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
595.79Ј9—dc21
99-30198 CIP
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



Contents

Preface ix
New Names xiv
Abbreviations xiv
1.
2.
3.
4.
5.
6.
7.
8.
9.

10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.

About Bees and This Book 1
What Are Bees? 2
The Importance of Bees 3
Development and Reproduction 4
Solitary versus Social Life 9
Floral Relationships of Bees 13
Nests and Food Storage 19
Parasitic and Robber Bees 26
Body Form, Tagmata, and Sex
Differences 38
Structures and Anatomical Terminology
of Adults 40
Structures and Terminology
of Larvae 53
Bees and Sphecoid Wasps as a Clade 54

Bees as a Holophyletic Group 55
The Origin of Bees from Wasps 58
Classification of the Bee-Sphecoid
Clade 60
Bee Taxa and Categories 61
Methods of Classification 71
The History of Bee Classifications 72
Short-Tongued versus Long-Tongued
Bees 78
Phylogeny and the Proto-Bee 83
The Higher Classification of Bees 88
Fossil Bees 93
The Antiquity of Bee Taxa 94

24.
25.
26.
27.
28.
29.
30.
31.
32.
33.
34.
35.
36.
37.

48.

Diversity and Abundance 96
Dispersal 99
Biogeography 100
Reduction or Loss of Structures 104
New and Modified Structures 106
Family-Group Names 111
Explanation of Taxonomic Accounts
in Sections 36 to 119 112
Some Problematic Taxa 114
The Identification of Bees 115
Key to the Families, Based on Adults 116
Notes on Certain Couplets in the Key
to Families (Section 33) 120
Practical Key to Family-Group Taxa,
Based on Females 121
Family Stenotritidae 123
Family Colletidae 126
38. Subfamily Colletinae 130
39. Subfamily Diphaglossinae 164
40. Tribe Caupolicanini 165
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
Family Andrenidae 225
49. Subfamily Alocandreninae 228

50. Subfamily Andreninae 229
51. Subfamily Panurginae 260
52. Tribe Protandrenini 262
vii


59.

66.

73.

83.

53. Tribe Panurgini 273
54. Tribe Melitturgini 278
55. Tribe Protomeliturgini 281
56. Tribe Perditini 282
57. Tribe Calliopsini 292
58. Subfamily Oxaeinae 301
Family Halictidae 304
60. Subfamily Rophitinae 307
61. Subfamily Nomiinae 317
62. Subfamily Nomioidinae 330
63. Subfamily Halictinae 333
64. Tribe Halictini 339
65. Tribe Augochlorini 377
Family Melittidae 396
67. Subfamily Dasypodainae 399
68. Tribe Dasypodaini 400

69. Tribe Promelittini 405
70. Tribe Sambini 406
71. Subfamily Meganomiinae 409
72. Subfamily Melittinae 412
Family Megachilidae 417
74. Subfamily Fideliinae 419
75. Tribe Pararhophitini 420
76. Tribe Fideliini 421
77. Subfamily Megachilinae 424
78. Tribe Lithurgini 427
79. Tribe Osmiini 431
80. Tribe Anthidiini 474
81. Tribe Dioxyini 521
82. Tribe Megachilini 526
Family Apidae 570
84. Subfamily Xylocopinae 575
85. Tribe Manueliini 577
86. Tribe Xylocopini 578
87. Tribe Ceratinini 593
88. Tribe Allodapini 600

Color plates follow page 32.

viii

89. Subfamily Nomadinae 614
90. Tribe Hexepeolini 618
91. Tribe Brachynomadini 620
92. Tribe Nomadini 624
93. Tribe Epeolini 627

94. Tribe Ammobatoidini 633
95. Tribe Biastini 636
96. Tribe Townsendiellini 639
97. Tribe Neolarrini 640
98. Tribe Ammobatini 641
99. Tribe Caenoprosopidini 646
100. Subfamily Apinae 647
101. Tribe Isepeolini 652
102. Tribe Osirini 654
103. Tribe Protepeolini 658
104. Tribe Exomalopsini 660
105. Tribe Ancylini 665
106. Tribe Tapinotaspidini 667
107. Tribe Tetrapediini 674
108. Tribe Ctenoplectrini 676
109. Tribe Emphorini 679
110. Tribe Eucerini 686
111. Tribe Anthophorini 720
112. Tribe Centridini 731
113. Tribe Rhathymini 739
114. Tribe Ericrocidini 740
115. Tribe Melectini 747
116. Tribe Euglossini 754
117. Tribe Bombini 761
118. Tribe Meliponini 779
119. Tribe Apini 806
Literature Cited 809
Addenda 871
Index of Terms 873
Index of Taxa 877

