in Kushiro and Nemuro, whereis the main harvested species, is around10 thousand tons in dry weight, with a gradualdecreasing trend in recent years (Fig.2, Hokkaido
Regional Agricultural Administration Office, 2017). A
similar trend is seen in other kelp species in otherareas in Hokkaido. Akaike (2017) suggested that
there is a high probability change of the marine
environment has affected the production of kelp
species in Hokkaido. The present study focused ondetermination of the environmental factors affecting
the variation in the growth and fisheries productionof(Miyabe) in eastern Hokkaido, Japan.
Materials and methods
The fisheries cooperative association of Habomaihas been monitoring the blade size of thein May and June in its harvest grounds along morethan 15 km of coastline in Nemuro, eastern Hokkaido(from 43.30°
N, 145.67°
E to 43.39°
N, 145.82°
E, Fig.3).
In each monitoring, one to 20 sporophytes of thekelp were collected using long handle gears in 28 to
40 locations, and the blade length, maximum width
and the wet weight of the kelp were measured. The
variations in the blade size of the kelp over age 1+ (2ndyear sporophyte) from 2000 to 2014 were analyzed inthis study.

is a perennial species, andthe kelp over age 1+ is targeted for fisheries harvestusing long handle gears between June and October.
Thin bladed sporophytes identified as less than age
1+, were excluded from the calculative analysis. The

Fig. 1.
. (a): overview of
sporophytes, (b): lower intertidal to upper subtidal
habitats, (c) and (d): drying process on artificial stone
fields.

growth67

incongruous sporophytes, with unknown collection
sites and unusual weight to length ratio, were also
excluded from the analysis.
Effects of environmental factors on the blade
weight in May were estimated using correlation
analysis. Blade weight was used for the representative
variable ofsize in the correlation

analysis. Monthly average water temperature in
Kushiro, monthly mean daylight hours and windspeed in Nemuro in the previous and same years
were used as the environmental factors in thisanalysis. Moreover, the effects of water temperatureon the blade weight in May were estimated using ageneralized linear regression model (GLM) because

Fig. 2. Fisheries production of kelp species ineastern Hokkaido (Kushiro and Nemuro).
is assumed to contribute about 70 % of thefisheries production of kelps in this area. Values arein dry weight.

the correlation analysis revealed that only coefficients
between the blade weight in May and the meanwater temperature had significant trends throughout
the years (see Result and Discussion). To avoid themulti-collinearity of the mean water temperature
among successive months, monthly mean watertemperature for January, April, July and October,which were selected as the representative months ofeach quarter of the year, were used as the dependent
variables for the GLM analysis. In addition, GLM
analysis was also performed between the mean
blade weight in May and the monthly mean watertemperature, with a significant correlation withthe former (P < 0.05). But January in the previous
year and January, March in the same year were
excluded to avoid multi-collinearity (see Results andDiscussion). Longitudes of the sampling sites werealso used as explanation variables for locations inthese models. Dependent variables (blade weight inMay) were assumed to follow the gamma distribution(log link). Model selection based on Akaikeʼs
information criterion (AIC) was then performed, andFig. 3. Monitoring sites forin Habomai area and monitoring stations for watertemperature in Kushiro and daylight hours and windspeed in Nemuro, eastern Hokkaido, Japan.

those with the minimum AICs were regarded as thebest fit model. Monthly mean water temperature
in Kushiro was calculated from the temperature(43.331°N, 145.586°E). Relationships between meanof the intake water for the experimental facilities

blade weight in May and June, the mean bladeof Hokkaido National Fisheries Research Instituteweight in May and fisheries production of kelp

(Kushiro Laboratory), Japan Fisheries Research andspecies in Nemuro (Hokkaido Regional Agricultural

Education Agency (42.949°N, 144.442°E), which is

Administration Office, 2017) were analyzed for eachlocated 100 km west of the study area in Habomai.

site using a correlation analysis. In the correlation

Monthly average daylight hours and wind speed

analysis, blade weight and fisheries production were

were obtained from the Automated Meteorologicaltransformed logarithmically. The significance ofData Acquisition System (AMeDAS) in Nemuro

the correlation coefficients was tested by Pearson's

68

Natsuki HASEGAWA, Toshihiro ONITSUKA, Sayaka ITO, and Tomonori AZUMAYA

product-moment correlation, and P < 0.05 wasconsidered statistically significant.
Results and discussion
From the 15 year monitoring data, 4,149
sporophytes and 469 site mean blade weights and4,543 sporophytes and 396 site mean blade weights
were used for the analysis for May and June,
respectively, in this study of. The

monitoring data showed that the blade weight in
May varied among years (Fig.4). Overall, mean of theblade weight in May was 703 ± 174 gWW (grams wet
weight ± standard deviation (SD)). The mean blade
weight in May was heavier in 2002 and 2009 than theFig. 5. Variations in correlation coefficient betweensite mean blade weight ofinMay and monthly mean water temperature, daylight
hours and wind speed.

overall mean + SD, whereas the mean weight waslighter in 2001, 2013 and 2011 than the overall mean
- SD. Correlation analysis revealed that coefficients
between the blade weight in May and monthly
mean water temperature displayed certain trends
throughout the years (Fig.5 and 6); the correlation
coefficients between the mean blade weight in May
and the mean water temperature in the previous
spring to autumn were negative (r = -0.28 to -0.08),
and those between the mean blade weight in May
and the mean water temperature in winter andspring in the same year were positive (r = 0.33 to0.48). The mean blade weight in May had a significant

Fig. 4. Monitored and estimated blade weight ofin May in Habomai area,
eastern Hokkaido, Japan. Values are in wet weight(WW). Dashed line shows the estimated weight by
the model including longitudes and monthly meanwater temperatures (January, April, July, October
during same year and January, April during sameyear).

Fig. 6. Relationships between site mean blade weightofin May and monthly meanwater temperature. (a): January, (b): April, (c): July, (d):October in the previous year, (e): January, (f): April inthe same year.

69

growthcorrelation with the mean water temperature,(6,347) than the null model (6,513), and it effectively

except for in April, August and November in theestimated the variation of the mean weight in May

previous year. The mean blade weight in May was(Fig.4). In this model, the mean blade weight in May

significantly correlated with the mean daylight hours

had a negative GLM coefficient with the quarterly

in March (r = -0.23), September (0.13), and November

mean water temperature in April to October in the(-0.16) in the previous year and January (-0.24),

previous year and positive coefficients in January

February (-0.43) and April (0.29) in the same year.

and April in the same year, which was similar to the

The mean blade weight in May was also significantly

trend shown in the correlation coefficient analysis.

correlated with monthly mean wind speed in January

The GLM coefficient of the longitude was positive(r = 0.10), February (0.15), April (-0.16), August (-0.16),

both in the best model and the model including only

September (-0.18), November (-0.28), and December

water temperature and longitude.

(-0.12) in the previous year and January (-0.14) andOverall, mean of the blade weight in June wasMarch (0.36) in the same year. However, unlike water

1,038 ± 210 gWW. The mean weight in June ranged

temperature, neither the daylight hours nor the

between 716 ± 169 gWW in 2014 to 1,385 ± 252 gWW

wind speed showed correlative tends with the bladein 2009. The per site mean blade weight in June wasweight throughout the years.

positively correlated with the blade weight in May,

The GLM analysis of the blade weight in May

with a correlation coefficient of 0.45 (Fig.7), and therevealed that the model including water temperaturemean blade weight in May was positively correlated

in February, May-July, September, and December

with fisheries production of the kelp in Nemuro, within the previous year and February and April in thea correlation coefficient of 0.58 (Fig.8). These results

same year was the best fit model, with the smallest

revealed that the blade weight of

AIC value of 6,329 (Table 1). The model including

May remarkably represents the growth situation

only water temperature of each quarter of theof the kelp of the year and is useful to predict theyear and longitude also had a smaller AIC value

fisheries production in this area. This association

inTable 1. Result of generalized linear model analysis of site mean blade weight ofin May in
Habomai, eastern Hokkaido Japan. Values of each variable represent mean estimate coefficient ± standard error.
Check marks represent the independent variables included in each model.
,QGHSHQGHQWYDULDEOHV(VWLPDWHFRHIILFLHQW)XOOPRGHO%HVWPRGHO(VWLPDWHFRHIILFLHQW)XOO %HVW PRGHO  

‫ݲ‬

‫ݲ‬

  

‫ݲ‬  ‫ݲ‬)HEUXUDU\

  

‫ݲ‬

‫ݲ‬

0DUFK

  ‫ݲ‬  

‫ݲ‬

0D\

  

‫ݲ‬

‫ݲ‬

-XQH

  

‫ݲ‬

‫ݲ‬

-XO\

  

‫ݲ‬

‫ݲ‬

  ‫ݲ‬

6HSWHPEHU

  

‫ݲ‬

‫ݲ‬

2FWREHU

  ‫ݲ‬  ‫ݲ‬  

‫ݲ‬

‫ݲ‬
  ‫ݲ‬  

‫ݲ‬

‫ݲ‬

  

‫ݲ‬

‫ݲ‬

  ‫ݲ‬  

‫ݲ‬

‫ݲ‬

  





1XOOPRGHO,QWHUFHSW:DWHUWHPSHUDWXUH3UHYLRXV\HDU-DQXDU\$SULO$XJXVW

1RYHPEHU'HFHPEHU
6DPH\HDU-DQXUD\)HEUXUDU\
0DUFK
$SULO

/RQJLWXGH
$,&



‫ݲ‬


70

Natsuki HASEGAWA, Toshihiro ONITSUKA, Sayaka ITO, and Tomonori AZUMAYA

Fig. 7. Relationship between site mean blade weightofin May and June. Values are
in wet weight (WW).

Fig. 8. Relationships between annual mean blade
weight ofin May and annual
fisheries production of kelp species in Nemuro, where
was the main harvested kelp species.
Blade weight and fisheries production are in wet
weight (WW) and dry weight (DW), respectively.

occurred despite the fact that the fisheries productionof the kelp was often affected by the number of daysof harvest and fishermen (Shinada. 2014).

Growth status of the age 1+ sporophytes until

related with the water temperature in the previous
spring. Moreover, Shinada. (2014) concluded

May is an important factor in determining thethat dissolved inorganic nitrogen concentration infisheries production of the kelp in this area, and GLM

March and sea urchin (consumer of kelp) biomass

analysis and correlation analysis feasibly revealed

were important for changes in first year biomass ofthat the growth was affected by the ambient watervar.

, but there were no clear

temperature. High temperature in the previous

relationships between the kelp biomass and water

autumn and extremely low temperature in thetemperature. These relationships between growthprevious winter to spring reduced the blade weightand biomass ofof the kelp in the summer harvest season. Sasaki

were different from the results of our study probably(1973) reported that regeneration of

due to the differences in species and age of kelps.

and water temperature

sporophytes starts around November, with a daily

General trends in the blade weight variation in

growth rate of blade length ranging from 5 to 10

May was well-estimated by the models that included

mm day-1 until March, and growth reaches thequarterly mean water temperature and longitude,

maximum of 68 mm day-1 during May and June.

but there was a large difference between the

Early decrease of water temperature in the previous

estimated and actual mean blade weight in 2011,

year might cause early start of regeneration of theduring which the tsunami generated by the great

sporophytes, and the growth of sporophytes mighteast Japan earthquake hit this area with the wave

be enhanced by warmer conditions during winterheight over 4.5 m (Japan Meteorological Agency，

and spring, when water temperature is below 4℃ in2013). Disturbance caused by the tsunami might havethis area. Meanwhile, Kirihara. (2003) reported

damaged the blades and inhibited the kelp growth.

that the growing densities of age 1+ sporophytes

In addition, drift ice physically scrapes off the kelps

offrom the rocky substrates and causes declines inin early summer were negatively

71

growththe fisheries production. However, intense drift ice

environmental factor to determine the growth ofincreases the fisheries production of the kelp in the. In the sea off Kushiro (offshore offollowing year through creating a new substrate foreastern Hokkaido), an upward trend in sea surface

the kelp (Sasaki 1973).

temperature (SST) is clear during autumn, in which

In the GLM analysis, longitude was shown toregeneration of S. longissima sporophytes starts,

positively affect the blade weight in May. This

both on a long-term basis and since the year 2000

may be explained by the ocean currents in the(Fig.9, Global Environment and Marine Department,

study area. In the coastal area of eastern Hokkaido,

Japan Meteorological Agency, 2017). In addition, sincelarge amounts of nutrients are supplied by the first

2000, SST during the spring growing season of

branch of the Oyashio current, which runs westward(Tanakafrequently below the grand mean from., 1991). Therefore, the faster growth of

1981 to 2010. This trend in water temperatures may

the sporophytes might be attributable to the higher

be one of the factors decreasing the growth and thenutrient supply in eastern part of the monitoring

fisheries production of the kelp in eastern Hokkaido,

area, located upstream in the Oyashio current.

and there is a concern that the deterioration of the

In conclusion, water temperature is an important

kelp fisheries may be aggravated if the present watertemperature trend persists.
Acknowledgment
We express our respect for long term monitoring ofkelp by fisheries cooperative association of Habomai
and are grateful to Y. Fuchigami for organizing thesemonitoring data. This study was carried out under
the framework of the conference on kelp research in
Nemuro city.
References
Akaike S., 2017: Sea has changed? ~ Change ofkelp fisheries and marine environment ~.
Hokusuishidayori, 95, 9-12. (in Japanese)
Global Environment and Marine Department, Japan
Meteorological Agency, 2017: Long-term change
tendency in surface water temperature near
Japan. https://www.data.jma.go.jp/kaiyou/data/
shindan/a̲1/japan̲warm/japan̲warm.html,(Press: 12th, March 2018)
Hokkaido Regional Agricultural Administration
Office, 2017: Annual report of agriculture,
Forestry and Fishery statistics in Hokkaido

Fig. 9. Deviation of seasonal mean sea surface
temperature from the grand mean values in sea off
Kushiro (offshore of eastern Hokkaido, Japan). The
grand mean values for each season were calculated
from the seasonal mean sea surface temperaturefrom 1981 to 2010. Data was obtained from Global
Environment and Marine Department, Japan
Meteorological Agency (2017).

(Fisheries), 74pp. (in Japanese)
Japan Meteorological Agency, 2013: Report on the2011 off the Pacific Coast of Tohoku Earthquake
by Japan Meteorological Agency, Part 1.
, 133, 1-354. (in Japanese)
Kirihara S., Nakamura T., and Notoya M., 2003:

72

Natsuki HASEGAWA, Toshihiro ONITSUKA, Sayaka ITO, and Tomonori AZUMAYA
Effect of water temperature on the growth of(Annotated bibliography)

at the coast of Shiriyazaki, Shimokita Peninsula,
Japan.

(1) Sasaki S., 1973: Studies on the life history of, 51, 273-280.

(in Japanese with English abstracts)
Lane C. E., Mayes C., Druehl L. D., and Saunders G.
W., 2006: A multi-gene molecular investigation of
the kelp (substantial taxonomic re-organization.

var.

.

Hokkaido Kushiro Fisheries Experimental Station,
Kushiro, 141pp.
This paper was published in 1970s when this) supports

species increasingly became of high fisheries.,

importance around eastern Hokkaido, Japan. The

42, 493-512.

author summarized the life history of

Mizuta H., 2003: Distribution of Laminaria species

var.

., which has

in coastal Oyashio region and their nutritional

been recently renamed as Saccharina longissima.

requirements.

This paper includes the studies about the life., 41, 33-38. (inJapanese with English abstracts)

history of two seasonal germinal groups in winter

Sasaki S. (ed), 1973: Studies on the life history ofand summer to provide information for stockvar.

enhancements, the importance of suspended culture,.

Hokkaido Kushiro Fish. Exp. Stn., Kushiro,

reviewing position of the

141pp. (in Japanese)

kelp fisheries with evaluating the factors affecting

in Japanese

Shinada A., Nishida Y., Kuribayashi Y., Goda H.,

its fisheries production such as the floating ice. Some

Kawai T., and Akaike S., 2014: Effect of marine

parts of these studies were published in Journal ofenvironment on annual changes in first year

Hokkaido Fisheries Experimental Station in Japanese.

biomass ofvar.

Although the marine and social environments for

at Rishiri island, Japan.

., 51, 39-45. (inJapanese with English abstracts)

fisheries have markedly changed since
1970s, intensive studies such as one done by Sasaki

Steneck R. S., Graham M. H., Bourque B. J., Corbett(1973) have not been conducted since then.

D., Erlandoson J. M., Estes J. A., and Tegner
M. J., 2002: Kelp forest ecosystem biodiversity,(2) Yotsukura N., 2010: The hierarchy of Laminariales

stability, resilience and future.

in Japan.

.,29, 436-459.

, 3, 193-198.

This paper reviews the hierarchy of laminarialean

Tanaka K., Sato Y., and Kakuda T., 1991: Seasonalalgae which has been proposed by molecularchanges in nutrient concentrations in the coastal

phylogenetic analyses. There is a variety ofarea of eastern Hokkaido.

laminarialean species in Japanʼs coastal areas where, 55, 161-172. (in Japanese withEnglish abstracts)

are harvested or cultured on a large scale. These

Yotsukura N., 2010: The hierarchy of Laminariales inJapan.
with English abstracts)some species including, 3, 193-198. (in Japanese

species have been classified based on morphologicalcharacteristics although there are variations in
its morphology among its growth stages andenvironmental conditions. Author enumerated 37
laminarialean species belonging to 7 families in Japan.

水 研 機 構 研 報， 第 49 号，73 − 79， 平 成 31 年
Bull. Jap. Fish. Res. Edu. Agen. No. 49，73−79，201973

Harmful algal blooms and shellfish aquaculture in changing
environment
Leila BASTI＊1, Kiyohito NAGAI＊2, Susumu SEGAWA＊3, Yuji TANAKA＊1, Toshiyuki SUZUKI＊4,and Satoshi NAGAI＊4

Abstract: Shellfish aquaculture is mainly carried out in sheltered coastal areas that are affected byseveral anthropogenic stressors, including eutrophication, pollution, biofouling, invasive species,
expanding diseases, and harmful algal blooms. In particular, harmful algal blooms (HAB) have been
known to cause fish and shellfish kills; contamination of fish, but mainly shellfish, with potent toxinsthat cause mild to severe poisonings in humans; and in many cases, alteration of ecosystem functions.
In shellfish, notably in bivalve molluscs, in addition to mass mortalities, HAB are known to cause
acute to chronic physiological and pathological alterations that lead to impediments to aquaculture
farms via reduction of bivalve fitness or following closure of production due to long-term
contamination with toxins detrimental to human health.
The frequency, magnitude, duration, and in several cases, the geographic distribution of HAB
have been increasing, putting shellfish aquaculture farms under further stress. Several factors havebeen attributed to such increase in HAB, including climate change. Range expansions of somecosmopolitan HAB species associated with warming ocean temperature have been reported acrossthe North Atlantic and North Pacific. In addition, range expansions of some other cosmopolitan HAB
species have been projected across the North Western European Shelf-Baltic Sea system and North
East and South East Asia, associated with increased nutrient loads under projected climate change
scenario A1B of the IPCC, IPSL-CM4. Warming water temperature driven by climate change is also
expected to induce thermodynamic changes in physiological functions of shellfish, with potential
shifts in their thermal sensitivity and performance, and it is also expected to alter the responses ofbivalves to HAB.
In this mini-review, the effects of HAB and ocean warming ‒ and other climate driven stressors
like ocean acidification ‒ on these important cultured shellfish species will be discussed in light of
the findings of relevant studies reported in the literature.
Key words: harmful algal blooms, shellfish, aquaculture, climate change

Introduction

the expansion of aquaculture activities to offshore
production, most of the mariculture activities are

Human consumption from aquaculture exceeded

still carried out in sheltered coastal areas (Trujillothat from wild resources for the first time in 2014,., 2012). These areas are subjected to several

and aquaculture has become the fastest growing foodanthropogenic stressors, including eutrophication,

production system in the world (FAO, 2014). Despite

pollution, biofouling, invasive species, expanding

2018年８月31日受理（Accepted on August 31, 2018）
Department of Ocean Sciences, Tokyo University of Marine Science and Technology, Minato, Tokyo 108-8477, Japan.
＊2
K. Mikimoto and Co. Ltd., Osaki Hazako, Hamajima-Cho, Shima, Mie 517-0403, Japan＊3
Department of Aqua Bioscience and Industry, Tokyo University of Agriculture, 196 Yasaka, Abashiri 099-2493, Japan＊4
National Research Institute of Fisheries Science, Fisheries Research and Education Agency, 2-12-4 Fukuura, Kanazawa, Yokohama, Kanagawa
236-8648, Japan
E-mail: lbasti1@kaiyodai.ac.jp＊1Leila BASTI, Kiyohito NAGAI, Susumu SEGAWA, Yuji TANAKA, Toshiyuki SUZUKI,
and Satoshi NAGAI

74

diseases, and harmful algal blooms (HAB) (Rogers andand scallops. Several pathologies in almost all organs

Laffoley, 2011).

of bivalve molluscs have also been shown to be

HAB pose a significant threat to marine andcaused by species of HAB, including inflammation,

freshwater ecosystems as they cause a wide range

necrosis and atrophy (Shumway and Cucci, 1987;

of cascading impacts either via their increased

Gainey and Shumway, 1988: Bricelj

biomass or via the production of potent toxins andBastibioactive compounds (Burkholder, 1998). These

2010a; Haberkorn

HAB have increased over the past decades with

Several pathologies in almost all organs of bivalve

associated increases in their effects on ecosystems

molluscs have also been shown to be caused byand related human activities, including tourism,species of HAB, including inflammation, necrosis

fishing, and aquaculture (Smayda, 1990; Hallegraeff,and atrophy. Modulation of the immune system,

1993; Van Dolah, 2000; Zingone and Enevoldsen, 2000;

antioxidant system and neuroenzymatic activity, as

Allenwell as modification of the physiological energetics,., 2006; Matsuyama and Shumway, 2009).

In addition, a wide diversity of HAB species causes., 2009; Basti., 1996;., 2011a; Haberkorn., 2010b; Hégaret.,., 2012).

can also occur (Hégaret and Wikfors, 2005; Basti

intoxication of humans following the consumption., 2016). The reproduction and the recruitment ofof seafood products, mainly bivalve molluscs thatshellfish are also affected by several species of HAB,

have accumulated their toxins, leading to closures ofwith numerous recruitment failures reported fromshellfish beds and long-term suspension of production

the field, in addition to several negative effects inin aquaculture farms (Van Dolah, 2000). Several

gametes, fertilization, embryos and larvae of clams,

species of HAB have also been known to cause

oysters and scallops (Basti

mass mortalities of aquatic organisms and numerous

2013; Basti

documented deleterious effects on the physiology of

HAB have been shown to affect the susceptibility ofcultured shellfish (Landsberg, 2002; Basti

shellfish to diseases and, thus, facilitate the expansion., 2018a).

Coastal areas witnessing expansion of HAB events., 2011b; Basti., 2015a; Banno

of diseases in aquaculture farms (e.g. Da Silva

are also at risk of impacts from climate change-

2008; Hégaret

driven forcing, including sea level rise; alteration in

2002; Basti.,., 2018). In addition,.,., 2010; reviewed in: Landsberg,., 2018a).

nutrients, sediment and salinity regimes; changes
in circulation patterns, water residence time andEffects of warming and ocean acidification on

upwelling; frequency and intensity of storms; oceanshellfish

warming; and ocean acidification (Scavia
2002; Caldeira and Wickett, 2005; Harley.,., 2006;

The effects of climate change on the world ocean., 2013). The

are being documented worldwide (IPCC, 2007; Doney

impacts of HAB on shellfish aquaculture, mainly., 2012). Climate-driven changes in the physicalbivalve molluscs, and the potential impacts of climate-and chemical systems of the oceans are inducing

driven changes on the interactions HAB-shellfish arechanges in the biological systems as well as humanreviewed.

uses of ocean resources. Warming water temperature

Domingues., 2008; Ruckelshaus

has already been shown to affect the survival,
Effects of harmful algal blooms on shellfish

growth, reproduction, health and phenology of marineorganisms (Doney., 2012). Warming could result

HAB affect shellfish aquaculture by causing acute,in changes in the primary production and food web

chronic, and sublethal effects in several species

structure and function and, thereafter, changes in lifeof shellfish (Shumway, 1990; Landsberg, 2002). In

history processes such as spat-fall of shellfish, as well

shellfish, in addition to mass mortalities, HAB affectas physiological stresses leading to decreased growth

the behavior and physiology of several commerciallyand production (Allison

important species. Reduction of filtration, respiration,

review, Comptonand valve gaping have been reported in several

will have more impacts on the survival, range andcultured species, including clams, oysters, mussels,

productivity of tropical than temperate shellfish., 2011). In a literature. (2007) found that warming

75

Environmental stressors to shellfish aquaculture
species, which might lead to shift in species cultured

Referencesin aquaculture farms in the future oceans. On theother hand, ocean acidification (OA) has been shown

Allen J. I., Anderson D., Burford M., Dyhrman

to affect calcifying organisms, including mussels,S., Flynn K., Glibert P. M., Granéli E., Heil C.,

clams and oysters. Despite the extensive literature on

Shellner K., Smayda T., and Zhou M., 2006: Global

the effects of OA on marine organisms, generalization

Ecology and Oceanography of Harmful Algalon the biological effects of OA remains disputable,

Blooms, Harmful Algal Blooms in Eutrophic

especially that the mechanisms of sensitivity to

Systems, GEOHAB Report 4IOC and SCOR,

long-term exposures to OA are not well understood

Paris and Baltimore, 74pp.

(Berge., 2006; Gazeau

2009; Miller
Allisson., 2007; Cochran.,Allison E. H., Badjek M. C., and Meinhold K., 2011:., 2009; Talmage and Gobler, 2010;

The implications of global climate change for., 2011; Barton

molluscan aquaculture, in “Shellfish Aquaculture., 2012). There is little information, however, on., 2011; Waldbusser

and the Environment” (ed. by Shumway S. E.),the effects of both warming and OA on shellfish. For

John Wiley & Sons Ltd, Chichester, pp. 461-490.

instance, in a short- and long-term laboratory studies,

Banno K., Oda T., Nagai K., Nagai S., Tanaka Y., andthe fertilization and early-life development of Sydney

Basti L., 2018: Deleterious effects of harmfulrock oyster were shown to be severely affected by

dinoflagellates and raphidophytes on egg

the synergistic effects of warming and OA (Parker

viability and spermatozoa swimming velocity., 2009).

in the Japanese pearl oyster, 37, 41-48.

Impacts of harmful algal blooms and climate change
on shellfish aquaculture

Barton A., Hales B., Waldbusser G. G., Langdon C., andFeely R. A., 2012: The Pacific oyster,, shows negative correlation to naturally

Evidence that climate change has been influencing
HAB events at a global scale has been accumulating(Mooreelevated carbon dioxide levels: implications fornear-term ocean acidification effects.

., 2008). Climate-driven changes in, 57, 698-710.

temperature, irradiance, chemical composition of

Basti L., Nagai K., Shimasaki Y., Oshima Y., Honjo

seawater, nutrients, water stratification, grazing

T., and Segawa S., 2009: Effects of the toxic

pressures, phytoplankton species, and strain

dinoflagellateinteractions is expected to affect the prevalence andthe valve movement behavior of the Manila clam

toxicity of HAB (Wellson., 2015). Changes in HAB, 291, 41-47.

prevalence and toxicity will affect the responses

Basti L., Endo M., and Segawa S., 2011a: Physiological,of shellfish to these global stressors as well as

pathological, and defense alterations inaquaculture activities. For instance, warming water

Manila clams (short-neck clams),

temperature has been shown to affect the metabolism, induced byof the most widespread HAB toxin (Paralytic Shellfish., 30, 829-844.

Toxins) in commercial oysters from Australia (Farrell

Basti L., Go J., Higuchi K., Nagai K., and Segawa., 2015). Similarly, increased temperatures andS., 2011b: Effects of the toxic dinoflagellate

OA were shown to increase production of HAB
toxins and negative effects in shellfish (Tatters., 2013; Basti., 2015b; Basti

on larvae of Pearloyster., 2018b). These(Dunker, 1873).
., 30, 177-186.

data show that climate-driven warming and OA

Basti L., Nagai K., Tanaka Y., and Segawa S., 2013:

may increase future risks of HAB effects on shellfish

Sensitivity of gametes, fertilization, and embryo

physiology and aquaculture farms.

development of the Japanese pearl oyster,, to the harmful
dinoflagellate,., 160, 211-219.

Leila BASTI, Kiyohito NAGAI, Susumu SEGAWA, Yuji TANAKA, Toshiyuki SUZUKI,
and Satoshi NAGAI

76

Basti L., Nagai S., Go J., Okano S., Nagai K., Watanabe

Caldeira K. and Wickett M. E., 2005: Ocean model

R., Suzuki T., and Tanaka Y., 2015a: Differential

predictions of chemistry changes from carbon

inimical effects ofdioxide emissions to the atmosphere and ocean.

spp. and

spp. on cleavage, hatching, and two larvalstages of Japanese pearl oyster110. doi:10.1029/2004JC002671
Cochran K., De Yo C., Soto D., and Bahri T., 2009:, 43, 1-12.

