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Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2017. Revisiting Brucellosis in the Greater Yellowstone Area. Washington, DC: The National Academies Press. doi: 10.17226/24750.
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PR REPUBLICATION COPY N Y ADVA ANCE CO OPY NO FOR PUBLIC RELEAS BEFORE OT SE Tuesday May 31, 2017 y, , 11 a.m. EDT T A Report of This prepublica ation version has been p n provided to th public to he facili itate timely access to the committee findings. A a e e’s Although the e subbstance of th report is final, editoria changes w be made he al will through hout the text and citatio will be ch t, ons hecked prior to publication. r

THE NATIONAL ACADEMIES PRESS 500 Fifth Street, NW Washington, DC 20001 This study was supported by Grant #14-9795-2254-GR between the National Academy of Sciences and the U.S. Department of Agriculture Animal and Plant Health Inspection Service. Any opinions, findings, conclusions, or recommendations expressed in this publication do not necessarily reflect the views of any organization or agency that provided support for the project. International Standard Book Number-13: 978-0-309-45831-3 International Standard Book Number-10: 0-309-45831-5 Digital Object Identifier: https://doi.org/10.17226/24750 Additional copies of this publication are available for sale from the National Academies Press, 500 Fifth Street, NW, Keck 360, Washington, DC 20001; (800) 624-6242 or (202) 334-3313; http://www.nap.edu. Copyright 2017 by the National Academy of Sciences. All rights reserved. Printed in the United States of America Cover photo courtesy of Mark Gocke, Wyoming Game and Fish Department. Suggested citation: National Academies of Sciences, Engineering, and Medicine. 2017. Revisiting Brucellosis in the Greater Yellowstone Area. Washington, DC: The National Academies Press. doi: https://doi.org/10.17226/24750. Prepublication Copy—Subject to Further Editorial Revision

The Natio onal Academ of Science was estab my es blished in 186 by an Act of Congress signed by Presi- 63 t s, dent Linc coln, as a priv vate, nongov vernmental in nstitution to advise the n nation on issu related t sci- ues to ence and technology. Members ar elected by their peers for outstand re y ding contribu utions to rese earch. Dr. Marcia McNutt is president. a p The Natio onal Academ of Engine my eering was established in 1964 unde the charte of the Nat e n er er tional Academy of Sciences to bring th practices of engineer s he ring to advis sing the nati ion. Member are rs elected by their peer for extrao b rs ordinary cont tributions to engineering. Dr. C.D. M Mote, Jr., is presi- dent. The Natioonal Academ of Medicin (formerly the Institute of Medicine was estab my ne y e e) blished in 197 un- 70 der the charter of the National Ac c e cademy of Sc ciences to addvise the nat tion on medi ical and heal is- lth sues. Memmbers are eleected by their peers for distinguished contribution to medicin and health Dr. d d ns ne h. Victor J. Dzau is president. The three Academies work together as the Nat e tional Acadeemies of Scie neering, and Med- ences, Engin icine to provide indep p pendent, objjective analy and advic to the nat ysis ce tion and con nduct other a activi- ties to so olve complex problems an inform pu nd ublic policy d decisions. The National Ac e cademies als en- so courage education an research, recognize outstanding c e nd o contributions to knowled s dge, and inc crease public understanding in matters of science, engineering, an medicine. f nd . Learn mo about the National Ac ore e cademies of Sciences, Eng S gineering, an Medicine a www.nati nd at ional- academie es.org. Prepublic cation Copy— —Subject to Fu urther Editori Revision ial

Reports document th evidence- he -based conseensus of an authoring co ommittee of experts. Reeports typically include findi ings, conclus sions, and rec commendati ons based on information gathered b the n n by committe and comm ee mittee delibeerations. Rep ports are pee reviewed and are app er proved by the Na- tional Aca ademies of Sciences, Engineering, and Medicine. d Proceedings chronicle the presen ntations and discussions at a worksho symposiu op, um, or other con- r vening evvent. The sta atements and opinions contained in proceedings are those of the partici ipants and have not been en ndorsed by other particip pants, the pla anning comm mittee, or the National A e Acade- mies of Sc ciences, Engi ineering, and Medicine. d For inform mation about other produ t ucts and acti ivities of the National Ac e cademies, ple ease visit nat tional academie es.org/whatw wedo. Prepublicati on Copy—Su ubject to Furth Editorial Revision her