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 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
ix


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.
x


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
xi


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
xii


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.

xiii


 

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.

xiv

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 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 even 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 16,000 species have
been placed as to genus and subgenus (see Sec. 16); no attempt 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 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.
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.
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.
1


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

2

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 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 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 Paraphyletic also arose from such an ancestor but do not include 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 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, Bombus 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.
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, appear to be major factors adversely affecting wild bee populations. 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).

3

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
4

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.


4. Development and Reproduction

has proved to be variable among bees and probably relevant to bee phylogeny. Torchio, in various papers (e.g.,
1986), has studied eggs of several different bee taxa immersed in paraffin oil to render the chorion transparent.
Before hatching, the embryo rotates on its long axis, either 90˚ or 180˚. In some bees (e.g., Nomadinae) the
chorion at hatching is dissolved around the spiracles, then
lengthwise between the spiracles; eventually, most of the
chorion disappears. In others the chorion is split but otherwise remains intact.
Larvae of bees are soft, whitish, legless grubs (Fig. 4-1bd). In mass-provisioning bees, larvae typically lie on the
upper surface of the food mass and eat what is below and
in front of them, until the food is gone. They commonly
grow rapidly, molting about four times as they do so. The
shed skins are so insubstantial and hard to observe that
for the great majority of bees the number of molts is uncertain. For the honey bee (Apis) there are five larval instars (four molts before molting into the pupal stage);
and five is probably the most common number in published reports such as that of Lucas de Olivera (1960) for
Melipona. In some bees, e.g., most nonparasitic Apinae
other than the corbiculate tribes (i.e., in the old Anthophoridae), the first stage remains largely within the
chorion, leaving only four subsequent stages (Rozen,
1991b); such development is also prevalent in the Megachilidae. In the same population of Megachile rotundata

(Fabricius) studied by Whitfield, Richards, and Kveder
(1987), some individuals had four instars and others five.
The first to third instars were almost alike in size in the two
groups, but the terminal fourth instar was intermediate in
size between the last two instars of five-stage larvae.
Markedly different young larvae are found in most
cuckoo bees, i.e., cleptoparasitic bees. These are bees
whose larvae feed on food stored for others; details are
presented in Section 8. Young larvae of many such parasites have large sclerotized heads and long, curved,
pointed jaws with which they kill the egg or larva of the
host (Figs. 82-5, 89-6, 103-3). They then feed on the
stored food and, after molting, attain the usual grublike
form of bee larvae.
Other atypical larvae are those of allodapine bees,
which live in a common space, rather than as a single larva
per cell, and are mostly fed progressively. Especially in the
last instar, they have diverse projections, tubercles, large
hairs, and sometimes long antennae that probably serve
for sensing the movements of one another and of adults,
and obviously function for holding masses of food and retaining the larval positions in often vertical nest burrows
(Fig. 88-6). Many of the projections are partly retracted
when the insect is quiet, but when touched with a probe
or otherwise disturbed, they are everted, probably by
blood pressure.
It has been traditional to illustrate accounts of bee larvae (unfortunately, this is largely not true for adults). The
works of Grandi (culminating in Grandi, 1961), Michener (1953a), McGinley (1981), and numerous papers by
Rozen provide drawings of mature larvae of many species.
Various other authors have illustrated one or a few larvae
each. Comments on larval structures appear as needed
later in the phylogenetic and systematic parts of this

