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Committee on Assessing Numeric Limits for Living Organisms in Ballast Water Water Science and Technology Board Division on Earth and Life Studies THE NATIONAL ACADEMIES PRESS Washington, D.C. www.nap.edu

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T HE NATIONAL ACADEMIES PRESS 500 Fifth Street, N.W. Washington, DC 20001 NOTICE: The project that is the subject of this report was approved by the Govern- ing Board of the National Research Council, whose members are drawn from the councils of the National Academy of Sciences, the National Academy of Engineer- ing, and the Institute of Medicine. The members of the panel responsible for the report were chosen for their special competences and with regard for appropriate balance. Support for this study was provided by the EPA and U.S. Coast Guard under contract no. EP-C-09-003, TO#11. Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the author(s) and do not necessarily reflect the views of the organizations or agencies that provided support for the project. International Standard Book Number-13: 978-0-309-21562-6 International Standard Book Number-10: 0-309-21562-5 Photo on the front cover is courtesy of Gregory M. Ruiz. Photo on the back cover is courtesy of Stephan Gollasch. Additional copies of this report are available from the National Academies Press, 500 5th Street, N.W., Lockbox 285, Washington, DC 20055; (800) 624-6242 or (202) 334-3313 (in the Washington metropolitan area); Internet, http://www.nap.edu. Copyright 2011 by the National Academy of Sciences. All rights reserved. Printed in the United States of America.

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The National Academy of Sciences is a private, nonprofit, self-perpetuating socie- ty of distinguished scholars engaged in scientific and engineering research, dedicat- ed 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 government on scien- tific and technical matters. Dr. Ralph J. Cicerone is president of the National Acad- emy 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 mem- bers, sharing with the National Academy of Sciences the responsibility for advising the federal government. The National Academy of Engineering also sponsors engi- neering programs aimed at meeting national needs, encourages education and re- search, and recognizes the superior achievements of engineers. Dr. Charles M. Vest 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 Insti- tute 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. Harvey V. Fineberg 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 Acade- my, the Council has become the principal operating agency of both the National Academy of Sciences and the National Academy of Engineering in providing ser- vices to the government, the public, and the scientific and engineering communities. The Council is administered jointly by both Academies and the Institute of Medi- cine. Dr. Ralph J. Cicerone and Dr. Charles M. Vest are chair and vice chair, re- spectively, of the National Research Council. www.national-academies.org

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Committee on Assessing Numeric Limits for Living Organisms in Ballast Water JAMES T. CARLTON, Chair, Williams College/Mystic Seaport, Mystic, Connecticut GREGORY M. RUIZ, Vice-Chair, Smithsonian Environmental Research Center, Edgewater, Maryland JAMES E. BYERS, University of Georgia, Athens ALLEGRA CANGELOSI, Northeast-Midwest Institute, Washington, D.C. FRED C. DOBBS, Old Dominion University, Norfolk, Virginia EDWIN D. GROSHOLZ, University of California, Davis BRIAN LEUNG, McGill University, Montreal, Quebec HUGH J. MACISAAC, University of Windsor, Ontario MARJORIE J. WONHAM, Quest University, Squamish, British Columbia NRC Staff LAURA J. EHLERS, Study Director ELLEN DE GUZMAN, Research Associate v 

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Water Science and Technology Board DONALD I. SIEGEL, Chair, Syracuse University, New York LISA M. ALVAREZ-COHEN, University of California, Berkeley EDWARD J. BOUWER, Johns Hopkins University, Baltimore, Maryland YU-PING CHIN, Ohio State University, Columbus OTTO C. DOERING III, Purdue University, West Lafayette, Indiana M. SIOBHAN FENNESSY, Kenyon College, Gambier, Ohio BEN GRUMBLES, Clean Water America Alliance, Washington, DC GEORGE R. HALLBERG, The Cadmus Group, Watertown, Massachusetts KENNETH R. HERD, Southwest Florida Water Management District, Brooksville GEORGE M. HORNBERGER, Vanderbilt University, Nashville, Tennessee LARRY LARSON, Association of State Floodplain Managers, Madison, Wisconsin DAVID H. MOREAU, University of North Carolina, Chapel Hill DENNIS D. MURPHY, University of Nevada, Reno MARYLYNN V. YATES, University of California, Riverside Staff STEPHEN D. PARKER, Director JEFFREY JACOBS, Scholar LAURA J. EHLERS, Senior Staff Officer STEPHANIE E. JOHNSON, Senior Staff Officer LAURA J. HELSABECK, Staff Officer M. JEANNE AQUILINO, Financial/Administrative Associate ELLEN A. DE GUZMAN, Research Associate/Senior Program Associate ANITA A. HALL, Senior Program Associate MICHAEL STOEVER, Research Associate SARAH BRENNAN, Senior Project Assistant   vi 