COMMITTEE ON REVISITING BRUCELLOSIS IN THE GREATER YELLOWSTONE AREA Chair TERRY F. MCELWAIN, NAM1, Washington State University Members L. GARRY ADAMS, Texas A&M University CYNTHIA L. BALDWIN, University of Massachusetts Amherst MICHAEL B. COUGHENOUR, Colorado State University PAUL C. CROSS, U.S. Geological Survey RICHARD D. HORAN, Michigan State University DAVID A. JESSUP, University of California, Davis DUSTIN P. OEDEKOVEN, South Dakota Animal Industry Board DAVID W. PASCUAL, University of Florida VALERIE E. RAGAN, Virginia-Maryland College of Veterinary Medicine GLYNN T. TONSOR, Kansas State University Staff PEGGY TSAI YIH, Study Director and Senior Program Officer JENNA BRISCOE, Research Assistant ROBIN A. SCHOEN, Director, Board on Agriculture and Natural Resources 1 National Academy of Medicine. Prepublication Copy—Subject to Further Editorial Revision v

BOARD ON AGRICULTURE AND NATURAL RESOURCES Chair CHARLES W. RICE, Kansas State University, Manhattan, KS Members SUSAN CAPALBO, Oregon State University, Corvallis, OR GAIL CZARNECKI-MAULDEN, Nestlé Purina PetCare, St. Louis, MO GEBISA EJETA, Purdue University, West Lafayette, IN ROBERT B. GOLDBERG, NAS1, University of California, Los Angeles, CA FRED GOULD, NAS1, North Carolina State University, Raleigh, NC MOLLY M. JAHN, University of Wisconsin–Madison, WI ROBBIN S. JOHNSON, Cargill Foundation, Wayzata, MN JAMES W. JONES, NAE2, University of Florida, Gainesville, FL A.G. KAWAMURA, Solutions from the Land, Washington, DC STEPHEN S. KELLEY, North Carolina State University, Raleigh, NC JULIA L. KORNEGAY, North Carolina State University, Raleigh, NC JIM E. RIVIERE, NAM3, Kansas State University, Manhattan, KS Staff ROBIN A. SCHOEN, Director CAMILLA YANDOC ABLES, Senior Program Officer JENNA BRISCOE, Research Assistant KARA N. LANEY, Senior Program Officer PEGGY TSAI YIH, Senior Program Officer 1 National Academy of Sciences. 2 National Academy of Engineering. 3 National Academy of Medicine. vi Prepublication Copy—Subject to Further Editorial Revision

Preface With a global incidence of over half a million human cases annually, brucellosis is a zoonotic dis- ease of public health concern for much of the world. Fortunately, due in large part to the brucellosis erad- ication program begun by the U.S. Department of Agriculture more than 80 years ago, the incidence of human brucellosis in the United States is now less than 0.5 cases/million population, a dramatic reduction from the high of over 6,000 cases annually in 1947. Unlike in 1947, nearly all U.S. human brucellosis cases are now caused by Brucella melitensis acquired while traveling outside the United States, not B. abortus. The only remaining U.S. reservoir of B. abortus infection is in the Greater Yellowstone Area (GYA), where wildlife transmitted cases spill over into domestic cattle and domestic bison. Yet this spill- over is now occurring with increasing frequency, raising the possibility of brucellosis reoccurrence out- side the GYA. This report examines the changing dynamic of brucellosis in the GYA, providing a com- prehensive update of what is new since the 1998 National Research Council report Brucellosis in the Greater Yellowstone Area and exploring various options for addressing the challenge of brucellosis dis- ease management. Much has changed in the 19 years since the previous report. There is now clear evidence that trans- mission of B. abortus to domestic livestock in the GYA has come from infected elk, not bison, posing greater challenges for control of transmission to domestic species. This is coupled with significant chang- es in land use around the GYA, and the increasing value that the public places on our wild lands and the wildlife they support. Indeed, change has been the norm, even during the course of the committee’s delib- erations. New cases have been recognized in cattle and domestic bison since the start of the study. Poli- cies of state agencies trying to counter the increasing incidence of brucellosis have changed. The study was conducted during the 100th anniversary year of our national park system, with Yellowstone National Park the “granddaddy” of them all. And the bison, an icon of Yellowstone National Park and a key player in brucellosis control, was officially designated as our national mammal, further raising the visibility of brucellosis management efforts in the GYA. The committee gained insight from invited speakers and an impassioned audience expressing multi- ple perspectives in public meetings. In addition to the study’s sponsor, USDA, stakeholders range from additional federal and state agencies to non-governmental organizations, and from the public who gain value and satisfaction from our wild lands and the animals they support to those who have for generations derived their livelihoods from privately owned land in and around the GYA. All are impacted by efforts to manage brucellosis caused by B. abortus in the last remaining disease reservoir. There is a complexity and interdependency in addressing the issue that mirrors the complexity of the ecosystem in which brucel- losis occurs, and which defies both simple solutions and a perfect solution. The committee has taken an objective, science-based approach in addressing its Statement of Task, and presents this report as a com- prehensive starting point for discussions among all stakeholders to address a problem of increasing con- cern. We trust this report will be helpful in those deliberations. I would like to express thanks to all the committee members for their dedication and perseverance during the long course of the committee’s deliberations and writing. On behalf of the committee, sincere thanks are also extended to the study director, Peggy Yih, who did an outstanding job of directing a chal- lenging task, and to Robin Schoen and Jenna Briscoe who provided background support for the study. As Prepublication Copy—Subject to Further Editorial Revision vii

