[Charles D. Michener] The Bees of the World 2nd Ed(BookZZ.org)

  The Bees of the World

  The Bees of theWorld

Charles D. Michener

University of Kansas Natural History Museum

and Department of Entomology The Johns Hopkins University Press Baltimore and London

  © 2000 The Johns Hopkins University Press All rights reserved. Published 2000

Printed in the United States of America on acid-free paper

9 8 7 6 5 4 3 2 1 The Johns Hopkins University Press 2715 North Charles Street Baltimore, Maryland 21218-4363 www.press.jhu.edu Library of Congress Cataloging-in Publication Data Michener, Charles Duncan, 1918–

  The bees of the world / Charles D. Michener. p. cm. Includes bibliographical references.

  ISBN 0-8018-6133-0 (alk. paper)

  1. Bees Classification. I. Title QL566.M53 2000 595.79 99-30198 CIP

  ⬘9—dc21 A catalog record for this book is available from the British Library. Title page illustration from H. Goulet and J. T. Huber (1993). Used with permission. To my many students, now scattered over the world, from whom I have learned much

and to my family, who lovingly tolerate an obsession with bees

  Preface ^ix New Names ^xiv Abbreviations ^xiv

  39. Subfamily Diphaglossinae ¹⁶⁴

  29. Family-Group Names ¹¹¹

  30. Explanation of Taxonomic Accounts in Sections 36 to 119 ¹¹²

  31. Some Problematic Taxa ¹¹⁴

  32. The Identification of Bees ¹¹⁵

  33. Key to the Families, Based on Adults ¹¹⁶

  34. Notes on Certain Couplets in the Key to Families (Section 33) ¹²⁰

  35. Practical Key to Family-Group Taxa, Based on Females ¹²¹

  36. Family Stenotritidae ¹²³

  37. Family Colletidae ¹²⁶

  38. Subfamily Colletinae ¹³⁰

  40. Tribe Caupolicanini ¹⁶⁵

  27. Reduction or Loss of Structures ¹⁰⁴

  41. Tribe Diphaglossini ¹⁶⁸

  42. Tribe Dissoglottini ¹⁷⁰

  43. Subfamily Xeromelissinae ¹⁷¹

  44. Tribe Chilicolini ¹⁷²

  45. Tribe Xeromelissini ¹⁷⁷

  46. Subfamily Hylaeinae ¹⁷⁸

  47. Subfamily Euryglossinae ²¹⁰

  48. Family Andrenidae ²²⁵

  49. Subfamily Alocandreninae ²²⁸

  50. Subfamily Andreninae ²²⁹

  28. New and Modified Structures ¹⁰⁶

  26. Biogeography ¹⁰⁰

  1. About Bees and This Book ¹

  12. Bees and Sphecoid Wasps as a Clade ⁵⁴

  2. What Are Bees? ²

  3. The Importance of Bees ³

  4. Development and Reproduction ⁴

  5. Solitary versus Social Life ⁹

  6. Floral Relationships of Bees ¹³

  7. Nests and Food Storage ¹⁹

  8. Parasitic and Robber Bees ²⁶

  9. Body Form, Tagmata, and Sex Differences ³⁸

  10. Structures and Anatomical Terminology of Adults ⁴⁰

  11. Structures and Terminology of Larvae ⁵³

  13. Bees as a Holophyletic Group ⁵⁵

  25. Dispersal ⁹⁹

  14. The Origin of Bees from Wasps ⁵⁸

  15. Classification of the Bee-Sphecoid Clade ⁶⁰

  16. Bee Taxa and Categories ⁶¹

  17. Methods of Classification ⁷¹

  18. The History of Bee Classifications ⁷²

  19. Short-Tongued versus Long-Tongued Bees ⁷⁸

  20. Phylogeny and the Proto-Bee ⁸³

  21. The Higher Classification of Bees ⁸⁸

  22. Fossil Bees ⁹³

  24. Diversity and Abundance ⁹⁶

  51. Subfamily Panurginae ²⁶⁰ Contents

  273 ⁶¹⁴

  53. Tribe Panurgini _{278 618}

  89. Subfamily Nomadinae

  54. Tribe Melitturgini _{281 620}

  90. Tribe Hexepeolini

  55. Tribe Protomeliturgini ₂₈₂

  91. Tribe Brachynomadini ₆₂₄

  56. Tribe Perditini _{292 627}

  92. Tribe Nomadini

  57. Tribe Calliopsini ₃₀₁

  93. Tribe Epeolini ₆₃₃

  58. Subfamily Oxaeinae ₃₀₄

  94. Tribe Ammobatoidini ₆₃₆

  59. Family Halictidae ₃₀₇

  95. Tribe Biastini ₆₃₉

  60. Subfamily Rophitinae _{317 640}

  96. Tribe Townsendiellini

  61. Subfamily Nomiinae _{330 641}

  97. Tribe Neolarrini

  62. Subfamily Nomioidinae ₃₃₃

  98. Tribe Ammobatini ₆₄₆

  63. Subfamily Halictinae _{339 647}

  99. Tribe Caenoprosopidini

  64. Tribe Halictini 100. Subfamily Apinae _{377 652}

  

