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Home , Aglae, Apidae, Apinae, Austroplebeia, Bombini, Cephalotrigona

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9-21-1990

Classification of the ()

Charles D. Michener University of Kansas

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Recommended Citation Michener, Charles D., "Classification of the Apidae (Hymenoptera)" (1990). Mi. Paper 153. https://digitalcommons.usu.edu/bee_lab_mi/153

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I • • •_ ••^«_«).•>.• •.*.« THE UNIVERSITY OF KANSAS SCIENC5;^ULLETIN LIBRARY Vol. 54, No. 4, pp. 75-164 Sept. 21,1990 OCT 23 1990 HARVARD Classification of the Apidae^ (Hymenoptera) BY Charles D. Michener'^

Appendix: genalis Friese, a Hitherto Unplaced New Guinea

BY Charles D. Michener and Shoichi F. Sakagami'^ CONTENTS

Abstract 76 Introduction 76 Terminology and Materials 77 Analysis of Relationships among Apid Subfamilies 79 Key to the Subfamilies of Apidae 84 Subfamily Meliponinae 84 Description, 84; , 85; Nest, 85; Social Behavior, 85; Distribution, 85 Relationships among Meliponine Genera 85 History, 85; Analysis, 86; Biogeography, 96; Behavior, 97; Labial palpi, 99; Wing venation, 99; Male genitalia, 102; Poison glands, 103; Chromosome numbers, 103; Convergence, 104; Classificatory questions, 104 Fossil Meliponinae 105 Meliponorytes, 106; Kelneriapis, 106; Proplebeia, 106 Taxonomic Account of Recent Genera of Meliponinae 107 110 Genus 112

Plebeia s. str. 114 Subgenera , 113; , 113; , 114; , Genus 115

Genus 115 Genus 116 Genus 116 Genus 117 Genus 118 Genus 118 Genus Trigona 119 Subgenera Lepidotrigona, 121; Papuatrigona, 122; , 122; , 123; , 123; , 125; , 125; Homotngona, 125; Heterotrigona, 126; Trigona s. str., 127

'Contribution number 2031 from thk Department of ENTOMOLOcn. University of Kansas, Lawrence. ^Departments of Entomology and of Systematics & Ecology, and Snow Entomological Museum, University OF Kansas, Lawrence, Kansas 66045. ^KiTA-Ku, AiNos.ATO 1-JO 6-cHOME, 2-2-610 Sapporo, 002 Japan. 76 The University of Kansas Science Bulletin 128 Genus Trichotrigona 129 Genus Hypotrigona 129 Genus Pariotrigona 131 Genus Lisotrigona 131 Genus 132 Genus Liotrigona 132 Genus Cleptotrigona 133 Genus 134 Genus s. 137 Subgenera ^.v«/o/n^owa, \3\\ Meliplebeia, \35\ Me/iponula str., Genus Plebeina 137 138 Genus Dactylurina 138 Subfamily 140 Description, 138; Larva, 139; Nest, 140; Social behavior, 140; Distribution, Taxonomic Account of Apinae 140 140 Genus Apis 142 Subfamily Euglossinae Description, 142; Larva, 142; Nest, 142; Social behavior, 142 142 Relationships among Euglossine Genera History, 142; Analysis, 143 Taxonomic Account of Euglossinae 144 144 Genus 144 Genus 145 Genus Genus 145 Genus 145 Subfamily Bombinae 145 147 Description, 145; Larva, 147; Nest, 147; Social behavior, 147; Distribution, 148 Relationships among Bombine Genera and Subgenera 151 History, 148; Genitalia of the Bombinae, 150; Fossil Bombinae, Taxonomic Account of Bombinae 151 Genus Bombus 151 Genus 152 Acknowledgments 152 153 Appendix (Papuatrigona) Literature Cited 157 ABSTRACT

This is a review of the classification of the family Apidae. Alternative phylogenies for the are subfamilies are presented. The Meliponinae is considered in greatest detail; 21 genera worker recognized. Keys are provided for genera and subgenera. Male genitalic characters, little in the are sting rudiments, and worker palpal characters have been used past and incorporated in this work. An African group of genera that has been regarded as ancestral in of new the past is here considered to be derived from an American group genera. A Friese from subgenus, Papuatrigona Michener and Sakagami, is described for Trigona genalis New Guinea. The subfamilies Euglossinae, Bombinae, and Apinae are treated in less detail, but with keys to genera and synonymies.

INTRODUCTION

As This is an account of the classification of (bumble ), and Apinae (honey bees). the family Apidae in the sense of Michener explained by Sakagami and Michener to be the sister (1974), Sakagami and Michener (1987) and (1987), the Apidae appears many others. So understood, the Apidae group of the , which is currently includes four taxa here considered sub- usually included in the Anthophoridae. This will be when families: the Meliponinae (stingless honey arrangement probably changed of bees are bees), Euglossinae (orchid bees), Bombinae studies of the higher categories Classification of the Apidae 77

finished. If the Anthophoridae is then united of each subfamily and appear to be family with {\n- Apidae, the Apidae in the present characteristics. sense will probably beeome the subfamily Cephalic salivary glands present and Apinae, and the four current sublaniilies will lormed of many alveoli. In other families be tribes. The classification would then be these glands are tubular (sometimes locally that of Michener (1944). But for the time expanded) or absent (Cruz-Landim, 1967). being it is sufficient to note that the Apidae Hypopharyngeal glands attenuate, usu- in the present sense appears to be a holo- ally pedunculate, each discharging through a phyletic clade unless its complex poUen- single duct. In other families these glands manipulatiiig behavior and associated struc- are usually shorter, sessile, crowded against tures arose independently in two or more the hypopharyngeal plate or rods, the single subfamilies. This possibility seems unlikely duct at each side absent or hidden among the because of other synapomorphies. acini (Cruz-Landim, 1967). The following character states are well Thoracic salivary glands made up of known synapomorphies of the Apidae, al- short, simple tubes, quite distinct from col- though they have been lost in parasitic gen- lecting ducts; cells cubical and secretory era and in queens of highly social forms tubes formed by cuboid cells. In other fami- (Meliponinae and Apinae): Corbicula pre- lies the tubes are of diverse types but not as sent on outer surface of hind tibia in females. in the Apidae (Cruz-Landim, 1967, 1973). Rastellum (comb of setae across inner sur- Larva (except in Apis) with small, conical face of apex of hind tibia) present in females dorsolateral tubercles on at least the thoracic (weak in some Meliponinae). Hind basitar- segments (Michener, 1953). sus of female articulated near anterior end of In this paper the largest subfamily, Meli- apex of tibia. These character states are, of poninae, is treated in some detail because of course, associated with the -carrying new findings as to relationships within this and manipulation behaviors which are dis- group. The other subfamilies are treated in a tinctive for Apidae (Michener, Winston and more cursory way. Jander, 1978). Other synapomorphies of the TERMINOLOGY AND MATERIALS family are: Basitibial plate completely ab- sent. absent. Max- Pygidial plate completely The terminology used is that of Michener illary palpus reduced, one or two segmented. (1944) with some modifications. The word Nests usually constructed in large or irreg- is used for the thorax plus the propodeum, while ular cavities, cells built up rather than exca- segments 2-9 of the abdomen are referred to as 1-8 of the so that vated in the substrate. (In most other bees segments metasoma, segment numbers will conform to those used in almost all although not in many cells and taxonomic work on bees. It would be to burrows are excavated into a substrate. logical use the word mesosoma for the thorax plus the Sakagami [1966] has pointed out that the propodeum, but no confusion results from use of ability to excavate in substrates, so obvious the shorter and more familiar word, thorax. in is absent in Anthophoridae, virtually Api- Confusion as to segment numbering would result dae. This is a presumably synapomorphy, if the word abdomen were to be used instead of Bombinae although and Meliponinae often metasoma, because the propodeum is the first enlarge subterranean cavities and young abdominal segment. The abbreviations Tl, etc., queens of the former excavate hibernacula in and SI, etc., refer to metasomal terga and sterna number. The term basal area is the soil.) by of propodeum as a Listed below are other character states continued, convenience, even though the area most of the that show that the four subfamilies of Apidae triangular (which comprises basal area in Apidae) is apparently the metapost- are related to one another, i.e., that no one notum (Brothers, 1976). (The triangular area is of them is an anthophorid group that has vaguely defined if recognizable at all in Apidae; convergently evolved the external features of loss of the lines demarking the triangle also occurs These characters suffer from not Apidae. in certain other bees.) been examined in having many species; yet The word keirotrichia (introduced by Michener, have they been examined in various species 1981: 4) is used for the small hairs of uniform 78 The University of Kansas Science Bulletin length, blunt or (in other families of bees) briefly Meliponinae commonly have strong setae arising from distinct bifid or spatulate, occupying part of the inner bases. In some genera there are surface of the hind tibia. The area occupied, the also, or instead of such setae, minute hairs. These are keirotrichiate area, is of great importance in the consistently much smaller than the setae and classification of Meliponinae. Unfortunately distinctive setal bases are invisible at a magnifica- nothing is known about the function of these tion of 160 X . hairs. The male genitalia of Meliponinae sometimes Several special terms are associated with the have the gonocoxites opening basad, in a more or pollen carrying and manipulating structures of less straight line across the base of the genital Apidae. All are unique to females of the family capsule, as in most other bees. However, in some (see Introduction, above) or to parts of the family. genera and in some preparations of others the They are absent in most parasitic or robber ta.xa, capsule is split longitudinally from the base by a and in queens of highly social bees. The corbicula V-shaped incision and the gonocoxites open is the smooth, concave or sometimes flat area, mesad along the arms of the V. To avoid repeated surrounded by long hairs, on the outer surface of wordy descriptions, I call the former rectigonal, the the hind tibia. The rastelhnn is the comb of strong, latter, schizogonal, and forms believed able to usually blunt tipped bristles across the inner exhibit both conformations are called amphigonal. surface of the apex of the hind tibia (Fig. 184). It The matter is discussed in greater detail under is reduced to ordinary hairs in some Meliponi- the subfamily Meliponinae. nae; I have described it in such cases as a The uses of certain other descriptive terms are rastellum made up of hairs, or tapering (pointed) indicated in the accounts of characters in Tables 1 hairs. I could have said "rastellum absent" but and 2. since there are all degrees of reduction, it is hard Except as otherwise indicated in the text, and to say at what point such a comment would be except for some "subgenera" of Bombus and appropriate. The auricle is the posterior expansion Psithyrus, specimens of the type species of each of the base of the hind basitarsus for pushing named supraspecific taxon (whether or not rec- pollen up into the corbicula. It is absent in ognized as distinct) were examined. In the Meli- Meliponinae. The penicillum is a compact tuft of poninae, the worker sting apparatus provides strong bristles arising near the front of the apical useful characters. The sting and associated struc- margin of the hind tibia, usually directed posteri- tures were removed, usually with part of the orly, sometimes almost parallel to the apical tibial metasoma, from relaxed specimens and placed margin (Fig. 184). It is found only in Meliponi- for a few hours in a 10% solution of KOH at nae. The anterior and posterior parapenicilla are room temperature. Meliponines are weakly scle- groups of bristles arising at the anterior and rotized; prolonged treatment and high tempera- posterior apical angles, respectively, of the hind ture are not desirable. After passage through tibia of some Meliponinae. There are always hairs acidulated (with acetic acid) water and dissection in these positions; how coarse they must be to be as needed to reveal the structures, the material called parapenicilla is a matter of judgment. The was placed in glycerin for study and eventually posterior parapenicillum is developed only in the for preservation, like male genitalia, in microvials genus Meliponula. The anterior parapenicillum is with the specimens from which they were taken. more widespread. Since these terms are difficult Mouthparts were similarly treated, sometimes to define, I have used them only sparingly. without KOH, and sometimes were preserved in I have described positions of structures on the glycerin jelly on slides. legs in the traditional way. Some authors advocate In my sketches of meliponine stings, the lateral standardization by considering all legs to project parts of the sting apparatus give only a general laterally from the body. The following tabulation impression of the first valvifer, base of the second shows equivalent terms for the hind tibia and valvifer, and their connections. These parts are basitarsus; I use those in the first column: weakly sclerotized, often difficult to see, and are outer surface anterior surface often curved away from the observer. A new inner surface posterior surface study, perhaps with uncleared material examined posterior margin upper margin at right angles to the plane in which the structures anterior margin lower margin lie, might reveal additional interesting characters. Following Plant and Paulus (1987), I use the By no means all species of each meliponine term brum in place of submentum as used by taxon were dissected, but divergent species of Michener (1944, 1985). each were dissected where possible. Males are The lengths of the jugal and vannal lobes of the unknown for many species and three genera. It is hind wing are both measured from the wing base often possible to verify major features of worker to the niost distal part of the lobe. The gonostyli gonostyli and sting stylets, and of lancets if they (third valvulae or sting sheaths) of workers in are long, by opening the apex of the metasoma of Classification of the Apidae 79

clear- for a relaxed speciiiu-n. without dissection and rite, synapomorphic ABE. But Xylocopa tor various to deter- ing. This was done species was the wrong outgroup; and other found in mine the consistency of character states small Xylocopinae, and most other long- material of related dissected species. tongued bees, have a delicate sclerite and the ANALYSIS OF RELATIONSHIPS strong sclerite in Xylocopa is probably related AMONG APID SUBKWIILIES to the strength of the proboscis in that genus. The strong sclerite in M is therefore an Rclationship.s among the four subfamilies, autapomorphy, not a plesiomorphy. Apinac (A). Bombinae (B), Euglossinae (E), Kimsey (1984) correctly points out that and Meliponinae (M), have been considered the loss of the basistipital process, as a for many years and are discussed in several synapomorphy of A B E as stated by Win- recent papers (Winston and Michener, 1977; ston and Michener (1977), is an error be- Kimsey, 1984; Plant and Paulus, 1987; A. cause the process is present in B E, as in M. VVeller, unpublished). The loss is therefore an autapomorphy of A. Unlike previous authors, I have ignored Kimsey (1984) described the sclerotic autapomorphies in this analysis. Although bridge below the foramen magnum (her autapomorphies are important in showing postgenal lobes) as showing similarity be- monophyly of the subfamilies, inclusion of tween B and E. It is true that in these two autapomorphies in a statistical analysis of groups the bridge is over half as wide as the it is narrower in relationships among subfamilies allows one foramen magnum whereas to maximize the consistency index and thus A; in M it is also usually narrow but is improve the apparent strength of the analy- variable, so that I have chosen to ignore this In all four sis without really adding information on feature for present purposes. relationships among taxa. Each subfamily is subfamilies the bridge includes a lightly scle- quite distinctive and numerous autapomor- rotized invagination, well illustrated for M phies could be listed, fewer for B than for the by Camargo, Kerr, and Lopes (1967, pi. B). other three. Partly because the subfamilies When the bridge is broad the invagination is are so diflierent from one another, largely large, especially so in E, but in no species because of autapomorphies, structure in the that I have seen is the lower part of the relationships among them has been hard to bridge incomplete as illustrated by Kimsey establish. for E. Plant and Paulus (1987) also did not Table 1 is a list of actual or potential consider this character state as a synapomor- synapomorphies that vary among sub- phy. families of Apidae. The apomorphous condi- The slender base of the hind basitarsus of tion (1) was recognized by comparison with workers of Meliponinae (Figs. 184-187), i.e., plesiomorphies (0) found in Manuelia (the the lack of an auricle in contrast to the other base group of Xylocopinae, probable sister three subfamilies of Apidae (Figs. 188, 189), group of the Apidae, Sakagami and Mich- seems at first to be a plesiomorphy because ener, 1987) and other Anthophoridae, specif- other families of bees also lack an auricle and basitarsal base. ically and . Condition have a relatively slender the (2), when present, is presumably derived However, in all pollen collecting Apidae distal from (1), so that the codes for the states are basitarsus arises from near the anterior ordered. angle of the tibia, i.e., from near the anterior A few supposed synapomorphies that have end of the apical tibial margin. In other seemed useful previously were omitted from families of bees the basitarsus arises nearer

Table 1 . The stipital sclerite of the maxilla the median axis of the tibia. After discussion (Winston, 1979; called the subgaleal sclerite with Michael Prentice of the University of by Winston and Michener, 1977) was found California, I believe it likely that the family to be strong with an anteriorly projecting characteristic of Apidae, anterior position of angle at each end in M (as in Xylocopa), but the hind tibiotarsal articulation, permitted relatively delicate in A B E. Because of development of the auricle by providing similarity to Xylocopa, the strong sclerite was space for it. The auricle was later lost in considered plesiomorphic, the delicate scle- ancestors of the Meliponinae when a differ- 80 The University of Kansas Science Bulletin ent pollen manuipulating device (involving the penicillum) evolved, although the posi- tion of the tibiotarsal articulation was re- tained. Loss of the auricle is therefore an autapomorphy at the subfamily level and is not included in the cladistic analysis. Of course if this interpretation is incorrect, the meliponine condition probably would be ple- relative to other and a siomorphic Apidae LENGTH 17 is sister strong indication that M the group C,L .76 of A B E. Larval apids are not particularly similar to Figure 1 . Dendrogram showing possible cladis- those of the outgroup, Xylocopinae, presum- tic subfamilies of latter have lost cocoon relationships among Apidae. ably because the = A = Apinae, B = Bombinae, E Euglossinae, and spinning behavior and correlated structures. M = Meliponinae. Length = total number of The larval mandibles of A M are weakly character state changes in 12 characters. CI = sclerotized, the or with fine apices simple consistency index. denticles. The larval mandibles of B E are robust, with considerable sclerotization, dae. have found other subfamilial without denticles but with a strong tooth on They characters, the details of which will the upper margins (Michener, 1953). Nei- they describe and illustrate. Of their characters I ther type of mandible occurs in the Xy- found to be useful and locopinae but mandibles similar in general eight particularly form to those of B E occur in various polarizable with some confidence, using the same that I used Anthophorinae. Nonetheless a decision as to outgroups previously. These are four characters of the which apid type is apomorphic is not clear, prosternum, which are one of the and I have chosen not to use this character in particularly strong, internal in front of the middle coxa, the cladistic analysis. The weak larval man- ridge two of the maxilla, and one of the dibles of A and M are quite different from phar- one another and their weakness could be yngeal plate. the convergent, not synapomorphic. Analysis using parsimony computer PAUP version 2.4 For cladistic analysis the synapomorphies program (Swofford, 1985) (hypothetical ancestor, all listed in Table 1 were plotted upon all pos- plesiomorphies) (for 12 characters) di- sible topologically different dendrograms for yielded my original the four subfamilies. Five of the results are chotomous trees like Figure 1 . However, for all 20 characters, the result was like 3. shown in Figures 1-5. The character states of Figure the four subfamilies are indicated in the PAUP version 3.0 gave two equally short trees for all 20 characters; one was di- same table by the initials (A, B, E, and M) chotomous like 1 the other had a indicated above. Figure , The total number of character state branching pattern like Figure 3 (tree length changes, i.e., dendrogram length, as well as 28, consistency index .786, retention index corresponding consistency indices, are indi- .714). cated in Figures 1-5. The calculations were I believe that the evidence is strong that made by the computer program McClade the A and M are sister groups, as indicated version 2.1 (Maddison and Maddison, 1987) by Figures 1 and 3. This is not in agreement using a hypothetical outgroup consisting of with the recent views of Winston and all the plesiomorphies. The most par- Michener (1977) and Kimsey (1984), who simonious tree is Figure 1, which corre- regarded M as the sister group to the clade of sponds to the traditional view of apid classifi- ABE, as in Figures 4 and 5. Some common cation (Michener, 1974). character states for A and M, i.e., states that Subsequently Michael Prentice and support the sister group relationship of these Howell V. Daly of the University of Califor- subfamilies, are losses. However striking, nia kindly sent me their as yet unpublished they might be independently evolved in A analysis of subfamilial relationships of Api- and M. Examples are: reduction of man- Classification of the Apidae 81

TABLE 1. Characters usc-d in rladistic analysis of subfamilies of Apidae. Distribution of character = = = = states is indicated thus: A Apinae; B Bombinae; E= Euglossinae; M Meliponinae. (0) the = plesiomorphous character state; (l) thc apomorphous alternative.

slender Character 1. Bodv size. (0) Small to middle-sized and often rather (A M). (1) Large and robust (B E). Polarization is based on the small size oi Manudia but since some anthophorids are large, it may be incorrect. In Character 2. Papillae on distal parts of wings. (0) Absent (A M). (1) Present (B E). various groups of bees, large sized taxa have e\olved, and they often (although not always) have papillate wings. There is no certainty that these character states are homologous in the large Apidae (B E). Moreover, since the as large body size and wing papillae are often associated, this character suffers from same problems character 1; neither is a strong character. Characters. Grooves and ridges on outer surface of mandible. (0) Present (Figs. 173, 174)(BE).(1) not to of Absent (Fig. 175), or in M with a single groove (Fig. 172) apparendy homologous grooves other bees (A M). A M are almost the only bees with greatly reduced mandibular grooves (Michener and Fraser, 1978). Therefore loss of grooves is likely to be homologous. However, as in all loss characters, convergence is possible and seems more likely because the highly social bees (A M) are the ones in which extensive nest structures of wax are made. Possibly relatively weak and more or less since these burrows grooveless mandibles are adequate for such work, especially bees do not excavate and cells. = B Plant Character 4. Mentum and "lorum" ( submentutn). (0) United (E). (1) Separated (A M). but and Paulus (1987) showed that these sclerites which have been regarded as primitively separate united in most bees (Michener, 1985) actually evolved in the opposite direction and are separated only in A B M. It appears to be a strong character. This reduction and Character 5. Arolia. (0) Present (A M). (1) Greatly reduced (B). (2) Absent (E). loss could have occurred independently, since arolia are lost in diverse groups of bees. The character states are ordered. and Character 6. Upper margin of main axis (basal part of malus) of strigilis. (0) Not expanded of and without an apical prong (Fig. 176) (M). (1) Expanded (anterior velum Schonitzer, 1986) ending in a short prong or lamella above the pointed apex of the malus (Fig. 177) (A B E). The expansion is weakly developed in some , , etc., but otherwise appears to be a synapomor- is was lost in and the phy for A B E. A distinct possibility, however, that the expansion M, polarity therefore reversed. is a it Character 7. Hind tibial spurs. (0) Present (B E). (1) Absent (A M). Since the apomorphy loss, might have arisen twice rather than once. Loss of tibial spurs is exceedingly rare in other bees, however. Character 8. Stigma. (0) Large, several times as long as prestigma (Figs. 162-171) (M). (1) Small, in such a wide of bees shorter than prestigma (Figs. 178-182) (A B E). Stigmal reduction occurs variety that there is no strong evidence of its homology in A B and E. Alternatively, enlargement of the stigma occurs in minute Hymenoptera (Danforth, 1989), perhaps including minute meliponines, so that the polarization shown here may be wrong. in so Character 9. First recurrent vein. (0) Longer, more oblique, not angulate or B moderately sometimes absent in This (Figs. 178-181) (B E). (1) Short and angulate (Figs. 162-171, 182), M (A M). veins character seems strong but may be in part related to size. As Danforth (1989) has shown, oblique tend to be more transverse (hence shorter) in small forms and more longitudinal (hence longer) in large is in A and M. forms. The angulation seems to remain as an indication that the condition^ homologous^ The states could have been considered as a developmental series from E B A M but evidence for vein in B is the origin of the short, angulate vein of A M from the longer and somewhat angulate lacking; I have therefore recognized only two states for this character. Absent Character 10. Jugal lobe of hind wing. (0) Present (Figs. 162-171, 182) (A M). (1) (Figs. E. it did not occur in 178-181) (B E). This loss could have occurred independently in B and However, the other bees. Plant and Paulus (1987) depreciate the loss as a synapomorphy, noting that in E jugal not that the lobe lobe is replaced by a row of brisdes. This is true, but the presence of bristles does show was not first lost. or so Character 11. Gonobase of male. (0) Well developed (Figs. 189, 190) (B E). (1) Absent nearly (Figs. 138-161, 183) (A M). or almost absent Character 12. S7 and 8 of male. (0) Well developed (B E). (1) Much reduced S8 (A M). Characters 11 and 12 involve reductions and losses that could have occurred independently, in these features. especiallv considering the great morphological differences between A and M However, loss of the gonobase is rare among bees and is therefore possibly homologous in the Apidae. 82 The University of Kansas Science Bulletin dibular grooves (3, Table 1), loss of hind Schonitzer, 1986) found on the velum of A B tibial E. spurs (7, Table 1), and reduction of An approach to such a structure occurs in hidden sterna and most male genitalia parts some anthophorids such as , al- in most bees it is (11, 12, Table 1). Some prosternal syn- though including Manuelia apomorphies, however, such as its slender simple. If Figures 1 and 3 represent the most body, large anterior region and anterolateral probable cladistic patterns, the strigilis of M processes, elongate groove instead of round probably represents a reversion. Likewise the of apophyseal pit, etc., are not loss features and large stigma M (8) seems to be seem unlikely to have evolved convergently. plesiomorphic relative to the reduced stigma Another such synapomorphy of A and M is of A B E, since large stigmata generally the broad pharyngeal plate with transverse characterize the more primitive bees, includ- (rather than longitudinal) fields of sensilla ing A/arzu^/w, etc. As is well known, however, (to be illustrated by Prentice and Daly). relative stigmal size is negatively correlated The choice between a cladistic pattern like with body size in aculeate Hymenoptera Figure 1 and a pattern like Figure 3 is not (Danforth, 1989). The reduced wing vena- tion of clear. To support the latter, one needs strong M suggests that this group originated synapomorphies for the clade ABM. The as minute bees, which may therefore have had an as a reversion that articulation of the lorum and mentum (4), enlarged stigma has been retained with reduced vena- unique among bees, is the only strong, along convincing character state of this sort, al- tion even in larger meliponines. Finally, the though one prosternal character state and slender base of the hind basitarsus of work- the lack of states of the mesepisternum (in front of coxa ers, i.e., an auricle, long seemed 2) and pharyngeal plate also support ABM to me an important plesiomorphy contrast- as a clade; these and others will be described ing with the unique synapomorphy, presence of and illustrated by Prentice and Daly. In an auricle, in A B E. For reasons dis- support of the alternative, the dichotomous cussed above I now regard loss of the auricle in to be an or reversion. pattern of Figure 1, are apparent syn- M autapomorphy apomorphies of B E. Body size and papillate These same comments apply to the Plant wings (1,2) perhaps are not polarized cor- and Paulus (1987) diagram of relationships rectly, and the presumed derived conditions (Fig. 2), except that in place of ABE, one appear repeatedly among other bees, so should read A B. might have arisen independently in B and E. A cladogram with M as the lowest branch to B Large size and papillate wings are often (sister group A E) seems reasonable because is correlated among bees. The great reduction we know that M old (; or loss of Michener and is the jugal lobe of the hind wing (10) Grimaldi, 1988a, b). M is unique among bees and thus strongly also the most widely distributed; in appro- supports the sister group relationship of B priate climatic zones it occurs worldwide. and The other three all E, although the actual condition is — subfamilies are geograph- rather different in the two subfamilies. Like- ically limited A to Eurasia and Africa be- wise, the great reduction in B and loss in E of fore being dispersed by man, B to the the arolium and associated structures (5) Holarctic, Oriental (montane) and Neotrop- supports the sister group relationship of ical regions, and E to the Neotropics. Such these taxa. Both of these are losses and of distributions might indicate groups less old than course could have evolved independently. M. Some apparent plesiomorphies appear in It will probably be possible to greatly M, their corresponding apomorphies char- increase the number of characters showing acterizing ABE. These are responsible for the similarities of large, robust taxa (B E) as the trees such as Figures 4 and 5, showing M opposed to the small bodied taxa (A M). For as the sister group for A B E, as advocated example, the lateral promotor of the mid by Winston and Michener (1979) and coxa in B E is V-shaped and the lower Kimsey (1984). One such character is (6), branch extends forward behind the second the simple main axis of the malus of the and third pleuroaxillary muscles. In A M strigilis in M, contrasted with the expanded this muscle is much smaller, not or scarcely lamella or prong (anterior velum of V-shaped, and does not extend so far for- Classification of the Apidae 83

LENGTH 23

C.I. .57

Figures 2-5. Dendrograms showing possible relationships among subfamilies of Apidae. Explana- tion as for Figure 1 .

ward (Wille, 1956). Likewise the dilator of decide on a classification that indicates struc- the salivary syringe has its origin below the ture among the four taxa. For this reason posterior lateral margin of the prementum in and because of their phenetic distinctness, I B E, on the anterior lateral margin in A M term them all subfamilies. Even if one of the (Wille, 1971); the latter condition is consid- cladograms were known to represent the ered derived by Wille. These internal char- truth, I see no reason to unite two or three of acters and characters 2, 8, and possibly 9, the taxa in a single subfamily since all four Table 1, are likely to be related to size and are so different from one another. robustness rather than phylogeny. There is, of course, considerable interest The number of plesiomorphies that unite in the question of whether the highly social B and E could be augmented, but the corre- behavior of A and M is homologous or sponding presumed apomorphies of A and convergent. If either of the hypotheses indi- M are not necessarily homologous. Besides cated by Figures 1 or 3 is correct, as is likely, characters 3, 7, 9, 11, and 12, such such behavior probably arose once. The plesiomorphies include (a) the form of the other three cladograms (Figs. 2, 4, 5) suggest penis valves, which are very divergently independent origin of highly social behavior modified in A and M; and (b) the presence of in the two subfamilies, a view supported by volsellae in the male (see discussion of Bom- Sakagami (1971), Winston and Michener binae), which are absent in A and M. Char- (1977) and Kimsey (1984). acters 11 and 12 are actually divisible into Unfortunately fossil Apidae as now known several such states that may have evolved do not help in the solution of the problems independently. discussed above. For most of them, anatom-

While 1 3 Figures and appear to represent ical details are not sufficiently well preserved the best cladograms, it is difficult to choose or described. The fossil Apidae have been between the It is two. therefore premature to reviewed by Zeuner and Manning (1976) 84 The University of Kansas Science Bulletin

with clear nae Zeuner and and and in part by Wille (1977). Those by Manning) Electrapis relations to existing subfamilies are dis- (with subgenera Protobombus and Roussyana, cussed under the subfamilies, below. Taxa ot placed in the Apinae by Zeuner and Man- to All these are from the Eocene Baltic greater interest, because they appear rep- ning). on is so well or resent extinct types that might shed light amber and none preserved studied that definitive is the relationships of the subfamilies, are Chal- placement possible. cobomhus, Sophrobombus (placed in Meliponi-

KEY TO THE SUBFAMILIES OF APIDAE labrum 1. Posterior tibial spurs absent; arolia present; jugal lobe of posterior wing present; three to four times as broad as long; marginal cell open or with veins narrow or evanescent to within one-third or less of distally or, if completely delimited by strong veins, reaching 2 its length from wing tip of —Posterior tibial spurs present; arolia greaUy reduced or absent; jugal lobe posterior wing absent or much reduced; labrum at most twice as broad as long; apex of marginal cell completely delimited by strong veins, separated from wing tip by a distance equal to at 3 least half length of cell broad 2. Marginal cell open (or its veins weak) distally (Figs. 162-171), tapering from base; second recurrent vein absent; stigma of moderate to large size, extending well beyond base exsertable of vein r; claws of female simple; sting reduced, not Meliponinae its recurrent vein — Marginal cell complete, parallel-sided for a large part of length; second minute, not base of vein r; claws cleft; sting well present; stigma" tapering beyond

developed . . Apinae 3. Proboscis reaching at least to base of metasoma in repose; scutellum produced tibiae of male posteriorly to a margin overhanging metanotum and propodeum; posterior usually swollen, always with a deep hairy fossa on apical half of posterior margin Euglossinae — Proboscis usually not reaching behind middle coxae; scutellum rounded posteriorly, overhanging metanotum but not propodeum; posterior tibiae of male neither swollen nor fossate Bombinae

