Pesticide Risk Assessment for Pollinators E-Book

David Fischer

• Herausgeber: John Wiley & Sons
• Kategorie: Fachliteratur
• Sprache: Englisch
• Veröffentlichungsjahr: 2014

Seitenzahl: 573

Beschreibung

Pollinators play a vital role in ecosystem health and are essential to ensuring food security. With declines in both managed and wild pollinator populations in recent years, scientists and regulators have sought answers to this problem and have explored implementing steps to protect pollinator populations now and for the future. Pesticide Risk Assessment for Pollinators focuses on the role pesticides play in impacting bee populations and looks to develop a risk assessment process, along with the data to inform that process, to better assess the potential risks that can accompany the use of pesticide products. Pesticide Risk Assessment for Pollinators opens with two chapters that provide a biological background of both Apis and non-Apis species of pollinators. Chapters then present an overview of the general regulatory risk assessment process and decision-making processes. The book then discusses the core elements of a risk assessment, including exposure estimation, laboratory testing, and field testing. The book concludes with chapters on statistical and modeling tools, and proposed additional research that may be useful in developing the ability to assess the impacts of pesticide use on pollinator populations. Summarizing the current state of the science surrounding risk assessment for Apis and non-Apis species, Pesticide Risk Assessment for Pollinators is a timely work that will be of great use to the environmental science and agricultural research communities. * Assesses pesticide risk to native and managed pollinators * Summarizes the state of the science in toxicity testing and risk assessment * Provides valuable biological overviews of both Apis and non-Apis pollinators * Develops a plausible overall risk assessment framework for regulatory decision making * Looks towards a globally harmonized approach for pollinator toxicity and risk assessment

Leseprobe

Other Titles from the Society of Environmental Toxicology and Chemistry (SETAC)

ESCORT3: Linking Non-Target Arthropod Testing and Risk Assessment with Protection Goals

Alix, Bakker, Barrett, Brμhl, Coulson, Hoy, Jansen, Jepson, Lewis, Neumann, Sμβenbach, van Vliet 2012

Ecotoxicology of Amphibians and Reptiles, 2nd ed.Sparling, Linder, Bishop, Krest 2010

Ecological Assessment of Selenium in the Aquatic EnvironmentChapman, Adams, Brooks, Delos, Luoma, Maher, Ohlendorf, Presser, Shaw 2010

Soil Quality Standards for Trace ElementsMerrington, Schoeters 2010

Semi-Field Methods for the Environmental Risk Assessment of Pesticides in SoilSchäffer, van den Brink, Heimbach, Hoy, de Jong, Römbke, Roβ-Nickoll, Sousa 2010

Mixture Toxicity: Linking Approaches from Ecological and Human Toxicologyvan Gestel, Jonker, Kammenga, Laskowski, Svendsen 2010

Application of Uncertainty Analysis to Ecological Risks of PesticidesWarren-Hicks, Hart 2010

Risk Assessment Tools: Software and User’s GuideMayer, Ellersieck, Asfaw 2009

Derivation and Use of Environmental Quality and Human Health Standards for Chemical Substances in Water and SoilCrane, Matthiessen, Maycock, Merrington, Whitehouse 2009

Linking Aquatic Exposure and Effects: Risk Assessment of PesticidesBrock, Alix, Brown, Capri, Gottesbμren, Heimbach, Lythgo, Schulz, Streloke 2009

Aquatic Macrophyte Risk Assessment for PesticidesMaltby, Arnold, Arts, Davies, Heimbach, Pickl, Poulsen 2009

Ecological Models for Regulatory Risk Assessments of Pesticides: Developing a Strategy for the FutureThorbek, Forbes, Heimbach, Hommen, Thulke, van den Brink, Wogram, Grimm 2009

Veterinary Medicines in the EnvironmentCrane, Boxall, Barrett 2008

Relevance of Ambient Water Quality Criteria for Ephemeral and Effluent-dependent Watercourses of the Arid Western United StatesGensemer, Meyerhof, Ramage, Curley 2008

Extrapolation Practice for Ecotoxicological Effect Characterization of ChemicalsSolomon, Brock, De Zwart, Dyer, Posthuma, Richards, Sanderson, Sibley, van den Brink 2008

Environmental Life Cycle CostingHunkeler, Lichtenvort, Rebitzer 2008

Pesticide Risk Assessment for Pollinators

Edited by

David Fischer

Environmental Safety Bayer CropScience LP Research Triangle Park, North Carolina, USA

Thomas Moriarty

Office of Pesticide Programs US Environmental Protection Agency Washington DC, USA

from the SETAC Pellston Workshop on Pesticide Risk Assessment for Pollinators

January 15-21, 2011 Pensacola, Florida, USA

Coordinating Editor of SETAC BooksLawrence Kapustka LK Consultancy Calgary, Alberta, Canada

This edition first published 2014 © 2014 by Society of Environmental Toxicology and Chemistry (SETAC).

Editorial offices: 1606 Golden Aspen Drive, Suites 103 and 104, Ames, Iowa 50010, USA The Atrium, Southern Gate, Chichester, West Sussex, PO19 8SQ, UK 9600 Garsington Road, Oxford, OX4 2DQ, UK

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Contributions to this book by Thomas Steeger and Thomas Moriarty were made as part of their duties for the US Environmental Protection Agency (USEPA). However, the publication of this book has not been formally reviewed by the USEPA and does not necessarily reflect the views of the USEPA.

Library of Congress Cataloging-in-Publication Data

Pesticide risk assessment for pollinators / edited by David Fischer, Thomas Moriarty.         pages cm     Includes bibliographical references and index.     ISBN 978-1-118-85252-1 (cloth)    1. Bees--Effect of pesticides on.    2. Honeybee--Effect of pesticides on.    3. Bees--Health.    4. Pesticides--Environmental aspects.    5. Pesticides and wildlife.    I. Fischer, David, 1955–    II. Moriarty, Thomas.     SF538.5.P65P47 2014     638′.159–dc23

2013046761

A catalogue record for this book is available from the British Library.

Wiley also publishes its books in a variety of electronic formats. Some content that appears in print may not be available in electronic books.

Cover image: Leafcutting bee on blanket flower, photograph by Mace Vaughan (Xerces Society for Invertebrate Conservation).

SETAC Publications

Books published by the Society of Environmental Toxicology and Chemistry (SETAC) provide in-depth reviews and critical appraisals on scientific subjects relevant to understanding the impacts of chemicals and technology on the environment. The books explore topics reviewed and recommended by the Publications Advisory Committee and approved by the SETAC North America, Latin America, Asia/Pacific, or Africa Board of Directors; the SETAC Europe Council; or the SETAC World Council for their importance, timeliness, and contribution to multidisciplinary approaches to solving environmental problems. The diversity and breadth of subjects covered in the series reflect the wide range of disciplines encompassed by environmental toxicology, environmental chemistry, hazard and risk assessment, and life cycle assessment. SETAC books attempt to present the reader with authoritative coverage of the literature, as well as paradigms, methodologies, and controversies; research needs; and new developments specific to the featured topics. The books are generally peer reviewed for SETAC by acknowledged experts.

SETAC publications, which include Technical Issue Papers (TIPs), workshop summaries, newsletter (SETAC Globe), and journals (Environmental Toxicology and Chemistry and Integrated Environmental Assessment and Management), are useful to environmental scientists in research, research management, chemical manufacturing and regulation, risk assessment, and education, as well as to students considering or preparing for careers in these areas. The publications provide information for keeping abreast of recent developments in familiar subject areas and for rapid introduction to principles and approaches in new subject areas.

