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Handbook of

Ecological

Indicators for

Assessment of

Ecosystem

Health

Handbook of

Edited by

Sven E. Jørgensen

Robert Costanza

Fu-Liu Xu

Ecological

Indicators for

Assessment of

Ecosystem

Health

This book contains information obtained from authentic and highly regarded sources.

Reprinted material is quoted with permission, and sources are indicated. A wide variety of

references are listed. Reasonable efforts have been made to publish reliable data and

information, but the author and the publisher cannot assume responsibility for the validity of

all materials or for the consequences of their use.

Neither this book nor any part may be reproduced or transmitted in any form or by any

means, electronic or mechanical, including photocopying, microfilming, and recording, or by

any information storage or retrieval system, without prior permission in writing from the

publisher.

All rights reserved. Authorization to photocopy items for internal or personal use, or the

personal or internal use of specific clients, may be granted by CRC Press, provided that $1.50

per page photocopied is paid directly to Copyright Clearance Center, 222 Rosewood Drive,

Danvers, MA 01923 USA. The fee code for users of the Transactional Reporting Service is

ISBN 1-56670-665-3/05/$0.00+$1.50. The fee is subject to change without notice. For

organizations that have granted a photocopy license by the CCC, a separate system of

payment has been arranged.

The consent of CRC Press does not extend to copying for general distribution, for

promotion, for creating new works, or for resale. Specific permission must be obtained in

writing from CRC Press for such copying.

Direct all inquiries to CRC Press, 2000 N.W. Corporate Blvd., Boca Raton, Florida 33431.

Trademark Notice: Product or corporate names may be trademarks or registered

trademarks, and are used only for identification and explanation, without intent to infringe.

Visit the CRC Press Web site at www.crcpress.com

 2005 by CRC Press

No claim to original U.S. Government works

International Standard Book Number 1-56670-665-3

Library of Congress Card Number 2004015982

Printed in the United States of America 1 2 3 4 5 6 7 8 9 0

Printed on acid-free paper

Library of Congress Cataloging-in-Publication Data

Handbook of ecological indicators for assessment of ecosystem health / edited

by Sven E. Jørgensen, Robert Costanza, Fu-Liu Xu.

p. cm.

Includes bibliographical references and index.

ISBN 1-56670-665-3

1. Ecosystem health. 2. Environmental indicators. I. Jørgensen, Sven Erik,

1934. II. Costanza, Robert. III. Xu, Fu-Liu. IV. Title.

QH541.15.E265H36 2005

577.27--dc22 2004015982

The Editors

Sven Erik Jørgensen is professor of environmental chemistry at the Danish

University of Pharmaceutical Sciences. He has doctorates in engineering from

Karlsruhe University and sciences from Copenhagen University. He has been

editor in chief of Ecological Modelling since the journal started in 1975. He is

chairman of the International Lake Environment Committee. He has edited or

authored 58 books in Danish and English and written 300 papers of which two￾thirds have been published in peer-reviewed international journals. He was the

first person to receive the Prigogine Award in 2004 for his outstanding work in

the use thus far of equilibrium thermodynamics on ecosystems. He has also

received the prestigious Stockholm Water Prize for his outstanding contribu￾tion to a global dissemination of ecological modeling and ecological manage￾ment of aquatic ecosystems, mainly lakes and wetlands.

Robert Costanza is Gordon Gund professor of ecological economics and

director of the Gund Institute for Ecological Economics in the Rubenstein

School of Environment and Natural Resources at the University of Vermont.

His research interests include: landscape-level integrated spatial simulation

modeling; analysis of energy and material flows through economic and

ecological systems; valuation of ecosystem services, biodiversity, and natural

capital; and analysis of dysfunctional incentive systems and ways to correct

them. He is the author or co-author of over 350 scientific papers and 18 books.

His work has been cited in more than 2000 scientific articles since 1987 and

more than 100 interviews and reports on his work have appeared in various

popular media.

Fu-Liu Xu is an associate professor at the College of Environmental Sciences,

Peking University, China. He was a guest professor at the Research Center for

Environmental Quality Control (RCRQC), Kyoto University, from August

2003 to January 2004; and at the Research Center for Environmental Sciences,

Chinese University of Hong Kong (CUHK), from August to October 2001. He

is a member of the editorial boards for two international journals. He received

his Ph.D. from Royal Danish University of Pharmacy in 1998. His research

fields include system ecology and ecological modeling, ecosystem health and

ecological indicators, ecosystem planning and management.