book. Unless otherwise specified, such statements always

5

concern mature larvae or prepupae. Accounts of larvae are
listed in a very useful catalogue by McGinley (1989), organized by family, subfamily, and tribe. It is therefore unnecessary except for particular cases to cite references to
papers on larvae in this book, and such citations are
mostly omitted to save space.
As in other aculeate Hymenoptera, the young larvae of
bees have no connection between the midgut and the
hindgut, so cannot defecate. This arrangement probably
arose in internal parasitoid ancestors of aculeate Hymenoptera, which would have killed their hosts prematurely if they had defecated into the host’s body cavity. In
some bees defecation does not begin until about the time
that the food is gone; in others, probably as a derived condition, feces begin to be voided well before the food supply is exhausted. After defecation is complete the larva is
smaller and often assumes either a straighter or a more
curled form than earlier and becomes firmer; its skin is
less delicate, and any projections or lobes it may have are
commonly more conspicuous (Fig. 4-2). This last part of
the last larval stage is called the prepupa or defecated
larva; this stage is not shown in Figure 4-1. Most studies
of larvae, e.g., those by Michener (1953a) and numerous
studies by Rozen, are based on such larvae, because they
are often available and have a rather standard form for
each species; feeding larvae are so soft that their form frequently varies when preserved. Prepupae are often the
stage that passes unfavorable seasons, or that survives in
the cell for one to several years before development resumes. Houston (1991b), in Western Australia, recorded
living although flaccid prepupae of Amegilla dawsoni
(Rayment) up to ten years old; his attempts to break their
diapause were not successful. Such long periods of developmental stasis probably serve as a risk-spreading strategy so that at least some individuals survive through long
periods of dearth, the emergence of adults being somehow synchronized with the periodic blooming of vegetation. Even in nondesertic climates, individuals of some

species remain in their cells as prepupae or sometimes as
adults for long periods. Thus Fye (1965) reported that in
a single population and even in a single nest of Osmia
atriventris Cresson in Ontario, Canada, some individuals
emerge in about one year, others in two years.
Mature larvae of many bees spin cocoons, usually at
about the time of larval defecation, much as is the case in
sphecoid wasps. The cocoons are made of a framework of
silk fibers in a matrix that is produced as a liquid and then
solidifies around the fibers; the cocoon commonly consists of two to several separable layers. Various groups of
bees, including most short-tongued bees, have lost cocoon-spinning behavior and often are protected instead
by the cell lining secreted by the mother bee. Cocoon
spinning sometimes varies with the generation. Thus in
Microthurge corumbae (Cockerell), even in the mild climate of the state of São Paulo, Brazil, the cocoons of the
overwintering generation are firm and two-layered but
those of the other generation consist of a single layer of
silk (Mello and Garófalo, 1986). Similar observations
were made in California by Rozen (1993a) on Sphecodosoma dicksoni (Timberlake), in which larvae in one-layered cocoons pupated without diapausing, whereas those
in two-layered cocoons overwintered as prepupae. In


6

THE BEES OF THE WORLD

a

Figure 4-2. Change of a mature larva to a prepupa shown
by last larval stadium of Neff-

apis longilongua Ruz. a, Predefecating larva; b, Postdefecating larva or prepupa. (The
abdominal segments are numb

bered.) From Rozen and Ruz,
1995.

other cases, in a single population, some individuals make
cocoons and others do not. Thus in Exomalopsis nitens
Cockerell, those that do not make cocoons pupate and
eclose promptly, but those that make cocoons diapause
and overwinter (Rozen and Snelling, 1986).
When conditions are appropriate, pupation occurs;
for all eusocial species and many others this means soon
after larval feeding, defecation, and prepupal formation
are completed. In other species pupation occurs only after a long prepupal stage. Pupae are relatively delicate,
and their development proceeds rapidly; among bees the
pupa is never the stage that survives long unfavorable periods. Because they are delicate and usually available for
short seasons only, fewer pupae than larvae have been preserved and described. Pupal characters are partly those of
the adults, but pupae do have some distinctive and useful
characters of their own (see Michener, 1954a). Most conspicuous are various spines, completely absent in adults,
that provide spaces in which the long hairs of the adults
develop. Probably as a secondary development, long
spines of adults, like the front coxal spines of various bees,
arise within pupal spines.
Adults finally appear, leave their nests, fly to flowers
and mate, and, if females, according to species, either return to their nests or construct new nests elsewhere. Many
bees have rather short adult lives of only a few weeks.
Some, however, pass unfavorable seasons as adults; if such
periods are included, the adult life becomes rather long.
For example, in most species of Andrena, pupation and

