Oceanography and Marine Biology: An Annual Review, Volume 48

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v

Contents

Preface vii

Margaret Barnes DSc FRSE FIBiol, 1919–2009 ix

Toward ecosystem-based management of marine macroalgae—The bull kelp,

Nereocystis luetkeana 1

Yuri P. Springer, Cynthia G. Hays, Mark H. Carr & Megan R. Mackey

The ecology and management of temperate mangroves 43

Donald J. Morrisey, Andrew Swales, Sabine Dittmann, Mark A. Morrison, Catherine E.

Lovelock & Catherine M. Beard

The exploitation and conservation of precious corals 161

Georgios Tsounis, Sergio Rossi, Richard Grigg, Giovanni Santangelo, Lorenzo Bramanti &

Josep-Maria Gili

The biology of vestimentiferan tubeworms 213

Monika Bright & François H. Lallier

Historical reconstruction of human-induced changes in U.S. estuaries 267

Heike K. Lotze

Author Index 339

Systematic Index 373

Subject Index 381

vii

Preface

The 48th volume of this series contains five reviews written by an international array of authors. As

usual, these reviews range widely in subject, taxonomic and geographical coverage. The editors wel￾come suggestions from potential authors for topics they consider could form the basis of appropriate

future contributions. Because the annual publication schedule places constraints on the timetable

for submission, evaluation and acceptance of manuscripts, potential contributors are advised to

make contact with the editors at an early stage of manuscript preparation. Contact details are listed

on the title page of this volume.

The editors gratefully acknowledge the willingness and speed with which authors complied

with the editors’ suggestions, requests and questions and the efficiency of CRC Press, especially

Marsha Hecht, in ensuring the timely appearance of this volume.

It is with great regret that we report the death of Margaret Barnes in October 2009. Margaret

was associated with Oceanography and Marine Biology: An Annual Review for 40 years and was

editor from 1978 to 2002. An appreciation of her life and work is included in this volume.

ix

Margaret Barnes DSc FRSE FIBiol

1919–2009

Managing Editor Oceanography and Marine Biology: An Annual Review 1978–1994

Editor 1995–2002

Margaret Barnes began her scientific career in 1939 soon after receiving her BSc. Her further edu￾cation was interrupted by the outbreak of WWII, and she went to work in industry and spent the fol￾lowing 6 years using her training as a chemist to investigate colloidal graphite lubricants. During this

period, she continued her education in her spare time and at the end of the war in 1945 was awarded

an MSc. She had met her future husband, Harold, while at college, and they married in 1945. Harold

was also a chemist but in 1943 had been seconded to the Marine Station of the Scottish Marine

Biological Association (SMBA) at Millport in the Firth of Clyde, Scotland. There he was involved

in the development of antifouling paints. After their marriage, Margaret joined him in Millport, and

it was there that their lifelong partnership in science began. His early work was varied but he had

developed an interest in barnacles during his antifouling work and began publishing on the group in

the early 1950s. Margaret acted as his assistant (officially designated by the Marine Station in the

restrictive practices of the SMBA of the time as an ‘unpaid permanent visiting worker’), and their

first joint article appeared in 1953, albeit on Calanus finmarchicus. Subsequently, their barnacle

articles came on stream covering a wide range of topics, including general biology, morphology,

distribution, reproduction and development, settlement, biochemistry, physiology and metabolism.

In 1967 the SMBA opened its new laboratory in Oban and Harold and Margaret moved there from

Millport to continue their barnacle studies.

Before moving, however, in 1963 Harold had started the review series Oceanography and

Marine Biology: An Annual Review. The husband and wife team, now becoming recognised as

world authorities in barnacle biology, continued their partnership in editing ‘The Review’, as they

Margaret Barnes

x

called it. Not content with starting one journal, and with Margaret’s support, Harold followed

Oceanography and Marine Biology 4 years later in 1967 with the Journal of Experimental Marine

Biology and Ecology (JEMBE). The first issue of JEMBE was published in September, and it is

significant that the first article in that issue was coauthored by Harold and Margaret. Margaret was

an integral, experienced and tireless other half of the editorial team on both periodicals so that on

his sudden and untimely death in early 1978, it was natural for her to assume the editorship of both

publications and so ensure their smooth continuation. The year following Harold’s death was a dif￾ficult one for Margaret but she showed little outward signs of her grief and buried herself in finish￾ing the writing of manuscripts that had been unfinished and in the considerable amount of editorial

work the two periodicals entailed. At that time Oceanography and Marine Biology had reached its

15th volume and Margaret’s immediate task was to ensure that the manuscripts for Volume 16 were

prepared to meet the deadline for publication by Aberdeen University Press (AUP) in the summer.

She also had to be involved in the painful task of discussing with the publishers her future role.