SUBFAMILY MELIPONINAE Forewing with venation reduced {Figs. 162-171); mar- ginal cell often open apically, at least distal parts of its veins narrower than veins of basal These are the stingless honey bees found much near to moderate sized, vein in tropical and southern subtropical areas part stigma; stigma large r arising near middle; in Melipona stigma slender throughout the world (Roubik, 1989). They but in other genera stigma rather broad and are the social bees the true only highly except margin within marginal cell convex; prestigma honey bees, subfamily Apinae. There are short, often almost absent; second recurrent vein first recurrent vein, when short several hundred species, an approximation absent; present, and strongly angled near anterior end; first and to the real number being impossible because second submarginal cells, at most, weakly de- of the abundance of cryptic species, differing fined, third not defined, because of weakness or from their relatives only on the bases of absence of transverse cubital veins. Hind wing one half to one seemingly trivial characters. Most genera in with well developed jugal lobe third as as vannal lobe. flat, not most areas have not been adequately ana- long Clypeus protuberant. Maxillary palpus minute, one-seg- for of such forms; a lyzed recognition good mented, sometimes less than twice as long as wide start for of one is the part genus (Partamona) and extremely inconspicuous. Male S8 absent fine work by Camargo (1980). except for laterally compressed remnant of spicu- sclero- Description: Minute (1.8 mm long) to moderate lum (largest in Fig. 145); S7 flat, weakly sized (13.5 mm long), sparsely hairy or short tized and usually without large apodemes; S6 haired to moderately hairy bees. Eyes usually transverse, with lateral apodemes and usually ab- bare. Claws offemale simple; arolia present; hind tibial with median apical process. Male gonobase sent or narrow ribbon or weak spurs absent; strigilis without prong on anterior represented by side; hind basitarsus rather slender at base, with- lateral sclerites; gonostylus long, usually slender, out auricle; hind tibia of worker with penicillum. simple (presumably this is the upper gonostylus, Classification oi- thk Apidae 85

Hambali Inoue, Yamane, and the lower one being absent); penis valve large (1983); Sakagami, curved, Roubik and works with heavily selerotizeci, slender, tapeimg Salniah (1983); (1979, 1983); vulsella absent. are apex; spalha usually present; cited therein. Reviews by Sakagami (1982), structures re- Female with sting and associated greatly Wille (1983), and Michener (1974). duced (Figs. 9-48). Social behavior: This is one of the two groups of hitherto unrecorded ot Melipo- colonies A aiJoinorphy highly social bees, with "permanent" attention Ricardo is ninae, called to my by Ayala, and morphologically very different female castes the demarcation of the In most bees, preaxilla. (queens and workers). In contrast to the Apini, and numer- including other subfamilies of Apidae new nests are begun by workers going back and of the is ous groups anthophorids, preaxilla sepa- forth from an existing colony, carrying building surface of the mesoscutum rated from the dorsal materials and food. Ultimately a young queen a carina, immediately mesad and by strong supra-alar goes to the new site, workers stay there, is a that the scuto-scutellar to which groove joins independence from the old colony is gradually In suture posteriorly (Michener, 1944), Melipo- attained. Long distance dispersal by individual ninae the carina and groove is supra-alar adjacent reproductives or by swarms therefore impossi- The dorsal surface of the mesoscutum are absent. ble. Colony size ranges from a few dozen workers an is either separated from the preaxilla by angle to thousands. could be called a weak carina but is not raised) social behav- (it Distinctive aspects of meliponine onto the with a or it rounds preaxilla only change ior include oviposition rituals and communica- the of the in sculpturing to indicate upper margin tion concerning resources. These are discussed preaxilla. further in the next section, on relationships and an Camargo, Kerr, Lopes (1967) give among meliponine genera. of mar- excellent morphological account Melipona Distribution: This subfamily is found in the Wille (1983), not east of the ginata Lepeletier. Sakagami (1982), tropics of the world (except of and Roubik (1989) review biology Meliponi- in the Pacific). To the south it nae. extends into temperate regions (about 35°S in Larva: Without strong tubercles, but with and South America, 28°S in Africa). To conical, dark dorsolateral tubercles on first of small, the north it extends little beyond the Tropic three to ten segments. Mandible attenuate, body Cancer (23.5°N). apex blunt, concave on inner surface, margins and often apex denticulate but without large Genera teeth. Relationships among Meliponine Larvae are described and illustrated by Mich- History: The classification of stingless honey ener and Oliveira (1965). (1953) bees has been presented very difierently by Nest: The nests of most species occupy cavities different authors (see review by Sakagami, that the bees find, and may limit by walling off Schwarz and Michener (1944) unused areas, but the bees usually do little or no 1982). (1948) Meli- two principal genera, excavating. Some excavating is probably done by recognized only and Lestrimelitta was often rec- certain of the species that nest in the ground, and pona Trigona. establish robber is done by some species that regularly ognized as a distinct genus, lacking The cavities structures their nests in nests of Nasutitermes. pollen collecting and carrying used from small, an abandoned ceram- and and vary e.g., (e.g., by Schwarz, 1948) Meliponula to hollows in a tree trunk or status bycid burrow, large Dactylurina often received generic in the soil. Other however, do not Wille cavity species, by Wille and Michener, 1973). on tree (e.g., occupy cavities but make exposed nests (1979b) likewise recognized Trigona (with branches or on cliff faces. numerous and Melipona, but in are made of mixtures of wax secreted subgenera) Nests Dac- addition five small genera: Cleptotrigona, from the metasomal terga and resins and gums Lestrimelitta, Meliplebeia, and Melipo- collected by the bees. A few species add mud, tylurina, the nula. feces, or other materials to certain parts of elevated construct. Moure (1951, 1961), however, level and Cells are mass provisioned and either clustered many of the subgenera to the genus or arranged in combs which are usually horizon- described additional genera so that in 1961 tal. The cells horizontally) open upward (rarely he recognized 23 genera (no subgenera) after an is laid on the and are closed egg provi- from the Old World and 10 from the New sions. Food is stored in difierent from pots, quite World. In the New World, however, he of nest archi- and larger than brood cells. Details and 27 supraspecific taxa (genera tecture are dealt with by Schwarz (1948); Mich- recognized elevated some of Fletcher Moure (1971) ener (1961); Wille and Michener (1973); subgenera). inference others) to and Crewe (1981); Sakagami, Yaniane, and the subgenera (and by 86 The University of Kansas Science Bulletin

ol able. the taxa had been based on the genus level, making his classification Originally New World Meliponinae more nearly com- external characters of workers. addi- Table 2 is a list of characters with parable to that of the Old World. An syn- tional genus was added subsequently apomorphic character states. Autapomor- (Camargo and Moure, 1983). phies were not included in the computer Sakagami (1975, 1982) presented an in- analysis and most of them are not listed in termediate system, in some ways similar to Table 2. They are often numerous, however, that developed in the present study. and contribute to the recognition of taxa but Many of Moure's genera (based on exter- not to an understanding of their rela- nal characters of workers) seemed to me so tionships. similar that I saw no need to recognize them Using a character matrix based on the in the at the genus level, especially since some were characters 1-16 listed Table 2 and justified largely on the basis of a single PAUP 2.4 computer program (Swofford, character. Nonetheless, the male genitalia of 1985), a preliminary cladistic analysis of two of his externally similar genera, Liotri- supraspecific taxa was made. Six of the gona and Hypotrigona, turned out to be so characters had either three or four states. = different that I could not consider them PAUP options were as follows: Root = — congeneric (Brooks and Michener, 1988). ancestor; addseg. closest; swap global. Some details could not even be homologized. Some of the characters were polarized, as The sixth and seventh sterna were also very indicated within Table 2; others were not different, as were the gonostyli of the work- polarized for reasons stated in that Table. ers. These are all characters that can only be Bombus and Manuelia were used as out- revealed by dissection. On the basis of exter- groups, but the "ancestor" in the PAUP nal characters of workers. Brooks and Mich- computer analysis was artificial, consisting ener (1988) could not place certain species as of all the character states coded 0, i.e., to genus. plesiomorphic for the polarized characters. Analysis: In view of the situation described Usually because of similarity to other above, I reviewed all the supraspecific taxa, taxa, but sometimes because of lack of mate- examining the worker gonostyli and sting, rial (males not known), certain taxa were worker labial palpi (see Michener and Rou- omitted from the computer analysis. Of 52 bik, in press), as well as the male genitalia supraspecific taxa recognized by one or more and hidden sterna when males were avail- authors, 26 were included in the preliminary

TABLE 2. Characters used or considered in cladistic analyses of genera and subgenera of Meliponi- nae. Characters marked with asterisks were used in the generic analysis, after generic limits had been = determined. (0) the plesiomorphous character state; (1), (2), etc., indicate apomorphous alternatives in sequence such that (1) is thought to be derived from (0), (2) from (1), etc.

Character 1. Apical margin of mandible of worker (Fig. 172). (0) Most or at least lower half of mandibular margin edentate, usually one or two small teeth at upper end (or in the upper half) of margin. (1) With four or five teeth occupying entire margin. In other subfamilies of the Apidae the in other mandibular margin (at least of females) is partly edentate (Michener and Fraser, 1978) but bees with a broad mandibular margin (Xylocopinae, Megachilidae), it is usually dentate. This condition therefore could be plesiomorphic for the Meliponinae. This interpretation is supported by the fully toothed mandibular margin of the Cretaceous Trigona prtsca Michener and Grimaldi (1988a, b). However, a toothed mandibular margin is found in only two recent taxa, Trigona (Trigona) and Paratrigona, quite unrelated groups neither of which is near the base of the dendrogram derived later. This distribution suggests that a fully dentate mandibular margin may be a derived feature. Moreover, the presence in Meliponinae of the oblique mandibular groove, not homologizable with grooves of other bees, suggests that such mandibular features are basic for Meliponinae, with teeth developed later, as apomorphies not homologous to teeth of xylocopine or other bees. In summary, the polarity of this character is in doubt but probably multiple teeth are a derived feature. This character was not used teeth in the generic analysis (a) because of doubtful polarity; (b) because within Trigona multiple characterize only one, derived subgenus (for cladistic analysis involving a variable feature, one should use the plesiomorphic condition since the objective is to clarify basal connections, not evolution within Classification of the Apidae 87

teeth characterize the taxon); and (c) because as a generic character state, multiple only Paratrigona and are thus in effect an autaponiorphy. Character 2. Mandible of male. (0) With apiciil acute point and preapic al tooth on upper margin (Fig. 135), i.e., the apex of the pollex (see Michener and Fraser, 1978). I'his is the mandibular form of many bees, including Manuclia and Anthophora. (1) With apical point rounded, little exceeding pollex, the two separated by only a shallow emargination, or apex of mandible truncate, rounded, or rarely pointed (Fig. 136, 137). The supposedly plesiomorphic condition described above (0) is found among in the character state Meliponinae in Ih'potrigona. Ths character was not used generic analysis since (1) is either a unicjuely retained plesiomorphy or an autapomorphy o{ Hypntrigona. *Character 3. Scutellar fovea of worker. (0) Shining transverse depression on scutoscutellar line a simple. (1) Depression on scutoscutellar line extending posteriorly into scutellum on midline, forming V'-shaped or U-shaped fovea in scutellum (Fig. 190). Character state (1) is not found outside of the Meliponinae and is therefore no doubt a derived feature. It characterizes Nannotrigona and Scaptotrigona. *Character 4. Keirotrichia of worker. (0) Keirotrichia uniformly distributed (as in other subfamilies of Apidae) over wide area from premedian longitudinal ridge of tibia nearly to posterior margin of at a bare in Pleheia s. str. Keirotrichia tibia, leaving most narrow margin (as , Fig. 184). (1) leaving broad bare tibial margin (as in Hypotrigona). (2) Keirotrichia restricted to median longitudinal band on in all tibia (as in Trigona, Fig. 185). There is more or less a continuum between (0) and (2) but nearly cases there was no problem in assigning a species to one category or another, using the exemplars listed sort of tibia lack above. All other Apidae show state (0). Xylocopinae have a very different but bare zones comparable to those for states (1-2). The polarity indicated above can be questioned on the basis that the oldest fossil bee, the late Cretaceous Trigona prisca Michener and Grimaldi, has state (2). Moreover the Oligocene Proplebeia dorninicana (Wille and Chandler) has state (1). These findings are hardly decisive, however. *Character 5. Hind tibial cross-section of worker. (0) Inner surface of hind tibia flat from premedian longitudinal ridge (most elevated part of inner surface) to posterior margin (with or without hairless margin) as in other Apidae. (Anthophoridae have no bare margin.) (1) Inner surface of hind tibia with narrow depressed zone along posterior margin (as in Plebeia s. str., Fig. 184). (2) Inner surface of hind tibia with broad depressed posterior zone (as in Hypotrigona). (3) Inner surface of hind tibia with broad raised median longitudinal zone with keirotrichia, behind which the depressed smooth zone is often as 4 broad as the median ridge (as in Trigona, Fig. 185). This character is related to character but provides additional information. For example there are forms having character state (0) of character 4 but state fossils as for (1) of character 5. The polarity indicated above can be questioned on the basis of character in Pleheia 4. There is evidence that state (1) has arisen more than once or has reverted to (0). Thus (Scaura) timida (Silvestri) the condition is intermediate between (0) and (1), although its relatives have also exist. state (1) and in the distantly related genus Meliponula intermediate conditions Character 6. Fringe along posterior margin of hind tibia of worker. (0) Composed entirely of simple this character hairs (Figs. 184, 186, 187). (1) Including plumose hairs (Fig. 185). Polarization of remains uncertain, since plumose hairs are found in some other Apidae (Bombus) and on the equivalent tibial area of many Xylocopinae. However, the groups with such plumose hairs (Dactylurina and most the Trigona) are not basal in the dendrograms developed later, a finding that supports polarization indicated. (A few branched hairs are also found in Plebeina and some species oi Meliponula, and in two oi Plebeia. This character was not used in because a is a species ) generic analysis plumose fringe generic character state only for Dactylurina and thus would appear as an autapomorphy. Although plumose in that hairs are prevalent in Trigona, the presumably plesiomorphic alternative also exists genus and would be used in analysis at the genus level. (See explanation for character 1.) (See also character 28.) Character 7. Hairs on posterior apical angle (or curve) of hind tibia of worker. (0) Slender, often very hairs long but similar in form and color to nearby hairs. (1) Robust bristles, thicker than nearby and amber to blackish in color, forming the "posterior parapenicillum" of Wille (1979b). This character was not used in the generic analysis because all forms having state (1) are considered congeneric; the chaiacter state is therefore an autapomorphy o{ Meliponula at the genus level. soft *Character 8. Rastellum. (0) Of strong bristles, mostly ending somewhat bluntly. (1) Of hairs, In others with slender, tapering apices, suggesting tapering hairs of other bees. Dactylurina and some is absent the bristles are strong but taper to slender points; they were coded as (1). Since the rastellum in other families of bees, one would assume that in the Apidae a rastellum of ordinary hairs should be plesiomorphic relative to a rastellum of strong bristles. However, all subfamilies of Apidae other than Meliponinae have the rastellum strong in all nonparasitic, non-queen females. If, within the Meliponinae, the rastellum evolved from weak to strong, the same must have happened elsewhere in I the view that the Apidae, i.e., there must have been at least two origins of the strong rastellum. prefer it originated once, in primitive Apidae, and is reduced in some Meliponinae, such as Meliponula. The potential for reduction and loss is indicated by its loss in parasitic genera of Euglossinae and Bombinae, robber genera of Meliponinae, and in cjueens of all highly social forms. The polarity indicated above is in accordance with this view. 88 The University of Kansas Science Bulletin

*Charactcr 9. Submarginal cells of forewing. (0) At least first submarginal cell defined by line representing first transverse cubital vein (Figs. 162-164). (1) Not defined because transverse cubital veins are entirely absent (Fig. 168). Generally associated with states (0) and (1) are all the differences in forewing venation enumerated in couplet 1 of the key to genera. Venational reduction evidently occurred independently in various taxa of minute Meliponinae; even in some relatively large ones, e.g., Trigona (Papuatrigona), the transverse cubital veins are essentially absent, being indicated by denser setae than on the adjacent wing membrane. Character 10. Basal area of propodeum. (0) Bare, as in Xylocopinae and many other bees. (1) Hairy, as in other subfamilies of Apidae. Polarization of this character is in doubt on the basis of outgroups. Hairs crop up on the basal area of the propodeum of species widely scattered through the Meliponinae. At the genus level such hairs characterize four genera, Cephalotrigona, Melipona, Meliponula, and Partamona, but they occur also in Plebeia (Schwarziana), P. (Plebeia) caeridea (Friese), Trigona (Tetragona) lurida Smith, the Trigona (Heterolrigona) planifrons Smith group (part of Platy trigona), and T. (H.) canifrons Smith. Since polarity is not certain and hairs appear to have evolved sporadically (Figs. 82-129) even though they might be plesiomorphic in other cases, this character is omitted from the generic analysis. *Character 11. Gonostyli of worker. (0) Well separated at bases, usually parallel or converging apically (Figs. 9-33). (1) Adjacent or close together at bases, usually diverging apically (Figs. 40-48). In functional stings the bases of the gonostyli are well separated and the gonostyli converge to sheath the sting. It is therefore probable that even in the greatly reduced meliponine sting, separation of the stylar bases is the plesiomorphic condition. The bases are adjacent or nearly so in certain genera, and also in various species of diverse genera as an infrageneric apomorphy *Character 12. Setae or bristles on gonostylus of worker. (0) abundant (unless gonostylus is reduced in size) and dispersed over nearly all parts of gonostylus (Figs. 9-39) (as in other bees). (1) Few and restricted to one edge or thickening on one side of gonostylus (Figs. 41-46). (2) Absent (Fig. 48). Characters 12 and 13 vary concordantly, states (1) and (2) of character 12 being correlated with state (1) of character 13. In theory a meliponine worker gonostylus with abundant setae as well as minute hairs should be possible. I know of no such gonostylus; possibly there is a developmental or physiological factor that prohibits such a combination. *Character 13. Minute, dense hairs on gonostylus of worker, usually much smaller than the smallest setae (Figs. 37-48). (0) Absent (Figs. 9-36). (1) Abundant. Minute hairs are scarce or absent in most related bees (other subfamilies of Apidae; Xylocopinae); Apu has an area of such hairs and numerous but small setae.

*Character 14. Sting stylet of worker (Figs. 9-48). All Meliponinae have the entire sting apparatus greatly reduced. This character concerns the fused second valvulae or stylet. (0) Stylet distinct, sharp (thus most nearly like a functional sting) (Figs. 9, 41, 43-45). (1) Stylet with ape.\ about right angular or with ape.x rounded, more often obtuse, broadly rounded, or reduced to a transverse band. Character 15. Apical process of S6 of male. (0) Strongly sclerotized, directed posteriorly or downward. (1) Strongly sclerotized, reflexed and ape.x directed forward. Characters states (0) and (1) intergrade and in some cases coding was arbitrary. Outgroups lack the process. Polarity is based only on the belief that such a structure is more likely to have evolved flat, then become reflexed. In scattered unrelated meliponine taxa, S6 is a broad, simple plate (Fig. 148) more or less like the preceding sterna and without or with only a small apical process. Such groups are Lestrimelitta, certain species oi Paratrigona, Trigona (Homotrigona), T. (Lepidotrigona) and a subgroup of T (Heterotrigona), i.e., = the subgroup called Odontotrigona Tetrigona. It is tempting to consider this the plesiomorphic (0) condition, because in many other groups of bees S6 is a simple plate. However, the appiearance of this state in groups that show no other special signs of plesiomorphy suggests independent reversions from the usual meliponine condition. All bees must possess genes for producing ordinary sterna (S2-5); a developmental shift could no doubt cause such genes to function for S6. (Further discussions under several of the taxa listed above.) Taxa lacking the apical process of S6 were coded 9 for the preliminary PAUP analysis, the hypothesis being that the process in some cases has been lost. Because of the dubious basis for polarity and because the states intergrade, this character was not used in the generic analysis. *Character 16. Gonobase. (0) Recognizable as separate band on each side. (1) A thin ribbon, or fused to gonocoxite, or absent. *Character 17. Base of male genital capsule. (0) Not curved ventrad and apicad. (1) Strongly produced ventrad and apicad {Liotrigona and Cleptotrigona, Figs. 153, 154). Meliponula s. str. has a slightly down-curved base of the genital capsule. *Character 18. Male genitalia (Figs. 130-161). (0) Rectigonal or amphigonal. (1) Seemingly permanently schizogonal. In most bees, including the Euglossinae and Bombinae, the genitalia are rectigonal. In most Meliponinae considered to exhibit state (0), the genitalia can probably take up the schizogonal conformation during the life of the individual, hence are termed amphigonal. Lestrimelitta Classification of the Apidae 89

be. and Hypotrii^ona, however, are probably permanently reetigonal and others may Character state (1), not found in other bees and hence clearly apomorphic, is found in Melipona and most of the African genera. *Charact€r 19. Gonostylus of male. (0) Slender, not much flattened. (1) Broadly flattened beyond slender base (Fig. 161). (This character state varies between the two species oi Daciylurtna.) Character 20. Attachment of gonostylus to gonocoxite of male. (0) At apex of gonocoxite, as in most of Hymenoptera. (1) Preapical on gonocoxite. (2) Near middle gonocoxite. (3) Near base of gonocoxite. The above coding of this character seemed appropriate for forms with elongate gonocoxites, but "apex" means something quite different for reetigonal and schizogonal gonocoxites. Moreover, in forms with short, transverse gonocoxites, the differences between the four states are its arises negligible. (In Tri^ona iridipennis Smith and close relations the gonostylus from the dorsum of the gonocoxite rather than from the side.) The character was ultimately abandoned for all cladistic analvsis and was not used in the generic cladogram. Character 21. Gonostylus of worker (Figs. 9-48). (0) Cylindrical or tuberculiform. (1) Flattened. Character state (0) most nearly resembles the form found in other bees. All degrees of flattening exist, and flattening is sometimes difficult to detect for these minute structures. There are already three characters (11-13) based on worker gonostyli. Moreover, ffattening is largely concordant with minute, dense hairs (character 13, state 1). Character 21 was therefore abandoned as difficult to quantify and unlikelv to provide additional information. It is listed here largely for historical reasons, because it was emphasized by VVille (1959a, 1979b). or less 'Character 22. Sting lancet (first valvula) of worker (Figs. 9-48). (0) Long, free, apex more longitudinal and attaining at least bases of gonostyli. (1) Shorter, largely transverse, but apex free. (2) Short to absent, included in membrane. As for character 14, polarity is based on the degree of divergence from the structure found in functional stings. The three states intergrade so that some coding decisions were arbitrary. 'Character 23. Scutellum. (0) Rounded and rather thick in lateral view. (1) Projecting as a thin shelf over metanotum and base of propodeum as seen in lateral \iew [Sannotrigona, Paratrigona, Scaptotrigona, Figs. 90-92). Character state (0) is suggestive of the condition in Bombinae, Apinae, and many other bees, and is therefore regarded as plesiomorphic. 'Character 24. Vein M of forewing. (0) Bent at point where it meets (or would meet) first recurrent the vein (Figs. 164, etc.). (1) Ending without such a bend (Figs. 168, 169). In other bees including outgroups the vein bends and continues beyond the first recurrent vein. As is suggested by the first couplet of the key to genera, this character is highly correlated with character 9. It does provide some additional information, however, and is therefore included in the study. 'Character 25. Submarginal angle in forewing. (0) Strongly acute (60°-70°). (1) Slightly acute to obtuse. A strongly acute angle is characteristic of most other bees, including the outgroups, and is therefore considered plesiomorphic. Character 26. Setae on posterior surfaces of worker labial palpal segments one and two (Figs. 49-81). not (0) Short, not or little longer than width of segments, and nearly straight. (1) Certain median (i.e., marginal) setae much enlarged ("giants"), much longer than palpal width, straight or curved (hooked in terminologN' of Michener and Roubik, in press). (2) As in (1) but some or all giant setae sinuous in all subfamilies of (wavy). Character state (0) is plesiomorphic to judge by its occurrence other this Apidae, and in other bees. States (1) and (2) are found in many Meliponinae. The problem with character is that reversals occur, as in robber genera, necrophagous species, etc., that do not collect in a pollen from flowers (Michener and Roubik, in press). It is therefore impossible to know whether, given case, short setae are plesiomorphic or derived. If they are all plesiomorphic except for the robbers, necrophages, etc., then giant and sinuous setae arose repeatedly. For these reasons I have not used this character in the phylogenetic analysis. Character 27. Hairs of outer surface and posterior margin of hind tibia of male. (0) All simple or some long hairs near posterior margin with short branches along one side. (1) With plumose hairs among longer simple hairs along posterior margin and sometimes also on outer surface. This is similar reason. to character 6 (the equivalent character for workers) and is not used in analysis for the same However, the distribution of the states is not the same as for workers. State (0) is found in all genera except Dactylurina and some subgenera of Trigona. This is true also for workers. Within the genus Trigone, state (0) is found in the subgenera Tetragona, Tetragonisca, Lepidotrigona and some Heterotrigona (some species but not all of the group, the Platytrigona group). Other Heterotrigona species and s. str. the subgenera such as Geotrigona, Frieseomelitta and Trigona have state (1). Of subgenera listed, only Lepidotrigona lacks equivalent plumose hairs in the worker. Illustrations of hind tibiae of some male melipones and discussion of assimilation of worker characteristics by males are given by Sakagami and Ito (1981). The outer surface of the hind tibia is usually convex but is concave and corbicula-like in some species having state (0) and in some with state (1). 90 The University of Kansas Science Bulletin computer analysis, as follows: Apotrigona, sting stylet as in 14(1) to 14(0). Such rever- Austroplebeia, Axestotrigona, Cephalotrigona, sals were from state 1 to for characters 9, Cleptotrigona, Dactylurina, Hypotrigona, Lepi- 14, and 16. is here called the dotrigona, Lestrimelitta, Lwtrigona, Melipleb- For what "generic to the eia, Melipona, Meliponula, Nannotrigona, study" (as opposed "preliminary characters 17 to 27 of Table 2 Nogueirapis, Oxytrigona, Paratrigona, Partam- analysis"), ona, Plebeia, Plebeina, Scaptotrigona, Scaura, were considered for the analysis. They had s. str. and not been or had not been Schwarziana, Tetragona, Trigona , recognized, appro- for the Trigonisca. Except for Trichotrigona, Lisotn- priately coded, preliminary analysis. cannot be gona, and Pariotngona, whose males are un- Several, however, reliably polar- known, there is no confusion as to the ized, or are weak for various reasons, but are relationships of the omitted taxa. Dissections discussed in the table because others have were made and the omitted taxa were ex- used them. None of them led to changes in cluded from the cladistic analysis because of the taxa that were considered as genera. A similarity to included taxa. That is, each new PAUP analysis, and a Hennig 86 analy- omitted taxon (except for the three listed sis (the results were the same) was based on above) is similar to an included taxon, either the 17 characters listed in Table 3 (marked being a sister group to the included taxon or by asterisks in Table 2) and the 21 taxa to be incorporated into the included taxon. recognized as genera. The reasons for ex- Most omitted taxa did not differ from corre- cluding the other characters are indicated sponding included taxa in any of the charac- below and in Table 2. The three genera ters used in this analysis and clearly, the whose males are not known were now in- included taxa cover the range of structural cluded, male character states being recorded diversity in Meliponinae. as unknown. Table 3 shows the states for the PAUP analyses were made using all 16 17 characters, the characters and states be- characters. Characters with three or four ing numbered as in Table 2. Certain genera states were coded as ordered, but were also are identical in the character states recorded tried unordered. Analyses yielded numerous in Table 3, as follows: genera 3 and 4; (>100) trees of which every tenth was genera 6, 7, and 8; and genera 13 and 14. trees printed. Consistency indices of shortest That is, complete resolution was impossible ranged from 0.41 to 0.47. Of course com- because some genera (recognizable by au- plete resolution was not achieved with so few tapomorphies at the genus level) did not characters. Inclusion of autapomorphies differ in strong, polarizable synapomor- would have distinguished all taxa but would phies. not have changed the topology of the clado- Some characters used in the preliminary gram as determined by the synapomorphies. analysis of 26 taxa were omitted in the because could not be Informal (i.e., non-numerical) phenetic generic study they observations along with examination of these polarized with any degree of confidence. preliminary PAUP results led to my deci- Others were eliminated because they were sions as to 21 genera to be recognized and not synapomorphic at the genus level. Char- in thus relegation of various taxa to subgeneric acter state 1(1), for example, occurs only or synonym status. Study of character state one (derived) subgenus of Trigona and in the distributions using McClade 2.1 (Maddison distantly related genus Paratrigona. Thus at and Maddison, 1987) was useful in this the genus level it does not characterize Tri- for Para- process. gona and becomes an autapomorphy state became an PAUP produces only the most par- trigona. Character 7(1) simonious cladograms without regard to autapomorphy at the genus level when the in the one's views as to the probability of reversals taxa possessing it fell together genus are in of particular characters. Some reversals that Meliponula. Other such cases explained appeared in PAUP-generated cladograms Table 2. trees were eliminated because they seem unlikely, As in the study of 26 taxa, numerous the Also as in e.g., reacquisition of lost wing veins as in resulted from PAUP analysis. a consen- 9(1) to 9(0) and redevelopment of an acute that study, rather than developing Classification of the Apidae 91

TABLE 3. (Characters of the 21 genera of Meliponinae used in the generic analysis. All characters are polarized, with as plesioniorphic, and the character states are ordered. The numbers of the characters correspond to those in Table 2.

