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ECOLOGICAL INDICATORS FOR THE NATION Committee to Evaluate Indicators for Monitoring Aquatic and Terrestrial Environments Board on Environmental Studies and Toxicology Water Science and Technology Board Commission on Geosciences, Environment, and Resources National Research Council NATIONAL ACADEMY PRESS Washington, D.C.

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NATIONAL ACADEMY PRESS 2101 Constitution Avenue, NW Washington, DC 20418 NOTICE: The project that is the subject of this report was approved by the Governing Board of the National Research Council, whose members are drawn from the councils of the National Academy of Sciences, the National Academy of Engineering, and the Institute of Medicine. The members of the committee re- sponsible for the report were chosen for their special competences and with re- gard for appropriate balance. This study was supported by the U.S. Environmental Protection Agency under Grant No. C R 825198-01. Ecological Indicators for the Nation is available from the National Academy Press, 2101 Constitution Ave., N.W., Box 285, Washington, DC 20055; (800) 624-6242 or (202) 334-3313 (in the Washington metropolitan area); Internet . Library of Congress Cataloging-in-Publication Data Ecological indicators for the nation / Committee to Evaluate Indicators for Monitoring Aquatic and Terrestrial Environments, Board on Environmental Studies and Toxicology [and] Water Science and Technology Board, Commission on Geosciences, Environment, and Resources, National Research Council. p. cm. Includes bibliographical references and index. ISBN 0-309-06845-2 (casebound) 1. Indicators (Biology) 2. Environmental monitoring. I. National Research Council (U.S.~. Committee to Evaluate Indicators for Monitoring Aquatic and Terrestrial Environments. QH541.15.I5 E36 2000 363.7'063'0973 dc21 00-008009 Cover art: Stewardship by Greg Mort. The piece, used courtesy of the artist, includes his reflections on the importance of understanding the biosphere. Copyright 2000 by the National Academy of Sciences. All rights reserved. Printed in the United States of America

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National Acaclemy of Sciences National Acaclemy of Engineering Institute of Meclicine National Research Council The National Academy of Sciences is a private, nonprofit, self-perpetuating society of distinguished scholars engaged in scientific and engineering research, dedicated to the furtherance of science and technology and to their use for the general welfare. Upon the authority of the charter granted to it by the Congress in 1863, the Academy has a mandate that requires it to advise the federal govern- ment on scientific and technical matters. Dr. Bruce M. Alberts is president of the National Academy of Sciences. The National Academy of Engineering was established in 1964, under the charter of the National Academy of Sciences, as a parallel organization of outstanding engineers. It is autonomous in its administration and in the selection of its members, sharing with the National Academy of Sciences the responsibility for advising the federal government. The National Academy of Engineering also sponsors engineering programs aimed at meeting national needs, encourages education and research, and recognizes the superior achievements of engineers. Dr. William A. Wulf is president of the National Academy of Engineering. The Institute of Medicine was established in 1970 by the National Academy of Sciences to secure the services of eminent members of appropriate professions in the examination of policy matters pertaining to the health of the public. The Institute acts under the responsibility given to the National Academy of Sciences by its congressional charter to be an adviser to the federal government and, upon its own initiative, to identify issues of medical care, research, and education. Dr. Kenneth I. Shine is president of the Institute of Medicine. The National Research Council was organized by the National Academy of Sciences in 1916 to associate the broad community of science and technology with the Academy's purposes of furthering knowledge and advising the federal govern- ment. Functioning in accordance with general policies determined by the Acad- emy, the Council has become the principal operating agency of both the National Academy of Sciences and the National Academy of Engineering in providing services to the government, the public, and the scientific and engineering commu- nities. The Council is administered jointly by both Academies and the Institute of Medicine. Dr. Bruce M. Alberts and Dr. William A. Wulf are chairman and vice chairman, respectively, of the National Research Council.