65. Tribe Augochlorini 101. Tribe Isepeolini

_{396 654}

  66. Family Melittidae 102. Tribe Osirini _{399 658}

  67. Subfamily Dasypodainae 103. Tribe Protepeolini _{400 660}

  

68. Tribe Dasypodaini 104. Tribe Exomalopsini

_{405 665}

  69. Tribe Promelittini 105. Tribe Ancylini _{406 667}

  70. Tribe Sambini 106. Tribe Tapinotaspidini _{409 674}

  71. Subfamily Meganomiinae 107. Tribe Tetrapediini _{412 676}

  

72. Subfamily Melittinae 108. Tribe Ctenoplectrini

_{417 679}

  73. Family Megachilidae 109. Tribe Emphorini _{419 686}

  74. Subfamily Fideliinae 110. Tribe Eucerini _{420 720}

  

75. Tribe Pararhophitini 111. Tribe Anthophorini

_{421 731}

  

76. Tribe Fideliini 112. Tribe Centridini

_{424 739}

  77. Subfamily Megachilinae 113. Tribe Rhathymini _{427 740}

  

78. Tribe Lithurgini 114. Tribe Ericrocidini

_{431 747}

  

79. Tribe Osmiini 115. Tribe Melectini

_{474 754}

  

80. Tribe Anthidiini 116. Tribe Euglossini

_{521 761}

  81. Tribe Dioxyini 117. Tribe Bombini _{526 779}

  

82. Tribe Megachilini 118. Tribe Meliponini

_{570 806}

  83. Family Apidae 119. Tribe Apini ₅₇₅

  84. Subfamily Xylocopinae _{577 809}

  85. Tribe Manueliini Literature Cited _{578 871}

  86. Tribe Xylocopini Addenda _{593 873}

  87. Tribe Ceratinini Index of Terms _{600 877}

88. Tribe Allodapini Index of Taxa Color plates follow page 32.

  Preface

In some ways this may seem the wrong time to write on the systematics

of the bees of the world, the core topic of this book. Morphological in-

formation on adults and larvae of various groups has not been fully de-

veloped or exploited, and molecular data have been sought for only a few

groups. The future will therefore see new phylogenetic hypotheses and

improvement of old ones; work in these areas continues, and it has been

tempting to defer completion of the book, in order that some of the new

information might be included. But no time is optimal for a systematic

treatment of a group as large as the bees; there is always significant re-

search under way. Some genera or tribes will be well studied, while others

lag behind, but when fresh results are in hand, the latter may well over-

take the former. I conclude, then, that in spite of dynamic current activ-

ity in the field, now is as good a time as any to go to press.

  

This book constitutes a summary of what I have been able to learn

about bee systematics, from the bees themselves and from the vast body

of literature, over the many years since I started to study bees, publishing

my first paper in 1935. Bee ecology and behavior, which I find fully as

fascinating as systematics, are touched upon in this book, but have been

treated in greater depth and detail in other works cited herein.

  

After periods when at least half of my research time was devoted to

other matters (the systematics of Lepidoptera, especially saturniid moths;

the biology of chigger mites; the nesting and especially social behavior of

bees), I have returned, for this book, to my old preoccupation with bee

systematics. There are those who say I am finally finishing my Ph.D. thesis!

My productive activity in biology (as distinguished from merely look-

ing and being fascinated) began as a young kid, when I painted all the native plants that I could find in flower in the large flora of Southern California. When, after a few years, finding additional species became

difficult, I expanded my activities to drawings of insects. With help from

my mother, who was a trained zoologist, I was usually able to identify them to family. How I ultimately settled on Hymenoptera and more

specifically on bees is not very clear to me, but I believe it had in part to

do with Perdita rhois Cockerell, a beautiful, minute, yellow-and-black in-

sect that appeared in small numbers on Shasta daisies in our yard each

summer. The male in particular is so unbeelike that I did not identify it

  

became more proficient in running small Hymenoptera, including bees,

through the keys in Comstock’s Introduction to Entomology.