adult maturation ccur in the late summer or fall, but the
resulting adults remain in their cells throughout the winter, leaving their cells and coming out of the ground in the
spring or summer to mate and construct new nests. In
most Halictinae, however, although pupation of reproductives likewise occurs in late summer or autumn, the
resulting adults emerge, leave the nest, visit autumn flowers for nectar, and mate. The males soon die, but the females dig hibernaculae (blind burrows), de novo or inside
the old nest, for the winter. A few bees live long, relatively
active adult lives. These include the queens of eusocial
species and probably most females of the Xylocopinae
and some solitary Halictinae. Among the Xylocopinae, a
female Japanese Ceratina in captivity is known to have
laid eggs in three different summer seasons, although only
one was laid in the last summer (for summary, see Michener, 1985b, 1990d). Females of some solitary Lasioglossum (Halictinae), especially in unfavorable climates (only
a few sunny days per summer month, as in Dartmoor, England) provision a few cells, stop by midsummer, and provision a few more cells the following year (Field, 1996).
Like the variably long inactivity of prepupae described
above, this may be a risk-spreading strategy.
The male-female interactions among bees are diverse;
they must have evolved to maximize access of males to receptive females and of females to available males. The
mating system clearly plays a major role in evolution. Reviews are by Alcock et al. (1978) and Eickwort and Ginsberg (1980); the following account lists only a few exam-


4. Development and Reproduction

ples selected from a considerable literature. Many male
bees course over and around flowers or nesting sites,
pouncing on females. In other species females go to particular types of vegetation having nothing to do with food
or nests and males course over the leaves, pouncing on
females when they have a chance. In these cases mating
occurs quickly, lasting from a few seconds to a minute or
two, and one’s impression is that the female has no choice;

the male grasps her with legs and often mandibles and
mates in spite of apparent struggles. The male, however,
may be quite choosy. In Lasioglossum zephyrum (Smith),
to judge largely by laboratory results, males over the nesting area pounce on small dark objects including females
of their own species, in the presence of the odor of such
females, but do so primarily when stimulated by unfamiliar female odor, thus presumably discriminating
against female nestmates, close relatives of nestmates, and
perhaps females with whom they have already mated
(Michener and Smith, 1987). Such behavior should promote outbreeding. Conversely, it would seem, males are
believed to fly usually over the part of the nesting area
where they were reared; they do not course over the whole
nesting aggregation (Michener, 1990c). Such behavior
should promote frequent inbreeding, since males would
often encounter relatives, yet they appear to discriminate
against their sisters. The result should be some optimum
level of inbreeding.
In communal nests of Andrena jacobi Perkins studied
in Sweden, over 70 percent of the females mated within
the nests with male nestmates (Paxton and Tengö, 1996).
Such behavior, with its potential for inbreeding, may be
common in communal bees. Given the rarity with which
one sees mating in most species of bees, it may be that
mating in nests is also common in some solitary species.
In species that have several sex-determining loci, inbreeding may not be particularly disadvantageous, because deleterious genes tend to be eliminated by the haploid-male system.
In some bees, females tend to mate only once. Males in
such species attempt to mate with freshly emerged young
females, even digging into the ground to meet them, as in
Centris pallida Fox (Alcock, 1989) or Colletes cunicularius (Linnaeus) (Cane and Tengö, 1981). In other species
females mate repeatedly. The behavior of males suggests
that there is sperm precedence such that sperm received

from the last mating preferentially fertilize the next egg.
Males either (1) mate again and again with whatever females they can capture, as in Dianthidium curvatum
(Smith) (Michener and Michener, 1999), or (2) remain
in copula for long periods with females as they go about
their foraging and other activities, thus preventing the females from mating with other males (many Panurginae,
personal observation).
In Colletes cunicularius (Linnaeus), Lasioglossum
zephyrum (Smith), Centris pallida Fox, and many others,
female-produced pheromones seem to stimulate or attract
males, but in Xylocopa varipuncta Patton a male-produced pheromone attracts females to mating sites (Alcock
and Smith, 1987). Some male Bombus scent-mark a path
that they then visit repeatedly for females (Haas, 1949). In
other species of Bombus, those with large-eyed males, the
males wait on high perches and dash out to passing objects
including Bombus females (Alcock and Alcock, 1983). Al-