Contributors

M. Austoni

University of Parma

Parma, Italy

S. Bargigli

University of Siena

Siena, Italy

Simone Bastianoni

University of Siena

Siena, Italy

Paul Bertram

U.S. Environmental Protection

Agency

Chicago, Illinois

Mark T. Brown

University of Florida

Gainesville, Florida

Villy Christiansen

University of British Columbia

Vancouver, Canada

Philippe Cury

Centre de Recherche Halieutique

Me´diterrane´enne et Tropicale

Se`te, France

Guilio A. De Leo

University of Parma

Parma, Italy

Robert Deal

Shawnee State University

Portsmouth, Ohio

Christina Forst

Oak Ridge Institute for Science

and Education, on appointment

to U.S. Environmental

Protection Agency

Oak Ridge, Tennessee

G. Giordani

University of Parma

Parma, Italy

Paul Horvatin

U.S. Environmental Protection

Agency

Chicago, Illinois

Sven E. Jørgensen

Danish University of

Pharmaceutical Sciences

Copenhagen, Denmark

Nadia Marchettini

University of Siena

Siena, Italy

Joao C. Marques

University of Coimbra

Coimbra, Portugal

William J. Mitsch

Ohio State University

Columbus, Ohio

Felix Mu¨ller

University of Kiel

Kiel, Germany

Miguel A. Pardal

University of Coimbra

Coimbra, Portugal

Jaciro M. Patrı´cio

University of Coimbra

Coimbra, Portugal

Charles Perrings

University of York

York, United Kingdom

I. Petrosillo

University of Lecce

Lecce, Italy

Martin Plus

Ifremer-Station d’Arcachon

De´partement Environnement

Littoral

Quai du Cdt Silhouette

Arcachon, France

Federico Maria Pulselli

University of Siena

Siena, Italy

Dave Raffaelli

University of York

York, United Kingdom

M. Raugei

University of Siena

Siena, Italy

Anna Renwick

University of York

York, United Kingdom

Marco Rosini

University of Siena

Siena, Italy

F. Salas

University of Coimbra

Coimbra, Portugal

Harvey Shear

Environment Canada

Downsview, Ontario, Canada

Jim Smart

University of York

York, United Kingdom

Yuri M. Svirezhev

Potsdam Institute for Climate

Impact Research

Potsdam, Germany

Sergio Ulgiati

University of Siena

Siena, Italy

P. Viaroli

University of Parma

Parma, Italy

Naiming Wang

Ohio State University

Columbus, Ohio

P.G. Wells

Environment Canada

Dartmouth, Nova Scotia, Canada

Piran White

University of York

York, United Kingdom

Xixyuan Wu

Texas A&M University

College Station, Texas

Fu-Liu Xu

Peking University

Beijing, China

N. Zaccarelli

University of Lecce

Lecce, Italy

Jose Manuel Zaldı´var-Comenges

European Commission, Joint

Research Center

Institute for Environment and

Sustainability

Inland and Marine Water Unit

Ispra, Italy

Li Zhang

Ohio State University

Columbus, Ohio

Giovanni Zurlini

University of Lecce

Lecce, Italy

Andy Zuwerink

Ohio State University

Columbus, Ohio

Contents

Chapter 1

Introduction ............................................................................................... 1

S.E. Jørgensen

1.1 The Role of Ecosystem Health Assessment in Environmental

Management ...................................................................................... 1

1.2 The Conceptual Flow in This Volume .............................................. 4

References .................................................................................................. 4

