The bees of the world

The Bees of the World


The Bees


of theWorld
SECOND EDITION

Charles D. Michener
Entomology Division
University of Kansas Natural History Museum
and Biodiversity Research Center
and
Entomology Program, Department of Ecology
and Evolutionary Biology
University of Kansas

The Johns Hopkins University Press
Baltimore


© 2000, 2007 The Johns Hopkins University Press
All rights reserved. Published 2007
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.—2nd ed.
p.
cm.
Includes bibliographical references.
ISBN-13: 978-0-8018-8573-0 (hardcover : alk. paper)
ISBN-10: 0-8018-8573-6 (hardcover : alk. paper)
1. Bees—Classification. I. Title.
QL566.M53 2007
595.79Ј9—dc22
2006023201
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


This page intentionally left blank


Contents

Preface to the Second Edition
Preface to the First Edition xi

Abbreviations xvi
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.

ix

About Bees and This Book 1
What Are Bees? 3
The Importance of Bees 4
Development and Reproduction 6

Solitary versus Social Life 12
Floral Relationships of Bees 16
Nests and Food Storage 23
Parasitic and Robber Bees 30
Body Form, Tagmata, and Sex
Differences 42
Structures and Anatomical Terminology
of Adults 44
Structures and Terminology
of Immature Stages 57
Bees and Sphecoid Wasps as a Clade 59
Bees as a Monophyletic Group 60
The Origin of Bees from Wasps 63
Classification of the Bee-Sphecoid
Clade 65
Bee Taxa and Categories 66
Methods of Classification 76
The History of Bee Classifications 77
Short-Tongued versus Long-Tongued
Bees 83
Family-Level Phylogeny and the
Proto-Bee 88
The Higher Classification of Bees 93
Fossil Bees 98

23.
24.
25.
26.
27.

28.
29.
30.
31.
32.
33.
34.
35.
36.
37.

49.

The Geological History of Bees 100
Diversity and Abundance 102
Dispersal 105
Biogeography 106
Reduction or Loss of Structures 110
New and Modified Structures 112
Family-Group Names 117
Explanation of Taxonomic Accounts
in Sections 36 to 121 118
Some Problematic Taxa 120
The Identification of Bees 121
Key to the Families, Based on Adults 122
Notes on Certain Couplets in the Key
to Families (Section 33) 126
Practical Key to Family-Group Taxa,
Based on Females 127
Family Stenotritidae 129

Family Colletidae 132
38. Subfamily Colletinae 136
39. Tribe Paracolletini 138
40. Tribe Colletini 167
41. Tribe Scraptrini 171
42. Subfamily Diphaglossinae 173
43. Tribe Caupolicanini 174
44. Tribe Diphaglossini 177
45. Tribe Dissoglottini 179
46. Subfamily Xeromelissinae 180
47. Subfamily Hylaeinae 187
48. Subfamily Euryglossinae 220
Family Andrenidae 235
50. Subfamily Alocandreninae 238
51. Subfamily Andreninae 239
vii


61.

68.

75.

85.

52. Subfamily Panurginae 270
53. Tribe Protandrenini 273
54. Tribe Panurgini 285
55. Tribe Nolanomelissini 290

56. Tribe Melitturgini 291
57. Tribe Protomeliturgini 295
58. Tribe Perditini 296
59. Tribe Calliopsini 306
60. Subfamily Oxaeinae 316
Family Halictidae 319
62. Subfamily Rophitinae 322
63. Subfamily Nomiinae 332
64. Subfamily Nomioidinae 345
65. Subfamily Halictinae 348
66. Tribe Halictini 354
67. Tribe Augochlorini 393
Family Melittidae 413
69. Subfamily Dasypodainae 416
70. Tribe Dasypodaini 417
71. Tribe Promelittini 422
72. Tribe Sambini 423
73. Subfamily Meganomiinae 426
74. Subfamily Melittinae 429
Family Megachilidae 434
76. Subfamily Fideliinae 436
77. Tribe Pararhophitini 437
78. Tribe Fideliini 438
79. Subfamily Megachilinae 441
80. Tribe Lithurgini 444
81. Tribe Osmiini 448
82. Tribe Anthidiini 491
83. Tribe Dioxyini 538
84. Tribe Megachilini 543
Family Apidae 587