Climate change implications for fisheries andBasti L., Endo M., Segawa S., Shumway S. E., TanakaY., and Nagai S., 2015b: Prevalence and intensity

aquaculture, FAO Fisheries and Aquaculture
Technical Paper 530, Rome, 212pp.

of pathology induced by the toxic dinoflagellate,Compton T. J., Rijkenberg M. J. A., Drent J., and, in thePiersma T., 2007: Thermal tolerance ranges

Mediterranean mussel,and climate variability: a comparison between., 163, 37-50.

bivalves from differing climates.

Basti L., Nagai S., Watanabe S., Oda T., and, 352, 200-211.

Tanaka Y., 2016: Neuroenzymatic activity

Da Silva P.M., Hégaret H., Lambert C, Wikfors G. H.,

and physiological energetics in Manila clam,

Le Goïc N., Shumway S. E., and Soudant P., 2008:

Ruditapes philippinarum, during short-term

Immunological responses of the Manila clam

sublethal exposure to harmful alga, Heterocapsa() with varying parasite

circularisquama.

() burden, during long term., 176, 76-87.

Basti L., Hégaret H., and Shumway S. E., 2018a:
Harmful algal blooms and shellfish, in “Harmful

exposure to the harmful alga,
and possible interactions.

, 51, 563-573.

Algal Blooms: A Compendium Desk Reference”

Domingues C. M., Church J. A., White N. J., Gleckler(ed. by Shumway S. E., Burkholder J. M., and

P. J., Wijffels S. E., Barker P. M., and Dunn J.

Morton S. L.), John Wiley & Sons Ltd, Chichester,R., 2008: Improved estimates of upper-ocean

pp. 135-190.

warming and multi-decadal sea-level rise.

Basti L., Suzuki T., Uchida H., Kamiyama T., and,453, 1090-1093.

Nagai S., 2018b: Thermal acclimation affects

Doney S. D., Ruckelshaus M., Duffy J. E., Barry J. P.,

growth and lipophilic toxin production in a

Chan F., English C. A., Galindo H. M., Grebmeier

strain of cosmopolitan harmful alga

J. M., Hollowed A. B., Knowlton N., Polovina, 73, 119-128.

J., Rabalais N. N., Sydeman W. J., and Talley

Berge J. A., Bjerkeng B., Pettersen O., Schaanning
M. T., and Øxnevad S., 2006: Effects of increased
seawater concentrations of CO2 on growth of
the bivalve

L.

L. D., 2012: Climate change impacts on marine
ecosystems.

, 4, 11-37.

FAO, 2014: The State of World Fisheries and, 62,

Aquaculture - Opportunities and Challenges,

Bricelj V. M., Cembella A. D., Laby D., Shumway S. E.,

Farrell H., Seebacher F., O'Connor W., Zammit A.,

and Cucci T. L., 1996: Comparative physiological

Harwood D. T., and Murray S., 2015: Warmer

and behavioral responses to PSP toxins in two

temperature acclimation impacts metabolism

bivalve molluscs, the softshell clam,of paralytic shellfish toxins from681-687.

FAO, Rome, 223pp.

and surfclam,,, in “Harmful

and Toxic Algal Blooms” (ed. by Yasumoto T.,

in commercial oysters.
, 21, 3402-3413.

Oshima Y., and Fukuyo Y.), Intergovernmental

Gainey L. G. and Shumway S. E., 1988: A compendium

Oceanographic Commission of UNESCO, Paris,of the responses of bivalve molluscs to toxic

pp. 405-408.

dinoflagellates.

, 7, 623-628.

Burkholder J. M., 1998: Implications of harmful marine

Gazeau F., Quiblier C., Jansen J. M., Gattuso J.

microalgae and heterotrophic dinoflagellates inP., Middelburg J. J., and Heip C. H. R., 2007:

management of sustainable marine fisheries.

Impact of elevated CO2 on shellfish calcification.

, 8 (Suppl.), S37-S62.

, 34, L07603.

77

Environmental stressors to shellfish aquaculture
Haberkorn H., Lambert C., Le Goïc N., Guéguen M.,

of harmful algal blooms on shellfisheries

Moal J., Palacios E., Lassus P., and Soudant P.,

aquaculture, in “New Technologies in2010a: Effects of

exposure

Aquaculture: Improving Production Efficiency,

upon physiological and hematological variables of

Quality and Environmental Management” (ed. by

diploid and triploid oysters,

Brunell G. and Allan G.), CRC Press, Woodhead., 97, 96-108.

Publishing, pp. 580-609.

Haberkorn H., Lambert C., Le Goïc N., Moal J., Suquet

Miller A. W., Reynolds A. C., Sobrino C., and Riedel

M., Guéguen M., Sunila I., and Soudant P., 2010b:

G. F., 2009: Shellfish face uncertain future in highEffects of

exposure on

nutrition-related processes and reproductive

CO2 world: influence of acidification on oyster
larvae calcification and growth in estuaries.
, 4, e5661. doi:10.1371/journal.pone.0005661

output in oysters

Moore S. K., Trainer V. L., Mantua N. J., Parker M. S.,, 9, 427-439.
Hallegraeff G. M., 1993: A review of harmful algal

Laws E. A., Backer L. C., and Fleming L. E., 2008:

blooms and their apparent global increase.

Impacts of climate variability and future climatechange on harmful algal blooms and human, 32, 79-99.
Harley C. D. G., Hughe A. R., Hultgren K. K., Miner

health.

, 7 (Suppl. 2), S4.

B. G., Sorte C. J. B., Thronber C. S., Rodriguez

Parker L. M., Ross P. M., and Oʼ Connor W. A., 2009:

L. F., Tomanek L., and Williams S. L., 2006: The

The effect of ocean acidification and temperature

impacts of CC in coastal marine systems.

on the fertilization and embryonic developmentof the Sydney rock oyster., 9, 228-241.
Hégaret H. and Wikfors G. H., 2005: Time-dependent(Gould 1850).

, 15, 2123-2136.

changes in hemocytes of eastern oysters,

Rogers A. D. and dʼA Laffoley D., 2011: International, and northern bay scallops,

Earth system expert workshop on ocean stresses, exposed toand impacts, Summary report, IPSO, Oxford,
18pp.

cultured strain of

Ruckelshaus M., Doney S. C., Galindo H. M., Barry J.

, 2, 187-199.
Hégaret H., Smolowitz R. M., Sunila I., Shumway

P., Chan F., Duffy J. E., English C. A., Gaines S.

S. E., Alix J., Dixon M., and Wikfors G. H.,

D., Grebmeier J. M., Hollowed A. B., Knowlton N.,

2010: Combined effects of parasite, QPX, andPolovina J., Rabalais N. N., Sydeman W. J., andthe harmful-alga,

Talley L. D., 2013: Securing ocean benefits foronsociety in the face of climate change.

northern quahogs,.

,

40, 154-159.

., 69, 337-344.
Hégaret H., Brokordt K. B., Gaymer C. F., Lohrmann

Scavia D., Field J. C., Boesch D. F., Buddemeier R. W.,

K. B., García C., and Varela D., 2012: Effects of

Burkett V., Cayan D. R., Fogarty M., Harwell M.

the toxic dinoflagellate

A., Howarth R. W., Mason C., Reed D. J., Royer T.

on histopathogical and escape responses ofC., Sallenger A. H., and Titus J. G., 2002: Climate

the Northern scallopchange impacts on US coastal and marine
ecosystems.

18, 74-83.
IPCC, 2007: Climate Change 2007: Mitigation of
Climate Change. Working Group III Contribution

Shumway S. E., 1990: A review of the effects of algal
blooms on shellfish and aquaculture. .
.

to the Fourth Assessment Report of theIntergovernmental Panel on Climate Change,., 21, 65-104.

Shumway S. E. and Cucci T. L., 1987: The effect of thetoxic

UNEP, Geneva.
Landsberg J. H., 2002: The effects of harmful algal
blooms on aquatic organisms.

, 25, 149-164.

., 10,

113-390.
Matsuyama Y. and Shumway S. E., 2009: Impacts

and behavior of bivalve molluscs.

on the feeding.

.,

10, 9-27.
Smayda T. J., 1990: Novel and nuisance phytoplankton
blooms in the sea: evidence for a global epidemic,

Leila BASTI, Kiyohito NAGAI, Susumu SEGAWA, Yuji TANAKA, Toshiyuki SUZUKI,
and Satoshi NAGAI

78

in “Toxic Marine phytoplankton: Proceedings of

distributions of two genera of harmful algae inthe 4th International Conference on Toxic Marine

coastal ecosystems of three regions of the globe

Phytoplankton” (ed. by Granéli E., Sundström

were examined. Range expansions and retractions

B., Edler L., and Anderson D. M.), Elsevier, New

were found for the two genera suggesting future

York, pp. 29-40.

shifts in the vulnerability of coastal ecosystems

Talmage S. C. and Gobler C. J., 2010: Effects of

to HAB events, increased regional HAB impacts

past, present and future ocean carbon dioxideon aquaculture leading to increase in the risks toconcentrations on the growth and survival of

human health and ecosystem services and associatedlarval shellfish.

economic consequences.

.

.

.

.

, 107,

17246-17251.
Tatters A. O., Flewelling L. J., Fu F., Granholm A.

(2) Basti L., Endo M., Segawa S., Shumway S.

G., and Hutchins D. A., 2013: High CO2 promotes

E., Tanaka Y., and Nagai S., 2015: Prevalence

the production of paralytic shellfish poisoning

and intensity of pathology induced by the toxic

toxins byfrom Southern

dinoflagellate,

California waters.

, 30, 37-43.

Mediterranean mussel,

Trujillo P., Piroddi C., and Jacquet J., 2012: Fish farms
at sea: the ground truth from Google Earth.
, 7, e30546.

, 163, 37-50.
The study examines the effects of temperatureon the pathologies induced by the shellfish-killing

Van Dolah F. M., 2000: Marine algal toxins: origin,health effects, and their increased occurrence.
.

, in the., 108, 133-141.

harmful alga,, in theMediterranean mussel,.

The study shows that increased temperature leads

Waldbusser G. G., Voigt E. P., Bergschneider H., Green

to increased prevalence and intensity of pathologies

M. A., and Newell R. I. E., 2011: Biocalcificationin the mussels in several vital organs, includingin the Eastern Oyster Crassostrea virginica ingills and intestines. The study shows that warming

relation to long-term trends in Chesapeake Bay

temperature may increase the effects of the harmfulpH.

., 34, 22-231.

alga on mussels even at low cell density, possibly

Wells M. L., Trainer V. L., Smayda T. J., Karlson B. S.

.

reducing the overall health of the mussels. It alsoO., Trick C. G., Kudela R. M., Ishikawa A., Bernard

shows that the range expansion of the harmful alga

S., Wulff A., Anderson D. M., and Cochlan W. P.,

associated with increased winter water temperature

2015: Harmful algal blooms and climate change:

may put bivalve aquaculture farms under further

Learning from the past and present to forecast

risks of mass mortalities and production failure.

the future.

, 49, 68-93.

Zingone A. and Enevoldsen H. O., 2000: The diversity(3) Filgueira R., Guyondet T., Comeau L. A., andof harmful algal blooms: a challenge for science

Tremblay R., 2016: Bivalve aquaculture-environment

and management.

interactions in the context of climate change.

.

., 43, 725-

748.

, 22, 3901-3913.
The study examines the interactions between
Annotated bibliography

bivalve aquaculture and the environment (baygeomorphic type, freshwater input), in the context(1) Glibert P. M., Allen J. I., Artioli Y., Beusen A.,

of climate change (sea level rise, temperature,

Bouwan L., Harle J., Holmes R., and Holt J., 2014:

precipitation). Based on a factorial deign of 336

Vulnerability of coastal ecosystems to changes inscenarios, the modeling showed that temperature isharmful algal bloom distribution in response to

the strongest climate change driver to affect bivalve

climate change: projections based on model analysis.

aquaculture as it can influence their metabolism.

, 20, 3845-3858.

Differences in thermal tolerance of the cultured

Using a global modeling approach, the effects ofnutrient loading and climate change on the projectedbivalve species would determine “winners” from“losers”.

79

Environmental stressors to shellfish aquaculture

North Atlantic and North Pacific oceans using high(4) Gobler J. C., Dohrty O. M., Hattenrath-Lehmann T.

resolution SST (sea surface temperature) over theK., Griffith A. W., Kang Y., and Litaker R. W., 2017:

past three decades. Increasing water temperature

Ocean warming since 1982 has expanded the niche

associated with climate change have expanded theof toxic algal blooms in the North Atlantic and Northniches of these toxic algae (Pacific oceans.

, 114, 4975-

4980.

and

) and might contribute toan expansion of the associated human health threat

The study models the trends in growth rates andvia the consumption of shellfish contaminated withduration of bloom seasons of two species of the mostdiarrheic shellfish poisoning (DSP) and paralytic

toxic and widespread harmful algal blooms in theshellfish poisoning (PSP).

水 研 機 構 研 報， 第 49 号，81 − 95， 平 成 31 年
Bull. Jap. Fish. Res. Edu. Agen. No. 49，81−95，201981

Defining an ecosystem approach to aquaculture (EAA)
for federal waters of the United States
Katherine A. McGRAW＊ and Michael B. RUST

Abstract: The increase in world population, along with increased demand for seafood as a source ofhuman nutrition, and stagnant wild fisheries catches, will necessitate the growth and diversificationof marine aquaculture globally. However, marine aquaculture development in many countries,
including the United States, lags behind that of freshwater aquaculture. The United States (U.S.),
despite having the worldʼs largest Exclusive Economic Zone (EEZ), imports about 90 percent of theseafood consumed domestically (by value). One solution to the seafood import deficit is to pursue thedevelopment of marine aquaculture including offshore aquaculture in the EEZ, also known as federalwaters.
Various laws and regulations give the National Oceanic and Atmospheric Administration (NOAA)
oversight of fisheries in federal waters. NOAAʼs National Marine Fisheries Service (NMFS) has longrecognized the importance of implementing ecosystem-based fisheries management in order toexplicitly account for environmental changes and make trade-off decisions for actions that affectmultiple species; however, this approach needs to be investigated for American aquaculture. In
many respects, US marine aquaculture may already be managed with an ecosystem approach owing
to the various environmental laws which underlie its regulation and management.
If marine aquaculture is to grow in accordance with US laws and social values there need to be
guidelines and a framework for this effort, just as there is for capture fisheries. In order to benefit
from marine aquaculture opportunities that are in line with these laws and values, the NOAA Officeof Aquaculture is exploring an Ecosystem Approach to Aquaculture (EAA). The NOAA EAA isbased on the definition of Ecosystem Based Fishery Management as defined under the US fisheries
laws (Magnuson-Stevens Act). This exercise may also serve to guide research, and as the first stepin articulating a more detailed approach for implementation of ecosystem-based management ofmarine aquaculture. This paper provides an overview of NOAAʼs Ecosystem Approach to
Aquaculture, including a definition of EAA, rationale for development of the document, and some ofthe expected benefits of EAA.
Key words: ecosystem approach, offshore aquaculture, federal waters

Introduction

seabass, and seabream (Fig.1). Marine aquaculture
production has incrementally increased in bothMarine aquaculture as it is now practiced in othervolume and value since 2009. Marine aquaculture

countries, is a relatively recent development in the

production in 2015 was 96.6 million pounds, a 6.6 %United States (Knapp and Rubino, 2016). The top

increase over 2014 production and a $7.9 million (2.1

marine species cultured and harvested in the US are:%) increase in value (NOAA, 2017).

oysters, clams, mussels, shrimp, and salmon (NOAA,

There is a huge potential to increase and expand2017); and much lesser amounts of yellowtail, moi,

marine aquaculture globally and in the US. In their

2018年８月31日受理（Accepted on August 31, 2018）NOAA Office of Aquaculture 1315 East-West Hwy, Silver Spring, MD 20910, U. S. A.
E-mail: Kay.McGraw@noaa.gov＊

82

Katherine A. McGRAW and Michael B. RUST

Fig. 1. U.S. Aquaculture production statistics for 2015. (NOAA, 2017). (2017),

allows for the production of more seafood, while also

. (2018) found that, even with many

protecting native species, maintaining a healthy,

constraints, there are vast areas in the worldʼs oceans

productive, and resilient ecosystem, fish habitats, andthat are suitable for offshore marine aquaculture. For

a viable seafood industry. One option to account for

example, Gentry. (2017) estimated that marine

the attainment of such diverse goals may be initiatedaquaculture could produce the equivalent of current

through the articulation of an Ecosystem Approachwild-capture fisheries using less than 0.015 % of theto Aquaculture (EAA).

studies, Kapetsky
and Oyinlola. (2013), Gentry

global ocean area ‒ a “surface area less than Lake
Michigan”. Kapetsky. (2013) also calculated that

What is an ecosystem approach to aquaculture?

most countries would only need to have aquaculture
in less than 1 % of their EEZ to produce all the seafood

Based on a similar NOAA definition for an

they currently require. In the U.S., production could be

Ecosystem Approach to Fisheries, we define anvastly increased by utilizing more offshore, or federal,

Ecosystem Approach to Aquaculture as follows:

waters (Kapetsky., 2013). Indeed, there are

An ecosystem approach to aquaculture is amany factors driving the development and expansion

systematic method of managing aquaculture that:of marine and offshore aquaculture1, as explained• is in a geographically specified area;

below. However, doing this in an environmentally• contributes to the resilience2 and sustainability3 ofsound and sustainable way requires a balance that
1

2

3

4

the ecosystem4;“Offshore Aquaculture may be defined as taking place in the open sea with significant exposure to wind and wave action, and where there isa requirement for equipment and servicing vessels to survive and operate in severe sea conditions from time to time. The issue of distancefrom the coast or from a safe harbor or shore base is often but not always a factor” (Drumm, 2010).
Resilience can be defined as the capacity of a(n) (eco)system to persist or maintain function in the face of exogenous disturbances. That is, thecapacity of an ecosystem to tolerate disturbance (e.g., such as intensive fishing) without collapsing into a different state that is controlled by adifferent set of processes. This is primarily encapsulated by two elements, resistance to and recovery from pressure (NOAA, 2016).
FAO defines sustainability (as synonymous with sustainable development) as “the management and conservation of the natural resource baseand the orientation of technological and institutional change in such a manner as to ensure the attainment and continued satisfaction of humanneeds for present and future generations. Such sustainable development (in the agriculture, forestry and fisheries sectors) conserves land,
water, plant and animal genetic resources, is environmentally non‐degrading, technically appropriate, economically viable and sociallyacceptable” (Welcomme and Barg, 1997)
In the NOAA Fisheries context, the term “ecosystem” means a geographically specified system of fisheries resources (including aquaculture),
the persons that participate in that system, the environment, and the environmental processes that control that ecosystemʼs dynamics(Murawski and Matlock, 2006). Aquaculturists, fishermen and the associated support communities are understood to be included in thedefinition.

83

Ecosystem Approach to Aquaculture• recognizes the physical, biological, economic, andsocial interactions among the affected aquaculturerelated components of the ecosystem, including
humans;• seeks to optimize benefits within a diverse set ofenvironmental and social constraints;” (Mizuta and Vlachopoulou, 2017).

• is adaptive over time.
Our definition of EAA adheres closely to somePurposeothers, such as that of the Food and Agriculture
Organization (Soto., 2008a), which defines EAA

as follows: “The purpose of this paper is to articulate
principles of marine aquaculture development andactivity within the context of the National Oceanicand Atmospheric Administrationʼs (NOAAʼs)
multiple stewardship missions and broader social,”.

environmental and economic goals. Meeting thisOur EAA definition fits within this more generalobjective will help NOAA to integrate environmental,

FAO definition, and is consistent with the specificsocial, and economic considerations in management

mandates and guidelines in the U.S.ʼs aquaculture

decisions concerning aquaculture. The EAA will alsolaw (National Aquaculture Act [NAA]) and fisheries

serve to reaffirm that aquaculture is an importantlaw (Magnuson-Stevens Fishery Conservation

component of NOAAʼs efforts to maintain healthy

Act [MSA]). It also respects other environmental

and productive marine and coastal ecosystems whilelaws under which the US operates and manages

providing seafood. Implementation of the EAA

aquaculture to fulfill its mission (see the section on

involves balancing competing uses of the marine“Major Laws” below for more information on these).

environment, creating employment and business

EAA includes considerations of interactions among

opportunities in our communities, and enabling theaquaculture, fisheries, protected species, habitats,production of safe and sustainable seafood.

and other ecosystem components, including thehuman communities that depend upon them andWhy have an ecosystem approach to aquaculture?

their associated ecosystem services. EAA examines
not only the broader suite of factors that affectAlthough aquaculture is considered a “fishery”

aquaculture efforts, but also considers the potential

under the US fisheries law (MSA), marine

impacts (positive and negative) of aquaculture on

aquaculture is also farming and adheres to all theother parts of the ecosystem (e.g., on nutrients,

other environmental laws and regulations pertaining

plankton, fish species, habitats, marine mammals

to all marine activities and all farming activities. A

and so on). “Societal goals” consider and include any

separate ecosystem approach is needed for marine

relevant economic, social, and other factors valued byaquaculture because it differs from capture fisheriessociety in the context of, or relating to aquaculture.

in several important structural aspects. First of

EAA is cognizant of both human and ecologicalall, the potential impacts from aquaculture on wild

considerations and seeks to optimize returns to bothfisheries stocks are indirect5 (habitat, stress, genetics),

as much as possible. This is an attempt to create

while capture fishing deals with direct (harvest)

a common framework that leads to ecosystem

and indirect impacts (habitat destruction, genetic

resiliency.

impacts, stress and so on). Some of the indirect effects

In many ways EAA is similar to the Japaneseconcept of “

5of aquaculture can be managed to be positive andproduce enhanced environments for wild stocks andNone of these directly remove members of wild populations from the ecosystem. This is in contrast to harvest from wild capture where thewhole point is to remove members of the wild populations from the ecosystem.

84

Katherine A. McGRAW and Michael B. RUST

other forms of aquaculture. For example, nutrients

extractive. It is time to define a NOAA ecosystemin the marine environment either provided by, or

approach for aquaculture ‒and explore the same way

taken up by, aquacultured organisms can be usedof thinking the agency has advocated with regard toto mitigate oligotrophication or eutrophication,

capture fisheries and other NOAA efforts.

respectively. Aquaculture structures can be
designed to provide habitat. Hatcheries may produce

Major laws and mandates governing aquaculture inorganisms for release to rebuild wild stocks. Second,the USthe management options for marine aquaculture are
greater, and of a different nature than for fisheries.

US marine aquaculture is arguably already

The main control for wild fisheries is management

managed with an ecosystem approach owing to theof harvest and habitat. Control over the harvestableenvironmental laws which underlie its regulation

biomass in wild fisheries is largely by acts of nature.

and management (Table 1). There are laws in theControl over the harvestable biomass in aquaculture

United States that compel NOAA to manage marine

is much more in the hands of people. Recruitment

fisheries and aquaculture so that the environment is

in aquaculture is controlled by a hatchery, but

considered and impacts minimized. Two of these areeven more so, the quality of recruits in terms of

the Magnuson-Stevens Act6 (MSA) and the National

growth and survival to harvest are determined by

Aquaculture Act (NAA). In terms of ecologicalgenetics, nutrition, environmental conditions andconsiderations, the MSA essentially states that

husbandry, which are all at least partially under thefisheries will be managed in a way that:

control of humans. Because of the greater number• integrates ecosystem considerations into fisheryand diversity of control points, the application of an
ecosystem approach to aquaculture is more complex
and differs in priorities from an ecosystem approachconservation and management actions,• minimizes the impacts of fishing on ecosystemcomponents, and• conserves important ecosystem components fromto fisheries.
For NOAA, this is not a new way of thinking, but

non-fishing threats.

just the adaptation of an ecosystem approach to a

Similarly, the National Aquaculture Act (NAA)

different endeavor that is not specifically resource

dictates that aquaculture will be conducted to:• promote and support the development of privateaquaculture;

Tables 1. Federal permits required for offshore
aquaculture operations in federal waters of the Gulf
of Mexico7• promote coordination among the various federal
agencies that have aquaculture programs andpolicies;

AgencyStatutes/Authorities

PurposeU.S. Army Corps ofEngineers(USACE)

Section 10 of theRivers and Harbors
Act and some
sections of Clean
Water Act

Required in navigable
waters of the U.S. toprotect navigation forcommerce

National Oceanicand Atmospheric
Administration(NOAA)

Magnuson- Stevens
Required forFishery Conservation operating offshore
and Management Act aquaculture facility in(Magnuson- Stevens Federal waters of theAct)
Gulf and other areasof federal waters

to enhance and restore species. The NAA isU.S.
Environmental
Protection
Agency(EPA)

Sections 402 and 403
of the Clean Water
Act

U.S. Department of Commerce (of which NOAA is a6

7

Required forthe discharge ofpollutants into watersof the U.S.

• Provide a legal mandate for NOAA Fisheries
to support the development of the U.S. marine
aquaculture industry.
The NAA also allows for the use of aquaculture
primarily administered by the U.S. Departmentof Agriculture (USDA), which is the lead Federal
agency for aquaculture in the U.S., along with thepart) and the U. Department of the Interior. NOAA
is specifically directed to support the development of

Although the term “aquaculture” is not mentioned specifically in the MSA, NOAA has a legal opinion that equates aquaculture to fisheries;
therefore, aquaculture endeavors in federal waters are also required to follow the same standards.
In the Gulf of Mexico, federal waters begin at 3 nautical miles from shore in Louisiana, Mississippi and Alabama and 9 nautical miles fromshore in Texas and Florida, and extend to approximately 200 nautical miles from the coast. (NOAA, 2017)

85

Ecosystem Approach to Aquaculture
the U.S. marine aquaculture industry, an increasingly
important economic component of marine ecosystems,
and use of aquaculture to enhance and restore

Tables 2. Federal authorizations required for offshore
aquaculture operations in federal waters of the Gulf
Agencyspecies for commercial, recreational and restoration
purposes. In addition, some types of aquaculture inCouncils.
In addition to the MSA and the NAA, there aremany other statutes and authorities that govern

U.S. Coast Guard(USCG)

33 U.S.C. 1221
33 CFR §66

1 - 3. Taken together, these laws, along with other

Ensure safe
navigation Authorize
Private Aids toNavigation

Authorizations for Aquaculture Operations Co-Located with OCS
Outer Continental
Bureau of Ocean
Energy Management Shelf Lands Act;
Energy Policy Act of(BOEM)
2005; 30 CFRmarine aquaculture permits and operations in the
U.S. Some of the federal laws are listed in the Tables

PurposeAuthorizations

federal waters are regulated under MSA in the Gulf
of Mexico, and are under consideration by other

Statutes/Authorities

Bureau of Safety
and Environmental
Enforcement (BSEE)

Required for any
offshore aquaculture
operations that utilize
or tether to existing
oil and gas facilities

Outer Continental
Shelf Lands Act

regulations, enable federal oversight and enforcement
to help protect the marine environments and thebiota inhabiting them (e.g., endangered species, fishbuild and operate aquaculture facilities in coastal andand wildlife, and essential fish habitat). Others pertain

federal waters must go through an arduous process,to navigation and fossil fuel extraction activities, as

designed primarily to protect the environment, towell as historic and cultural artifacts.

obtain them. Once their projects are operational, theyIn addition to these federal laws, individual states

must still adhere to federal and state laws governingand local government within states may also havewater pollution, threatened and endangered species,

others that are applicable to state waters.

marine mammals (i.e., entanglement in gear), and

The Coastal Zone Management Act (CZMA) was

others. This legal landscape helps ensure thatpassed by Congress in 1972 and is administeredaquaculture in U.S. marine waters is conducted inby NOAA. It provides for the management of theaccordance with the environmental aspects of thenationʼs coastal resources, including the Great Lakes.

principles of an ecosystem approach to aquaculture.

The goal is to “preserve, protect, develop, and where

The current system does not consider broad

possible, to restore or enhance the resources of thescale social and economic considerations in permit

nationʼs coastal zone.”decisions for aquaculture. An EAA might help to

One of the programs of the CZMA is the National
Coastal Zone Management Program (NCZMP), which

provide for a more diverse set of considerations inpermit decisions.

comprehensively addresses the nationʼs coastal issues
through a voluntary partnership between the federal

What are some of the benefits of EAA?

government and coastal and Great Lakes states
and territories. The program provides the basis for

As interest in aquaculture in the U.S. has increased,

protecting, restoring, and responsibly developing theso too has the debate about the potential economic,

nationʼs diverse coastal communities and resources.

environmental, and social effects of aquaculture.