Preface always, a National Academies report simply does not happen de novo and capable hands guide the pro- cess throughout. Lastly, the committee thanks all those who provided input during multiple public meet- ings and to those who provided answers in response to what may at times have seemed like an endless list of questions and requests. We are grateful for your efforts in supporting this report. Terry F. McElwain, Chair Committee on Revisiting Brucellosis in the Greater Yellowstone Area viii Prepublication Copy—Subject to Further Editorial Revision

Acknowledgments This report has been reviewed in draft form by individuals chosen for their diverse perspectives and technical expertise. The purpose of this independent review is to provide candid and critical comments that will assist the institution in making its published report as sound as possible and to ensure that the report meets institutional standards for objectivity, evidence, and responsiveness to the study charge. The review comments and draft manuscript remain confidential to protect the integrity of the deliberative pro- cess. We wish to thank the following individuals for their review of this report: Mark S. Boyce, University of Alberta Norman Cheville, Iowa State University Andrew Dobson, Princeton University Francis D. Galey, University of Wyoming Robert Garrott, Montana State University Colin Gillin, Oregon Department of Fish and Wildlife N. Thompson Hobbs, Colorado State University Bret Marsh, Indiana State Board of Animal Health Michael W. Miller, Colorado Division of Parks and Wildlife Robert Nordgren, Merial Daniel O’Brien, Michigan Department of Natural Resources Gary Splitter, University of Wisconsin Michael Springborn, University of California, Davis Although the reviewers listed above have provided many constructive comments and suggestions, they were not asked to endorse the conclusions or recommendations, nor did they see the final draft of the report before its release. The review of this report was overseen by Gordon H. Orians, University of Washington, and James E. Womack, Texas A&M University, who were responsible for making certain that an independent examination of this report was carried out in accordance with institutional procedures and that all review comments were carefully considered. Responsibility for the final content of this report rests entirely with the authoring committee and the institution. Prepublication Copy—Subject to Further Editorial Revision ix

Contents SUMMARY .................................................................................................................................................................. 1 1 INTRODUCTION ..................................................................................................................................... 10 Background, 10 The Greater Yellowstone Area, 11 Administrative Complexity of the GYA, 14 Purpose of This Study, 15 Approach to the Task, 15 Organization of the Report, 16 References, 17 2 GEOGRAPHIC SCOPE OF POPULATIONS AND DISEASE AND CHANGE IN LAND USE ......................................................................................................................... 19 Introduction, 19 Elk Populations and Distributions, 19 Changes in Land Use and Consequences for Elk, 32 Bison Populations and Distributions, 33 Livestock, 38 Implications of Changing Climate for Elk and Bison, 39 Summary, 41 References, 42 3 ECOLOGY AND EPIDEMIOLOGY OF BRUCELLA ABORTUS IN THE GREATER YELLOWSTONE ECOSYSTEM ..................................................................................... 48 Review of Brucellosis Cases Since 1998, 48 Disease Dynamics in Bison and Elk, 51 Effects of Population Size and Aggregation on Bison and Elk Transmission, 56 Supplemental Feedgrounds, 59 Potential Effects of Predators and Scavengers on Brucellosis, 60 Effect of Disease on Bison and Elk Populations, 61 References, 62 4 SCIENTIFIC PROGRESS AND NEW RESEARCH TOOLS .......................................................... 65 Infection Biology and Pathogenesis of B. abortus in Cattle, Bison, and Elk, 65 Diagnostics, 67 Commercial Vaccines in Wildlife, 71 New Scientific Tools Informing Brucellosis Infection Biology, Pathogenesis, and Vaccinology, 74 Conclusion, 75 References, 75 Prepublication Copy—Subject to Further Editorial Revision xi

