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

  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 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 595.79⬘9—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

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   Contents

  

  

  

  

  

  

  

  

  

  

  

  

  

  

  

  

  

  

  

  

  

  

  

  

  

  

  

  

  

  

  

  

  

  

  

  

  

  

  

  

  

  

  

  

  

  

  

   ^{Color plates follow pages 46 and 78.}

  

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inevitably goes out of date as new findings or interpretations are made, and also as errors or omissions in the original book are discovered.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 edi-

tion, I have tried to cover literature through 2005, with additional mate-

rial 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 classifica-

tion should represent relationships, or similarities when phylogenetic re-

lationships are in doubt. A classification that emphasizes differences can

result in an unnecessary multiplication of taxa that (1) often can be dis-

tinguished only with difficulty or (2) represent odd derivatives whose re-

lationships are better represented by inclusion within the recognized groups. There is no doubt, however, that some of the taxa here syn- onymized 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 phylo-

genetic 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 consider-

ably, I usually report the study but, for the sake of stability, I do not change the classification. Changes in classifications as a result of clado- grams subject to major change are not justified, because stability is an important feature for classifications. We should change a classification

  

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 Cen-

tris” by Ricardo Ayala, Estacion Chamela, Instituto de Biologia, Univer-

sidad Nacional Autonama de México, Ciudad de México.

  

I also appreciate the careful typing and editing by Anna J. Michener.

  Lawrence, Kansas July 18, 2006

  

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

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

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

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

groups. The future will therefore see new phylogenetic hypotheses and

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

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

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

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

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

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

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

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

  

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

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

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

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

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

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

  

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

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

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

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

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

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

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

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

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

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

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

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

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

  

became more proficient in running small Hymenoptera, including bees,

through the keys in Comstock’s Introduction to Entomology.

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

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

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

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

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

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

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

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

Cockerell for checking. He returned them, with identifications corrected

as needed, and some specimens even identified to species.

  

Moreover, Cockerell wrote supporting comments about work on bees

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

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

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

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

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

  

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

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

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

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

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

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

Probably for this reason he was especially enthusiastic about my interest

and encouraged the preparation and publication of my first taxonomic

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

dergraduate work at the University of California at Berkeley.

  

As a prospective entomologist I was welcomed in Berkeley and given

space to work among graduate students. During my undergraduate and

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

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

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

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

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

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

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

  

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

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

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

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

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

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

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

  

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

biology, having devoted myself to systematics, comparative morphology,

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

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

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

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

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

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

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

my systematic studies continued; behavior contributes to systematics and

vice versa, and the two go very well together.

  

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

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

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

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

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

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

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

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

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

logical Division of the Natural History Museum, and provided excellent

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

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

Ashlock, and her manuscript preparation along with that of Joetta

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

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

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

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

California.

  

The help of numerous bee specialists is acknowledged at appropriate

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

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

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

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

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

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

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

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

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

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

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

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

  

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

  

The persons listed above contributed toward preparation or comple-

tion of the book manuscript, or the papers that preceded it, and also in

some cases gave or lent specimens for study; the following additional persons or institutions lent types or other specimens at my request: Josephine E. Cardale, Canberra, ACT, Australia; Mario Comba,

Cecchina, Italy (Tetralonia); George Else and Laraine Ficken, London,

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

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

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

  

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

  

The colored plates reproduce photographs from the two sources indi-

cated in the legends: Dr. E. S. Ross, California Academy of Sciences, San Francisco, California, USA, and Dr. Paul Westrich, Maienfeldstr. 9, Tübingen, Germany. I am particularly indebted to Drs. Ross and noting here that many other superb photographs by Westrich were pub- lished in his two-volume work on the bees of Baden-Württemberg (Westrich, 1989).

  Svetlana Novikova and Dr. Bu Wenjun provided English translations of certain materials from Russian and Chinese, respectively. Their help is much appreciated.

  The text has been prepared with the help of the bees themselves, pub- lications about them, and unpublished help from the persons listed above. I have not included here the names of all the persons responsible for publications that I have used and from which I have, in many cases, derived ideas, illustrations, bases for keys, and other items. They are ac- knowledged in the text. Several persons, however, have contributed pre- viously unpublished keys that appear under their authorship in this book. Such contributions are listed below, with the authors’ affiliations.