86. Subfamily Xylocopinae 592
87. Tribe Manueliini 595
88. Tribe Xylocopini 596
89. Tribe Ceratinini 611

Color plates follow pages 46 and 78.

viii

90. Tribe Allodapini 619
91. Subfamily Nomadinae 633
92. Tribe Hexepeolini 637
93. Tribe Brachynomadini 639
94. Tribe Nomadini 643
95. Tribe Epeolini 646
96. Tribe Ammobatoidini 653
97. Tribe Biastini 656
98. Tribe Townsendiellini 659
99. Tribe Neolarrini 660
100. Tribe Ammobatini 661
101. Tribe Caenoprosopidini 666
102. Subfamily Apinae 667
103. Tribe Isepeolini 672
104. Tribe Osirini 674
105. Tribe Protepeolini 678
106. Tribe Exomalopsini 680
107. Tribe Ancylini 685
108. Tribe Tapinotaspidini 687
109. Tribe Tetrapediini 694
110. Tribe Ctenoplectrini 697

111. Tribe Emphorini 700
112. Tribe Eucerini 707
113. Tribe Anthophorini 742
114. Tribe Centridini 753
115. Tribe Rhathymini 762
116. Tribe Ericrocidini 763
117. Tribe Melectini 770
118. Tribe Euglossini 778
119. Tribe Bombini 785
120. Tribe Meliponini 803
121. Tribe Apini 830
Literature Cited 833
Addenda 905
Index of Terms 907
Index of Taxa 913


Preface to the Second Edition

Of course I was pleased when Johns Hopkins University Press indicated
an interest in a revised edition of The Bees of the World.
A large review or revisional work like the original The Bees of the World
inevitably goes out of date as new findings or interpretations are made,
and also as errors or omissions in the original book are discovered.
For the original edition (usually referred to below as Michener, 2000)
relevant publications were surveyed through 1997, with some additional
material being included as addenda or otherwise as it came to my notice
into 1999. Some publications that appeared in 1998 and 1999 were not
cited or were inadequately utilized and are now properly incorporated, as
are the items in the Addenda of the original edition. For the second edition, I have tried to cover literature through 2005, with additional material for 2006.

As in the original edition, arbitrary decisions about rank or recognition
of taxa were often needed. Some recently proposed genera and subgenera
are synonymized below, even though they constitute recognizable and
even useful groups, because I am following so far as possible the practices
involved in writing the first edition. The main point is that the classification should represent relationships, or similarities when phylogenetic relationships are in doubt. A classification that emphasizes differences can
result in an unnecessary multiplication of taxa that (1) often can be distinguished only with difficulty or (2) represent odd derivatives whose relationships are better represented by inclusion within the recognized
groups. There is no doubt, however, that some of the taxa here synonymized will be resurrected when new classifications are proposed,
based on phylogenetic hypotheses that are yet to be developed.
Noteworthy developments in recent years are the number of phylogenetic analyses based on molecular characters, morphological characters,
or both, prepared for groups of bees, and the classificatory changes based
on these analyses. When the hypotheses are robust, I have modified the
text in response. When it seems that changes in taxa studied or in the
characters included in the analyses would change the outcome considerably, I usually report the study but, for the sake of stability, I do not
change the classification. Changes in classifications as a result of cladograms subject to major change are not justified, because stability is an
important feature for classifications. We should change a classification
when we know that the change is justified, but otherwise we should not.
ix


The acknowledgments for the first addition still stand, of course. Some
of those listed have generously provided additional help. Other persons
who have helped for this edition, as follows:
John S. Ascher, New York City, New York, USA;
Michael S. Engel, Lawrence, Kansas, USA (the color photos and plates
of fossil bees, etc.);
Molly G. Rightmyer, Lawrence, Kansas, USA (Epeolini);
Allan H. Smith-Pardo, Lawrence, Kansas, USA (Augochlorini);
Michael Terzo, Mons, Belgium (Ceratina).
I especially appreciate the contribution of “Key to the Subgenera of Centris” by Ricardo Ayala, Estacion Chamela, Instituto de Biologia, Universidad Nacional Autonama de México, Ciudad de México.
I also appreciate the careful typing and editing by Anna J. Michener.