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Preface The human-mediated introduction of species to regions of the world they could never reach by natural means has had great impacts on the environment, the economy, and society. In the ocean, these invasions have long been me- diated by the uptake and subsequent release of ballast water in ocean-going ves- sels. Increasing world trade and a concomitantly growing global shipping fleet composed of larger and faster vessels, combined with a series of prominent bal- last-mediated invasions over the past two decades, have prompted active nation- al and international interest in ballast water management. Following the invasion of European zebra mussels (Driessena polymorpha) in the Great Lakes, the United States Congress passed the Nonindigenous Aqua- tic Nuisance Prevention and Control Act of 1990 (NANPCA), requiring the United States Coast Guard (USCG) to regulate ballast operations of ships. NANPCA was reauthorized and expanded in 1996 with the passage of the Na- tional Invasive Species Act. In 2008, the U.S. Environmental Protection Agen- cy (EPA) entered the ballast water management arena by issuing its first Vessel General Permit, under the authority of the Clean Water Act of 1972. Both the USCG and EPA ballast management programs are undergoing re- visions that focus on setting specific post-treatment discharge standards for bal- last water. Forthcoming regulatory deadlines prompted the EPA and the USCG to request the National Research Council’s (NRC) Water Science and Technolo- gy Board (WSTB) to undertake a study to provide technical advice on the deri- vation of numeric limits for living organisms in ballast water for the next EPA Vessel General Permit and for USCG programs. The sponsoring agencies asked the NRC to: 1. Evaluate the state of the science of various approaches that assess the risk of establishment of aquatic nonindigenous species given certain concentra- tions of living organisms in ballast water discharges. 2. Recommend how these approaches can be used by regulatory agencies to best inform risk management decisions on the allowable concentrations of living organisms in discharged ballast water in order to safeguard against the establishment of new aquatic nonindigenous species and to protect and preserve existing indigenous populations of fish, shellfish, and wildlife and other benefi- cial uses of the nation’s waters. vii 

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viii    Preface  3. Evaluate the risk of successful establishment of new aquatic nonindi- genous species associated with a variety of ballast water discharge limits that have been used or suggested by the international community and/or domestic regulatory agencies. Given the nature of this mandate, this report focuses on inoculum density, which is the basis of proposed discharge standards. Nonetheless, it is but one of many variables that determine whether a species will become a successful in- vader. The Committee recognized at the outset that any method that attempts to predict invasion outcomes based upon only one of many factors that influence the invasion process is likely to be characterized by a high level of uncertainty. At the request of the sponsors and given the limited time period for the study, it was not within the Committee’s charge to propose numeric discharge standards or to evaluate treatment systems that might be used in the future to achieve any such standards. Finally, the report contains a glossary of terms used. In developing this report, the Committee benefited greatly from the presen- tations and input of several individuals, including Henry Lee of EPA’s Office of Research and Development, Jim Hanlon and Ryan Albert of EPA’s Office of Wastewater Management, Richard Everett and Greg Kirkbride of the U.S. Coast Guard, Andrew Cohen of the Center for Research on Aquatic Bioinvasions, Maurya Falkner of the California State Lands Commission, and John Drake of the University of Georgia. We also thank the stakeholders who took time to share with us their perspectives and thoughts about the many complex issues associated with ballast water and other vector management, including Phyllis Green and Scott Smith, National Park Service; Vic Serveiss, International Joint Commission; Gabriela Chavarria and Tom Cmar, National Resources Defense Council; Doug Schneider, World Shipping Council; Azin Moradhassel, Cana- dian Shipowners Association; and Caroline Gravel, Shipping Federation of Can- ada. Finally, the committee thanks Miriam Tepper, Andrew Langridge, Kellina Higgins, and Cassandra Elliott—students at Quest University Canada, whose analysis of 47 papers that studied the relationship between propagule pressure and invasion rate greatly informed the discussion of models in Chapter 4. Completion of this report would not have been possible without the extraor- dinary efforts of study director Laura Ehlers, who kept us on task and on point at many potential diversions in the road, especially when shiny baubles began to distract us. The genetic disposition of the Committee to see the light at the end of the tunnel as the oncoming train was well-balanced by Laura’s equally genet- ic talent to sort wheat from chaff. Ellen de Guzman very ably supported meet- ing logistics and travel arrangements. This report has been reviewed in draft form by individuals chosen for their diverse perspectives and technical expertise, in accordance with procedures ap- proved by the NRC’s Report Review Committee. The purpose of this indepen- dent review is to provide candid and critical comments that will assist the insti- tution in making its published report as sound as possible and to ensure that the