SETAC recognizes and thanks the past coordinating editors of SETAC books:

Joseph W. Gorsuch, Copper Development Association, Inc. Webster, New York, USA

A.S. Green, International Zinc Association Durham, North Carolina, USA

C.G. Ingersoll, Columbia Environmental Research Center US Geological Survey, Columbia, Missouri, USA

T.W. La Point, Institute of Applied Sciences University of North Texas, Denton, Texas, USA

B.T. Walton, US Environmental Protection Agency Research Triangle Park, North Carolina, USA

C.H. Ward, Department of Environmental Sciences and Engineering Rice University, Houston, Texas, USA

This book is dedicated to the memory of Dr. Peter Delorme of Health Canada’s Pest Management Regulatory Agency. Dr. Delorme served as a member of the Steering Committee for the global SETAC Pellston Workshop on the Pesticide Risk Assessment for Pollinators, and is remembered for his contributions to this effort, and for his long service to protecting the environment.

Contents

Acknowledgments

About the Editors

Workshop Participants

Pellston Workshop Series

1 Introduction

1.1 Workshop Balance and Composition

Notes

2 Overview of the Honey Bee

2.1 Overview of Honey Bee Biology

3 Overview of Non-

Apis

Bees

3.1 Introduction

3.2 Non-

Apis

Bee Biology and Diversity

3.3 Opportunities for Non-

Apis

Bees to Inform Pollinator Risk Assessment

3.4 Conclusions

References

4 Overview of Protection Goals for Pollinators

4.1 Introduction

4.2 Elements and Proposed Protection Goals

4.3 Linking Protection Goals with Assessment Endpoints

4.4 Protection Goals and Monitoring

4.5 Conclusion

Reference

5 Overview of the Pesticide Risk Assessment and the Regulatory Process

5.1 Introduction

5.2 Current Approach for Assessing Effects of Pesticide Products to Pollinators

Notes

References

6 Problem Formulation for an Assessment of Risk to Honey Bees from Applications of Plant Protection Products to Agricultural Crops

6.1 What Is Problem Formulation?

6.2 Case 1: Problem Formulation for a Systemic Chemical Applied to the Soil, or as a Seed-Dressing

6.3 Case 2: Problem Formulation for a Contact Chemical Applied as a Foliar Spray

Notes

References

7 Assessing Exposure of Pesticides to Bees

7.1 Introduction

7.2 Potential Routes of Exposure for Non-

Apis

Bees

7.3 Methods and Models for Estimating Exposure of Bees to Pesticides

7.4 Physical and Chemical Properties of Pesticide Active Ingredients Which Affect Exposure

7.5 Information Needed to Develop Refined Predictive Exposure Models

7.6 Predicted Contact Exposure for Foliar-Applied Products

7.7 Predicted Dietary Exposure for Foliar-Applied Products

7.8 Predicted Exposure for Soil and Seed Treatment Systemic Compounds

7.9 Predicted Exposure for Tree-Injected Compounds

7.10 Measuring Pesticides in Matrices Relevant for Assessing Exposure to Bees

7.11 Higher Tier Studies to Assess Exposure of Pesticides to Bees

7.12 Health of Honey Bee Colonies Can Influence Exposure

7.13 Higher Tier Studies with Non-

Apis

Bee Species

7.14 Summary and Recommendations

Notes

References

8 Assessing Effects Through Laboratory Toxicity Testing

8.1 Introduction

8.2 Overview of Laboratory Testing Requirements Among Several Countries

8.3 Uncertainties in Current Testing Paradigms

8.4 Limitations and Suggested Improvements for Tier 1 Testing

8.5 Adult Oral Chronic Toxicity—

Apis

Bees

8.6 Honey Bee Brood Tests in the Laboratory

8.7 Adult Toxicity Testing with Non-

Apis

Bees

8.8 Sublethal Effects and Test Developments

8.9 Conclusions

References

9 Assessing Effects Through Semi-Field and Field Toxicity Testing

9.1 Introduction

9.2 Definition of Semi-Field and Field Studies

9.3 Design of a Semi-Field Study

9.4 Outline of a Semi-Field Study for

Apis

and Non-

Apis

Bees

9.5 Design of a Field Study

9.6 Outline of a Field Study for

Apis

and Non-

Apis

Species

9.7 Role of Monitoring and Incident Reporting

9.8 Summary

Notes

References

10 Overview of a Proposed Ecological Risk Assessment Process for Honey bees (

Apis mellifera

) and Non-

Apis

Bees

10.1 Introduction

10.2 Protection Goals, Assessment and Measurement Endpoints, Trigger Values for Transitioning to Higher Levels of Refinement, and Risk Assessment Terminology

10.3 Risk Assessment Flowcharts

10.4 Spray Applications

10.5 Soil and Seed Treatment Applications for Systemic Substances

10.6 Screening-Level Risk Assessments (Tier 1)

10.7 Factors Limiting Certainty in Screening Assessments

10.8 Refinement Options for Screening-Level Risk Assessment

10.9 Conclusions on the Risks and Recommendations

10.10 Recommending Risk Mitigation Measures

10.11 Additional Tools in Support of Risk Assessment and to Inform Risk Management

Notes

References

11 Ecological Modeling for Pesticide Risk Assessment for Honey Bees and Other Pollinators

11.1 Introduction

11.2 Example Model: Common Shrew

11.3 Rationale and Approaches of Mechanistic Effect Modeling

11.4 Modeling Practice for Risk Assessment

11.5 Existing Models of Pollinators

11.6 Discussion

References

12 Data Analysis Issues

12.1 Study Duration

12.2 Replicates and Dosing

12.3 Long-Term Tests

12.4 Statistical Models

13 Risk Mitigation and Performance Criteria

13.1 The Role of Risk Management in Pollinator Protection

13.2 Regulatory Risk Mitigation Methods

13.3 Non-Regulatory Risk Mitigation Methods

13.4 Suggested Techniques to Mitigate Risks to Other Species of Bees

13.5 Pesticide Application Technologies to Mitigate Exposure to Bees

Notes

References

14 Recommendations for Future Research in Pesticide Risk Assessment for Pollinators

14.1 Exposure

14.2 Effects

References

Appendix 1: Elements for a Chronic Adult Oral Toxicity Study

Appendix 2: Elements of a Larval Study

A2.1 Introduction: Importance of Larval Testing

A2.2 Proposed Elements for a Larval Study

A2.3 Larvae Termination and Collection

A2.4 Preparation of Rearing Material

A2.5 Preparation of the Pesticide Solutions

References

Appendix 3: Elements of Artificial Flower Test

Reference

Appendix 4: Elements of the Visual Learning Test

A4.1 Strengths and Weaknesses

References

Appendix 5: Foraging Behavior with Radio Frequency Identification

A5.1 Experimental Procedure

References

Appendix 6: Detailed Description of the Proposed Overall Risk Assessment Scheme

A6.1 Sprayed Treatments

A6.2 Soil or Seed Treatment With Systemic Active Substances

References

Glossary of Terms

Index

End User License Agreement

List of Tables

Chapter 3

TABLE 3.1

Potential Non-

Apis

Bee Species for Use in Laboratory, Semi-Field or Field Tests

a

Chapter 7

TABLE 7.1

Predicted Concentrations (in mg/kg) After Foliar Application of 1 kg/ha

TABLE 7.2

Comparison of Hazard Quotient (HQ), Toxicity/Exposure Ratios (TER) and Risk Quotients (RQ) Assuming a Predicted Contact Exposure Dose (PEDc) of 1.79 μg a.i./bee After an Application of 1 kg a.i./ha

TABLE 7.3

Day 0 Measured Concentrations of Three Foliar Applied Pesticides in Pollen and Nectar After Application to Flowering Mustard

TABLE 7.4

Day 0 Measured Concentrations of Two Foliar Applied Fungicides in Pollen and Nectar Collected from Honey Bees After Application to Flowering Oilseed Rape