Currently 34 coastal states participate in the

There are environmental challenges posed by

NCZMP. While state partners must follow basic

aquaculture when it is done poorly (e.g., habitat

requirements, the program also gives states thedestruction, excess nutrient discharges, water

flexibility to design unique programs that bestuse demands, invasive species, genetic impacts

address their coastal challenges and regulations.

and effects on protected species). There are also

By leveraging both federal and state expertise andsocioeconomic challenges, for example, competition

resources, the program strengthens the capabilities offor the use of marine space and potential effects

each to address coastal issues, including aquacultureof increased aquaculture production on prices ofactivities.

wild caught fish. However, aquaculture practiced inThus, aquaculturists wishing to obtain permits toconsideration of the ecosystem can result in many

86

Katherine A. McGRAW and Michael B. RUST

Tables 3. Required federal consultations and reviews. Agencies with permitting decisions for aquaculture facilities
including NOAA, EPA and USACE, will apply the relevant and applicable provisions of the laws identified below
to their federal actions. Many of these consultations and reviews may occur in tandem with the permit application
review process
Consultation or
Review

Description of the Requirement

Endangered
Species Act

Section 7 of the Endangered Species Act (ESA) requires any federal agency that issues a permit toconsult with NOAAʼs National Marine Fisheries Service (NMFS) and/or the U.S. Fish and Wildlife
Service (USFWS),
issuance of the permit may adversely affect ESA- listed species and/or thedesignated critical habitat for ESA-listed species. The Section 7 consultation process requires ananalysis of the effects of the proposed action on ESA-listed species and designated critical habitat
based on the best available science. The analysis must determine if the proposed action is likely
adversely affect an ESA-listed species and/or designated critical habitat. If the analysis determines theissuance of a proposed permit will adversely affect an ESA-listed species, but will not jeopardize its
continued existence, then reasonable and prudent measures and implementing terms and conditions
that minimize the adverse impacts must be developed.

Essential Fish
Habitat

The Essential Fish Habitat (EFH) provisions of the Magnuson-Stevens Act requires federal agencies
to consult with NMFS when activities they undertake or permit have the potential to adversely affect
EFH.

National HistoricPreservation Act

Section 106 of the National Historic Preservation Act (36 CFR Part 800) requires any federal agency
issuing a permit to account for potential effects of the proposed aquaculture activity on historic
properties,, shipwrecks, prehistoric sites, cultural resources. If a proposed aquaculture activity has
the potential to affect historic properties these details must be provided by the applicant as part of
the application packages.

Fish and Wildlife
Coordination Act

The Fish and Wildlife Coordination Act requires any federal agency issuing permits to consult with
USFWS and NMFS if the proposed aquaculture activities could potentially harm fish and/or wildlife
resources. These consultations may result in project modification and/or the incorporation of measures
to reduce these effects.

National Marine
Sanctuary
Resources Act

Section 304(d) of the National Marine Sanctuaries Act (NMSA) requires that any federal agency
issuing permits to consult with NOAAʼs National Marine Sanctuary Program (NMSP) if the proposed
aquaculture activity is likely to destroy or injure sanctuary resources. As part of the consultation
process, the NMSP can recommend reasonable and prudent alternatives. While such recommendations
may be voluntary, if they are not followed and sanctuary resources are destroyed or injured in thecourse of the action, the NMSA requires the federal action agency(ies) issuing the permit(s) to restore
or replace the damaged resources.

environmental, economic, and social benefits while“characteristic of resources that are managed so thatavoiding the challenges listed above.

the natural capital stock is non-declining throughtime, while production opportunities are maintained

Resilience and sustainability

for the future. Fishing is sustainable when it can

Aquaculture can contribute to the resilience andbe conducted over the long-term at an acceptablesustainability of seafood. NOAA defines resiliencelevel of biological and economic productivity

as the capacity of a system to persist or maintainwithout leading to ecological changes that foreclosefunction in the face of exogenous disturbances.

options for future generations” (Sutinen

That is, the capacity of an ecosystem to tolerate

Blackhart

disturbance without collapsing into a different state

applies to aquaculture, but is not a perfect fit due tothat is controlled by a different set of processes. Thisaquacultureʼs ability to scale with seafood demandis primarily encapsulated by two elements: resistanceversus capture fisheriesʼ dependence on a fixed

to, and recovery from, pressure. (NOAA, 2016)supply. There is no “natural capitol stock” to manage.

NOAA defines fisheries sustainability as a., 2000;., 2006). This definition somewhat

The World Bank (The World Bank 2014) puts it this87

Ecosystem Approach to Aquaculture
way:…

More efficient use of resources and feed
Aquaculture is one of the most efficient agricultural•̶systems, and is typically better than terrestrial
farming in terms of feed conversion (Hall., 2011;

Brummett, 2013), greenhouse gas emissions, land use,energy efficiency and freshwater use (Nijdam
•

̶

.,

2012). Aquaculture as practiced in the US provides
food at a smaller global environmental cost than•̶

agriculture, while developing an EAA could produce
this food with even a smaller negative environmental
cost, or potentially while providing environmental
benefits.
Restoration• Aquaculture plays a prominent role in restoring
populations of marine fish and shellfish. Hatcheries
provide organisms to rebuild oyster reefs (Fig.2),
coral reefs (Fig.3), enhance wild fish populations(e.g., salmon, red drum, flounder), and rebuild
populations that are threatened or endangered (e.g.,salmon and abalone, Fig.4).
• Fish hatcheries have long been used to augment
both freshwater and marine fish populations. Manysalmon runs in the U.S. are supplemented bysalmon hatcheries in an effort to rebuild natural
salmon populations that have declined due tovarious limits to natural recruitment, or to provide
catch in excess of what would be available naturally

Fig. 2. Example of Olympia oyster (Ostrea lurida
Carpenter 1864) restoration plot in Puget Sound, WA.
(Photo credit: NOAA Fisheries)

Fig. 3. A diver surveys coral pieces being cultured forcoral reef restoration. (Photo credit: NOAA Fisheries).

Fig. 4. Two month old white abalone larva cultured
in a hatchery. Photo credit: Kristin Aquilino, NOAA

88
(Hess

Katherine A. McGRAW and Michael B. RUST., 2012). In addition, aquaculture can be

and vegetation along shorelines and help prevent

used to restore physical and ecosystem function.

erosion. In some subtidal oyster reef restoration

For example, one use of hatchery-reared oysters

projects, hatchery-reared oysters are placed as anin the U.S. is in the creation of “living” or “green”

outer layer on mounds of clean shell (Fig.6).

shorelines to reduce erosion and wave action invulnerable coastal areas (Fig.5). In these projects,

Ecosystem services

oyster reefs are built using hatchery-reared oysters

There is growing recognition of the ecosystem(set on shell) in conjunction with seagrass orservices provided by aquaculture in the U.S. andsubmerged aquatic vegetation (SAV), marsh grass,other countries. Restoration practitioners haveand sometimes other structures to increase habitat

increasingly pursued bivalve, sea grass and kelp
restoration as a component of restoring historicalbaseline water quality conditions and functioning of
ecosystems (Rice, 2000). For example, restoration ofoyster reefs (Fig.7) can restore water clarity, help
reduce phytoplankton blooms caused by excess
nutrient loading and decrease turbidity (Everett., 1995; Carroll., 2008). Like bivalves, seaweedalso removes and sequesters carbon and nitrogen;and the structures of all types of aquaculture (cages,
ropes, buoys, rafts, etc.) may provide habitat foraquatic animals (North, 1987; Phillips, 1990; Zhen-hua
and Wei-ding, 2007).
Aquaculture of filter feeders (e.g., oysters andmussels) and macro-algae can enhance resilience ofthe estuarine ecosystem to eutrophication (Jackson., 2001; Lotze
habitat functions. (Carroll., 2006) and help enhance., 2008; Wall., 2008).

Conversely, much of the ocean is oligotrophic, andthe addition of nutrients from fed aquaculture in
Fig. 5. Volunteers restoring marsh grass in a coastal“living shorelines” restoration project. (Photo credit:
NOAA Fisheries)

Fig. 6. Rock Point Oyster Company Shellfish Farm in
Quilcene, WA. (Photo credit: Jenifer Rhoades, NOAAIOOS Program). Bagged spat on shell like this canalso be used in oyster restoration as well as living
shoreline restoration projects.

these types of areas may lead to enhanced ecosystemservices, biodiversity, and greater resiliency (Machias

Fig. 7. Oyster reef in the southeast U.S. (Photo credit:
NOAA Fisheries)

Ecosystem Approach to Aquaculture

89

Fig. 8. Flounder in seagrass bed. (Photo credit:
NOAA Fisheries)., 2004; Machias., 2005; Diana, 2009). There

has been much work on attempting to balance
nutrient inputs from fed aquaculture with nutrient

Fig. 9. Collection of white anemones (Metridium
senile) and other diverse invertebrates on a walkway
float of a net pen in Puget Sound, Washington.
(Photo credit: Jack Rensel, Rensel Associates Aquatic
Sciences, Arlington, WA)

extraction by filter feeders and macro-algae on a
local scale (Chopin., 2001; Chopin, 2008;.,leases were similar to seagrass habitat. Overall the2009; Chopin, 2015). This approach has been calledbiogenic habitat created by the aquaculture gear

Integrated Multi-Trophic Aquaculture (IMTA). EAA

was more diverse than without the gear (Fig.8). In

benefits from the mass balance nutrient relationships

addition, Rensel and Forster (2007) surveyed fish net

illuminated by IMTA studies, but differs bypens in Puget Sound, Washington to quantify theconsidering the nutrient (trophic) background oftypes and volumes of biofouling organisms and foundthe host environment and its ability to benefit fromthat the typical net pen system there was populated

additions or reductions in ambient nutrients fromby a diverse group of over 100 species of seaweeds

aquaculture at various ecosystem scales and under

and invertebrates, many of which are importantdifferent temporal patterns.

components of the food web (Fig.9). Some were also

Neori, 2008; Barrington., 2009; Troell

When marine organisms of all types are cultured

commercially important (e.g., mussels and kelp).

by using structures (long lines, cages, net-pens) the
structures themselves may also provide habitat andEconomic Sustainability

attachment surfaces for many other organisms such

The collapse of some fisheries, plus other economic

as ascidians, sponges, anemones, and mollusks. It is

and environmental factors (e.g., fleet consolidation,

well known that natural and enhanced oyster reefs

hurricanes) have resulted in a loss of jobs for someare habitat for many different species (Bahr andfishers and support industries in coastal areas

Lanier, 1981; Breitburg and Miller, 1998; Coen.,

involved in the seafood business. Aquaculture has., 1999). However, gear used in all

the potential to stimulate the economy in some

types of aquaculture may also provide similar habitat

locations by directly providing jobs in aquaculture,benefits. For example, Powers. (2007) foundand indirectly by servicing boats, seafood processing,that plastic mesh used in bottom clam culture hadmarketing, transportation, and other positions thatsignificantly greater macroalgal/epifaunal biomass

help keep and maintain working waterfronts (Rubino,

per unit than sandflats and were similar to that2008). For example, results of one modeling study

provided by natural seagrass. Also, the kinds ofpredict that the number of jobs created across all

invertebrates and juvenile fishes utilizing the clam

sectors per thousand metric tons of production per

1999; Posey

90

Katherine A. McGRAW and Michael B. RUST

year would be 102 jobs for mussels, 261 for salmon,
475 for cod, and 683 for scallops (Posadas, 2004).
When the development is properly scaled for thelocation and region, it can create entrepreneurial
opportunities that have a ripple effect in local
economies (Soto., 2008b).

Monitoring and adaptive management
Adaptive management (Fig.10) is “

” (Williams., 2009). It is a processthat allows for flexible decision making that takessome degree of uncertainty into consideration andadjusts actions and decisions to resolve the issue

Fig. 10. Conceptual diagram of the six-step adaptive
management cycle (adapted from Fig. 1.1 in Williams. (2009)).

or problem. The process improves understandingof a resource system and tests key assumptions
through monitoring. Monitoring and adaptive

approach to aquaculture is a systematic method ofmanagement are key to developing ecologicallymanaging aquaculture that: 1) is in a geographicallyresilient and sustainable aquaculture projects.

specified area, 2) contributes to the resilience andAdaptive management is a tool which should besustainability of the ecosystem, 3) recognizes theused not only to change a system, but also to learn

physical, biological, economic, and social interactions

about the system. Because adaptive management

among the affected aquaculture-related components

is based on a learning process, it improves long-of the ecosystem, including humans; 4) seeks toterm management outcomes. In this way, decision

optimize benefits among a diverse set of societal

making simultaneously meets one or more resource

goals and 5) is adaptive over time. The stage is set

management objectives and, either passively or

for an ecosystem approach to aquaculture to flourish

actively, accrues information needed to improvein the US. The current small US marine aquaculture

future management (Holling, 1978).

industry is an example of where EAA is alreadyguiding responsible and sustainable development.

Conclusion

EEA principles are being used in the US, but not asa management paradigm and the use of EEA tools is

NOAAʼs National Marine Fisheries Service has

not widely recognized.

long recognized the importance of implementing

Many factors affecting the success of marine

ecosystem-based fisheries management in orderaquaculture in the US are unknown; however, Knappto explicitly account for environmental changes(2008) cites several examples of offshore aquaculture

and make trade-off decisions for actions that affectventures that indicate a bright future for aquaculture

multiple species; however, this approach has not

expansion in the U.S. There is increasing interest

been applied specifically to aquaculture. If marine

in, and need for, a more robust marine aquaculture

aquaculture is to grow in accordance with societal

industry in the U.S., including finfish, seaweed,

values, there need to be guidelines and a framework

and bivalve farms. The impetus for aquaculture

for this effort, just as there are for capture fisheries.

expansion in the U.S., from both an economic and food

Based on a similar definition for an Ecosystem

sustainability perspective, has never been greater.

Approach to Fisheries, we define an Ecosystem
Approach to Aquaculture as follows: An ecosystem

91

Ecosystem Approach to Aquaculture
References37, 975-986.
Chopin T., Robinson S. M. C., Troell M., Neori A.,

Bahr L. M. and Lanier W. P., 1981: The ecology ofBuschmann A. H., and Fang J., 2008: Multitrophic

intertidal oyster reefs of the South Atlantic

integration for sustainable marine aquaculture,

coast: a community profile, US Fish and Wildlifein “The Encyclopedia of Ecology, Ecological

Service. U. S. Department of Interior, Washington

Engineering” (ed. by Jorgensen S. E. and Fath B.

D. C., 105pp.

D.), Elsevier, Oxford, pp. 2463-2475.

Barrington K., Chopin T., and Robinson S., 2009:

Coen L. D., Luckenbach M. W., and Breitburg D. L.,

Integrated multi-trophic aquaculture (IMTA)

1999: The role of oyster reefs as essential fishin marine temperate waters, in “Integrated

habitat: a review of current knowledge and somemariculture: a global review” (ed. by Soto D.),

new perspectives, in American Fisheries Society

FAO Fisheries and Aquaculture TechnicalPaper No. 529, FAO, Rome, pp. 7-46.

Symposium 22, pp. 438-454.
Diana J. S., 2009: Aquaculture Production andBlackhart K., Stanton D. G., and Shimada A. M.,

Biodiversity Conservation.

, 59, 27-38.

2006: NOAA Fisheries Glossary. NOAA

Drumm A., 2010: Evaluation of the promotion ofTechnical Memorandum NMFS-F/SPO-69,

offshore aquaculture through a technology

U.S. Department of Commerce, NOAA, Silver

platform (OATP), Marine Institute, Galway, 46pp.

Spring, 61 pp. An on-line version of this glossary

Everett R. A., Ruiz G. M., and Carlton J. T., 1995:

is available at: http://www.st.nmfs.gov/st4/

Effect of oyster mariculture on submerged

documents/F̲Glossary.pdf.

aquatic vegetation: an experimental test in a

Breitburg D. and Miller T., 1998: Are oyster reefs
essential fish habitat? Use of oyster reefs byecologically and commercially important species.
., 17, abstract only.

Pacific Northwest estuary.

.

.

.

.,

125, 205-217.
Gentry R. R., Froehlich H. E., Grimm D., Kareiva P.,
Parke M., Rust M., Gaines S. D., and Halpern B.

Brummett R., 2013: Growing aquaculture insustainable ecosystems, Agriculture andS., 2017: Mapping the global potential for marine
aquaculture.

.

.

., 1, 1317.

Environmental Services Department Notes, No.

Hall S. J., Delaporte A., Phillips M. J., Beveridge M.,

5, The World Bank, Washington D.C., Available

and OʼKeefe M., 2011: Blue frontiers: managing

at: http://documents.worldbank.org/curated/the environmental costs of aquaculture, The

en/556181468331788600/pdf/788230BRI0AES00

WorldFish Center, Penang, 92pp.

without0the0abstract.pdf.

Hess M. A., Rabe C. D., Vogel J. L., Stephenson J. J.,

Carroll J., Gobler C. J., and Peterson B. J., 2008:

Nelson D. D., and Narum S. R., 2012: Supportive

Resource-restricted growth of eelgrass in New

breeding boosts natural population abundanceYork estuaries: light limitation, and alleviation ofwith minimal negative impacts on fitness of anutrient stress by hard clams.

wild population of Chinook salmon.

., 369, 51-62.

.

., 21,

5236-5250.

Chopin T., 2015: Marine Aquaculture in Canada:

Holling C. S., 1978: Adaptive environmental

Well‐Established Monocultures of Finfish

assessment and management, John Wiley &and Shellfish and an Emerging Integrated

Sons, New York, 377pp.

Multi‐Trophic Aquaculture (IMTA) Approach

Jackson J. B., Kirby M. X., Berger W. H., Bjorndal K.

Including Seaweeds, Other Invertebrates, andA., Botsford L. W., Bourque B. J., Bradbury R.

Microbial Communities.

H., Cooke R., Erlandson J., and Estes J. A., 2001:, 40, 28-31.

Chopin T., Buschmann A. H., Halling C., Troell M.,
Kautsky N., Neori A., Kraemer G. P., Zertuche‐

Historical overfishing and the recent collapse ofcoastal ecosystems.

, 293, 629-637.

González J. A., Yarish C., and Neefus C., 2001:

Kapetsky J. M., Aguilar-Manjarrez J., and Jenness

Integrating seaweeds into marine aquacultureJ., 2013: A global assessment of offshore

systems: a key toward sustainability. .

mariculture potential from a spatial perspective,

.,

92

Katherine A. McGRAW and Michael B. RUSTFAO fisheries and aquaculture technical paper
No. 549, FAO, Rome., xvii + 181pp.

37, 760-770.
NOAA, 2016: National Marine Fisheries Servie Policy

Knapp G., 2008: Economic potential for US offshore

Directive 01-120: Ecosystem-based Managementaquaculture: an analytical approach, in

Policy of the National Marine Fisheries Service“Offshore aquaculture in the United States:(ed. by N. M. F. Service), NOAA, Silver Spring,

Economic considerations, implications and8pp. Available at http://www.nmfs.noaa.gov/op/

opportunities” (ed. by Rubino M. C.), NOAA

pds/index.html.

Technical Memorandum NMFS F/SPO-103, U.S.

NOAA, 2017: National Marine Fisheries Service

Department of Commerce, NOAA, Silver Spring,(2016), Fisheries of the United States 2016,

pp. 15-50.

NOAA Current Fishery Statistics No. 2016, U.S.

Knapp G. and Rubino M. C., 2016: The Political

Department of Commerce, NOAA, Silver Spring,

Economics of Marine Aquaculture in the United

134pp. Available at: https://www.fisheries.noaa.

States.

gov/resource/document/fisheries-united-states-., 24, 213-229.

Lotze H. K., Lenihan H. S., Bourque B. J., Bradbury R.

2016-report.

H., Cooke R. G., Kay M. C., Kidwell S. M., Kirby

North W. J., 1987: Oceanic farming of Macrocystis,

M. X., Peterson C. H., and Jackson J. B., 2006:

the problems and non-problems, in “Seaweed

Depletion, degradation, and recovery potential

Cultivation for Renewable Resources” (ed. byof estuaries and coastal seas.

Bird K. T. and Benson P. H.), Developments in, 312, 1806-

1809.

Aquaculture and Fisheries Sciences, Elsevier,

Machias A., Karakassis I., Giannoulaki M.,

Amsterdam, pp. 39-67.

Papadopoulou K., Smith C., and Somarakis S.,

Oyinlola M. A., Reygondeau G., Wabnitz C. C. C.,

2005: Response of demersal fish communities toTroell M., and Cheung W. W. L., 2018: Global

the presence of fish farms.

estimation of areas with suitable environmental

.

.

.

.,

288, 241-250.

conditions for mariculture species.

Machias A., Karakassis I., Labropoulou M., Somarakis, 13,e0191086.

S., Papadopoulou K., and Papaconstantinou C.,

Phillips M., 1990: Environmental aspects of seaweed

2004: Changes in wild fish assemblages after

culture, in “Regional Workshop on the Culture

the establishment of a fish farming zone in an

and Utilization of Seaweeds” (27-31 Aug, 1990),

oligotrophic marine ecosystem.

Cebu, pp. 27-31.

., 60, 771-779.

Posadas B. C., 2004: Potential economic impact of

Mizuta D. D. and Vlachopoulou E. I., 2017: Satoumi

commercial offshore aquaculture in the Gulf ofconcept illustrated by sustainable bottom-up

Mexico, Mississippi-Alabama Sea Grant College

initiatives of Japanese Fisheries Cooperative

Program publication number MASGP 04-036,

Associations.

, 78, 143-149.

Mississippi State University, Biloxi, pp. 1-21.

Murawski S. A. and Matlock G. C., 2006: Ecosystem

Posey M. H., Alphin T. D., Powell C. M., andscience capabilities required to support NOAAʼs

Townsend E., 1999: Use of oyster reefs as habitat

mission in the year 2020, NOAA Technicalfor epibenthic fish and decapods, in “Oyster reef

Memorandum NMFS-F/SPO-74, U.S. Department

habitat restoration: a synopsis and synthesis ofof Commerce, NOAA, Silver Spring, 97pp.

approaches” (ed. by Mann M. W. R. and Wesson

Neori A., 2008: Essential role of seaweed cultivation

J. A.), Virginia Institute of Marine Science Press,

in integrated multi-trophic aquaculture farms for
global expansion of mariculture: an analysis.
., 20, 567-570.
Nijdam D., Rood T., and Westhoek H., 2012: The

Gloucester Point, pp. 229-237.
Powers M. J., Peterson C. H., Summerson H. C., andPowers S. P., 2007: Macroalgal growth on bivalve
aquaculture netting enhances nursery habitat

price of protein: Review of land use and carbon

for mobile invertebrates and juvenile fishes.

footprints from life cycle assessments of animal., 339, 109-122.

food products and their substitutes.

Rensel J. and Forster J., 2007: Beneficial environmental

93

Ecosystem Approach to Aquaculture
effects of marine finfish mariculture, Final

Troell M., Joyce A., Chopin T., Neori A., Buschmann

Report to the National Oceanic and AtmosphericA. H., and Fang J.-G., 2009: Ecological engineering

Administration, #NA040AR4170130, Washington

in aquaculture−potential for integrated multi-

D. C., Available: https://www. wfga. net/

trophic aquaculture (IMTA) in marine offshore

documents/marine̲finfish̲finalreport. pdf. (April

systems.

2014).

, 297, 1-9.

Wall C. C., Peterson B. J., and Gobler C. J., 2008:

Rice M., 2000: A review of shellfish restoration asa tool for coastal water quality management.

Facilitation of seagrass
productivity by suspension-feeding bivalves.

, 3, 1-8.

., 357, 165-174.

Rubino M., 2008: Offshore aquaculture in the United

Welcomme R. and Barg U., 1997: FAO technicalStates: economic considerations, implications &guidelines for responsible fisheries-5, aquaculture

opportunities, NOAA Technical Memorandum
NMFS F/SPO-103, U.S. Department ofCommerce, NOAA, Silver Spring, 263pp.

development, FAO, Rome, 40pp.
Williams B. K., Szaro R. C., and Shapiro C. D., 2009:
Adaptive Management: The U.S. Department

Soto D., Aguilar-Manjarrez J., and Hishamundaof the Interior Technical Guide, Adaptive

N., 2008a: Building an Ecosystem Approach

Management Working Group, U.S. Department

to Aquaculture, FAO/Universitat de les Illesof the Interior, Washington, DC, 84pp. Available

Balears Expert Workshop (7‒11 May 2007,

at: https://www2.usgs.gov/sdc/doc/DOI-%20

Palma de Mallorca, Spain), FAO Fisheries andAdaptive%20ManagementTechGuide.pdf

Aquaculture Proceedings. No. 14, FAO, Rome,
221pp.

Yanagi T. 2005: " Sato-Umi"; New Concept for the
Coastal Sea Management.

Soto D., Aguilar-Manjarrez J., Brugère C., Angel D.,
Bailey C., Black K., Edwards P., Costa-Pierce B.,, 129, 109-111.

Chopin T., Deudero S., Freeman S., Hambrey J.,

Zhang S. Y., Wang Z. H., Lin J., and Wang W. D., 2007:

Hishamunda N., Knowler D., Silvert W., Marba

Variation of fisheries resources in summer andN., Mathe S., Norambuena R., Simard F., Tettautumn in seaweed beds of Gouqi Island.

P., Troell M., and Wainberg A., 2008b: Applying
an ecosystem-based approach to aquaculture:., 28, 45-52. (in Chinese with English
abstract)principles, scales and some management
measures, in “Building an ecosystem approach to

Annotated bibliographyaquaculture” (ed. by Soto D., Aguilar-ManjarrezJ., and Hishamunda N.), FAO/Universitat de les(1) Soto D., Aguilar-Manjarrez J., and Hishamunda,

Illes Balears Expert Workshop (7‒11 May 2007,

N. (eds), 2008: Building an ecosystem approach toPalma de Mallorca, Spain), FAO Fisheries andaquaculture, FAO/Universitat de les Illes Balears

Aquaculture Proceedings. No. 14, FAO, Rome,Expert Workshop (7‒11 May 2007, Palma de Mallorca,

pp. 15-35.

Spain), FAO Fisheries and Aquaculture Proceedings.

Sutinen J. G., Clay P., Dyer C. L., Edwards S. F., Gates

No. 14, FAO, Rome, 221pp.

J., Grigalunas T. A., Hennessey T., Juda L., Kitts

This FAO report summarizes findings from aA. W., and Logan P. N., 2000: A framework forworkshop co-organized with the Universitat de lesmonitoring and assessing socioeconomics andIlles Balears that took place from 7‒11 May 2007 ingovernance of large marine ecosystems, NOAA

Palma de Mallorca, Spain on “Building and ecosystem

Technical Memorandum NMFS-NE 158:2000,

approach to aquaculture” (EAA). Participants defined

U.S. Department of Commerce, NOAA, Silver

the phrase “ecosystem approach to aquaculture”

Spring, 32pp.

and several main principles that should guide the

The World Bank, 2014: Sustainable Aquaculture.

sustainable development of aquaculture. These(http://www.worldbank.org/en/topic/

included the development of aquaculture consistentenvironment/brief/sustainable-aquaculture).

with resilience of ecosystem functions; improving

94

Katherine A. McGRAW and Michael B. RUST

human wellbeing; and consideration of other relevant

National Oceanic and Atmospheric Administration

sectors (social, technical, economic, and political).

(NOAA) to manage the nationʼs living marine

They state that EAA should address the many

resources, including fisheries in a sustainable manner.

needs and desires of societies without compromising

In order to enable better decision-making among

ecological integrity. The workshop participants also

various groups and concerns, (e.g., commercial,agreed on various ecosystem approaches for different

recreational, and subsistence fisheries), aquaculture,scales (e.g., small or “farm”, regional or zone, andprotected species, biodiversity, and habitats,global) and that regulations should focus more on

NOAA is implementing Ecosystem-Based Fisheries

the recipient body of water (e.g., stream, estuary,

Management (EBFM). The policy directive issued inlarge marine ecosystems) rather than the scale andMay 2016 is a framework for an ecosystem approach

intensity of production.

to fisheries, which defines EBFM; describes thebenefits of EBFM; discusses how EBFM relates to(2) Aguilar-Manjarrez J., Soto D., and Brummett

existing legal authorities and requirements; andR., 2017: Aquaculture zoning, site selection andestablishes a framework of guiding principles forarea management under the ecosystem approach

implementing EBFM within NOAA Fisheries. It

to aquaculture: Full document, Report ACS113536,

builds on the NOAAʼs past progress and commitment

FAO, Rome, and World Bank Group, Washington,

to integrating its management programs for living

DC., 395pp.

marine resources and considering interactions

The Food and Agricultural Organization of theamong fisheries, protected species, aquaculture,

United Nations and the World Bank Group convened

habitats, and other ecosystem components, including

an expert workshop on Site Selection and Carrying

human communities in decision-making. The policy

Capacities for Inland and Coastal Aquaculture in

defines EBFM as “December 2010 in Northern Ireland. Spatial planningis becoming increasingly important in the growthof aquaculture and the issues involved require an
ecosystem approach to management that addresses
larger spatial units than just the individual farmor site. The main purpose of the workshop wasdevelopment of a guide or handbook for aquaculture.”site selection and carrying capacity estimation

The EBFM policy document specifically mentions

within an ecosystem approach to aquaculture thataquaculture as an ecosystem component, andcan be used by a broad range of stakeholders. The

NOAA includes aquaculture in the term “fisheries”.

publication provides useful and practical information

Therefore, this document although mostly intended

and guidance for managers, policy-makers, technicalfor commercial fisheries, forms the basis for thestaff, and aquaculturists about zoning, siting, anddevelopment of a separate Ecosystem Approach to

management based on experiences and examples

Aquaculture (EAA) which recognizes the similarities,

from ten case studies in countries around the world.

but also the distinct differences, between “capture” orThey identify relevant processes and activities“wild” fisheries and aquaculture. Although the EBFM

for various users on different spatial scales in a

directive focuses on “capture” or “wild” fisheries,

systematic fashion.

the language and concepts in it are also directly
applicable to aquaculture and, in most instances,(3) National Oceanic and Atmospheric Administration,

the phrase “ecosystem approach to aquaculture”,

2016: Ecosystem-based fisheries management policy

or EAA could easily be substituted for “ecosystem-of the National Marine Fisheries Service, National

based fishery management” (EBFM), and the word

Marine Fisheries Service Policy Directive 01-120.