  Southern California has a rich bee fauna, and as I collected more

species from the different flowers, of course I wanted to identify them to

the genus or species level. Somehow I learned that T. D. A.Cockerell at

the University of Colorado was the principal bee specialist active at the

time. Probably at about age 14 I wrote to him, asking about how to iden-

tify bees. He responded with interest, saying that Viereck’s Hymenoptera

of Connecticut (1916) (which I obtained for $2.00) was not very useful in

the West. Cresson’s Synopsis (1887) was ancient even in the 1930s, but was available for $10.00. With these inadequate works I identified to genus a cigar box full of bees, pinned and labeled, and sent them to

Cockerell for checking. He returned them, with identifications corrected

as needed, and some specimens even identified to species.

  

Moreover, Cockerell wrote supporting comments about work on bees

and invited me to meet him and P. H. Timberlake at Riverside, Califor-

nia, where the Cockerells would be visiting. Timberlake was interested in

my catches because, although I lived only 60 miles from Riverside, I had

collected several species of bees that he had never seen. Later, he invited

me to accompany him on collecting trips to the Mojave and Colorado deserts and elsewhere.

  

Professor and Mrs. Cockerell later invited me to spend the next sum-

mer (before my last year in high school) in Boulder with them, where I

could work with him and learn about bees. Cockerell was an especially charming man who, lacking a university degree, was in some ways a

second-class citizen among the university faculty members. He had never

had many students who became seriously interested in bees, in spite of his long career (his publications on bees span the years from 1895 to

1949) as the principal bee taxonomist in North America if not the world.

Probably for this reason he was especially enthusiastic about my interest

and encouraged the preparation and publication of my first taxonomic

papers. Thus I was clearly hooked on bees well before beginning my un-

dergraduate work at the University of California at Berkeley.

  

As a prospective entomologist I was welcomed in Berkeley and given

space to work among graduate students. During my undergraduate and

graduate career, interacting with faculty and other students, I became a

comparative morphologist and systematist of bees, and prepared a disser-

tation (1942) on these topics, published with some additions in 1944.

The published version included a key to the North American bee genera,

the lack of which had sent me to Professor Cockerell for help a few years

before. Especially important to me during my student years at Berkeley

were E. Gorton Linsley and the late Robert L. Usinger.

  

There followed several years when, because of a job as lepidopterist at

the American Museum of Natural History, in New York, and a commis-

sion in the Army, my research efforts were taken up largely with Lepi- doptera and with mosquitos and chigger mites, but I continued to do

limited systematic work on bees. It was while in the Army, studying the

biology of chigger mites, that I had my first tropical experience, in Panama, and encountered, for the first time, living tropical stingless

honey bees like Trigona and Melipona and orchid bees like Euglossa at or-

chid flowers. In 1948 I moved to the University of Kansas, and since

  

Until 1950, I had gained little knowledge of bee behavior and nesting

biology, having devoted myself to systematics, comparative morphology,

and floral relationships, the last mostly because the flowers help you find

the bees. In 1950, however, I began a study of leafcutter bee biology, and

a few years later I began a long series of studies of nesting biology and so-

cial organization of bees, with emphasis on primitively social forms and

on the origin and evolution of social behavior. With many talented grad-

uate students to assist, this went on until 1990, and involved the publica-

tion in 1974 of The Social Behavior of the Bees. Concurrently, of course,

my systematic studies continued; behavior contributes to systematics and

vice versa, and the two go very well together.

  

Across the years, I have had the good fortune to be able to study both

behavior and systematics of bees in many parts of the world. In addition

to shorter trips of weeks or months, I spent a year in Brazil, a year in Aus-

tralia, and a year in Africa. The specimens collected and ideas developed

on these trips have been invaluable building blocks for this book.

Without the help of many others, preparing this book in its present form

would have been impossible. A series of grants from the National Science

Foundation was essential. The University of Kansas accorded me free-

dom to build up a major collection of bees as part of the Snow Entomo-

logical Division of the Natural History Museum, and provided excellent

space and facilities for years after my official retirement. Students and other faculty members of the Department of Entomology also con-

tributed in many ways. The editorial and bibliographic expertise of Jinny

Ashlock, and her manuscript preparation along with that of Joetta

Weaver, made the job possible. Without Jinny’s generous help, the book

manuscript would not have been completed. And her work as well as Joetta’s continued into the long editorial process.

  It is a pleasure to acknowledge, as well, the helpful arrangements made by the Johns Hopkins University Press and particularly the energy and enthusiasm of its science editor, Ginger Berman. For marvelously de-

tailed and careful editing, I thank William W. Carver of Mountain View,

California.

  

The help of numerous bee specialists is acknowledged at appropriate

places in the text. I mention them and certain others here with an indica-

tion in some cases of areas in which they helped: the late Byron A.

