Pesticide Risk Assessment for Pollinators

By David Fischer and Tom Moriarty

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

• Language: English
• Publisher: Wiley
• Release date: Apr 29, 2014
• ISBN: 9781118852699

Book preview

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.

1

Introduction

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

2

Overview 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.

3

Overview 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