Chapter 2

Application of Indicators for the Assessment of Ecosystem Health ......... 5

S.E. Jørgensen, F.-L. Xu, F. Salas, and J.C. Marques

2.1 Criteria for the Selection of Ecological Indicators for EHA ............ 6

2.2 Classification of Ecosystem Health Indicators .................................. 7

2.2.1 Level 1.................................................................................... 7

2.2.2 Level 2.................................................................................... 8

2.2.3 Level 3.................................................................................... 8

2.2.4 Level 4.................................................................................... 8

2.2.5 Level 5.................................................................................... 9

2.2.6 Level 6.................................................................................... 9

2.2.7 Level 7.................................................................................... 10

2.2.8 Level 8.................................................................................... 10

2.3 Indices Based on Indicator Species.................................................... 10

2.3.1 Bellan’s Pollution Index ......................................................... 11

2.3.2 Pollution Index Based on Ampiphoids.................................. 12

2.3.3 AMBI ..................................................................................... 12

2.3.4 Bentix ..................................................................................... 13

2.3.5 Macrofauna Monitoring Index .............................................. 13

2.3.6 Benthic Response Index......................................................... 14

2.3.7 Conservation Index ................................................................ 14

2.4 Indices Based on Ecological Strategies.............................................. 16

2.4.1 Nematodes/Copepods Index .................................................. 19

2.4.2 Polychaetes/Amphipods Index ............................................... 19

2.4.3 Infaunal Index........................................................................ 19

2.4.4 Feldman Index ....................................................................... 20

2.5 Indices Based on the Diversity Value................................................ 21

2.5.1 Shannon–Wiener Index .......................................................... 21

2.5.2 Pielou Evenness Index.......................................................... 22

2.5.3 Margalef Index..................................................................... 23

2.5.4 Berger–Parker Index............................................................. 23

2.5.5 Simpson Index...................................................................... 23

2.5.6 Deviation from the Log-Normal Distribution..................... 23

2.5.7 K-Dominance Curves ........................................................... 24

2.5.8 Average Taxonomic Diversity.............................................. 24

2.5.9 Average Taxonomic Distinctness ......................................... 24

2.6 Indicators Based on Species Biomass and Abundance.................... 25

2.6.1 ABC Method........................................................................ 25

2.7 Indicators Integrating All Environment Information...................... 26

2.7.1 Trophic Index....................................................................... 27

2.7.2 Coefficient of Pollution ........................................................ 27

2.7.3 Benthic Index of Environmental Condition......................... 28

2.7.4 B-IBI..................................................................................... 28

2.7.5 Biotic Integrity (IBI) for Fishes ........................................... 28

2.7.6 Fish Health Index (FHI)...................................................... 29

2.7.7 Estuarine Ecological Index (EBI)......................................... 29

2.7.8 Estuarine Fish Importance Rating (FIR) ............................ 30

2.8 Presentation and Definition of Level 7 and 8 Indicators —

Holistic Indicators............................................................................ 30

2.9 An Overview of Applicable Ecological Indicators for EHA ........... 46

2.10 EHA: Procedures ............................................................................. 47

2.10.1 Direct Measurement Method (DMM) ............................... 47

2.10.2 Ecological Model Method (EMM) .................................... 47

2.10.3 Ecosystem Health Index Method (EHIM)......................... 47

2.11 An Integrated, Consistent Ecosystem Theory That Can Be

Applied as the Theoretical Basis for EHA ...................................... 49

References .................................................................................................. 55

Appendix A................................................................................................ 65

Chapter 3

Application of Ecological Indicators to Assess Environmental Quality in

Coastal Zones and Transitional Waters: Two Case Studies...................... 67

J.C. Marques, F. Salas, J.M. Patrı´cio, and M.A. Pardal

3.1 Introduction....................................................................................... 68

3.2 Brief Review on the Application of Ecological Indicators in

Ecosystems of Coastal and Transitional Waters ............................... 69

3.2.1 Indicators Based on Species Presence vs. Absence ................ 70

3.2.2 Biodiversity as Reflected in Diversity Measures.................... 76

3.2.3 Indicators Based on Ecological Strategies ............................. 77

3.2.4 Indicators Based on Species Biomass and

Abundance ............................................................................. 77

3.2.5 Indicators Accounting for the Whole Environmental

Information ............................................................................ 77

3.2.6 Thermodynamically Oriented and Network

Analysis-Based Indicators ...................................................... 78

3.3 How to Choose the Most Adequate Indicator? ................................ 78

3.4 Case Studies: Subtidal Benthic Communities in the Mondego

Estuary (Atlantic Coast of Portugal) and Mar Menor

(Mediterranean Coast of Spain) ........................................................ 78