TABLE 7.5

Day 1 Measured Concentrations of Chlorantraniliprole in Pollen and Nectar Collected from Honey Bees After Application to Flowering

Phacelia

Chapter 8

TABLE 8.1

Comparison of Acute Contact Test Guidelines (OECD 1998b and USEPA 2012a) and Acute Oral Test Guideline (OECD 1998a)

TABLE 8.2

Published Laboratory Tests with Non-

Apis

Bees and Associated Methodologies

TABLE 8.3

Larval Test Methods for Non-

Apis

Bee Species

Chapter 9

TABLE 9.1

Strengths and Weaknesses of Semi-Field Tests with

Apis Mellifera

TABLE 9.2

Strengths and Weaknesses of Semi-Field Tests with Non-

Apis

Bee Species

TABLE 9.3

Variability and Uncertainty in Semi-Field Studies with

Apis Mellifera

TABLE 9.4

Strengths and Weaknesses of Field Studies for Both

Apis

and Non-

Apis

Bee Species

TABLE 9.5

Variability and Uncertainty in Field Studies with

Apis

and Non-

Apis

Bee Species

Chapter 10

TABLE 10.1

Linkage of Protection Goals, Assessment Endpoints, and Measurement Endpoints for Social Bees (Including

Apis

) and Solitary (Non-

Apis

) Bees. Initials (L) and (F) Designate Endpoints Most Applicable to Laboratory (L) Studies and Field (F)

TABLE 10.2

Risk Estimates and Their Components Used by Regulatory Authorities

TABLE 10.3

Likelihood of Exposure to

Apis

and Non-

Apis

Bees from Various Routes

TABLE 10.4

Testing Methodologies Developed for the Risk Assessment to Non-Target Arthropods Developed in the European Process of Evaluation of Pesticides

TABLE 10.5

Available Laboratory and Field Tests with Representative Groups of Solitary and Social Non-

Apis

Bees

Chapter 11

TABLE 11.1

Colony Models That Include the Full Life Cycle of Worker Bees and Run Long Enough, that is, Two or More Years, to Assess Status and Survival of a Model Colony. The Third Column Lists Additional Factors Included in the Model That Can Affect Colony Status and Survival

Appendix 6

TABLE A6.1

Likelihood of Exposure to

Apis

and Non-

Apis

Bees from Various Routes

List of Illustrations

Chapter 4

FIGURE 4.1

Relationship between measurement endpoints to generic protection goals, used in assessing ecological risks.

FIGURE 4.2

Post-registration monitoring studies in a risk assessment framework.

Chapter 6

FIGURE 6.1

Scheme depicting problem formulation phase of the ecological risk assessment process. (Taken from USEPA 1998).

FIGURE 6.2

Depiction of stressor source, potential routes of exposure, receptors and attribute changes for a systemic pesticide applied to the soil or as a seed dressing.

FIGURE 6.3

Depiction of stressor source, potential routes of exposure, receptors and attribute changes for a nonsystemic pesticide applied as a foliar spray.

Chapter 7

FIGURE 7.1

Conceptual model showing how contaminants may potentially reach various matrices within honey bee colonies. Pollen and nectar are the main sources of in-hive contamination. Arrows show potential major contamination transfer routes. For minor routes, please refer to the text.

FIGURE 7.2

Leafcutter bee on blanket flower, photo by Mace Vaughan (Xerces Society for Invertebrate Conservation).

FIGURE 7.3

Micropipetting nectar samples, photo by Mike Beevers.

FIGURE 7.4

Hand collecting pollen by removing flower anthers, photo by Mike Beevers.

FIGURE 7.5

Honey bee semi-field study with

Phacelia

, photo provided by BASF SE.

FIGURE 7.6

Mason bee, photo by Mace Vaughan (Xerces Society for Invertebrate Conservation).

Chapter 8

FIGURE 8.1

Comparison of the contact toxicity (LD50) of 21 pesticides to adults of

Apis mellifera,

three species of the social bee Bombus and three species of solitary bees (Osmia, Megachilidae, and Nomia). Points below the diagonal line indicate greater sensitivity than

Apis mellifera

, while points above the diagonal line represent lower sensitivity than

Apis mellifera

(Johansen et al. 1983).

FIGURE 8.2

Comparison of the toxicity of pesticides to adults of

Apis mellifera

with the solitary bees

Megachile rotundata

and

Nomia melanderi

based on time for sprayed residues to decline to a concentration causing 25% or less mortality. Points below the diagonal line indicate greater sensitivity than

Apis mellifera

, while points above the diagonal line represent lower sensitivity than

A. mellifera

(Johansen et al. 1983).

FIGURE 8.3

Comparison of the toxicity (LD50) of sprayed residues of clothianidin, imidacloprid, lambda-cyhalothrin and spinosad to adults of

Apis mellifera, Megachile rotundata

, and

Osmia lignaria

. Points below the diagonal line indicate greater sensitivity than

A. mellifera

, while points above the diagonal line represent lower sensitivity than

A. mellifera

(Johansen et al. 1983).

FIGURE 8.4

Maze paths used before, during, and after treatment. Path 1 was used for the conditioning procedure and other paths were used for the retrieval tests. Each path started with the entrance (E), contained three decision boxes, six no-decision boxes, and finished with the reward box (R).

Chapter 10

FIGURE 10.1

Diagram of ecological risk assessment process employed by USEPA.

FIGURE 10.2

Insect pollinator screening-level risk assessment process for foliarly applied pesticides.

FIGURE 10.3

Higher tier (refined) risk assessment process for foliarly applied pesticides.

FIGURE 10.4

Insect pollinator screening-level risk assessment process for soil and seed treatment of systemic pesticides. Note that this flow chart may apply for trunk injection as well, as modalities of exposure of pollinators are similar as for soil or seed treatments. For trunk injection, however, further data are needed to appropriately describe the range of expected residue concentrations in nectar and pollen. As a consequence, no default value is currently available for a quantification of the risk (Boxes 3a and 3b). A compilation of available data could be made, with a particular attention to the corresponding injection protocols as it varies with the active substance involved and the tree.

FIGURE 10.5

Higher tier (refined) risk assessment process for soil and seed treatment applied systemic pesticides.

Chapter 11

FIGURE 11.1

Output of an individual-based model of the common shrew (Wang and Grimm 2007) on a certain day of the simulation. Black lines delineate home ranges of males, gray lines of females. Home ranges in cereal fields need to be larger than in grassland or hedges because of lower resource levels. Home ranges are drawn as minimum convex polygons by connecting the outmost cells occupied by their owners (from Wang and Grimm 2007).

FIGURE 11.2

Population dynamics in orchards with and without 20% hedges with a yearly application of 20% additional mortality on April 1 (from Wang and Grimm 2010).

FIGURE 11.3

Tasks of the “Modeling Cycle,” that is, of the iterative process of formulating, implementing, testing, and analyzing ecological models (after Schmolke et al. 2010b). Full cycles usually include a large number of subcycles, for example, verification leading to further effort for parameterization or reformulation of the model. The elements of this cycle are used to structure a new standard format for documenting model development, testing, analysis, and application for environmental decision making, TRACE (Schmolke et al. 2010b).

FIGURE 11.4

Conceptual diagram of the colony model of Martin (2001). Solid lines represent the flow of individuals between developmental stages and dotted lines represent influences (from Martin 2001).

Chapter 14

FIGURE 14.1

Guttation water on a strawberry leaf, photo by Mace Vaughan (Xerces Society for Invertebrate Conservation).

Appendix 4

FIGURE A4.1

Maze paths used before, during, and after treatment. Path 1 was used for the conditioning procedure and other paths were used for the retrieval tests. Each path started with the entrance (E), contained three decision boxes, six no-decision boxes, and finished with the reward box (R).