Alexander, Lawrence, Kansas, USA (phylogeny, Nomada); Ricardo Ayala,

Chamela, Jalisco, Mexico (Centridini); Donald B. Baker, Ewell, Surrey,

England, UK; Robert W. Brooks, Lawrence, Kansas, USA (Anthophor-

ini, Augochlorini); J. M. F. de Camargo, Ribeirão Preto, São Paulo, Brazil (Meliponini); James W. Cane, Logan, Utah, USA (Secs. 1-32 of

the text); Bryan N. Danforth, Ithaca, New York, USA (Perditini, Halic-

tini); H. H. Dathe, Eberswalde, Germany (palearctic Hylaeinae); Con-

nal D. Eardley, Pretoria, Transvaal, South Africa (Ammobatini); the late

George C. Eickwort, Ithaca, New York, USA (Halictinae); Michael S.

Engel, Ithaca, New York, USA (Augochlorini, fossil bees); Elizabeth M.

Exley, Brisbane, Queensland, Australia (Euryglossinae); Terry L. Gris- wold, Logan, Utah, USA (Osmiini, Anthidiini); Terry F. Houston, Perth,Western Australia (Hylaeinae, Leioproctus); Wallace E. LaBerge, Champaign, Illinois, USA (Andrena, Eucerini); G. V. Maynard, Can-

  D.C., USA (Halictini); Gabriel A. R. Melo, Ribeirão Preto, São Paulo,

Brazil (who read much of the manuscript); Robert L. Minckley, Auburn,

Alabama, USA (Xylocopini); Jesus S. Moure, Curitiba, Paraná, Brazil; Christopher O’Toole, Oxford, England, UK; Laurence Packer, North York, Ontario, Canada (Halictini); Alain Pauly, Gembloux, Belgium

(Malagasy bees, African Halictidae); Yuri A. Pesenko, Leningrad, Russia;

Stephen G. Reyes, Los Baños, Philippines (Allodapini); Arturo Roig- Alsina, Buenos Aires, Argentina (phylogeny, Emphorini, Tapinotaspi- dini, Nomadinae); David W. Roubik, Balboa, Panama (Meliponini);

Jerome G. Rozen, Jr., New York, N.Y., USA (Rophitini, nests and larvae

of bees, and ultimately the whole manuscript); Luisa Ruz, Valparaíso,

Chile (Panurginae); the late S. F. Sakagami, Sapporo, Japan (Halictinae,

Allodapini, Meliponini); Maximilian Schwarz, Ansfelden, Austria (Coe-

lioxys); Roy R. Snelling, Los Angeles, California, USA (Hylaeinae); Os-

amu Tadauchi, Fukuoka, Japan (Andrena); Harold Toro, Valparaíso,

Chile (Chilicolini, Colletini); Danuncia Urban, Curitiba, Paraná, Brazil

(Anthidiini, Eucerini); Kenneth L. Walker, Melbourne, Victoria, Aus-

tralia (Halictini); V. B. Whitehead, Cape Town, South Africa (Rediviva);

Paul H.Williams, London, England, UK (Bombus); Wu Yan-ru, Beijing,

China; Douglas Yanega, Belo Horizonte, Minas Gerais, Brazil, and Riverside, California.

  

The persons listed above contributed toward preparation or comple-

tion of the book manuscript, or the papers that preceded it, and also in some cases gave or lent specimens for study; the following additional persons or institutions lent types or other specimens at my request: Josephine E. Cardale, Canberra, ACT, Australia; Mario Comba, Cecchina, Italy (Tetralonia); George Else and Laraine Ficken, London,

England, UK; Yoshihiro Hirashima, Miyazaki City, Japan; Frank Koch,

Berlin, Germany; Yasuo Maeta, Matsue, Japan; the Mavromoustakis

Collection, Department of Agriculture, Nicosia, Cyprus (Megachilinae).

  

The illlustrations in this book are designed to show the diversity (or,

in certain cases, similarity or lack of diversity) among bees. It was entirely

impractical to illustrate each couplet in the keys—there are thousands of

them—and I made no effort to do so, although references to relevant text

illustrations are inserted frequently into the keys. Drs. R. J. McGinley and B. N. Danforth, who made or supervised the making of the many

illustrations in Michener, McGinley, and Danforth (1994), have permit-

ted reuse here of many of those illustrations. The other line drawings are

partly original, but many of them are from works of others, reproduced

here with permission. I am greatly indebted to the many authors whose

works I have used as sources of illustrations; specific acknowledgments accompany the legends. In particular I am indebted to J. M. F. de Ca-

margo for the use of two of his wonderful drawings of meliponine nests,

and to Elaine R. S. Hodges for several previously published habitus

drawings of bees. Modifications of some drawings, additional lettering as

needed, and a few original drawings, as acknowledged in the legends, are

the work of Sara L. Taliaferro; I much appreciate her careful work.