Characters 92 The University of Kansas Science Bulletin

Cephalotrigona Trigona .Oxytrigona N AsAu*"

Nannotrigona -Trichotrigona*

Paratrigona

Plebeia Partamona

Melipona

--i6(i;

Figure 6. Dendrogram based on generic analysis of Meliponinae. A indicates continuation in Figures 7 and 8. The fossil Proplebeia was inserted by hand on the basis of few characters. Character numbers (and states in parentheses) are those used in Tables 2 and 3. Those marked with heavy cross lines are particularly strong. Males of genera marked by asterisks are unknown. All these genera are Neotropical (N); Trigona is also found from Asia (As) to Australia (Au). any other Meliponinae. These would seem Meliponinae studied by Wille (1961). Thus to be plesiomorphic features, but are rever- the Plebeia-\'\\<.e Austroplebeia may indeed be sals according to Figures 7 and 8. the sister group of Trigonisca; alternatively, Trigonisca is geographically isolated (in the fusion inay be convergent. America) from other minute genera (all Af- The isolation oi Melipona at the base of the rican or Asiatic). The relation with cladogram (Fig. 6) is contrary to one of the Lisotrigona shown in Figures 7 and 8 may be relationships suggested previously, namely entirely wrong; when males o{ Lisotrigona are derivation of Melipona from Plebeia-Yike an- known they may indicate different rela- cestors (Wille, 1979b). The acute sting (Fig. tionships. The number of synapomorphies is 9; character 14) and acute submarginal an- so low that a few added characters could gle in the forewing (Fig. 162; character 25) greatly change the cladogram. In the prelim- are plesiomorphic features not shared by inary analysis (26 taxa) a sister-group rela- Plebeia, showing that Melipona could not have tion was shown between Austroplebeia evolved from Plebeia. However, Plebeia and re- (Australia) and Trigonisca. Such a rela- Melipona are in fact reasonably closely tionship is supported from an unexpected lated; only four character changes separate source. Trigonisca (along with Hypotrigona) them in Figure 6. and Austroplebeia have the last two metasomal Wille (1979b) considered the flattened ganglia completely fused, unlike other worker gonostyli of various African genera Classification of the Apidae 93

Cleptotrigona Meliponula Af Dactylurina Af

22(2)

Plebeina

Austropleb Af Au

otrigona

Lisotngona As

Trigonisca N

Hypotrigona Af

Pariotngona* As

-24(i;

-9(1)

-8(1]

Figure 7. Continuation of Figure 6, showing results of PAUP analysis with character states of equal = weight. Explanation as for Figure 6. Characters marked X represent reversals. N Neotropical, Af= Africa, As = Asia, Au = Australia. Autapomorphies are omitted but provide additional characters for taxa without indication of characters or with reversals onlv. 94 The University of Kansas Science Bulletin

Cleptotngona

Plebeina Af Dactylurina Af Af

Austroplebeia Au

Liotrigona 13(2) At

24(i;

22(1)x

18(1) ^ Meliponula

Lisotrigona* As

22(1

Tngonisca N

Hypotngona Af

Pariotrigona* As

Figure 8. Continuation of Figure 6, showing modification of PAUP analysis. See text. Explanation as for Figures 6 and 7.

as ancestral, probably because in two of the appear in other subfamilies of Apidae. I genera (Cleptotrigona and Meliponula) this therefore do not follow Wille in regarding character state is associated with a pointed the African genera as an ancestral group In- sting stylet. I consider the flattened gonostyli from which other Meliponinae arose. (Figs. 40-48; character 21, Table 2), pres- stead, the African, etc., group (Figs. 7, 8) ence of minute hairs on them (character 13), appears to have evolved from a cluster of reduction of setae on them (character 12), American genera (Fig. 6). and tendency of the gonostyli to diverge The genera appearing in Figure 6 have a from proximate bases (character 11), to be distinctive combination of plesiomorphic derived character states, since they do not and apomorphic character states. The for- Classification of the Apidae 95

Figures 9-34. Sting rudiments of workers of Meliponinae. 9, Melipona mfiventris Lepeletier. 10, Plebeia Plebeia Fossil, Proplebeia dominicana (Wille and Chandler). 11, (Pleheia) frontalis (Friese). 12, Plebeia (Plebeia) caerulea (Friese). 13, Plebeia (Plebeia) schrottkyi (Friese). 14, (Schwarziana) quadripunctata mirandula (Lepeletier). 15, Plebeia (Scaura) latitarsis (Friese). 16, Plebeia (Nogueirapis) (Cockerell). 17, Partamona near cupira (Smith). 18, Partamona zonata (Smith). 19, Paratrigona opaca (Cockerell). 20, limao Nannotrigona lestaceicorms (Lepeletier). 21, (Guerin). 22, Lestrimelitta (Smith). lermniata 23, Oxytrigona mellicolor (Packard). 24, Cephalotngona capitala (Smith). 25, Trigona (Lepidotngona) Cresson. Smith. 26, Trigona (Papuatrigona) genalts Friese. 27, Trigona (Frieseomelitta) nigra 28, Trigona (Geotrigona) mombuca Smith. 29, Trigona (Heterotrigona) carbonaria Smith. 30, Trigona (Tetragomsca) Smith. angustula Latreille. 31, Trigona (Tetragona) lurida Smith. 32, Trigona (Heterotrigona) apicalis 33, Trigona (Trigona) amalthea (Olivier). 34, Trigona (Trigona) cilipes (Fabricius). 96 The University of Kansas Science Bulletin

mer include cylindrical or papilliform, setose tropical genus, and Austroplebeia, an Aus- worker gonostyli (Figs. 9-34), commonly tralian genus, have worker gonostyli with converging apically, with well separated minute hairs like those of the African group bases and without minute hairs; the strong, but in the other characters listed above they usually blunt setae of the rastellum (Figs. agree with the genera that appear in Figure 184, 185); and the posterior or downward 6. The indicated stars in directed midapical process of S6 of the male. genera by Figures 6 Apomorphies include the obtuse or rounded to 8 are known only in the worker caste. Male characters are therefore un- sting remnant (except for Melipona) and re- genitalic duced gonobase remnants. known. Tnchotrigona is possibly a robber or The situation is in fact more complex. parasitic group derived from Trigona (Friese- Hypotrigona, which agrees in various features omelitta), as suggested by the narrow ridge with the genera in Figure 6, is restricted to with keirotrichia on the inner surface of the Africa. In Melipona, a Neotropical genus, the hind tibia. Lisotrigona and Pariotrigona are sting is right angular to acute, in some minute forms superficially similar to Hypotri- species (e.g., M. fulva Lepeletier) as strong gona, Liotrigona, and Trigonisca. Their rela- as in any African genus; the male gonocox- tionships remain uncertain until males are ites are elongate and the genitalia schiz- found (but see generic descriptions). ogonal; and the gonobase is represented by a Biogeography: While cladograms, especially slender strip. Except that the gonobase rem- it based on relatively few characters, provide nant is quite different from the remnants in only hypotheses of relationships, they are the African group, these character states are strengthened if they make sense geograph- suggestive of that group. Trigonisca, a Neo- ically or in terms of characters not used in

35-48. Figures Sting rudiments of workers of Meliponinae. 35, Hypotrigona braunsi (Kohl). 36, Pariotrigona pendleburyi (Schwarz). 37, Lisotrigona scintillans (Cockercll). 38, Trigonisca buyssoni (Friese). 39, Trigonisca longicornis (Friese). 40, Liotrigona mahafalya Brooks and Michener. 41, Cleptolrigona cubiceps (Friese). 42, Austroplebeia cassiae (Cockerell). 43, Meliponula (Meliplebeia) beccarii (Gribodo). 44, Meliponula (Axestotrigona) erythra (Schletterer). 45, Meliponula (Meliponula) bocandei (Spinola). 46, Meliponula (Meliplebeia) lendliana (Friese). 47, Plebeina denoiti (Vachal). 48, Dactylurina schmidti (Sta- delmann). Classification of the Apidae 97

cladogram construction. Figures 6 and 8 do would seem that attributes of this system make reasonable geographic sense. should be of phylogenetic significance. Meli- As indicated above, there is an African pona is quite different from the rest, in group of genera (Figs. 7, 8) with outhers, agreement with the cladogram. Otherwise, this sharing some of its derived features, in system does not seem closely related to the AustraHa (Austroplebeia) and the Neotropics branches shown in Figures 6 to 8. (Tngonisca), and a primarily Neotropical Rather, it seems that small forms (probably with small (also Indoaustralian because of Trigona) flight ranges) exhibit little recruit- group (Fig. 6) with an outlier (or third ment ability while larger species have better recruitment. group?), Hypotrigona, in Africa. Melipona Scent trails, i.e., series of odor for (Neotropical) could be a member of this spots recruiting, are known in Cephalotri- group but the evidence is weak. A bio- gona, Lestrimelilta, Oxytrigona, Scaptotrigona, is and geographical puzzle how Trigona came to Trigona (Geotrigona and Trigona s. str.). Kerr and Esch occur abundantly in the Neotropics and the (1965, fig. 10) provide some details Indoaustralian area while being absent from and exceptions [especially Trigona Africa. If male character states show Lisotri- (Duckeola) ghilianii (Spinola), a large species to not known to have gona be related to Trigonisca, they could scent trails]. Nest constitute together a second genus having a architecture, likewise, neither sup- nor refutes the distribution similar to that of Trigona. ports cladogram. The most No genus occurs both in Africa and South striking variation in nest architecture is in America. Therefore the meliponine faunas brood cell arrangement. This feature has been of these continents probably date from after emphasized by authors who wish to the origin of the South Atlantic ocean in the demonstrate that the subgenus Frieseomelitta late is archaic or Cretaceous. The cladogram suggests ancestral, having brood cefls in clusters rather that the Meliponinae arose in tropical Amer- than combs. ica (which at that time extended far into It is not unreasonable to suppose that cells North America). We know nothing of when in a disorganized cluster is a plesiomorphy the group moved between the American relative to cells arranged in combs. Most continents, but, as noted below, there is a Meliponinae arrange cells in horizontal late Cretaceous Trigona from New Jersey (sometimes spiral) combs. Cefls in clusters, characterize not afl (Michener and Grimaldi, 1988a, b). The however, only Trigona dissimilarity of the Neotropical and African (Frieseomelitta) but also T (Heterotrigona) can- faunas could suggest that meliponines ifrons Smith and most species of the reached South America from North America Tetragonula group of T (Heterotrigona). More- later, after considerable separation of South over, cells are placed in clusters by afl species America from Africa. of Austroplebeia [although layered, approach- Following the idea of Kerr and Maule ing combs, in^. cmcta (Mocsary); Michener, the (1964), meliponines (including Trigona) 1961], Cleptotrigona, Hypotrigona, Liotrigona, may have spread through what is now the Tnchotrigona, and Trigonisca, and by some Holarctic region when it was warmer. The species of both Plebeia (Plebeia) and Plebeia Eocene Kelneriapis from Baltic amber (see (Scaura). below) is evidence of meliponines in the As suggested by Michener (1961), cluster- Holarctic region. With climatic deteriora- ing may be the ancestral cefl arrangement tion during the Tertiary, Trigona is now for Meliponinae (perhaps retained by Aus- limited to southern Asia (south to Australia) troplebeia) while being derived for others. In and the Neotropical region. particular, it is probably derived for species The African fauna must have evolved like Trigona (Heterotrigona) fuscobalteata Cam- when Africa was substantially isolated from eron that nest in small, irregular cavities American and Eurasian invasions (Mich- where combs would be impractical. Indeed, ener, 1990). most cluster-makers are smafl to minute Behavior: In view of the diverse types of bees. Michener (1961) contended that nearly to recruitment food sources found in Melipo- spherical cells in clusters (as in Austroplebeia) ninae (Kerr, 1969; Michener, 1974), it are probably ancestral, that elongate cells 98 The University of Kansas Science Bulletin resulted from packing cells into combs, and nously. Such taxa are Plebeia (Plebeia) except that therefore species that make elongate as indicated above, Nannotrigona, Paratrigona, cells in clusters are derived from species that Trigona (Frieseomelitta) jiavicornis (Fabricius), made combs. Unfortunately for this theory, and T. (Heterotrigona) moorei Schwarz. It spherical cells are almost unknown in other should be noted that, in the successive families of bees, so there is no good evidence group, there are the following close relatives for polarity of this character. of taxa listed above as partially or fully Dactylurina is unique among Meliponinae synchronous: Plebeia (Schwarziana and in that its combs, instead of being horizontal Scaura), Trigona (Frieseomelitta) of other spe- or so with cells are T s. str. nearly opening upward, cies, (Trigona , Tetragona, Tetragonisca, vertical with cells on both sides opening Geotrigona, and the Tetragonula group o{ Heter- laterally, as in the combs of Apis. otrigona), and Trigonisca of other species. One Interesting aspects of social behavior of can only conclude that if successive cell Meliponinae are the oviposition rituals and construction is plesiomorphic, synchroniza- associated activities, much studied and de- tion has evolved independently in various scribed in a series of papers by Sakagami groups. and others (reviewed by Sakagami, 1982; see Cell provisioning is in general parallel to also Sakagami, Yamane and Inoue, 1983, cell construction, i.e., successive if cells are and Sakagami and Yamane, 1987). These finished successively, synchronous if cells are rituals are often group-specific and often constructed or finished synchronously. accompanied by laying of trophic eggs (usu- Oviposition proper by the queen is less ally queen food) by workers. The behavior of subject to brief summary than the features queens and workers during laying might mentioned above, but egg laying by workers produce characters of phylogenetic signifi- (in queenright colonies) is of interest. It is cance; some of the behavioral character not confirmed in Trigonisca muelleri (Friese), states are indicated below in the comments Trigona (Frieseomelitta) and probably T on various genera and subgenera. It must be (Duckeola). Oviposition by workers occurs in remembered, however, that these comments queenright colonies of all other forms stud- are based on few species and that sometimes ied. In Plebeia (Plebeia) except P. minima closely related forms differ considerably in Friese, in Hypotrigona, and in Lestrimelitta, the behavior. Therefore, generalizations as to a eggs are not laid in connection with the taxon's behavior may not always be applica- queen's oviposition process and are eaten by ble to all species. Polarization of most of workers or the queen. In other taxa, worker these behaviors is dubious since there are no laying is associated with queen oviposition, counterparts in outgroups. The following on or near a cell being provisioned, before are some examples, selected from many provisioning starts in the case of Trigona possible characters. (Geotrigona), but afterwards in all others. New brood cell construction in most cases Such eggs are usually eaten by the queen. is unsynchronized (called successive), so that Usually the trophic egg is laid on the cell new cells at the advancing front (Michener, margin. [Plebeia (Plebeia) minima Friese is 1961) are in various stages of construction. in this group.] It is much larger than the This apparently unorganized construction of queen's egg in Scaptotrigona and Plebeia new cells is likely to be plesiomorphic. In a (Schwarziana). In certain taxa, however, it is few taxa, while cell contruction starts suc- laid on the food mass like the queen's egg. cessively, it becomes synchronized by the Such taxa are Plebeia (Scaura), Paratrigona, time that a number of cells are completed. Trigonisca longicornis (Friese) (Ceietrigona), Such taxa are Trigona (Duckeola), T. (Lep- Melipona and Meliponula (Meliponula). If, as idotrigona), Plebeia (Plebeia) minima (Fuese) seems likely, the last (laying on the food mass and schrottkyi (Friese), and two groups of like the queen) is plesiomorphic, then modi- Trigonisca, namely T. muellen (Friese) and fications of that behavior must have occurred longicornis (Friese), i.e., and Cel- repeatedly and are not indicative of recog- etrigona, respectively. Finally, in some taxa, a nizable clades. number of cells are constructed synchro- It is of interest that in all the characters Classification of the Apidae 99

listed above relevant to oviposition, Melipona (between first abscissa of Rs and Rs-I-M), has the presumablv plesiomorphic behavior. i.e., the submarginal angle (character 25, This reintorces its position near the base ot Table 2), is acute in non-meliponine bees. It the cladogram rather than as a specialized is also acute (60°-70°), no doubt plesiomor- derivitive group. phic, in Melipona (Fig. 162). It is slightly Labial palpi: The hairs of the posterior acute in Cleptotrigona, Plebeina, most Plebeia, surfaces of the labial palpi of workers, char- and some Paratrigona. It is right angular or acter 26, provide character states that are of approximately so (i.e., the first abscissa of interest in connection with the cladograms Rs is more transverse) in most Meliponinae, (Figs. 49-81). Other subfamilies of Apidae, grading to slightly obtuse in several groups and various groups of Meliponinae, have such as Scaptotrigona, some Partamona, some these hairs if short (little any longer than Paratrigona, and Meliponula (Axestotrigona). It palpal width) and straight. This is probably is very strongly obtuse, correlated with a the plesioinorphic condition seen in Aielipona short first abscissa of Rs (often only about and also be in such other one tenth as as the basal vein = first may plesiomorphic long ( taxa as Cephalotrigona, Hypotrigona, Plebeia abscissa of M), in Cephalotrigona, Dactylurina, (Schwarziana and Scaura), Trigona (Geotrigona Oxytrigona, Trichotrigona, and some species of and TetragoTia) and even in Meliponula (Meli- each of the following subgenera of Trigona: plebeia). If so, then giant curved and often Frieseomelitta, Tetragona, Trigona s. str. (Figs. wavy setae must have arisen repeatedly if 166, 167). Other species of these subgenera Figures 6 to 8 mean anything. As indicated as well as the subgenera Geotrigona, Heterotri- by Michener and Roubik (in press), the gona, Hornotrigona, Lepidotrigona, and Tetrago- giant setae probably have to do with extract- nisca, have the angle weakly obtuse or right ing pollen from anthers, minute flowers, etc. angular. Thus a strongly obtuse angle is They appear to have been lost, i.e., replaced found only in taxa with a narrow keirotrichi- by short, straight setae, in bees that do not ate ridge on the inner surface of the hind collect pollen from flowers, e.g., the robber tibia, but has no doubt evolved independ- genera Lestrimelitta and Cleptotrigona, the pos- ently in some such taxa (at least Dactylurina sibly parasitic Trichotrigona, and the species vs. the others). It is not clear whether the of the carrion-feeding group of Trigona (Tri- subgenera of Trigona like Tetragonisca retain gona) hypogea Silvestri. When giant setae are an ancestral submarginal angle or have de- lost, the condition is not visibly diflTerent veloped to a right angle along with their from the plesiomorphic condition. These small body size. There are, however, rather setae are therefore of little value in reinforc- large species of Hornotrigona and Heterotrigona ing or weakening the cladogram although with the angle right angular. their diversity as shown in Figures 49 to 81 The first abscissa of Rs is relatively long in suggests that they are important characters. related subfamilies and families of bees. Wing venation: Characters 9, 24, and 25, Among Meliponinae it is about one fourth as Table 2, involve wing venation, but several long as the basal vein in Melipona as well as additional features of wing venation vary in Lestrimelitta, Nannotrigona, Paratrigona, and widely among meliponine bees. In general Plebeina. It is similarly rather long, one third they neither support nor refute the clado- to rarely one fifth (in Cleptotrigona) as long as grams, but I deal with them at some length the basal vein, in all the minute genera because they are conspicuous and have been segregated in couplet 1 of the generic key, used by others in the past. While of obvious and in the minute Plebeia (Plebeia) schrottkyi interest, they sometimes vary within taxa, (Friese). In Cephalotrigona and some species and some of them appear to vary with body of Trigona (Trigona and Tetragona) it is only size irrespective of phylogenetic relationship, about one tenth as long as the basal vein, an along the lines indicated by Danforth (1989) obviously derived condition. All other Meli- for other groups of bees. For example, the poninae have an intermediate Rs (first ab- basal vein is more transverse in small spe- scissa) length, one fifth to one eighth as long cies, more longitudinal in large ones. The as the basal vein. When the basal vein is it is basal angle of the first submarginal cell relatively long, 100 The University of Kansas Science Bulletin

Figures 49-64 (modified from Michener and Roubik, in press). Posterior surfaces of labial palpi of workers. Marginal hairs and small hairs are omitted. Mesal margins are uppermost. The first and to some degree the second segments are sheath-like so that breadth varies with compression and should not be considered a useful character. 49, Melipona fasciata Latreille. 50, Pleheia (Plebeia) frontalis (Friese). 51, Plebeia (Plebeia) schrottkyi (Friese). 52, Plebeia (Schwarziana) quadripunclata (Lepeletier). 53, Plebeia (Scaura) latitarsis (Friese). 54, Scaptotrigona pachysoma (Cockerell). 55, Paratrigona impunctata (Ducke). 56, Nannotrigona testaceicornis (Lepeletier). 57, Partamona near cupira (Smith). 58, Lestrwielitta lirnao (Smith). 59, Trigonisca buyssoni (Friese). 60, Hypotngona braunsi (Kohl). 61, Liotrigona mahafalya Brooks and Michener. 62, Cleptotrigona cubiceps (Friese). 63, Pariotrigona pendleburyi (Schwarz). 64, Lisotrigona scintillans (Cockerell). Figures 65, 66. Flabellum of workers. 65, (Smith). 66, Trigona Julviventris Guerin. Classification of the Apidae 101

Figures 67-81 (modified from Michener and Roubik, in press). Posterior surfaces of labial palpi of workers. Explanation as for Figures 49-64. 67, Cephalotrigona capitala (Smith). 68, Oxytrigona obscura (Friese). 69, Trigona (Tetragona) clavipes (Fabricius). 70, T. (Duckeola) ghilianii Spinola. 71, T. (Frteseomelitta) savannensis Kouhik. 72, T. (Tetragonisca) angustula Latreille. 73, T. (Heterotrigona) carbonaria Smith. 74, T. (Trigona) pallens (Fabricius). 75, T. (Trigona) species near hypogea Silvestri from . 76, Trichotrigona extranea Camargo and Moure. 77, Meliponula (Meliponula) bocandei (Spinola). 78, M. (Axestotrigona) erythra (Schletterer). 79, M. (Meliplebeia) heccani (Gribodo). 80, Dactylurina staudingeri (Gribodo). 81, Austroplebeia cassiae (Cockerell). 102 Thf University of Kansas Science Bulletit

be either usually straight except near its basal end. rectigonal or schizogonal [see Fig. This is the condition in most species of 134, based on two males of Partamona near Trigona and its relatives with keirotrichia on cupira (Smith) from Costa Rica]. The genital a ridge (Cephalotrigona, Trichotrigona, Oxytri- capsule is so loosely put together that the gona) as well as in Dactylurina, most Melipo- gonocoxites are hinged on the median points nula, Plebeia (Schwarziana), Plebeina, and where they meet and can fold basad to take Scaptotrigona. The basal vein is gently curved the schizogonal position, so that sometimes in all the other genera, although there are the originally basal margins almost meet one intermediates with very weak curvature such another. as Partamona, LestrimeUtta, some species of Commonly associated with this move- Plebeia, and some species of Trigona (Hetero- ment, the heavily sclerotized prong-like Irigona). penis valves rotate and at the same time flex The basal vein is basal to cu-v in most laterad. Note that in Figure 134, the shape of species of Trigona and its relatives with a the prong of the penis valve in lateral view is similar inner surface of the hind tibia (Cepha- the same as that shown in the dorsoventral lotrigona, Dactylurina, Oxytrigona, Trichotri- drawing of a schizogonal specimen. Thus gona). The same is true of Scaptotrigona, one has the same view of the penis valve in Plebeina, and some species of Plebeia and both cases because of its rotation. Paratrigona. The basal vein is distal to cu-v in Males often die with the penis valves the minute 1 genera segregated in couplet of directed laterally. It is not practical to return the to key genera, and in the minute Plebeia them to a more or less longitudinal position. (Plebeia) schrottkyi (Friese), also in Lestrimel- Some illustrations show them directed lat- itta, Meliponula, and some other species of erad. Perhaps this is the position in copula- Plebeia. The intermediate condition, the ba- tion, with the penis valves hooking into the sal vein meeting cu v or nearly so, is found body of the queen so that the genitalia are in the remaining groups including some pulled out of the male. Unfortunately lateral species of Plebeia and Trigona. views of genitalia in this condition are not Male genitalia: In the Meliponinae charac- worth much and dorsoventral views look ters of males have been infrequently used very different from those of the same species hitherto for genus or subgenus recognition with the penis valves directed apicad. because of the scarcity of males in collec- Some of the conspicuous differences tions. It is risky to use male characters, as I among genitalic preparations result from have repeatedly done in keys and descrip- mobility of parts. Apparently the mobility tions, when males remain unknown for varies; it is great in most meliponines, those many species. For various genera and sub- that are amphigonal, but can apparently be genera for which males of only one species slight in the permanently rectigonal and the are known, I have indicated the male charac- permanently schizogonal forms. ters of the taxon on the basis of that one Either by comparisons of different male species. I hope that males of related species specimens or of published drawings with with agree my characterization, but they specimens, it is clear that genitalia can ap- not. As males of may more species become pear either rectigonal or schizogonal (often known, any errors that I have introduced in with accompanying rotation of the penis this will way become evident. valves) in the following species: Austroplebeia A comment on schizogonal, rectigonal, essingtoni (Cockerell), Partamona cupira and amphigonal genital capsules is appropri- (Smith), Plebeia schrottkyi (Friese), Trigona ate here (see section on Terminology and amalthea (Olivier), and T pallens (Fabricius). Materials for explanation of these terms). I There are numerous other taxa in which originally thought that these terms repre- gonocoxal shape (about as long as broad) sented phylogenetically significant condi- probably permits such change in genital tions, rectigonal being the plesiomorphic appearance. These are Austroplebeia, Nanno- state and schizogonal derived. However, at trigona, Oxytrigona, Paratrigona, Partamona, least in various genera, this is clearly not the Plebeia, Scaptotrigona, Trigonisca, and most case, for specimens of the same species can subgenera of Trigona. Such forms are infor- Classification of the Apidae 103 mally called amphigonal, to save explana- etc., mostly by W. E. Kerr and his associates Mello and and Kerr tory space. (see Kerr, 1984, 1987, Nonetheless there are groups in wliich the for summaries). Table 4 presents the data derived from these sources. These authors genitalia appear to be permanently schiz- the ancestral chromosome number as ogonal, and in which this feature is therefore regard an apomorphic character state. These are 8, but since outgroups (other subfamilies of the groups in which the gonocoxites arc Apidea, Xylocopini) have 15 to 25 chro- it seems that sufficiently elongate that they could hardly mosomes, likely Trigonisca of adopt a rectigonal conformation; in some muelleri (Friese) (the Leurotrigona group with 8 chromosomes and Meli- such groups (especially Melipona) males of Trigonisca), with 9 or 10 achieved numerous species have been examined by pona chromosomes than reten- me or illustrated by previous authors; all are these numbers by fusion rather tion of ancestral numbers. schizogonal. Such taxa are Cleptotrigona, Dac- bee chromosomes are min- tylurina, Liotrigona, Melipona, Meliponula, Ple- Unfortunately, ute and details that these mat- beina, and Trigona (Geotrigona, Tetragonisca). In might clarify ters are little known. numbers at least some of these taxa the penis valves Using alone, no sensible of can flex laterad without great effect on pattern phylogenetic impor- tance is evident for the gonocoxal positions. Figure 161 shows this Meliponinae. for Dactylurina. In Liotrigona and Cleptotrigona the flexion is diff'erent in that each entirely TABLE 4. Haploid chromosome numbers penis valve flexes contralaterally, the penis (largely based on Mello and Kerr, 1984, and Kerr, valves crossing near their bases (Figs. 153, 1987). 154). Xylocopa 16 there are taxa in which the Finally geni- Melipona 9, 10, 18' talia are probably rigidly rectagonal: Lestri- Plebeia 18 melitta (Figs. 141-143) and probably Plebeia s. str. (including "Friesella") Schwarziana 16 Hypotrigona (Fig. 151). This condition should Partamona 1 7 be ancestral to judge by Bombinae, Euglossi- Paratrigona 1 8 and other families of bees. 6-8 nae, Figures Nannotrigona 1 7 do not support this view. Scaptotrigona 1 7 Lestrimelitta 1 4 Poison glands: Kerr and Lello (1962) inves- Oxytrigona 1 7 tigated remnants of the poison gland (and Cephalotrigona 1 7 in workers. storage sacs) meliponine They Trigona sacs in bocandei 1 7 found large Meliponula (Spin- Geotrigona 1 5 ola) and in Trigona (Frieseomelitta) freiremaiai Frieseomelitta 1 5 and assumed them to be Duckeola (Moure) apparently 17 Trigona s. str. 14, plesiomorphic. In fact, they are much larger Hypotrigona 1 4- than in bees and the stinging (Apis, Bombus) Tngonisca ' ' ' 8 large size must be a derived condition. In 'Leurotrigona 15 _ Nannotrigona, Plebeia [schrottkyi (Friese) and "Celetrigona" 1 8 Cleptotrigona droryana (Friese)] and Dactylurina the glands Meliponula are not but are well I 1 8 large developed; Axestotrigona suspect that this is the plesiomorphic condi- Meliplebeia 1 7 'Flebeiella" 18 tion. Melipona and Trigona (Tetragonisca) an- Meliponula s. str. 18 gustula (Latreille) have vestigial but Dactylurina 1 7 sacs. In other examined recognizable genera 1 Euplusia 5 the glands are vestigial or absent; such taxa Eulaema 15 20 are Partamona, Trigona (Trigona), Cephalotri- Bombus 18, 25 gona, Oxy trigona, Lestrimelitta, and Scaptotn- Psithyrus Apis 16 gona. ~

Chromosome numbers: chromosome ' Haploid Based on Kerr (1972). have been for numerous 2 this is numbers reported Kerr (in litt.) indicated that number meliponine bees as well as other Apidae, doubtful because of poor slides. 104 The University of Kansas Science Bulletin

Lestrimelitta Convergence: Unless there has been con- Cleptotrigona (Africa), (Neo- bees with vergence in such characters as worker tropical). Robber shiny, sparsely haired vertex and areas gonostyli, there has been remarkable con- bodies; genal broad; fossa narrowed vergence in external features of workers of proboscidial greatly posteri- labrum con- various meliponine bees. Wille (1979b) deals orly; eyes small; clypeus small; with this in some detail. The following para- cave between lateral prominences; corbicula and rastellum reduced to graphs summarize the main points: absent, penicillum hairs. Wille Melipona (Neotropical) and Meliponula s. tapering (1979b) correctly showed that in of their str. (Africa). Robust, thorax and head spite similarities, these are not related. densely hairy, integument dull, basal pro- genera closely vessel be- podeal area hairy, dorsal arched Partarnona, Scaptotrigona, and Trigona s. str. indirect muscles of tween longitudinal flight. {spinipes group), T (Geotrigona) (all Neotrop- of the dorsal characteristic short The arch vessel, ical). Robust, often black bees with of many large, fast-flying bees, may be re- metasomas, superficially similar in form and lated to the robust body and fast flight of color. of one's Melipona and Meliponula s. str.; the form of Classificatory questions: Regardless the dorsal vessel is documented for various methods, decisions as to classificatory levels taxa by Wille (1958, 1963, 1979b). are subjective. There will be some reason- Hypotrigona (Africa), Liotrigona (Africa), able disagreements with my decisions. Some as Lisotrigona (Asia), Pariotrigona (Asia) and Tn- would regard aU genus-group names gen- gonisca (Neotropical). Minute, sparsely era. I believe that this obscures relationships haired, pterostigma relatively large, wing that are useful to show in the classification. venational characters as listed in first alter- However, even if one accepts in a general native of key to genera, below. All except way the classification presented below, there possibly the two rare Asiatic taxa are at- are decisions that I had to make arbitrarily tracted to perspiration. At least Hypotrigona, and that could equally well have been differ- Liotrigona, and Trigonisca are quite unrelated ent. Chief among these are the following: the to one another (Fig. 6) to judge by sting Scaura could have been given generic sta- and male genitalic character states, although tus with Schwarzula as a monotypic subgenus almost superficially indistinguishable. Clepto- if desired, instead of placement oi Scaura as a falls in this but has trigona (Africa) also group subgenus of Plebeia. the special features of robbers. Scaptotrigona could have been placed as a (Neotropical; Dactylurina (Africa), Trigona subgenus of Nannotrigona. They are sister Asia to Australia). Typically rather elongate groups whose relationship might well be and although some American long-legged, indicated by the classification, but they are forms the Geotrigona and some (like subgenus different in appearance, easily distinguished, species of s. str.) have the metasoma Trigona and I hesitantly gave both generic status. short and broad. Inner surface of hind tibia Cephalotrigona could have been considered of worker with longitudinal band of kei- a subgenus of Trigona. rotrichia on elevated ridge usually Httle if could have been given sub- any wider than depressed, shining posterior generic status in Trigona, instead of syn- zone of tibia. Posterior fringe of hind tibia of onymizing it with the subgenus Tetragona. worker including plumose hairs except in Five groups of the subgenus Heterotrigona some small subgenera of Trigona. of Trigona could have been given subgeneric Austroplebeia (Australia), Meliponula (except status, as suggested in the discussion of s. %i\:.){Mv'\cdi), Nannotrigona, Paratrigona, and Subjectively these groups seem Plebeia (Neotropical), Plebeina (Africa). Heterotrigona. less distinct than the subgenera here recog- Mostly small, robust bees of superficially nized. No cladistic study of Trigona subgen- similar aspect, often with restricted dull yel- era has been made. lowish markings on head and thorax. Poste- rior margin of inner surface of hind tibia The four named groups of Trigonisca could status. commonly shiny, often depressed, but some- have been given subgeneric times with keirotrichia reaching margin. The three named groups of Meliponula Classification of the Apidae 105 subgenus Melipleheia could have been given from the Miocene of southern , Pro- subgeneric status. plebeia dominicana (Wille and Chandler, 1964) from the Oligoccne of the Dominican Re- Fossil Meliponinae public (see also Michener, 1982), and Tri- and Grimaldi The best described fossil Meliponinae are gona prisca Michener (1988a, from the late Cretaceous of New Plebeia (Nogueirapis) silacea (Wille, 1959b) b) Jersey.