Fortunately, AUP was aware of her contribution to the regular appearance of past volumes and was

content to allow her to continue as editor. The transition for JEMBE was not as smooth and Elsevier

insisted that others join her on the editorial team. Although Margaret was not initially happy with

this arrangement, she realised it was for the best because one person could not have managed the

burden of editing both journals single-handed. In the late 1980s she invited colleagues to become

assistant editors on Oceanography and Marine Biology to share the load. In 1998, and approaching

her 80th birthday, she decided it was time to take a back seat in the editorial team, and Alan Ansell

took over the reins as managing editor. Prior to this, however, AUP had collapsed as a result of what

was known at the time as the ‘Maxwell affair’, and the rights were bought by University College

London Press. Another change of publisher took place in 1998 (to Taylor & Francis). Margaret dealt

calmly with all these changes and continued as editor until Volume 40 was published in 2002, when

she decided to stand down, having retired from JEMBE in 1999, thus ending a 57-year contribution

to marine science.

She was a meticulous editor with a fine eye for detail who insisted on high standards of

English and spent many hours improving the texts both of authors whose first language was not

English and of many whose it was. She dealt diplomatically but firmly with tardy or recalcitrant

authors, and I well remember her patience when meticulously compiling the indexes for early vol￾umes of Oceanography and Marine Biology from entries on scraps of paper, which were then sorted

and typed by hand, a task now done in a fraction of the time by computer. She brought to both pub￾lications standards that few others could match.

Margaret travelled extensively in the course of her barnacle studies and was a founder

member of the European Marine Biology Symposium (EMBS), acted as minutes secretary

for the organisation for a while and in 1988 was elected for a term as president. She was inti￾mately involved with the two symposia that were held in her hometown of Oban in 1974 and

1989 and was instigator, organiser and senior editor of the proceedings of the latter meeting. In

later years when she no longer felt able to attend the symposia, I was frequently asked “How’s

Margaret?” and to pass on regards. At the EMBS and during her visits to numerous laboratories

throughout Europe and the United States she made contact with many people the world over,

and many of these contacts developed into lasting friendships. Always encouraging to young

scientists, especially young women, she was an independent and determined woman largely

overshadowed by her husband and her true scientific and editorial abilities only became appar￾ent after his death. She was also a gentle, modest, courteous and charming person, a good

listener, and she had a terrific sense of humour. In her younger days she was very active as a

keen cross-country skier, mountaineer and long-term member of the Austrian Alpine Club.

She remained sprightly until her death, working in her garden throughout the year, and we had

Margaret Barnes

xi

numerous conversations about hill walking and the state of her crops. However, I suspect that

many will particularly remember her for her coffee mornings and dinner parties. They were

deservedly famous for their wide-ranging and relaxed conversation and their cuisine, and it

gave her great pleasure to entertain students and visiting scientists of all ages and nationalities

at her home overlooking the sea.

Margaret died peacefully on 30 October 2009 after an accident while working in her garden.

She will be greatly missed by all who were privileged to call her friend or colleague.

Robin N. Gibson

1

Oceanography and Marine Biology: An Annual Review, 2010, 48, 1-42

© R. N. Gibson, R. J. A. Atkinson, and J. D. M. Gordon, Editors

Taylor & Francis

Toward Ecosystem-Based Management

of Marine Macroalgae—The Bull

Kelp, Nereocystis Luetkeana

Yuri P. Springer1, Cynthia G. Hays2, Mark H. Carr1,3,4 & Megan R. Mackey3

1Department of Ecology and Evolutionary Biology, University of California Santa Cruz,

Long Marine Laboratory, 100 Shaffer Road, Santa Cruz, CA 95060, USA

E-mail: [email protected] 2Bodega Marine Laboratory, University of California Davis,

P.O. Box 247, Bodega Bay, CA 94923, USA

E-mail: [email protected] 3Pacific Marine Conservation Council, 4189 SE Division Street, Portland, OR 97202, USA

E-mail: [email protected], [email protected] 4Corresponding author

Abstract Ecosystem-based management is predicated on the multifaceted and interconnected

nature of biological communities and of human impacts on them. Species targeted by humans

for extraction can have multiple ecological functions and provide societies with a variety of ser￾vices, and management practices must recognize, accommodate, and balance these diverse values.

Similarly, multiple human activities can affect biological resources, and the separate and interactive

effects of these activities must be understood to develop effective management plans. Species of

large brown algae in the order Laminariales (kelps) are prominent members of shallow subtidal

marine communities associated with temperate coastlines worldwide. They provide a diversity of

ecosystem services, perhaps most notably the fuelling of primary production and detritus-based

food webs and the creation of biogenic habitat that increases local species diversity and abundance.