  

The colored plates reproduce photographs from the two sources indi-

cated in the legends: Dr. E. S. Ross, California Academy of Sciences, San

Francisco, California, USA, and Dr. Paul Westrich, Maienfeldstr. 9, Tübingen, Germany. I am particularly indebted to Drs. Ross and

  

noting here that many other superb photographs by Westrich were pub-

lished in his two-volume work on the bees of Baden-Württemberg (Westrich, 1989).

  

Svetlana Novikova and Dr. Bu Wenjun provided English translations

of certain materials from Russian and Chinese, respectively. Their help is

much appreciated.

  

The text has been prepared with the help of the bees themselves, pub-

lications about them, and unpublished help from the persons listed

above. I have not included here the names of all the persons responsible

for publications that I have used and from which I have, in many cases,

derived ideas, illustrations, bases for keys, and other items. They are ac-

knowledged in the text. Several persons, however, have contributed pre-

viously unpublished keys that appear under their authorship in this

book. Such contributions are listed below, with the authors’ affiliations.

  

“Key to the Palearctic Subgenera of Hylaeus” by H.H. Dathe, Deutsches

Entomologisches Institut, Postfach 10 02 38, D-16202 Eberswalde,

Germany.

“Key to the New World Subgenera of Hylaeus” by Roy R. Snelling, Los

Angeles County Museum of Natural History, 900 Exposition Boule-

vard, Los Angeles, California 90007, USA.

“Key to the Genera of Osmiini of the Eastern Hemisphere,” “Key to the

Subgenera of Othinosmia,” and “Key to the Subgenera of Protosmia”

by Terry L. Griswold, Bee Biology and Systematics Laboratory, UMC

53, Utah State University, Logan, Utah 84322-5310, USA. “Key to the Genera of the Tapinotaspidini” by Arturo Roig-Alsina,

Museo Argentino de Ciencias Naturales, Av. A. Gallardo 470, 1405

  Buenos Aires, Argentina. I have modified the terminology employed in these keys, as necessary, to correspond with that in use in other parts of this book (see Sec. 10).

  Several contributions became so modified by me that the original au- thors would scarcely recognize them. I have identified them by expres- sions such as “modified from manuscript key by . . .”

Names of authors of species are not integral parts of the names of the

organisms. In behavioral or other nontaxonomic works I omit them ex-

cept when required by editors. But in this book, which is largely a sys-

tematic account, I have decided to include them throughout for the sake

of consistency.

  

A measure of the success of this book will be the need for revision as

new work is completed and published. Not only does this book contain

a great deal of information about bees, but, by inference or explicitly, it

indicates myriad topics about which more information is needed. I hope

that it points the way for the numerous researchers who will take our knowledge beyond what is here included, and beyond what is to be found in the nearly 2,500 items in the Literature Cited.

        

Abstractors may note that five new names are proposed in this book, as

follows:

  Acedanthidium, new name (Sec, 80) Andrena (Osychnyukandrena), new name (Sec. 50) Ceratina (Rhysoceratina), new subgenus) (Sec. 87) Fidelia (Fideliana), new subgenus (Sec. 76) Nomia (Paulynomia), new subgenus (Sec. 61)

  There are also numerous new synonyms at the generic or subgeneric levels and, as a result, new combinations occur, as noted in the text.

             The following are used in the text: BP = before the present time

  Code = International Code of Zoological Nomenclature Commission = International Commission on Zoological Nomemclature L-T = long-tongued (see Sec. 19) myBP = million years before the present s. str. (sensu stricto) = in the strict sense s. l. (sensu lato) = in the broad sense S-T = short-tongued (see Sec. 19) S1, S2, etc. = first, second, etc., metasomal sterna scutellum = mesoscutellum scutum = mesoscutum stigma = pterostigma of forewing T1, T2, etc. = first, second, etc., metasomal terga

  

The terminology of wing veins and cells also involves abbreviations; see

Section 10.

  The Bees of the World

1. About Bees and This Book

  Since ancient times, people have been drawn to the study of bees. Bees are spritely creatures that move about on pleasant bright days and visit pretty flowers. Anyone studying their behavior should find them attractive, partly because they work in warm sunny places, during pleasant seasons and times of day. The sights and odors of the fieldwork ambience contribute to the well-being of any researcher. Moreover, bees are important pollinators of both natural vegetation and crops, and certain kinds of bees make useful products, especially honey and wax. But quite apart from their practical importance, at least since the time of Aristotle people have been interested in bees because they are fascinating creatures. We are social ani- mals; some bees are also social. Their interactions and communications, which make their colonial life func- tion, have long been matters of interest; we wonder how a tiny brain can react appropriately to societal problems similar to those faced by other social animals, such as hu- mans. For a biologist or natural historian, bees are also fas- cinating because of their many adaptations to diverse flowers; their ability to find food and nesting materials and carry them over great distances back to a nest; their ability to remember where resources were found and re- turn to them; their architectural devices, which permit food storage, for example, in warm, moist soil full of bac- teria and fungi; and their ability to rob the nests of oth- ers, some species having become obligate robbers and others cuckoolike parasites. These are only a few of the in- teresting things that bees do.