IPS

of workers Figures 82-129. Profile (head to the right) of posterior part of thorax and propodeum at or near the middle of the (except as otherwise indicated) of Meliponinae. When hairs are present basal area of the propodeum, they are indicated. Otherwise hairs are omitted. 82, Melipona favosa (Fabricius). 83, Proplebeia dominicana (Wille and Chandler). 84, Plebeia (Plebeia) frontalis (Friese). 85, Plebeia Plebeia (Plebeia) caerulea (Friese). 86, Plebeia (Schwarziana) quadripunctata (Lepeletier). 87, (Scaura) Pariamona near latitarsis (Friese). 88, Plebeia (Nogueirapis) mirandula (Cockerell). 89, cupira (Smith). 90, mexicana Paratrigona opaca (Cockerell). 91, Nannotrigona testaceicorms (Lepeletier). 92, Scaptotrigona (Guerin). 93, Lestimelitta limao (Smith). 94, Oxytrigona rnellicolor (Packard). 95, Cephalotrigona capitata Friese. (Smith). 96, Trigona (Lepidotrigona) terminata Smith. 97, Trigona (Papuatrigona) genalis 98, Trigona Provancher. (Geotrigona) acapulconis Strand. 99, Trigona (Frieseomelitta) nigra paupera 100, Trigona (Tetragonisca) angustula Latreille. 101, Trigona (Tetragona) clavipes (Fabricius). 102, Trigona (Tetragona) Smhh. liirida '&m\\h. 103, Trigona (Ducfceola) ghilianii Spinola. 104, Trigona (Heterotrigona) apicalis 105, Smith. Trigona (Heterotrigona) itama Cockerell. 106, Trigona (Heterotrigona) camfrons 107, Trigona Cresson. (Heterotrigona) planifrons Smith. 108, Trigona (Heterotrigona) fuscobalteata 109, Trigona (Heterotri- Smith. thoracica gona) atripes Smith. 110, Trigona (Homotrigona) fimbriata Ill, Trigona (Heterotrigona) Guerin. Smith. 112, Trigona (Trigona) cilipes (Fabricius). 113, Trigona (Trigona) fulviventns 114, braunsi Trichotrigona extranaea Camargo and Moure. 115, Hypotngona (Kohl). 116, Panotrigona pendleburyi (Schwarz). 117, Lisotrigona scintillans (Cockerell). 118, Trigonisca buyssoni (Friese). 119, Trigonisca longicornis (Friese). 120, Liotrigona mahafalya Brooks and Michener. 121, Cleptotrigona cubiceps (Friese), nebulata male below. 122, Austropleheia cassiae (Cockerell). 123, Meliponula (Meliplebeia) (Smith). 124, Meliponula (Meliplebeia) lendliana (Friese). 125, Meliponula (Meliplebeia) beccarii (Gribodo). 126, Meliponula bocandei Plebeina denoiti (Axestotrigona) erythra (Schletterer). 127, Meliponula (Meliponula) (Spinola). 128, (Vachal). 129, Dactylurina schmidti {SiadeXmann). 106 The University of Kansas Science Bulletin

reasonable in the conte.xt of the broad Information on less fully studied fossil sting- interpreta- tion of that genus adopted here. More material less bees is summarized by Wille (1977) and will be necessary to place this genus. Zeuner and Manning (1976). P. silacea is no doubt correctly placed, Genus Kelneriapis Sakagami

it is close at the level to Recent since species Kelneriapu Sakagami, 1978 (June):232. Type species: eocemca species of Plebeia (Nogueirapis). The other Trigona (Hypotrigona) Kelner-Pillault, 1970, by monotypy. fossils are with little because placed certainty Kelnermelia Moure and Camargo, 1978 (November we now know that convergence in external 17):565. Type species: Trigona (Hypotrigona) eocemca Kelner-Pillault, 1970, features is rampant in Meliponinae. The by original designation. gonostyli of workers are visible in at least one This generic name is based on a species from the fossil of the Antillean Proplebeia, which is best late Eocene Baltic amber. Many details of its structure are indicated regarded as a separate genus. by Kelner-Pillault (1970) and reworded Moure and The true position of T. prisca must be by Camargo (1978). Unfortunately the inner surface of the hind tibia viewed as dubious, even though it was origi- was not visible and the description and illustra- nally described as a species of Trigona s. str. tion do not even verify the existence of a corbicula with which it agrees in toothed mandibles on the outer surface. Lack of a corbicula (and and other external characteristics except the apparently of a penicillum) suggests that the hairs of the mar- probably simple posterior specimens were males. The antenna is illustrated In the latter feature it gin of the hind tibia. and described as 13-segmented, further support- resembles the subgenus Lepidotrigona and ing the sex assignment. Nothing in the descrip- tions Kelner-Pillault or perhaps Papuatrigona. There may have been a by by Moure and realization that have very few branched hairs, as in some Trigona Camargo suggest they may been is in its comparing male characters with the worker (Geotrigona). Thus there nothing characters known for other external characters to exclude it from the genera. The bee was minute (3 mm long) with wing genus Trigona in spite of its great antiquity. venation more or less like that of modern minute The problem is that the same can be said of species (couplet 1 of key to genera). Its rela- the African yet the worker Dactylunna, tionships to modern genera remain unknown. and male show that Dacty- gonostyli genitalia Re-examination of the type might partially lurina is related to The only distantly Trigona. clarify the situation. At the Institute of Geology problem is accentuated by the realization and Paleontology, University of Gottingen, how- that in the Cretaceous when T prisca was ever, the type, which should have been there to the could not be living, its location (New Jersey) was not far according original description, found in the late Dr. S. Kelner- from Africa, where Dactylunna now lives. (inquiry 1976); Pillault wrote that she no had it in Paris at Three genus-group names have been longer that time. based on fossils. The current status of our knowledge of each is indicated below. Genus Proplebeia Michener Trigona (Proplebeia) Michener, 1982:44: Type species: Genus Tosi Meliponorytes Trigona (Liotrigona) dominicana Wille and Chandler, 1964, Meliponorytes Tosi, 1896:352. Type species: Meliponorytes by original designation. of succini Tosi, 1896, by designation Sandhouse, This from am- 1943:570. species, presumably Oligocene ber from the Dominican Republic, was illustrated Two species were placed in this genus by Tosi and described in considerable detail by Wille and (1896). Both were in Miocene Sicilian amber. Chandler (1964), with additional characters de- The specimens have been destroyed (Wille, scribed and illustrated by Michener (1982). It is a 1977). Schwarz (1948), Kerr and Maule (1964), common fossil and hundreds of specimens are and Zeuner and Manning (1976) give detailed known, all workers. In the Snow Entomological interpretations of Tosi's descriptions and figures. Museum, University of Kansas, is one specimen Schwarz believed that Tosi's figures showed the (in an amber block containing many specimens) inner surface of the hind tibia to be like mat of with the apex of the metasoma open, clearly Melipona while Zeuner and Manning interpreted showing the gonostyli and somewhat less clearly, the same figures to show a structure like that of the sting stylet (Fig. 10). Trigona (Tetragona). Biogeographic considerations The gonostyli are separated by about 1.5 stylar suggest a possible relationship to the African widths at the bases and converge apically. Thev group, e.g., Meliponula. The relation to Meliponula clearly have a few setae, visible along the outer was rejected by Wille (1977) but seems more margin of one gonostylus. Probable setal bases Classification of the Apidae 107

in arc visible on all parts of the gonostyli but against have been described in detail and included are not the pale background the setae themselves keys by Moure (1951, 1961) as well as by visible. There is no evidence of hairlike spicules Wille (1959a). For this reason, although the but thev would be invisible. It seems probably classification is quite changed, no full de- almost certain that the gonostyli are like those of scriptions are necessary here. Comments on most American genera; very clearly they are not each taxon are limited to interesting prob- like those of Liotrigona to which the species was lems and character states, and structures not originally attributed. described by previous authors. Included spe- The sting stvlet in some views is convincingly cies are listed for each and visible, dark in color, slender and acute. If this genus subgenus. and for the smallest taxa, these lists are interpretation is correct, the sting stylet Except those of limited to a few well-known or for some gonostyli considered together resemble Melipona, but no other genus. reason important species, and will serve of near Plebeia The placement Proplebeia by principally to facilitate the work of users of still seems reasonable. As noted Michener (1982) this paper whose collections were identified at that time, the smooth posterior margin of the when most species of the subfamily were inner surface of the hind tibia is broader than in placed in the genus Trigona. More compre- in Plebeia (Plebeia), about as Hypolrigona (illus- hensive lists of included species are found in trated by Michener, 1982). Moreover, the bristles the works cited, or in some cases are not of the rastellum, while strong, are pointed at the ot available. Useful regional keys to su- apices, not blunt as usual in Plebeia. The profile with taxa and to are included the propodeum (Fig. 83) is more declivous, praspecific species less of a subhorizontal basal area, than in Plebeia in the following works: Schwarz (1934), Pan- and most other Meliponinae. If Proplebeia were aina; Schwarz (1937), Borneo; Schwarz be with 1 Recent, there would problems couplet (1938), ; Schwarz (1939a), Indo- below. The first transverse of the key to genera, malayan region; Schwarz (1948), Neotrop- cubital vein is indicated by a strong spur at the ical i-egion; Schwarz (1949), Mexico; end, tapering to a weak line posterior (or basal) Sakagami, Inoue, and Salmah (1985), the definition of the first that completes submargi- Sumatra. nal cell. The veins outlining cell second Cu illustration distally are weak but recognizable (see The following key will be most useful if But as in the by W'ille and Chandler, 1964). attention is given to the geographical infor- of minute vein M of the genera meliponines, mation provided. In certain cases (Pariotri- ends abruptly without a bend (misstated forewing gona and Lisotngona) generic status is as curved by Michener, 1982), and Proplebeia is tentative, pending discovery of males, and minute. It must be noted that veins seem weaker geographic information is essential. in wings preserved in amber (or balsam) than in with vein wings in the air. Except for the problem The key is based primarily on workers. well to Plebeia in the M, Proplebeia runs reasonably Male characters have been added in various key to genera. When "workers" are not from couplets. specified, The principal differences of Proplebeia the character states given apply to males also Plebeia are the acute sting stylet and the broad but are often less well developed in males, so smooth margin of the inner surface of the hind not accom- ^ bris- that identification of a male, tibia, supplemented by the pointed rastellar workers, will often be difficult. des and the straight apex of vein M. Proplebeia panied by males are almost found seems best regarded as a distinct genus. Fortunately always with workers. Queens have been available Taxonomic Account of Recent Genera of for only a few taxa and their characters have Meliponinae not been incorporated into the key or the

The supraspecific taxa of Meliponinae descriptions.

Key to the Recent Genera of Meliponinae

cells and if visible at clear and 1. Hind wing without closed cells, veins closing R Cu, all, unpigmented; forewing with transverse cubital veins almost always completely absent so that there are no indications of submarginal cells; at least distal part of cell second Cu of forewing undefined or defined by completely unpigmented vein traces; vein M of forewing 108 The University of Kansas Science Bulletin

terminating without bend at about position of anterior end of first recurrent vein (1st m- much cu) which, however, is absent (Fig. 168); minute, forewing length less, usually less, than 4 mm (See comment at end of key.) 2 — Hind wing commonly with cells R and Cu closed by at least weakly brownish veins; forewing with one or two transverse cubital veins usually weakly indicated, first submarginal cell usually recognizable; cell second Cu of forewing completely indicated at least by faint veins; vein M of forewing except in some minute species of Plebeia, Trigona least of anterior end of first (Heterotrigona), etc. extending at slightly beyond position recurrent vein and angulate at end of that vein, which is usually at least faintly visible; forewing length commonly (but not always) over 4 mm (See comment at end of key.) . 9

2. Outer surface of hind tibia of worker convex, corbicula and penicillum absent; clypeus much more than twice as wide as long (Africa) Cleptotrigona — Distal part of outer surface of hind tibia of worker flat or concave, forming corbicula; 3 penicillum present; clypeus twice as wide as long or less of 3. Posterior apical part of hind tibia of worker forming distinct angle; gonostyli worker 4 adjacent or separated by one or two gonostylar widths — Posterior apical part of hind tibia of worker rounded; gonostyli of worker minute, tuberculiform, separated by several diameters (Africa) Hypotrigona 4. Australia or New Guinea; scutellum and usually scutum and face with well developed yellow markings Austroplebeia (part) — From other continents; scutellum, scutum, and face in some Neotropical species with white or yellow markings, otherwise without markings or scutellum and edges of scutum sometimes with straw-colored streaks 5 5. Southeast Asia (males unknown) 6 — Africa, Madagascar, and Neotropics 7 6. Malar space almost one fifth as long as eye, much longer than flagellar diameter; gonostylus of worker with setae but without minute hairs Pariotrigona minute hairs — Malar space shorter than flagellar diameter; gonostylus of worker with many (in addition to setae along outer and distal margins) Lisotrigona within 7. Base of marginal cell broad, its basal angle (between stigmal margin and vein r, of worker with marginal ceU) slightly acute (about 68°) to nearly right angular; gonostylus a few setae in addition to minute hairs (Neotropical region) Trigonisca — Base of marginal cell of usual shape, its basal angle strongly acute, not over 50°; 8 gonostylus of worker with setae or minute hairs but not both 8. Gonostylus of worker with minute hairs but no setae (Africa and Madagascar) Liotrigona — Gonostylus of worker with setae but no minute hairs (Neotropics) Plebeia (part) 9. Inner surface of hind tibia with strongly depressed, shining, posterior marginal area which at least apically is usually about as broad as longitudinal median keirotrichiate as keirotrichiate ridge, and midway of tibial length is at least half as wide ridge (Fig. 10 185) less than —Inner surface of hind tibia with depressed posterior marginal area narrow (much to or close to half as wide as area with keirotrichia) or absent, keirotrichia extending 14- margin (Fig. 184) 10. rastellum reduced to hairs America) Trichotrigona Eyes hairy; tapering (South H — Eyes bare; rastellum strongly developed of worker 11. First metasomal segment longer than broad; gonostyli (third valvulae) but without rasteUum of adjacent basally, flattened, with minute hairs setae; consisting tapering bristles (Africa) Dactylunna at bases —First metasomal segment broader than long; gonostyli of worker usually separated but no minute by at least width of a gonostylus, not flattened, with strong setae hairs; Classification of the Apidae 109

rastellum with at least some bristles blunt (Neotropical and Indoaustralian regions). . . 12 12. Face short and broad, minimum distance between eyes much greater than length of eye; clypeus less than twice as broad as long; malar space almost twice as long as flagellar diameter; keirotrichiate zone on inner side of worker hind tibia nearly twice as wide as depressed marginal zone at midlcngth of tibia (Neotropical region) Oxytrigona — Face of ordinary shape, ininimum distance between eyes little more than to less than length of eye; clypeus usually more than twice as broad as long; malar space usually little over 1.5 times as long as flagellar diameter or usually much less; keirotrichiate zone on inner surface of worker hind tibia usually narrower, rarely over 1.5 times as wide as depressed marginal zone at midlength of tibia (Neotropical and Indoaustralian regions) 13 13. Preoccipital carina strong and shining across full width behind vertex; lower face and genal area shining and coarsely punctate in contrast to dull, densely, minutely punctate area and scutum —upper face, genail Cephalotrigona Preoccipital carina absent; lower face and genal area finely sculptured like upper part of head and scutum Trigona 14. First flagellar segment of worker nearly as long as second plus third, of male nearly as long as second; outer surface of hind tibia convex, without corbicula, anterior margin convex like posterior margin; penicillum absent; rastellum consisting of tapering hairs —(Neotropical region) Lestrimelitta First flagellar segment of worker shorter than second plus third together, of male much shorter than second; outer surface of hind tibia of worker (and some males) flat or concave at least distally, anterior margin gently convex to concave, unlike largely or wholly convex posterior margin; penicillum present; rastellum variable 15 15. Gonostylus of worker with setae having strong bases, without minute hairs; rastellum consisting of strong bristles, usually some of them with blunt apices (Neotropical region) 16 — Gonostylus of worker without or with few setae, with numerous minute hairs; rastellum usually consisting of weaker, flexible looking bristles or hairs that taper to attenuated apices and are sometimes plumose (Africa, Australia, New Guinea) 21 16. Hamuli 9-14 (rarely 8); wings extending little if any beyond apex of metasoma; stigma with margin within marginal cell straight or weakly concave (Fig. 162). (Body robust; basal propodeal area dull, hairy) Melipona —Hamuli 5-7, rarely up to 9 or even 10; wings long, extending well beyond apex of

metasoma; stigma with margin within marginal cell slightly convex (Figs. 163-171). . . 17 17. Anterior part of scutellum with longitudinal V- or U-shaped median shining depression opening anteriorly into scutoscutellar fossa (Fig. 190); preoccipital carina present, extending far down laterally on each side of foramen magnum 18 — Anterior part of scutellum without such a median, shining depression (Fig. 191); preoccipital carina absent or with transverse part only, behind vertex and weakly indi- cated 19 18. Head and thorax, or at least scutellum, with extremely coarse, cribriform punctation; posterior margin of scutellum notched or emarginate medially as seen from above; anterior margin of pronotal lobe with strong, transverse carina Nannotrigona — Head and thorax with fine punctation; posterior margin of scutellum entire; anterior margin of pronotal lobe rounded Scaptotrigona 19. Mandible of worker with four apical teeth (lower two sometimes united by translucent septum but teeth still recognizable); scutellum seen in lateral view projecting posteriorly as — thin shelf over median part of metanotum Paratrigona Mandible of worker with (rarely without) one or two denticles at upper end of apical 110 The University of Kansas Science Bulletin

margin, otherwise without teeth; scutellum in lateral view rather thick and rounded, not projecting as thin shelf over metanotum 20 20. Hind tibia of worker greatly broadened, spoon-shaped, about three times as wide as femur, outer surface largely occupied by corbicula (Fig. 187); basal area of propodeum — densely hairy Partamona Hind tibia of worker triangular, not greatly broadened, much less than three times as wide as femur, corbicula extending but little if at adl basad of middle of tibia (Fig. 184); basal area of propodeum usually hairless Plebeia (part) 21. Male genital capsule rectigonal, gonocoxite transverse, much wider than long; gonobase absent New — completely (Australia, Guinea) Austroplebeia (part) Male genital capsule schizogonal, gonocoxite longer than broad; gonobase represented by fragment on each side (Africa) 22 22. Hind tibia of worker rather spoon-shaped, posterior apical angle rounded but with coarse, amber colored to blackish bristles (posterior parapenicillum); sting stylet of worker — distinct, acute Meliponula Hind tibia of worker slender, triangular with distinct posterior apical angle which supports long hairs that are neither especially coarse nor amber colored; sting stylet of worker a mere rounded convexity Plebeina

Note on Couplet 1. This couplet conveniently separates some groups of minute species from the rest of the Meliponinae. Unfortunately, no one of the characters listed is completely reliable. For this reason Plebeia and Austroplebeia can be run both ways. Minute species exist among other genera [e.g., Trigona (Heteroterigona) fuscobalteata Cameron] and various such minute or merely small species possess some of the character states listed in the first alternative of couplet 1, yet should be run with the second alternative. Species such as T. fuscobalteata Cameron would run to 2 although cell second Cu is better defined than in most minute forms; it can easily be distinguished from all of the forms that should go to 2 by the characteristic Trigona-\\V.e inner surface and marginal fringe of the hind tibia. Many specimens oi Plebeia (Plebeia) schrottkyi (Friese) lack the bend at the end of vein M shown in Figure 164, and would easily run to 2; this is why Plebeia can be run through either alternative. P. schrottkyi also lacks closed cells in the hind wing. The narrow depressed shining possterior margin of the inner surface of the hind tibia easily places this species in Plebeia. In Austroplebeia cincta (Mocsary) traces of a transverse cubital vein and of cell second Cu are evident, yet vein M ends without a bend. Some other species of the genus lack such traces and run easily to 2. I have placed this genus in the key twice to take care of this problem. The following character states exclude small species from the first alternative and send them to 9 in the key: (1) Hind tibia with plumose hairs among simple ones along posterior margin (Trigona). (2) Shining posterior margin of inner side of hind tibia absent or less than one third as wide as keirotrichiate zone at midlength of the tibia, except for Cleptotrigona and Pariotrigona. The forms that should go to 2 have the shining, marginal zone at least one third as wide as the keirotrichiate zone except for Pariotrigona (southeast Asia) and the African robber bee, Cleptotrigona, which lacks corbicula and penicillum. (3) Rastellum consisting of strong, usually amber bristles, usually some of them blunt. In forms that should be run to 2 (except Plebeia), the rastellum consists of pallid, flexible, tapering hairs; such rastella also occur in some groups that run to 9, such as Meliponula.

the others until well into the Genus Melipona Illiger present century (see It consists of rather (Figs. 9, 49, 82, 130, 162, 172, 176) Schwarz, 1932). large (8-15

.^ ; , T„- ,onc 1 T- A r rnm long) species, mostly somewhat more robust 1806: 157,n Melipona Illiger, Type species: Apis favosa , { r a ,»,-ii /^r^^«l^ • a* than workers oi Wille and Moure Fabricius, 1798, by designation of Latreillc, 1810: Apis. (1979b) 439. (1951, 1961) tabulated the most distinctive fea- Mehpona (Michenena) Kerr, Pisani and 1967: 139 Ally, tures (as the tribe Meliponini), which include Orfila (not and Rossi, 1956). Type species: Melipona ,u * » j r.*i r u j *u c T • • that extend little it the ol scutellaris, „ . „ ,o,, u 1 J wmgs* any^ beyond apex^ Latreille, 1811, by original designation. . / . ^he slender that is not convex Melipona (Muhmelia) Moure, 1975: 621. New ''name for metasoma, stigma Michenena Kerr, Pisani and Aily. Type species: Meli- within the marginal cell, and 9 to 14 hamuli. The pona scutellaris Latreille, 1811 (autotypic) (new syn- setae of the labial palpus are short and straight. The sting stylet of the worker is right angular or This is the most distinctive meliponine genus acute, sometimes (as in M. fulva Lepeletier, Fig. although it. was not reliably distinguished from 9) as strong as in the African genus Meliponula, Classification of the Apidak 111 and the male genital capsule is schizogonal, the phies, as is the indication of a gonobase in males not Illustrations gonocoxites elongate, transverse. in the form of a slender sclerotic strip. of male genitalia and hidden sterna can be found Melipona also differs from all other Meliponinae in Schwarz (1932), Snodgrass (1941), Camargo, in having the third abdominal ganglion of work- Kerr ers and Lopes (1967), and Camargo, Moure and males (it innervates metasomal segment and Roubik (1988). In the sting stylet and genital 2) in the thorax, the next one in the petiolar characters Melipona resembles the African group region and the last in metasomal segment 3 of genera. Unlike that group, however, the (Willc, 1961; Cruz-Landim et al., 1972). This rastellum is strongly developed with many of the cephalization is an apomorphy of the genus. Also, bristles blunt or abruptly narrowed at apices and the digestive tract is relatively long (Cruz- the worker gonostyli are widely separated, setose Landim and Rodrigues, 1967). and without minute hairs. It is the only Recent In nesting biology, Melipona is unique among genus with such gonostyli and at the same time Meliponinae in rearing numerous small queens with an acute sting and long male gonocoxites. in cells that are identical to worker cells. In all All three of these character states are plesiomor- other genera only a few large queens are pro-

Figures 130-134. Male genitalia of Meliponinae, dorso-ventral views (dorsal at left) and lateral views with gonostylus and (for 130, 131) penis valve omitted or apex omitted. In this and other sets of figures of male genitalia, arrows indicate the basal opening of the gonocoxites into the metasomal 8 — relictual of S8. 131 Plebeia cavity; probable spiculum 130, Melipona fulva Lepeletier. , (Plebeia) frontalis (Friese). 132, Plebeia (Plebeia) schrottkyi (Friese). 133, Plebeia (Plebeia) caerulea (Friese). 134, Partamona near cupira (Smith) rectigonal conformation at left, schizogonal conformation with gonostyli omitted at right. Figures 135-137. Mandibles of male Meliponinae, apices at left. 135, Hypotngona braunsi (K.oh\). 136, Liotrigona mahajalya Brooks and Michener. 137, Trigona (Trigona) fulviventris Guerin. 112 The University of Kansas Science Bulletin

or absence of hairs on the duced in special large cells. Caste determination presence plumose of the hind tibia of workers of Melipona is apparently partly genetic. The posterior margin method of recruitment to resources is also differ- (character 6, Table 2). In Plebeia s. str. there are one or two hairs with a branch or two near ent from that of other Meliponinae. See review by often the of the and in P. Michener (1974). apex posterior margin, caerulea and P. In view of its many autapomorphies, the recog- (Plebeia) (Friese) (Schwarziana) quad- numerous hairs have short nition of a tribe Meliponini for Melipona can be ripunctata (Lepeletier) branches on one side. In Plebeia it is the hairs justified on phenetic bases. Cladistic analysis does long that have such branches; in the hairs not strongly reinforce this tribal arrangement Trigona long are and intercalated shorter hairs are (Fig. 6) and tribal rank does not seem necessary simple for a single genus. usually plumose. The worker are to The division of the genus into two groups by gonostyli adjacent widely Kerr, Pisani and Aily (1967) does not seem to me separated, converging apically, overlapping api- when at setose. The to necessitate subgeneric names. I have therefore cally adjacent bases, sting is rounded or The lancet is included Michmelia as a synonym, but this is a stylet broad, irregular. it is at the in the matter of judgement. short; free apex only subgenus Schwarziana. Melipona ranges from Mexico to and The male of Plebeia s. str. contains about 40 species. The species were re- genitalia (Figs. 131-133 and and and vised by Schwarz (1932) with an important re- Camargo Moure, 1988) view of the classification by Moure and Kerr Schwarziana (illustrated by Schwarz, 1948) are rather (1950). Some well known species are M. beecheii similar, rectigonal [in reality amphigonal at least in P. schrottkyi for which Bennett, /a^na/fl 'LaivuxWe, favosa (Fabricius),/;^/^ (Plebeia) (Friese), both and are Lepeletier, margmata Lepeletier, rufiventris Lep- rectigonal schizogonal preparations at hand all are eletier, and seminigra Friese. (probably species amphigonal)]. Unlike most such forms, the gonocoxites are Genus Plebeia Schwarz nearly as long as broad or longer. In Scaura (see This genus has shiny cephalic and thoracic Schwarz, 1948) the gonocoxites are short and integument with minute [somewhat larger in P. transverse as in most rectigonal (amphigonal) is true of (P.) caerulea (Friese)], well separated punctures, Meliponinae and the same probably varying to dull, densely and minutely punctate, Nogueirapis in view of Wille's (1964) comparison in the subgenus Schwarziana and in P. (P.) schrottkyi of the male genitalia of P. (N.) mirandula (Cock- is with those of of s. str. I have (Friese). The scutellum rounded in lateral view, erell) species Trigona not shelf-like, and often but not always overhangs not seen males of the subgenus Nogueirapis; appar- and hides the median part of the metanotum as ently males are not present in the collection at the seen from above. The scutellum lacks a median Universidad de Costa Rica where Wille's mate- depression in the anterior margin like that of rial is preserved. Nannotrigona and Scaplolrigona, but in some species The forms listed above with dull cephalic and there is a weak indication of such a depression. thoracic integument are not closely related to one The preoccipital carina is weak but present dor- another as judged by tibial and other characters. sally in the subgenus Schwarziana and some spe- In Trigona, also, there is a subgenus with fine, dull cies oi Plebeia s. str. but the lateral parts extending thoracic integument (Lepidotrigona), a subgenus down toward the mandibles are always absent. with a somewhat more shining and less closely The broad area with keirotrichia on the inner side punctate thoracic integument (Papuatrigona), in of the hind tibia extends nearly to the posterior addition to the majority, which are shiny with margin of the tibia but the margin is shiny, well separated, minute punctures. Also in Partam- largely bare (Fig. 184), and abruptly depressed ona there are dull as well as shiny species. The [except not depressed on distal third of tibia of P. idea that this is necessarily a generic or sub- (Scaura) timida (Silvestri) and not at all depressed generic character should be abandoned. in the subgenus Nogueirapis]; the area with kei- Brood cell construction is particularly variable rotrichia may or may not reach the rastellum. in this genus. It is successive in the subgenera The explanation of the inclusion of Nogueirapis as Schwarziana and Scaura, synchronous in most Pleb- a subgenus in the genus Plebeia is given under the eia s. str., and intermediate (starting successively discussion of the subgenus. but becoming synchronous) in Plebeia (Plebeia) A widely used character in Meliponinae is the schrottkyi (Friese) and minima (Friese).