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Preface ix report meets institutional standards for objectivity, evidence, and responsiveness to the study charge. The review comments and draft manuscript remain confi- dential to protect the integrity of the deliberative process. We thank the follow- ing individuals for their review of this report: Sarah Bailey, Great Lakes Labora- tory for Fisheries and Aquatic Sciences, Fisheries and Oceans, Canada; Lisa Drake, U.S. Naval Research Laboratory in Key West, Florida; Gustaaf Halle- graeff, University Tasmania, Australia; Russell Herwig, University of Washing- ton, Seattle; Chad Hewitt, Central Queensland University, Australia; Alex Horne, Alex Horne Associates, El Cerrito, California; Christopher Jerde, Uni- versity of Notre Dame, Indiana; and Daniel Simberloff, University of Tennesse, Knoxville. Although these reviewers have provided many constructive com- ments and suggestions, they were not asked to endorse the conclusions and rec- ommendations nor did they see the final draft of the report before its release. The review of this report was overseen by William Chameides, Duke Univer- sity, who was appointed by the NRC’s Report Review Committee and by Judith Weis, Rutgers University, who was appointed by the NRC’s Division on Earth and Life Studies. Appointed by the National Research Council, they were re- sponsible for making certain that an independent examination of this report was carried out in accordance with institutional procedures and that all review com- ments were carefully considered. Responsibility for the final content of this report rests entirely with the authoring committee and institution. James T. Carlton Gregory M. Ruiz Committee Chair Committee Vice-Chair

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Contents Summary .............................................................................................................. 1 1 SETTING THE INVASIVE SPECIES MANAGEMENT STAGE ........... 11 Introduction ................................................................................................ 11 The Number of Vessels and the Volume of Ballast Water in Play ............. 13 The Diversity of Organisms in Ballast Water Entering U.S. Coastal Waters ............................................................................ 15 Organism Concentration in Ballast Water ................................................. 19 U.S. Invasions from Ballast Water ............................................................. 25 A Further Challenge: The Polyvectic World ............................................. 26 Request for the Study and Report Roadmap .............................................. 26 References .................................................................................................. 29 2 POLICY CONTEXT FOR REGULATING LIVE ORGANISMS IN BALLAST DISCHARGE ................................................................... 35 Statutory Background of Ballast Management .......................................... 35 Standard-Setting Processes of the Two Statutes ........................................ 38 Current International, Federal, and State Standards ................................... 41 Conclusions ................................................................................................ 52 References .................................................................................................. 53 3 SOURCES OF VARIATION INFLUENCING THE PROBABILITY OF INVASION AND ESTABLISHMENT ........................................ 55 Propagule Pressure ..................................................................................... 56 Species Traits ............................................................................................. 59 Environmental Traits ................................................................................ 63 The Best-Case Scenario for an Invasion .................................................... 66 Conclusions ................................................................................................ 67 References .................................................................................................. 67   xi 

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xii    Contents  4 RELATIONSHIP BETWEEN PROPAGULE PRESSURE AND ESTABLISHMENT RISK ................................................................. 72 The Risk–Release Relationship ................................................................. 72 Single-Species Models ............................................................................... 78 Multi-Species Approaches ......................................................................... 92 Conclusions and Recommendations ........................................................ 105 References ................................................................................................ 108 5 OTHER APPROACHES TO SETTING A BALLAST WATER DISCHARGE STANDARD ............................................................. 114 Expert Opinion as an Approach to Decision-Making .............................. 114 IMO Standard Setting Approach .............................................................. 116 Zero-Detectable Discharge Standard ....................................................... 117 Natural Invasion Rates ............................................................................. 118 Conclusions............................................................................................... 119 References ................................................................................................ 120 6 THE PATH FORWARD ......................................................................... 122 Introduction .............................................................................................. 122 Models and Data Gaps ............................................................................. 124 Strategies for Moving Forward: Gathering Observational and Experimental Data ............................................................................ 127 Conclusions and Recommendations ........................................................ 130 References ................................................................................................ 134 Glossary .......................................................................................................... 137 Appendix A Committee Biographical Information ......................................... 141