“aquaculture” substituted for “fisheries”.

May 23, 8pp.
Several national laws or mandates require theSince there are distinct and important differences
between capture fisheries and aquaculture, theEcosystem Approach to Aquaculture

95

NOAA Office of Aquaculture is developing adevelopment and management, and provides theseparate Ecosystem Approach to Aquaculturebasis for the policy and some background information.

(EAA). An EAA is the first step or level along a

The policy also describes the benefits and challenges

continuum toward a more complex and detailed planof sustainable aquaculture in the U.S. and sets

for implementing ecosystem-based management offorth NOAA aquaculture priorities and actions foraquaculture.

implementing the policy in terms of regulations,interactions with various agencies and groups in the(4) National Oceanic and Atmospheric Administration,

U.S., and cooperation with other nations. One of the

2011: Marine Aquaculture Policy, NOAA Office ofstated goals in the policy is ecosystem compatibility;

Aquaculture, Issued June 2011.

that is to say, aquaculture development in federal

The NOAA Office of Aquaculture developed awaters should be compatible with the functioning ofMarine Aquaculture Policy in 2011 to enable thehealthy, productive, and resilient marine ecosystem.

development of sustainable marine aquaculture

In keeping with this goal, aquaculture operators

within the context of NOAAʼs multiple stewardshipshould be held accountable for protecting the species

missions and legal mandates. The document definesand environment in which they are working. Other

aquaculture as “goals include compatibility of aquaculture facilities
with other authorized uses of marine waters and”. It includes production for food, wild stock
replenishment or restoration (for finfish as well asshellfish and other marine organisms), and rebuilding
populations of threatened or endangered species. It
contains specific goals with regard to aquaculturebasing management decisions on the best available
science and information.

水 研 機 構 研 報， 第 49 号，97 − 109， 平 成 31 年
Bull. Jap. Fish. Res. Edu. Agen. No. 49，97−109，201997

Spatial planning for shellfish aquaculture and seagrasses in US West
Coast estuaries: considerations for adapting to an uncertain climate
Brett R. DUMBAULD＊1, Jennifer L. RUESINK＊2, and George G. WALDBUSSER＊3

Abstract: Shellfish aquaculture has been an important contributor to the local economy of several communities
along the US West Coast for almost 100 years and in most of the estuaries where it occurs it has coexistedwith the native seagrass (eelgrass,). Eelgrass provides numerous ecosystem services including

nursery habitat for juvenile fish and invertebrates, but is declining in many locations worldwide, and istherefore now protected by no net loss provisions in US laws and regulations. We have studied the interaction
between oyster aquaculture and eelgrass at both the local process scale and at the estuarine landscape scale
in Willapa Bay, Washington. While there are important differences, most US West coast estuaries like Willapa
Bay are small relative to the nearby coast, experience less riverine influence during the summer growing
season and have shorter residence times than estuaries where oysters are cultured on eastern edges ofcontinents, and the majority of culture takes place in intertidal areas. The ecology of eelgrass and cultured
Pacific oysters as well as their role as habitat is thus directly influenced by bathymetry and proximity to thecoastal ocean. We summarize studies on the interaction between eelgrass and oyster culture at local scales,present data that suggest culture practices are important to consider, but the cumulative interaction is notnecessarily negative for eelgrass at the estuarine landscape scale in Willapa Bay. We also briefly summarize
studies on the influence of sea level rise (SLR) and sea water chemistry (ocean acidification, OA), two projectedchanges in climate that are expected to occur over a broader spatial and longer temporal scale. SLR isprojected to enhance the presence and interaction of eelgrass with oyster aquaculture in Willapa Bay, though
this effect was mostly driven by bathymetry in our simplistic model and landward eelgrass expansion could
be restricted elsewhere. OA has already influenced oyster culture especially in commercial hatcheries where
it changes aragonite saturation state and the ability of larval oysters to deposit shell. Evidence for direct effectsof carbonate chemistry in estuaries like Willapa Bay is more equivocal due to complex interactions, yet still
related to the proximity of cold upwelled ocean water which likely influences natural spawning on this coast.
The presence of eelgrass may also buffer water chemistry at least over short time scales, but this is less likely
to directly affect survival of juvenile than larval oysters and instead eelgrass may impact juvenile oyster
growth via this and other mechanisms. These physical effects of structure also influence conspecific eelgrass
plants and appear to be more important than water chemistry feedbacks.
Recent initiatives to expand shellfish aquaculture in US west coast estuaries have received increased
regulatory scrutiny due in large part to this interaction with eelgrass. Our review suggests that a permit
process that simply evaluates and prevents direct negative effects of oyster culture on eelgrass at small spatial
and immediate temporal scales would greatly and perhaps unnecessarily restrict expansion of culture
operations. A broader adaptive approach could be employed that considers bathymetric and along estuary
gradients that affect both of these resources and the services they provide, especially given projected futureclimate.
Key words: oyster aquaculture, sea level rise, ocean acidification2018年８月31日受理（Accepted on August 31, 2018）
Agricultural Research Service, U.S. Dept. of Agriculture, Hatfield Marine Science Center, Newport, OR 97365, U. S. A.
＊2
Department of Biology, University of Washington, Seattle, WA 98195, U. S. A.
＊3
College of Earth, Ocean and Atmospheric Sciences, Oregon State University, Corvallis, OR 97365, U. S. A.
E-mail: brett.dumbauld@ars.usda.gov＊1

98

Brett R. DUMBAULD, Jennifer L. RUESINK, and George G. WALDBUSSER
Introduction

and thus viewed by scientists and managers as athreat to native habitats like seagrass, despite recent

Seagrasses and Oyster Aquaculture in US West

recognition of the omnipresent and embedded role

Coast estuaries

of humans and cultural aspects involved in crafting

Oyster aquaculture became an importanta sustainable future for these estuarine systems andcontributor to local US West coast economies when

the role of aquaculture in in both the US and Japanthe Pacific oyster(Broitman

was introducedin the early 1900ʼs and largely replaced the native
oyster., 2017; Carpenter., 2009; Mizuta

and Vlachopoulou, 2017).

, which had been extensively

fished commercially and mostly overharvested or
succumbed to other factors including pollution (Blakeand Ermgassen, 2015; Dumbauld

West Coast estuaries function
While there are important exceptions like the., 2011; Kirby,

Salish Sea in Washington State, most U.S. West

2004; Polson and Zacherl, 2009; Steele, 1964). Pacificcoast estuaries are small relative to the extensive

oysters were cultured and harvested from leased

spatial extent of the nearby open coastline. Willapa

and privately owned estuarine tidelands, and theBay, which is the single largest cultured oyster

industry relied on juvenile seed oysters shipped fromproduction site in the US and the third largest

Japan through the late 1970ʼs when local hatchery

estuary on this coast has only a 358 km2 signature

production of oyster larvae succeeded (Chew, 1984).

(Fig.1), which roughly equals the size of the James

Though the extent and interaction between theseRiver sub-estuary in Chesapeake Bay, which is theresources has only recently been actively quantified

largest estuary on the US East Coast with an 11,600

at large scales (Dumbauld and McCoy, 2015), these

km2 signature. It is further dwarfed by the Seto

aquaculture operations have coexisted for almost

Inland Sea in Japan which has a 23,204 km2 area.

100 years with the native seagrass (eelgrass,

The spatial footprint of the oyster culture industry), which grows on some of these tidelands.

in this estuary is also relatively small (1,764 ha ofEelgrass provides numerous ecosystem services

active culture) on 12,384 ha of privately deeded andincluding habitat for some fish and invertebrates

leased oyster grounds representing about 58 % of the(McDevitt-Irwin., 2016), but seagrasses

intertidal area in the estuary (Dumbauld and McCoy,

are threatened and declining in many locations2015). Estuaries like Willapa Bay also experience lessworldwide (Waycott., 2009). Seagrass habitat has

riverine influence during the summer months andbeen protected by no net loss provisions in US laws

have shorter residence times than estuaries where

and regulations since the late 1970ʼs, but recognition

oysters are present on eastern edges of continentsof this wide-scale seagrass loss, as well as increasing(Hickey and Banas, 2003), and the majority of oyster

threats to and declining populations of otherculture takes place across broad intertidal mudflats

important species that utilize eelgrass as habitat,

the which represent about 58 % of the estuarine

has heightened concern resulting in re-evaluations ofarea. This relatively shallow bathymetry and lack

permits for existing aquaculture operations and newof a strong salinity gradient result in well mixed

restrictions for expanded culture (NMFS, 2017). Reef

water column, with often turbid conditions driven

forming bivalves like oysters are now also widely

primarily by surface winds at least during spring

recognized to provide valuable estuarine habitat andand summer. The US west coast is also adjacent

this reef habitat is also threatened (Beck., 2011;to the California current ecosystem, an eastern., 2012). Though oysters raised inboundary upwelling system so estuaries are subject

Zu Ermgassen

aquaculture are not generally allowed to establish

to seasonal events where nutrient rich, high pCO2

reefs, they still provide three dimensional structure

water is transported to the surface and episodic

and this service has mostly not yet been recognizedintrusions into these estuaries can significantly lower

for Pacific oysters by US west coast managers.

saturation state and pH (Feely., 2010; Hauri

This is in part because the oysters are introduced., 2013). This physical context clearly influences

and cultured in US west coast estuaries by humans

the distribution and ecology of both cultured Pacific99

Planning for shellfish aquaculture and seagrasses
A

B

influence of sea level rise (SLR) and sea waterCchemistry (ocean acidification, OA), two projectedchanges in climate that are expected to occur overSeaƩůea broad spatial and long temporal scale in thesesystems. Current management of eelgrass andPorƚůandoysters in the US is largely focused on regulations
that stipulate conditions or types of activity thatcan occur at relatively small scales. While there isa nationwide permit issued for shellfish aquaculture(Nationwide permit 48; ACOE, 2016), it nonethelessstipulates activities that can occur at individualsites and considers no net loss of seagrass at this or

San Francisco

even a smaller (individual plant) spatial scale. This2009

is also typically the scale used to evaluate success2100

for seagrass restoration or mitigation for loss. The
Fig. 1. A) Willapa Bay is the second largest estuary
along the US West Coast, south of the Salish Sea westof Seattle, but is small relative to the extent of the
nearby coast that greatly influences its hydrography.
B) Eelgrass () coverage across the tideflat in
Willapa Bay based on aerial photography in 2009 andC) the predicted probable densities of eelgrass at year
2100 for the most conservative sea level rise scenarios(RCP 2.6 with 2.0 mm yr-1 sediment accretion) using
boosted regression tree models. Numbers on thecolorbar correspond to the probability ofpresence (zero to 100 %) within - 1.5 and 1.2 meters
elevation relative to MLLW for each pixel in theimage. Shellfish aquaculture beds are overlaid in red.

temporal scale is also relatively short with the yearthat the permit is issued most often used as thebaseline reference and permit lifetime is perhaps up
to 5 years over which reference conditions must be
re-established or loss mitigated.
Here we briefly review existing data on botheelgrass and oysters as habitat features in Willapa
Bay as the single most important US west coast
estuary for oyster production and then discuss
how these two future changes in climate might be
addressed at a broader “seascape” scale. Our intent
is to broaden the discussion about the interaction
between shellfish aquaculture and eelgrass to thisseascape scale and at least contemplate using alonger temporal scale to better define goals andoysters and eelgrass in these estuaries, as well as

perhaps adaptively manage these two resources overthe interaction between them and the role that bothtime to meet them. This exploration is consistentof these resources play as habitat for other fish andwith ecosystem-based management in the US andinvertebrates. Natural disturbances due to wind andthe Japanese concept of

sediment movement are a regular feature in these

explicitly includes a bottom‒up social contract with

soft sediment dominated systems (Norkko, though the latter.,

local resource users (Mizuta and Vlachopoulou,

2010). In some cases this context already directly2017). We pose and attempt to address the following

influences management. For example Pacific oyster

questions:

growth is clearly modulated by the distribution of

1. How much does the presence of oyster aquaculture

phytoplankton as food and Willapa Bay and growers

affect eelgrass at the broad seascape scale?

have long adapted to this by moving oysters from

2. How do effects differ by culture practice, and are

beds located near the southern end of this estuary tothey chronic or transitory from one year to thebeds that are closer to the ocean where food supply

next?

is greater and the oysters successfully “fatten” formarket (Banas., 2007).

3. What are the consequences of projected climatechange to seagrass at the seascape scale and what

These larger spatial scales and gradients become

should the baseline be? Is no net loss of seagrass

important considerations when evaluating thebased on a single contemporary date a useful

100

Brett R. DUMBAULD, Jennifer L. RUESINK, and George G. WALDBUSSER

management target?

90 % culture above + 1.2 m MLLW.

4. How would management outcomes differ if

Once these spatial data layers for eelgrass as

projected temporal changes to both eelgrassthe dependent variable and shellfish aquaculture

and aquaculture at the seascape scale were(the primary independent variable of interest) wereincorporated?

created, the next step involved constructing models
to describe the effects of other physical and biotic
Methodology

factors that might influence eelgrass presence quite
apart from the effect of aquaculture. This stepMethods for collecting data on shellfish aquaculturenecessarily involves assembling or collecting spatialand seagrass at broad spatial scales differ from thosedata for these factors at this scale. In our case theseused in most small experimental scale studies.

data included tidal elevation (digital elevation model

Detailed methods for the studies we conducted in

DEM raster created by measuring this during

Willapa Bay can be found in Dumbauld and McCoy

the ground survey with a Trimble ProXr® unit

(2015) and Graham. (unpublished manuscript,

and combining with existing LiDAR data for theavailable from the authors), but in general involved

upper intertidal), distance to the estuary entrance

the use of aerial color infrared photos (1: 20,000) of(cumulative cost distance m), Euclidean distance

Willapa Bay taken in 2005, 2006, and 2009. An on

to the nearest channel with water present in the

ground survey to truth the original photos and collectaerial photos (m), cumulative wave stress (calculated

additional data was conducted in 2006 - 7 where 4,238

using average wind speed and direction measured at

individual locations at intersection points of a 200 m x

Toke Pt. in 2009, fetch distance, and tide stage), and

200 m grid across the estuarine tideflat were visited

salinity using a model based on the 5th quantile of wet

and data collected on seagrass cover that would beseason salinity measured at 5 long term monitoring

recognizable in the photographs. This data along withlocations in the estuary. Each of these factors wasother characters that would help quantify habitat at

resampled to a 5 x 5 m grid for further analyses

this seascape scale (oyster shell cover, burrowing

and we extracted data from a set of random points

shrimp and other benthic fauna burrows, macroalgal

outside of aquaculture. We initially used generalcover, sediment composition) were recorded into a

additive models (GAMʼs), but have since increased

Trimble Geo XT ®mapping grade GPS system. The

predictive performance using boosted regression

0.25 m color infrared photos were geo rectified andtree models (BRT's, Elith

we extracted mean values for each color band in a 5

model interactions among predictor variables andm radius around each of the ground survey points

enable improved internal cross-validation to evaluate

to develop a model to predict the probable cover ofeffects on eelgrass outside of culture areas. We thenfor each pixel in the imagery. All data

similarly extracted eelgrass data from a set of random

was imported into R (R Development Core Team,

points across the entire estuarine tideflat for each of2015) for analyses. We then created models to predictthe 3 years and compared predicted and observed

the relationship between on ground density and color

amounts of eelgrass in areas with aquaculture whichbands and used this to predict probable density ofwere then summed to assess effects.

., 2008), which alsoeelgrass for each pixel (mean of 1 m by 1 m values)

Finally we evaluated the potential effects of climate

in the aerial imagery. The photo extracted coverchange on shellfish aquaculture and seagrass at thewas then used as the actual cover and distribution

estuary scale in Willapa Bay. The effects of sea leveloffor each year. Spatial data layers forrise (SLR) were examined by applying offsets to theaquaculture were built using data gathered from

DEM to represent 4 local SLR scenarios and predict

interviews with individual shellfish farmers including

eelgrass coverage for several scenarios at 3 future

location, species, bed type, and harvest method for

endpoints (years 2030, 2050 and 2100) using the sameeach of 458 beds. For most analyses we then createdspatial data layers described above. While we havea 5 x 5 m raster layer for presence/absence of

not yet developed spatial layers that allow us tooysters and limited this to the 282 active beds with >evaluate the more complex effects of enhanced CO2

101

Planning for shellfish aquaculture and seagrasses
and other changes to seawater chemistry, we review

thus depend on culture method and location.

data collected along the estuarine gradient in Willapa

Bivalves have been shown to enhance seagrass

Bay that could potentially be used in such an analysis.

growth indirectly via nutrient biodeposition and/or

Seawater samples were either collected at discrete

filtering and clearing water which changes the lightsampling locations along an estuarine gradientenvironment. While oysters were shown to perform(details in Ruesink

both of these services in Willapa Bay (Wagner., 2015; Ruesink., 2018a) or.,at a single location over a broad temporal scale (Hales

2012; Wheat and Ruesink, 2013), neither mechanism., 2017) and related to either plankton samples

seemed important at the locations studied because(for oyster larvae) from the same locations, oyster

background nutrient conditions were not limiting

and seagrass data collected at nearby locations,and the local light environment was more influenced

or optimal conditions for oyster larvae based on

by water flow and sediment. This in turn influenced

results of detailed laboratory studies. In both cases

shoot density resulting in self-shading which also

discrete seawater samples were analysed for two

influenced seedling success (Wisehart

components of the carbonate chemistry systemYang., 2007;., 2013).

(dissolved inorganic carbon and the partial pressure

Our initial seascape scale study revealed thatof carbon dioxide (pCO2)) at Oregon State University

eelgrass declined slightly over the 3 years we(Bandstra., 2012). Thesemodeled its presence in Willapa Bay, but oyster

values were then used to calculate other parameters

aquaculture reduced the overall eelgrass presenceof the seawater chemistry system like aragonite andby less than 1.5 % in any single year (Dumbauld andcarbonate saturation that directly influence oyster

McCoy, 2015). The general additive model we used tolarval growth and survival (Waldbusser

predict eelgrass distribution outside of aquaculture., 2006; Barton., 2015).

only explained about 50 % of the variation in eelgrass
Results and Discussion

distribution which was likely due to the limited set ofvariables for which we had spatial data at this scale.

Previous research on the interaction between

Distance to the estuary mouth and tidal elevationoyster culture and eelgrass in Willapa Bay conducted

were the most significant factors, but these variables

mostly at a small experimental scale (< 20 m2 plots),

were likely only proxies for mechanistic factors likebut in some cases up to the shellfish culture bed scaletemperature, nutrient availability, flow, and turbidity(10 - 75 ha) suggests that:as they influenced available light discussed above

1 - Eelgrass density declines with oyster density inand shown to be important at the local scale. Mixed

all intertidal oyster aquaculture areas. This is mostly

effects models that considered culture practices

a threshold function and either due to competition

revealed that harvest method influenced eelgrassfor space where > 20 % shell cover results in lesspresence, but not type of bed (e.g., oysters raised oneelgrass (Wagner., 2012) and/or shading andlonglines, beds only used for small oyster seed, orlight in the case of off-bottom longline oyster culture

beds only used for larger oysters to fatten). Results(Ruesink., 2009; Rumrill and Poulton, 2004;

were variable but beds that were mechanically

Wisehart., 2007).

harvested tended to have chronically less eelgrass

2 - Harvest disturbance significantly affects

present than those harvested by hand, yet even theseeelgrass density. Density is lowest in mechanicallybeds had an average of 92 ‒ 99 % of the predicted

harvested beds especially right after harvest, buteelgrass cover present with clear temporal recovery

eelgrass growth is slightly greater in these areas

trends across years. Many individual beds had

and recovery is site specific ranging from 1- 4 years

well over the predicted amount of eelgrass present(Tallissuggesting that aquaculture could enhance eelgrass., 2009)

3 - Eelgrass relative growth rate, plant size,

presence at the seascape scale, perhaps by removing

and therefore production are affected by oyster

bioturbators or stabilizing substrate.

aquaculture, but these effects are variable andnot always negative (Tallis., 2009). Effects

Separate examinations of eelgrass biometrics along
the estuarine gradient in Willapa Bay at least in part

102

Brett R. DUMBAULD, Jennifer L. RUESINK, and George G. WALDBUSSER

confirm these seascape scale patterns. Shoot size,

to 44 ‒ 52 % in 2100 and this will occur on as many

density and above ground biomass varied seasonallyas 325 beds representing 70 % of all beds (4,195 ha,(responding to daylength and perhaps temperature),

Fig.1). This will represent challenges for the shellfish

but also with tidal elevation (usually with larger lessgrowers including potential impacts to oyster

dense shoots found at lower elevation; Ruesink.,

growth and ability to efficiently harvest product, but2010). Shoot density and above ground biomass also

also potential regulatory constraints. We have notdeclined from the mouth of the estuary to the upriverused similar models to hindcast this interaction forend at the same tidal elevation (Ruesink., 2015).

conditions that occurred before Pacific oysters were

There were however no consistent trends in relative

introduced to Willapa Bay in the 1800ʼs, but historical

growth of individual plants along these gradients, andmaps suggest that native oysters (short term reciprocal transplant experiments suggest

occupied about 17 % of the low intertidal and shallowthat plant size and branching are plastic, while life

subtidal area. Based on estimated tidal elevations

history strategy of source plants (e.g., presence ofalone the suitable area for eelgrass is estimated toflowering shoots and seedlings) was more persistent

have been about 3,139 ha (Borde(Ruesink, 2018b). Seedling survival has also been

1850ʼs. We estimated there would have been about

shown to vary along stressor gradients (Yanga 45 % overlap with these oysters albeit at a mostly.,2013).

) once., 2003) in thelower tidal elevation than todayʼs culture operations,and today eelgrass exists as a monotypic meadow

Temporal change
Eelgrass currently covers about 27 % of the tideflat

in many of those locations where native oyster beds
have not returned.

in Willapa Bay and about 43 % of its distribution

Large scale temporal changes in seawater

overlaps with commercial oyster aquaculture whichcarbonate chemistry (ocean acidification, OA) are also

covers about 15 % of the tideflat. Taking a broader

expected to influence both seagrasses and shellfish

temporal view, we also evaluated the potential effects

and their interaction in US West Coast estuaries

of sea level rise (SLR) as one aspect of a changing(Feelyclimate on this eelgrass oyster aquaculture interaction.

Salisbury, 2014). Changes to the carbonate mineral

Rising global mean sea level will result in changes insaturation state have been shown to negatively affectwater depth in estuaries, but these projections are

the acid base balance, biocalcification, and metabolism

specific to the region and system given tectonicof oyster larvae (Waldbusser

shifts and sediment accretion/erosion. We modeledseasonal upwelling of nutrient rich low pCO2 acidified

seagrass distribution and the interaction withwater is a regular feature in nearshore coastal

aquaculture in Willapa Bay using two representative

waters of the California Current ecosystem, episodic

rates (4 mm and about 8 mm yr-1, IPCC pathways

intrusions of this water into estuaries where shellfish

2.6 and 8.5 respectively) for three temporal endpoints

hatcheries use it have already caused significant(2030, 2050, and 2100) and adjusted for expectedissues for the commercial aquaculture industry andtectonic uplift and sediment accretion. In addition topractices to mitigate these losses have already been

elevation, we used the same additional parameters

adopted (adding buffering agents and adjusting times(salinity, distance to mouth, distance to channel,

when water is drawn, Barton

cumulative wave stress) and boosted regression tree

due to their efficient uptake of aqueous CO 2 formodels to describe current and future distributions

photosynthesis, seagrasses are expected to increaseof eelgrass. We could not predict change for thesein productivity with rising levels in the environment

other parameters, but using a boosted regression tree

and therein may also have the potential to mitigate

allowed for model cross-validation. Results suggest as

effects of this chemistry on other organisms likemuch as a 36 % increase in eelgrass cover by 2100

shellfish (Hendriks., 2016; Feely., 2010; Waldbusser and., 2015). Because., 2015). In contrast,., 2014; Pacella., 2018).

with similar or even greater proportional increases

Estuarine water chemistry is however highly

on oyster aquaculture beds. Mean coverage among

variable over both relatively short (daily, diel) andall beds is projected to increase from 41 % (current)

long term (seasonal, annual) temporal scales and103

Planning for shellfish aquaculture and seagrasses

A)

2011

2012

2013

2014

B)
E

W

2011

Fig. 2. Seawater carbonate chemistry measured at locations south of the fattening/recruitment line inWillapa Bay, Washington. Shown here are A) aragonite mineral saturation state calculated from observed., 2017) and B)
temperature, salinity, TCO2 and pCO2 at Nahcotta in 2011 ‒ 2014 (modified from Hales
aragonite mineral saturation state calculated from the same parameters measured at discrete locations
along the western side of the estuary (left graph, red circle) and east side (right graph, blue circle) in2011 (modified from Ruesink., 2018a). Also denoted (red horizontal line) is the threshold for acuteeffects on oyster larvae.

along spatial estuarine gradient scales within eachat a Nahcotta mooring with some variation between

system. In Willapa Bay as salinity declined andyears. pCO2 and pH varied less over the season thantemperature increased along a gradient from thethese other parameters and aragonite saturation

mouth to the Naselle River at the southern end of thestate was decoupled from them, suggesting there

estuary, aqueous CO2 increased and pH was reduced

was a very short window during summer whenon a single cruise and one point in time during theconditions would be favorable for oyster larvalsummer (Ruesink

development (Fig.2A, Hales., 2015). These parameters., 2017). There were

were much more variable, especially at both mouth

again differences between the western and easternand river endpoints when continuously measured

half of the estuary with aragonite saturation statewith moored instruments at single locations overgenerally exceeding critical minimums measured in

the course of a summer month. A strong influence

the laboratory on the western, but not eastern sideof upwelling events was evident near the estuary(Fig.2B, Ruesinkmouth, whereas., 2018a).

consistent tidal variation in pH

The direct effects of water chemistry on eelgrass

occurred near the river endpoint. Less variation wasand oyster larval survival and settlement at theobserved at locations near mid-bay, and there were

population level in the field are more difficultclear differences between conditions in the eastern

to assess due to the presence of and inability to(Naselle River) and western (Nahcotta) arms of thecontrol multiple other factors/stressors, so results

estuary (Ruesink., 2018a). As expected large

to date are more equivocal. Nonetheless while tissue

seasonal fluctuations were observed in temperature,

carbon measured in eelgrass blades increased atsalinity, alkalinity, and TCO2 over the course of a year

eight stations along the estuarine gradient and this104

Brett R. DUMBAULD, Jennifer L. RUESINK, and George G. WALDBUSSER

was coincident with depleted C-13 reflecting water

2012; Hendrikscarbon chemistry gradients, production (relative

night produces an asymmetrical diel signal for thisgrowth rate) did not vary and instead seemed

effect and there is little research on whether the

to be more related to sediment organic content

most sensitive bivalve larval stages benefit at thisand wave exposure (Ruesink., 2015). This is

short temporal scale, recent studies suggest that postconsistent with recent measurements which suggest

settlement growth and survival of juvenile oysters

that eelgrass has the capacity to achieve similar

is enhanced in eelgrass (WADNR, 2017; Smith,productivity across much broader ocean basin and2016). It is however yet unresolved whether thislatitudinal scales, despite marked differences in

effect can be attributed solely to water chemistrymorphometric characteristics (Ruesink., 2018b).

and distinguished from the effects of other factors

Oyster larvae are most responsive to augmented CO2

like reduced flow in seagrass which results in lessand reduced aragonite saturation in the laboratory

sediment but enhanced desirable phytoplankton

as they cross two important and relatively shortfood intake (Lowe, unpublished). Reduced flow

physiological transitions; initial shell formation andalso reduces settlement of fouling organisms thatmetamorphosis/settlement when metabolic energy

potentially compete with oysters for space and foodallocation is crucial (Panand also alters the abundance of bivalve predators.