Appendix 6

FIGURE A6.1

Insect pollinator screening-level risk assessment process for foliarly applied pesticides.

FIGURE A6.2

Higher tier (refined) risk assessment process for foliarly applied pesticides.

Guide

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Acknowledgments

We gratefully acknowledge the financial support for the workshop from the following organizations:

BASF Corporation Bayer CropScience Chemicals Regulation Directorate to the Health and Safety Executive Dow AgroSciences International Commission For Plant Bee Relationships Julius Kuhn Institut Monsanto Company Pennsylvania State University Pollinator Partnership Project Apis m. Syngenta US Department of Agriculture US Environmental Protection Agency Valent U.S.A Corporation

About the Editors

Thomas Moriarty serves as a Risk Manager and Chemical Team Leader in the US Environmental Protection Agency, Office of Pesticide Programs (OPP), Pesticide Re-evaluation Division, and serves as the Chair of the USEPA Pollinator Protection Team. He has also worked as a Risk Assessor in the Human Health Effects Division of OPP, and served on the technical team that developed the USEPA Risk Assessment Framework for Bees that was presented to a Federal Insecticide, Fungicide, and Rodenticide Act (FIFRA) Scientific Advisory Panel in September 2013. He co-chairs the Risk Management workgroup of the Pesticide Effects on Insect Pollinators subgroup for the Organisation for Economic Co-operation and Development (OECD) Working Group on Pesticides, and was a member of the Steering Committee for the SETAC Pellston Workshop on Pollinator Risk Assessment. Tom has an MS in Public Policy from the University of Maryland and a BS in Political Science from Providence College.

David Fischer is Director and Head of the Environmental Toxico-logy and Risk Assessment group within the Development North America Department of Bayer CropScience LP. Fischer holds a BS degree in Zoology from the University of Massachusetts, an MS degree in Zoology from Western Illinois University, and a PhD in Zoology from Brigham Young University. His MS and PhD research projects were on the ecology of Bald Eagles and Accipiter Hawks. He has been working in the field of ecotoxicology and risk assessment since 1986, the last 26 years with Bayer CropScience and Legacy companies. Fischer has supervised the conduct of hundreds of laboratory and field toxicology studies of crop protection chemicals and animal pharmaceuticals, authored dozens of chemical risk assessments, and published more than 20 peer-reviewed scientific papers. His expertise is in the area of terrestrial ecotoxicology and risk assessment. A member of SETAC since 1988, he helped organize previous Pellston Workshops on Wildlife Radiotelemetry Applications for Wildlife Toxicology Field Studies and Application of Uncertainty Analysis to Ecological Risks of Pesticides. For the past decade or so, Fischer's research interests have focused on improving the testing and risk assessment process for honey bees and other pollinators.

Workshop Participants

Steering Committee

Dave Fischer, Bayer CropScience, USA

Tom Moriarty, US Environmental Protection Agency

Anne Alix, Ministry of Agriculture, Food, Fisheries, Rural Affairs and Spatial Planning, France

Mike Coulson, Syngenta Ltd., UK

Peter Delorme, Health Canada, Pest Management Regulatory Agency, Canada

Jim Frazier, Pennsylvania State University, USA

Christopher Lee-Steere, Australian Environment Agency Pty Ltd., Australia

Jeff Pettis, US Department of Agriculture

Jochen Pflugfelder, Swiss Bee Research Center, Switzerland

Thomas Steeger, US Environmental Protection Agency

Franz Streissl, European Food Safety Authority

Mace Vaughan, Xerces Society for Invertebrate Conservation, USA

Joseph Wisk, BASF Corporation, Crop Solutions, USA

Exposure Workgroup

Jens Pistorius, co-chair, Julius Kühn-Institut, Institute for Plant Protection in Field Crops and Grassland, Germany

Joseph Wisk, co-chair, BASF Corporation, Crop Solutions, USA

Mike Beevers, California Agricultural Research, Inc., USA

Richard Bireley, California Department of Pesticide Regulation, USA

Zac Browning, Browning's Honey Company, Inc., USA

Marie-Pierre Chauzat, French Agency for Food, Environmental and Occupational Health Safety, Sophia Antipolis, France

Alexander Nikolakis, Bayer CropScience AG, Development—Environmental Safety—Ecotoxicology— Bees, Germany

Jay Overmyer, Syngenta Crop Protection, LLC, USA

Robyn Rose, US Department of Agriculture Animal and Plant Health Inspection Service

Robert Sebastien, Health Canada, Pest Management Regulatory Agency, Canada

Bernard Vaissière, French National Institute for Agricultural Research, France

Mace Vaughan, Xerces Society for Invertebrate Conservation, USA

Hazard, Laboratory Workgroup

Jim Frazier, co-chair, Pennsylvania State University, USA

Jochen Pflugfelder, co-chair, Swiss Bee Research Center, Switzerland

Pierrick Aupinel, INRA, Centre Poitou-Charentes, UE d'entomologie, France

Pamela Bachman, Monsanto Company, USA

Axel Decourtye, ACTA, UMT PrADE, Germany

Axel Dinter, DuPont de Nemours (Deutschland) GmbH, Germany

Jamie Ellis, Honey Bee Research and Extension Laboratory, University of Florida, USA

Volker Grimm, Helmholtz Center for Environmental Research—UFZ, Leipzig, Germany

Zachary Huang, Michigan State University, USA

Roberta C.F. Nocelli, Center for Agricultural Science—UFSCar—Araras—SP, Brazil

Helen Thompson, Food and Environment Research Agency, UK

William Warren-Hicks, EcoStat, Inc., USA

Hazard, Semi-field and Field Workgroup

Ingo Tornier, co-chair, Eurofins Agroscience, Germany

Jeff Pettis, co-chair, US Department of Agriculture

Roland Becker, BASF Aktiengesellschaft, Germany

Mark Clook, Chemicals Regulation Directorate, Health and Safety Executive, UK

Mike Coulson, Syngenta Ltd., UK

Wayne Hou, Health Canada, Pest Management Regulatory Agency, Canada

Pascal Jourdan, ITSAP—Institut de l'abeille, France

Muo Kasina, Kenya Agricultural Research Institute, Kenya

Glynn Maynard, Office of the Chief Plant Protection Officer, Department of Agriculture, Fisheries and Forestry, Australia

Dick Rogers, Bayer CropScience, USA

Cynthia Scott-Dupree, School of Environmental Sciences, University of Guelph, Canada

Teodoro Stadler, Laboratorio de Toxicologia Ambiental, Instituto de Medicina y Biologia Experimental de Cuyo (IMBECU), Centro Cientifico Teconlogico CONICET, Argentina

Klaus Wallner, University of Hohenheim, Apiculture Institute, Germany

Bernard Vaissière, French National Institute for Agricultural Research, France

Risk Assessment Workgroup

Anne Alix, co-chair, Ministry of Agriculture, Food, Fisheries, Rural Affairs and Spatial Planning, France

Thomas Steeger, co-chair, US Environmental Protection Agency

Claire Brittain, Leuphana University of Lüneburg, Germany

Dave Fischer, Bayer CropScience, USA

Rolf Fischer, Federal Office of Consumer Protection and Food Safety, Germany

Michael Fry, American Bird Conservancy, USA

Erik Johansen, Washington State Department of Agriculture, USA

Reed Johnson, University of Nebraska—Lincoln, USA

Christopher Lee-Steere, Australian Environment Agency Party Ltd., Australia

Mark Miles, Dow AgroSciences, UK

Tom Moriarty, US Environmental Protection Agency

Franz Streissl, European Food Safety Authority

Non-Apis Workgroup

Mike Coulson, co-chair, Syngenta Ltd., UK

Mace Vaughan, co-chair, Xerces Society for Invertebrate Conservation, USA

Claire Brittain, Leuphana University of Lüneburg, Germany

Axel Dinter, DuPont de Nemours (Deutschland) GmbH, Germany

Erik Johansen, Washington State Department of Agriculture, USA

Muo Kasina, Kenya Agricultural Research Institute, Kenya

Glynn Maynard, Office of the Chief Plant Protection Officer, Department of Agriculture, Fisheries, and Forestry, Australia