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BOARD ON ENVIRONMENTAL STUDIES AND TOXICOLOGY GORDON ORIANS (Chair), University of Washington, Seattle DONALD MATrISON (Vice Chair), March of Dimes, White Plains, New York DAVID ALLEN, University of Texas, Austin INGRlD C. BURKE, Colorado State University, Fort Collins WILLIAM L. CHAMElDES, Georgia Institute of Technology, Atlanta JOHN DOULL, The University of Kansas Medical Center, Kansas City CHRISTOPHER B. FIELD, Carnegie Institute of Washington, Stanford, California JOHN GERHART, University of California, Berkeley I. PAUL OILMAN, Celera Genom~cs, Rockville, Maryland BRUCE D. HAMMOCK, University of California, Davis MARK HARWELL, University of Miami, Miami, Florida ROGENE HENDERSON, Lovelace Respiratory Research Institute, Albuquerque, New Mexico CAROL HENRY, Chemical Manufacturers Association, Arlington, Virginia BARBARA HULKA, University of North Carolina, Chapel Hill JAMES F. KITCHELL, University of Wisconsin Madison DANIEL KREWSKI, University of Ottawa, Ottawa, Ontario JAMES A. MACMAHON, Utah State University, Logan MARIO I. MOLINA, Massachusetts Institute of Technology, Cambridge CHARLES O'MELLA, The Johns Hopkins University, Baltimore, Maryland WILLEM F. PASSCHIER Health Council of the Netherlands KIRK SMITH, University of Califomia, Berkeley MARGARET N. STRAND, Oppenheimer Wolff Donnelly & Bayh, Washington, D.C. TERRY F. YOSIE, Chemical Manufacturers Association, Arlington, VA Senior Staff JAMES J. REISA, Director DAVID J. POLICANSKY, Associate Director and Senior Program Director for Applied Ecology CAROL A. MACZKA' Senior Program Director for Toxicology and Risk Assessment RAYMOND A. WASSEL, Senior Program Director for Environmental Sciences and Engineering KULBIR BAKSHI. Program Director for the Committee on Toxicology LEE R. PAULSON, Program Director for Resource Management PREPUBLICATION COPY

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COMMITTEE TO EVALUATE INDICATORS FOR MONITORING AQUATIC AND TERRESTRIAL ENVIRONMENTS GORDON H. ORIANS (Chair), University of Washington, Seattle MARTIN ALEXANDER, Cornell University, Ithaca, New York PATRICK L. BREZONIK, University of Minnesota, St. Paul GRACE BRUSH, The Johns Hopkins University, Baltimore, Maryland EVILLE GORHAM, University of Minnesota, Minneapolis ANTHONY rANETOS, World Resources Institute, Washington, D.C. ARTHUR H. rOHNSON, University of Pennsylvania, Philadelphia DANIEL V. MARKOWITZ, Malcolm Pirnie, Akron, Ohio STEPHEN W. PACALA, Princeton University, Princeton, New Jersey rOHN PASTOR, University of Minnesota, Duluth GARY W. PETERSEN, Pennsylvania State University, University Park TAMES R. PRATT, Portland State University, Portland, Oregon TERRY ROOT, The University of Michigan, Ann Arbor MICHAEL L. ROSENZWEIG, University of Arizona, Tucson MILTON RUSSELL, University of Tennessee, Knoxville SUSAN STAFFORD, Colorado State University, Fort Collins National Research Council Staff DAVID POLICANSKY, Project Director rEFFREY W. rACOBS, Senior Staff Officer ANITA A. HALL, Project Assistant STEPHANIE L. VANN, Project Assistant v

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BOARD ON ENVIRONMENTAL STUDIES AND TOXICOLOGY GORDON ORIANS (Chair), University of Washington, Seattle DONALD MATTISON (Vice Chair), March of Dimes, White Plains, New York DAVID ALLEN, University of Texas, Austin INGRID C. BURKE, Colorado State University, Fort Collins WILLIAM L. CHAMEIDES, Georgia Institute of Technology, Atlanta rOHN DOULL, The University of Kansas Medical Center, Kansas City CHRISTOPHER B. FIELD, Carnegie Institute of Washington, Stanford, California rOHN GERHART, University of California, Berkeley I. PAUL OILMAN, Celera Genomics, Rockville, Maryland BRUCE D. HAMMOCK, University of California, Davis MARK HARWELL, University of Miami, Miami, Florida ROGENE HENDERSON, Lovelace Respiratory Research Institute, Albuquerque, New Mexico CAROL HENRY, Chemical Manufacturers Association, Arlington, Virginia BARBARA HULKA, University of North Carolina, Chapel Hill TAMES F. KITCHELL, University of Wisconsin, Madison DANIEL KREWSKI, University of Ottawa, Ottawa, Ontario TAMES A. MACMAHON, Utah State University, Logan MARIO I. MOLINA, Massachusetts Institute of Technology, Cambridge CHARLES O'MELIA, The Johns Hopkins University, Baltimore, Maryland WILLEM F. PASSCHIER, Health Council of the Netherlands KIRK SMITH, University of California, Berkeley MARGARET N. STRAND, Oppenheimer Wolff Donnelly & Bayh, Washington, D.C. TERRY F. YOSIE, Chemical Manufacturers Association, Arlington, VA Senior Staff TAMES I. REISA, Director DAVID J. POLICANSKY, Associate Director and Senior Program Director for Applied Ecology CAROL A. MACZKA, Senior Program Director for Toxicology and Risk Assessment RAYMOND A. WASSEL, Senior Program Director for Environmental S. , ~ . . clences ana tngmeermg KULBIR BAKSHI, Program Director for the Committee on Toxicology LEE R. PAULSON, Program Director for Resource Management Al