3.4.1 Study Areas and Type of Data Utilized ................................ 78

3.4.2 Selected Ecological Indicators................................................ 83

3.4.3 Summary of Results............................................................... 83

3.4.3.1 Mondego Estuary .................................................... 83

3.4.3.2 Mar Menor .............................................................. 91

3.5 Was the Use of the Selected Indicators Satisfactory in the

Two Case Studies? ............................................................................. 94

3.5.1 Application of Indicators Based on the Presence

vs. Absence of Species: AMBI ............................................... 94

3.5.2 Indices Based on Ecologic Strategies:

Polychaetes/Amphipods Ratio ............................................... 95

3.5.3 Biodiversity as Reflected in Diversity Measures:

Margalef and Shannon–Wienner Indices............................... 95

3.5.4 Indicators Based on Species Biomass

and Abundance: W statistic ................................................... 96

3.5.5 Thermodynamically Oriented and Network

Analysis-Based Indicators: Exergy Index,

Specific Exergy and Ascendancy............................................ 96

3.5.5.1 Exergy and Specific Exergy ..................................... 96

3.5.5.2 Ascendancy .............................................................. 97

3.5.6 Brief Conclusions ................................................................... 97

References .................................................................................................. 99

Chapter 4

Development and Application of Ecosystem Health Indicators in the

North American Great Lakes Basin ........................................................ 105

H. Shear, P. Bertram, C. Forst, and P. Horvatin

4.1 Introduction..................................................................................... 106

4.1.1 Background on the Great Lakes Basin................................ 106

4.1.2 Indicator Selection ............................................................... 107

4.1.3 Definition of the Selected Indicators ................................... 109

4.2 General Considerations.................................................................... 110

4.2.1 Ecological Description of the Great Lakes Basin................ 110

4.2.1.1 Toxic Contaminants .............................................. 110

4.2.1.2 Land Use ............................................................... 110

4.2.1.3 Invasive Species ..................................................... 111

4.2.1.4 Habitat Status Including Wetlands ....................... 111

4.2.1.5 Lake Ecology ......................................................... 111

4.2.1.6 Nutrients ................................................................ 112

4.2.2 Data Collection Methods..................................................... 112

4.3 Results.............................................................................................. 113

4.3.1 State Indicators — Complete............................................... 113

4.3.1.1 Hexagenia .............................................................. 113

4.3.1.2 Wetland Dependent Bird Diversity

and Abundance...................................................... 114

4.3.1.3 Area, Quality and Protection of

Alvar Communities................................................ 114

4.3.2 State Indicators — Incomplete ............................................ 115

4.3.2.1 Native Freshwater Mussels.................................... 115

4.3.3 Pressure Indicators — Complete.......................................... 116

4.3.3.1 Phosphorus Concentrations and Loadings............ 116

4.3.3.2 Contaminants in Colonial Nesting Waterbirds ..... 118

4.3.3.3 Contaminants in Edible Fish Tissue...................... 118

4.3.4 Pressure Indicators — Incomplete ....................................... 119

4.3.4.1 Mass Transportation ............................................. 119

4.3.4.2 Escherichia Coli and Fecal Coliform Levels in

Nearshore Recreational Waters............................. 120

4.3.5 Response Indicators — Incomplete ..................................... 121

4.3.5.1 Citizen/Community Place-Based Stewardship

Activities ................................................................ 121

4.4 Discussion ........................................................................................ 122

4.4.1 Land Use.............................................................................. 122

4.4.2 Habitat Degradation ............................................................ 123

4.4.3 Climate Change.................................................................... 123

4.4.4 Toxic Contamination ........................................................... 123

4.4.5 Indicator Development ........................................................ 124

4.5 Conclusions...................................................................................... 124

References ................................................................................................ 125

Chapter 5

Application of Ecological and Thermodynamic Indicators for the

Assessment of Lake Ecosystem Health.................................................... 127

F.-L. Xu

5.1 Introduction..................................................................................... 128

5.1.1 Ecosystem Type and Problem.............................................. 128

5.1.2 The Chapter’s Focus ............................................................ 129

5.2 Methodologies.................................................................................. 129

5.2.1 A Theoretical Frame............................................................ 129

5.2.2 Development of Indicators................................................... 130

5.2.2.1 The Procedure for Developing Indicators ............. 130

5.2.2.2 Lake Data for Developing Indicators ................... 130

5.2.2.3 Responses of Lake Ecosystems to

Chemical Stresses................................................... 131

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