Roberta C.F. Nocelli, Center for Agricultural Science—UFSCar—Araras—SP, Brazil

Cynthia Scott-Dupree, School of Environmental Sciences, University of Guelph, Canada

Helen Thompson, Food and Environment Research Agency, UK

Bernard Vaissière, French National Institute for Agricultural Research, France

Pellston Workshop Series

The workshop from which this book resulted, Potential Risks of Plant Protection Products to Pollinators, held in Pensacola Beach, Florida, USA, January 16–22, 2011, was part of the successful SETAC Pellston Workshop Series. Since 1977, Pellston Workshops have brought scientists together to evaluate current and prospective environmental issues. Each workshop has focused on a relevant environmental topic, and the proceedings of each have been published as peer-reviewed or informal reports. These documents have been widely distributed and are valued by environmental scientists, engineers, regulators, and managers for their technical basis and their comprehensive, state-of-the-science reviews. The workshops in the Pellston series are as follows:

Estimating the Hazard of Chemical Substances to Aquatic Life. Pellston, Michigan, June 13–17, 1977. Published by the American Society for Testing and Materials, STP 657, 1978.

Analyzing the Hazard Evaluation Process. Waterville Valley, New Hampshire, August 14–18, 1978. Published by the American Fisheries Society, 1979.

Biotransformation and Fate of Chemicals in the Aquatic Environment. Pellston, Michigan, August 14–18, 1979. Published by the American Society of Microbiology, 1980.

Modeling the Fate of Chemicals in the Aquatic Environment. Pellston, Michigan, August 16–21, 1981. Published by Ann Arbor Science, 1982.

Environmental Hazard Assessment of Effluents. Cody, Wyoming, August 23–27, 1982. Published as a SETAC Special Publication by Pergamon Press, 1985.

Fate and Effects of Sediment-Bound in Aquatic Systems. Florissant, Colorado, August 11–18, 1984. Published as a SETAC Special Publication by Pergamon Press, 1987.

Research Priorities in Environmental Risk Assessment. Breckenridge, Colorado, August 16–21, 1987. Published by SETAC, 1987.

Biomarkers: Biochemical, Physiological, and Histological Markers of Anthropogenic Stress. Keystone, Colorado, July 23–28, 1989. Published as a SETAC Special Publication by Lewis Publishers, 1992.

Population Ecology and Wildlife Toxicology of Agricultural Pesticide Use: A Modeling Initiative for Avian Species. Kiawah Island, South Carolina, July 22–27, 1990. Published as a SETAC Special Publication by Lewis Publishers, 1994.

A Technical Framework for [Product] Life-Cycle Assessments. Smuggler's Notch, Vermont, August 18–23, 1990. Published by SETAC, January 1991; 2nd printing September 1991; 3rd printing March 1994.

Aquatic Microcosms for Ecological Assessment of Pesticides. Wintergreen, Virginia, October 7–11, 1991. Published by SETAC, 1992.

A Conceptual Framework for Life-Cycle Assessment Impact Assessment. Sandestin, Florida, February 1–6, 1992. Published by SETAC, 1993.

A Mechanistic Understanding of Bioavailability: Physical–Chemical Interactions. Pellston, Michigan, August 17–22, 1992. Published as a SETAC Special Publication by Lewis Publishers, 1994.

Life-Cycle Assessment Data Quality Workshop. Wintergreen, Virginia, October 4–9, 1992. Published by SETAC, 1994.

Avian Radio Telemetry in Support of Pesticide Field Studies. Pacific Grove, California, January 5–8, 1993. Published by SETAC, 1998.

Sustainability-Based Environmental Management. Pellston, Michigan, August 25–31, 1993. Co-sponsored by the Ecological Society of America. Published by SETAC, 1998.

Ecotoxicological Risk Assessment for Chlorinated Organic Chemicals. Alliston, Ontario, Canada, July 25–29, 1994. Published by SETAC, 1998.

Application of Life-Cycle Assessment to Public Policy. Wintergreen, Virginia, August 14–19, 1994. Published by SETAC, 1997.

Ecological Risk Assessment Decision Support System. Pellston, Michigan, August 23–28, 1994. Published by SETAC, 1998.

Avian Toxicity Testing. Pensacola, Florida, December 4–7, 1994. Co-sponsored and published by Organisation for Economic Co-operation and Development (OECD), 1996.

Chemical Ranking and Scoring (CRS): Guidelines for Developing and Implementing Tools for Relative Chemical Assessments. Sandestin, Florida, February 12–16, 1995. Published by SETAC, 1997.

Ecological Risk Assessment of Contaminated Sediments. Pacific Grove, California, April 23–28, 1995. Published by SETAC, 1997.

Ecotoxicology and Risk Assessment for Wetlands. Fairmont, Montana, 30 July–3 August 1995. Published by SETAC, 1999.

Uncertainty in Ecological Risk Assessment. Pellston, Michigan, August 23–28, 1995. Published by SETAC, 1998.

Whole-Effluent Toxicity Testing: An Evaluation of Methods and Prediction of Receiving System Impacts. Pellston, Michigan, September 16–21, 1995. Published by SETAC, 1996.

Reproductive and Developmental Effects of Contaminants in Oviparous Vertebrates. Fairmont, Montana, July 13–18, 1997. Published by SETAC, 1999.

Multiple Stressors in Ecological Risk Assessment. Pellston, Michigan, September 13–18, 1997. Published by SETAC, 1999.

Re-evaluation of the State of the Science for Water Quality Criteria Development. Fairmont, Montana, June 25–30, 1998. Published by SETAC, 2003.

Criteria for Persistence and Long-Range Transport of Chemicals in the Environment. Fairmont Hot Springs, British Columbia, Canada, July 14–19, 1998. Published by SETAC, 2000.

Assessing Contaminated Soils: From Soil-Contaminant Interactions to Ecosystem Management. Pellston, Michigan, September 23–27, 1998. Published by SETAC, 2003.

Endocrine Disruption in Invertebrates: Endocrinology, Testing, and Assessment (EDIETA). Amsterdam, The Netherlands, December 12–15, 1998. Published by SETAC, 1999.

Assessing the Effects of Complex Stressors in Ecosystems. Pellston, Michigan, September 11–16, 1999. Published by SETAC, 2001.

Environmental–Human Health Interconnections. Snowbird, Utah, June 10–15, 2000. Published by SETAC, 2002.

Ecological Assessment of Aquatic Resources: Application, Implementation, and Communication. Pellston, Michigan, September 16–21, 2000. Published by SETAC, 2004.

Toxicity Identification Evaluation/Toxicity Reduction Evaluation: What Works and What Doesn't. Pensacola, Florida, June 23–27, 2001. Proceedings published by SETAC in 2005.

The Global Decline of Amphibian Populations: An Integrated Analysis of Multiple Stressors Effects. Wingspread, Racine, Wisconsin, August 18–23, 2001. Published by SETAC, 2003.

Methods of Uncertainty Analysis for Pesticide Risks. Pensacola, Florida, 24 February–1 March 2002.

The Role of Dietary Exposure in the Evaluation of Risk of Metals to Aquatic Organisms. Fairmont Hot Springs, British Columbia, Canada, 27 July–1 August 2002. Published by SETAC, 2005.

Use of Sediment Quality Guidelines (SQGs) and Related Tools for the Assessment of Contaminated Sediments. Fairmont Hot Springs, Montana, August 17–22, 2002. Published by SETAC, 2005.