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WATER SCIENCE AND TECHNOLOGY BOARD HENRY I. VAUX, rR. (Chair), University of California, Riverside CAROL A. rOHNSTON (Vice Chair), University of Minnesota, Duluth RICHELLE M. ALLEN-KING, Washington State University, Pullman GREGORY B. BAECHER, University of Maryland, College Park rOHN S. BOYER, University of Delaware, Lewes rOHN BRISCOE, The World Bank, Washington, D.C. DENISE FORT, University of New Mexico, Albuquerque STEVEN P. GLOSS, University of Wyoming, Laramie EVILLE GORHAM, University of Minnesota, St. Paul WILLIAM A. rURY, University of California, Riverside GARY S. LOGSDON, Black & Veatch, Cincinnati, Ohio RICHARD G. LUTHY, Carnegie Mellon University, Pittsburgh, Pennsylvania rOHN W. MORRIS, I. W. Morris Ltd., Arlington, Virginia PHILLIP A. PALMER, DuPont Engineering, Wilmington, Delaware REBECCA T. PARKIN, The George Washington University, Washington, D.C. rOAN B. ROSE, University of South Florida, St. Petersburg RHODES TRUSSELL, Montgomery Watson, Inc., Pasadena, California ERIC F. WOOD, Princeton University, Princeton, New Jersey Staff STEPHEN D. PARKER, Director CHRIS ELFRING, Senior Staff Officer LAURA EHLERS, Senior Staff Officer rEFFREY W. rACOBS, Senior Staff Officer rEANNE AQUILINO, Administrative Associate MARK GIBSON, Research Associate ANITA A. HALL, Administrative Assistant ELLEN de GUZMAN, Senior Project Assistant ANIKE rOHNSON, Project Assistant . . v''

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COMMISSION ON GEOSCIENCES, ENVIRONMENT, AND RESOURCES GEORGE M. HORNBERGER (Chair), University of Virginia, Charlottesville RICHARD A. CONWAY, Union Carbide Corporation (Retired), S. Charleston, West Virginia THOMAS E. GRAEDEL, Yale University, New Haven, Connecticut THOMAS I. GRAFF, Environmental Defense Fund, Oakland, California EUGENIA KALNAY, University of Maryland, College Park DEBRA KNOPMAN, Progressive Policy Institute, Washington, D.C. KAI N. LEE, Williams College, Williamstown, Massachusetts RICHARD A. MESERVE, Covington & Burling, Washington, D.C. BRAD MOONEY, rR., I. Brad Mooney Associates, Ltd., Arlington, Virginia HUGH C. MORRIS, E1 Dorado Gold Corporation, Vancouver, British Columbia H. RONALD PULLIAM, University of Georgia, Athens MILTON RUSSELL, University of Tennessee, Knoxville THOMAS C. SCHELLING, University of Maryland, College Park ANDREW R. SOLOW, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts VICTORIA I. TSCHINKEL, Landers and Parsons, Tallahassee, Florida E-AN ZEN, University of Maryland, College Park MARY LOU ZOBACK, U.S. Geological Survey, Menlo Park, California Staff ROBERT M. HAMILTON, Executive Director GREGORY H. SYMMES, Associate Executive Director NANETTE SPOON, Administrative and Financial Officer SANDI FITZPATRICK, Administrative Associate MARQUITA SMITH, Administrative Assistant/Technology Analyst . . . v'''