., 2015; Waldbusser.,., 2014). Although respiration at2015). They are however subject to widely varying

Perhaps most relevant on the broader temporalconditions over their 2 - 3 week larval period in theand estuary wide spatial scales we consider here

estuary. As noted above, aragonite saturation state

however is recognition that both of these resources

was lower on the eastern more river influenced

are likely not responding to average conditions andside of the southern end of Willapa Bay versus thethe window of favorable conditions continues towestern side when examined during three separate

shift and narrow as atmospheric CO2 concentration

summers. Survival of four cohorts of Pacific oyster

continues to rise (Hales., 2017; Pacellalarvae tracked simultaneously over these 3 summers., 2018). Thus variation about the average andwas similar between these two sides and subsequentfavorable windows of carbonate “weather” in both

settlement generally higher on the eastern sidetime and space could be important considerations

where aragonite chemistry was less favorable

when considering mitigating and adapting to future(Ruesink., 2018a). This decoupling of population

climate. Organisms may also have the ability to adapt

level effects from water chemistry conditions could

over time to local conditions, but recognizing where

have been due to the fact that aragonite saturationthese conditions occur outside of the laboratory andconditions on both sides were very close to, but on

beyond the experimental scale at individual sites will

average above the ~ 1.4 threshold for acute effects

be important.

established for risk assessments based on laboratory
results (Ekstrom., 2015), that favorable conditions

Conclusions and Management Considerations

were present during the critical windows or because
a multitude of other factors such as temperature,

Initiatives to expand shellfish aquaculture inadvection, predation, etc. were responsible. Larval

US West coast estuaries have received regulatory

condition may also reflect a “carryover” effect fromscrutiny due to interactions with eelgrass, but our

adult brooding conditions and lipid stores in eggs andresearch in Willapa Bay, an important estuary forthus not tie directly to stresses present during theoyster culture on the US West Coast, suggests thatlarval period (Bartoncontext and scale are very important considerations.

., 2015; Hettinger., 2012).

Eelgrass has also recently been hypothesized to

While significant small scale and short term

potentially mitigate the negative effects of ocean

temporal effects due to harvest method occur, oyster

acidification on bivalves by ameliorating wateraquaculture only reduced eelgrass presence inchemistry via photosynthesis and CO2 uptake during

Willapa Bay by less than 1.5 % at the seascape scale

the day at least at very local scales (Washington

and more eelgrass was present than predicted inState Blue Ribbon Panel on Ocean Acidification,

many aquaculture areas.

105

Planning for shellfish aquaculture and seagrasses
Oysters have coexisted with eelgrass in theand McLaughlin K., 2015: Impacts of Coastal

seascape for a long time in Willapa Bay though

Acidification on the Pacific Northwest Shellfish

the distribution of both across the tidal elevation

Industry and Adaptation Strategies Implemented

gradient has changed. Unlike other locations wherein Response.

, 28, 146-159.

eelgrass is threatened by eutrophication and other

Beck M.W., Brumbaugh R. D., Airoldi L., Carranzaanthropogenic disturbance, our models predicted aA., Coen L. D., Crawford C., Defeo O., Edgar

3 ‒ 11 % increase of eelgrass coverage within Willapa

G. J., Hancock B., Kay M. C., Lenihan H. S.,

Bay oyster aquaculture beds by 2021 given projected

Luckenbach M. W., Toropova C. L., Zhang G. F.,

sea level rise.

and Guo X. M., 2011: Oyster reefs at risk and

US West Coast shellfish hatcheries have alreadyadapted and modified practices in response to changes
in carbonate chemistry that routinely exceed average

recommendations for conservation, restoration,and management.

, 61, 107-116.

Blake B. and Ermgassen P. S. E. Z., 2015: The History

global conditions projected to occur in the future due

and Decline ofto their size and proximity to upwelling conditions

Washington.

in Willapa Bay,., 34, 273-280.

along this eastern ocean boundary. This creates a

Borde A. B., Thom R. M., Rumrill S., and Miller L.

distinct estuarine gradient and temporal variability inM., 2003: Geospatial habitat change analysis inconditions that make it difficult to attribute changes

Pacific Northwest coastal estuaries.

in natural oyster spawning and larval settlement to,26, 1104-1116.

changes in water chemistry. While the long term

Broitman B. R., Halpern B. S., Gelcich S., Lardies M.

average trend is for acidified conditions, oysters may

A., Vargas C. A., Vásquez-Lavín F., Widdicombe

be more responsive to extremes and the range ofS., and Birchenough S. N. R., 2017: Dynamic

conditions, which in turn must be evaluated along

Interactions among Boundaries and thethese estuarine gradients where eelgrass seems lessExpansion of Sustainable Aquaculture.

directly affected, but the mitigative effects it has onshellfish growth and survival could be important.

., 4. doi.org/10.3389/fmars.2017.00015
Carpenter S. R., Mooney H. A., Agard J., CapistranoD., DeFries R. S., Diaz S., Dietz T., Duraiappah

References

A. K., Oteng-Yeboah A., Pereira H. M., Perrings
C., Reid W. V., Sarukhan J., Scholes R. J., and

ACOE, 2016: U.S. Army Corps of Engineers Decision
Document Nationwide Permit 48.

services: Beyond the Millennium Ecosystem

Banas N. S., Hickey B. M., Newton J. A., and Ruesink
J. L., 2007: Tidal exchange, bivalve grazing, andpatterns of primary production in Willapa Bay,
Washington, USA.

Whyte A., 2009: Science for managing ecosystem., 341,

123-139.

Assessment.

., 106,1305-1312.
Chew K. K., 1984: Recent advances in the cultivationof molluscs in the Pacific United States andCanada.

, 39, 69-81.

Bandstra L., Hales B., and Takahashi T., 2006: High-Dumbauld B. R., Ruesink J. L., Trimble A. C., andfrequency measurement of seawater total carbon

Kauffman B. E., 2011: The Willapa Bay oyster

dioxide.

reserves in Washington State: Fishery collapse,., 100, 24-38.

Barton A., Hales B., Waldbusser G. G., Langdon C., andFeely R. A., 2012: The Pacific oyster,, shows negative correlation to naturally
elevated carbon dioxide levels: Implications fornear-term ocean acidification effects.
., 57, 698-710.

creating a sustainable replacement, and thepotential for habitat conservation and restoration.
., 30, 71-83.
Ekstrom J. A., Suatoni L., Cooley S. R., Pendleton L. H.,
Waldbusser G. G., Cinner J. E., Ritter J., Langdon
C., van Hooidonk R., Gledhill D., Wellman K.,

Barton A., Waldbusser G. G., Feely R. A., Weisberg

Beck M. W., Brander L. M., Rittschof D., Doherty

S. B., Newton J. A., Hales B., Cudd S., Eudeline

C., Edwards P. E. T., and Portela R., 2015:

B., Lang. J., Jefferds I., King T., Suhrbier A.,

Vulnerability and adaptation of US shellfisheries

106

Brett R. DUMBAULD, Jennifer L. RUESINK, and George G. WALDBUSSER
to ocean acidification.

., 5, 207-

214.

habitats from temperate to tropical regions: ameta-analysis.

Elith J., Leathwick J. R., and Hastie T., 2008: A
working guide to boosted regression trees.

., 557, 133-143.

Mizuta D. D. and Vlachopoulou E. I., 2017: Satoumi
concept illustrated by sustainable bottom-up., 77, 802-813.

initiatives of Japanese Fisheries Cooperative

Feely R. A., Alin S. R., Carter B., Bednarsek N., Hales

Associations.

, 78, 143-149.

B., Chan F., Hill T. M., Gaylord B., Sanford E.,

NMFS, 2017: WA eelgrass and shellfish aquaculture

Byrne R. H., Sabine C. L., Greeley D., and Juranekworkshop report (ed. by Hoberecht L.), NationalL., 2016: Chemical and biological impacts ofMarine Fisheries Service Western Region,

ocean acidification along the west coast of North
America.

Seattle, 64pp.

., 183, 260-270.

Norkko J., Norkko A., Thrush S. F., Valanko S., andFeely R. A., Alin S. R., Newton J., Sabine C. L., Warner

Suurkuukka H., 2010: Conditional responses toM., Devol A., Krembs C., and Maloy C., 2010: The

increasing scales of disturbance, and potential

combined effects of ocean acidification, mixing,

implications for threshold dynamics in soft-and respiration on pH and carbonate saturation

sediment communities.

in an urbanized estuary.

413, 253-266.

.,

88, 442-449.

.,

Pacella S. R., Brown C. A., Waldbusser G. G., Labiosa

Hales B., Suhrbier A., Waldbusser G. G., Feely R.

R. G., and Hales B., 2018: Seagrass habitatA., and Newton J. A., 2017: The Carbonate

metabolism increases short term extremes andChemistry of the "Fattening Line," Willapa Bay,

long-term offset of CO 2 under future ocean

2011-2014.

acidification.

., 40, 173-186.

Hauri C., Gruber N., Vogt M., Doney S. C., Feely R.

, 115,

3870-3875.

A., Lachkar Z., Leinweber A., McDonnell A.

Pan T. C. F., Applebaum S. L., and Manahan D. T.,

M. P., Munnich M., and Plattner G. K., 2013:2015: Experimental ocean acidification alters theSpatiotemporal variability and long-term trends

allocation of metabolic energy.
., 112, 4696-4701.

of ocean acidification in the California Current
System.

, 10, 193-216.

Hendriks I. E., Olsen Y. S., Ramajo L., Basso L.,

Polson M. P. and Zacherl D. C., 2009: Geographic
distribution and intertidal population status for

Steckbauer A., Moore T. S., Howard J., andthe Olympia oyster,

Duarte C. M., 2014: Photosynthetic activity

1864, from Alaska to Baja.

buffers ocean acidification in seagrass meadows.
, 11, 333-346.
Hettinger A., Sanford E., Hill T. M., Russell A. D.,

Carpenter, 28,

69-77.
R Develoment Core Team, 2015: R: A language
and environment for statistical computing, R

Sato K. N. S., Hoey J., Forsch M., Page H. N., andFoundation for Statistical Computing, Vienna.

Gaylord B., 2012: Persistent carry-over effects ofRuesink J. L., Hacker S. D., Dumbauld B. R., and Harbell

planktonic exposure to ocean acidification in theS., 2009: Scale-dependent and indirect effects

Olympia oyster.

of filter feeders on eelgrass: Understanding, 93, 2758-2768.

Hickey B. M. and Banas N. S., 2003: Oceanography

complex ecological interactions to improveof the US Pacific Northwest Coastal Ocean andenvironmental impacts of aquaculture, in “Finalestuaries with application to coastal ecology.

Report to the Western Regional Aquaculture, 26, 1010-1031.
Kirby M. X., 2004: Fishing down the coast: Historicalexpansion and collapse of oyster fisheries alongcontinental margins.
, 101, 13096-13099.
McDevitt-Irwin J. M., Iacarella J. C., and Baum J. K.,
2016: Reassessing the nursery role of seagrassCenter, 1-25”, Dept. of Biology, University ofWashington, Seattle.
Ruesink J. L., Hong J. S., Wisehart L., Hacker S. D.,
Dumbauld B. R., Hessing-Lewis M., and Trimble
A. C., 2010: Congener comparison of native() and introduced ()

eelgrass at multiple scales within a Pacific107

Planning for shellfish aquaculture and seagrasses, 12, 1773-1789.

Waldbusser G. G., Hales B., Langdon C. J., Haley B. A.,

Ruesink J. L., Yang S., and Trimble A. C., 2015:

Northwest estuary.

Schrader P., Brunner E. L., Gray M. W., Miller C.

Variability in Carbon Availability and EelgrassA., Gimenez I., and Hutchinson G., 2015: Ocean(

acidification has multiple modes of action on) Biometrics Along an Estuarine

Gradient in Willapa Bay, WA, USA.

bivalve larvae.

., 38, 1908-1917.

, 10.

Waldbusser G. G. and Salisbury J. E., 2014: Ocean

Ruesink J. L., Sarich A., and Trimble A. C., 2018a:

acidification in the coastal zone from an

Similar oyster reproduction across estuarineorganism's perspective: Multiple system

regions differing in carbonate chemistry.

parameters, frequency domains, and habitats.

., 75, 340-350.

., 6, 221-247.

Ruesink J. L., Stachowicz J. J., Reynolds P. L., Bostrom

Washington State Blue Ribbon Panel on Ocean

C., Cusson M., Douglass J., Eklof J., Engelen

Acidification, 2012: Ocean Acidification: FromA. H., Hori M., Hovel K., Iken K., Moksnes P.

Knowledge to Action, Washington State'sO., Nakaoka M., O'Connor M. I., Olsen J. L.,

Strategic Response (ed. by Adelsman H. andSotka E. E., Whalen M. A., and Duffy J. E.,

Bender L. W.), Washington State Dept. Ecology,

2018b: Form-function relationships in a marine

Olympia, 100pp.

foundation species depend on scale: a shoot toWaycott M., Duarte C. M., Carruthers T. J. B., Orthglobal perspective from a distributed ecological

R. J., Dennison W. C., Olyarnik S., Calladine A.,

experiment.

Fourqurean J. W., Heck Jr. K. L., Hughes A. R.,, 127, 364-374.

Rumrill S. S. and Poulton V. K., 2004: Ecological role

Kendrick G. A., Kenworthy J. W., Short F. T.,

and potential impacts of molluscan shellfish

and Williams S. L., 2009: Accelerating loss ofculture in the estuarine environment ofseagrasses across the globe threatens coastal

Humboldt Bay, Ca, in “Final Annual Report toecosystems.

the Western Regional Aquaculture Center, 22”,12377-12381.

OR: Oregon Dept. State Lands, South Slough
Natl. Estuarine Res.Reserve, Charleston.

Wheat E. and Ruesink J. L., 2013: Commerciallycultured oysters (Smith S. R., 2016: Seagrasses as potential chemical) exert top-

down control on intertidal pelagic resources inrefugia for acidification-sensitive bivalves (MSWillapa Bay, Washington, USA.

thesis), Oregon State University, Corvallis, 66pp.

33-39.

Steele E. N., 1964: The immigrant oyster (, 106,., 81,

Wisehart L. M., Dumbauld B. R., Ruesink J. L., and) now known as the Pacific oyster, Warren's
Quick Print, Olympia.

Hacker S. D., 2007: Importance of eelgrassearly life history stages in response to oyster

Tallis H. M., Ruesink J. L., Dumbauld B. R., Hacker,
S. D., and Wisehart L. M., 2009: Oysters andaquaculture practices affect eelgrass density andproductivity in a Pacific Northwest estuary.

aquaculture disturbance.

.,

344, 71-80.
Yang S., Wheat E. E., Horwith M. J., and Ruesink J.
L., 2013: Relative Impacts of Natural Stressors., 28, 251-261.

on Life History Traits Underlying Resilience of

WADNR, 2017: Can eelgrass improve shellfish growthand pH in a halo around the meadow? Washington

Intertidal Eelgrass (.).

., 36, 1006-1013.

State Department of Natural Resources. https://Zu Ermgassen P. S. E., Spalding M. D., Blake B., Coen

www.dnr.wa.gov/publications/aqr̲aamt̲halo2̲

L.D., Dumbauld B., Geiger S., Grabowski, J. H.,

eelgrass.pdf

Grizzle, R., Luckenbach M., McGraw K., Rodney

Wagner E. L., Dumbauld B. R., Hacker S. D., Wisehart

W., Ruesink J. L., Powers S. P., and Brumbaugh

L. M., and Ruesink J. L., 2012: Density-dependentR., 2012: Historical ecology with real numbers:

effects of an introduced oyster,

past and present extent and biomass of anon a native intertidal seagrass,., 468, 149-160.

,

imperilled estuarine habitat.
, 279, 3393-3400.

108

Brett R. DUMBAULD, Jennifer L. RUESINK, and George G. WALDBUSSER
The authors review the role of shellfish aquaculture
Annotated bibliography

in US West Coast estuaries. While subsequent studies
have clarified this role and the interaction between(1) Barton A., Waldbusser G. G., Feely R. A., Weisberg

shellfish culture and other estuarine habitats likeS. B., Newton J. A., Hales B., Cudd S., Eudeline B.,

seagrass, general conclusions remain the same

Langdon C. J., Jefferds I., King T., Suhrbier A., andand suggest that most forms of shellfish culture as

McLaughlin K., 2015: Impacts of coastal acidification

currently practiced have only short term impacts inon the Pacific Northwest shellfish industry andWest coast US estuaries and habitats like eelgrass

adaptation strategies implemented in response.

are generally resilient to these changes.

, 28, 146-159.
This is the most recent review of the history(4) Hales B., Suhrbier A., Waldbusser G. G., Feely R.

and science underpinning the effects of changing

A., and Newton J. A., 2017: The carbonate chemistry

seawater chemistry on bivalve shellfish larvae andof the "Fattening Line," Willapa Bay, 2011-2014.

the impacts that have already taken place to the., 40, 173-186.

commercial shellfish aquaculture industry on the

The authors present detailed data on seawater

US West Coast. Multiple authors contributed to thischemistry (especially pCO2 and aragonite saturation

review which addresses a broad audience but covers

state) for Willapa Bay, Washington where Pacificthe leading research on direct effects to bivalve

oysters have been the mainstay of the oyster

larvae as well as monitoring seawater conditions andaquaculture industry for almost 100 years and there

adapting to these changes.

is a long term record of spawning and setting. They
reconstruct this record for a longer historical period(2) Dumbauld B. R. and McCoy L. M., 2015: The effectand their data suggest that recent conditions provide

of oyster aquaculture on seagrass ()

a smaller window of optimal conditions (low aragonite

at the estuarine landscape scale in Willapa Bay,saturation state and warm enough temperatures

Washington (USA).

for oyster spawning) than occurred historically.

., 7, 29-47.

The authors groundtruthed and analyzed aerial

While they did not sample larvae (see Ruesink

photographs taken in three separate years to build., 2018a below) and therefore canʼt confirm effects,

spatial layers for seagrass cover in Willapa Bay,they substantiate the complexity of measuring these

Washington, USA. They created spatial layers for

effects and atrributing them to a single cause in ashellfish aquaculture and several other factors suchvariable estuary.

as distance to the estuary mouth and intertidal
bathymetry that could influence eelgrass and then(5) Ruesink J. L., Sarich A., and Trimble A. C., 2018a:

built a model to evaluate eelgrass cover in areas

Similar oyster reproduction across estuarine regions

outside of shellfish aquaculture beds. This model wasdiffering in carbonate chemistry.

used to predict expected values within aquaculture

75, 340-350.

beds and compare this with actual values to estimate.,

These authors measured seawater chemistry

the effect of aquaculture. The approach is uniquein Willapa Bay,Washington, but unlike Halesin that it examined effects at the estuary scale and(2017), they also present simultaneously collected data.

over several years and the authors have submitted

on four cohorts of Pacific oyster larvae that werea second manuscript that uses a similar approach tocollected over three summers. The southern end ofasses sea level rise.

Willapa Bay has two arms which create distinctly
different characteristics because one is much more

(3) Dumbauld B. R., Ruesink J. L., and Rumrill S.

affected by riverine conditions that cause reduced

S., 2009: The ecological role of bivalve shellfish

aragonite saturation relative to the other. Oyster

aquaculture in the estuarine environment: A review

settlement differed greatly between cohorts, but they

with application to oyster and clam culture in West

did not find differences they could attribute to thisCoast (USA) estuaries.

different water chemistry and instead found thermal, 290, 196-223.

Planning for shellfish aquaculture and seagrasses
conditions were perhaps more important.

109

in Willapa Bay, Washington. They demonstrated thatwhile eelgrass responded to carbonate chemistry(6) Ruesink J.L., Yang S., and Trimble A. C., 2015:(increased tissue carbon up estuary where pCO 2

Variability in carbon availability and eelgrass (increased due to freshwater input), eelgrass) biometrics along an estuarine gradient in
Willapa Bay, WA, USA.

., 38, 1908-1917.

These authors collected data on eelgrass ( .

)and seawater chemistry along an estuarine gradientproduction was unchanged and instead responded
more to a gradient with more organic rich sediments
at this end.

水 研 機 構 研 報， 第 49 号，111 − 119， 平 成 31 年
Bull. Jap. Fish. Res. Edu. Agen. No. 49，111−119，2019111

Offshore mussel aquaculture: strategies for farming in the changing
environment of the Northeast U.S. shelf EEZ
Darien D. MIZUTA＊1,2, Mark S. DIXON＊1, Edward J. MANEY Jr.＊3, Mark FREGEAU＊3,
and Gary H. WIKFORS＊1

Abstract: In many aquaculture producing countries, there is increased interest in moving
aquaculture offshore, in particular to areas within national Exclusive Economic Zones. Off the US
northeast Atlantic coast, the blue mussel,, is a promising candidate for cultivation.

Environmental research has revealed the area to be suitable for successful mussel farming; yetcommercial activity has been slow to develop. This paper offers a brief overview of current
knowledge relevant to commercial blue mussel offshore aquaculture, focusing on U.S. Northeast
areas and addressing several points related to the activity as a potentially pivotal contributor to
American seafood production and safety.
Key words: offshore aquaculture, blue mussel, American Northeast, environmental conditions,
feasibility

Introduction

only 10 % of the national seafood demand; in 2014 the
US spent more than 20,317 million dollars on seafood

The northeast region historically has been an

imports. This trade imbalance marks the United

economic hub for fisheries in the United Sates. The

States as the largest seafood importer in the world,

region has a legacy of fisheries for lobster, cod, sea

ahead of the past leader Japan, because of the nationʼsscallops, groundfish, and quahogs. More recently,

limited domestic production (Kapetsky

shellfish aquaculture, mainly oysters and clams in

Fig.1). Imported species include salmon, shrimp, andcoastal areas, is expanding to occupy a central roleseveral shellfish, including the blue mussel, especiallyin regional fisheries and local cuisine. Increasingfrom Prince Eduard Island (PEI) in Canada, now theinterest in expanding shellfish aquaculture to

top bivalve import (USDA, 2018; Fig.2).

., 2013;

offshore areas prompted requests for lease permits

Offshore aquaculture activities are proposed to bewith regulatory agencies, the Arms of Corps andlocated in federal waters of the Exclusive Economic

NOAA, for mussel farms. As with any new activity,

Zones (EEZ), between 3 and 200 NM from shore

the initiative was anticipated to cause controversies;(Environmental Law Institute, 2015), but shore-

however, the perception of offshore aquaculture

based access requirements limit the activity to areas

is particularly negative in US because of a serious

with 100 m maximum depth (Kapetsky

misunderstanding about the different kinds of risks

Fig.3). Another possible limitation for aquaculture

associated with different forms of aquaculture anddevelopment is climate change. Expected

cultured species (Froelich., 2017). Concurrently,

warming and salinity changes, decreased pH, and

the American situation concerning seafood demand

accompanying indirect effects, are expected toand safety is unsettling. Domestic production meets

present many risks to farming operations, including:

2017年２月28日受理（Accepted on February 28, 2017）
Northeast Fisheries Science Center (NEFSC), NOAA, 212 Rogers Ave, Milford, CT 06460 U. S. A.
＊2National Academy of Sciences, 2101 Constitution Ave NW, Washington, DC 20418 U. S. A.
＊3
Cat Cove Marine Lab, Salem State University, 352 Lafayette Street Salem, MA 01970 U. S. A.
E-mail: darien.mizuta@noaa.gov＊1., 2013;

112

Darien D. MIZUTA, Mark S. DIXON, Edward J. MANEY Jr., Mark FREGEAU,
and Gary H. WIKFORS
increased incidence of diseases and mortalities, shifts
in local biodiversity, declining primary production,
altered time of spawning, increased harmful algal
blooms, and a variety of physiological responses
affecting mussel performance (Allison., 2011;Jo., 2016;., 2012; Pershing

Gobler., 2015; Hare., 2017).

Although research conducted at trial farms
addressed many fundamental aspects of mussel
farming with encouraging results (Langan andHorton, 2003; Lindell, 2016), these studies lacked theability to secure the development and establishment
Fig. 1. Map of New England area and the Long Islandwith depths up to 100 m that are prospective sites foroffshore aquaculture development, especially mussel
farming.

of an offshore aquaculture industry that is essentiallynon-existent more than a decade after initialresearch. In part, stalled commercial development
can be attributed to failure to convince prospective
entrepreneurs that risks can be managed andthat policy makers are ready to implement a
predictable permit process. Such communication
among diverse sectors is usually a long-term process.
This reticence on the part of both commercial andregulatory participants, and the aforementioned
risks associated with expected environmental
change, justifies the necessity for contemporary
research to address persistent doubts and knowledge
gaps and to encourage industry development;
while at the same time assuring protection of theenvironment at prospective farming areas. This

Fig. 2. American bivalve shellfish imports for theperiod of 2013 to 2017 (Department of Commerce,2018).

paper clarifies recurrent concerns about offshoremussel farming feasibility and builds on the current
state of knowledge to encourage the development ofsustainable offshore mussel farming activities in the
New England area and worldwide.
Why go offshore?
Seafood security can be met only with a national
fishery strategy that incorporates aquaculture
production, which thus far is mainly limited tocoastal areas. Space limitations and competition incoastal areas has triggered interest in expanding
aquaculture offshore (Klingler and Naylor, 2012).
Additionally, offshore areas also are considered to be
more advantageous locations because of potentiallyFig. 3. Comparison of US, Japan and China annual
expenditures with seafood imports. Values between
brackets show variation between both years (FAO,
2016).

compromised coastal water quality and sanitary
safety, as well as concerns about negative visual
impact and improved spatial use (Kapetsky., 2013).

Ecological concerns have been raised about shellfish

113

Offshore mussel farming in the Northeast United States
density in near-shore farms possibly contributing to

can recover quickly from the toxic effects after

top-down phytoplankton depletion starving local foodingesting another non-toxic phytoplankton (Galimany

webs (see for example: Gibbs, 2004). Such concerns., 2008). For domoic acid, produced by indigenous

are relatively small in areas with considerable water

species (Fuentes and Wikfors,

exchange, such as the open ocean (Comeau, 2013).

2013), the recovery takes place in a matter of hours

Furthermore, there is a consensus among the pioneer(Novaczek

researches on the topic that damaging bottom

security-related harvest closures and related costs

sedimentation resulting from shellfish farming inof those delayed harvests in comparison to otheroffshore areas is unlikely because of higher waterbivalve species such as oysters that accumulate andcirculation and greater depth facilitating dispersal ofeliminate toxins at slower rates (Shumway, 1990).

organic matter prior to sedimentation (Crawford
2003; Cheney., 1992), thus significantly shortening.,., 2010; Gallardi, 2014). Comparisons

between inshore and offshore sites also revealed the

Encouraging prospects, even in the face of climatechange challenges

increased distance from shore contributed to superior

The blue mussel was identified as a highlymussel quality related to epibiontes because offshore

vulnerable species in an assessment conducted

there are impoverished fouling communities, which

considering climate-change-induced projections foris largely attributed to limited dispersal abilities

several environmental factors such as temperature,(Atalahsalinity, air exposure, pH, and others (Hare., 2016). Offshore, the probability of

disease spread also is diminished (Röckmann.,

2016). Pershing.,. (2015) considered a section of2017), and parasites such as trematodes, commonly

the study area, the Gulf of Maine, as the quickest-

found in coastal mussels, were not present in farms

warming oceanic area in the world, with 3 possible

off Massachusetts where little biofouling was foundseawater warming scenarios ranging from 0.02

(Maney and Fregeau, 2018, pers. obs.). These results

to 0.07 °C/year. Considering these alarming

are similar to successful crops obtained from offshore

forecasts, a “habitat suitability assessment” wasfarms in Germany, where health conditions withwarranted to project the long-term sustainability

regard to parasites and fitness were described asof offshore aquaculture enterprises in this region.

excellent (Brenner

The importance of environmental conditions as a., 2012; Buck., 2017).

critical step in site selection was already portrayed
The Native Blue Mussel as a suitable species

in an FAO publication summarizing global offshore

There are environmental and economic benefits

aquaculture potential assessments, dedicated in its

to targeting mussels, in this case the Blue mussel

entirely to environmental conditions rather than, as a species for offshore aquaculture

prohibited/permitted areas based upon policyin the study area. Mussels, as suspension-feeding(Kapetsky., 2013).

bivalves, require no artificial feeds ‒ the origin of most

Mizuta and Wikfors (in review) performed anegative perceptions towards aquaculture. Mussels

habitat suitability assessment of southern New

assimilate in situ primary production, growing fast,

England and Long Island EEZ areas, using NOAAʼs

and promoting nutrient assimilation (Cheney.,open source climatological and remote-sensing data., 2017). In high-energy, open-of temperature and chlorophyll a from the period

ocean environments, mussel culture is performedof 2005 to 2012. The rationale for this work iswith submerged long-lines in middle-depths to avoid

based upon direct and indirect temperature effects,

the harsh conditions at the surface (Buck, 2007).

controlling energy allocation to reproduction, as

Mussel attachment to hard substrate by byssus

well as affecting byssus tenacity and adherence toorgans and threads constitutes another advantageous

farming ropes (Lachancecharacteristic of the species to suit offshore culture

provided new insights into the necessity that long-(Cheney

2010; Galimany., 2008). This study., 2010). When exposed to high levels oflines in an offshore farm be submerged to depths

toxicity during a harmful algal bloom (HAB) event,where temperature is suitable for the species. Results

which are common in the study area, the blue mussel

suggested mussel ropes be submerged during

Darien D. MIZUTA, Mark S. DIXON, Edward J. MANEY Jr., Mark FREGEAU,
and Gary H. WIKFORS

114

summer to a minimum of 15 m depth in northernareas and 20 m depth in southern areas of New
England where temperature is between 10-14 °C
and phytoplankton biomass is also abundant. During
winter, temperatures are around 5 °C, which do notinhibit filtration and are thus consistent with positive
growth. From those thresholds, deeper deployments
could be used to adapt to future warming scenarios,
providing confidence that mussel farming offshoreof southern New England and New York is resilient
to climate change by simple adjustment of culture
depth to adapt to changing seasonal conditions.
Phytoplankton to sustain growth is available in thearea, where winter/summer averaged concentrations
were above the limiting level of 0.5 mg/m3 determinedfor offshore mussel farming according to FAOʼsassessment (for details please refer to Kapetsky., 2013, page 53). Based upon the ideal depths
previously mentioned, mussels would take advantage
of maximum chlorophyll concentrations that are well
above the limiting level. For instance, in initial trials in
offshore areas in New Hampshire, mussels achieved
harvest size in 1.5 year and a 900-m rope produced
up to 12,000 kg mussel/year (Langan and Horton,
2003). In an offshore experimental farming site off
Cape Ann, Massachusetts, mussels grew better thancoastally at a rate of 0.5 mm/month (Maney

Fig. 4. Successful spat settlement on the header lineof the Cat Cove Marine Laboratory trial farm, proving
local availability of seeds and future possibility of
seed collection. The naturally set spats grew to 5.5
cm in 10 - 12 months.