Science for Assessment of the Impacts of Human Pharmaceuticals on Aquatic Ecosystem. Snowbird, Utah, June 3–8, 2003. Published by SETAC, 2005.

Population-Level Ecological Risk Assessment. Roskilde, Denmark, August 23–27, 2003. Published by SETAC and CRC Press, 2007.

Valuation of Ecological Resources: Integration of Ecological Risk Assessment and Socio-Economics to Support Environmental Decisions. Pensacola, Florida, October 4–9, 2003. Published by SETAC and CRC Press, 2007.

Emerging Molecular and Computational Approaches for Cross-Species Extrapolations. Portland, Oregon, July 18–22, 2004. Published by SETAC and CRC Press, 2006.

Veterinary Medicines in the Environment. Pensacola, Florida, February 12–16, 2006. Published by SETAC and CRC Press, 2008.

Tissue Residue Approach for Toxicity Assessment: Invertebrates and Fish. Leavenworth, Washington, June 7–10, 2007. Published in SETAC Journal

Integrated Environmental Assessment and Management

(IEAM), 2011.

Science-Based Guidance and Framework for the Evaluation and Identification of PBTs and POPs. Pensacola Beach, Florida, 27 January–1 February 2008.

The Nexus between Ecological Risk Assessment (ERA) and Natural Resource Damage Assessment (NRDA). Fairmont, Montana, January 28–31, 2008. Published in SETAC Journal

Integrated Environmental Assessment and Management

(IEAM), 2009.

Ecological Assessment of Selenium in the Aquatic Environment. Pensacola Beach, Florida, February 22–27, 2009. Published by SETAC and CRC Press, 2010.

A Vision and Strategy for Predictive Ecotoxicology in the 21st Century: Defining Adverse Outcome Pathways Associated with Ecological Risk. Forest Grove, Oregon, April 19–23, 2009. Published in SETAC Journal

Environmental Toxicology and Chemistry

(ET&C), 2011.

Problem Formulation for Ecological Risk Assessments. Pensacola Beach, Florida, April 18–24, 2010.

Potential Risks of Plant Protection Products to Pollinators. Pensacola Beach, Florida, January 16–22, 2011.

Life Cycle Assessment Database Global Guidance. Kanagawa, Japan, 30 January–4 February 2011. Published by the UNEP/SETAC Life Cycle Initiative, 2011.

Influence of Global Climate Change on the Scientific Foundation and Application of Environmental Toxicology and Chemistry. Racine, Wisconsin, July 16–21, 2011. Published in ET&C, 2012.

Guidance on Bioavailability/Bioaccessibility Measurements Using Passive Sampling Devices and Partitioning-Based Approaches for Management of Contaminated Sediments. Costa Mesa, California, November 7–9, 2012. To be published in ET&C and IEAM, 2013.

1Introduction

CONTENTS

1.1 Workshop Balance and Composition

Worldwide declines in managed and non-managed pollinators have led to an increased global dialogue and focus concerning the potential factors that may be causing these declines. Although a number of factors have been hypothesized as potential contributors to pollinator declines, at this time, no single factor has been identified as the cause. The available science suggests that pollinator declines are a result of multiple factors which may be acting in various combinations. Research is being directed at identifying the individual and combined stressors that are most strongly associated with pollinator declines. Pesticide use is one of the factors under consideration.

In an effort to further the global dialogue, the Society of Environmental Toxicology and Chemistry (SETAC) held a Pellston Workshop1 to explore the state of the science on pesticide risk assessment for pollinators. The proposal for this SETAC Workshop was developed by a steering committee (hereafter referred to as the Steering Committee) comprised of members from the government and nongovernmental organizations who were interested in advancing the science to understand the effect of pesticides on nontarget insects. Workshop participants were tasked to advance the current state of the science of pesticide risk assessment by more thoroughly vetting quantitative and qualitative measures of exposure and effects on the individual bee, and where appropriate, on the colony. In doing so, the Workshop aimed to synthesize the global understanding and work that has, thus far, taken place, and to move toward a harmonized process for evaluating and quantitatively characterizing risk to pollinators from exposure to pesticides; and to identify the data needed to inform that process. The Workshop focused on four major topics:

design and identify testing protocols to estimate potential exposure of bees to pesticide residues in pollen and nectar, as well as exposure through other routes;

design and identify testing protocols to measure the effects of pesticides on developing brood and adult honey bees at both the individual and the colony levels;

propose a tiered approach for characterizing the potential risk of pesticides to pollinators; and

explore the applicability of testing protocols, used for honey bees (

Apis

bees), to measure the effects of pesticides and pesticide risk to other non-

Apis

bee species.

Although the term “pollinators” encompasses a broad number of taxa, for the purposes of this SETAC Workshop and its proceedings, the term “pollinators” refers specifically to subspecies and strains of Apis mellifera that originated in Europe (i.e., the honey bee) and other (non-Apis mellifera) bees, for example, bumble bees, solitary bees, and stingless bees. The Workshop built upon the numerous efforts of different organizations, regulatory authorities, and individuals, both nationally and internationally, aiming to better understand the role and effects of pesticide products on honey bees2 and other bee species.

1.1 WORKSHOP BALANCE AND COMPOSITION

Similar to other timely and relevant scientific issues addressed by SETAC Pellston Workshops, the issue of pollinator protection is of high interest to scientists employed by governments, business, academia, and nongovernmental organizations. For this reason, SETAC requires that its workshops be similarly balanced. The Workshop on Pesticide Risk Assessment for Pollinators represented an exceptionally diverse composition by both sector (employer) and geography. The 48 participants (35 panelists and 13 Steering Committee members) included individuals from industry, nongovernmental organizations, federal and state governments, the beekeeping community, and academia and represented five continents (South America, Europe, Australia, North America, and Africa) (see Acknowledgments).

This proceeding of the Workshop on Pesticide Risk Assessment for Pollinators has several sections:

Chapters 2–6 provide background and overview of key elements such as bee biology, ecological risk assessment, and protection goals.

Chapters 7–10 capture recommendations by the Workshop on the elements of exposure assessment, effects assessment (laboratory and field testing), and risk assessment.

Chapters 11–14 capture discussion around statistical analysis, modeling, risk management, and research needs.

Pollinators, and the honey bee in particular, have been identified as a valued group of organisms because of the services they provide to agriculture and to ecosystem biodiversity. While both managed and unmanaged (Apis and non-Apis) bees contribute to crop pollination, most of the current knowledge of the side effects of agricultural pesticides on pollinators is in relation to the honey bee. Since it is not possible to test all species, regulatory authorities rely on one or several surrogate species to represent a wider range of species within a taxon. Unlike the North American process that uses the honey bee as a surrogate for other terrestrial invertebrates, the European process includes testing requirements for honey bees specifically (representing pollinating insects), and includes other surrogate test species for nontarget arthropods in general. The proposed process discussed herein relies mainly on the honey bee, but includes other species, such as bumble bees, for example, to represent the many different species of bees. Therefore, it is important to understand the ecology and biology of the Apis bee as a test organism, as well as that of non-Apis bees.