Key to the Subgenera of Plebeia

1. Hind basitarsus thickened, nearly as broad as or broader than tibia. (Face without yellow markings.) Scaura Classification of the Apidae 113

— Hind basitarsus flat, much narrower than tibia 2 2. Body (including metasomal terga) dufl, minutely and closely punctured; I'orewing length about 6 mm; S3 of male with enormous procurved band of erect hooked hairs, behind — which is a concave membranous area with erect hairs Schwarziana Body or at least metasoma shining; forewing length less than 5 mm, usually 4 mm or less; S3 of male vmmodified 3 3. Hind tibia with posterior margin of inner surface narrowly depressed, shining, in sharp — contrast to keirotrichiate area (Fig. 185) Pleheia s. str. Hind tibia with posterior margin of inner surface narrowly shining but not or scarcely depressed Nogueirapis

Subgenus Plebeia Schwarz, s. str. intermedia (Wille) between Plebeia s. str. and (Figs. 11-13, 50, 51, 84, 85, 131-133, 163, 164, Schwarziana. This species is large for a Plebeia s. 184) str., with a rather closely punctured thoracic dorsum and with the scutellum not Trigona (Plebeia) Schwarz, 1938: 480. Type species: extending Trigona mosquito Smith, 1863, by original designation. over the metanotum, features suggesting Schwar- Mourella Schwarz. in Moure, 1946a; 442. Type species: ziana. However, the generally shiny surface, the Melipona caerulea Friese. 1900, by original designation. shiny basal area of the propodeum, etc., are as in Friesella Moure, 1946a: 441; 1946b: 611. Type species: Plebeia s. str. and I that when the male is Melipona schrottkyi Friese, 1900. by original designa- suspect tion. found, it will not have the characteristics of Schwarziana. This is a subgenus of small bees, mostly with Plebeia s. str. ranges from Mexico to Argentina. whitish or yellow markings on the face and There are about 30 several occur in most thora.x. Unlike Scaura, which commonly has a species; areas. The unusual P. (P.) schrottkyi more slender metasoma, that oi Plebeia s. str. is as species, (Friese) and caerulea (Friese), occur in southern broad as the thorax. Except in P. (P.) caerulea and adjacent countries; P. (P.) intermedia (Friese), the labial palpi have five to nine large (Wille) is from . setae. At least one [in P. (P.) frank i (Friese)] is Familiar names are Plebeia caerulea cursed and usually most are curved; in some (Plebeia) (Friese), droryana (Friese), emerina (Friese), /raw/;? species those on segment two are slightly sinuous. (Friese), frontalis jatiformis (Cockerell), Two unusual species have received genus- (Friese), minima (Friese), mosquito (Smith), remota (Holm- group names. Mourella was proposed for a rather berg), schrottkyi (Friese), and tica (Wille). large, robust species with the head and thorax dark blue-green (the only metallic meliponine), P. Schwarziana Moure caerulea (Friese), with the mesoscutum a little Subgenus 14, more coarsely punctate than in other species, and (Figs. 52, 86) with hairs on the basal area of the propodeum Trigona (Schwarziana) Moure, 1943: 147. Type species: except medially. Unlike other Plebeia s. str., the Melipona quadnpunclala Lepeletier, 1836, by original designation. scape of the worker is long, reaching to within one ocellar diameter of the median ocellus, and large I have retained this name for a large species setae are absent on the labial palpi, the hairs (body length 7 mm) that suggests in body form being short and straight. Friesella was proposed for and pale markings a large Plebeia s. str. with a a tiny species, P. schrottkyi (Friese). It has the minutely punctate, dull body (including the meta- dull mesoscutum with small close punctures and somal terga). The dorsal propodeal area has a few lacks yellow marks on the face; such marks on the hairs. The most remarkable features are those of thorax are absent in males, in workers there is the male sterna, which are highly modified as commonly a weak pale line next to the tegula and illustrated by Schwarz (1948); see also above key sometimes a spot on the axilla. The wing vena- to the subgenera. The base of the propodeum is tion is much reduced (see note after key to hairy, unlike other subgenera except for P. (Pleb- While these two genera). species are clearly quite eia) caerulea (Friese). The scape is long, reaching different from I ordinary species oi Plebeia, doubt nearly to the median ocellus, as in P. (P.) caerulea. if subgcneric names are needed for them. Mourella The male genitalia are similar to those oi Plebeia s. was described and illustrated by Schwarz (1948). str. (see Schwarz, 1948; Camargo, 1974). The of s. Descriptions Plebeia str. (and of the mono- lack of large setae on the labial palpi (numerous typic Friesella and Mourella, here synonymized) short straight setae present) might be a plesiomor- were given by Moure (1951). phic feature. Thus this could be the sister group Wille (1960) emphasized the intermediacy oi P. to the subgenus Plebeia as here understood. Full 114 The University of Kansas Science Bulletin

and mirandula and descriptions were given by Moure (1951) and Camargo), (Cockerell), ranges from Costa Rica to Bolivia. In addition, it in- Camargo (1974). cludes the Miocene fossil Plebeia The single species, Plebeia (Schwarziana) quadri- species (Nogueir- silacea from southern Mexico. punctata (Lepeletier), is found in Brazil (Goiaz apis) (Wille, 1959b) and Minas Gerais southward), Paraguay, and Scaura northern Argentina. Subgenus Schwarz (Figs. 15, 53, 87) Subgenus Nogueirapis Moure Trigona (Scaura) Schwarz, 1938: 479. Type species: (Figs. 16, 88) Trigona laliiarsis Friese, 1900, by original designation. Partamona (Nogueirapis) Moure, 1953: 247. Type species: Schwarzula Moure, 1946a: 439. Type species: Trigona Trigona butteli Friese, 1900, by original designation. timida Silvestri, 1902, by original designation.

has hitherto been either as a Nogueirapis placed This subgenus differs from other Meliponinae of /'artowo;!^ 1953, or as subgenus (Moure, 1982) in the hind basitarsi which are nearly as broad as with Par- an independent genus. The association to broader than the tibia and convex on the outer tamona is an error. It differs from that in the genus surfaces, at least apically, as illustrated along with and hind ordinary (not enlarged spoon-shaped) other character states (including those of male tibia of the worker as well as small size, abundant genitalia and sterna) of the latitarsis group by the few and curved yellow markings, mostly Schwarz (1948). These are small bees; P. timida setae of the labial (as in (none sinuous) large palpi (Silvestri) has the form of a Plebeia s. str., the various oi Plebeia s. str. and the species ), shining others have variably more slender metasomas, and hairless basal area as was indicated propodeal very slender in P. tenuis (Ducke) and longula Wille The detailed of by (1964). descriptions (Lepeletier). An interesting feature, best devel- Plebeia and Wille in all Nogueirapis by (1959) agree oped in P. (S.) latitarsis (Friese), is the series of details as follows: is said to except (1) Nogueirapis flat, curved bristles on the posterior margins of S4 have the posterior apical angle of the worker hind and S5 of the worker. The head and thorax are tibia Plebeia s. it rounded, str., angular. Actually black, without the yellow markings characteristic is in both and some of Plebeia s. angular species of nearly all species of Plebeia s. str. The body str. have the tibia almost as in exactly Nogueirapis. surface is shining with small, scattered punctures The inner surface of the hind tibia of (2) Nogueir- like those of most Plebeia s. str. Unlike nearly all has a narrow, bare, but not apis shiny, depressed species oi Plebeia s. str., the labial palpi lack large whereas it is in Plebeia posterior margin depressed setae; the setae are rather short and straight. A s. str. This last character state has been the full description oi Scaura was given (as a genus) by hallmark of Plebeia and would exclude Nogueirapis Moure (1951). from Plebeia. No one character, however, should The subgenus consists of two units that differ alone determme the classification, especially in a considerably. P. (S.) timida (Silvestri) has more group so noted for convergence as the Meliponi- plesiomorphies, as shown by the two denticles on nae. Moreover, P. (Scaura) timida (Silvestri) is the part of the apical mandibular margin intermediate in this character, which is also vari- upper and the less broad hind basitarsi which are only able within the genus Meliponula. In view of the weakly convex on the outer surface. Unlike other many similarities between Plebeia s. str. and No- species of the genus Plebeia (except Nogueirapis), gueirapis, I regard them as congeneric. the posterior margin of the inner surface of the Inclusion of Nogueirapis in the genus Plebeia hind tibia is not depressed in the apical third or results in a genus (Plebeia) with no known diag- fourth of the tibia. P. timida has been placed in a nostic apomorphies. The depressed posterior monotypic genus or subgenus Schwarzula. The hind tibial margin is a probable synapomorphy other species of Scaura have untoothed mandibles for the rest of the genus. However, this character (or the two denticles near the upper end of the state is probably subject to reversals. A partial apical margin are barely perceptible), broader reversal is likely for P. (Scaura) tirnida (Silvestri) and more convex hind basitarsi, and a fully and polarization of this character is not at all depressed inner posterior margin of the hind tibia convincing in the genus Meliponula. Thus the as in Plebeia s. str. P. timida appears to be the sister condition in Nogueirapis could be derived from to all other species oi Scaura, and I have elected to that in other groups of Plebeia instead "^f the include it in Scaura, thus synonymizing Sch- reverse. It is therefore best to place Nogueirapis on warzula. the basis of its close phenetic resemblance to to Brazil Plebeia s. str., while hoping for the discovery of Scaura ranges from southern Mexico relevant synapomorphies. and Bolivia; there are four species, Plebeia (Scaura) tenuis This subgenus contains three species, Plebeia latitarsis (Friese), longula (Lepeletier), (Nogueirapis) butteli (Friese), minor (Moure and (Ducke), and timida (Silvestri). Classification of the Apidae 115

Genus Partamona Schwarz countries. Familiar species are Partamona bilineata helleri (Figs. 17, 18, 57, 89, 134, 187, 191) (Say), cupira (Smith), (Friese), peckholti (Friese), testacea (Klug), and zonata (Smith). Ex- Trigona (Patera) Schwarz, 1938: 475 (not Lesson, 1837; as otherwise the references to and not Albers, 1850). Type species: Melipona testacea cept indicated, Klug, 1807, by original designation. illustrations of "Partamona near cupira" are based Schwarz, 1939b: 23. Trigona (Partamona) Type species: on Mexican specimens that are probably P. bi- testacea 1807 and Atelipona Klug, (autobasic original lineata. designation). Replacement ibr Patera Schwarz, which is preoccupied. Genus Schwarz Trigona (Parapartamona) Schwarz, 1948: 428. Type spe- Paratrigona cies: zonata Smith, 1854, Trigona by original designa- (Figs. 19, 55, 90) tion. Trigona (Paratrigona) Schwarz, 1938: 487. Type species: This genus is composed of relatively robust Melipona prosopiformis Gribodo, 1893. Moure, 1951: 60. forms superficially suggestive of Scaptotrigona, Paratrigona (Aparatngona) Type spe- cies: Melipona impunctata Ducke, 1916. some of s. str. etc. Partamona species Trigona , differs from such forms by having yellowish face This genus contains small species with the head marks (often restricted), by the rather dense and thorax (often also the abdomen) dull with covering of erect hair on the basal propodeal area, extremely minute punctation and with conspic- and by the hind tibial structure of workers. This uous yellow to white markings on the thorax and tibia is greatly broadened, about three times as usually on the face. As in Nannotrigona and Scapto- wide as the femur, spoon-shaped, the outer sur- trigona, the scutellum is produced posteriorly as a face mostly occupied by the enormous corbicula thin shelf hiding the median part of the meta- (Fig. 187). There are two hairs, often about as notum as seen from above. The scutellum, how- long as the tibial width and often apically wavy, ever, lacks the anteromedian depression arising from the posterior part of the corbicula. characteristic of those genera. The proboscis is The inner surface of the tibia has the broad unusually long, the first segment of the labial keirotrichiate area extending nearly to the poste- palpus being about three times as long as the rior margin, which is shining but not depressed. second which is about six times as long as wide. The worker gonostyli are mere rounded tubercles The eight or nine large setae of the labial palpi are with a few setae or in P. zonata (Smith) about 1.5 strongly curved. The preoccipital carina is com- times as long as broad. The sting stylet is pletely absent. The inner surface of the hind tibia rounded, the lancet is moderately long and the has the broad keirotrichial area extending nearly distal part free of the membrane, or almost absent to the posterior margin which is not depressed. in P. zonata. The male genital capsule is amphi- There are two unusually long hairs (about as long gonal [both conformations seen in P. cupira as tibial width) arising from the posterior part of the (Smith), Fig. 134]. It is illustrated here as well as corbicula; this is suggestive of Partamona but by Snodgrass (1941). The large setae of the labial less conspicuous than in that genus because the palpus are about 11 to 13 in number, mostly tibia is narrower. The four-toothed mandibles of sinuous but some only curved. workers distinguish this genus from all Meliponi- In most species the cuticle is shining with nae except Trigona (Trigona); the two lower teeth minute, widely separated punctures. In P. zonata, may be united by a thin septum, however, so that the type species of Parapartamona, however, the the mandibular profile looks like that of an ordi- cuticle is dull and exceedingly minutely punctate nary meliponine with the two denticles on the or roughened. Other species that have the ex- upper part of the apical margin unusually large. tremely long wings of Parapartamona have inter- Full descriptions are given by Schwarz (1948) and mediate cuticular structure, or even as in P. Moure (1951), and Schwarz gives an illustrated grandipennis (Schwarz), cuticle like that of typical account of the species, including figures of male Partamona. For these reasons I do not think that genitalia and hidden sterna. Parapartamona should be recognized as a sub- The worker gonostyli are widely separated, genus. A full description of Partamona was given setose, convergent apically. The sting stylet is by Moure (1951) and oi Parapartamona by Moure broad, rounded and the lancet, if present, is a (1953). mere strip in the membrane. The male genital Partamona has not been revised as a whole but capsule is rectigonal, but may well be really the Parapartamona group was dealt with by Sch- amphigonal. No specimens with the schizogonal warz (1948) and the species with testaceous bodies conformation have been seen, however. by Camargo (1980). Moure (1951) separated two unusually robust The genus, with about 16 species, ranges from species as a subgenus Aparatrigona. There is no Mexico to central Brazil and , but appears to doubt that they constitute a monophyletic unit be absent from southern Brazil and adjacent that is the sister group to the rest of the genus. 116 The University of Kansas Science Bulletin

The are They possess plesioniorphies relative to other may be permanent. genitalia strangely those of The species such as a partly smooth metasoma and similar to Trigona (Tetragonisca). large of the labial are about relatively abundant hair (other species are nearly setae worker palpi few, 10, of the are nude). I doubt that Aparatrigona is sufficiently sinuous. Full descriptions genus given his and different from Paratrigona s. str. to necessitate by Moure (1951) under genus subgenus recognition of the subgenus for only two species. Nannotrigona. looks like a It is noteworthy that in P. opaca (Cockerell) S6 Nannotrigona deeply punctate, pitted Pkbeia s. str. Thus it is different in of the male is a plate entirely without the apical quite appear- ance from the robust As process usual in meliponines and found in other larger, Scaptotrigona. Schwarz and Wille species of Paratrigona. A somewhat intermediate emphasized by (1938:483) however, and condition exists in P. prosopiformis (Gribodo), in (1959a, 1979b), Nannotrigona Scapto- share numerous character states and I do that S6 is broader than usual and the apical trigona not doubt their close process triangular (see illustrations of Schwarz, relationship. is so distinctive that Cockerell 1948). These character states are not associated Nannotrigona with other distinctive features and additional (1922), who was generally conservative in such matters, named it as a distinct while leav- supraspecific taxa do not seem to be desirable for genus other in the these species. In Trigona (Heterotrigona) also there ing Meliponinae except Melipona About nine from is a species, T. (H.) apicalis Smith, with S6 similar genus Trigona. species range Mexico to southern Brazil and The to more anterior sterna; see also Trigona (Homo- Paraguay. most familiar is testaceicornis tngona). Nannotrigona Lep- eletier. Paratrigona ranges from Mexico to Argentina. There are about a dozen see the revision species; Genus Scaptotrigona Moure by Schwarz (1948). Familiar names are Paratri- (Figs. 21, 54, 92, 139, 140, 190) gona impunctata (Ducke), lineata (Lepeletier), opaca Trigona (Scaptotrigona) Moure, 1942: 315. Type species: (Cockerell), and peltata (Spinola). Trigona postica Latreille, 1807, by original designa- tion. Genus Nannotrigona Cockerell (Figs. 20, 56, 91, 138) These are among the most robust of the Meli- The head and thorax are rather Nannotrigona Cockerell, 1922: 9. Type species: Melipona poninae. strongly testaceicornis Lepeletier, 1836. punctate, more coarsely so than in Plebeia and its This genus is characterized by the very strong, relatives (although approached in coarseness by usually cribriform punctation of the head and Pkbeia caerulea Friese) and with shining ground thorax or at least the scutellum; the scutellum between the punctures. As in Nannotrigona the produced posteriorly as a thin shelf (side view) scutellum is produced as a thin shelf (side view) hiding the median part of the metanotum in hiding the median part of the metanotum from dorsal view; the notched or emarginate apex of above. Also as in Nannotrigona there is a shining the scutellum (dorsal view); the presence of a depressed V or U-shaped median depression on shining, depressed V- or U-shaped median de- the anterior margin of the scutellum (Fig. 190) pression in the anterior margin of the scutellum and the preoccipital carina and hind tibia are also (as in Fig. 190); the straight lateral clypeal mar- as described for Nannotrigona. Scaptotrigona differs gins (concave in most other Meliponinae); the from Nannotrigona not only in form and puncta- distinct preoccipital carina, laterally extending tion but also in the rounded apex of the scutellum down toward the mandibles, although weak dor- (seen from above) and the rounded anterior solaterally; the strong transverse carina across the margin of the pronotal lobe. A full description of anterior margin of the pronotal lobe; the distinct the genus is given by Moure (1951) as a subgenus (although not carinate) angle between the ante- of Nannotrigona. rior and lateral surfaces of the mesepisternum; The worker gonostyli are setose, convergent and the broad area of keirotrichia on the inner apically. The sting stylet is broad and irregularly side of the hind tibia, extending to or nearly to the rounded and the lancet, if present at all, is short posterior margin of the tibia which is not abruptly and fades into the membrane. The male genital depressed, and extending apically to the bases of capsule is schizogonal in specimens of iS. pectoralis the rastellar bristles. The worker gonostyli are (Dalla Torre) and rectigonal in 5. mexicana short, separated at the bases by less than a stylar (Guerin). Probably it is really amphigonal in width, strongly convergent and overlapping dis- both. The setae of the labial palpus are short and tally. The sting stylet is broad and rounded, the straight. lancet absent. The male genital capsules exam- Most character states oi Scaptotrigona are plesio- ined are schizogonal, very thick, with the spatha morphic relative to Nannotrigona although the nearly vertical; the schizogonal conformation larger size and robust form may be derived Classification of the Apidae 117

Figures 138-143. Male genitalia of Meliponinae, dorso-ventral views (dorsal at left), or separate dorsal and ventral views for Lestrimelitta, and lateral views with gonostyli omitted, penis valves also = omitted in Figures 138 and 139. Arrows are explained with Figures 130-134; s spatha. 138, Nannotrigona testaceicornis (Lepeletier), gonostylus omitted on ventral view. 139, Scaptotrigona bar- rocoloradensis (Schwarz), gonostylus omitted on ventral view, schizogonal conformation. 140, Scaptotri- gona mexicana (Guerin), right gonostylus omitted, rectigonal conformation. 141-143. Lestrimelitta Imiao (Smith), dorsal, lateral (gonostylus omitted, attachment indicated by jagged line), and ventral views.

features. The genus is so distinct from the highly Meliponinae, especially species of the genera derived Nannotrigona that it is reasonable to recog- Plebeia and Nannotrigona, more rarely Melipona, nize it at the genus level. Moreover, the worker- Scaptotrigona and Trigona; they even attack weak laid trophic eggs of Scaptotrigona are much larger colonies of Apis. As in other forms that do not than eggs of the queen, while in Nannotrigona they forage from flowers, there are only short, straight are not so large. This is no doubt an apomorphy setae on the labial palpus. of Scaptotrigona, supporting the view that the two Unlike nearly all other Meliponinae, S6 of the are sister groups. male lacks a median apical process and has Scaptotrigona contains about two dozen species instead a small notch. S7 has a broad, squarish and ranges from Mexico to Argentina. Familiar body. Both S6 and S7 have long basolateral species are Scaptotrigona hellwegeri (Friese), mexicana apodemes (see illustrations by Schwarz, 1948).

(Guerin), pectoralis (Dalla Torre), postica These features seem ancestral (i.e., more like (Latreille), and tubiba (Smith). more basal sterna) relative to the specialized or reduced of these sterna in other Genus Lestrimelitta Friese aspects Meliponi- nae. However, it seems unlikely that a robber (Figs. 22, 58, 93, 141-143, 165) genus would preserve archaic structure, for its Trigona (Lestrimelitta) Friese, 1903: !361. Type species: habits and the related features such as loss of the Trigone limao Smith, 1863 (monobasic). corbicula and rastellum are obviously derived. Like Cleptotrigona, this is a robber genus. The Another explanation is that since genes for ordi- workers do not forage except in nests of other nary sterna are obviously present, a developmen- 118 The University of Kansas Science Bulletin tal change could lead to their control of the more lower paraocular areas; the long malar space of the one third as as the apical sterna as well as the preceding ones. The worker (about long eye); external generic character states were listed by the convex genal area of the worker, providing of the bifid Schwarz (1948), Moure (1951) and Wille space for the posterior ramus deeply the abun- (1979b). mandibular gland (Michener, 1974); The male genital capsule is probably perma- dant, large, straight setae on the labial palpus of nently rectigonal; unlike other rectigonal and the worker, a feature unique in the Meliponinae; amphigonal Meliponinae except some Plebeia, the the simple hairs of the posterior margin of the gonocoxites are about as long as broad, thus not hind tibia; the largely vertical propodeal profile that of the strongly transverse. The male gonostyli are (quite different from Trigona); and shorter than in most Meliponinae and broadly worker gonostyli which are four or five times as fused to the gonocoxites (Fig. 141 and Schwarz, long as wide, converging distad, separated at or and 1948). The worker gonostyli are a little longer their bases by three more stylar diameters, than broad, separated basally by a little more bearing numerous setae. Unique among Melipo- is than the than a gonostylar width, convergent distally, and ninae the short second valvifer, shorter lancet of the is with setae (without minute hairs). The sting stylet gonostylus (Fig. 23). The sting is broad and blunt and the lancet, although short, almost invisible, and may not be realistically has the apex free of membrane. illustrated in Fig. 23. As in many species of The hind tibia of the worker, on the inner Tngona, the genital capsule is rectigonal but surface, has only a narrow, slightly depressed, probably in reality amphigonal; the gonocoxites marginal zone without keirotrichia, suggesting are strongly transverse. Schwarz (1948) listed the tibia is included and de- Plebeia (Plebeia). This may be because the species (as varieties) provided not flattened and expanded posteriorly as in tailed descriptions and illustrations of Oxytrigona; forms with a corbicula. However the keirotrichi- Camargo (1984) added species and raised some ate area is broad; this combined with the nar- varieties to the species level. Moure (1951) de- rowness of the marginal zone may indicate scribed the genus comparatively. is the secretion of the derivation from an ancestor of Plebeia (Plebeia). An attribute of interest The rastellum is reduced to tapering hairs. mandibular glands which contain formic acid Lestrimelitta consists of possibly ten species (Roubik, Smith and Carlson, 1987). Workers, in into the skin of an (mostly unnamed), of which L. limao (Smith) is nest defense, bite this liquid best known. The genus is widespread in the intruder, causing painful and long-lasting lesions "fire Neotropical region — Mexico to Argentina. In- in human skin (Michener, 1974). The name is therefore in use for this . cluded species were described and illustrated by bee" wide contains about related Schwarz (1948), Moure (1951), Wille (1979b), Oxytrigona eight closely to Bolivia and and Roubik(1980). species ranging from Mexico southern Brazil. 0. tataira (Smith) is the best Genus Oxytrigona Cockerell known of these species. (Figs. 23, 68, 94)

Trigona (Oxytrigona) CockereW, 1917a: 124. Type species: Genus Cephalotrigona Schwarz Tngona Jiaveola medioruja Cockerell, 1913, by original designation. (Figs. 24, 65, 67, 95, 166, 172)

ScYiv^dirz. 1940: 10. This genus is closely related to Trigona and Tngona (Cephalotrigona) Type species: Tngona capitata Smith, 1854, by original designation. could be considered a subgenus of that genus. Oxytrigona has several striking character states of This genus is closely related to Trigona and its own, however, and Trigona has at least one could be considered a subgenus of that genus. probable synapomorphy (the narrower, better The body seems more strongly sclerotized than in defined keirotrichiate band) that usually distin- Trigona. Unique features include (1) the strongly, guishes it from Oxytrigona and suggests that Oxytri- coarsely punctate and shining clypeus, lower gona is the sister genus of Trigona plus supraclypeal area, lower paraocular area, and Cephalotrigona. When this character state fails in lower genal area contrasting with the dull, reticu- Trigona, the marginal depressed zone is nonethe- late frons, the dull, closely punctate vertex and less quite broad. In Oxytrigona it is narrower, scutum, and the extremely dull and minutely suggestive of that of Plebeia although not so punctate upper genal area; (2) the distal margin narrow as in that genus. of the mandible of the worker which has a single Noteworthy features of Oxytrigona include the large tooth at the upper extremity, separated by a following: the short, wide face (see key to genera); broad, shallow concavity from the rest of the the small clypeus, widely separated from the eyes; margin which is edentate; and (3) the strong, the shining but distinctly punctate clypeus and shining preoccipital carina across the interocular Classification of the Apidae 119 width of the head. The large, broad mandibular zone without keirotrichia, usually about as wide tooth is more like the upper tooth of the mandible as the elevated zone, at least toward the apex of the tibia of Trigona (Trigona) than the one or two small or (Fig. 185). In Trigona the slope separat- sharp teeth (denticles) on the mandibles of most ing the keirotrichiate ridge from the smooth zone Meliponinae. It may not be homologous to such behind it is abrupt (except in the subgenera denticles. Additional interesting features are the Lepidotrigona and Papuatrigona) and extends basad as a channel to the following: The keirotrichiate, median, elevated shining nearly base of the zone of the inner surface of the hind tibia is about tibia. The male genitalia and hidden sterna are as wide as the shining marginal zone and sepa- similar in many members of the genus to those of as shown illustrations of rated from it by a gentle slope, not an abrupt one; Oxytrigona, by Schwarz 144 this slope fades away in the basal fifth of the tibia (1939, 1948) and Figures to 150; they are rather than continuing as a channel nearly to the known to be amphigonal in some species and tibial base. The propodeal triangle has conspic- probably are in others. However, in the subgen- uous hair bases and, like the rest of the propod- era Geotrigona, Tetragonisca, and Homotrigona the eum, abundant plumose hairs. S6 of the male has genital capsule is probably permanently schiz- a short median process and lateral processes ogonal and the gonocoxites about as long as or about as long as the median one (see illustrations broad longer than broad (Figs. 145, 146). The in Schwarz, 1948). The male genitalia are rec- gonostyli of the workers are setose, without min- ute hairs. tigonal (probably amphigonal) with extremely They vary from about 1.5 to 6 or 7 short, broad gonocoxites. The labial palpus of times as long as broad. They vary even within workers and males has abundant short, straight species groups. Thus within the iridipennis setae and lacks large setae. (Tetragonula) group of the subgenus Heterotrigona, in carbonaria are less 1.5 Cephalotrigona could be merely a specialized T Smith they than times as as little derivative of Trigona, in which case it probably long broad and separated by more than should not receive generic status. However, the one stylar length while in T fuscobalteata Cameron better defined keirotrichiate band of Trigona is they are about twice as long as broad and sepa- probably an apomorphy suggesting that Cephalo- rated by about two stylar lengths. The gonostyli are trigona is the sister group of Trigona. S. F. typically separated by two or more stylar as diameters and In Sakagami (in litt.) regards Cephalotrigona a basally converge apically. T subgenus of Trigona because he considers its (Frieseomelitta) nigra Cresson and T (Trigona) cilipes differences from Trigona to be no greater than (Fabricius), however, the gonostyli are separated differences among some subgenera of that genus. by one basal stylar diameter or less (Figs. 27, 34). In This was my opinion also early in the develop- T cilipes [but not in other species of Trigona ment of this work, but rather arbitrarily and for (Trigona), e.g., amalthea (Olivier), chanchamayoensis the reasons indicated above, I have decided to Schwarz, and julinventris Guerin], the gonostyli recognize it at the generic level. Sakagami notes diverge apically (Figs. 33, 34). that the oviposition behavior, with frequent The sting stylet is ordinarily a mere convexity "body insertions" by workers alternating with but in T. (Tetragona) lurida Smith (Fig. 31) its inspections by the queen of the cell in which she lateral margins are at an acute angle to one will oviposit, is similar in Cephalotrigona and Tri- another although the apex is broadly rounded and the gona (Tetragona, Frieseomelitta part, Duckeola and in T. (Trigona) cilipes (Fabricius) (Fig. 34) sting s. str. is rounded at the The Trigona ). stylet only narrowly apex. and The characters of the genus are well illustrated stronger, longer stylet in the last two species be related by Schwarz (1940, 1948) and described com- the diverging gonostyli in T cilipes may these later- paratively by Moure (1951). The genus contains to the elongate metasomas of species, about three species (listed as varieties by Sch- ally compressed in T cilipes. warz, 1948) and is found from Mexico to Argen- The lancets of the sting are ordinarily much lie in the sometimes tina. Cephalotrigona capitata (Smith) is the best reduced and membrane, invisible. \r\ known species. being transparent and almost T (T) amalthea but not in T. Genus (Olivier) (T) cilipes (Fabri- Trigona Jurine free cius), etc., the apices of the lancets are of the This is the largest and most widely distributed membrane. genus of Meliponinae. It is distinguished from all Trigona is found in the Neotropics from Mexico other genera except Oxytrigona, Cephalotrigona, and to Argentina and in the Indoaustralian region the superficially similar Dactylurina by the inner from and to Taiwan, east to the surface of the hind tibia of the worker which has a Caroline Islands (introduced?), the Solomon Is- longitudinal elevation covered with keirotrichia, lands, and south throughout and New behind which is a depressed shining marginal Guinea to about latitude 34°S in Australia. 120 The University of Kansas Science Bulletin

In several subgenera of Trigona there is a well- their large hind basitarsi as convergent rather defined sericeous area of short, dense, easily lost than as a synapomorphy. of hairs (Fig. 184) on the base of the inner surface In most species of Trigona the scutum is shining the hind basitarsus. Such an area is present in with minute, widely separated punctures. In the workers, and in some subgenera, in males also. It subgenus Lepidotrigona it is dull with minute, is not a generic characteristic since it is altogether dense punctures, as in the genus Cephalotrigona. absent, the surface being uniformly setose, in Papuatrigona is intermediate with minute punc- some subgenera. Any bee with the sericeous area, tures separated by about a puncture width of however, belongs to the genus Trigona. Inter- shiny ground. estingly, the worker of Dactylurina staudingeri (Gri- The two teeth of the upper part of the apical bodo) but not D. schmidti (Stadelmann) has a margin of the worker mandible are large and weakly ditferentiated approach to such a sericeous occupy about half of the mandibular margin in T. area. (Homotrigona) fimbriata Smith, but they are nearly In the great majority of species of Trigona and as large in the Heterotrigona groups of T apicalis hairs in all those in the Americas, some of the Smith, reepeni Friese (the only member of the are along the rear margin of the hind tibia Tetragonula group with large teeth), and canifrons plumose (Fig. 184). No other Meliponinae except Smith. T (Tetragona) lurida (Ptilotrigona) from the for the African genus Dactylurina have such hairs. Neotropical region has similarly large teeth. (There are a few on the distal part of the margin There seem to be no other characters that associ- Plebeia. This in some species of Aieliponula and ) ate these large-toothed species. T (Heterotrigona) characteristic is therefore useful in generic recog- itama Cockerell and erythrogastra Cameron in nition of most species of the genus. southeast Asia have only one such tooth. As is The subgenus with the hairs on the posterior well known, the species of Trigona (Trigona) have margin of the hind tibia all simple, Lepidotrigona, four or usually five mandibular teeth. has sometimes been given generic status. Because T (Tetragona) lurida (Ptilotrigona) in the Neo- it is basically similar to the other subgenera, and tropics and T (Heterotrigona) planifrons Smith, because Papuatrigona has plumose hairs only on flaviventris Friese, keyensis Friese (Platy trigona) and the apical sixth of the posterior tibial margin and canifrons Smith (Lophotrigona) in southeast Asia are is thus intermediate, I have chosen not to do so. unusual in the hairy basal area of the propodeum, As noted below, Papuatrigona is also intermediate a feature that crops up several times in unrelated between Lepidotrigona and the other subgenera in Meliponinae and does not even characterize all

scutal sculpturing. Lepidotrigona and Papuatrigona species of the planifrons group (i.e., Platytrigona) . differ from the remaining subgenera (and agree The American and Asiatic species show no other with the genus Cephalotrigona) m the less sharp significant similarities and probably evolved the distinction between the elevated keirotrichiate hairs independently; the Asiatic groups may also zone on the inner surface of the hind tibia and the have evolved such hairs independently. shiny margin. In Lepidotrigona and Papuatrigona An architectural character that has received the area with keirotrichia is not abruptly elevated. attention in classification of the genus Trigona is In the genus Cephalotrigona the same is true. In the arrangement of the brood cells. Various species genus Oxytngona it is more abruptly elevated but is arrange the cells in combs. In the iridipennis group unusually wide, so that at the middle of the tibia it (Tetragonula), however, most species arrange cells is much wider than the depressed, shiny, mar- in clusters although some (e.g., T carbonaria ginal zone. A broad keirotrichiate zone is also Smith) make combs and others are intermediate found in some forms clearly placed in Trigona (7^ hockingsi Cockerell) (see Michener, 1961). T Frieseornelitta also such as T. (Heterotrigona) carbonaria Smith and canifrons Smith and the subgenus their cells in clusters. the clus- planifrons Smith, but in such species the zone is arrange Probably more elevated and its delimitation extends almost ter arrangement within the genus Trigona is de- to the base of the tibia (see couplet 1, key to rived, presumably independently in the subgenera). Indoaustralian and American taxa, the ancestral Workers of the genus Oxytrigona and of Trigona pattern being horizontal combs. (Lepidotrigona) have unusually broad hind In most subgenera of Trigona brood cell con- basitarsi, convex on the outer surfaces, thus struction is successive (Sakagami, 1982), a pre- but in the suggesting Plebeia (Scaura). In Oxytrigona and in sumed plesiomorphic state, subgenus species of Lepidotrigona without greatly broadened Lepidotrigona and in T. (Frieseornelitta) fiavicornis tibiae, such as T. (Lepidotrigona) terminata Smith, (Fabricius) but not other species of its subgenus, the basitarsal width is about equal to the width of it is synchronous. It is intermediate, initially the tibia at midlength. In view of the dissimilarity successive but becoming synchronous, in the of Oxytrigona, Lepidotrigona, and Scaura, I regard subgenus Duckeola. Classification of the Apidak 121