Species of kelp have also been collected for a variety of purposes throughout the history of human

habitation of these coastlines. The bull kelp, Nereocystis luetkeana, provides a clear example of how

the development of sustainable harvest policies depends critically on an understanding of the mor￾phological, physiological, life-history, demographic, and ecological traits of a species. However, for

Nereocystis as well as many other marine species, critical biological data are lacking. This review

summarizes current knowledge of bull kelp biology, ecological functions and services, and past and

ongoing management practices and concludes by recommending research directions for moving

toward an ecosystem-based approach to managing this and similarly important kelps in shallow

temperate rocky reef ecosystems.

Introduction

Why the interest in ecology and ecosystem-based

management of Nereocystis?

Among the many tenets of ecosystem-based management (EBM) of marine resources, two are cen￾tral to the goal of a more comprehensive approach to resource management. First, EBM recognizes

Y.P. Springer, C.G. Hays, M.H. Carr & M.R. Mackey

2

that species targeted for extraction can have multiple ecological functions and provide society with a

variety of ecosystem services. Management practices therefore should strive to accommodate these

diverse values (Field et al. 2006, Francis et al. 2007, Marasco et al. 2007). Second, EBM recognizes

that multiple and diverse human activities, from local fisheries to global climate change, affect

the state and sustainability of marine resources and the ecosystems that support them, and that

a thorough understanding of both the independent and interactive effects of these activities must

underpin management plans for these to be effective (Leslie & McLeod 2007, Levin & Lubchenco

2008, McLeod & Leslie 2009). As management goals move from maximizing the sustainable use

of marine resources along a single axis (e.g., single species-based sustainable fishery yields) to a

more comprehensive balancing of multiple services with each other in a manner that ensures the

sustainability of those services and their associated ecosystems, knowledge of the ecological func￾tions and services of species and of how human activities influence them will be critical. Models for

both EBM and strategies to move toward EBM must recognize species that provide multiple, well￾characterized ecological functions and services and that are known to be influenced by a variety of

human activities.

Species of large brown macroalgae of the order Laminariales, commonly referred to as kelps,

are a conspicuous component of coastal rocky reef habitats in temperate oceans throughout the

world. Kelps have been harvested throughout the history of human habitation of temperate coast￾lines for a variety of purposes, including human consumption, the production of pharmaceuticals,

and as food for commercial mariculture. However, kelps also provide a diversity of ecosystem ser￾vices to the biological communities of which they are part. As such, the consequences of human

impacts on kelps are not limited to the direct effects on kelp populations themselves, but also influ￾ence indirectly the many species that depend on or benefit from the presence of these macroalgae

in nearshore habitats.

Along the western coast of North America, two genera, the giant kelp Macrocystis spp. (here￾after Macrocystis), and the bull kelp Nereocystis luetkeana (hereafter Nereocystis), form extensive

forests in shallow (<30-m depth) rocky habitats. Because of their fast growth rate and large stature,

these algae are thought to contribute markedly both to the productivity of shallow coastal marine

ecosystems and as habitat for a diversity of fishes and invertebrates (Foster & Schiel 1985, Graham

2004, Graham et al. 2008). Both of these fundamental ecosystem functions of kelps are realized not

only by those species that reside in kelp forests throughout their lives (i.e., kelp forest residents) but

also by species that use these habitats as foraging grounds (e.g., shorebirds, sea otters) and nurseries

(particularly fishes) because of the enhanced growth and survival provided to them by the produc￾tivity and structural refuge created by kelp (see review by Carr & Syms 2006). Many of the species

that utilize kelp habitat have been strongly affected by overfishing and are themselves the focus of

conservation efforts (e.g., abalone, rockfishes, sea otters). In addition to these effects on primary and

secondary productivity in nearshore habitats, the physical barrier created by kelp forests along the

shoreline dampens ocean waves, thereby reducing coastal erosion (Lovas & Torum 2001, Ronnback

et al. 2007). Kelps also represent important biological links between marine ecosystems. The bio￾mass and nutrients they produce, in the forms of detritus or entire detached plants, are exported by

storms to sandy beaches and submarine canyons, where they fuel food webs in the absence of other

sources of primary production (Kim 1992, Vetter 1995, Harrold et al. 1998). Floating kelp rafts

may also serve as habitat for larval and juvenile fishes and invertebrates, effectively transporting

them among spatially isolated local populations of adults (Kingsford 1992, Kokita & Omori 1998,

Hobday 2000, Thiel & Gutow 2005). Furthermore, kelps are of great social, cultural, and economic

importance because of the many human activities they foster (e.g., recreational fishing, scuba div￾ing, bird watching, kayaking); tourism and recreation are included in one of the fastest-growing

sectors of California’s economy today (Kildow & Colgan 2005). Separately and in combination,