NOTES

1

The first Pellston Workshop was held in 1977 to address the needs and means for assessing the hazards of chemicals to aquatic life. Since then, many workshops have been held to evaluate current and prospective environmental issues. Each has focused on a relevant environmental topic, and the proceedings of each have been published as a peer-reviewed or informal report. These documents have been widely distributed and are valued by environmental scientists, engineers, regulators, and managers because of their technical basis and their comprehensive, state-of-the-science reviews. The first four Pellston workshops were initiated before the Society of Environmental Toxicology and Chemistry (SETAC) was effectively functioning. Beginning with the 1982 workshop, however, SETAC has been the primary organizer and SETAC members (on a volunteer basis) have been instrumental in planning, conducting, and disseminating workshop results. Taken from

http://www.setac.org/node/104

2

USDA Technical Working Group Report on Honey Bee Toxicity Testing, July 8 and 9, 2009,

http://www.aphis.usda.gov/plant_health/plant_pest_info/honey_bees/downloads/twg_report_july_2010.pdf

; International Commission for Plant–Bee Relationships 10th International Symposium, 2009,

http://www.uoguelph.ca/icpbr/pubs/2008%20ICPBR%20symposium%20archives%20Pesticides.pdf

2Overview of the Honey Bee

J. Pettis

CONTENTS

2.1 Overview of Honey Bee Biology

A key goal of regulatory authorities charged with licensing the use of pesticide products is to protect nontarget organisms from the potential adverse effects from those pesticide products. As it is not possible to test all species, the pesticide risk assessment framework relies on surrogate species to represent major taxa, including insect pollinators. The European honey bee (Apis mellifera), among the many different bee species, is a desirable surrogate test species in that it is both commercially valued and is also adaptable to laboratory research. In many countries, such as Canada and the United States, the honey bee is used as a surrogate for insect pollinators and many other nontarget terrestrial insects. While honey bees may be subject to collateral effects from the use of pesticides in crop production, they are also the beneficiaries of pesticide applications, as beekeepers routinely employ registered pesticides to manage pest problems that occur in managed hives. The in-hive use of pesticides by beekeepers and the potential exposure of honey bees to environmental mixtures of pesticides used in agriculture coupled with the complex social organization and biology of honey bees can complicate pesticide risk assessment. While these are major challenges facing risk assessment, their resolution will require additional research efforts and so they are beyond the scope of this document and are not addressed further herein (see Chapter 14).

2.1 OVERVIEW OF HONEY BEE BIOLOGY

From a risk assessment perspective, there are several aspects of honey bee biology which are important to consider as they potentially influence the toxicity studies required as well as the approach for evaluating potential risks. Colony growth and survival are dependent on the collective actions of individuals that perform various critical tasks; therefore, honey bee colonies act collectively as a “superorganism.” The different castes of bees within the hive structure have different functions which can result in differential exposure in terms of route, duration, magnitude, and mode (direct vs. indirect, secondary exposure). The survival of an individual bee may be of little consequence as colonies typically have a 10–30% reserve of workers, which reflects and accommodates the high turnover rate (of the individual) and flexibility of the colony to adapt to its environment. An examination of the roles of various castes within the hive and the implication for risk assessments follows.

A honey bee colony is made up of one queen, several drones, thousands of workers, and many immature bees in various stages of development (eggs, larvae, pupae). Worker bees are sexually undeveloped females and constitute the vast majority of the adults in a colony. All work, inside and outside the colony, is done by worker bees. Older workers forage outside the hive for pollen and nectar and thus are potentially more exposed to pesticides via contact during foraging (e.g., by direct overspray or by contact with pesticide residues on treated plant surfaces), as well as dietary exposure during collection or ingestion of pollen and nectar. Workers also are a medium by which environmental contaminants come back to the hive. Young workers clean cells and attend brood whereas middle-aged workers do a variety of tasks mainly within the hive. Both young and middle-aged workers can be exposed to pesticides through contaminated food brought back to the hive. Each colony has a single queen. Once she mates with drones, the queen returns to the hive to begin the task of egg laying; she will lay up to 1200 eggs per day for several years. The queen performs no other work in the hive and continues to be fed royal jelly throughout her lifespan. Drones are male bees whose sole function in the hive is to serve as sperm donors for new queens. Like younger and middle-aged workers, queens and drones can also be exposed to pesticides through contaminated food brought back to the hive or intentionally used in the colony by beekeepers.

Inputs by worker bees into the colony include pollen, nectar, water, and plant exudates (e.g., sap) used to make propolis. Pollen is used as the source of protein. It may be consumed directly, consumed and used to produce brood food or royal jelly, or stored and consumed later as bee bread. While larval bees may consume small quantities of raw pollen directly, they as well as the queen depend on processed secretions (brood food and royal jelly) produced by nurse bees. Availability and the quality of pollen can have a great influence on the health status of the colony. Nectar is used as a source of carbohydrates, it may be consumed directly or stored inside the hive converted to honey and consumed later.

From a risk assessment perspective, the large forage area of honey bees complicates the task of estimating potential exposure. Honey bees typically forage in the middle of the day for food within 2–3 km (1–2 mi) of the hive, but may forage 7 km (5 mi) or more if food of suitable quality is lacking nearby. The large forage range increases the potential that the pollen and nectar collected by the honey bee may contain pesticide residues used in the foraging vicinity. The time of day when foraging occurs in relation to pesticide application may also influence exposure and therefore the risk assessment. As will be discussed in the following chapters, numerous other factors should be considered in light of bee biology that can impact the design or interpretation of data intended to inform pesticide risk assessment with these organisms.

3Overview of Non-Apis Bees

M. Vaughan, B.E. Vaissière, G. Maynard, M. Kasina, R.C.F. Nocelli, C. Scott-Dupree, E. Johansen, C. Brittain, M. Coulson, and A. Dinter

CONTENTS

3.1 Introduction

3.2 Non-

Apis

Bee Biology and Diversity

3.2.1 Generalist and Specialist Foragers

3.2.2 Social and Solitary Behavior

3.2.2.1 Social Bees

3.2.2.2 Social, Stingless Bees

3.2.2.3 Solitary Bees

3.2.3 Status of Toxicity Testing for Non-

Apis

Bees

3.3 Opportunities for Non-

Apis

Bees to Inform Pollinator Risk Assessment

3.4 Conclusions

References

3.1 INTRODUCTION

Honey bees (Apis mellifera L.) are frequently employed in pesticide toxicity testing either as a representative species (i.e., surrogate) for pollinating insects (such as in the European Union (EU)) or in other cases to represent other non-target terrestrial invertebrates (such as in North America). As with many surrogate test organisms, there are considerations or limitations to using A. mellifera as a representative species for pollinators and terrestrial invertebrates in general. For example, field tests with honey bees can be challenging because of their very long foraging range, the variability of their foraging area and the forage resources they utilize (Visscher and Seeley 1982). In semi-field tests, honey bees do not respond well to being kept in cages or indoor environments for a long period.

Uncertainties also exist regarding the extent to which pesticide toxicity data for honey bees can be considered protective for non-Apis bees. Studies have demonstrated variable and inconsistent toxicity among various bee groups (Johansen et al. 1983; Malaspina and Stort 1983; Torchio 1983; Macieira and Hebling-Beraldo 1989; Peach et al. 1995; Malone et al. 2000; Moraes et al. 2000; Scott-Dupree et al. 2009; Roessink et al. 2011; Biddinger et al. 2013). This variability results, in part, from the basic biological differences between the highly social honey bees and other non-eusocial species, as well as intrinsic differences in physiology, life cycle, and behavior between any two insect species (Thompson and Hunt 1999).

The need to thoroughly explore pesticide risk assessment for non-Apis pollinators is more important now than in the past as many areas around the world are seeing an increasing demand for insect pollination. The decline of available managed honey bees and the consequential rising costs for honey bee pollination services have left the needs of agriculture unmet. (Aizen and Harder 2009). As a result, across the globe many farmers are looking to other managed or wild (unmanaged) non-Apis bee species, and scientists are documenting that many crops are pollinated to a significant level by non-Apis bees (Garibaldi et al. 2013). For example, managed bumble bees (Bombus spp.) are increasingly being used to support agricultural and horticultural production. Over 1 million bumble bee colonies of different species were sold worldwide in 2006, primarily for greenhouse fruit and vegetable production (e.g., tomato, Lycopersicon esculentum), but also increasingly for commercial orchards and seed production (Velthuis and van Doorn 2006).