.,

2018). Similarly, mussels of different species, blue,
Mediterranean, and greenshell mussels, reportedly

15 m depth that after 10-12 months of deployment

grew faster offshore in comparison to inshore control

produced 7 kg/m of mussels of good quality and taste

sites, a result attributed to better water exchange(Maneyand relatively more stable environmental conditionsin spawning season resulting from climate change,(Cheney., 2010). Nevertheless, there are ongoing

research is ongoing to better assess recruitment.

plans for validation of suitability of selected sites by

Previous spat collection experiments conductedassessing the performance of mussels in situ with

offshore New Hampshire also showed seed collection

a portable flow-through device employed in several

feasibility, reaching 2,000 seed/m when seed size wasmussel research projects near shore (described in

25 mm in shell length1 (Langan and Horton, 2003).

details in Galimany(Fig.4)., 2013).

., 2018). With the possibility of changes

One of the industryʼs known challenges is seed

The extreme rainfall and river flow events

availability; mussel seeds are rarely produced

associated with climate change prediction in coastalin hatcheries, and natural variation in wild spat

areas is expected to decrease resilience of mussels

availability is inevitable (Buck., 2017). In

in coastal estuaries, thus offshore allocation of

Massachusetts experimental spat collection has beenaquaculture can also mitigate for the decreased insuccessful; abundant seed could be collected during

suitable framing areas on the coast (Allison

summer in 2016 on submerged, longline ropes at2011). In relation to the robustness of the mooring

1

Length here is defines as the distance between shell umbo and extremity in the same valve.

.,

115

Offshore mussel farming in the Northeast United Statessystem, until present, the offshore farm system andwhich should decrease production costs. In truth, toattached mussels in the experimental off Cape Ann

be economically feasible domestic aquaculture needs

have withstood the local storms.

to match neither cost nor production dictated bycompetitors (Knapp, 2008), but it can take advantage

Opportunities for multifunctional marine structuresof the shift to value-added markets. There are otherPressures for adoption of clean energy in theapproaches to guarantee profit by exploring niche-

Northeast area has led to adoption of offshore

markets (Knapp, 2008), such as the selection forwind farm construction plans by Maine and New

traits possibly valued by consumers (for example a

Hampshire, and Massachusetts has at present angolden shell color) and informative labels that appeal

offshore area leased, but still not in use (Baranowski

to the increased willingness of US consumers to., 2017), while Rhode Island hosts an active

pay for environmentally-friendly and local products

windfarm off of Block Island. Thus, co-siting of wind

(Coddington, 1990; Kecinski

power and aquaculture offers an opportunity forthe relative lower value of common mussel products

clean energy and seafood production to be performedin relation to other shellfish. Because mussel

in the same area. The idea is not new and wascultivation is relatively more sustainable than otherproposed as early as the 1990ʼs in association withtypes of aquaculture, cultivated mussels are naturally

oil and gas platforms (Caswell, 1991; Kaiser.,“green.” The shift to cultivation in cleaner, US

2011) and most recently more focused mainly inopen-ocean areas and away from imports to locally-

co-location with windfarms (Van Den Burg.,

produced seafood increases traceability, boosting2017). Aquaculture would take advantage of platformthe potential for offshore-produced seafood to be

structures to moor farming systems and use spacemarketed as “sustainably-sourced” and “premium” inbetween turbines, a multi-use marine spatial planningseafood markets and restaurants.

., 2018), compensating

initiative already being promoted in both Germany
and The U.K. (Corbin., 2017; Stelzenmuller.,

Discussion2017). Concurrently, production of multiple species,
especially in different trophic levels, referred to as

Shellfish consumers tend to prefer seafood

integrated multitrophic aquaculture or IMTA, hasproduced in their own nation (see for example

been widely discussed. Species such as bivalves, fish,

Anacleto

deposit feeders, and marine plants each consuming

production in the U.S. is positive for the national

different artificial food, available phytoplankton,

economy and is expected to increase product quality

organic particulates, or dissolved nutrients, could, inavailable to American seafood consumers. Historically,

theory, maintain background nutrient levels throughfishery activities were mostly conducted withrecycling.

respect to demand, often overlooking environmental., 2014); therefore, increasing seafoodsustainability. In the present, such a careless attitude
Offshore mussel as a potential “niche-market”

has no place in local markets; therefore, it is in the

product

best interest of seafood producers, policy makers,

Despite the scientifically-based environmental

scientists, and the general public that aquaculture

suitability of waters offshore of the Northeast for

production is increased in the most sustainable way

mussel culture, investments in aquaculture may be

and be resilient to environmental changes, because

awaiting even more favorable economic prospects.

growth in seafood production is dependent upon

Although required farming technology is moreaquaculture. This is especially true for the U.S.

elaborate than coastal long-lines, and expectedly more

Northeast where fisheries and shellfish production

costly, economic analysis proved the offshore culture

have been important historical economic activities

feasibility, provided that good production is achieved

fostering many jobs and local culture.

(Kite-Powell, 2011). Offshore mussel farming has been

Offshore aquaculture studies in the U.S. havecharacterized by a shorter grow-out period, lower

pointed to the technical, ecological, and economic

intensity of biofouling, and less risk of predation losses,

feasibility of the activity that is already in advanced

116

Darien D. MIZUTA, Mark S. DIXON, Edward J. MANEY Jr., Mark FREGEAU,
and Gary H. WIKFORS

development in other nations such as Germany,
Belgium, Italy, UK, and France (Buck., 2017).

References

Even in face of climate change, offshore aquacultureof blue mussels seems to be adaptable and resilient

Allison E. H., Badjeck M. C., and Meinhold K., 2011:

with proper management. Accordingly, it should

The implications of global climate change for

not be a question of “whether to,” but a question

molluscan aquaculture, in “Shellfish Aquacultureof “how to” best promote development of offshore

and the Environment” (ed. by Shumway S. E.),aquaculture. Each country is expected to identify

Wiley-Blackwell, West Sussex, pp. 461-490.

most suitable species, locations, and cultivation

Anacleto P., Barrento S., Nunes M. L., Rosa R., andsystems (Cheney., 2010). For example, in Japan,

Marques A., 2014: Portuguese consumersʼ

where eating mussels is not part of the tradition,

attitudes and perceptions of bivalve molluscs.

offshore culture can be performed with the Japanesescallop (, 41, 168-177.

), using the already

Atalah J., Fletcher L. M., Hopkins G. A., Heasman

established knowledge developed for pearl oyster

K., Woods C. M. C., and Forrest B. M., 2016:

culture. The sharing of offshore aquaculture related

Preliminary assessment of biofouling on offshore

knowledge will allow for more rapid development ofmussel farms.

activity.

376-386.

., 47(3),This research article compiling updated offshore

Baranowski R., Oteri F., Baring-Gould I., and Tegenscientific knowledge and generalizing researchS., 2017: State of wind development in the United

findings is expected to support management andStates Region. Technical NREL/TP-5000-67624,

contribute to awareness in stakeholders and theReport National Renewable Energy Laboratory,

general population. Puzzling problems such as

U.S. Department of Energy.

farming designs that guarantee the safety of marine

Brenner M., Buchholz C., Heemken O., Buck B.

protected species ‑ should interactions occur ‑ that

H., and Koehler A., 2012: Health and growth

are abundant in the areas are still to be solved.

performance of blue mussels (With fast-developing technology and current) from two different hanging cultivation sites

integrated science-based management that follows

in the German Bight: A nearshore−Offshore

an environmental sustainability framework, however,offshore mussel aquaculture can be developedwith the benefit of lessons learned from decadesof incremental improvements in management of
capture fisheries (Finley, 2017).

comparison.

, 20, 751-778.

Buck B. H., 2007: Experimental trials on the feasibilityof offshore seed production of the mussel
in the German Bight: installation, technicalrequirements and environmental conditions.
., 61, 87-101.

Acknowledgment

Buck B. H., Nevejan N., Wille M., Chambers M.,
and Chopin T., 2017: Offshore and multiuse

The authors would like to thank the Japanesethaquaculture with extractive species: seaweeds

research team that organized the 45 United States-and bivalves, in “Aquaculture Perspective ofJapan National Resources Symposium in Hiroshima

Multi-Use Sites in the Open Ocean” (ed. by Buckfor their warm welcome. We also would like to thankB. H.and Langan R.), Springer Open, Switzerland,

Captain Bill Lee, FV Ocean Reporter (Rockport, MA)

pp. 23-69.

for his assistance, Legal Sea Foods as an industry

Caswell M., 1991: Co-development of coastal resources:

partner and financial supporter and to acknowledge

oil versus mariculture.

the supports received through a research travel9(1), 92-100.

.

,

grant from the NOAA Office of Aquaculture, andCheney D., Langan R., Heasman K., Friedman B., andthe postdoctoral fellowship from NRC Research

Davis J., 2010: Shellfish culture in the open ocean:

Associateship Program from the National Academy

lessons learned for offshore expansion.

of Sciences.

., 44 (3), 55-67.

117

Offshore mussel farming in the Northeast United States
Coddington W., 1990: Itʼs no fad. Environmentalism
is now a fact of corporate life, Marketing News,
October 15, 7pp.

recovery.

, 7, 702-708.

Galimany E., Rose J. M., Dixon M. S., and Wikfors G.
W., 2013: Quantifying feeding behavior of ribbed

Comeau L. A., 2013: Suspended versus bottom oyster

mussels () in two urban sites

culture in eastern Canada: Comparing stocking(Long Island Sound, USA) with different seston

densities and clearance rates.

characteristics.

, 410-

411, 57-65.

., 36, 1265-1273.

Galimany E., Wikfors G. H., Dixon M. S., Newell C. R.,

Corbin J. S., Holmyard J., and Lindell S., 2017:

Meseck S. L., HenningD., and Rose J. M., 2017:

Regulation and Permitting of Standalone andCultivation of the Ribbed Mussel (Geukensia

Co-located Open Ocean Aquaculture Facilities,

demissa) for nutrient bioextraction in an urban

in“Aquaculture Perspective of Multi-Use Sites inestuary.

the Open Ocean” (ed. by Buck B. H. and LanganR.), Springer Open, Switzerland, pp. 187-229.

., 51(22), 13311-

13318.
Gibbs M. T., 2004: Interactions between bivalve

Crawford C. M., Macleod C. K. A., and Mitchell I. M.,

shellfish farms and fishery resources.

2003: Effects of shellfish farming on the benthic
environment.

.

, 224, 117-140.

, 240, 267-296.
Gobler C.J., Doherty O. M., Hattenrath-Lehmann T. K.,

Department of Commerce, 2018: U.S. Census Bureau.

Griffith A. W., Kang Y., and Litaker R. W., 2017:

Aquaculture trade ‒ Recent years and top

Ocean warming since 1982 has expanded thecountries. Available at: https://www.ers.usda.

niche of toxic algal blooms in the North Atlantic

gov/data-products/aquaculture-data/.

and North Pacific oceans.

Environmental Law Institute, 2015: U.S. Army Corpsof Engineers Regulation of Offshore Aquaculture, 114(19), 4975-

4980.
Hare J., Morrison W. E., Nelson N. W., Stachura(February 2015). Available at: www.eli.org.

M. M., Teeters E. J., Griffis R. B., Alexander

FAO, 2016: SOFIA ‒ State of World Fisheries and

M. A., Scott J. D., Alade L., Bell R. J., Chute A.

Aquaculture, FAO, Rome. Available at: http://

S., Curti K. L., Curtis T. H., Kircheis D., Kocik

www.fao.org/fishery/sofia.

J. F., Lucey S. M., McCandless C. T., Milke L.

Finley C., 2017: All the boats on the ocean ‒ how

M., Richardson D. E., Robillard E., Walsh H. J.,

government subsides led to global overfishing,

McManus M. C., Marancik K. E., and Griswold C.

University of Chicago Press, Chicago, 206pp.

A., 2016: A vulnerability assessment of fish andFroelich H. E., Gentry R. R., Rust M. B., Grimm D.,

invertebrates to climate change on the northeast

and Halpern B. S., 2017: Public perceptions ofaquaculture: evaluating spatiotemporal patternsof sentiment around the world.

, 12(1),e0169281.

U.S. continental shelf.

, 11(2), e0146756.

Jo Q., Hur T. B., Cho K. C., Jeon C. Y., and Lee D. C.,
2012: Potential Influence of Climate Change on
Shellfish Aquaculture System in the Temperate

Fuentes S. and Wikfors G. H., 2013: Control of
domoic acid toxin expression in

Region.

., 28(3), 277-291.

Kaiser M. J., Snyder B., and Yu Y., 2011: A review

by copper and silica: Relevance tomussel aquaculture in New England (USA).

of the feasibility, costs, and benefits of platformbased open ocean aquaculture in the Gulf of., 83, 23-28.

Mexico.

., 54, 721-730.

Gallardi D., 2014: Effects of Bivalve Aquaculture on

Kapetsky J. M., Aguilar-Manjarrez J., and Jenness.

the Environment and Their Possible Mitigation:J., 2013: A global assessment of offshore

A Review.

mariculture potential from a spatial perspective,., 5(3), 105.

Galimany E., Sunila I., Hegaret H., Ramos M., andWikfors G. H., 2008: Experimental exposure

FAO Fisheries and Aquaculture TechnicalPaper 549, FAO, Rome.

of the blue mussel () to theKecinski M., Messerb K. D., and Peob A. J., 2018:

toxic dinoflagellate:

When cleaning too much pollution can be a bad

Histopathology, immune responses, andthing: a field experiment of consumer demandDarien D. MIZUTA, Mark S. DIXON, Edward J. MANEY Jr., Mark FREGEAU,
and Gary H. WIKFORS

118
for oysters.

, 146, 686-

695.

Sherwood G. D., and Thomas A. C., 2015: Slow
adaptation in the face of rapid warming leads toKite-Powell H. L., 2011: Business planning for mussel
longline operations. Offshore Mussel Aquaculture

collapse of the Gulf of Maine cod fishery.

,350(6262), 809-812.

Farming Workshop (WHOI, February 7, 2011).

Röckmann C., Lagerveld S., and Stavenuiter J., 2017:

Available at: http://www.mbl.edu/bell/scientific-

Operation and Maintenance Costs of Offshore

aquaculture/2011-mussel-farming-workshop/.

Wind Farms and Potential Multi-use Platforms

Klinger D. and Naylor R., 2012: Searching forin the Dutch North Sea, in “Aquaculture

solutions in aquaculture: charting a sustainable

Perspective of Multi-Use Sites in the Opencourse.

Ocean” (ed. by Buck B. H. and Langan R.),., 37, 247-276.

Knapp G., 2008: Economic Potential for U.S. Offshore
Aquaculture: An Analytical Approach, in

Springer Open, Switzerland, pp. 97-113.
Shumway S., 1990: A review of the effects of algal“Offshore Aquaculture in the United States:

blooms on shellfish and aquaculture.

Economic Considerations, Implications &., 21(2), 65-104.

Opportunities” (ed. by Rubino M.), NOAA

Stelzenmuller V., Gimpel A., Gopnik M., and Gee

Technical Memorandum NMFS F/SPO-103, U.S.

K., 2017: Aquaculture site-selection and marine

Department of Commerce, Silver Spring, 263pp.

spatial planning: the roles of GIS-based tools andLachance A. A., Myrand B., Tremblay R., Koutitonsky

models, in “Aquaculture Perspective of Multi-Use

V., and Carrignton E., 2008: Biotic and abiotic

Sites in the Open Ocean” (ed. by Buck B. H. andfactors influencing attachment strength of blue
mussels Mytilus edulis in suspended culture.
.

., 2, 119-129.

top countries. Available at: https://www.ers.

Langan R. and Horton F., 2003: Design, Operation andeconomics of submerged longline mussel culturein the Open Ocean. Bull.

Langan R.), Switzerland, pp. 131-148.
USDA, 2018: Aquaculture trade ‒ recent years and.

,103(3), 11-20.

usda.gov/data-products/aquaculture-data.aspx.
Van den Burg S. W. K., Kamermans P., Blanch M.,
Pletsas D., Poelman M., Soma K., and Dalton G.
J., 2017: Business case for mussel aquaculture

Lindell S., 2016: Hatchery and nursery for improved
production of blue mussels. Annual Report of

in offshore wind farms in the North Sea.
, 85, 1-7.

the Northeast Fisheries Aquaculture Center,for the period of 2015 and 2016, United States

Annotated bibliography

Department of Agriculture, Maryland, pp. 1630. Available at: http://agresearch.umd.edu/(1) Allison E. H., Badjeck M. C., and Meinhold K.,

nrac/annual-reports#overlay-context=nrac/

2011: The implications of global climate change forpublications-0.

molluscan aquaculture, in “Shellfish Aquaculture andManey E. Jr., Fregeau M., and Lee B., 2018: First
year results from offshore shellfish aquacultureTh

the Environment.Shumway” (ed. by Shumway S. E.),
Wiley-Blackwell, West Sussex, pp. 461-490.

Milford

The authors of this chapter instead of developing

Aquaculture Seminar, 8-10 January, NOAA

models predicting possible climate changes, discuss

Fisheries, Shelton.

the impacts of the climate to shellfish aquaculture

in Federal waters of the Atlantic. 38

Novaczek I., Madhyastha M. S., Ablett R. F., Donald

and market based on an extensive review of different

A., Johnson G., Nijjar M. S., and Sims D. E., 1992:

relevant chemical and physical elements affecting

Depuration of domoic acid from live blue mussels

the oceans. Authors also suggest mitigation and(management plans that can be applied for the

).

, 49,

312-318.

sustainability of the shellfish farming.

Pershing A. J., Alexander M. A., Hernandez C.
M., Kerr L. A., Le Bris A., Mills K. E., Nye J.

(2) Buck B. H. and R. Langan R. (Eds.), 2017:

A., Record M. R., Scannell H. A., Scott J. D.,

Aquaculture Perspective of Multi-Use Sites in theOffshore mussel farming in the Northeast United StatesOpen Ocean, Springer Open, Switzerland, 404pp.

119

and protected species. Exposure factors were defined

The entire book, to which we refer many chapters,

as: ocean surface temperature (upper 10 m), ocean

is an important compilation of the status of researchsurface salinity (upper 10 m), surface air temperature,

on general offshore aquaculture around the world,

precipitation, surface pH (upper 10 m), currents, andwith each chapter treating relevant issues such as

sea-level rise. Results showed high vulnerability

different species, technical designs, experimentalof diadromous and benthic invertebrate species,

trials, management and related policy.

including the blue mussel, while positive effects
were identified to some species. The findings of this(3) Hare J., Morrison W. E., Nelson N. W., Stachura

paper are important to enable appropriate adaptive

M. M., Teeters E. J., Griffis R. B., Alexander M. A.,

fisheries and conservation management.

Scott J. D., Alade L., Bell R. J., Chute A. S., Curti
K. L., Curtis T. H., Kircheis D., Kocik J. F., Lucey S.

(4) Kapetsky J. M., Aguilar-Manjarrez J., and Jenness

M., McCandless C. T., Milke L. M., Richardson D. E.,

J., 2013: A global assessment of offshore mariculture

Robillard E., Walsh H. J., McManus M. C., Marancik

potential from a spatial perspective, FAO Fisheries

K. E., and Griswold C. A., 2016: A vulnerability

and Aquaculture Technical Paper 549, FAO, Rome.

assessment of fish and invertebrates to climatechange on the northeast U.S. continental shelf.
, 11 (2), e0146756.

In this publication from FAO, offshore aquaculture
is assessed in an international context addressing
species and desirable conditions for farming, besides

Authors in this study conducted a climate

potential for different areas in the world. It is andvulnerability assessment, as impacts to abundance orintroduction to siting decision and sustainableproductivity, on 82 fish and invertebrate species inaquaculture development.

the Northeast U.S. Shelf including exploited, forage,

水 研 機 構 研 報， 第 49 号，121 − 127， 平 成 31 年
Bull. Jap. Fish. Res. Edu. Agen. No. 49，121−127，2019121

Effects of fish aquaculture on inorganic nutrient levels in Gokasho Bay
Satoshi WATANABE＊1, Masayuki MINAKAWA＊2, Yuka ISHIHI＊1, Natsuki HASEGAWA＊1,
and Toshie MATSUMOTO＊1

Abstract: Eutrophication derived from aquaculture effluent and consequent environmental
deterioration are becoming increasingly problematic in many parts of the world. On the other hand,eutrophication has been reduced in coastal waters of Japan because of mitigation efforts over the
past thirty years. While such efforts have positive effects on maintaining environmental integrity,
excessive reduction of nutrient load to the coastal environment is thought to have reduced the
productivity of many fishery resources and unfed aquaculture. Our hypothesis is that putting
aquaculture effluent into practical use enhances the production of coastal fisheries and unfedaquaculture. To acquire basic information on the influential extent of aquaculture effluent oncarrying capacity of coastal waters, environmental surveys were conducted to investigate thebehavior of nutrients and primary production covering the whole bay area and more intensively
around the red seabream,, aquaculture cages in Gokasho Bay, Mie, Japan. Seawater

samples were collected monthly at 3 depths (surface, mid-layer and bottom) at 19 points in the bay,and seasonally at surface and depth of 5 m (i.e. midpoint of the cage depth) at 47 points approximately
20 m apart from one another around the red seabream aquaculture cages. The concentration of thefollowing nutrients was analyzed: dissolved inorganic nitrogen (DIN: NH4-N, NO2-N, NO3-N), PO4-P
and SiO2-Si. A CTD was used to obtain the vertical profile of temperature, salinity, dissolved oxygen(DO), and chlorophyllfrom the surface to the bottom. Although the DIN-N and DO levels in

December 2016 were comparable to those from the same month in 1980s where aquaculture wasmore prosperous, the PO4-P level was an order of magnitude lower probably due to diminishedaquaculture production and improved feeding management, including the switch from raw bait toformulated feed. During a diatom bloom observed in November 2016, the depletion of SiO2-Si impliedthat the availability of Si, but not N or P, was the limiting factor for the diatom growth in Gokasho
Bay. There were spots with higher NH4-N levels at the center and 20 m outside the red seabream
cage area in January 2017. The chlorophyll

level was higher and NO3-N was lower around thecages than in the surrounding water. The observed lower NO3-N concentration may indicate thatthe enhanced primary production triggered by the NH4-N supply from the aquaculture effluent
rapidly consumed not only NH4-N but the background NO3-N in the area, thereby indicating that
DIN-N excreted from red seabream may not travel a long distance from the cages before absorbed
by primary producers. In order to fertilize seaweed with red seabream aquaculture effluent, theseaweed should be cultured near the fish cages. The elevation of chlorophyll

indicates thepossibility of productive co-culture of red seabream and bivalves.
Key words: dissolved nutrients, oligotrophication, primary production

2018年８月31日受理（Accepted on August 31, 2018）
National Research Institute of Aquaculture, Japan Fisheries Research and Education Agency, 422-1 Nakatsuhamaura, Minamiise, Mie, 516-0193,
Japan＊2
National Research Institute of Aquaculture, Japan Fisheries Research and Education Agency, 224-1 Hiruda, Tamaki, Mie, 519-0423, Japan
E-mail: swat@affrc.go.jp
＊1

122

Satoshi WATANABE, Masayuki MINAKAWA, Yuka ISHIHI, Natsuki HASEGAWA,
and Toshie MATSUMOTO
Introduction

Such aquaculture effluents used to be a cause of
eutrophication of water and sediment resulting inWith the global expansion of aquaculture

environmental deterioration. However, eutrophication

production, eutrophication derived from aquaculture

has subsided due to reduced aquaculture intensity

effluent and consequent environmental deteriorationand improved feeding techniques.

are becoming increasingly problematic in many

Our hypothesis is that moderate eutrophication

parts of the world. On the other hand, eutrophication

is favorable for primary production and putting

has been reduced in coastal waters of Japanaquaculture effluent into practical use enhances the

because of mitigation efforts over the past thirty

carrying capacity and, thus, production of coastal

years. The Total Pollutant Load Control Systemfisheries and unfed aquaculture. This paper is a

(TPLCS) has been implemented for water pollution

partial report of the long-term periodical monitoring

management of Seto Inland Sea, Tokyo Bay and Iseof water quality in Gokasho Bay, Mie, Japan, theBay since 1979; it regulates the allowable amountresults of which will be used as a basis for designingof terrestrial nitrogen/phosphorus discharge to theeffective integrated multi-trophic aquaculturesea. Allowable discharge of aquaculture effluent to(IMTA) techniques (Chopin, 2006).

the surrounding environment has been regulated by
Sustainable Aquaculture Production Assurance Act

Materials and Methods(APAA) issued by the Fisheries Agency since 1999.
Aquaculture operators set the stocking density of

To acquire basic information on the influential

their commodities in consultation with prefecturalextent of aquaculture effluent on carrying capacity

government under APAA.

of coastal waters, environmental surveys have been

While such efforts have positive effects on

conducted to investigate the behavior of nutrients

maintaining environmental integrity, excessive

and primary production covering the whole area of

reduction of nutrient load to the coastal environment

Gokasho Bay, Mie prefecture, Japan, and also moreis thought to have reduced the productivity of many

intensively around the red seabream (fishery resources and unfed aquaculture in Japan.

aquaculture cages in Hasamaura Cove in Gokasho

The oligotrophication of coastal waters has reduced

Bay.

)

the carrying capacity of the coastal ecosystem,

Seawater samples have been collected monthly at

resulting in a continuous decline in fishery resources

3 depths (surface, mid-layer and bottom) at 19 points

and reduced productivity in unfed aquaculture,in the bay, and seasonally at surface and depth ofwhich relies on naturally available nutrition. The

5 m (i.e. midpoint of the cage depth) at 47 points

reduction of benthic fish fisheries production in Seto

approximately 20 m apart from one another around

Inland Sea, for instance, is considered to be related

the red seabream aquaculture cages using a Kitahara

with the declining dissolved inorganic nitrogen (DIN)

water sampler since November 2016. An aliquot (12level in the coastal water (Handa and Harada, 2012).

ml) of the seawater samples were filtered with a 0.2

Bleaching of) thalli due toµm syringe filter and stored at -30℃ until analyses.

insufficient DIN has been problematic in Seto Inland

The concentration of the following nutrients has

Sea and Ariake Sound since 1990s, causing a great

been analyzed: dissolved inorganic nitrogen (DIN:(

economical loss to thefarmers (Nishikawa andHori, 2004; Yamamoto, 2003).

NH4-N, NO2-N, NO3-N), PO4-P and SiO2-Si with an autoanalyzer (TRAACS 800, Bran+Luebbe).

Fed aquaculture of finfish usually has high feed

A CTD (RINKO profiler, JFE Advantech) has been

conversion ratio (FCR). The FCR of red seabream

used to obtain the vertical profile of temperature,(), for instance, is between about 2.1 andsalinity, dissolved oxygen (DO), and chlorophyll

2.7 when fed artificial diet (Furukawa, 2008; Ono andat depths of every 10 cm from the surface to

Nakahara, 2009), meaning that it takes 2.5 kg (i.e. FCR

the bottom. The DO concentration was calibrated= 2.5) of feed to produce 1 kg of fish. Thus, 1.5 kg ofusing more precisely analyzed values with a DO

the feed is wasted as feces, metabolites and leftover.

meter (MM-60R, TOA DKK) in the laboratory.