Lawrence, Kansas
July 18, 2006

x


Preface to the First Edition

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 information on adults and larvae of various groups has not been fully developed 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 research 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 overtake the former. I conclude, then, that in spite of dynamic current activity 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 looking 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 insect 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
as a bee for several years; it was a puzzle and a frustration and through it I
xi


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 identify 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, California, 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 summer (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 undergraduate 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 dissertation (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 commission in the Army, my research efforts were taken up largely with Lepidoptera 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 orchid flowers. In 1948 I moved to the University of Kansas, and since
about 1950 almost all of my research has been on bees.
xii


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 social organization of bees, with emphasis on primitively social forms and
on the origin and evolution of social behavior. With many talented graduate students to assist, this went on until 1990, and involved the publication 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 Australia, 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 freedom to build up a major collection of bees as part of the Snow Entomological 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 contributed 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 detailed 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 indication 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 (Anthophorini, 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, Halictini); H. H. Dathe, Eberswalde, Germany (palearctic Hylaeinae); Connal 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. Griswold, Logan, Utah, USA (Osmiini, Anthidiini); Terry F. Houston,
Perth,Western Australia (Hylaeinae, Leioproctus); Wallace E. LaBerge,
Champaign, Illinois, USA (Andrena, Eucerini); G. V. Maynard, Canberra, ACT, Australia (Leioproctus); Ronald J. McGinley, Washington
xiii


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 RoigAlsina, Buenos Aires, Argentina (phylogeny, Emphorini, Tapinotaspidini, 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 (Coelioxys); Roy R. Snelling, Los Angeles, California, USA (Hylaeinae); Osamu Tadauchi, Fukuoka, Japan (Andrena); Harold Toro, Valparaíso,
Chile (Chilicolini, Colletini); Danuncia Urban, Curitiba, Paraná, Brazil
(Anthidiini, Eucerini); Kenneth L. Walker, Melbourne, Victoria, Australia (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 completion 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 permitted 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 Camargo 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 indicated 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
Westrich for making available their excellent photographs. It is worth
xiv


noting here that many other superb photographs by Westrich were published 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, publications 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 acknowledged in the text. Several persons, however, have contributed previously 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 Boulevard, 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 authors would scarcely recognize them. I have identified them by expressions 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 except when required by editors. But in this book, which is largely a systematic 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.
Lawrence, Kansas

1999

xv


abbreviations
The following are used in the text:
BP = before the present time
Code = International Code of Zoological Nomenclature
Commission = International Commission on Zoological
Nomenclature
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.

xvi


The Bees of the World

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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 animals; some bees are also social. Their interactions and
communications, which make their colonial life function, 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 humans. For a biologist or natural historian, bees are also fascinating 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 return to them; their architectural devices, which permit
food storage, for example, in warm, moist soil full of bacteria and fungi; and their ability to rob the nests of others, some species having become obligate robbers and
others cuckoolike parasites. These are only a few of the interesting things that bees do.
I consider myself fortunate to work with such a biologically diverse group of insects, one of which is the common honey bee, Apis mellifera Linnaeus. In terms of physiology and behavior, it is the best-known insect. Educated
guesses about what happens in another bee species are often possible because we know so much about Apis mellifera. 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 concerns bees (the great majority) that are not social.
Sections 2 to 28, and what follows here, are intended

to provide introductory materials important to an understanding of all bees and aspects of their study. Some
topics are outlined only briefly to provide background information; 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, subfamilies, tribes, genera, and subgenera are characterized by
means of keys and (usually brief ) text comments to facilitate identification. I include many references to such revisional papers or keys as exist, so that users can know
where to go to identify species. About 17,500 species have
been placed as to genus and subgenus (see Sec. 16); no attempt has been made even to list species here, although
the approximate number known for each genus and sub-

genus is given in Table 16-1, as well as under each genus
or subgenus in Sections 36 to 121. Aspects of bee biology,
especially social and parasitic behavior, nest architecture,
and ecology, including floral associations, are indicated.
Major papers on bee nesting biology and floral 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 family, and
because they are often complex and difficult to describe,
numerous illustrations are included, as well as references
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 information on the diversity of bees and their classification and
identification, this book will in some mostly indirect ways
contribute to pollination biology.
To a significant degree, studies of bees, especially nontaxonomic studies, have developed in Russia more or less
independently from those in the rest of the world. It is fortunate, therefore, that a huge list of publications by Russian authors and others in the former U.S.S.R., with summaries in English, has recently been published (Pesenko
and Astafurova, 2003). This large work, covering the period from 1771 to 2002 provides information on 3,027
publications by 1,126 authors. Michener (2000) and
many earlier works utilized the publications in Russian
on bee systematics and the like; it is especially in pollination biology, ecology, nesting behavior, and related fields
that much Russian work has been little known in the
West.
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 managed colonies of Apis mellifera Linnaeus and A. cerana
Fabricius, are excluded. The findings about sensory physiology as well as behavioral interactions, including communication, foraging behavior, and caste control are virtually 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 under 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 themselves melittologists and their field of study melittology.
1


2

THE BEES OF THE WORLD

I would include under the term “melittology” the taxonomic, 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 glossary. 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 included 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 accordingly.