In the United States, many growers of alfalfa seed (Medicago sativa), almond (Prunus dulcis), apple (Malus domestica), blueberry (Vaccinium spp.), and sweet cherry (Prunus avium) are using managed solitary bees such as wood-nesting alfalfa leafcutting bees (Megachile rotundata), blue orchard bees (Osmia lignaria), and ground-nesting alkali bees (Nomia melanderi). In some places, the use of these non-Apis pollinators is already widespread or is becoming more common (Bosch and Kemp 2001). For example, in the United States, approximately 35 000 tons of alfalfa seeds are produced annually with pollination provided by alfalfa leafcutting bees from Canada (Mayer and Johansen 2003; Stephen 2003; Pitts-Singer 2008; James 2011; Pitts-Singer, personal communication, December 9, 2011). In Japan, the hornfaced bee (Osmia cornifrons) is managed to pollinate orchards of apple and pear (Pyrus communis) (Matsumoto et al. 2009), and in Brazil, the carpenter bee Xylocopa frontalis can be managed to pollinate the passion fruit (Passiflora edulis; Freitas and Oliveira Filho 2003). In Kenya, solitary bees have not yet been commercialized for pollination purposes, but efforts are underway to develop management protocols for solitary bees such as Xylocopa calens, Xylocopa incostans, and Xylocopa flavorufa for high-value greenhouse crops (Kasina, personal communication, October 5, 2011).

In the tropics, efforts are also underway to develop meliponiculture (stingless beekeeping) as a source of revenue from honey production, other hive products, and rentals for crop pollination. Meliponiculture is well established in countries such as Brazil and Mexico (Nogueira-Neto 1997; Villanueva-Gutiérrez et al. 2005). In Africa there are ongoing efforts to improve the management and expand the use of regionally native stingless bees, for example in Ghana (Kwapong et al. 2010) and in Kenya (Kasina, personal communication, October 5, 2011).

At the same time, across the world, there is a growing emphasis on the role of unmanaged or wild bees in agro-ecosystems among agriculture and conservation agencies. For example, in the United States this includes national-level ecosystem restoration efforts by the US Department of Agriculture's Natural Resources Conservation Service (USDA-NRCS), mandated under the Food, Conservation and Energy Act of 2008 (Vaughan and Skinner 2009). These conservation efforts are based upon general trends demonstrating declines in populations of wild bees in agricultural landscapes (Kremen et al. 2004; Biesmeijer et al. 2006; National Research Council 2007), as well as the increasingly large body of research demonstrating the significant role that unmanaged non-Apis bees may play in crop pollination (Kremen et al. 2002; Kremen et al. 2004; Njoroge et al. 2004; Winfree et al. 2007; Campos 2008; Winfree et al. 2008; Kasina et al. 2009; Isaacs and Kirk 2010; Vieira et al. 2010; Carvalheiro et al. 2011; Gariboldi et al. 2013). Furthermore, recent research highlights the importance of a diverse pollinator guild for optimal pollination (Klein et al. 2003; Höhn et al. 2008), as well as the benefits of the interaction between honey bees and wild bees to enhance the pollination effectiveness of honey bees (Greenleaf and Kremen 2006a, 2006b; Carvalheiro et al. 2011).

Non-Apis bees are often specialized for foraging on particular flower taxa, such as squash, berries, forage legumes, or orchard crops (Tepedino 1981; Bosch and Kemp 2001; Javorek et al. 2002; Brunet and Stewart 2010). This specialization is usually associated with more efficient pollination on an individual bee visit basis, which can lead to production of larger and more abundant fruit or seed from certain crops (Greenleaf and Kremen 2006a, 2006b; Klein et al. 2007, but see also Rader et al. 2009). In one study, researchers estimated that non-managed bees contribute an estimated US$3 billion worth of crop pollination annually to the US economy (Losey and Vaughan 2006). More recently, researchers estimated that in California alone, unmanaged non-Apis bees pollinated US$937 million to US$2.4 billion worth of crops (Chaplin-Kramer et al. 2011). In addition to their impact on agro-ecosystems, non-Apis pollinators are crucial to native flora. More than 85% of flowering plants benefit from animal pollinators (Ollerton et al. 2011), most of which are insects and the most important of which are bees (Apiformes).

Because of the recent increase in our understanding of the value of non-Apis bees for agriculture (Garibaldi et al. 2013) and the critical role they play in natural ecosystems, researchers have suggested that non-Apis bees could play a useful role in risk-assessment for pollinators (Biddinger et al. 2013). Specifically, they recommend that at least one solitary managed species, such as the wood-nesting alfalfa leafcutting bees (M. rotundata) or the blue orchard bees (O. lignaria) (Abbott et al. 2008; Ladurner et al. 2008), and one managed social non-Apis bee, such as bumble bees (e.g., Bombus impatiens or Bombus terrestris) in temperate climates (Thompson and Hunt 1999) or the highly social stingless bees (e.g., Melipona spp. or Trigona spp.) in the tropics (Valdovinos-Núñez et al. 2009) is incorporated into regulatory testing schemes. To develop appropriate toxicity tests and risk assessment protocols for non-Apis bees, however, it is important to understand more about non-Apis bees and the unique exposure pathways relevant for them.

3.2 NON-APIS BEE BIOLOGY AND DIVERSITY

Worldwide, there are over 20 000 recorded species of bees (Michener 2007; Ascher and Pickering 2011). They range in size from approximately 2 mm (1/12 inch) to more than 25 mm (1 inch), exhibit a wide variety of foraging and nesting strategies, vary from solitary to highly social, and exhibit other diverse life histories.

Bees use nectar mainly as a carbohydrate source and pollen as a source of protein, fatty acids, minerals, and vitamins. Some species also use other plant resources such as resins, leaves, plant hairs, oil, and fragrances to feed their larvae, build and protect nests, or attract mates (Michener 2007). Because they use plant products during all life cycle stages, they are vulnerable to plant protection products that are present or expressed in pollen and nectar, or that are found in or on other plant resources.

During their life cycle, bees undergo a complete metamorphosis where they develop through egg, larval, pupal, and adult stages. It is only the last of these stages, the adult, which most people see and recognize as a bee. During the first three stages, the bee is inside a brood cell of the nest. The length of each stage varies widely between species and is often defined by whether the bee is solitary or social (O'Toole and Raw 1999). In the case of solitary bees, each female works alone to create a brood cell, place a mixture of pollen and nectar into it, and then lay an egg on (or more rarely in) the food. Solitary bees may take a year to complete metamorphosis, although it can happen faster, that is, 4–6 weeks in those species that have two or three generations per year. Social bees, on the other hand, take only a few weeks to complete growth and emerge as adults.

The quantity of food provided at the time of egg-laying depends on whether the larvae are mass-provisioned (i.e., all of the bee's food is supplied in the cell at one time), or if the larvae are progressively fed (i.e., the food is delivered in small amounts over time). Most solitary bees mass provision their brood cells, as do most stingless bees, whereas honey bees and most bumble bees feed their brood progressively.

Female bees of most species have special morphological structures that enable them to carry pollen back to their nests. For example, the tibiae on the hind legs of honey bees, bumble bees, and stingless bees are modified into corbiculae (a flattened, shallowly depressed area margined with a narrow band of stiff hairs) into which the bee accumulates pollen wetted with nectar and packed into place. Other bee species have scopae to transport pollen. Scopae are fringes, tufts, or brushes of hair on their legs, their thorax, or the undersurface of the abdomen. Scopae are used to transport large amounts of pollen, usually in a dry state.

The wide range of life history traits of bees has implications for their exposure to pesticides (Brittain and Potts 2011) and so relevant aspects of their natural history is described below.

3.2.1 GENERALIST AND SPECIALIST FORAGERS