Contents 5 FEDERAL, STATE, AND REGIONAL MANAGEMENT EFFORTS ........................................... 83 Brief Historical Overview of Brucellosis Control Efforts, 83 Changes in Status and Classification of States, 83 Regional and National Control Programs, 84 Interagency Cooperative Bodies, 90 Surveillance, 92 Bison Separation and Quarantine, 95 Costs of Programs, 95 References, 98 6 ADAPTIVE MANAGEMENT .............................................................................................................. 101 Defining Adaptive Management, 101 Adaptive Management in the GYA: Case Studies, 103 References, 106 7 MANAGEMENT OPTIONS ................................................................................................................. 110 Introduction, 110 Incentivizing Risk Mitigation Efforts, 110 Use of Feedgrounds, 111 Hunting of Wildlife, 113 Land Use, 116 Zoning Using Designated Surveillance Areas, 117 Test and Remove, 118 Vaccines and Delivery Systems for Cattle, Bison, and Elk, 120 Sterilization and Contraceptives, 121 Predation and Scavengers, 122 References, 123 8 ECONOMIC ISSUES IN MANAGING BRUCELLOSIS ................................................................ 128 Introduction, 128 Bioeconomic Framework, 129 Economic Efficiency in a Dynamic, Coupled System, 137 Promoting Private Disease Control Efforts, 143 Summary, 148 References, 148 9 REMAINING GAPS FOR UNDERSTANDING AND CONTROLLING BRUCELLOSIS ...................................................................................................... 153 Introduction, 153 Disease Ecology, 153 Economics, 154 Immunology, 155 Vaccines and Delivery Mechanisms, 157 Genotyping and Genetics, 159 Diagnostics, 161 References, 163 10 OVERALL FINDINGS, CONCLUSIONS, AND RECOMMENDATIONS ................................. 169 What’s New Since 1998?, 169 Adopting an Active Adaptive Management Approach, 170 Adaptive Management Options to Reduce Risk, 171 Bioeconomics: A Framework for Making Decisions, 179 A Call to Strategic Action, 179 xii Prepublication Copy—Subject to Further Editorial Revision

Contents Research Agenda, 182 Concluding Remarks, 185 References, 185 APPENDIXES A BIOGRAPHICAL SKETCHES OF COMMITTEE MEMBERS ................................................ 186 B OPEN SESSION MEETING AGENDAS ....................................................................................... 190 BOXES, FIGURES, AND TABLES BOXES 1-1 Statement of Task, 16 7-1 Land Management Risk Assessment to Reduce Disease Risks, 112 FIGURES 1-1 Map of the Greater Yellowstone Area by jurisdiction, 12 1-2 Map showing GYA boundary and designated surveillance areas as of 2016, 13 2-1 Map of migration corridors, winter ranges (blue polygons) and summer ranges (tan polygons) of 9 of 11 major elk herds in the GYA, 20 2-2 Northern Yellowstone elk numbers, 21 2-3 Elk numbers and percentages north of Yellowstone National Park and on Dome Mountain, 22 2-4 Elk management units in Montana and elk hunt units in Wyoming, and game management units in Idaho relation to the designated surveillance area and the YNP boundary, as of 2014, 25 2-5 Trends in elk numbers in Montana elk management units, 26 2-6 Histogram of the elk group size distribution from the eastern portion of the GYA in Wyoming, 27 2-7 Elk population trends in herds east of YNP, 28 2-8 Elk population trends in herds south and southeast east of YNP, 29 2-9 Elk population trends in herds the furthest south of YNP, 29 2-10 Bison range distribution conservation areas, and Zone 2 bison tolerance areas, 34 2-11 Bison counts and annual removals, northern and central herds, 35 2-12 Bison population growth rates versus population sizes in the previous year, northern and central herds, 37 2-13 Grazing allotments throughout the GYA, 39 2-14 Active U.S. Forest Service grazing allotments in Bridger-Teton National Forest, 40 3-1 Number of cattle and domestic bison herds infected with B. abortus in the Greater Yellowstone Area by state from 1990 to 2016, 48 3-2 States to which animals leaving Brucellosis-affected herds in the GYA were traced, 2002-2016, 52 3-3 Maps of seroprevalence in elk using data prior to 2000 (left) and from 2010 to 2015 (right), 53 3-4 Maps of sampling effort in elk prior to 2000 (left) and from 2010 to 2015 (right), 53 3-5 Elk seroprevalence in the East Madison Hunt District 362 (left plot) and Gardiner Area HD 313 (right plot), 54 3-6 Elk seroprevalence in the Cody (left plot) and Clarks Fork (right plot) regions of Wyoming, 55 3-7 Elk seroprevalence in the South Wind River (left plot) and West Green River (right plot) regions of Wyoming, both of which are south and adjacent to regions with supplemental feedgrounds, 55 3-8 Elk seroprevalence over time for two management units in Idaho, District 66A (left), District 76 (right), 56 3-9 Elk seroprevalence over time for management units in Idaho where the seroprevalence may be increasing (Districts 61, 62, and 67), 57 Prepublication Copy—Subject to Further Editorial Revision xiii