  “Key to the Palearctic Subgenera of Hylaeus” by H.H. Dathe, Deutsches Entomologisches Institut, Postfach 10 02 38, D-16202 Eberswalde, Germany. “Key to the New World Subgenera of Hylaeus” by Roy R. Snelling, Los Angeles County Museum of Natural History, 900 Exposition Boule- vard, Los Angeles, California 90007, USA. “Key to the Genera of Osmiini of the Eastern Hemisphere,” “Key to the Subgenera of Othinosmia,” and “Key to the Subgenera of Protosmia” by Terry L. Griswold, Bee Biology and Systematics Laboratory, UMC 53, Utah State University, Logan, Utah 84322-5310, USA. “Key to the Genera of the Tapinotaspidini” by Arturo Roig-Alsina, Museo Argentino de Ciencias Naturales, Av. A. Gallardo 470, 1405

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

  Several contributions became so modified by me that the original au- thors would scarcely recognize them. I have identified them by expres- sions such as “modified from manuscript key by . . .” Names of authors of species are not integral parts of the names of the organisms. In behavioral or other nontaxonomic works I omit them ex- cept when required by editors. But in this book, which is largely a sys- tematic account, I have decided to include them throughout for the sake of consistency.

  A measure of the success of this book will be the need for revision as new work is completed and published. Not only does this book contain a great deal of information about bees, but, by inference or explicitly, it indicates myriad topics about which more information is needed. I hope that it points the way for the numerous researchers who will take our knowledge beyond what is here included, and beyond what is to be found in the nearly 2,500 items in the Literature Cited.

  Lawrence, Kansas 1999

   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.

  The Bees of the World

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

  I consider myself fortunate to work with such a bio- logically diverse group of insects, one of which is the com- mon honey bee, Apis mellifera Linnaeus. In terms of phys- iology and behavior, it is the best-known insect. Educated guesses about what happens in another bee species are of- ten possible because we know so much about Apis mellif-

  era. In this book, however, Apis is treated briefly, like all

  other bee taxa, its text supplemented by references to books on Apis biology; the greater part of this book con- cerns bees (the great majority) that are not social.

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

  This book is largely an account of bee classification and of phylogeny, so far as it has been pieced together, i.e., the systematics of all bees of the world. All families, subfam- ilies, tribes, genera, and subgenera are characterized by means of keys and (usually brief) text comments to facil- itate identification. I include many references to such re- visional papers or keys as exist, so that users can know where to go to identify species. About 17,500 species have been placed as to genus and subgenus (see Sec. 16); no at- tempt 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 relation- ships 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 infor- mation 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 non- taxonomic studies, have developed in Russia more or less independently from those in the rest of the world. It is for- tunate, therefore, that a huge list of publications by Rus- sian authors and others in the former U.S.S.R., with sum- maries in English, has recently been published (Pesenko and Astafurova, 2003). This large work, covering the pe- riod 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 pollina- tion 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 man- aged colonies of Apis mellifera Linnaeus and A. cerana Fabricius, are excluded. The findings about sensory phys- iology as well as behavioral interactions, including com- munication, foraging behavior, and caste control are vir- tually omitted, although they constitute some of the most fascinating aspects of biology and in the hands of Karl von Frisch led to a Nobel prize. A major work, principally about communication, is Frisch (1967).

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

  Users of this book may wonder about the lack of a glos- sary. Definitions and explanations of structures, given mostly in Section 10, are already brief and would be largely repeated in a glossary. The terms, including many that are explained only by illustrations, are therefore in- cluded in the Index of Terms, with references to pages where they are defined, illustrated, or explained. Some terminology, e.g., that relevant only to certain groups of bees, is explained in other sections, and indexed accord- ingly. ^{2 T H E B E E S O F T H E W O R L D}

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

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

  As indicated above, the Apoidea are divisible into two groups: the sphecoid (or apoid) wasps, or Spheciformes, and the bees, or Apiformes (Brothers, 1975). Older au- thors also used the term Anthophila for the bees and the name was resurrected by Engel (2005); Apiformes is a ju- nior 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 char- acteristics of bees, are explained in Section 12.

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

  The monophyletic Apiformes is believed to have arisen from the paraphyletic Spheciformes. Monophyletic is used here in the strict sense sometimes called Holo-

  phyletic. 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 Sec- tion 12.

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

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

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

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

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

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

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

  Although some bees, e.g., Euglossini and many Meliponini, inhabit undisturbed forests, especially in the tropics, many and probably most bee species inhabit sa- vannas and forest margins and thrive in moderately dis- turbed 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 be- come abundant and presumably play important roles as pollinators of the vegetation. Even unbroken prairie ap- pears to have fewer bees than more or less abandoned dis- turbed 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 se- lected 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 tions. Introduction or augmentation of a major competi- tor for food, the honey bee, has probably also affected some species of wild bees. Recent accounts of such prob- lems and some possible solutions were published by Banaszak (1995) and Matheson et al. (1996); see also O’Toole (1993).

  National and international organizations are now seri- ously 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 polli- nation) is telling. Bees from two forest fragments (46 and

  111 hectares) translated into ⬃US$60,000 per year added income for the farm (Ricketts et al., 2004). An- other relevant work is Imperatriz-Fonesca, Saraiva, and De Jong (2006). A useful bibliography for the neotropics is Anonymous (2006).