  I consider myself fortunate to work with such a bio- logically diverse group of insects, one of which is the com- mon honey bee, Apis mellifera Linnaeus. In terms of phys- iology and behavior, it is the best-known insect. Educated guesses about what happens in another bee species are of- ten possible because we know so much about Apis mellif- era. In this book, however, Apis is treated briefly, like all other bee taxa, its text supplemented by references to books on Apis biology; the greater part of this book con- cerns bees (the great majority) that are not even social.

  Sections 2 to 28, and what follows here, are intended to provide introductory materials important to an un- derstanding of all bees and aspects of their study. Some topics are outlined only briefly to provide background in- formation; others are omitted entirely; still others are dealt with at length and with new or little-known insights when appropriate.

  This book is largely an account of bee classification and of phylogeny, so far as it has been pieced together, i.e., the systematics of all bees of the world. All families, subfam- ilies, tribes, genera, and subgenera are characterized by means of keys and (usually brief) text comments to facil- itate identification. I include many references to such re- visional papers or keys as exist, so that users can know where to go to identify species. About 16,000 species have been placed as to genus and subgenus (see Sec. 16); no at- tempt has been made even to list them here, although the approximate number of known species for each genus and subgenus is given in Table 16-1, as well as under each genus or subgenus in Sections 36 to 119. Aspects of bee biology, especially social and parasitic behavior, nest ar- chitecture, and ecology, including floral associations, are indicated. Major papers on bee nesting biology and flo- ral relationships are also cited. The reader can thus use this book as a guide to the extensive literature on bee biology. Because the male genitalia and associated sterna of bees provide characters useful at all levels, from species to fam- ily, and because they are often complex and difficult to de- scribe, numerous illustrations are included, as well as ref- erences to publications in which others are illustrated.

  Besides entomologists, this book should be useful to ecologists, pollination biologists, botanists, and other naturalists who wish to know about the diversity and habits of bees. Such users may not be greatly concerned with details of descriptive material and keys, but should be able to gain a sense of the taxonomic, morphological, and behavioral diversity of the bee faunas with which they work. As major pollinators, bees are especially important to pollination biologists. I hope that by providing infor- mation on the diversity of bees and their classification and identification, this book will in some mostly indirect ways contribute to pollination biology.

  The title of this book can be read to indicate that the book should deal, to at least some degree, with all aspects of bee studies. It does not. All aspects of apiculture, the study and practice of honey bee culture, based on man- aged colonies of Apis mellifera Linnaeus and A. cerana Fabricius, are excluded. The findings about sensory phys- iology as well as behavioral interactions, including com- munication, foraging behavior, and caste control are vir- tually omitted, although they constitute some of the most fascinating aspects of biology and in the hands of Karl von Frisch led to a Nobel prize. A major work, principally about communication, is Frisch (1967).

  Whether the scientific study of communication in Apis is part of apiculture is debatable, but the study of all the other species of bees is not; such studies are subsumed un- der the term melittology. Persons studying bees other than Apis and concerned about the negative and awkward expression “non-Apis bees” would do well to call them- selves melittologists and their field of study melittology. I would include under the term “melittology” the taxo- nomic, comparative, and life history studies of species of the genus Apis, especially in their natural habitats. This book is about melittology.

  Users of this book may wonder about the lack of a glos- sary. Definitions and explanations of structures, given mostly in Section 10, are already brief and would be largely repeated in a glossary. The terms, including many that are explained only by illustrations, are therefore in- cluded in the Index of Terms, with references to pages where they are defined, illustrated, or explained. Some terminology, e.g., that relevant only to certain groups of bees, is explained in other sections, and indexed accord- ingly.

2. What Are Bees?

  A major group of the order Hymenoptera is the Section Aculeata, i.e., Hymenoptera whose females have stings— modifications of the ovipositors of ancestral groups of Hymenoptera. The Aculeata include the wasps, ants, and bees. Bees are similar to one group of wasps, the sphecoid wasps, but are quite unlike other Aculeata. Bees are usu- ally more robust and hairy than wasps (see Pls. 3-15), but some bees (e.g., Hylaeus, Pl. 1; Nomada, Pl. 2) are slender, sparsely haired, and sometimes wasplike even in col- oration. Bees differ from nearly all wasps in their depen- dence on pollen collected from flowers as a protein source to feed their larvae and probably also for ovarian devel- opment by egg-laying females. (An exception is a small clade of meliponine bees of the genus Trigona, which use carrion instead of pollen.) Unlike the sphecoid wasps, bees do not capture spiders or insects to provide food for their offspring. Thus nearly all bees are plant feeders; they have abandoned the ancestral carnivorous behavior of sphecoid wasp larvae. (Adult wasps, like bees, often visit flowers for nectar; adult sphecoid wasps do not collect or eat pollen.)