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Preface The U.S. Environmental Protection Agency (EPA) is reevaluating its approach to environmental monitoring. In this context, the agency asked the National Research Council (NRC) to conduct a critical scientific evaluation of indicators to monitor ecological changes from either natural or anthropogenic causes. Specifically, EPA asked the NRC to identify criteria for evaluating biological indicators, to evaluate methods of indicator development, to provide examples of indicators that have proven useful, and to identify areas where further research is likely to yield more useful and powerful indicators. The NRC was also asked to examine what aspects of environmental conditions and trends should be monitored. It was also requested to identify aspects of ecosystem struc- ture and functioning that have been particularly difficult to characterize by means of indicators and to assess whether new approaches might allow some of these aspects to be better characterized. In response to EPA's request, the NRC established the Committee to Evaluate Indicators for Monitoring Aquatic and Terrestrial Environments (hereafter referred to as the "Indicators Committees. This committee has focused on ecological indicators for EPA's Environmental Monitoring and Assessment Program (EMAP), and for the needs of the ecological moni- toring programs of other federal and state agencies as well. The Indica- tors Committee's focus on ecological indicators of environmental status and trends is timely, because the development of ecological indicators has been more difficult than that of physical indicators, which has a rich and extensive history. Today, the use of a number of physical indicators, such 1 ~

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x PREFACE as atmospheric concentrations of carbon dioxide, already command con- siderable attention within the United States and internationally. Ecological processes and products are varied and often complex, and large numbers of ecological indicators have been developed and used. These indicators are often intended to inform decision makers about the status and trends in populations of particular species and small groups of species, and in particular ecosystems. Useful though some of these indi- cators may be, they do not provide a basis for evaluating in general terms the state of the nation's ecosystems and how they are changing. Thus, most current ecological indicators have limited use for guiding national environmental policies. With this in mind, the Indicators Committee decided that its main task was to identify and characterize general eco- logical indicators capable of informing the public and decision makers about the overall state of the nation's ecosystems and how those ecosys- tems may be changing due to anthropogenic and other pressures. Decision makers and the public need accurate information on eco- logical conditions and changes for three major reasons. First, a long-term record of conditions is needed as a reference to evaluate current condi- tions and trends. Second, detailed information on the ecological effects of various human activities and natural events such as pollution, develop- ment, agriculture, climate change, and geomorphological events is es- sential for selecting and implementing management options to address problems successfully. Finally, long-term ecological data are needed for society to measure the effectiveness and efficiency of management inter- ventions and to improve them. In responding to its charge, the Indicators Committee examined pre- vious relevant reports of the National Research Council, including re- views of EPA's Environmental Monitoring and Assessment Program (Re- view of EPA's Environmental Management and Assessment Program: Forests and Estuaries t1994}, Surface Waters t1994}, Overall Evaluation t1995~), A Review of the USGS. National Water Quality Assessment Pilot Program (1990), Review of the Department of the Interior's Biomonitoring of Environmental Status and Trends Program: The Draft Detailed Plan (1995), Biologic Markers of Air-Pollution Stress and Damage in Forests (1989), Managing Troubled Wa- ters: The Role of Marine Environmental Monitoring (1990), Animals as Senti- nels of Environmental Health Hazards (1991), and four reviews of the Miner- als Management Service's Outer Continental Shelf Environmental Studies Program (Assessment ofthe U.S. Outer Continental ShelfEnvironmental Stud- ies Program: I. Physical Oceanography 119901, II. Ecology 119921, III. Social ~All published by National Academy Press, Washington, D.C.

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PREFACE Xl i and Economic Studies t1992}, and IV. Lessons and Opportunities 1993. Recognizing that much effort had already been expended by many ca- pable and informed people to devise ecological indicators, the Indicators Committee also reviewed a wide array of documents produced by fed- eral, state, and private agencies and individual investigators, many of which have been published in peer-reviewed journals and books. The Indicators Committee gratefully acknowledges the valuable pre- sentations made at its meetings by Robert Huggett, Vice President for Research and Graduate Studies, Michigan State University (then Assis- tant Administrator for Research and Development, U.S. Environmental Protection Agency); Steven Paulsen, Director of the Environmental Moni- toring and Assessment Program (EMAP), National Health and Environ- mental Effects Research Laboratory (NHEERL), Western Ecology Divi- sion, U.S. Environmental Protection agency; Gilman Veith, Associate Director for Ecology, NHEERL, U.S. Environmental Protection Agency; Ray Wilhour, Associate Director for Science, Gulf Ecology Division, NHEERL, U.S. Environmental Protection Agency. As always, the work of the committee has depended greatly on its supporting NRC staff. Anita Hall and Stephanie Vann have been respon- sible for the complex logistics involved in committee meetings, and lef- frey lacobs helped locate essential literature. km Reisa's insights and experience with the topic much improved the clarity of this report. The committee particularly acknowledges the extensive efforts and intellec- tual contributions of the project director, David Policansky. Carole Rosenzweig helped arranged the venue for a very productive meeting of the committee in Arizona in February 1998. Gordon Orians, Chair