Key to the Subgenera of Trii^ona

all or 1. Hairs along posterior margin of hind tibia of workers and males simple some median zone of plumose only on apieal iifth or sixth of margin; elevated, keirotrichiate inner surface of hind tibia separated from shining posterior marginal zone by gentle 2 slope — Hairs along posterior margin of hind tibia of workers and some males partly plumose (in or three branches so some species of Geotrigona the few branched hairs may have only two that plumosity is inconspicuous); elevated, keirotrichiate median zone of inner surface of hind tibia separated from shining marginal zone by abrupt slope 3 2. Head and thorax dull with minute close punctures; propodeal dorsum finely reticulate; scutum with posterior margin of hind tibia of worker without plumose hairs; margined whitish, densely plumose ("scalelike") hairs (Southeast Asia) Lepidotrigona — Head and thorax shining although with minute, rather close punctures; propodeal dorsum hairs smooth, shining; posterior margin of hind tibia of worker with plumose among hairs bristles on apical fifth or sixth of margin; scutum without conspicuous plumose (New Guinea) Papuatngona 3. Mandible of worker with 4 or 5 teeth along distal margin; inner surface of hind basitarsus of males and workers with basal sericeous area (Neotropical region) Trigona s. str. — Mandible of worker with lower half or two thirds of distal margin edentate, upper part of male without margin with one or usually two teeth; inner surface of hind basitarsus of basal sericeous area, of worker variable (Neotropical region; Asia to Australia) 4 4. Metasoma short, dorsoventrally flattened, about as wide as thorax; posterior margin of hind tibia of w^orker usually with few plumose hairs, most of them with only two to six scattered branches not concentrated toward apices; yellow markings absent; vein M of forewing dark almost to wing margin (Neotropical region) Geotrigona of — Metasoma usually narrower than thorax, often noticeably elongate; posterior margin hind tibia of worker with numerous strongly plumose hairs, usually with abundant of branches toward apices; yellowish or reddish markings present on face some Neotrop- widest of ical species; vein M of forewing usually fading away near part wing (Neotropical 5 region; Asia to Australia) 5. Inner surface of hind basitarsus of worker with basal sericeous area covered with minute 6 setae or sometimes lacking setae (Fig. 184) — Inner surface of basitarsus of worker rather uniformly setose, without basal sericeous area ' 6. S6 of male with median apical process very broad and long so sternuin is much longer than broad (Neotropical region) Tetragomsca — S6 of male much broader than long (Indoaustralian region) Hcterotrigorm 7. S6 of male a broad sternum without apical process (Southeast Asia) .... Horfiotngona form — S6 of male with median apical process of the usual slender, heavily sclerotized (male 8 oi Duckeola unknown) (Neotropical region) 8. Posterior margin of vertex elevated as strong, hairy ridge between summits of eyes; Duckeola posterior distal angle of hind tibia of worker acute worker — Posterior margin of vertex not elevated; posterior distal angle of hind tibia of broadly rounded 9 Frieseomelitta 9. Labial palpi with large, sinuous setae on first two segments or so — Labial palpi with setae no longer than palpal width and straight nearly Tetragona

Schwarz described and illustrated the Subgenus Lepidotrigona Schwarz (1939a) main features of this subgenus; Moure (1961) (Fiffs 25 ' 96)

• listed included ~. /r •. ,c u ,n^n 1QO T described it comparatively and TriPona 1939a: 1.52. . • (Lepidotrigona) Schwarz, lype spe- ^, , ,• , -i These are delicate bees similar to many cies: Tngom nitidiventris Smith. 1857, by original species. designation. species of the subgenus Heterolrigona, but differing 122 The University of Kansas Science Bulletin not only in the character states listed in the key result of convergence; all these characteristics are but also in the mostly dull, minutely roughened apparently results of a single tendency in facial integument and, in males, in the pair of long development. The unique vestiture of the labial of spines on S5 [but see T. (Heterotngona) itama palpus Oxytrigona (abundant long, straight is not shared which has Cockerell]. S6 is more like an ordinary sternum setae) by Papuatrigona, than in most other males, having a moderately about eleven large, sinuous setae, thus falling of large disc with the median process short and within the range of variation Heterotrigona. The well con- triangular, as illustrated by both Schwarz (1939a) worker gonostyli are setose, separated, and Sakagami (1975). The genital capsule is vergent; the second valvifer is not unusually short it is in the keirotrichiate rectigonal, probably actually amphigonal. The as Oxytrigona. While ridge labial palpus of the worker has about 18 large, is similar in breadth in Oxytrigona and Papuatri- sinuous setae (or some merely curved); this is gona, it is abruptly defined in the former, not in within the range of variation found in Heterotn- the latter. gona. The hind tibia of the worker especially of T. Features distinguishing Papuatrigona from Heter- nitidiventris Smith and trochantenca Cockerell, is otrigona and Homotngona include the tibial char- slender, expanded apically, thus "racket- acter states listed above and also, for Heterotrigona, shaped," a convergence with some species of the the lack of a sericeous area on the inner surface of New World subgenus Frieseomelitta. the hind basitarsus. Papuatrigona is most similar to This subgenus of about four species (plus color Lepidotrigona, which also lacks the sericeous variants) occurs from India to the and basitarsal area. Lepidotrigona has the head and Taiwan, south to Sumatra, Borneo and Java. thorax dull with minute, dense punctation. The Included species are Trigona (Lepidotrigona) nitidi- surface is less dull and the punctation less dense ventris Smith, terminata Smith, trochantenca Cock- in Papuatrigona, which also lacks the areas of S. F. hairs erell and ventralis Smith (list provided by dense, highly plumose ("scalelike") found hairs Sakagami, in litt.). in Lepidotrigona. Lepidotrigona has plumose among simple hairs on the posterior apical angle Papuatrigona Michener and Subgenus of the hind tibia but not extending along the Sakagami posterior margin. The inner surface of the hind (Figs. 26, 97, 195, 196, 198, 199, 201-205, 207, tibia is alike, however, in the two subgenera. The 208-210, 212-219) longer malar area, wider face and interalveolar Michener and see Papuatrigona Sakagami, Appendix. space, smaller mandibular teeth, smooth basal Type species: Trigona genalis Friese, 1908, by original propodeal area, smaller corbicula, etc., as de- designation. tailed in the Appendix, all differentiate Papuatri- This is described in the subgenus (which fully gona from Lepidotrigona. at first seems to lack hairs on Appendix) plumose This subgenus includes only one species, Tri- the posterior of the hind tibia, but such margin gona (Papuatrigona) genalis Friese. It is known only hairs are hairs on the distal present among simple from New Guinea. Details of its character states fifth or sixth of the tibial The keirotrichi- margin. are given in the Appendix. ate ridge on the inner surface of the hind tibia is Moure nearly twice as wide as the depressed marginal Subgenus Geotrigona zone, and the slope from the ridge to the marginal (Figs. 28, 98, 145) zone is gentle, the ridge not being high; distally Trigona (Geotrigona) Moure, 1943: 146. Type species: mombuca 1863. there is almost no slope, the ridge being un- Trigona Smith, defined and scarcely higher than the zone behind This subgenus consists of robust black species, it; proximally the slope is more distinct and superficially resembling because of the short, extends well into the basal fourth of the tibia. The broad metasoma some of the black species of outer surface of the hind basitarsus has a poste- Partamona, Scaptotrigona, and Trigona (Trigona). rior basal concavity behind a longitudinal, The Geotrigona group was included in Tetragona by curved, hairy ridge (Figs 207, 210) as in Lepidotri- Wille (1979b) and others and it is closely related gona and many species of Heterotrigona, suggesting to that subgenus. In both, the hairs of the labial a relationship with those subgenera, and also with palpi are short and straight. Geotrigona differs, Homotngona which also has such a concavity. Such however, not only in the body form but in the a basitarsal concavity also occurs in the American relatively short legs (hind tibia much shorter than genus Oxytrigona which Papuatrigona resembles in cell R of forewing) and the sparseness of branched certain features. The broad face, long malar hairs, and of the branches themselves, on the space, and broad clypeocular space, so unusual posterior margin of the hind tibia. The branches and distinctive of Oxytrigona, are all approached in are scattered along the hairs, not concentrated Papuatrigona. I presume this resemblance is a toward the apices. These hairs are especially Classification of the Apidae 123

sparse and with few branches in T. (G.) acapulconis and contains about four species, of which Trigona Strand, and are thus intermediate between the (Tetragonisca) angustula Latreille, buchwaldi Friese, simple hairs of the preceding subgenera and the and pfeijferi Friese are well known. strongly plumose hairs of Heterolrigona, Homotri- A characteristic of workers of Tetragonisca is the gona, Tetragonisca, Tetrigona, and Trigona s. str. The extremely small corbicula, the concavity being male genital capsule is schizogonal, probably limited to the apical fifth of the tibia and not permanently so, the gonocoxites being at least as occupying the full tibial width. The same feature long as broad {T. momhuca Smith examined). characterizes the subgenus Frieseomelitta which, Moure (1951) described the external features of however, lacks the sericeous area on the inner the subgenus comparatively. surface of the hind basitarsus. Species included in This subgenus contains a few similar species these two groups are listed by Wille (1962). The and ranges from Mexico to Argentina (Santiago African genus Dactylurina has equally reduced del Estero). Well known names in this subgenus corbiculae. This must be an independently de- include leu- Trigona (Geotrigona) acapulconis Strand, rived feature in Trigona and Dactylurina, probably and mombuca also cogastra Cockerell, (Smith). independent in the Trigona subgenera Tetrago- nisca and Frieseomelitta. Intermediates between Subgenus Tetragonisca Moure such small corbiculae and large ones occur in (Figs. 30, 72, 100, 146) various groups of the subgenera Tetragona and Tetragonisca }^\o\iTC, 1946; 438. species: Trigonajaty Type Heterotrigona. Smith, 1863 {= Trigona angustula Latreille, 1811). Subgenus Tetragona Lepeletier and Serville This is one of a group of subgenera separated (Figs. 31, 69, 101, 102, 147, 149) from Tetragona with some hesitation. It consists of small, slender species, and is the only Neotropical Trigona (Tetragona) Lepeletier and Serville, 1828: 710. Type species: Trigona elongala Lepeletier and Serville, group other than Trigona s. str. with a sericeous 1828 = ( clavipes Fabricius, 1804) by original area on the base of the inner side of the hind designation. basitarsus of the not the worker (but male). The Trigona (Ptilotrigona) Moure, 1951: 47. Type species: labial palpus differs from that of the subgenus Trigona heideri Friese, 1900 {= Trigona lurida Smith, 1854) by original designation. Tetragona in having 12 to 15 large, sinuous setae; there are no large setae in Tetragona. In this This subgenus as here limited consists of long- respect Tetragonisca resembles Frieseomelitta. Males legged bees, similar in form to Tetragonisca and at least of T (Tetragonisca) angustula Latreille differ Frieseomelitta but somewhat less delicate. The hind from Tetragona in the probably permanently schiz- tibia is nearly as long as cell R of the forewing. ogonal genital capsule and from all other Melipo- Ptilotrigona is based on a distinctive species, differ- ninae in the enormous (broad and long), not ing from the rest of the subgenus in its large size, especially sclerotized, median apical process of large mandibular teeth (two, on upper part of 86, making the sternum much longer than broad, apical margin), and hairy propodeal triangle. The and in the elongate S7, reaching beyond the apex amount of difference is probably not enough to of S6. The male genitalia are unusual for Trigona justify subgeneric rank for a single divergent to F. (but interestingly similar the very different species, but J. M. Camargo (in litt.) tells me of genus Nannotrigond) in the great thickness of the two undescribed species of Ptilotrigona. One could genital capsule with the spatha almost vertical easily justify recognizing it as a subgenus. Com- (Fig. 146). External characteristics are listed by parative descriptions are provided by Moure Moure (1951). (1951). The male metasomal character states are ap- Tetragona differs from the Indoaustralian Hetero- omorphies that suggest that Tetragonisca is derived trigona in the uniformly setose inner surface of the from Tetragona, leaving the latter paraphyletic. hind basitarsus of the worker, and in lack of large However, given the widespread occurrence of the setae on the labial palpi (palpal setae are short sericeous area on the hind basitarsus (Heterolri- and straight). See also the discussion o{ Heterotri- gona, Trigona s. str., and Tetragonisca), it seems gona. Given the similarity of Tetragona and Hetero- quite possible that it is lost in Tetragona, so that trigona it is necessary to compare the species Tetragonisca and Tetragona could be sister groups. groups of both of these subgenera, along with S. F. Sakagami (in litt.) notes that the oviposition Duckeola, Frieseomelitta, Geotrigona, Tetragonisca, and behavior of Tetragonisca is very different from that Homotrigona, to see if some other classification of Cephalotrigona and Trigona [Duckeola, Frieseome- makes more sense. The variation among the litta (part), Tetragona and Trigona s. str.]. Without species groups is kaleidoscopic, each character knowledge as to the polarity of these characters, it seemingly distributed differently from the others. is difficult to use them in classification. Moure's (1961) tabulation of character states of Tetragonisca ranges from Mexico to Argentina the Indoaustralian groups shows the lack of con- 124 The University of Kansas Science Bulletin

Figures 144-150. Male genitalia of Meliponinae, dorso-ventral views (dorsal at left, dorsal and ventral for 145 and 150), gonostylus usually omitted from ventral views, lateral views with gonostyli omitted, apex of penis valve omitted in lateral 145, 146, 149. Arrows are explained with Figures 130-134. 144, Trigona (Frieseomelitta) nigra paupera Frovancher. 145, Tngona (Geotrigona) mombuca Smith, gonostyli omitted from ventral view. 146, Trigona (Tetragonisca) angustula Latreille. 147, Trigona 149. (Tetragona) clavipes (Fabricius). 148. S6 of Trigona (Heterotrigona) apicalis melanoleuca Cockerell. Trigona (Tetragona) lurida Smith. 150. Trigona (Trigona) fulviventris Guerin. Classification of the Apidae 125 cordancc among characters. The same is observ- the worker with the posterior apical angle able with the American groups. strongly produced apicad and acute, and in the in 7" about 20 setae of the labial which are Male genitalia are rectigonal (Tetragona) large palpi in a male of T. at most about 1 .5 times as as the clavipes (Fabricius) and schizogonal only long palpal are curved or sinuous. (T.) lurida Smith; probably they are really amphi- width, yet mostly slightly In other with curved or sinuous gonal. meliponines About 13 species of I'etragona are found from setae, these setae are much longer. Mexico to Brazil. Well known species are Trigonn Two species, Trigona (Duckeola) ghilianii Spinola dorsalis are found in Brazil. Males are (Tetragona) clavipes (Fabricius), Smith, and pavani Moure, lurida Smith, and perangulata Cockerell. unknown.

Subgenus Frieseomelitta von Ihering Subgenus Homotrigona Moure (Figs. 27, 71, 99, 144) (Fig. 110)

Frieseomelitta von Ihering, 1912: 5. Type species; Tngona Homotrigona Moure, 1961: 200. Type species: Trigona silveslrii Friese, 1902 (monobasic). fimhriata Smith, 1857, by original designation.

This subgenus consists of slender, delicate- Like Duckeola, Frieseomelitta, Geotrigona, Hetero- in sub- this is looking species that agree with Tetragona trigona, and Tetragonisca, subgenus sepa- of hesitation. The generic attributes except that the labial palpus rated from Tetragona with some the worker possesses many (19-23 in species male shows plesiomorphic features (especially S6) are for the examined) large, sinuous setae. Such setae that suggest this as a possible outgroup in It reasonable to absent in Tetragona, although present Tetrago- rest of Trigona. therefore seems nisca. give it subgeneric status. Other phenetically dis- Frieseomelitta is further distinguished from all tinctive groups, such as the group of T (Heterotri- other American groups of the genus— Tngona in the gona) itama Cockerell, are distinguished by clearly arrangement of the brood cells in clusters rather derived, autapomorphic features and are not than in combs. This architectural character does recognized here at the subgenus level. not separate subgenera among the Indoaustralian Homotrigona consists of rather large, robust Tngona and in the genus Plebeia, but appears to do species with the metasoma short. The two man- so in American Tngona. Another architectural dibular teeth are large, occupying the upper half character state of Frieseomelitta is the elongate of the distal mandibular margin, and are along a their storage pots. Elongate storage pots are also found the mandibular axis so that line between of of the in the genus Trigonisca and in some species apices is almost parallel to the long axis Trigona (Heterotrigona). mandible. Homotrigona is the only Indoaustralian The male genitalia are rectigonal in T. (F.) subgenus of Trigona except Lepidotrigona and Papu- the base of nigra Cresson and silvestrii Friese (see Camargo atngona that lacks the sericeous area on are and Moure, 1988); probably in reality they the inner side of the hind basitarsus; in this amphigonal. respect it resembles the American subgenera Frieseomelitta contains about ten species and Duckeola. Frieseomelitta, and Tetragona. The most ranges from Mexico to Brazil. Well known spe- unusual feature is S6 of the male, which is a cies are Trigona (Frieseomelitta) nigra Cresson, sil- rather ordinary looking sternum, without traces vestrii Friese, and vana Lepeletier. of the heavily sclerotized median apical process usual in Meliponinae. Lestrimelitta, Paratngona Duckeola Moure Subgenus opaca Cockerell but not other species of the genus, (Figs. 70, 103) Trigona (Heterotrigona) apicalis Smith and its rela- = of Duckeola Moure, 1944a; 72. Type species: Trigona huberi tives (i.e., the Odontotrigona Tetrigona group 1901 Friese, {—Tngona ghiliann Spinola, 1853) by Heterotrigona) but not other species of that sub- original designation. genus, and Trigona (Lepidotrigona) also have S6 in the last it has a tri- This subgenus consists of a large, rather robust broad although short, These forms do not species, so different from other Tetragona-\\kc bees angular median process. related to another. that it must be placed in its own subgenus. It seem closely one The shape setal of S6 are so in resembles Tetragona in lacking a sericeous area on and pattern similar, however, the inner surface of the hind basitarsus of the males of Homotrigona and T. (Heterotrigona) apicalis indicate a worker. It differs from Tetragona and all other Smith (Fig. 148) that they must com- subgenera in the strong, hairy ridge on the mon origin. To judge by bees in general, this condition should be but see com- posterior margin of the vertex between the sum- plesiomorphic, on this character under Lestrimelitta. Prof. S. mits of the eyes (this is different from the shiny, ment F. to the com- hairless carina in a similar position in the genus Sakagami has called my attention absence of a in the male of Cephalotngona), in the rather slender hind tibia of plete spatha genitalia 126 The University of Kansas Science Bulletin

the the setae and Homotrigona, a character state shared with straight only moderately long. for these hind basitarsal and char- genus Dactylurina and with the Tetragonula and Except palpal labial there are no other known attributes Platytrigona groups of Heterotrigona. The acters, group that differentiate from I palpus of the worker has the large setae long and Heterotrigona Tetragona. Asiatic of decided to be- straight; in nearly all other species hesitantly recognize Heterotrigona and cause of these character states the first is Trigona at least one or two are curved, (only and because it occurs on the frequently they are sinuous. entirely reliable) The external character states o{ Homotrigona are other side of the world from the neotropical given by Moure (1961) and those of the male by Tetragona. The are in T Sakagami (1963). Moure listed the included taxa, genitalia rectigonal (Heterotrigona) itama Smith probably representing a single species, Trigona Cockerell, apicalts (Tetrigona), atripes Smith moorei Schwarz (Homotrigona) jimbriata Smith, that ranges from (Tetragonilla), (Trigonella), west to Vietnam and south to Sumatra and various representatives of the iridipennis and Borneo. group (Tetragonula), varying to schizogonal among other species of the group (Sakagami, 1978; Subgenus Heterotrigona Schwarz Sakagami and Inoue, 1985, 1987). Among all the 29, 32, 73, 104-109, 111, 148, 184, 197, (Figs. above, the appearance of the genitalia suggests 200, 206, 209) that each species is amphigonal, i.e., capable of Schwarz, 1939a: 96. Trigona (Heterotrigona) Type species; either the rectigonal or schizogonal conformation. itama Cockerell, 1918, by original designa- Trigona the of tion. Unfortunately type species Heterotrigona, itama is aberrant relative to Platytrigona Moure, 1961: 203. Type species: Trigona T (H.) Cockerell, planifrom Smith, 1864, by original designation. nearly all of the rest of the species. Workers have Moure, 1961: 205. Type species: Trigona Lophotngona only one denticle instead of two on the upper part canifrons Smith, 1857, by original designation. of the apical mandibular margin. Males have a Tetragonula Moure, 1961: 206. Type species: Trigona and hind iridipennis Smith, 1854, by original designation. greatly enlarged apically pointed tibia; 1961: 210. Tetragonilla Moure, Type species: Trigona much shortened small segments of the hind tar- Smith, 1857, by original designation. atripes sus; long, thickened, and only briefly cleft hind Geniotngona Moure, 1961: 212. Type species: Tigona claws; and long, fingerlike lateroapical processes thoracica Smith, 1857, by original designation. S5 These character states Odontotngona Moure, 1961: 213. Type species: Trigona on (Schwarz, 1939a). haematoptera Cockerell, 1919, by original designa- were the basis for Heterotrigona, a name which tion. heretofore has been used only for T. (H.) itama Ttrigona Moure, 1961: 215. Type species: Trigona api- and erythrogastra Cameron, along with various calis Smith, 1857, by original designation. Males of the Tigonella Sakagami and Moure, in Sakagami, 1975: 57. probable synonyms (Moure, 1961). mono- Type species; Trigona moorei Schwarz, 1939, by group of T. (H.) moorei Schwarz (Trigonella) have typy. hind legs and other features somewhat modified This subgenus contains minute to moderate- in the direction of T. (H.) itama as shown by sized Indoaustralian bees with a sericeous area on Sakagami and Inoue (1987). The same is true for the base of the inner side of the hind basitarsus of T thoracica Smith (Geniotngona), at least insofar as workers but not in males. The unity of Heterotri- the hind tarsi are concerned (Sakagami and In- the gona and Homotrigona is indicated, however, by the oue, 1989). These findings support placement as itama. frequently concave surface of the posterobasal of other groups in the same subgenus T have shown in part of the hind basitarsus, this area being delim- Sakagami and Inoue (1989) of what 1 call ited anteriorly by a low ridge bearing a row of greater detail the close relationship the thoracica hairs (the "additional" row of hairs of the pollen itama, moorei, and species groups. of Smith and press, Wille, 1979a; Figs. 206, 207, 209, 210). The males T (H.) apicalis other This structure is weakly developed or unrecog- melanoleuca Cockerell (Tetrigona), differ from I in which is an nizable in small species. Contrary to Wille, do species oi Heterotrigona S6, ordinary a distal area of coarse not find it in any American species of Trigona, but looking sternum with large it is not short and it is present in Oxytrigona. Another character that hairs (Fig. 148); heavily is useful although not decisive in separating the sclerotized with a median apical process as in Indoaustralian species from Tetragona is the setae other Heterotrigona and most other Meliponinae. see of the labial palpus. In Tetragona there are no large In this respect they resemble Homotrigona; that setae. In Heterotrigona and Homotrigona there are comments on this character under subgenus. large setae and at least one or two are curved; The name Heterotrigona is used here in a broad frequently most are curved or sinuous. All inter- sense, as the oldest name for the various species gradations occur from about six with only one or groups listed in the above synonymy. Of these, two curved to about 35, mostly sinuous. Only in several are monotypic or probably so; only the than T. (H.) canifrons among Indoaustralian species are iridipennis group (Tetragonula) contains more Classification of the Apidae 127

in the well as see two or three species. The named taxa group (as Lepidotrigona, Sakagami, Females of T. atricornis cannot be in synonymy appear to represent natural groups or 1975). placed do not seem ditlerent with could be in the single distinctive species but Platytrigona certainty; they I have of enough to recognize at the subgenus level. Trigonella subgroup Heterotrigona. not seen males of all of them, however, and male There are some 36 species in this subgenus. sub- and characters might indicate recognition (at the They were listed by Moure (1961) Sakagami of Moure's are abundant in southeast Asia genus level) of more genera. (1978). They Sakagami and Khoo (1987) have already united including Borneo and Sumatra. The number of diminishes westward to three in Tetragunula and Tetragonilla. Detailed descriptions species only of external features are provided by Moure (1961) India, one of which reaches Sri Lanka; few and illustrations of genitalia and other structures species are found east and south to the Philip- and and Australia to by Schw^arz (1939a), Sakagami (1978), pines, Solomon Islands, (south Sakagami and Inoue (1985, 1989). about 34°S). The subgenus also occurs in the it is to have been Prof. S. F. Sakagami (in litt.) has kindly given Caroline Islands, where likely the me his opinions about the classification of introduced. It apparently does not reach Taiwan. in Hetewtri- in such as Sri species of Trigona that I have placed The species marginal regions in full with his most of and Australia are all in the gona. While I am not agreement Lanka, India, of view that five subgenera should be recognized iridipennis group {Tetragonula). Familiar species instead of one, I recognize his groups and present Heterotrigona are those listed above as type species his conclusions as follows: oi Heterotrigona and its synonyms, and those listed of five To this list Group 1. Heterotngona {T. itama Cockerell, eryth- in the above account subgroups. moorei be added carbonana Togaster Cameron), Trigonella {T. Schwarz, may Trigona (Heterotrigona) lieftincki Sakagami and Inoue), Geniotrigona {T. Smith and fuscobalteata Cameron. thoracica Smith). Similarity of these three sub- Species not included by Moure (1961) are T and from Kai and groups are indicated in a paragraph above by (Heterotrigona) keyensis Friese, 1901, from Sakagami and Inoue (1989). New Guinea and atricornis Smith, 1864, with colora- Group 2. Odontotrigona and Tetrigona {T. apicalis New Guinea. They are largely red, Smith, haematoptera Cockerell, melanoleuca Cock- tion like that of T (Papuatrigona) genalis Friese, but are no of Heterotri- erell and peninsularis Cockerell). There are members of the planifrons group to of that major differences among these species justify gona. T. keyensis differs from members S6 two subgroups. See the comments above about group listed by Moure and from his characteriza- of the male. tion of the group ("genus Platytrigona'") in the Like malar Group 3. Lophotrigona {T. camfrons Smith). wider interalveolar space; much shorter its of most species of Tetragonula, this species places space (about two thirds flagellar diameter); brood cells in clusters rather than combs. ocelloccipital distance about equal to ocellar di- and Group 4. Tetragonula (numerous species) ameter; scutellum not surpassing metanotum; and bifurcation of veins and Cu well Tetragonilla (four species). See Sakagami M beyond cu-v; Khoo, 1987. This group differs from others ex- etc. Thus it reduces the distinctness of Platy- dis- For identification of T I am cept number 3 by the exaggerated posterior trigona. keyensis F. For informa- placement of the scutellum (Figs. 108, 109). indebted to Prof. S. Sakagami. Sakagami recognizes seven subgroups in tion on T atricornis, see Appendix. Tetragonula. Subgenus Trigona purine s. str. 5. Platytngona. Recognized by Moure Group (Figs. 33, 34, 66, 74, 75, 112, 113, 137, 150, 167, the basis of the (1961) on medially hairy pro- 172, 185) but this character is variable. podeal triangle amallhea Trigona Jurine, 1807: 245. Type species: Apis three Sakagami recognizes subgroups: a, Olivier, 1789, by designation of Latreille, 1810: 439. 1815: 123. Platytrigona sensu Moure (7^ planifrons Smith, Amallhea Rafinesque, Unnecessary replace- ment name for Trigona Jurine. Type species: Apis flavtventris Friese, keyensis Friese), recognized by amallhea Olivier, 1789, autobasic. the hairy propodeal triangle; b, T hobbyi Schwarz wnth the middle of the propodeal triangle glabrous The principal characteristics of this subgenus and without strong bristles on the vertex and and the included species were well illustrated by scutellum; and c, T. atricornis Smith with a pro- Schwarz (1948) and Camargo and Moure (1988) podeum like that of Papuatrigona, i.e., hairless and were listed comparatively by Moure (1951). Place- male and associated sterna of T. dorsally except for small lateral patches. The genitalia illustrated ment of T atricornis is based on the male genitalia, cilipes (Fabricius) were (as T compressa this and which have a long neck joining the midbasal part Latreille) by Snodgrass (1941) and of The of the penis valves with the median articulation of other species by Schwarz (1948). genitalia but for the gonocoxites. This is as in the planifrons sub- were shown in most cases as rectigonal, 128 The University of Kansas Science Bulletin others as schizogonal. As noted above, both Genus Trichotrigona Camargo and Moure for T. amalthea conformations are known (T.) (Figs. 76, 114) and (Fabricius), and doubtless all (OHvier) pallens Trichotrigona Camargo and Moure, 1983: 421. Type There are species are in reality amphigonal. only species: Trichotrigona extranea Camargo and Moure, two taxa of Meliponinae with the distal margin of 1983, by original designation. the mandible of the worker toothed in its lower This genus, known from a single nest collection and often for its full — part (Fig. 172) length in Amazonas, Brazil, was well described and s. str. and The teeth are best Trigona Pamtrigona. illustrated by Camargo and Moure (1983). It has in the former, and are either four or developed many features of Trigona (Frieseomelitta) including five in number. Sometimes in T. (T.) cilipes cluster rather than comb arrangement of its brood the distal teeth are united a thin (Fabricius) by cells. The keirotrichiate ridge on the inner surface the dentate is still distinct septum, but margin of the hind tibia is as in Frieseomelitta and most from the convex with at most two denti- margin other subgenera of Trigona, with the shiny con- cles near its as in most upper end, Meliponinae cave channel marking its posterior margin ex- 1 The labrum differs from other (Fig. 72). Melipo- tending onto the basal fourth of the tibia. J . M . F. ninae in that the is to a distinct apex produced Camargo has kindly sent me a sketch of the sting s. str. have a angle. Males and workers of Trigona rudiments and associated structures of Trichotri- basal sericeous area on the inner side of the hind gona. The structure is similar to that illustrated basitarsus. Such an area occurs elsewhere in only here for Trigona (Heterotrigona) carbonaria Smith workers of the subgenera Tetragonisca, Tetrigona, (Fig. 29) but with the gonostyli longer, as in T and The labial of workers have Heterotrigona. palpi (Frieseomelitta) nigra Cresson (Fig. 27). six to about 38 sinuous setae, large, mostly except Extraordinary features of Trichotrigona are (1) that in T. and its relatives there are hypogea only the hairy eyes and unusually hairy body and setae. short, straight wings, with most of the hairs of the body coarse, Trigona s. str. is found from Mexico to Argen- almost bristle-like, not plumose; (2) the short, tina. It contains about 30 species, or more as broad second segment of the labial palpus, about sibling species are recognized. Well known spe- as broad as long and only somewhat over one cies are Trigona (Trigona) amalthea (Olivier), cilipes fourth as long as the first segment [large setae on (Fabricius), corvina CockereW, fulvivenlris Guerin, these segments few (about 5) and straight]; (3) the fuscipennis Friese, hyalinata Lepeletier, hypogea Sil- rudimentary penicillum and the replacement of vestri, nigerrima Cresson, pallens (Fabricius), sil- the rastellar bristles with slender, tapering hairs; vestnana Vachal, and williana Friese. The (4) the slender, parallel-sided, hind basitarsus of subgenus was revised by Schwarz (1948). the worker (nearly four times as long as broad) Various species of this subgenus are attracted with all its hairs directed apicad (i.e., without the to carrion (Baumgartner and Roubik, 1989) and posteriorly directed hairs and associated ridges probably use it as a supplementary protein source near the base that contribute to the pollen press as well as for nest construction. The group of T. function in most Meliponinae; Wille, 1979a); (5) (T) hypogea Silvestri does not collect pollen, uses the lack of plumose hairs on the posterior margin carrion as its protein source, lacks large palpal of the hind tibia except at its apex where it rounds setae, has reduced corbiculae, and has relatively onto the convex apical margin of the tibia, which narrow hind tibiae (Schwarz, 1948; Roubik, has numerous plumose hairs; (6) the presence of 1982). numerous, scattered, rather short hairs on the surface of the corbicula in addition to a few As noted previously, Trigona prisca Michener longer the robust front tibia covered on the and Grimaldi (1988a, b) from the New Jersey hairs; (7) surface with Upper Cretaceous was placed in Trigona s. str. on outer coarse, weakly spatulate hairs; the bare the basis of the single known worker specimen. It and (8) flattened, pointed, projection has toothed mandibles similar to those of ordi- suggestive of a pygidial plate on T6. Males of are unknown. nary specimens of T (Trigona) cilipes (Fabricius). Trichotrigona rastellum and and lack The hairs on the posterior margin of the hind The reduced penicillum of structures of the hind tibia are probably simple, unlike most Trigona, pollen press basitarsus, hairs on the but there may be a few, sparsely plumose ones as the presence of rather numerous and also the in Trigona (Geotrigona) acapulconis Strand. The surface of the corbicula, perhaps that the gonostyli are invisible in the fossil. In view of the labial palpus as described above suggest impressive convergence of external characteristics only species, Trichotrigona extranea Camargo and is bee like Lestrimelitta and in some Meliponinae, it could be that T. prisca is Moure, a robber convergent with rather than closely related to Cleptotrigona or possibly the only known melipo- Trigona s. str. nine social parasite. The single known colony was Classification of thk Apidae 129