  Bees and the sphecoid wasps together constitute the superfamily Apoidea (formerly called Sphecoidea, but see Michener, 1986a). The Apoidea as a whole can be recog- nized by a number of characters, of which two are the most conspicuous: (1) the posterior pronotal lobe is dis- tinct but rather small, usually well separated from and be- low the tegula; and (2) the pronotum extends ventrally as a pair of processes, one on each side, that encircle or nearly encircle the thorax behind the front coxae. See Section 10 for explanations of morphological terms and Section 12 for more details about the Apoidea as a whole.

  As indicated above, the Apoidea are divisible into two groups: the sphecoid wasps, or Spheciformes, and the bees, or Apiformes (Brothers, 1975). Structural charac- ters of bees that help to distinguish them from sphecoid wasps are (1) the presence of branched, often plumose, hairs, and (2) the hind basitarsi, which are broader than the succeeding tarsal segments. The proboscis is in gen- eral longer than that of most sphecoid wasps. The details, and other characteristics of bees, are explained in Sec- tion 12.

  A conveniently visible character that easily distin- guishes nearly all bees from most sphecoid wasps is the golden or silvery hairs on the lower face of most such wasps, causing the face to glitter in the light. Bees almost never exhibit this characteristic, because their facial hairs are duller, often erect, often plumose, or largely absent. This feature is especially useful in distinguishing small, wasplike bees such as Hylaeus from similar-looking sphe- coid wasps such as the Pemphredoninae.

  The holophyletic Apiformes is believed to have arisen from the paraphyletic Spheciformes. Holophyletic is used here to mean monophyletic in the strict sense. Such a group (1) arose from a single ancestor that would be considered a member of the group, and (2) includes all taxa derived from that ancestor. Groups termed Para-

  phyletic also arose from such an ancestor but do not in-

  clude all of the derived taxa. (See Sec. 16.)

3. The Importance of Bees

  Probably the most important activity of bees, in terms of benefits to humans, is their pollination of natural vegeta- tion, something that is rarely observed by nonspecialists and is almost never appreciated; see Section 6. Of course the products of honey bees—i.e., wax and honey plus small quantities of royal jelly—are of obvious bernefit, but are of trivial value compared to the profoundly im- portant role of bees as pollinators. Most of the tree species of tropical forests are insect-pollinated, and that usually means bee-pollinated. A major study of tropical forest pollination was summarized by Frankie et al. (1990); see also Jones and Little (1983), Roubik (1989), and Bawa (1990). In temperate climates, most forest trees (pines, oaks, etc.) are wind-pollinated, but many kinds of bushes, small trees, and herbaceous plants, including many wild flowers, are bee-pollinated. Desertic and xeric scrub areas are extremely rich in bee-pollinated plants whose preser- vation and reproduction may be essential in preventing erosion and other problems, and in providing food and cover for wildlife. Conservation of many habitats thus de- pends upon preservation of bee populations, for if the bees disappear, reproduction of major elements of the flora may be severely limited.

  Closer to our immediate needs, many cultivated plants are also bee-pollinated, or they are horticultural varieties of bee-pollinated plants. Maintenance of the wild, bee- pollinated populations is thus important for the genetic diversity needed to improve the cultivated strains. Gar- den flowers, most fruits, most vegetables, many fiber crops like flax and cotton, and major forage crops such as alfalfa and clover are bee-pollinated.

  Some plants require bee pollination in order to pro- duce fruit. Others, commonly bee-pollinated, can self- pollinate if no bees arrive; but inbreeding depression is a frequent result. Thus crops produced by such plants are usually better if bee-pollinated than if not; that is, the numbers of seeds or sizes of fruits are enhanced by polli- nation. Estimates made in the late 1980s of the value of insect-pollinated crops (mostly by bees) in the USA ranged from $4.6 to $18.9 billion, depending on various assumptions on what should be included and how the es- timate should be calculated. Also doubtful is the estimate that 80 percent of the crop pollination by bees is by honey bees, the rest mostly by wild bees. But whatever estimates one prefers, bee pollination is crucially important (see O’Toole, 1993, for review), and the acreages and values of insect-pollinated crops are increasing year by year.