7

though playing a role in all cases, vision is no doubt especially important also in other bees with large-eyed males,
such as Apis mellifera Linnaeus, the males of which fly in
certain congregating areas and mate with females that
come to those areas; see also the comments on mating
swarms of large-eyed males in Section 28.
Most male bees can mate more than once, but in
Meliponini and Apini the male genitalia or at least the endophallus is torn away in mating, so that after the male
mates he soon dies.
Males in many species of bees in diverse families have
enlarged and modified legs, especially the hind legs (see
Sec. 28), or broad heads with long, widely separated
mandibles. These are features that help in holding females

for mating, and may be best developed in large males.
Many males of Megachile have elaborately enlarged, flattened, pale, fringed front tarsi (Fig. 82-19). Wittmann
and Blochtein (1995) found epidermal glands in the
front basitarsi; at mating these tarsi hold the female’s antennae, or cover her eyes. This behavior and gland product are presumably associated with successful mating or
mate choice.
Large-headed males occur especially in some Andrenidae—both Andreninae and Panurginae—and in
some Halictinae. Large heads appear to be characteristic
of the largest individuals of certain species, no doubt as
an allometric phenomenon. In two remarkable examples,
one an American Macrotera (Panurginae) (Danforth,
1991b) and the other an Australian Lasioglossum (Chilalictus) (Halictinae) (Kukuk and Schwarz, 1988; Kukuk,
1997), the large-headed males (Figs. 4-3, 56-3, 56-4)
have relatively short wings and are flightless nest inhabitants in communal colonies. The large-headed males also
have large mandibles and fight to the death when more
than one is present in a nest. Smaller males of each species
have normal-sized wings and fly. Great size variation
among males and macrocephaly may be most frequent in,
or even limited to, communal species. Unlike most male
bees that leave the nest permanently and mate elsewhere,
short-winged males mate with females of their own
colony. Thus such a male is often the last to mate with a
female before she lays an egg.
In some other bees the male mating strategy also varies
greatly with body size. Large males usually fly about the
nesting sites, finding young females as they emerge from
the ground or even digging them out of the ground, presumably guided by odor. Small males seek females on
flowers or in vegetation near the nesting area. Such dual
behavior is documented for Centris pallida Fox (Alcock,
1989) in the Centridini, and for Habropoda depressa
(Fowler) (Barthell and Daly, 1995) and Amegilla dawsoni

(Rayment) (Alcock, 1996), both in the Anthophorini.
Such behavior seems akin to that of Anthidium manicatum (Linnaeus), in which large males have mating territories that include flowers visited by females (Severinghaus, Kurtak, and Eickwort, 1981), whereas small ones
are not territorial, and to that of certain Hylaeus (Alcock
and Houston, 1996), in which large males with a strong
ridge or tubercle on S3 are territorial whereas small ones
with reduced ventral armature or none are not territorial.
The ventral armature is apparently used to grasp an adversary against the thoracic venter by curling the metasoma.


8

THE BEES OF THE WORLD

b

a
c

e

d

An interesting and widespread feature in Hymenoptera is the prevalence of yellow (or white) coloration on
the faces of males. If a black species has any pale coloration at all, it will be on the face (usually the clypeus)
of males. Species with other yellow markings almost always have more yellow on the face of the male than on
that of the female, although on the rest of the body yellow markings often do not differ greatly between the
sexes. Groups like Megachile that lack yellow integumental markings frequently have dense yellow or white hairs
on the face of the male, but not on that of the female. In
mating attempts males usually approach females from
above or behind, so that neither sex has good views of the

face of the other. Therefore I do not suppose that the
male’s yellow face markings have to do with male-female
recognition or mating. Rather, I suppose that they are involved in male-male interactions, when males face one
another in disputes of various sorts. Sometimes, males of

Figure 4-3. Male morphs of Lasioglossum (Chilalictus) hemichal-

ceum (Cockerell) from Australia. a, Ordinary male; b, c, Heads of
same; d, Large, flightless male; e, Head of same. From Houston,
1970.

closely related species, such as Xylocopa virginica (Linnaeus) and californica Cresson, differ in that one (in this
case virginica) has yellow on the face but the other does
not. Someone should study the male-male interactions in
such species pairs. Presumably, male behavior linked to
yellow male faces is found in thousands of species of Hymenoptera.
Obviously, the variety of mating systems in bees deserves further study, both because of its interest for bee
evolution and for evolutionary theory. Moreover, because
of the frequency of morphological or chromatic correlates, mating systems and such correlates are important
for systematists.