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 usually 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 coloration. Bees differ from nearly all wasps in their dependence on pollen collected from flowers as a protein source
to feed their larvae and probably also for ovarian development 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 recognized by a number of characters, of which two are the
most conspicuous: (1) the posterior pronotal lobe is distinct but rather small, usually well separated from and below 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 (or apoid) wasps, or Spheciformes,
and the bees, or Apiformes (Brothers, 1975). Older authors also used the term Anthophila for the bees and the
name was resurrected by Engel (2005); Apiformes is a junior synonym of Anthophila. No priority rules govern
such names. I prefer Apiformes because it contrasts well
with Spheciformes and because the word itself makes its
meaning immediately clear. Structural characters 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 general longer than
that of most sphecoid wasps. The details, and other characteristics of bees, are explained in Section 12.
A conveniently visible character that easily distinguishes 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 sphecoid wasps such as the Pemphredoninae.
The monophyletic Apiformes is believed to have arisen
from the paraphyletic Spheciformes. Monophyletic is
used here in the strict sense sometimes called Holophyletic. 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 Paraphyletic also arose from such an ancestor but
do not include all of the derived taxa. Brief explanations
of other terms used by systematists are appended to Section 12.

3


3. The Importance of Bees
Probably the most important activity of bees, in terms of
benefits to humans, is their pollination of natural vegetation, 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 important 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 preservation and reproduction may be essential in preventing
erosion and other problems, and in providing food and

cover for wildlife. Conservation of many habitats thus depends 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, beepollinated populations is thus important for the genetic
diversity needed to improve the cultivated strains. Garden 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 produce fruit. Others, commonly bee-pollinated, can selfpollinate 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 pollination. 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 estimate 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 decrease 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 various crops for which honey bees are poor pollinators compared to wild bees. Examples of wild bees already commercially used are Osmia cornifrons (Radoszkowski),
which pollinates fruit trees in Japan; Megachile rotundata
(Fabricius), which pollinates alfalfa in many areas; Bom4

bus terrestris (Linnaeus), which pollinates tomatoes in European 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 Tepedino (1987), Torchio (1991), and Richards (1993).
Since honey bees do not sonicate tubular anthers to obtain 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 eggplants, 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. Therefore, anyone investigating the importance of wild bees as
pollinators needs to know about kinds of bees. The classification presented by this book can suggest species to
consider; for example, if one bee is a good legume pollinator, a related one is likely to have similar behavior. Proboscis length is an important factor in these considerations, 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.
Although some bees, e.g., Euglossini and many
Meliponini, inhabit undisturbed forests, especially in the
tropics, many and probably most bee species inhabit savannas and forest margins and thrive in moderately disturbed areas. Temperate forests were presumably never
good places for most bees since they consist largely of trees
that do not produce flowers visited by bees. There were
probably fewer bees in primeval temperate forests than
now inhabit the same areas. Now, with pastures, waste
lands, road and field margins, and forests that have been
opened by cutting, once scarce species of bees have become abundant and presumably play important roles as
pollinators of the vegetation. Even unbroken prairie appears to have fewer bees than more or less abandoned disturbed areas. Thus Laroca (1983) found more species and
individuals in a little used, often disturbed university
campus area, not planted with lawn or other vegetation,
than in nearby prairie in Kansas. Of course the bees in
such areas are the species that may pollinate agricultural
crops or ornamental plants and, therefore, may be selected for practical use as pollinators.
Although disturbed areas often have more bees than

undisturbed areas, it does not follow, of course, that the
more disturbance, the better for the bees. When a whole
area becomes a monoculture of corn or any other crop,
most bees become dependant on small waste areas or road
verges, and with small isolated populations, the number
of species and individuals will soon be reduced.
In many countries the populations of wild bees have
been seriously reduced by human activity. Destruction of
habitats supporting host flowers, destruction of nesting
sites (most often in soil) by agriculture, roadways, etc.,
and overuse of insecticides, among other things, appear
to be major factors adversely affecting wild bee popula-