123

Effects of aquaculture on nutrient environment

0 40 80
0 40 80
0 40 80

0
4
8

0
4
8

0
4
8

0
8
16

0 40 80

0
8
17

0
15
30

0 40 80
0
9
18

0
8
16

̑

0 40 80011
22
00 40 80

0
8
17

0
15
27
0 40
0 80
0
11
21

DIN-N (Pg/l)
612Depth (m)

0
7
14

0
0 40
08
80
08
17
1
7

0 40 80
0
̑
̕
0 4
40
08
80
0

0
10
0 40 8019

0 40 8800
80 40 80 16

Hasamaura Cove04
90 40 80

0 40 80

Red seabream cages

0 40 8000 40 800714BlueĮn tuna cages

Gokasho Bay

1 km

0 40 800
14
27

Fig. 1. Dissolved inorganic nitrogen (DIN-N) concentration in Gokasho Bay, Mie, Japan in
December 2016.

The chlorophyll

concentration was obtained

area were more than double of those at the mouthby converting the fluorescence intensity of theof Gokasho Bay opening to the Pacific. The DIN-N

CTD, using the relationship between the CTD

concentration did not differ with the depth at thereadings and chlorophyll

concentration of cultured

bay mouth, which is considered to be under a strong) measured with a

influence of outer seawater. The PO4-P concentration

chlorophyll fluorometer (10 AU fluorometer, Turnershowed similar trends with DIN-N (Fig.2). These

Designs).

indicate that effluent from red seabream aquaculture

phytoplankton (Horizontal distribution of the nutrients andelevates dissolved inorganic N and P concentrations

around the red seabream aquaculture

in Hasamaura Cove. Higher nutrient concentrations

cages were obtained by R software with the Akima

in the bottom water may be partially attributable to

add-on package for linear interpolation and mapping.

decomposition of sediment organic matter on the sea

chlorophyll

bottom deposited from the fish culture.
Results and Discussion

A comparison of nutrient levels in the aquaculturearea in December was made between 2016 and 1980s.

The DIN-N (i.e., the sum of NH4-N, NO2-N, NO3-N)

The National Research Institute of Aquaculture

levels were often found to be higher in the area

conducted water nutrient monitoring in Gokasho

with red seabream aquaculture cages and the inner

Bay in late 1980s (Sugiyama., 1991), where redpart of Hasamaura Cove, especially in the bottom

seabream and yellow tail ()

water in our monthly water parameter monitoring.

aquaculture was more intensive than recent years

An example of the DIN-N concentration distribution

and self-pollution was an issue (Abo, 2000). The DIN-N

in December 2016 is shown in Fig.1. The DIN-N

concentration was reduced by about 25% from 1980s

concentrations in the red seabream aquaculture(the mean of 1986 - 1988) to 2016 (Fig.3). The PO4-P

124

Satoshi WATANABE, Masayuki MINAKAWA, Yuka ISHIHI, Natsuki HASEGAWA,
and Toshie MATSUMOTO

Fig. 2. Dissolved inorganic phosphate (PO4-P) concentration in Gokasho Bay, Mie, Japan in
December 2016.

concentration was reduced by about 80 % (Fig.3).
The reduction in the nutrient levels may be relatedwith the reduction of aquaculture production in thearea. The large reduction of PO 4-P concentration
may also be attributable to the shift of aquaculture
feed from raw bait to formulated feed. The DOlevel has moderately increased in the bottom water.
Supposedly, because of the reduced organic loads,
and a reduction in harmful algal blooms and hypoxiaof the bottom water which have no longer been
rampant in Gokasho Bay in recent years.
However, diatom blooms sporadically occur inGokasho Bay. In the case of a diatom bloom observedin November 2016, chlorophyll

concentration was

higher in the surface and mid-layer water in the
red seabream aquaculture area compared with theFig. 3. Dissolved inorganic nutrient and dissolved
oxygen levels near red seabream ()
aquaculture cages in December 2016 and 1980s. Data
for 2016 are from this study, and data from 1986 to
1988 are after Sugiyama. (1991).

other locations in Gokasho Bay, reaching about 27µg/l (Fig.4). Despite the diatom bloom, neither DIN-N
nor PO4-P were depleted in the aquaculture area,factor for diatom production in this area. Reduced

but SiO2-Si was depleted (Fig.5). Nutrient load from

Si discharge from rivers to the marine environment

the aquaculture seemed to maintain relatively highassociated with the entrapment at dams is perceived

DIN-N and PO4-P concentrations at the depletion

to enhance production of non-diatom species

level of SiO2-Si, probably making SiO2-Si the limiting

including harmful red tide species (Harashima, 2008).

Effects of aquaculture on nutrient environment

Fig. 4. Chlorophyll

125

concentration in Gokasho Bay, Mie, Japan, in November 2016.

Oligotrophication is problematic in some coastal
waters in Japan, reducing unfed aquaculture
profitability of some bivalves and seaweed (Handa
and Harada, 2012; Yamamoto, 2003). In Gokasho Bay,Hasamaura Cove with red seabream aquaculture
had relatively higher dissolved inorganic N and P
concentrations, which may be used to enhance unfedaquaculture productivity through integrated multitrophic aquaculture (IMTA) approach (Robinson andChopin, 2004; Chopin, 2006).
During the intensive water analysis around thered seabream aquaculture cages in Hasamaura Covein January 2017, there were spots with a higher
NH4-N level at the center and 20 m outside the cagearea (Fig.6). The chlorophyll

level was higher,

and NO 3-N was lower around the cages than in

Fig. 5. DRelationship between chlorophyll
concentration and DIN-N, PO 4 -P and SiO 2 -Si
concentrations during a diatom bloom in Gokasho
Bay, Mie, Japan, in November 2016. Dotted red circles
indicate the data from the red seabream aquaculturearea in Hasamaura Cove.

the surrounding water (Fig.6). The observed lower
NO3-N concentration may indicate that the enhanced
primary production triggered by the NH4-N supply

cages, being readily consumed by localized primaryfrom the aquaculture effluent rapidly consumed not

production. In Gokasho Bay, green alga (only NH4-N but also the background NO3-N in the) is intensively cultured. To effectively fertilize

area. Under this assumption, DIN-N excreted fromthe seaweed with the red seabream aquaculture

red seabream may not travel a long distance from theeffluent, the seaweed should be cultured near theSatoshi WATANABE, Masayuki MINAKAWA, Yuka ISHIHI, Natsuki HASEGAWA,
and Toshie MATSUMOTO

126

Fig. 6. Horizontal topography of NH4-N, NO3-N, chlorophyll and PO4-P concentrations at
5 m depth around the red seabream aquaculture area. Dotted red rectangles indicate thearea with red seabream cages.

cages. The elevation of chlorophyllin the fish cagearea indicates that the red seabream aquaculture canincrease food availability for aquaculture of bivalves,
such as Pacific oyster (clam (

major.

, 74, 902-903. (inJapanese)
Handa H. and Harada K., 2012: Setonaikai toubu) and Manila(harimanada) no eiyouen kankyou to gyogyou). Field experiments(nutrient environment and fishery in Easternshould be further carried out to design an effective

Seto Inland Sea)

IMTA system including these species.

Japanese), 199, 132-141. (inHarashima A., 2008: Role of the Diatom-Silicon Process
Referencesin Marine Ecosystem. .

.

., 8,

9-16. (in Japanese)
Abo K., 2000: Fluctuation of hypoxic water masses in

Nishikawa T. and Hori Y., 2004: Effects of nitrogen,a fish farming ground of semi-enclosed estuaryphosphorus and silicon on the growth of thefacing the ocean.

diatom.,29, 141-216. (in Japanese with English abstract)
Chopin T., 2006: Integrated multi-trophic aquaculture:caused bleaching of

seaweedisolated from Harima-Nada,

Seto Inland Sea, Japan.

,

what it is, and why you should care and70, 31-38. (in Japanese with English abstract)donʼt confuse it with polyculture, Northern

Ono S. and Nakahara N., 2009: Current Conditions

Aquaculture, July/August, pp.4.
Furukawa K., 2008: Utilization of self-feeding to thecommercial cultivation of red sea bream Pagrus

and Issues in the Fish Aquaculture Industry.
., 57, 149-164. (in Japanese withEnglish abstract)Effects of aquaculture on nutrient environment
Robinson S. M. C. and Chopin T., 2004: Defining the127ammonium-N as the main component may be suitableappropriate regulatory and policy frameworkforaquaculture. The nitrogenous fertilizer should

for the development of integrated multi-trophic

be provided toaquaculture practices: summary of the workshop

duration to avoid induction of phytoplankton bloom.

at a low concentration over a longand issues for the future.
(2) Kakehi S., Fujiwara T., and Yamada H., 2005:., 104-3: 4-10, 73-84.
Sugiyama M., Tanaka N., Asakawa A., Sakami T.,

Seasonal variation in the nutrient standing mass

Iikura T., Toda T., Kitamura S., Honjo T., Shiraishi

and nutrient budget of Ise Bay.

M., Awaji M., Yamamoto S., Sako H., and Kumada(Oceanography in Japan), 14, 527-540.

H., 1991: Records of oceanographic observation in

The authors estimated the standing mass ofGokasho Bay, Mie Prefecture (1986-89), National

dissolved inorganic nitrogen (DIN) and dissolved

Research Institute of Aquaculture, Fisheriesorganic phosphorus (DIP) by the linear regression

Agency, Mie, 49pp. (in Japanese)of apparent oxygen utilization (AOU) or the

Yamamoto T., 2003: The seto inland sea -interpolation of the surface and bottom nutrient
concentrations to elucidate the seasonal variations

eutrophication or oligotrophication?.

in Ise Bay, Japan. The DIN standing mass in the, 47, 37-42.

bottom layer ranged from 1500 to 2600 t, tending tobe higher in summer than in winter. The DIN was

Annotated bibliographysmaller in the surface layer than in bottom layer in(1) Yamamoto T., 1992: Constant uptake ofsummer, and comparable between the two layers inammonium-N and nitrate-N bywinter. The DIP standing mass showed more distinct

thalli.

., 31,

seasonal trend. It was 200 t in surface and bottom
layer in winter; whereas it increased to 400 t in the155-159.
The author experimentally determined thesurface and 800 t in the bottom later in summer.

uptake rates of ammonium-N and nitrate-N by

The temporal change of the standing mass of the15

Nnutrients was more dependent upon biological and) is anchemical processes than physical processes such asimportant seaweed in Japan. Specific uptake rateseawater exchange. Chlorophyll level is inverselyof ammonium-N (0.0017/hr) was more than 8 times

related with DIN and DIP in the surface layer

higher than that of nitrate-N (0.0002/hr). The uptake

in summer, but DIN and DIP are not completely

rates were constant over the 120-minute experiment,

synchronous. The DIP seemed to be released fromunlike in the case of phytoplankton that is known to

the sea sediment in summer where hypoxic water is

rapidly absorb nutrients to satiation. Fertilizers withformed in the bottom layer. Denitrification seemed to(currently
as a tracer.

)

using
(laver or

take place year-round.

水 研 機 構 研 報， 第 49 号，129 − 134， 平 成 31 年
Bull. Jap. Fish. Res. Edu. Agen. No. 49，129−134，2019

129

Challenges and opportunities of IMTA in Hawaii and beyond
Cheng Sheng Lee＊

Abstract: Available consumable seafood for 7.3 billion population in 2014 was 20 kg per capita (FAO,
2016). To maintain this level of seafood supply for expected 9.7 billion population in 2050, the total
world seafood supply requires additional 48 million metric tonnes. With the stagnant yield from
capture fisheries, the increase has to come from aquaculture. Although the annual growth of
aquaculture production has slowed down, theoretically aquaculture production will reach thetargeted production level. However, current intensive mono-aquaculture practices have faced thechallenges of sustainability and must change its operation to meet the criteria of sustainable
development defined and adopted by UNʼs 193 Member in 2015. UN members adopted the 2030
Agenda for Sustainable Development and call for an integrated approach that addresses all three
dimensions of sustainable development (economic, social and environmental).
Current aquaculture practices consume nature resources and compete with each other. Ecosystem
based aquaculture management is essential to co-exist with other social activities and to efficiently
utilize natural resources for food production and conservation of nature stocks. Integrated multitrophic aquaculture (IMTA), an old concept with new knowledge, appears to be the answer tosustainable development in aquaculture. IMTA practice combines the cultivation of fed aquaculture
species, and extractive aquaculture species (both organic and inorganic ones) to reduce wastes andto create balanced eco-systems. Additionally, IMTA can play important roles in disease control andmanagement, climate change mitigation, and others. As a result, IMTA has received more and more
attentions at the turn of the century. However, the feasibility of IMTA comparing to mono-culture
has yet to be documented.
This presentation discusses the sustainability of IMTA by reviewing the practice of IMTA
concept in traditional Hawaii aquaculture back to 1000 A.D. to current practices in the U.S. andbeyond; updates US-Korea bilateral IMTA project; and challenges of IMTA.
Key words: IMTA, Aquaculture, Sustainability, Hawaii

Introduction

to cultivate the seas just as we do the land. If we do
it right, aquaculture can be one more step toward

Among food production sectors in agriculture,saving ourselves. And if we do it well, we may

seafood is the only one still rely on wild caught fish aseven enjoy the taste of it.” With the effort by many

the main supply channel. Indeed, the harvest of fish

stakeholders in seafood business, aquaculture has

has reached the peak and plateaued around 90 million

shown impressed growth (FAO, 2016). In 2014, themetric tons since early 1990 (Fig.1, FAO, 2016).

statistics showed aquaculture supplied half of edible

However, as stated by Walsh (2011) “If we're all going

seafood. Capture fisheries used to contribute major

to survive and thrive in a crowded world, we'll needseafood to human consumption as show in this slide

2018年８月31日受理（Accepted on August 31, 2018）
Center for Tropical and Subtropical Aquaculture
c/o HNFAS, College of Tropical Agriculture and Human Resources
University of Hawaii at Manoa
1955 East West Road, Ag. Sci. 216, Honolulu, HI 96822, U. S. A.
E-mail: chenglee@hawaii.edu

＊

130

Cheng Sheng Leefrom aquaculture to meet the demand if the seafood
consumption rate remains the same. However, thedemand for seafood will probably increase as the
population structure changes and several challenges
may hamper the increase in aquaculture production.
For the sustainable development of aquaculture,
integrated approach to overcome the challenges
facing aquaculture development is essential. In 2015,
193 members of United Nation adopted the “2030Fig. 1. World seafood production from 1950 to 2014.
(FAO, 2016)

Agenda for Sustainable Development” (https://www.un.org/sustainabledevelopment/developmentagenda/) and its 17 Sustainable Development Goals.
They call for an integrated approach that addresses
all three dimensions of sustainable development:
economic, environmental and social factors. At
Global aquaculture alliance (GAA) 2013 meeting,the concluded five major challenges were: healthand disease management, feeds, environmental/social Accountability, investment capital and market
support. Therefore, a sustainable aquaculture has toFig. 2. Contribution to human seafood consumption
from capture and aquaculture. (FAO, 2016)

be integrated approach and to address key challenges
for the development. This paper discusses a practicewhich may meet all criteria to be a sustainable one.
Integrated Multi-Trophic Aquaculture (IMTA)
Integrated Multi-Trophic Aquaculture (IMTA) is
a new term (Neori., 2004) for an old concept.

Polyculture has been practiced in China since 2200
BC to fully utilize the nutrients inside an enclosed
pond. IMTA takes one step further to reduce theecological footprint from aquaculture practice and at
the same time to create economic diversity and to
Fig. 3. World population growth and seafood supply.
(FAO, 2016)

call for social acceptability (Troell., 2009). IMTA,

therefore, equals to polyculture but polyculture is notnecessary an IMTA. Since aquaculture can be theuntil 2014 (Fig.2). From 1950 to 2014, the food supply

farming of several aquatic organisms which interact

increased faster than the population increased (Fig.3).

through water in shared or connected systems,

The available seafood for the 7.3 billion population in

one organism wastes can be another resource

2014 was 20 kg per person. If the projected 9.7 billion(Butterworth, 2010).

population in 2050 is correct, we need additional 48

When feed is offered to an aquatic organism, only

million MT seafood to meet the 20 kg per capita level

portion of digested nutrients is incorporated into

in 2014. Average annual growth rates for aquaculturebiomass of the target organism. The rest of unused

were over 10 % in both 80s and 90s (FishStat.

digested nutrients, along with indigestible nutrients

FAO, 2016). It has decreased since but still aroundand un-eaten feed will increase nutrients levels andan impressed rate of 6 %. The rate may decrease

become solid waste in surrounding environment

in the future but we should have enough seafood(Reid., 2007). The quality and quantity of total

Challenges and opportunities of IMTA

131

Fig. 4. Conceptual diagram of the integrated multitrophic aquaculture
system. (Zhang., 2016)

Table 1. Key species have been in IMTAin IMTA are fed aquaculture and extractive
aquaculture. The diagram presented by Zhang

Key Species Cultured in Modern IMTA Systems(Integrated mariculture, FAO-529)
Cold Seawater

Temperate Sea water

Salmo
Oncorhynchus sp.
Gadus

Pagraus major
Sparus aurata
Dicentrarchus labrax
Lates calcarifer

Crassostrea sp.
Mytilus sp.
Haliotis rufescens
HamarusStrongylocentrotus
Paracentrotus
Laminaria sp.
Macrocystis sp.
Porphyra sp.
Saccharina
Undaria
Nereis, Arenicola, sea
cucumberWarm Seawater

Sparus aurata
Lates calcarifer
Mugil cephalus
ChanosEpinephelus sp.
Mercenaria
Crassostea gigas
Crassostea sp.
Tapes japonica
Ostrtrea edulis
Haliotis diversicolor
Mytilus
Penaeus spp.
Ruditapes semidecussatus
Penaeus spp.
Gracilaria sp.
Gracilaria changii
Ulva sp.
Ulva lactuca
Kappaphycus

Nereis, Arenicola, sea
cucumber

Nereis, Arenicola,sea
cucumber, mullet. (2016) gives a good illustration (Fig.4). IMTA canbe implemented in freshwater system or saltwater
system at either land based or open water operation.
Depending on the water quality and location, a wide
variety of species have been tested in IMTA system
as shown in Table 1 (Soto, 2009). Target species cancover all cultivated species from plankton, plant to
invertebrate and vertebrate species. The optimal
species combination should be based on meeting thegoal of sustainable development mention above.
IMTA in Hawaii and USA
The “Ahupuaʼa” is the basic self-sustaining unit inancient Hawaii land system, recognizes the connection
between resources from mountain to the sea. It has
the resources the human community needed andnutrients released are determined by the cultivatedemphasizes the interrelationship in the activities of

species and the dominant fraction is in a dissolved

daily and seasonal life. Ancient Hawaiian fishpond

form, particular for nitrogen (Troell., 2003). To

within this land management system also practices

fully utilize all nutrients as a result of feeding, IMTA

this interrelationship concept to stock aquatic species

practice composes of species at different trophic

within the aquatic compartment surrounding bylevels may be the solution. An essential component

coral reef and volcano rock. All target species will

132

Cheng Sheng Lee

compromise with each other on nutritional needs

Other practice can be found at the publication by

and balance the essential optimal ecosystem for all in

Bellona (2013) and Soto (2009).

the pond. Species including carnivorous, herbivorous,
omnivorous, and seaweed can be found in Hawaiian

Challenges for IMTA

fishpond as stated in Moliʼi fishpond (Sato and Lee,2007). However, number of Hawaiian fishpond has

The above background information on IMTA

decreased due to the socioeconomic change. Many

proves this system can protect the surroundingof the sites have been converted to other social

environment around the farm site and diversify

activities for greater economic return.

products. The concept of IMTA is also supported

On December 3 and 4, 2009, an internationalby the aquaculture industry in Norway. Norwegianworkshop on “Bioextractive Technologies for Nutrient

aquaculture industry has shown significant growthRemediation” was held to address the management ofsince 1970s and targeted to triple the production

eutrophication and hypoxia in Long Island Sound.

by 2025 from over 1.3 million tonnes level in 2012.

The positive contributions from the bio-extraction of

However, Bellona report in 2013 (Bellona, 2013)

nutrients from use of macroalgae to absorb inorganic

clearly indicated it is an unsustainable target unless

nutrients and use of filter and deposit feeders to

IMTA concept is introduced. IMTA is also supported

reduce organic waste released from fish production

by publics. According to the survey conducted by

was presented (RoseYip., 2010). The nutrient. (2012) at Northwest USA, it revealed 44.3 %bioextraction by seaweed and bivalves as reviewed

of consumers favored the IMTA operation and wereby Yarish and Kim (2017) is very significant. Anotherwilling to pay a price premium of 9.8 %.

benefit of IMTA practice showed by Molloy.

On contrary to those favor of IMTA, the practice of(2011) study that individual blue mussel can remove

IMTA in large scale is still very limited. The recent

copepodids from water column. Therefore, co-culture

survey conducted by Kinney (2017) also indicatedwith blue mussel () may be the potentialthat financial returns for IMTA did not justify thealternative method to drug to deal with sea louse

continuous operation of majority farmers. Only two(

aquaculturists out of eight continued after the initial) issue in Atlantic salmon

aquaculture. Furthermore, Molloy. (2014) study

trial. Therefore, the challenges to the implementation

found that infectious salmon anaemia virus (ISAV)of IMTA have to be overcome. A workshop at Port

was ingested by blue mussels and no viable ones

Angeles, Washington (Thomas, 2011) was conducted

were found in digestive gland tissue.

to analyze strength, weakness, opportunity, andAnother type of IMTA practice in Hawaii isthreat on IMTA regarding ecological, economic

aquaponics. The nutrients from fish culture are

and social impacts. Information from this workshop

used as fertilizer for vegetables. Current practices

should provide good base for strengthening thein freshwater system is tilapia with various typepositive impacts from the practice of IMTA.

of vegetables. Although tilapia is the most popular

In conclusion, if we do it right, IMTA can overcome

species, it does not exclude other species which is

at least some of the 4 out of 5 major challenges totolerable to the water quality condition in aquaponics

aquaculture development. Before IMTA can besystem. Other than the freshwater system, several

widely applied to aquaculture production, morestudies are on-going to test seacucumber and/or

research in IMTA are needed. To fully understandseaweed with shrimp, abalone and marine finfish

the optimal ration of fed to extractive organisms is

in marine environment. Seacucumber may plan

critical. The startup cost and profitability have to beimportant role in improving the benthic condition by

improved to be affordable and acceptable by farmers.

cleaning the detritus at the bottom of rearing facility.

Then, the research module has to be able to expand

The study by Hannah. (2013) demonstrated

to commercial scale. Finally, the products from IMTA

seacucumber is able to utilize the heavy fraction ofhave to be distinguishable from other traditional

waste from a sablefish farm. Aquaponics has also

practice to command higher price.

been practiced in other locations in the US as well.

133

Challenges and opportunities of IMTA
References

Soto D.(ed.), 2009: Integrated mariculture‑A global
review, FAO Fisheries and Aquaculture

Bellona, 2013: Traditional and Integrated Aquaculture.
Bellona report 2013, The Bellona Foundation,
Oslo, 113pp. https://www.bellona.org

Technical Paper 529, FAO, Rome, 184pp.
Thomas S. A., 2011: White paper of Integrated multitrophic aquaculture: A workshop at Peninsula

Butterworth Adam, 2010: Integrated multi-trophic
aquaculture systems incorporating abalone andseaweeds, Nuffield Australia Project No 0914,
39pp.

College September 14-15, 2010, Port Angeles,
46pp.
Troell M., Halling C., Neori A., Buschmann A. H.,
Chopin T., Yarish C., and Kautsky N., 2003:

FAO, 2016: The state of world fisheries andaquaculture 2016, Contributing to food security
and nutrition for all, FAO, Rome, 200pp.

Integrated mariculture: asking the rightquestions.

, 226, 69-90.

Troell M., Joyce A., Chopin T., Neori A., Buschmann

Hannah L., Pearce C. M., and Cross S. F., 2013:

A. H., and Fang J. G., 2009: Ecological engineering

Growth and survival of California sea cucumbers

in aquaculture() cultivated withtrophic aquaculture (IMTA) in marine offshore

sablefish () at an integrated

systems.

multi-trophic aquaculture site.

Potential for integrated multi, 297, 1-9.

, 406-Walsh B., 2011: The end of the line. Times July 7,

Kinney H., 2017: Aquaculturists' perceptions of

Yarish C. and Kim J. K., 2017: Cultivation ofIntegrated Multi-Trophic Aquaculture (IMTA)

economically important seaweeds in New(Open Access Master's Theses. Paper 1024),

England for nutrient bioextraction and IMTA

University of Rhode Island, 75pp. https://systems. Presented at International Symposium

407, 34-42.

2011.

digitalcommons.uri.edu/theses/1024
Molloy S. D., Pietrak M. R., Bouchard D. A., andon the IMTA September 14 to 15, 2017, Busan.
Yip W., Knowler D., and Haider W., 2012: Assessing

Bricknell I., 2011: Ingestion of

the willingness to pay for more sustainably

by the blue mussel

farmed Atlantic salmon in the Pacific Northwest:, 311, 61-64.

combining discrete choice experiment and latent

Molloy S. D., Pietrak M. R., Bouchard D. A., andclass analysis. Paper presented at Western

Bricknell I., 2014: The interaction of infectious

Economics Association International Annual

salmon anaemia virus (ISAV) with the blue

Conference June 29- July 3, 2012, San Francisco.

., 45, 509-518.

Zhang J., Kitazawa D., and Yang C., 2016: A numerical

Neori A., Chopin T., Troell M., Buschmann A.,

mussel,modeling approach to support decision-making

Kraemer G. P., Halling C., Shpigel M., and Yarish

on design of integrated multitrophic aquacultureC., 2004: Integrated aquaculture: rationale,for efficiently mitigating aquatic waste.

evolution and state of the art emphasizing., 21, 1247-1261.

seaweed biofiltration in modern mariculture.
, 231, 361-391.

Annotated bibliography

Rose J. M., Tedesco M., Wikfors G. H., and Yarish C.,
2010: International Workshop on Bioextractive(1) Sato V. T. and Lee C.-S., 2007: Keeper of Molii

Technologies for Nutrient Remediation Summary

pond, The Oceanic Institute, Waimānalo, 148pp.

Report, Northeast Fish. Sci. Cent. Ref. Doc. 10-

An oral history of a man, George Uyemura

19, US Dept. Commer., 12pp. Available from:

who spent 70 years of his life at Molii Pond was

National Marine Fisheries Service, 166 Water

documented at this book to share his knowledge

Street, Woods Hole, MA 02543-1026, or online atand experience in managing the fish pond. This

https://www.nefsc.noaa.gov/nefsc/publications/book offers a look at the history and methodology ofSato V. T. and Lee C.-S., 2007: Keeper of Molii pond,sustainable management of Hawaiian fishponds. It is

The Oceanic Institute, Waimānalo, 148pp.

a start reference book to know more about Hawaiian

134

Cheng Sheng Lee

fishpond.

impacts of IMTA. It concluded IMTA could help tomove the US toward becoming a major aquaculture(2) Soto D. (ed.), 2009: Integrated mariculture- A global

producer in the world, because it might resolve somereview, FAO Fisheries and Aquaculture Technicalof the issues that seem to be limiting such progress.

Paper 529, FAO, Rome, 184pp.

This is a good reference base for any further SWOT

This report contains three desk studies

analysis.

encompassing global views of practices andfuture prospects for integrated aquaculture in(4) Bellona, 2013: Traditional and Integrated

coastal and marine areas in three climatic zones:

Aquaculture. Bellona report 2013, The Bellona

temperate, tropical and Mediterranean Sea as aFoundation, Oslo, 113pp. https://www.bellona.org

special Mediterranean enclosed ecosystem. The

Bellona has been involved in the hunt for new

commissioned review papers describing integrated

solutions, new resources and new products that will

aquaculture in coastal and marine environments

be important for the future. This report points out

were technically supervised by Mrs. Doris Soto,

that salmonid industry has high ambitions for growth,

Senior Fisheries Officer (FIMA). The activity andbut it must happen in harmony with the ecosystem.

the publication have been partly funded through a

It explains why aquaculture should progress fromJapanese Trust Fund Project (Towards Sustainablesalmonid monoculture to integrated and sustainable

Aquaculture: Selected Issues and Guidelines). It is

ecosystems and how. Also, this progress depends ona good reference report to get start to know about

the aquaculture industry, research institutions andintegrated mariculture.

politicians working together. It is a good lesson forother aquaculture industry to learn from a mature(3) Thomas S. A. (ed.) 2011: Integrated Multi-Trophic

salmonid industry to think ahead.

aquaculture: A Workshop at Peninsula College
Port Angeles, Washington.
, 109-2, 13. https://www.researchgate.net/
publication/257819653
This report summarized the first US-based(5) Gunning D., Maguire J., and Burnell G., 2016: The
development of sustainable saltwater-based foodproduction systems: a review of established andnovel concepts.

, 8(12), 598.

workshop on integrated multi-trophic aquaculture

This review article examines the potential negative(IMTA). The two daysʼ workshop included

impacts of saltwater mono-aquaculture operations

presentation and breakout sessions to conduct

and how the novel approach such as IMTA,“strengths-weaknesses-opportunities-threats”

constructed wetlands and saltwater aquaponics will

(SWOT) analysis for ecological, economic, and social

mitigate the negative impacts.