several setae but without minute found in the Amazon valley as a nest of Trii^ona (Fig. 35) hairs; those of all other African have min- (Frieseomelitta) paranigra Schwarz was being Meliponinae ute hairs. The is a mere opened; the relation if any to the paranigra colony sting stylet convexity. lancet is in the membrane. A is unknown: no connection was observed. Three The insignificant, of the workers from the nest of 7] cxtranca had remarkable feature is the fusion of the second ac- valvifer with the The pollen on the corbiculae and hind basitarsi eighth hemitergite. strongly the bidentate male mandible is like that of cording to J. M. F. Camargo (in lilt.). Ciiven (Fig. 135) families of bees but unlike that of hind tibiotarsal structure, it is not clear how they many other the other The setae of the labial would get pollen onto the corbicula using Meliponinae. palpus short and The external char- usual apid movements (Michener, Winston and are straight. generic acter states were listed in detail Moure Jander, 1978). One could imagine, however, by (1961). nest on The mandibular and sternal characteristics of placement of sticky pollen from the host male could be If so, the hind legs in the same way that meliponines Hypotrigona plesiomorphous. then the alternative characters of other manipulate and carry resin. Meliponi- nae would be that Probably Trichotrigona is a derivative of Trigona apomorphies showing Hypotri- the latter is the sister to all the other (Frieseomelitta). If so, its existence makes gona group genera. the transverse male and the genus Trigona paraphyletic taxa. Tnchotri- However, short, gonocoxites, the reduced are gona is so distinctive, however, that generic status wing venation, etc., apomorphies tolerate shared of the other for it is justified. Even those who do not by only part meliponine of It therefore seems to paraphyletic taxa should hesitate until males genera. premature place its cladistic is as the first branch of the Trichotrigona are known and position Hypotrigona meliponine clearly ascertained. J. M. F. Camargo (in litt.) is cladogram. is a The mesoscutum is dull; in the worker strongly of the opinion that Trichotrigona typically of the hind tibia is relictual type not closely related to Frieseomelitta in the posterior apical angle and the scutellum spite of common character states. absent, i.e., broadly rounded; is wholly dark. These are character states that Cockerell Genus Hypotrigona usually distinguish Hypotrigona from other minute how- (Figs. 35, 60, 115, 135, 151) Meliponinae. Brooks and Michener (1988), ever, were unable to certain workers Trigona (Hypotrigona) Cockerell. 1934: 47. Type species: distinguish Trigona gribodoi Magretti, 1884, by original designa- from Liotrigona on the basis of these and other tion. characters. Dissection of the workers shows that This is one of the genera of minute stingless their Sp. 2 is a Hypotrigona; the gonostylar charac- bees that exhibit (convergendy) the character teristics were not known to these authors in 1988. states listed in couplet 1 of the above key to Hypotrigona is widespread and abundant in isolated — south to An- genera. It is, however, a distinct and tropical Africa Ghana to Kenya, — a genus (with the possible exception that Pariotri- gola and Natal although represented by only in gona, unknown in the male, may be related). few species. It does not occur Madagascar. Character states unique within the Meliponinae Included species were listed by Moure (1961), include the apical process of S5 of the male who, however, had not seen and did not place combina- (considered to be S6 by Brooks and Michener, Hypotrigona magrettii (Friese, 1900) new in 1988) which is not especially heavily sclerotized tion. It is the smallest Hypotrigona, about 2 mm and lies horizontally in the concavity of S6 (S7 in body length. The type specimen (from Accra, like 1988); the U-shaped S6 with strong basolateral Ghana) has a dull, closely punctate scutum, apodemes like those of more anterior sterna; and that of typical Hypotrigona; the posterior apical are the form of S7 (S8 in 1988) which is a transverse angle of the hind tibia is rounded; there no bar with a small, median, basal angle. The pale streaks on the scutellum; and I have not sternal characteristics were illustrated by Brooks examined the worker gonostyli. Well known spe- braunsi and Michener (1988), who interpreted what I cies are Hypotrigona araujoi (Michener), believe is the apical process of S5 as S6 fused to (Kohl) and gribodoi (Magretti). S5. The male genital capsule is illustrated by the Genus Pariotrigona Moure same authors, and in Figure 151. It is rectigonal (Figs. 36, 63, 116) but unique among Meliponinae in the completely Moure, 1961: 192. Trigona dorsal basal opening of the gonocoxites and the Pariotrigona Type species: pendleburyi Schwarz, 1939, by original designation. largely membranous basal bulb of the penis valves. The male gonostyli are freely articulated This is another genus of minute Meliponinae, of in 1 of but do not break off easily. The gonostyli sharing the character states listed couplet from workers are minute to papilliform, not flattened, the above key to genera. As it is known only separated by several times their lengths, with workers, its generic status and its position relative 130 The University of Kansas Science Bulletin

Figures 151-155. Male genitalia of Meliponinae, dorsal (at left), ventral, and lateral views (dorso- ventral for Figs. 152 and 155). Arrows are explained with Figures 130-134. 151, Hypotrigona braunsi on dorsal view Brooks (Kohl). 152, Tngonisca buyssoni {Yri&?,&) , gonostylus only. 153, Liotrigona mahafalya and Michener, gonostylus only at right side of dorsal view, penis valve at right of dorsal view and on lateral view. 154, Cleptotrigona cubueps (Friese), penis valve on right side of dorsal view only. 155, AustToplebeia essingtoni (Cockerell).

to other in The setae in in genera remain doubt. large apical angle Pariotrigona , lacking Hypotrigona. of the worker labial palpus are few (two on The long malar space o{ Pariotrigona suggests some as in a segment 1, one on segment 2) and curved, species of the Neotropical genus Tngonisca, an- Lisotrigona. The gonostyli of workers bear setae similarity strengthened by the nearly right cell and the and lack minute hairs (Fig. 36). The only other gular basal angle of the marginal minute genus with such gonostyli is Hypotrigona. transverse rows of hairs on the inner surface of However, those oi Parwtngona are quite different, the hind basitarsus. Tngonisca, however, has quite being broadened at the bases and separated by different worker gonostyli. The external generic little more than a stylar width. The sting lancet is characteristics were listed by Moure (1961). uncommon absent, the stylet a broad convexity. The hind Pariotrigona is known from two spe- to Indo- tibia has a distinct although rounded posterior cies found from the Malay Peninsula Classification of the Apidae 131

china, Borneo and Sumatra. I have dissected only other genus-group names was proposed for a second related P. pendlehuryi (Schwarz) but P. klossi (Schwarz) single divergent species. A species appears certainly congeneric. to Trigonisca muelleri (Friese), i.e., of the Leuro- trigona group, has recently been described, how- Genus Lisotrigona Moure ever (Moure, Camargo, and Garcia, 1988). 37, 64. 117) (Figs. (Unfortunately due to a lapsus the description is 1961: 194. Lisotrigona Moure, Tyix- specit-s: Melipona headed with the name muelleri, but the intended cacciae Nurse. 1907. by original designation. new name pusilla Moure and Camargo appears in This genus of minute bees shares the character the abstract, figure captions, etc., and is thus states listed in couplet 1 of the above key to validated.) In the present classification it would genera. It is known only from workers; hence its be Trigonisca pusilla (Moure and Camargo) new is in doubt. position relative to other genera The combination. a is of the gonostyli of workers are Hat, separated by Trigonisca one minute, Hypotrigona-Wke median concavity about as wide as a gonostylus, genera segregated in couplet 1 of the key to and are covered with abundant minute hairs; on genera. It is the only such genus found in the the outer and distal margin of each there are Western Hemisphere although a few minute several long, delicate setae. Thus the gonostylar American species exist in other genera, e.g., vestiture is similar to that of Trigonisca. The sting Plebeia (Plebeia) schrottkyi (Friese) and P. (Nogueir- is minor and stylet is merely convex. The lancet, however, apis) (Moure Camargo). differs all other American Meli- long and free. The hind tibia has a much rounded 'Trigonisca from side in the hairs which are posterior apical angle, the hairs on the inner poninae minute widespread of the hind basitarsus are not in noticeable rows, on the worker gonostyli. In addition there are and the base of the marginal cell is acute; in these setae, mostly or all along the outer margin of each It are or features Lisotrigona differs from Trigonisca. dif- gonostylus. The gonostyli adjacent sepa- fers from the other minute Asiatic Meliponinae rated by somewhat over one gonostylar width, T. so that when at the [ignoring small species of Trigona such as and converge adjacent bases, the worker of the (Heterotngona) fuscoballeata Cameron], i.e., they overlap distally. The gonostyli states are similar but are genus Parwtrigona, not only by the character Asiatic Lisotrigona somewhat indicated in the key but by the acute base of the short, do not converge, and are separated by an marginal cell and other features listed by Moure emargination. The sting stylet of the worker is or The (1961) who described both groups in detail. The broadly rounded very obtusely angulate. are is short but its is large hairs of the labial palpi, however, lancet of the worker sting apex free of the male is essentially as in Pariotrigona and within the range membrane. The genital capsule in that I have studied and as of variation found in Trigonisca. rectigonal specimens illustrated and Garcia Lisotrigona contains two perhaps distinct, un- by Moure, Camargo, I it as common species known from Sri Lanka and (1988), although categorize amphigonal Madhya Pradesh in India to Vietnam, Borneo because it can probably assume the schizogonal and Sumatra. I have seen only L. scintillans conformation, the gonocoxites being transverse, broader than or about as as (Cockerell) but Moure (1961) indicates its close much long long broad. The setae of the worker labial similarity to L. cacciae (Nurse). large palpus are few (5-7), straight or curved. Genus Trigonisca Moure An unusual feature is the vestiture on the inner 59, 118, 119, 152, 168, (Figs. 38, 39, 186) surface of the hind basitarsus of the worker; the 1950a: 249. Hypotrigona (Trigonisca) Moure, Type spe- hairs are in transverse rows, suggesting ^/)w and cies: Trigona duckei Friese, 1900, by original designa- the Asiatic genus Pariotrigona. Also, some of the tion. large hairs on the posterior margin of the hind Hypotrigona (Leurotrigona) Moure, 1950a: 244. Type spe- tibia arise tubercles which are cies: Trigona muelleri Friese, 1900, by original designa- from (Fig. 186) tion. particularly conspicuous in the species with the Moure, 1950a: 246. Type spe- Hypotrigona (Celetngona) tibia slender. Thus the posterior edge of the tibia cies: Trigona longicornis Friese, 1903, by original desig- nodulose to nation. appears weakly strongly tuberculate, instead of smooth as in other The Hypotrigona (Dolichotrigona) Moure, 1950a: 248. Type Meliponinae. species: Trigona longitarsis Ducke, 1916, by original right angular or weakly obtuse basal angle of the designation. marginal cell, associated with a broad base of this Of the four simultaneously published names cell, as indicated in couplet 7 of the key to genera, is variable and In listed above, Wille (1979b) selected Trigonisca for requires some explanation. T the inclusive taxon (here recognized as a genus); muelleri (Friese) the marginal cell is much more as in other than is that of other several species resemble T duckei and were in- Meliponinae Trigo- nisca. in muelleri the basal of cluded in Trigonisca by Moure while each of the Nonetheless, T angle 132 The University of Kansas Science Bulletin the cell (between the stigma! margin and vein r) is thickening, suggesting that of Cleptotrigona, but it about 68° and the width of the marginal cell at bears minute hairs rather than coarse setae. The the apex of the stigma is greater than the distance sting stylet is unsclerotized, blunt. The lancet is across the submarginal cell area from vein Rs to moderately long, free of the membrane. vein M. In other genera the basal angle is less The male genital capsule is elongate, perma- than 50° and the width of the marginal cell at the nently schizogonal, the gonocoxites much longer apex of the stigma is not greater than the distance than broad and broadly fused ventrally, the bases across the submarginal cell area. These charac- (plus possibly the gonobase) curled under and ters, among others, show the relationship of the directed apicad, fused to one another except four groups listed in the generic synonymy. distally. The gonostyli are slender, arising near The external character states of the genus are the apices of the gonocoxites, easily detached listed in detail and those of each from the dissection. As in by Moure ( 1951) gonocoxites during group within the genus by Moure (1950); see also Cleptotrigona, the flexion of the penis valves is the above key to genera. Unlike most species contralateral so that they cross one another when which have two small denticles at the upper end of flexed. The genitalia and hidden sterna are iflus- trated Brooks and the apical mandibular margin, T. longitarsis by Michener (1988). The sterna (Ducke) and schuUhessi (Friese) have only one. differ greatly from those of Hypotrigona; T6 The former has a bituberculate labrum, suggest- has a midapical reflexed process that is much ing Lestnmelitta. If more species of these groups broader than in most Meliponinae. The large are found, it will be reasonable to recognize the hairs of the labial palpus of the worker are few names in the above synonymy as subgenera. 1 (5-6), mostly curved, unlike Hypotrigona which think it is important, however, to indicate their lacks such hairs. The external generic characteris- tics are close relationship (shown by the worker gonostyli, listed in detail by Moure (1961). the broad base of the the tubsrcu- marginal cell, Workers of Liotrigona can usually be distin- late hind to the rest of tibiae, etc.) Trigonisca. guished without dissection from Hypotrigona by the there is considerable varia- Within genus the shiny mesoscutum with only minute well tion in brood cell construction and worker separated punctures; the distinct posterior apical In s. str. construction is oviposition. Trigonisca angle of the hind tibia, and the presence of pale or successive but in T. muelleri and (Friese) longicornis yellowish streaks on the preaxilla and posterior (Friese) it starts successively but becomes syn- margin of the scutellum. As noted above in the chronized the time a of cells are by number discussion of Hypotrigona, these character states Worker-laid are unknown in T. completed. eggs occasionally fail, and Brooks and Michener muelleri but are on the food mass like deposited (1988) were unable to place certain undescribed those of the in T. queen longicornis (Sakagami, species. Dissection of the worker gonostyli shows The observations are for 1982). fragmentary that their Sp. 1 is a Liotrigona. these tiny bees but may support subgeneric status Liotrigona is widespread but not very common for the four names listed in the above synonymy. in Africa— Ethiopia to Natal, Ghana to Angola— These minute bees are attracted to perspiration and is common in Madagascar. There are six or and are sometimes pests from Mexico to Para- more species (Brooks and Michener, 1988; Mich- guay. There are about 17 species; familiar ones ener, 1989) of which the most familiar names are are Trigonisca buyssoni (Friese), duckei (Friese), L. bottegoi (Magretti), madecassa (Saussure), and and muelleri longicornis (Friese), longitarsis (Ducke), mahafalya Brooks and Michener. (Friese).

Genus Liotrigona Moure Genus Cleptotrigona Moure (Figs. 40, 61, 120, 136, 153) (Figs. 41, 62, 121, 154)

Lwtngona Moure, 1961: 223. Type species: Trigona Lestrimelitta (Cleptotrigona) Moure, 1961: 219. Type spe- 1895 = ? madecassa cies: Lestrirnelitta bottegoi Magretti, ( Trigona Sau- cubiceps Friese, 1912, by original ssure, 1891), by original designation. designation.

This is one of the genera of minute bees Cleptotrigona forages in nests of Hypotrigona and segregated in couplet 1 of the above key to probably Liotrigona. It is not known to visit genera. Unlike the superficially similar Hypotri- flowers. This African robber genus is strongly gona, Liotrigona is a member of the African group convergent with the American robber, Lestrimel- so that with flattened worker gonostyli bearing numerous itta, Moure (1961) regarded them as minute hairs. The gonostylar bases are separated congeneric. Wille (1979b), however, emphasized by less than the width of a gonostylus, and setae their distinctness and recognized their re- are absent. The gonostyli do not diverge as in semblances as convergent, although extending most African Meliponinae. Each has a dorsal beyond loss of the pollen carrying and manipulat- Classification of the Apidae 133

structures. Both authors charac- ing Hsted many species are listed by Moure (1961). Trigona rnagret- tii Friese ters. (1900), considered as a possible Cleptotri- In Cleptotrigona workers the gonostyli are flat, gona by Moure, is a Hypotrigona. divergent, the bases separate by about half a Genus Austroplebeia Moure gonostylar width; they bear many minute hairs in (Figs. 42, 81, 122, 155, 169) addition to several setae along the edges of a Moure, 1961: 195. dorsal thickening. The sting stylet is slender, Austroplebeia Type species; Trigona cassiae CockcrcW, 1910, by original designation. acute, and little sclerotized, especially basally. The lancet is long and largely free of membrane. This genus includes bees that superficially The male gonocoxites are longer than broad, closely resemble species of the Neotropical group broadly fused apically to gonostyli that are broad Plebeia (Plebeia) as well as the African Plebeina. and flattened at the bases and tapering apically. Austroplebeia species are rather robust with distinct Such gonost\li are unique in the Meliponinae yellow areas on the scutellum and axillae, usually and strikingly different from the extremely also on the lateral margins of the scutum and on slender, easily deciduous gonostyli of Liotrigona. the face. It diff'ers from Plebeia in the abundant, The genitalia appear to be permanently schiz- minute hairs and few small setae on the worker ogonal although the base of the genital capsule is gonostyli and the slender and pointed bristles of perhaps secondarily rectigonal, curled under the the rastellum. The worker gonostyli are slightly rest of the genitalia and extends apicad as far as divergent, separated at the bases by about a the bases of the gonostyli as two slender lobes. gonostylar width. The sting stylet is rounded. This suggests the structure oi Liotrigona in which, The lancet is quite long, mostly free of the however, the lobes are fused to one another membrane. The five to about seven large setae of except apically. The sixth and seventh sterna are the labial palpus are curved to weakly sinuous. quite ordinary for Meliponinae, not platelike as Austroplebeia difl'ers from the Plebeia-Wkc African in Lestrimelitta, the sixth with a midapical reflexed genera Plebeina and Meliponula by the well sepa- process. rated worker gonostyli which are not noticeably Cleptotrigona is one of the genera of minute flattened; the not or scarcely depressed posterior Meliponinae segregated in couplet 1 of the above margin of the inner surface of the hind tibia key. The short, straight setae of the worker labial (variable in Meliponula); the short, transverse, palpus suggest Hypotrigona but probably reflect amphigonal male gonocoxites [both conforma- loss of large setae associated with the robbing way tions seen in A. essingtoni (Cockerell)]; and lack of of life (Michener and Roubik, in press). Cleptotri- the male spatha and gonobase. gona appears to be the sister group oi Liotrigona, as In the reduced wing venation, especially the indicated especially by the curled-under base of lack of a bend near the end of vein M of the the genital capsule. Moreover, in both genera the forewing and lack [except in A. cincta (Mocsary)] penis valves, when extended laterad, cross at of vestiges of the first transverse cubital vein, their bases, so that the left hand penis valve is Austroplebeia resembles the minute genera segre- directed to the right, and the right hand one to the gated in the first couplet of the key to genera (see left (Fig. 153). This is unlike other Meliponinae Note after that key). Although small, Aus- and is a probable synapomorphy supporting the troplebeia's robust form does not resemble that of relationship shown in Figure 8. Liotrigona has the other minute genera. Unlike those genera, the apomorphies not shared by Cleptotrigona (smaller, inner side of the hind tibia has the keirotrichiate less slender sting stylet of workers; fused ventral area closely approaching the posterior margin of lobes of the genital capsule of males), indicating the tibia, leaving a narrow shiny margin as in that Cleptotrigona was not derived from Liotrigona. Plebeia s. str. but less depressed or even not Both have the rastellum reduced to tapering depressed. hairs. Because of its male genitalic character states The rather flat scutellum, not at all overhang- this genus does not appear related to African ing the metanotum and elevated but little above genera, but rather to American ones. The hair- the level of the dorsal surface of the propodeum like spicules of the worker gonostyli are shared (Fig. 121) is unique in the Apidae. Among bees as only with Trigonisca in America, Lisotrigona in a whole this feature is a plesiomorphy but within Asia, and most African genera. Discovery of the Apidae it must be an apomorphy, i.e., a males of Lisotrigona might expose a relationship reversion to the condition found in many non- between it and Austroplebeia. External features of apid bees. Austroplebeia were described by Moure (1961). Cleptotrigona consists of two species, C. cubiceps This genus contains several species found in (Friese) and curriei (Cockerell) known from Lib- the northern half of Australia and in New eria to Tanzania, Angola and South Africa. The Guinea. The specific names involved were listed 134 The University of Kansas Science Bulletin

the rounded or by Michener (1965, as Plebeia) and by Moure apex; very obtuse posterior apical (1961). Well known specific names are Auslro- angle of the worker hind tibia so that the tibia is cincta rather the of plebeia australis (Friese), cassiae (Cockerell), spoon-shaped; presence coarse, am- ber or blackish bristles this (Mocsary) and essingtoni (Cockerell). arising from or near . what Wille calls the __ , ,. , /-, , 1, angle forming (1979b) poste- . • • Cockerell > Genus Meltponula^ .,, jy j /c i ^ l nor parapeniciUum m M. bocandei (bpmola); the is in a sense to This generic name used new presence of hairs, at least laterally, on the basal include not only the type species, M. bocandei area of the propodeum, and the acute worker also a series of smaller African (Spinola), but sting stylet. Like P/c^^Vza and unlike other African forms placed in other genera (see subgenera, genera, M^/z/jonw/a has a broad area of keirotrichia below) by Moure (1961) and Wille (1979b). Some on the inner surface of the worker hind tibia; the as beccarii and of the latter, such M. (Gribodo) posterior margin may be depressed and shining, are almost as robust and erythra (Schletterer), almost as in PMfi'a s. str., only slighdy depressed as M. bocandei. shares Melipona-\\ke Meliponula (e.g., in A/<'/;/?onM/a s. str.), or poorly defined and other African the flat- with most Meliponinae not at all depressed (subgenus Axestotrigona). The with minute hairs tened worker gonostyli many smaller species of Meliponula resemble the larger also with a few the of (sometimes setae), presence species of Plebeia s. str. superficially, but differ a conspicuous remnant of the gonobase attached from most Plebeia not only in character states to the male gonocoxite lateroventrally, the schiz- indicated in the above discussion but in the dense ogonal (presumably permanently) male genital punctation at least of the mesoscutum. capsule with the gonocoxites longer than broad. The reduction of the rastellum to slender hairs at least in ventral and the reflexed view, strongly is not found among other moderate-sized, pollen- of S6 of the male. median apical process collecting Meliponinae, although it is seen in the Meliponula resembles Cleptotrigona and some minute genera. Given the function of the American genus Melipona in having the sting comblike rastellum in other Apidae (Michener, stylet of workers distinct and acute. Meliponula Winston, and Jander, 1978), a study of the pollen differs from Plebema in the reduction of the manipulating movements in Meliponula would be rastellum to slender hairs, no coarser than those interesting, of similar length on adjacent parts of the tibial

Key to the Subgenera of Meliponula

1. Propodeal profile largely vertical; corbicula occupying less than distal half of hind tibia; apical reflexed process of S6 of male short and rounded; metasomal terga dull, minutely — sculptured Meliponula s. str. Propodeal profile with slanting dorsal portion rounding onto vertical portion; corbicula occupying more than distal half of hind tibia; apical reflexed process of S6 of male longer than body of sternum; metasomal terga at least partly shining 2 2. Head and thorax without yellow markings; inner surface of worker hind tibia without well defined shining, depressed posterior margin, although keirotrichiate area does not reach margin at least distally Axestotrigona — Head and thorax with yellow markings; inner surface of worker hind tibia with shining posterior margin at least slightly depressed Meliplebeia

Subgenus Axestotrigona Moure mostly curved on segment one, sinuous on seg- ment two. The male arises near the (Figs. 44, 78, 126, 158) gonostylus apex of the gonocoxite. I regard the genitalia Axestotrigona Moure, 1961: 237. Type species: Melipona as as in the Jenuginea Lepeletier, 1836, by original designation. (Fig. 158) permanently schizogonal, other subgenera. However, this is only evident in This subgenus contains moderate-sized robust dorsal view, for ventrally the gonocoxites are species. There are delicate plumed hairs among broadly expanded so that they are secondarily the marginal bristles at the posterior apical angle rectigonal. The principal characteristics are indi- of the worker hind tibia and across the apex of the cated in the above key and in the description by tibia. The sting stylet of the worker is long and Moure (1961). are slender, almost as in Meliponula s. str., but the There are several species; their names lancet is weak and in the membrane. The about indicated by Moure (1961). The most common 24 large hairs of the worker labial palpus are species is Meliponula (Axestotrigona) erythra (Schlet- Classification of the Apidae 135

lateral Figures 156-161. Male genitalia of Meliponinae, dorso-ventral views (dorsal at left) and views, gonostyli omitted from most lateral and ventral views. Arrows and "8" are explained with Figures 130-134. 156, Meliponula (Meliplebeia) beccani (Gribodo). 157, Meliponula (Meliplebeia) lendliana bocandei (Friese). 158, Meliponula (Axestotrigona) erythra (Schletterer). 159, Meliponula (Meliponula) (Spinola). 160, Plebeina denoitt (Vachal). 161, Dactylurina schmidti (Stadelmann).

at the same time. The three terer) which may be a form oi' ferruginea (Lep- proposed groups from to Moure are different from one eletier). The subgenus ranges Gambia named by distinctly moderate-sized Kenya, south to Angola and the Transvaal. another. The subgenus contains M. beccani to small lendliana Moure [e.g., (Gribodo)] [M. Subgenus Meliplebeia beccani (Friese)] species. In Meliponula (Meliplebeia) (Figs. 43, 46, 79, 123-125, 156, 157) there are delicate plumed hairs among the brisdes 1961; 229. hind Meltplebeta Moure, Type species: Trigona near the posterior apical angle of the worker beccani Gribodo, 1879, by original designation. hairs tibia, as in the subgenus Axestotrigona. Such Plebeiella Moure, 1961: 226. Type species: Tngona are absent in the other groups oi Meliplebeia. The lendliana Friese, 1900, by original designation. lancet of the worker is weak and in mem- Apotngona Moure, 1961: 233. Type species: Tngona sting nebulata Smith, 1854, by original designation. brane in M. (M.) beccarii but quite long and in M. (M.) Wille (1979b) selected the name Meliplebeia for apically free, although transparent, lendliana and nebulata The hairs this group, rather than either of the other names (Friese) (Smith). 136 The University of Kansas Science Bulletin of the first two segments of the labial palpus of available specimen). Unfortunately the male of workers in M. (M.) beccani are short and straight, M. (M.) nebulata (Smith) is unknown to me. Until while in both M. nebulata and lendliana there are its character states are known, 1 have decided that large setae, hooked and slightly sinuous. the best classification is one that shows the close In view of the characters listed above, it is relationship of the three groups given generic tempting to recognize two subgenera Meliplebeia names by Moure, especially in view of the small and Plebeiella, with Apotrigona as a synonym of number of species involved. Plebeiella. The differences between the groups of Meliplebeia contains several species (represen- from to Meliplebeia are accentuated by S6 of males. In M. tatives listed above) and ranges Senegal (M.) beccarii (Gribodo) S6 is a transverse band not Ethiopia, south to Namibia and Natal. The spe- character states are listed greatly different from that oi Axestotrigona, and the cies names and external reflexed median apical process, although long, by Moure (1961) under his three generic names ends in a rounded apex. In M. (M.) lendliana (see above synonymy). The emphasis that Moure on mesoscutal in (Friese) S6 is enlarged, dorsoventrally thickened places sculpturing (punctate tessellate in the seems to me laterally, and the reflexed apical process is bifid Apotrigona, others) near the base, one prong above the other, both misplaced. It is dull, finely and closely punctate, long and slender, the upper one extending toward finest in M. lendliana (Friese). the base of the metasoma (broken off in the one

Figures 162-167. Wings of Meliponinae. 162, Melipona fasciata Latreille. 163, Plebeia (Plebeia) frontalis (Friese). 164, Plebeia (Plebeia) schrottkyi (Friese). 165, (Smith). 166, Cephalotri- gona capitata (Smith). 167, Trigona (Trigona) chanchamayoensis Schwarz. Classification of the Apidae 137

Subgenus Meliponula Cockerell s. str. Melipona and Meliponula s. str., not an indication (Figs. 45, 77, 127, 159, 170, 172) of close relationship. The single species, bo- Trtgona (Meliponula) Cockerell, 1934: 47. Type species: Meliponula (Meliponula) candei Melipona bocandei Spinola, 1851, by original designa- (Spinola), ranges from Liberia, the Central tion. African Republic, and Uganda south to Angola.