3. The Importance of Bees

tions. Introduction or augmentation of a major competitor for food, the honey bee, has probably also affected
some species of wild bees. Recent accounts of such problems and some possible solutions were published by
Banaszak (1995) and Matheson et al. (1996); see also
O’Toole (1993).
National and international organizations are now seriously considering and publicizing the need to conserve
native pollinators (mostly bees) to maintain agricultural
production as well as survival and well-being of native
vegetation. Recent accounts of pollination problems
worldwide have been included in numerous reports; see
Kevan and Imperatriz-Fonseca (2002) and Freitas and
Pereira (2004).
A single example analyzing the economic impact of
bees (Apis and Meliponini) on a 1,065-hectare coffee
plantation (this crop does not even require insect pollination) is telling. Bees from two forest fragments (46 and

5

111 hectares) translated into ϳUS$60,000 per year
added income for the farm (Ricketts et al., 2004). Another relevant work is Imperatriz-Fonesca, Saraiva, and
De Jong (2006). A useful bibliography for the neotropics
is Anonymous (2006).
One of the problems in verifying recent declines of pollinating insects has always been lack of firm quantitative
data on abundance in times past. Collectors’ recollections
and museum specimens suffice for presence (and even absence) information, but not for changes in abundance. A
recent study (Biesmeijer et al., 2006) in The Netherlands
and United Kingdom, however, compares older (before
1980) versus recent (after 1980) data and shows substantial declines in local bee diversity, in particular, declines
of oligolectic and other specialist species, and parallel declines in plant species dependent for pollination services
on such bees.


4. Development and Reproduction
As in all insects that undergo complete metamorphosis,
each bee passes through egg, larval, pupal, and adult
stages (Fig. 4-1).
The haplodiploid system of sex determination has had
a major influence on the evolution of the Hymenoptera.
As in most Hymenoptera, eggs of bees that have been fertilized develop into females; those that are unfertilized develop into males. Sex is controlled by alleles at one or a
few loci; heterozygosity at the sex-determining locus (or
loci) produces females. Development without fertilization, i.e., with the haploid number of chromosomes, produces males, since heterozygosity is impossible. Inbreeding results in some diploid eggs that are homozygous at
the sex-determining loci; diploid males are thus produced. Such males are ordinarily reproductively useless,
for they tend to be short-lived (those of Apis are killed as
larvae) and to have few sperm cells; moreover, they may
produce triploid offspring that have no reproductive potential. Thus for practical purposes the sex-determining

mechanism is haplodiploid.
When she mates, a female stores sperm cells in her
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 female-producing eggs in large cells with more provisions,
male-producing eggs in small cells. In Apis, the males of
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-producing eggs in cells near the entrance, from which the resultant adults can escape without disturbing the slowerdeveloping 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
care and attention to their few offspring by nest-site selection, 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 Lithurgus, within) the food mass provided for larval consumption. In bees that feed the larvae progressively (Apis, Bombus, and most Allodapini), however, the eggs are laid with
little or no associated food. Eggs are commonly of moderate size, but are much smaller in highly social bees,
which lay many eggs per unit time, and in Allodapula (Allodapini), which lays eggs in batches, thus several eggs at
about the same time. Eggs are also small in many cleptoparasitic bees (see Sec. 8) that hide their eggs in the
6

brood cells of their hosts, often inserted into the walls of
the cells; such eggs are often quite specialized in shape and
may have an operculum through which the larva emerges
(see Sec. 8). Conversely, eggs are very large in some subsocial or primitively eusocial bees like Braunsapis (Allodapini) and Xylocopa (Xylocopini). Indeed, the largest of
all insect eggs are probably those of large species of Xylocopa, which may attain a length of 16.5 mm, about half
the length of the bee’s body. Iwata and Sakagami (1966)
gave a comprehensive account of bee egg size relative to
body size.
The late-embryonic development and hatching of eggs

a

c
b

d

e

f

Figure 4-1. Stages in the life cycle of a leafcutter bee, Megachile
brevis Cresson. a, Egg; b-d, First stage, half-grown, and mature larvae; e, Pupa; f, Adult. From Michener, 1953b.