水 研 機 構 研 報， 第 49 号，135 − 135， 平 成 31 年
Bull. Jap. Fish. Res. Edu. Agen. No. 49，135−135，2019

135

Abstracts of Poster Presentations
List of Presentations
1:

Possible effects of terrestrial managements on seagrass ecosystem functionings. (Christopher BAYNE,
National Research Institute of Fisheries and Environment of Inland Sea, FRA)

2:

Genetic effects of the tiger puffer stock enhancement program on wild population in the sea around Japan.
(Daisuke KATAMACHI, National Research Institute of Fisheries and Environment of Inland Sea, FRA)

3:

Assessment of the ichthyotoxicity of harmful marine microalgaesea bream (spp. using cultured gill cells from red). (Nobuyuki OHKUBO, National Research Institute of Fisheries and Environment of

Inland Sea, FRA)

4:

Asari clam predation by intertidal fishes: feeding habits of immature black porgy,in Yamaguchi Bay, western Seto Inland Sea, Japan. (Toshihiro SHIGETA, National Research Institute ofFisheries and Environment of Inland Sea, FRA)

5:

Evaluation of inexpensive Raspberry Pi-based time-lapse camera system for tidal flat ecosystem observation.
(Naoaki TEZUKA, National Research Institute of Fisheries and Environment of Inland Sea, FRA)

6:

Development of Free-Ocean Real-Time Experimental System (FORTES) for in-situ CO2 manipulation ineelgrass beds. (Tatsuki TOKORO, National Research Institute of Fisheries and Environment of Inland Sea,
FRA)

7:

A comparison of environmental and biological parameters at asari,, fishing grounds inJapan for understanding the cause of recent catastrophic decrease of asari clam. (Motoharu UCHIDA, National
Research Institute of Fisheries and Environment of Inland Sea, FRA)

水 研 機 構 研 報， 第 49 号，137 − 144， 平 成 31 年
Bull. Jap. Fish. Res. Edu. Agen. No. 49，137−144，2019137

Abstracts of Poster Presentations
1:

Possible effects of terrestrial managements on

interactive effect of insecticide with eutrophication

seagrass ecosystem functionings

on ecosystem functioning of seagrass beds using
manipulative experiments in Seto Inland Sea, Japan.

＊

Christopher BAYNE , Hideki HAMAOKA, and＊Masakazu HORI

In the manipulation, we used the insecticide carbaryl
to exclude invertebrate herbivores and the fertilizer
to add nutrients, which is a technique developed by＊

National Research Institute of Fisheries andthe Zostera Experimental Network (ZEN), a global

Environment of Inland Sea, FRA, 2-17-5 Maruishi,

collaborative network of scientists studying the

Hatsukaichi, Hiroshima 739-0452, Japan

structure and functioning of ecosystems supported

E-mail: bayne@affrc.go.jp

by eelgrass. The technique enables us especially todemonstrate the indirect effect of epiphyte grazing

Abstractby the associated invertebrates on eelgrass growth(e.g. Whalen., 2013). The carbaryl loading

Seagrass species function as typical foundation

significantly decreased the density and diversity of

species which support high productivity and diversity

herbivorous invertebrates and indirectly increased

because of their high rates of primary production andepiphyte biomass, resulting in a significant difference

their ability to provide associated organisms within seagrass growth, although carbaryl concentrations

trophic support, refuge from predation, and spawning

were within the safety standards even at thesubstrates. Seagrass associated species, especiallyexperiment site. However, the nutrient addition

herbivorous invertebrates, can regulate thesignificantly changed the indirect effect of carbaryl

ecosystem functioning of seagrass beds, suggestingloading on seagrass growth. These results suggestthat this interaction is an important key to clarify

that seagrass-associated herbivores can regulate

the relationship between biodiversity and ecosystemecosystem functioning of seagrass beds, and indicate

functioning in coastal ecosystems. Seagrass

the possibility that both agrichemical and nutrient

communities are characterized by wide occurrence inloading can easily change the seagrass ecosystemshallow nearshore areas, where there is a boundaryfunctionings even in lower concentration. Bothbetween terrestrial and marine ecosystems.

agrichemical and nutrient loading from terrestrial

Therefore, seagrass communities are often influenced

habitat to nearshore areas would be easy to change

by various factors derived from terrestrial habitats,and vary spatially with land use change, so that wesuch as agrichemicals and nutrients through freshshould pay attention to the management for thewater input. Although terrestrial nutrients are

adjacent terrestrial habitats.

essential for productivity for nearshore marine
plants including seagrass species, increased nutrients

Annotated Bibliography of Key Workscause eutrophication and phytoplankton blooming
resulting in the degradation of seagrass growth(1) Duffy J., Reynolds P., Boström C., Coyer J., Cusson

and distribution. Agrichemicals from river, adjacentM., Donadi S., and Fredriksen S., 2015: Biodiversity

agriculture fields and forests also have serious effects

mediates top‒down control in eelgrass ecosystems: aon seagrass communities; in particular insecticide

global comparative‐experimental approach.

has caused mass mortality of the seagrass-associated18(7), 696-705.

.,

invertebrates, resulting in vulnerable ecosystem

This paper investigates top-down and bottom-

functioning of seagrass beds. The inflow of bothup effects of adding nutrient and deterrents toagrichemical and nutrients into nearshore areas has

eelgrass (increased with the change of the adjacent terrestrial

range of this species. They found that removing

management. In this study, we demonstrated

grazers had a stronger average effect on epiphytic) beds at 15 sites across the

138biomass than local addition of nutrients, revealing

2:stronger top-down control by grazers. Also, theyenhancement program on wild population in the sea

found that the influences of biodiversity in theiraround Japan

Genetic effects of the tiger puffer stockglobal analysis are very similar to results from othersmall-scale experiments. These include sites with

Daisuke KATAMACHI

more genotypically diverse eelgrass with higher
crustacean biomass and lower algal biomass at sites

National Research Institute of Fisheries andwith increased grazer species.

Environment of Inland Sea, FRA, 2-17-5 Maruishi,
Hatsukaichi, Hiroshima 739-0452, Japan(2) Reynolds P., Stachowicz J., Hovel K., Boström C.,

E-mail: kata79@fra.affrc.go.jp

Boyer K., Cusson M., and Duffy J., 2017: Biogeographyof predation pressure in eelgrass across the Northern

Abstract

Hemisphere, Unpublished manuscript, Virginia
Institute of Marine Science, Virginia USA.

Since 1977, millions of hatchery-reared tiger puffer,Studies across broad geographic ranges exploring, juveniles have been released for

drivers of change in predator interactions arestock enhancement in the sea around Japan. The stock

relatively rare. The authors surveyed predation on aenhancement program has contributed to catches,common amphipod prey in eelgrass ()

however, no information about genetic effects of thebeds at 42 sites across the Northern Hemisphere.

program on wild population is available. The genetic

At all coasts, predation declined with latitude, buteffects were evaluated with highly polymorphic DNA

declined more in areas where temperature gradientsmarker sets (1962 bp mitochondrial DNA sequences

are steeper.

and 11 microsatellite DNA loci) using 316 maturewild adults from nine identified or possible spawning(3) Whalen M., Duffy J., and Grace J., 2013: Temporalsites in the sea around Japan, 276 wild juveniles

shifts in top-down vs. bottom-up control of epiphytic

in the Ariake Sea which is a possible spawningalgae in a seagrass ecosystem.

site and an identified nursery, 85 hatchery-reared, 94, 510-520.

The authors used a cage-free approach ofjuveniles, 150 mature hatchery-released adults in the

manipulating mesograzer abundance and epiphytic

Ariake Sea. Both types of markers indicated thatloading over a temporal period, by using deterrent

hatchery-reared and hatchery-released populations

and nutrient treatments. They found that reduction

had lower genetic variability than wild populations,of mesograzer abundance and increase in nutrients

however, hatchery-released population had closer

can allow increased epiphytic algae growth on

genetic variability to wild populations. Microsatellite

eelgrass (). By performing the

F ST estimates indicated hatchery-reared andexperiment in the fall and summer, they foundhatchery-released populations were significantly

that the dominant factors that controlled epiphytic

different from wild populations. On the other hand,algae abundance changed. In fall, there was asignificant differences were observed only between

natural decrease in mesograzer abundance, and byhatchery-reared population and wild populations

adding nutrients, which caused bottom-up factors towith mitochondrial ΦST estimates. Microsatellite FST

dominate, increased epiphyte biomass. In summer,

estimates and Bayesian clustering analysis revealed

added deterrents, stimulating strong top-down

population structure of the tiger puffer, however,factors, decreased mesograzer abundance and caused

the population structure was not associated with the

an increase in epiphyte biomass. Also, unexpectedly,

history and scale of stock enhancement program.

they found that drift macroalgae indirectly reduced

The genetic variability was almost equivalent

epiphytes by proving structure for mesograzers.

among wild populations, no significant deviationfrom Hardy-Weinberg equilibrium and significant
linkage disequilibrium were detected from wild
populations. Moreover, putative wild juveniles

139

Abstracts of Poster
having a high possibility of being related to mature

years. The programme has successfully augmented

hatchery-released adults were detected based

commercial catches in the bay (released juveniles

on relatedness among individuals in the Ariake

have been produced from the captive broodstock,

Sea. These results suggested that there is a highrepeatedly used over multiple generations). Samples

possibility that hatchery-released fish breed in thewere also obtained from outside the bay, where

wild, however, negative genetic effects of the stock

limited stocking has occurred. Genetic diversity

enhancement program on wild populations were notindices measured as number of haplotypes, haplotype

likely in the tiger puffer. As one of the factors, it isrichness, haplotype diversity and nucleotide diversity

considered that mature hatchery-released population

were lower in hatchery-released fish than in wild

is composed of multiple groups and year classes andfish. Genetic differences in wild fish from the bay,

have close genetic characteristics to wild populations.

especially in the inner bay, compared with fishfrom outside the bay were detected in terms of

Annotated Bibliography of Key Worksdecreased genetic diversity indices and changed
haplotype frequencies. Unbiased population pair-(1) Araki H., Cooper B., and Blouin M. S., 2007: Genetic

wise FST estimates based on an empirical Bayesianeffects of captive breeding cause a rapid, cumulative

method, however, revealed low genetic differentiation

fitness decline in the wild.

between samples from the bay and its vicinity. Mixed, 318, 100-103.

Captive breeding is used to supplement populations

stock identification analyses estimated the proportionof many species that are declining in the wild. The

of hatchery-released fish in wild populations in thesuitability of and long-term species survival frominner and central bays at 39.0 and 8.7%, respectively,

such programs remain largely untested, however.

although the precision of the estimates was very low

We measured lifetime reproductive success of the

because of the small genetic differentiation between

first two generations of steelhead trout that were

populations and relatively small sample sizes. Hence,

reared in captivity and bred in the wild after they

the long-term extensive hatchery release programme

were released. By reconstructing a three-generation

has affected the genetic diversity of wild populations

pedigree with microsatellite markers, we show thatin the bay; however, the genetic effects were low andgenetic effects of domestication reduce subsequentappeared to remain within the bay.

reproductive capabilities by ~ 40 % per captivereared generation when fish are moved to natural(3) Blanco Gonzalez E., Aritaki M., Sakurai S., andenvironments. These results suggest that even a

Taniguchi N., 2013: Inference of potential genetic

few generations of domestication may have negative

risks associated with large-scale releases of red

effects on natural reproduction in the wild andsea bream in Kanagawa prefecture, Japan basedthat the repeated use of captive-reared parents toon nuclear and mitochondrial DNA analysis.

supplement wild populations should be carefullyreconsidered.

., 15, 206-220.
Since 1978, millions of hatchery-reared red sea
bream ()

juveniles have been released(2) Hamasaki K., Toriya S., Shishidou H., Sugaya T.,

in Sagami Bay and Tokyo Bay in Kanagawa

and Kitada S., 2010: Genetic effects of hatchery fish

Prefecture, Japan. The stock enhancement programon wild populations in red sea bream

has contributed to total catch; however, no(Perciformes, Sparidae)

information regarding the genetic interactions withinferred from a partial

sequence of mitochondrial DNA.

., 99,

2123-2136.

wild counterparts is available. Here, we combined
15 microsatellite loci and mitochondrial D-loop

Variation in the mitochondrial DNA transcriptionalsequencing to characterize the genetic resources ofcontrol region sequence was investigated in wild

red sea bream in Sagami Bay and Tokyo Bay andand hatchery-released red sea bream

to elucidate the potential harmful genetic effects

from Kagoshima Bay, where an extensive hatchery-

associated with fish releases. Both types of markers

release programme has been conducted for > 30

evidenced higher levels of genetic diversity in wild

140
samples (SB and TB) compared with offspring before

with the large census size. A Ryman‒Laikre effectstocking (H07 and H08) as well as a hatchery-released

was not likely in the Japanese Spanish mackerel.

sample recaptured in Sagami Bay (HR). Microsatellite
F ST estimates and Bayesian clustering analysis
found significant genetic differences among samples

3:

Assessment of the ichthyotoxicity of harmful(FST = 0.013-0.054), except for the two wild samples

marine microalgae(FST = 0.002) and HR vs. H07 (FST = 0.007). On the othergill cells from red sea bream (spp. using cultured)

hand, mitochondrial-based ФST suggested haplotypic
similarity between SB, H07, and HR. The low effective

Nobuyuki OHKUBO＊1 , Yuji TOMARU＊1 , Haruo

number of females contributing to the offspring overY A M G U C H I ＊2 , S e t s u k o S A K A M O T O ＊1 , a n dmultiple generations may be responsible for the lackKazuhiko MOCHIDA＊1

of haplotypic differentiation. Moreover, the putative
hatchery origin to three fish (8 %) without deformity＊1

in the inter-nostril epidermis was inferred for the first

Environment of Inland Sea, FRA, 2-17-5 Maruishi,

National Research Institute of Fisheries andtime. Our results showed the usefulness of combining

Hatsukaichi, Hiroshima 739-0452, Japan

nuclear and mitochondrial markers to elucidate＊2

genetic interactions between hatchery-released andKochi 783-8502, Japan

wild red sea bream and warned about potential

E-mail: nobuyuki@affrc.go.jp

Faculty of Agriculture, Kochi University, Nankoku,

harmful genetic effects should interbreeding takes
Abstract

place.
(4) Nakajima K., Kitada S., Habara Y., Sano S.,

The present study reports the development of

Yokoyama E., Sugaya T., Iwamoto A., Kishino H.,a method to investigate ichthyotoxicity of harmfuland Hamasaki K., 2014: Genetic effects of marine

marine microalgae using cultured red sea breamstock enhancement: a case study based on the highly(

piscivorous Japanese Spanish mackerel.

adherent 1‒2 layers on the bottom of the culture., 71, 301-314.
We used a before‒after control‒impact design toquantify the genetic effects of the large piscivorous) gill cells. The cultured gill cells formed

plate, and could tolerate seawater exposure for 4 h
without significant alteration in cell survival. The
microalgae
andJapanese Spanish mackerel () stock enhancement program on wild

were cultured, then directly

populations in the Seto Inland Sea. Samples of

exposed to gill cells. Live gill cell coverage afterand

1424 wild and 230 hatchery fish collected from.

13 sites around Japan were genotyped using fiveexposure were significantly lower than

microsatellite markers. A total of 758 wild and 103

in the cells exposed to a seawater-based medium

hatchery fish were sequenced for the mitochondrial

SWM-3 and IMK (control cells; P < 0.05). Toxicity

DNA D-loop region. The population structure ofofJapanese Spanish mackerel was panmictic aroundwere ruptured, and was almost inexistent when

Japan. Hatchery fish had significantly lower genetic

the algal cells were removed from the culture by

diversity indices than did wild fish. However, there

filtration. Significant cytotoxicity was detected in thewas no significant change in any of the diversity

concentrated ruptured cells, although cytotoxicity

indices in the Seto Inland Sea, despite the substantial

was weakened in the concentrated of ruptured cells

genetic mixing proportion of hatchery-origin genes

after freezing and thawing; whereas, cytotoxicity(7.8 % ‒ 14.5 % from releases in 2001 and 2002), a

almost disappeared after heat treatment. In addition,

conclusion supported by simulations. The estimatedexamination of the distribution of toxic substances

effective population size was surprisingly small (~from the ruptured cells showed that cytotoxicity

430 ‒ 970) but stable in the Seto Inland Sea comparedmainly occurred in the fraction with the resuspended

cells was weakened when the cells

141

Abstracts of Poster
pellet after centrifugation at 3000 × g.

June. In July, it reached 2.9, the highest annual value,
after which the CPUE maintained high values from
August to November. From December values were

4:

Asari clam predation by intertidal fishes:low (0 - 0.4) again. These results indicate that immature

feeding habits of immature black porgy,

occurs seasonally in the tidal flats fromin Yamaguchi Bay,

June to November. Bases on the stomach contents ofwestern Seto Inland Sea, Japanthe porgy, bivalves such as Asian mussel,, Japanese razor clam,

＊1

＊1

were

Toshihiro SHIGETA , Mutsumi TSUJINO , Takeshi

the most important prey items in wet weight. Next,

TOMIYAMA＊2 , Yoichi SAKAI＊2 , and Hidetoshi

Japanese mud shrimp,

＊2

SAITO

major was thesecond important one. These benthic animals werein common and are filter feeders on phytoplankton,＊1

National Research Institute of Fisheries andbenthic microalgae, and detritus. Immature-sized

Environment of Inland Sea, FRA, 2-17-5 Maruishi,

porgy preyed on juvenile Asari clams ranging from

Hatsukaichi, Hiroshima 739-0452, Japan

2.8 to 18.0 mm shell length. The values of stable＊2

Graduate School of Biosphere Science, Hiroshima

isotopes of δ13C and δ15N on black porgy showed -17.6

University, Higashi-Hiroshima, Hiroshima 739-8528,〜-16.0 ‰ and 16.2〜17.7 ‰, respectively. In the Seto

Japan

Inland Sea of Japan, resources of benthotrophic fishE-mail: shigeta@fra.affrc.go.jp

species, such as flatfishes and pufferfishes, which use
the estuary in their early life history, have decreased

Abstract

remarkably. For recovery and regeneration ofthese critical resources, it is necessary to clarify theBlack porgy,(Family:), is a commercially important fish in Japan.

relationships between organisms and the estuarine
ecosystem.

In 2015, commercial catches of the porgy in Japanand the Seto Inland Sea of western Japan were 3,181

Annotated Bibliography of Key Works

metric tons and 1,508 metric tons, respectively. This
species is known as a major predator of Asari clam,in tidal flats. On the other
hand, Asari clam is a commercially important species,(1) Shigeta T. and Usuki H., 2012: Predation on
the short-neck clambyintertidal fishes: a list of fish predators.

too. Recently, the clam catches have decreased in., 5(1), 1-19. (in Japanese with English abstract)

Japan. Especially in the Seto Inland Sea, the catches

Recently, commercial catches of the short-neckhave remarkably dropped to 137 metric tons in 2015

clamfrom 45,023 metric tons in 1985 (peak level). Several

Japan. Especially in the Seto Inland Sea, western

reports concerning protecting clam beds with netting

Japan, the clam catches have remarkably dropped.

suggest that predation is one of the most important

Several reports suggest that predation by fishes isfactors for the survival of the clam. In order toone of the most important factors for the survival

restore Asari clam resource, it is necessary to clarifyof the clam. In this review, we made a list of fish

the habits of the porgy. In this study, we investigatedspecies that forage on the short-neck clam in thethe seasonal occurrence and feeding habits offield. Twenty-three fishes ranging fromimmature-sized porgy (less than about 25 cm total

tolength) in tidal flats from 2005 to 2017 in Yamaguchi

Among them, 21 intertidal fishes (12 families) occur in

Bay, western Seto Inland Sea. 102 individuals of theJapan. It was clarified that five fishes, the Longheaded

porgy (10.4 - 27.7 cm TL) were collected by rod-and-eagle rayhave decreased in(12 families) are listed in the world.

line fishing there. The monthly catch per unit effort(CPUE: number of fish caught/3 hours/person) of the
porgy ranged 0 - 2.9. The CPUE rapidly increased in, the Black porgy, the Yellowfin seabream, the Kyuusen wrasse
and the Grass puffer, foraged

142
on whole adult-sized clam (> 20 mm shell length).

Raspberry Pi-based underwater time-lapse camera

At least, the siphon was cropped by eight fishes

system to observe the tidal flat ecosystem processes.

including the Stone flounder, the

The Raspberry Pi is an inexpensive single-board

Marbled sole

, andcomputer that can be connected to a dedicated. Meanwhile, thecamera module. Our system consists of RaspberryBlack porgy and the Kyuusen wrasse preyed on all

Pi with a camera module, USB battery, time-lapse

parts except the foot of the clam. We are continuing

power control unit, and optional light emitting

to analyze details of the interaction between these

diode (LED) module and temperature sensor. Theintertidal fishes and the short-neck clam.

camera system uses the command line interface for

the Japanese sillago

operation setting, i.e., setting the initial wakeup time,
repeat times, and the interval. It takes still and/or
5:

Evaluation of inexpensive Raspberry Pi-

video images after wakeup, and then shuts down

based time-lapse camera system for tidal flat

until the next scheduled wake-up time. We placed

ecosystem observation

the entire system, excluding the LED module andtemperature sensor, in an inexpensive underwater

Naoaki TEZUKA＊1 and Kazumasa OGURI＊2

housing structure made with polyvinyl chloride(PVC) water pipe sockets and an acrylic window. The＊1

National Research Institute of Fisheries andcamera system successfully captured underwater

Environment of Inland Sea, FRA, 2-17-5 Maruishi,

time-lapse images during observations, except under

Hatsukaichi, Hiroshima 739-0452, Japan

low visibility conditions, or when biofouling occurs.

＊2Japan Agency for Marine-Earth Science andHowever, certain improvements are required, which

Technology, Natsushima, Yokosuka, Kanagawa 237-

include improving the image quality under low-light

0061, Japan

conditions by increasing the brightness of the light

E-mail: tezukan9@affrc.go.jp

module, widening the field of view of the image, andadding an anti-biofouling mechanism.

Abstract
In recent years, changes in the structure of coastal

6:

Development of Free-Ocean Real-Time

ecosystems, leading to a collapse of conventional

Experimental System (FORTES) for in-situ CO2

fisheries, have been widely reported. Maintaining

manipulation in eelgrass beds

clam fisheries or aquaculture production in general
has becoming increasingly difficult without adequate

Tatsuki TOKORO＊1,2, Masakazu HORI＊1, Tomohiro

predator prevention measure, especially in the tidal

KUWAE＊2, Yuichi ISAKA＊3, Hyojin AHN＊3, andflats of western Japan, indicating certain changes

Masahiro NAKAOKA＊3

in the structure of the ecosystem. It is suggested
that migratory fish species influence the benthic＊1community structure through predation in the tidal

Environment of Inland Sea, FRA, 2-17-5 Maruishi,

National Research Institute of Fisheries andflat ecosystem. However, inadequate information

Hatsukaichi, Hiroshima 739-0452, Japan

exists on the abundance or frequency of the＊2

appearance of migratory fish species in tidal flats;

Yokosuka, Kanagawa 239-0826, Japanhence, its impacts on the benthic community are＊3

unclear. Observation using an underwater time-

Akkeshi, Hokkaido 088-1113, Japanlapse camera system can be an effective approachE-mail: ttokoro@affrc.go.jp

Port and Airport Research Institute, Nagase,
Akkeshi Marine Station, Hokkaido University,

to understanding the temporal change in theabundance of migratory fish species in tidal flats

Abstract

and their influence on the ecosystem. We have,therefore, developed and tested an inexpensive

Ocean acidification (OA) causes various effect on143

Abstracts of Poster
coastal resources. For eelgrass beds, positive anddevelopments.

, 11, 4057-4075.

negative effects are expected on different functional

Free-ocean CO2 enrichment (FOCE) systems aregroups of biological communities. In addition,

designed to assess the impact of ocean acidification

the acidification level in coastal ecosystems varyon biological communities in situ for extended

greatly due to the CO2 consumption and production

periods of time (weeks to months). They overcome

by marine plants and input of freshwater. To

some of the drawbacks of laboratory experiments

understand the actual influences of OA under suchand field observations by enabling (1) precise

complicated conditions, in-situ field experiments

control of CO2 enrichment by monitoring pH as anfor manipulating CO2 are promising. FOCEs (Free

offset of ambient pH, (2) consideration of indirect

ocean carbon experiments, Gattuso., 2014) haveeffects such as those mediated through interspecificalready been established in several marine habitats

relationships and food webs, and (3) relatively longsuch as coral reefs andseagrass beds.

experiments with intact communities. Bringing

However, these systems have several problems suchperturbation experiments from the laboratory to

as changing in-site hydrodynamic conditions, thethe field is, however, extremely challenging. The

needs to electrical power to operate the system, andmain goal of this paper is to provide guidelines onhigh installation cost. To overcome such difficulties,

the general design, engineering, and sensor options

we have developed a newly CO2 manipulating system

required to conduct FOCE experiments. Anotheron the site, named FORTES (Free-Ocean Real-Timegoal is to introduce xFOCE, a community-led

Experimental System). The system allows control of

initiative to promote awareness, provide resources

the acidification level in the area of square meters offor in situ perturbation experiments, and build a user

eelgrass beds by supplying a high concentration ofcommunity. Present and existing FOCE systems

CO2-dissolved water under mostly opened condition.

are briefly described and examples of data collected

No electrical power is required because this systempresented. Future developments are also addressed

could be operated by the pressure and buoyancy

as it is anticipated that the next generation of FOCE

of injected CO2. The CO2-dissolved water is always

systems will include, in addition to pH, options foremitted to the experimental area from the upstream

oxygen and/or temperature control. FOCE systems

direction even when the current direction changes

should become an important experimental approachwith tide and other factors. In the test trials offor projecting the future response of marine

FORTES in eelgrass beds in Oki Island and Akkeshi

ecosystems to environmental change.

lagoon in Japan, the acidification level expected in
2100 was reproduced successfully. Furthermore, thissystem enables the supply of water-soluble nutrients7:

A comparison of environmental and biologicaland the deterrent of invertebrate grazers along withparameters at asari,,

the CO2 for simultaneous control of nutrient levels

fishing grounds in Japan for understanding theand grazer densities. This orthogonal design allows

cause of recent catastrophic decrease of asari

the experiments to examine interacting effects ofclam

ocean acidification and other factors in the eelgrass
bed community.

Motoharu UCHIDA＊1, Mutsumi TSUJINO＊1, Naoaki
TEZUKA＊1 , Toshihiro SHIGETA＊1 , Yoshitake

Annotated Bibliography of Key Works

TAKADA＊2, Yuka ISHIHI＊3, Satoshi WATANABE＊3,
Shuhei SAWAYAMA＊4, Hiroaki KUROGI＊4, and(1) Gattuso J. P., Kirkwood W., Barry J. P., Cox

Kentaro NIWA＊5

E., Gazeau F., Hansson L., Hendriks I., Kline D. I.,
Mahacek P., Martin S., McElhany P., Peltzer E. T.,＊1

Reeve J., Roberts D., Saderne V., Tait K., Widdicombe

Environment of Inland Sea, FRA, 2-17-5 Maruishi,

National Research Institute of Fisheries andS., and Brewer P. G., 2014: Free-ocean CO2 enrichment

Hatsukaichi, Hiroshima 739-0452, Japan(FOCE) systems: present status and future＊2

Japan Sea National Research Institute, FRA, 1-5939-

144
22, Suido-cho, Chuo, Niigata 951-8121, Japan

well characterized to explain the widespread and＊3

National Research Institute of Aquaculture, FRA,

long-term decrease of the catch. We conducted422-1 Nakatsuhamaura, Minamiise, Mie, 516-0193,

comprehensive comparison of environmental andJapanbiological characteristics among asari fishing grounds＊4in Japan. Significant relationship was observed

National Research Institute of Fisheries Science,

Yokosuka Station, FRA, 6-31-1 Nagai Yokosuka,

between water nutrient level (Kanagawa 238-0316, Japan

chlorophyll＊5National Research Institute of Fisheries Science,isotope ratio of asari was found to be a useful indicator

FRA, 2-12-4 Fukuura, Kanazawa, Yokohama,representing not only the nutrient level but also the

Kanagawa 236-8648, Japan

asari catch per unit area. Significant relationshipE-mail: uchida@affrc.go.jp

was also observed between the benthos biomass., total nitrogen and) and the asari catch. Stable carbon(macrobenthos, meiobentos, and nematodes) and
Abstract

the asari catch. All these observations suggest thatrecent catastrophic biomass decrease is occurring

The catastrophic decrease of catch of the asari
clam,, has been observed

not only for asari but also for wide range of benthic
organisms in Japanʼs coastal waters.

for the last three decades in Japanʼs coastal waters.

This study was conducted by a research fund

Many factors including overfishing, disease, habitat

entitled a feasibility study on biodiversity assessment

loss, competition with invasive species, global

methods in fishing ground environment fromwarming, and altered trophic cascade are suggested

Fisheries Agency.

to be involved. However, major factor is still not