  Wild bees may now become even more important as pollinators than in the past, because of the dramatic de- crease in feral honey bee populations in north-temperate climates due to the introduction into Europe and the Americas of mites such as Varroa and tracheal mites, which are parasites of honey bees. Moreover, there are var- ious crops for which honey bees are poor pollinators com- pared to wild bees. Examples of wild bees already com- mercially used are Osmia cornifrons (Radoszkowski), which pollinates fruit trees in Japan, Megachile rotundata (Fabricius), which pollinates alfalfa in many areas, Bom-

  bus terrestris (Linnaeus), which pollinates tomatoes in Eu-

  ropean greenhouses, and other Bombus species that do the same job elsewhere. O’Toole (1993) has given an account of wild bee species that are important in agriculture, and the topic was further considered by Parker, Batra, and Te- pedino (1987), Torchio (1991), and Richards (1993). Since honey bees do not sonicate tubular anthers to ob- tain pollen (i.e., they do not buzz-pollinate; see Sec. 6), they are not effective pollinators of Ericaceae, such as blueberries and cranberries, or Solanaceae such as egg- plants, chilis, and tomatoes.

  Many bees are pollen specialists on particular kinds of flowers, and even among generalists, different kinds of bees have different but often strong preferences. There- fore, anyone investigating the importance of wild bees as pollinators needs to know about kinds of bees. The clas- sification presented by this book can suggest species to consider; for example, if one bee is a good legume polli- nator, a related one is likely to have similar behavior. Pro- boscis length is an important factor in these considera- tions, for a bee with a short proboscis usually cannot reach nectar in a deep flower, and probably will not take pollen there either, so is unlikely to be a significant pollinator of such a plant.

  In many countries the populations of wild bees have been seriously reduced by human activity. Destruction of natural habitats supporting host flowers, destruction of nesting sites (most often in soil) by agriculture, roadways, etc., and overuse of insecticides, among other things, ap- pear to be major factors adversely affecting wild bee pop- ulations. Introduction or augmentation of a major com- petitor for food, the honey bee, has probably also affected some species of wild bees. Recent accounts of such prob- lems and some possible solutions were published by Banaszak (1995) and Matheson et al. (1996); see also O’Toole (1993).

4. Development and Reproduction

  As in all insects that undergo complete metamorphosis, brood cells of their hosts, often inserted into the walls of each bee passes through egg, larval, pupal, and adult the cells; such eggs are often quite specialized in shape and stages (Fig. 4-1). may have an operculum through which the larva emerges

  The haplodiploid system of sex determination has had (see Sec. 8). Conversely, eggs are very large in some sub- a major influence on the evolution of the Hymenoptera. social or primitively eusocial bees like Braunsapis (Allo- As in most Hymenoptera, eggs of bees that have been fer- dapini) and Xylocopa (Xylocopini). Indeed, the largest of tilized develop into females; those that are unfertilized de- all insect eggs are probably those of large species of Xylo- velop into males. Sex is controlled by alleles at one or a copa, which may attain a length of 16.5 mm, about half few loci; heterozygosity at the sex-determining locus (or the length of the bee’s body. Iwata and Sakagami (1966) loci) produces females. Development without fertiliza- gave a comprehensive account of bee egg size relative to tion, i.e., with the haploid number of chromosomes, pro- body size. duces males, since heterozygosity is impossible. Inbreed- The late-embryonic development and hatching of eggs ing results in some diploid eggs that are homozygous at the sex-determining loci; diploid males are thus pro- duced. Such males are ordinarily reproductively useless, for they tend to be short-lived (those of Apis are killed as _a larvae) and to have few sperm cells; moreover, they may produce triploid offspring that have no reproductive po- tential. Thus for practical purposes the sex-determining mechanism is haplodiploid. ^c

  When she mates, a female stores sperm cells in her _b spermatheca; she usually receives a lifetime supply. She can then control the sex of each egg by liberating or not liberating sperm cells from the spermatheca as the egg passes through the oviduct.

  Because of this arrangement, the female (of species whose females are larger than males) is able to place fe- male-producing eggs in large cells with more provisions, male-producing eggs in small cells. In Apis, the males of _d which are larger than the workers, male-producing cells are larger than worker-producing cells and presumably it is the cell size that stimulates the queen to fertilize or not to fertilize each egg. Moreover, among bees that construct cells in series in burrows, the female can place male-pro- ducing eggs in cells near the entrance, from which the re- sultant adults can escape without disturbing the slower- developing females. The number of eggs laid during her lifetime by a female bee varies from eight or fewer for some solitary species to more than a million for queens of some highly social species. Females of solitary bees give _e care and attention to their few offspring by nest-site se- lection, nest construction, brood-cell construction and provisioning, and determination of the appropriate sex of the individual offspring. Of course, it is such atttention to the well-being of offspring that makes possible the low reproductive potential of many solitary bees.

  The eggs of nearly all bees are elongate and gently curved, whitish with a soft, membranous chorion (“shell”) (Fig. 4-1a), usually laid on (or rarely, as in Lithur-