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Acknowledgment of Reviewers This report has been reviewed by individuals chosen for their diverse perspectives and technical expertise, in accordance with procedures approved by the National Research Council's Report Review Com- mittee. The purpose of this independent review is to provide candid and critical comments that will assist the institution in making the published report as sound as possible and to ensure that the report meets institu- tional standards for objectivity, evidence, and responsiveness to the study charge. The review comments and draft manuscripts remain confidential to protect the integrity of the deliberative process. We wish to thank the following individuals for their participation in the review of this report: Ann Bartuska, U.S. Forest Service William C. Clark, Harvard University T. Clarence Davies, Resources for the Future Richard Fisher, Texas A&M University Lisa Graumlich, Montana State University Mark A. Harwell, University of Miami H. Ronald Pulliam, University of Georgia Stephen Running, University of Montana While the individuals listed above provided constructive comments and suggestions, it must be emphasized that responsibility for the final content of this report rests entirely with the authoring committee and the institution. . . . x'''

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XIV 6 INDICATORS FOR NATIONAL ECOLOGICAL ASSESSMENTS The Nation's Ecological Capital: The Capacity of the Nation's Ecosystems to Function, 57 Indicators of Ecological Capital: A. Biotic Raw Materials, 65 Indicators of the Performance of the Nation's Ecosystems, 78 Indicators of Nutrient-Use Efficiency and Nutrient Balances in Agroecosystems, 90 Research Needs, 96 LOCAL AND REGIONAL INDICATORS Introduction, 99 Productivity Indicators, 99 Forests as an Example, 100 Indicators of Species Diversity, ~ 04 REFERENCES APPENDIXES A B C Contents 56 VARIABILITY, COMPLEXITY, AND THE DESIGN OF SAMPLrNG PROCEDURES ......................................................................................................... MARKOV MATRICES OF LANDSCAPE CHANGE '' BIOGRAPHICAL SKETCHES OF COMMITTEE MEMBERS AND STAFF PREPUBLICATION COPY 99 113 .135 143 147

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Contents EXECUTIVE SUMMARY Scales and Applicability of Indicators, 2 Criteria for Evaluating Indicators, 3 The Committee's Conceptual Model for Choosing Indicators, 6 Policy Perspectives, 7 The Recommended Indicators, 7 Timing and Cost of Implementing the Committee's Recommendations, 13 Local and Regional Indicators, 14 Care and Handling of Environmental Data, 17 Research, 17 1 INTRODUCTION Why Are Ecological Indicators Needed?, 18 This Study, 21 Key Ecological Processes and Products That People Value, 22 Establishing Baselines to Evaluate Trends, 23 Evaluating Indicators, 25 Realistic Expectations about the Value of Indicators, 26 xv 1 18

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XVI CONTENTS 2 THE EMPIRICAL AND CONCEPTUAL FOUNDATIONS OF INDICATORS Scientific Underpinnings of Indicators, 29 Using Multiple Approaches, 31 Historical and Paleoecological Data As Aids to Indicator Development, 31 Sources of Information about Current Ecological Processes, 34 Models to Assess Ecosystem Functioning, 43 The Committee's Conceptual Model for Choosing Indicators, 48 3 A FRAMEWORK FOR INDICATOR SELECTION Criteria for Evaluating Indicators, 52 Information Handling and Calibration, 58 Data Quality Control, Archiving, and Assignment of Responsibilities, 59 Use of the Committee Framework, 62 27 51 4 INDICATORS FOR NATIONAL ECOLOGICAL ASSESSMENTS 64 The Extent and Status of the Nation's Ecosystems, 67 Indicators of Ecological Capital: A. Biotic Raw Materials, 75 Indicators of Ecological Capital: B. Abiotic Raw Materials, 83 Indicators of the Performance of the Nation's Ecosystems, 90 Indicators of Nutrient-Use Efficiency and Nutrient Balances in Agroecosystems, 104 Research Needs, 113 5 LOCAL AND REGIONAL INDICATORS Introduction, 116 Productivity Indicators, 117 Forests as an Example, 117 Indicators of Species Diversity, 123 6 REFERENCES APPENDIXES A VARIABILITY, COMPLEXITY, AND THE DESIGN OF SAMPLING PROCEDURES B MARKOV MATRICES OF LANDSCAPE CHANGE C BIOGRAPHICAL SKETCHES OF COMMITTEE MEMBERS AND STAFF INDEX 116 131 151 159 165 171

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ECOLOGICAL I N DICATORS FOR THE NATION

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