Contents 3-10 Elk seroprevalence over time for several management units in Idaho (Districts 64, 65, and 66) that are too weakly sampled to assess any temporal trends, 58 4-1 Greater Yellowstone Area tri-state schematic for serological testing of elk, 70 5-1 Seroprevalence of B. abortus in elk by year for test and slaughter pilot project at Muddy Creek Feedground, 89 5-2 Efficacy of elk Brucella strain 19 vaccination, 90 8-1 A bioeconomic assessment of economic costs and benefits, 130 TABLES 2-1 Elk Numbers in Elk Management Units (Hunting Districts) North and Northwest of YNP, But Within the Brucellosis DSA, in 2015, 24 2-2 Numbers of Elk in Herds East of YNP in Wyoming in 2015, 27 2-3 Numbers of Elk in Herds South and Southeast of YNP in Wyoming in 2015, 28 2-4 Elk Herds in Idaho in the GYA, 30 3-1 Brucellosis Herds Detected in the Greater Yellowstone Area, 2002-2016, 49 4-1 Summary of RB51’s Efficacy in Bison, 73 5-1 Federal Agency Jurisdiction and Involvement in Brucellosis, 85 5-2 State Agency Jurisdiction and Involvement in Brucellosis, 88 5-3 Estimated Number of Samples Collected by Slaughter Plant for FY2017 (October 1, 2016, through September 30, 2017), 94 xiv Prepublication Copy—Subject to Further Editorial Revision

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Brucellosis is a nationally and internationally regulated disease of livestock with significant consequences for animal health, public health, and international trade. In cattle, the primary cause of brucellosis is Brucella abortus, a zoonotic bacterial pathogen that also affects wildlife, including bison and elk. As a result of the Brucellosis Eradication Program that began in 1934, most of the country is now free of bovine brucellosis. The Greater Yellowstone Area (GYA), where brucellosis is endemic in bison and elk, is the last known B. abortus reservoir in the United States. The GYA is home to more than 5,500 bison that are the genetic descendants of the original free-ranging bison herds that survived in the early 1900s, and home to more than 125,000 elk whose habitats are managed through interagency efforts, including the National Elk Refuge and 22 supplemental winter feedgrounds maintained in Wyoming.

In 1998 the National Research Council (NRC) issued a report, Brucellosis in the Greater Yellowstone Area, that reviewed the scientific knowledge regarding B. abortus transmission among wildlife—particularly bison and elk—and cattle in the GYA. Since the release of the 1998 report, brucellosis has re-emerged in domestic cattle and bison herds in that area. Given the scientific and technological advances in two decades since that first report, Revisiting Brucellosis in the Greater Yellowstone Area explores the factors associated with the increased transmission of brucellosis from wildlife to livestock, the recent apparent expansion of brucellosis in non-feedground elk, and the desire to have science inform the course of any future actions in addressing brucellosis in the GYA.

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