The Wisdom of the Hive THE WISDOM The Social Physiology OF THE HIVE of Honey Bee Colonies THOMAS D. SEELEY HARVARD UNIVERSITY PRESS Cambridge, Massachusetts London, England 1995 [(H2P)] iii Copyright © 1995 by the President and Fellows of Harvard College All rights reserved Printed in the United States of America Library of Congress Cataloging-in-Publication Data Seeley, Thomas D. The wisdom of the hive : the social physiology of honey bee colonies / Thomas D. Seeley. p. cm. Includes bibliographical references and index. ISBN 0-674-95376-2 (acid-free) 1. Honeybee—Food. 2. Honeybee—Behavior. I. Title. QL568.A6S445 1995 595.79′9—dc20 95-3645 Designed by Gwen Frankfeldt iv To Saren and Maira, who waited patiently, and to Robin, who helped in all ways Contents Preface xi PART I. INTRODUCTION 1 1. The Issues 3 1.1. The Evolution of Biological Organization 3 1.2. The Honey Bee Colony as a Unit of Function 7 1.3. Analytic Scheme 16 2. The Honey Bee Colony 22 2.1. Worker Anatomy and Physiology 23 2.2. Worker Life History 28 2.3. Nest Architecture 31 2.4. The Annual Cycle of a Colony 34 2.5. Communication about Food Sources 36 2.6. Food Collection and Honey Production 39 3. The Foraging Abilities of a Colony 46 3.1. Exploiting Food Sources over a Vast Region around the Hive 47 3.2. Surveying the Countryside for Rich Food Sources 50 3.3. Responding Quickly to Valuable Discoveries 52 3.4. Choosing among Food Sources 54 3.5. Adjusting Selectivity in Relation to Forage Abundance 59 3.6. Regulating Comb Construction 61 3.7. Regulating Pollen Collection 63 3.8. Regulating Water Collection 65 Summary 66 PART II. EXPERIMENTAL ANALYSIS 69 4. Methods and Equipment 71 4.1. The Observation Hive 71 4.2. The Hut for the Observation Hive 74 4.3. The Bees 75 4.4. Sugar Water Feeders 77 4.5. Labeling Bees 79 4.6. Measuring the Total Number of Bees Visiting a Feeder 81 4.7. Observing Bees of Known Age 81 4.8. Recording the Behavior of Bees in the Hive 81 4.9. The Scale Hive 82 4.10. Censusing a Colony 83 5. Allocation of Labor among Forage Sites 84 How a Colony Acquires Information about Food Sources 85 5.1. Which Bees Gather the Information? 85 5.2. Which Information Is Shared? 88 5.3. Where Information Is Shared inside the Hive 88 5.4. The Coding of Information about Profitability 90 5.5. The Bees’ Criterion of Profitability 94 5.6. The Relationship between Nectar-Source Profitability and Waggle Dance Duration 98 5.7. The Adaptive Tuning of Dance Thresholds 102 5.8. How a Forager Determines the Profitability of a Nectar Source 113 Summary 119 How a Colony Acts on Information about Food Sources 122 5.9. Employed Foragers versus Unemployed Foragers 122 5.10. How Unemployed Foragers Read the Information on the Dance Floor 124 viii Contents 5.11. How Employed Foragers Respond to Information about Food-Source Profitability 132 5.12. The Correct Distribution of Foragers among Nectar Sources 134 5.13. Cross Inhibition between Forager Groups 142 5.14. The Pattern and Effectiveness of Forager Allocation among Nectar Sources 145 Summary 151 6. Coordination of Nectar Collecting and Nectar Processing 155 How a Colony Adjusts Its Collecting Rate with Respect to the External Nectar Supply 156 6.1. Rapid Increase in the Number of Nectar Foragers via the Waggle Dance 156 6.2. Increase in the Number of Bees Committed to Foraging via the Shaking Signal 158 How a Colony Adjusts Its Processing Rate with Respect to Its Collecting Rate 162 6.3. Rapid Increase in the Number of Nectar Processors via the Tremble Dance 162 6.4. Which Bees Become Additional Food Storers? 173 Summary 174 7. Regulation of Comb Construction 177 7.1. Which Bees Build Comb? 177 7.2. How Comb Builders Know When to Build Comb 181 7.3. How the Quantity of Empty Comb Affects Nectar Foraging 187 Summary 191 8. Regulation of Pollen Collection 193 8.1. The Inverse Relationship between Pollen Collection and the Pollen Reserve 194 8.2. How Pollen Foragers Adjust Their Colony’s Rate of Pollen Collection 195 8.3. How Pollen Foragers Receive Feedback from the Pollen Reserves 198 Contents ix 8.4. The Mechanism of Indirect Feedback 201 8.5. Why the Feedback Flows Indirectly 204 8.6 How a Colony’s Foragers Are Allocated between Pollen and Nectar Collection 207 Summary 209 9. Regulation of Water Collection 212 9.1. The Importance of Variable Demand 213 9.2. Patterns of Water and Nectar Collection during Hive Overheating 215 9.3. Which Bees Collect Water? 218 9.4. What Stimulates Bees to Begin Collecting Water? 220 9.5. What Tells Water Collectors to Continue or Stop Their Activity? 221 9.6. Why Does a Water Collector’s Unloading Experience Change When Her Colony’s Need for Water Changes? 226 Summary 234 PART III. OVERVIEW 237 10. The Main Features of Colony Organization 239 10.1. Division of Labor Based on Temporary Specializations 240 10.2. Absence of Physical Connections between Workers 244 10.3. Diverse Pathways of Information Flow 247 10.4. High Economy of Communication 252 10.5. Numerous Mechanisms of Negative Feedback 255 10.6. Coordination without Central Planning 258 11. Enduring Lessons from the Hive 263 Glossary 269 Bibliography 277 Index 291 x Contents Preface n the fall of 1978, having just completed a Ph.D. thesis, I wondered what to study next with the bees, my favorite animals for scien- Itific work. One subject that greatly attracted me was the organi- zation of the food-collection process in honey bee colonies. The recent work by Bernd Heinrich, beautifully synthesized in his book Bum- blebee Economics, had demonstrated the success of viewing a bumble bee colony as an economic unit shaped by natural selection to be ef- ficient in its collection and consumption of energy resources. I was in- trigued by the idea of applying a similar perspective to honey bees. Because colonies of honey bees are larger than those of bumble bees and possess more sophisticated communication systems, it was ob- vious that they must embody an even richer story of colony design for energy economics. Of course, much was known already about the inner workings of honey bee colonies, especially the famous dance language by which bees recruit their hivemates to rich food sources. This communication system had been deciphered in the 1940s by the Nobel laureate Karl von Frisch, and its elucidation had set the stage for one of his students, Martin Lindauer, to conduct in the 1950s sev- eral pioneering studies which dealt explicitly with the puzzle of colony-level organization for food collection. Their discoveries and those of many other researchers provided a solid foundation of knowledge on which to build, but it was also clear that many mys- teries remained about how the thousands of bees in a hive function as a coherent system in gathering their food. It seemed that the best way to begin this work was to describe the foraging behavior of a whole colony living in nature, for simply ob- serving a phenomenon broadly is generally an invaluable first step toward understanding it. So in the summer of 1979, Kirk Visscher and I teamed up to determine the spatiotemporal patterns of a colony’s foraging operation. To do this, we established a colony in a glass- walled observation hive, monitored the recruitment dances of the colony’s foragers, and plotted on a map the forage sites being adver- tised by these dances. This initial study revealed the amazing range of a colony’s foraging—more than 100 square kilometers around the hive—and the surprisingly high level of dynamics in a colony’s for- age sites, with almost daily turnover in the recruitment targets. It also presented us with the puzzle of how a colony can wisely deploy its foragers among the kaleidoscopic array of flower patches in the sur- rounding countryside. From here on, the course of the research arose without a grand design as I and others simply probed whatever topic seemed most interesting in light of the previous findings. Even the central theme of this book—the building of biological organization at the group level—emerged of its own accord from these studies. This book is not just about honey bees. These aesthetically pleas- ing and easily studied insects live in sophisticated colonies that vividly embody the answer to an important question in biology: What are the devices of social coordination, built by natural selection, that have enabled certain species to make the transition from independent organism to integrated society? The study of the honey bee colony, especially its food collection, has yielded what is probably the best- understood example of cooperative group functioning outside the realm of human society. This example deepens our understanding of the mechanisms of cooperation in one species in particular and, by providing a solid baseline for comparative studies, helps us under- stand the means of cooperation within animal societies in general. In writing this book, I have tried to summarize—in a way intelligible to all—what is currently known about how the bees in a hive work to- gether as a harmonious whole in gathering their food. This book will have served its purpose if readers can gain from it a sense of how a honey bee colony functions as a unit of biological organization. I owe deep thanks to many people and institutions that have helped me produce what I report here.