This subgenus contains the largest and most Genus Plebeina Moure Melipona-\\k.e species of the genus. It is robust, compact in form, and lacks yellow markings (Figs. 47, 128, 160) although it has yellowish brown areas, for exam- Plebeina Moure, 1961: 228. Type species: Melipona denoili Vachal, 1903, ple, the scutellum and axillae. On the posterior (Trtgona) by original designa- tion. and distal margins of the hind tibia there are bristles, no plumose hairs. The inner surface of This African genus is similar to the Neotropical the worker hind tibia has a well defined but rather Plebeia (Plebeia) in body form, presence of limited dull, slightly depressed posterior margin. The yellowish marks at least on the face, and the worker sting stylet is unusually long and slender narrow, depressed, shining posterior margin of and the lancet is long and largely free. The about the inner surface of the worker hind tibia. It 15 large setae of the worker labial palpus are differs in having the worker gonostyli diverging curved to slightly sinuous. The male gonostylus apically, flattened, without setae and with numer- arises near the base of the gonocoxite. Other ous minute hairs; the sting lancet moderately long character states are indicated in the above key and largely free of membrane, the male gonocox- and in Moure's (1961) comparative description, ites schizogonal (probably permanently) and and especially in Wille (1963). An interesting much longer than wide; and the gonobase rem- feature emphasized by Wille is the arch of the nants rather large. These features are as in most aorta between the longitudinal muscles of the African Meliponinae. In spite of its appearance, thorax. This is as in Melipona, but unlike other this genus is evidently not closely related to stingless bees [including Meliponula (Meliplebeia) Plebeia. Another character state that distinguishes beccarii (Gribodo), see Wille, 1958]. It is, how- it from most Plebeia is the presence of branched ever, a feature of many moderate-sized and large, hairs at the posterior distal angle of the worker fast Hying bees and is doubtless a convergence in hind tibia and a few on the distal fourth of the

Figures 168-171. Wings of Meliponinae. 168, Trigonisca buyssoni (Ynese). 169, Austroplebeia ausfralis (Friese). 170, Meliponula (Meliponula) bocandei (Spinola). 171, Daciylurina schmidti (Stadelmann). 138 The University of Kansas Science Bulletin

is other posterior margin of the tibia. This as in some basally, slightly divergent apically, covered is with species of Meliponula, a genus to which Plebeina minute hairs, and without setae. The sting closely related. In two species of Plebeia, P. (Pleb- stylet is a mere convexity. The lancet is short and P. in the unlike that of African eia) caerulea (Friese) and (Schwarziana) quad- membrane, most rimaculata (Lepeletier), there are branches on one Meliponinae. The male genital capsule is schiz- side of numerous hairs. Plebeina differs from ogonal (probably permanently), the gonocoxites Meliponula in the about right angular posterior longer than broad. The gonobase appears to be apical angle of the worker hind tibia, this angle absent. The male gonostyli are hairless, firmly bearing long, slender whitish hairs; in the strong attached to the gonocoxites and, although slender although pointed bristles of the rastellum; in the in D. staudingeri (Gribodo), are broad and flat- hairless basal area of the propodeum; and espe- tened in D. schmidti (Stadelmann). The gonocox- is ites side. cially in the sting stylet of the worker which are wide open on the ventral The labial merely a rounded, membranous prominence. palpi of the worker have about six large, curved The about 15 large setae on the worker labial setae; an unusual feature is that segments three palpus are curved to weakly sinuous. A full and four together are much longer than segment description of external characteristics is given by two. The worker gonostyli and male gonoco.xites Moure (1961). show the relationship of this genus to other This genus contains one variable species, Plebe- African genera. As shown in Figure 6 it appears ina denoiti (Vachal), or a few closely related spe- to be the much modified sister group of Plebeina. cies. Moure (1961) omitted presumably There are two species, Dactylurina staudingeri inadvertently the name of a form considered in (Gribodo) from west Africa and schmidti (Sta- from east Africa. the last paragraph of his discussion of the genus. delmann) Considered —together It was Plebeina denoiti katangensis (Cockerell). The they are widespread in tropical Africa Kenya genus ranges from Kenya and Uganda to eastern and Tanzania to Zaire and Liberia. Zaire, Botswana, northern Transval and Natal. It may be absent from West Africa. SUBFAMILY APINAE Genus Cockerell Dactylurina These are the trtie honey bees. More has 48, 80, 129, 161, 171) (Figs. been written about Apis mellifera Linnaeus Dactylurina Cockerell, 1934: 47. Type species; Tngona than any other insect. Probably because of staudingeri Gribodo, 1893, by original designation. the familiarity and importance of that spe- This is the African that has the only group long cies, there has been considerable prolifera- slender hairs on the legs, body, plumose posterior tion of names, considering that Apis is a margin of the hind tibia, and narrow keirotrichi- small and morphologically and behaviorally ate ridge on the inner surface of the hind tibia, as unified group. Maa (1953) made a careful in Trigona; the resemblance is closest to some revision of the subfamily, recognizing four species of the subgenera Heterotrigona and Frieseo- names and His melitta. A further similarity to some Trigona is genus-group many species. found on the inner surface of the hind basitarsus work has often been ignored because of the belief that there are four of workers of D. staudingeri (Gribodo), but not D. widespread only schmidti (Stadelmann). In the former, in the basal species. While he clearly split more than have a well- area where many Trigona species necessary at both the genus-group and spe- defined sericeous area covered with short, dense, cies levels, more and more of his conclusions fine and sometimes deciduous there is an hairs, are turning out to be correct. His work is the ill-defined somewhat sericeous area where the basic one for a study of apine systematics. bristle-like setae are sparse. In D. schmidti the Many more recent papers have been re- bristle-like setae are uniformly distributed as in viewed by Ruttner (1987), whose mor- most Meliponinae. studies are at the in- Dactylurina has sometimes been given generic phometric important level. A treatment is status in the past because of its nest architecture fraspecific phylogenetic Alexander (see introductory section on this topic). Its male provided by (in press). Small mm to mm genitalia and worker gonostyli show that it is only Description: (7 long) large (19 long), moderately hairy, rather elongate bees. distantly related to Trigona in spite of its re- Eyes hairy. Claws of female cleft; arolia present; semblance to species of that genus. Unusual hind tibial spurs absent; strigilis with prong on features include the slender, metasoma fingerlike anterior side; hind basitarsus of worker almost as and the of one denticle on the presence only upper broad at base as at middle, with posterior basal of the mandibular part apical margin. projection or auricle; hind tibia without pen- The worker gonostyli are adjacent to one an- icillum. Forewing with complete, strong vena- Classification of the Apidae 139

174b

Figures 172-175. Mandibles of females (workers in social species) of Apidae. 172, Meliponinae; a, Meliponula bocandei (Spinola), b, Cephalotrigona capitata (Smith), c, Trigona (Trigona) cilipes (Fabricius). 173, Bombinae; a, Bombus pennsylvanicua (Degeer), b, Psithyrus variabilis (Cresson). 174, Euglossinae; a, Eufrtesea vwlacea (Blanchard), b, (Guerin). 175, Apinae; Apis mellijera Linnaeus. Figures 176-177. Strigilis of worker, inner surface. 176, Lepeletier. 177, Bombus pennsylvanicus (Degeer). tion, marginal cell about four times as long as without a spiculum; S7 hidden by S6, transverse, lateral distance from its apex to wing tip; stigma small sometimes attenuate medially, with strong and slender, scarcely recognizable in large spe- apodeme. Male genitalia of other Hymenoptera largely cies, vein r arising near middle, margin within replaced by huge and elaborate endophallus; gonobase marginal cell straight to concave; prestigma al- absent; gonocoxite represented by plate bearing a most as long as stigma; second ancl third trans- minute, hairy, apical projection, broader than verse cubital veins directed posterodistad and long, presumably the gonostylus; gonocoxites forming acute angles with vein M. Hind wing sometimes widely separated by membrane; penis with jugal lobe little more than half to nearly two valves thick, blunt, hairy (incorrectly identified as thirds as long as vannal lobe (measured from gonostyli by Smith, 1970); spatha and volsella wing base); ju^a/ and vannal incisions shallow (Fig. absent (Fig. 183). 182). Clypeus gently convex but scarcely pro- Larva: Without small conical tubercles but with tuberant. Maxillary palpus minute, two seg- transverse dorsolateral elevations on segments 1 mented. Male S8 reduced to a transverse bar, to 4, strongest on 1 and progressively weaker to 140 The University of Kansas Science Bulletin the rear. Mandible scarcely sclerotized, bluntly need to recognize multiple genera; it is or with of small teeth at pointed, edentate fringe important instead to emphasize the similar- inner surface. apex, without concavity on ity among the species. Larvae are described and illustrated by Ruttner (1987) followed tradition in rec- Michener Torchio and Torchio (1953), ognizing only four "or at most five" modern and others. (1975), species of Apis although Maa (1953) had Nest: Nests are exposed or in cavities such as recognized many more. Recent work has hives or hollow trees, sometimes in cavities in the demonstrated that a few more of Maa's ground. The nests are made primarily of wax are valid, but the total number is secreted by the sternal wax glands of workers. species small. The two names based on Cells are subhorizontal, forming vertical combs genus-group direc- fossils both have the characteristic of two layers of cells opening in opposite highly no character tions, their bases constituting a median vertical Apis wing venation and have wax sheet. Food for larvae is provided progres- states that separate them at a genus level are not closed until the larva has sively; cells from Apis. Synapis is from the Oligocene, finished A nest consist of a single feeding. may Hauffapis from the upper Miocene, both comb or of combs, in a exposed multiple usually from Germany. cells cavity. Brood cells for workers and storage for honey or pollen are hexagonal, similar in Genus Apis Linnaeus for are similar but diameter; brood cells males (Figs. 175, 182, 183) cells are not in combs larger. Queen-producing Apis Linnaeus, 1758: 343, 574. Type species: Apis combs of worker and tend to hang from brood mellifica Linnaeus, 1761 =A. mellifera Linnaeus, 1758, cells. designation of Latreille, 1810: 439. 1814; 29 (unnecessary replacement Social behavior: This is the only group of highly Apicula Rafinesque, ior Linnaeus; automatically the same as for colonies Apis type social bees (i.e., bees with "permanent" Apis). different other and morphologically very castes) Apiarus Rafinesque, 1815: 123 (unnecessary replace- the same than the Meliponinae. New colonies are formed ment for Apis Linnaeus; type automatically as for Apis). by fission, the old queen and a swarm of workers Megapis Ashmead, 1904: 120. Type species: to find a new site. sizes range from leaving Colony Fabricius, 1793, by original designation. or workers. a few thousand to 60,000 more Micrapis Ashmead, 1904: 122. Type species: Apis fiorea Accounts of behavior can be found in Michener Fabricius, 1787, by original designation. Apis (Synapis) Cockerel), 1907: 229. Type species: Apis (1974) and Ruttner (1987), and in innumerable (Synapis) henshawi Cockerell. 1907 (fossil), by mono- books on the bee mellifera Linnaeus); honey {Apis typy references an excellent recent one with numerous Hauffapis Armbruster, 1938: 37. Type species: Hauffapis scheuthlei armbrusteri Zeuner, to others is by Winston (1987). Armbruster, \9'iQ=Apis 1931 (fossil), designation of Zeuner and Manning, There are no parasitic or obligate robber spe- 1976: 243. Hauffapis is not a valid name. It was cies. proposed to include several species. No type species Distribution: This subfamily is primarily trop- was designated by Armbruster; original type designa- tion is for names ical, and was restricted to the Old World until required genus-group proposed Unlike after 1930 (Internal. Code Zool. Nomen., article Apis mellifera was introduced worldwide. 13c). The subsequent type designation by Zeuner the the Meliponinae, Apinae spread primarily and Manning was in the synonymy oi Apis and thus northward from the tropics. Apis mellifera proba- does not validate the name as Hauffapis Zeuner and

Z.N. , art. bly being native as far north as southern Norway Manning (I.e. lie). Maa, 1953: 556. and A. cerana as far as northern China and the Apis (Sigmatapis) Type species; Fabricius, 1793, by original designation. Pacific maritime provinces of the U.S.S.R. Only As noted by Ruttner (1987), various authors in Africa does the original range of Apis extend have A. fiorea Fabricius (or its group) as into the south temperate zone, to the south- regarded the first branch of a dendrogram of Apis species. ernmost part of the continent. In the tropical Information from various sources has led to this asiatic islands. Apis ranges south to Java and east conclusion, but one of the formerly most convinc- to Timor and the Philippines, but did not reach ing works concerns geotaxis (Jander and Jander, New Guinea, Australia, etc., before A. mellifera which is similar in diverse was introduced. 1970), (progeotactic) families of bees ( to Apis fiorea) but is Taxonomic Account of Apinae different (metageotactic) in Apis dorsata Fabricius, cerana Fabricius, and mellifera Linnaeus. (The in the There is only one genus, Apis, Janders' study, in Malaysia, was doubtless based which is subfamily Apinae. The relatively few species on A. andreniformis Smith, not on fiorea, Horn has are so impressively similar that there is no rare or absent there.) (1975), however, Classification of the Apidae 141

shown that the progeotaxis of A. florea is different The following is a list of the species that are from that of Bombus and presumably other bees, probably distinct, annotated to explain or give so that the Janders' conclusion may not have the references to accounts justifying specific rank for phylogenetic significance originally attributed to forms not considered specifically distinct by Rutt- it. But it has been widely overlooked that mor- ner (1987): data on males of the sort regularly used phological florea Fabricius, 1787. by Snodgrass (1941), by systematists, published andremformis Smith, 1858. Sympatric with^or^a in show that in certain characters A. is plesio- florea southern China and parts of southeast Asia relative to .-4. cerana and mellifera. morphic (Wu and Kuang, 1986, 1987). of the A. Some plesiomorphies florea group dorsata Fabricius, 1793. because are more like other (recognized they binghami Cockerell, 1906. (This is an allopatric as well as other apids bees, e.g., anthophorids, insular form from Sulawesi (Celebes). It seems such as Bombus) are listed below, followed by the distinctive enough to justify specific separation of A. cerana and corresponding apomorphies from dorsata, but this is a subjective decision.) in mellifera parenthesis: breviligula Maa, 1953. (A Philippine form; com- and the as for B. Gonoco.xites large and alinost meeting (small ments same binghami. ) widely separated). laboriosa Smith, 1871. A Himalayan species prob- S7 and S8 separated by suture (fused medially). ably parapatric with dorsata although the two Area behind S8 membranous (a sclerotized, ster- are sometimes found at the same place num-like region). (Sakagami, Matsumura, and Ito, 1980; Rou- and the bik, Sakagami and Kudo, 1985; McEvoy Of the remaining species (i.e., other than are Underwood, 1988). florea group), A. cerana and mellifera obviously cerana 1793. dorsata must Fabricius, close relatives, so that the group = koschevnikovi Buttel-Reepen, 1906. (Th\?, vechti constitute the second branch of a phylogenetic Maa, 1953, and is sympatric with its closest tree, after divergence oi florea. This viewpoint is relative, A. cerana, in Borneo; Tingek et al., supported by the male sternal and genitalic char- 1988.) acteristics o{ A. dorsata, which, according to Alex- 1758. of A. mellifera Linnaeus, ander (in press), are similar to those as Additional of the cerana and mellifera, but with some features such gonocox- species mellifera be ite size differing in the direction of ^. florea. groups may eventually recognized.

Figures 178-181. Wings of Euglossinae and Bombinae. 178, Exaerete smaragdina (Guerin). 179, Eulaema Bombus Eufriesea violacea (Blanchard). 180, cingulata (Fabricius). 181, pennsylvamcus (Degeer). 142 The University of Kansas Science Bulletin

than broad, with strong, usually pointed apical process and short, posterolaterally directed apo- demes; S7 with apically hairy, sometimes bifid disc and long lateral apodemes (see illustrations in Sakagami and Michener, 1987). Male genitalia strongly sclerotized with distinct gonobase (nar- row but almost continuous ventrally); large gono- coxite; small to moderate-sized, sometimes bifid, hairy upper gonostylus; minute to large, hairy, lower gonostylus; and rather small, minutely hairy volsella (Fig. 192). Larva: With small, pointed dorsolateral tuber- cles on thoracic segments and at least sometimes on first abdominal segment and a pair of similar tubercles on vertex. Mandible heavily sclerotized, blunt, with large apical concavity on inner sur- face. Larvae of Eufriesea were described by Michener of Roberts and Dodson Figures 182, 183. 182, Wings of Apis mellifera (1953), Euglossa by Linnaeus. 183, Genitalia of male oi Apis mellifera (1967). Nest: Nests are of Eu- Linnaeus, endophallus omitted; dorsal view at exposed (some species = = or in cavities in banks, tree trunks, logs, left, ventral at right. P penis valve, PA penis glossa) = = old buildings, etc. Aside from the outside cover- valve apodeme, S gonostylus (#), C gono- of the construction consists coxite. ing exposed nests, principally of brood cells, which are mass provi- sioned. There are no or cells SUBFAMILY EUGLOSSINAE storage pots storage as in other apid subfamilies. Construction mate- rials are resin resin often mixed with These are the orchid bees of the American (Euglossa), bark fragments (Eufriesea), and mud or feces tropics, so called because the males are perhaps with resin (Eulaema). of the larger orchids of that re- Social behavior: Some species are solitary (Eu- gion. The name is also because appropriate glossa, Eufriesea). Some species of Eufriesea often of the size and coloration of large gaudy produce aggregations of cells in protected places. of many the bees themselves. Some species of Euglossa and perhaps all Eulaema Males are attracted to various aromatic regularly have several females per nest. The nature of the interactions them are diverse compounds (Dodson et al., 1969; Dressier, among and little but the colonies are 1982a). For this reason they have been much known, seemingly not eusocial. collected in recent years. A list of species was The genns Aglae is cleptoparasitic in the nests of given by Kimsey and Dressier (1986). Eulaema: Exaerete is in nests of to cleptoparasitic Description: Moderate-sized (8.5 mm long) Eulaema and Eufriesea. very large (29 mm long), moderately to densely with These and other aspects of euglossine biology hairy, usually robust bees. Claws of female are summarized Dressier basal tooth, of male similar or cleft; arolia absent; by (1982a). Distribution: for which is known hind tibial spurs present; strigilis with prong on Except Aglae, anterior side; hind basitarsus of nonparasitic from eastern Panama to Bolivia, each genus basal females broadest at base, with posterior ranges from Mexico to Argentina, mostly in the angle or auricle; hind tibia of nonparasitic fe- moist forests. males greatly expanded with immense corbicula, without penicillum; hind tibia of males with large Relationships among Euglossine Genera tibia hairy slit on upper margin distally, male hind greatly swollen in nonparasitic genera. Forewing History: The genera of this subfamily, al- less with complete, strong venation, marginal cell though rather diverse in appearance, are than twice as as distance from apex to wing long remarkably uniform in many features, and tip; stigma minute, vein r arising near middle, all the nonparasitic species were included in margin within marginal cell straight or concave; au- prestigma shorter than to longer than stigma. Euglossa early in this century by most Hind wing withoutjugal lobe, with comb of bristles in its thors. The opposite extreme was achieved by place (Figs. 178-180). Clypeus strongly pro- Moure (1944b) who placed the five genera tuberant; labrum much less than twice as wide as here recognized in five monogeneric tribes long, thus longer than in other apids, sometimes and two subfamilies. Moure himself longer than broad. Maxillary palpus two-seg- (1950b) mented. Male S8 large, strongly sclerotic, longer retreated from this extreme, however, recog- Classification of the Apidae 143 nizing only two tribes, Exaeretini for the families of bees, polarization based on out- is often For cleptoparasites, for the others, group comparisons impossible. on the surface of the replacing his two subtainilics of 1944. Since example, outer mid tibia of males there are areas the two cleptoparasitic genera seem to be velvety whose independently derived from nonparasitic an- number, size, and shape provide generic character states characters 6 cestors, there is no justification for these (Kimsey's and tribes. 7). And on the hind tibia of males there is a slit characters into Females of the parasitic forms lack cor- hairy (Kimsey's 13-15) the aromatic collected biculae and other pollen carrying and ma- which compounds by males are No of these nipulating structures. The hind tibiae are placed. homologues are in other bees. If therefore slender, not excessively broadened structures found polar- as in females of nest-making genera. Inter- ization is to be done, it inust be by methods also other than estingly, males of the parasitic genera out-group comparisons. Kimsey have slender hind tibiae, not swollen like uses the notion that a widespread character state is relative to a less wide- those of the non-parasites. Since the hind plesiomorphic tibiae of males receive the aromatic com- spread alternative, but as is well known, this is often unreliable. I can see no basis pounds collected by males, and this function logical for that two midtibial is probably related somehow to mating be- concluding adjacent one and one is havior, one wonders why males of parasitic velvety areas, large small, ancestral to other or that a genera would not have hind tibiae as en- arrangements, hind tibial slit is ancestral to a larged as those of other genera. Perhaps the large, long short one. bases such as I consider slender hind tibiae of males are plesiomor- On these, that of characters phic features preserved in parasitic forms, as polarization Kimsey's 3, and 14 is in doubt. occurs in various other groups of parasitic 5, 9, bees. The single supposed synapomorphy unit- Analysis: Kimsey (1982, 1987) presented ing Euglossa and Exaerete in Kimsey's clado- two different cladograms for the genera of gram is 14, curvature of the hind tibial slit of Euglossinae. Unfortunately, in presenting the male. Since both its polarity and the the second one, she did not discuss the first homology of the rather different looking cladogram or the reasons for changes. The curvature is in doubt, the reasonable course difference between the two is that in 1982 she is to consider that Euglossa, Exaerete, and the placed Aglae as the sister group to all other remaining genera are connected at a trifur- genera, while in 1987 she placed it as the cation rather than showing the weakly justi- sister to Eulaema only. The reason for this fied additional cladistic structure. Syn- change is a change in polarization of a single apomorphies 19 and 25, as well as 16 with a character, the thickness of S8 in profile. reversion for Aglae, seem to unite the three The following comments refer only to the remaining genera, but the four synapomor- 1987 cladogram. It is based on 25 charac- phies used by Kimsey to unite Aglae and ters, 16 of which consist of a character state Eulaema as the sister group to Eujriesea turn of a single genus, contrasting with all the out to be dubious. Numbers 3,5, and 9 are rest; these states are presumably autapomor- not reliably polarizable, and 1 is not a phies. Character states of single genera of unique synapomorphy for it is a loss (of two course could be plesiomorphic (the other palpal segments) that occurs also in some genera being united by the alternative syn- species of Exaerete; it could have arisen inde- apomorphies) but Kimsey's interpretations pendently in Aglae and Eulaema. The con- (that they are derived) seem reasonable in all servative course, showing only what is not cases. The remaining 9 characters involve too speculative, is to unite Aglae, Eujriesea, synapomorphies and are therefore poten- and Eulaema at an unresolved trifurcation. tially useful in cladogram construction. Thus the best cladogram now possible can be These are her characters 1,3,4, 5, 9, 14, 16, summarized thus: (Euglossa, Exaerete, (Eu- 19, and 25. Kimsey correctly emphasizes jriesea, Eulaema, Aglae)). This is not as satisfy- that, because most euglossine characters ing as a fully dichotomous cladogram but have no homologues in other subfamilies or better demonstrates our current ignorance. 144 The University of Kansas Science Bulletin

few dull colored species). Eufnesea and Eu- Taxonomic Account of Euglossinae laema are similar superficially, large and con- This subfamily contains five genera that spicuously hairy, except that some species of the are separable by the key given below. For Eufriesea are less hairy and brilliantly metal- most part they are easily separable in general lic, resembling Euglossa. There are cases of appearance also: Exaerete species are large, all probable Miillerian involving Eu- green, not conspicuously hairy; Aglae is friesea and Eulaema (Dressier, 1979) so that slender, blue; and Euglossa is small and close examination may be needed to recog- usually brilliantly metallic (but there are a nize the usually rarer Eufriesea.

Key to the Genera of Euglossinae (modified from Kimsey, 1987)

1. Hind tibia three or more times as long as broad in both sexes; female hind tibia somewhat inflated, without corbicula; cleptoparasitic species 2 — Hind tibia twice as long as broad or less in both sexes; female hind tibia flat and shield-like with enormous corbicula (Fig. 188); nonparasitic species 3 2. Hind femur swollen and usually denticulate ventrally; hind tibia curved and expanded apically; scutellum dorsally convex, with sublateral tubercle or welt Exaerete — Hind femur slender and unmodified; hind tibia straight and apically narrowed; scutellum flat Aglae 3. Labrum whitish with two large, dark oval spots; male hind tibial slit short, not reaching apical margin of tibia, and basally curved; male midtibia with two, or less commonly 1 or 3, small felty patches in basal end of large patch; female with median, black scutellar tuft — Euglossa Labrum dark in color; male hind tibial slit long, reaching apical margin, broad and not curved basally; male midtibia with one relatively large basal felty patch adjacent to large patch; female with (Eulaema) or without (Eufriesea) scutellar tuft 4 4. Labial palpus 4-segmented; face metallic without white markings; clypeal ridging various, usually without single medial ridge Eufriesea — Labial palpus 2-segmented; face black or brown, often with white markings; clypeus with single strong medial ridge Eulaema

Genus Eufriesea Cockerel! laema except for weak metallic reflections at least the face. (Figs. 174, 179, 192) on Nests consist of linear or branched series of Pimm Hoffmannsegg 1817: 52 (not Hubncr, 1806). cells of resin often with bark Type species: Plusia superba Hoffmannsegg, 1817 cylindrical mixed (monobasic). fragments. They are located in protected crevices Eumorpha Friese 1899: 126 Hiibner, (not 1807). Type or cavities, under overhangs of rocky banks, species: Euglossa pulchra Smith, 1854, by designation under in burrows in of Cockerel), 1908: 41. buildings, pre-existing wood, Eufriesea Cockerell 1908: 41 (new name for Eumorpha in nests, etc. Although such nests are Friese, 1899). Type species: Euglossa pulchra Smith, sometimes aggregated, there is no evidence of 1854 (autobasic). social organization. Kimsey (1982) suinmarizes Euplusia Moure 1943: 189 (new name for Plusia Hoff- what is known about the nests. mannsegg, 1817). Type species: Plusia superba Hoff- mannsegg. 1817 (autobasic). Genus Aglae Lepeletier and Serville

This genus, most species of which were placed Aglae Lepeletier and Serville, 1825: 105. Type species: caerulea and 1825 in Euplusia from 1943 to about 1980, was revised Aglae Lepeletier Serville, (mono- basic). by Kimsey (1982). She showed (1979b) that the broad, flat scutellum formerly thought to separate This is a monotypic genus of relatively slender, Eufriesea from Euplusia cuts across natural groups steel blue bees reported to be cleptoparasites of and is not a useful generic or subgeneric character Eulaema. It is the most distinctive euglossine state. There are about 52 species, many of them genus, as indicated by Kimsey (1982) who con- brilliantly metallic but others with colorful yellow sidered it the sister group of all the other genera, and black hairs and superficially resembling Eu- and Kimsey (1987) who documents its many Classification of the Ahidae 145 autapomorphies. In thi- latter work she regards it relative remains undetermined, although Kimsey as the sister group ol' Eulaema, but sec my com- (1987) places it as a sister group of Euglossa. ments above on relationships among the genera. Genus Eulaema Lepeletier Genus Euglossa Latreille (Fig. 180)

(Fig. 188) Eulaema Lepeletier, 1841: 11. Type species: Apis di- midiata = Fabricius, 1793 ( menana Olivier, Euglossa Latreille. 1802a: 436. Type species: Apis cordata Apis 1789) of 1833: 85. Linnaeus, 1758, bv designation of Blanchard, 1849: by designation Taschenberg, Eulaema 219. (Apeulaema) Moure 1950b: 184. Type species: Eulaema 1841 = Centris Cnnnidium Perty 18.33: 148, not Goldf'uss, 1826. Type Jasciata Lepeletier, { cingulata Fabricius, 1804), species: Cnemidium viride Perty, 1833 (monobasic). by original designation. Euglossa (Glossura) Cockerel! 1917b: 144. Type species: This genus was at one time called by the name Euglossa piliventris Guerin, 1845, by original designa- Centris tion. Fabricius (1804) (Sandhouse, 1943; Mich- Euglossa (Euglossella) Moure 1967: 401. Replacement for ener, 1944) because of an early and usually Cnemidium 1833. viride Perty, Type species: Cnemidium ignored type designation for Centris. However, the 1833 Perty, (autobasic). usual meanings of the names Centris and Eulaema Euglossa (Dasystilbe) Dressier, 1978: 193. Type species: have been thanks to 567 of Euglossa villosa Moure, 1968, by original designation. preserved, Opinion

. the Euglossa (Glossurella) Dressier, 1982b: 131 Type species: International Commission on Zoological No- Euglossa bursigera Moure, 1970, by original designa- menclature. Sandhouse (1943) lists two un- tion. justified emendations of the name Eulaema. This genus consists of moderate-sized (the This genus consists of about 13 species of large smallest of Euglossinae) to rather large, usually bees, all black or with conspicuous patterns of brilliantly metallic species. With 103 species de- yellow or orange hair, sometimes with limited scribed, it is the largest genus of the subfamily. metallic tints, usually on the metasoma. Dressier (1978) provided a classification of the Nests consist of clusters of oval cells made of species, placing them in 12 species groups organ- mud, feces, and probably resin, located in cavities ized into four subgenera {Dasystilbe Dressier, Glos- in soil, banks, tree trunks, etc. Often more than sura s. str. one female works in a Cockerell, Euglossa Latreille, , and simultaneously single nest, Euglossella Moure). The subgenera are seemingly but details of interactions among individuals re- natural groups but there is some intergradation main little known (Michener, 1974). among them. Later Dressier (1982b) elevated The genus was revised by Moure (1950b) and another group to subgeneric status under the Dressier (1979). Moure (1950b) gives the distinc- name Glossurella. As I have nothing to dd to tions in detail between the subgenera Eulaema s. s str. and Dressier' classification, further comment seems Apeulaema. R. L. Dressier (in litt.) indi- unnecessary. cates that there are four species groups; it is not Nests of some species are constructed of resin clear whether any of them justify subgeneric and located on stems or twigs in the open. The status. cells are into the interior of a more or less packed SUBFAMILY BOMBINAE spherical resinous envelope. Other species con- struct cells, isolated or in small clumps, in small This subfamily consists of the buinble cavities in tree branches or trunks, earthen banks, bees. Except for the parasitic species, all are or in buildings. Some nests are built and occupied eusocial. The 250 by lone females while others contain several primitively approximately species are monotonous females seemingly living more or less cooper- morphologically to the and atively (Roberts and Dodson, 1967). compared Euglossinae especially to the Meliponinae. Nonetheless there is Genus Exaerete Hoffmannsegg interesting diversity in a few structures — the (Figs. 174, 178) male genitalia, stings, mandibles, etc. Most of the Exaerete Hoffmannsegg, 1817: 53. Type species: Apis classification of the group is based on dentata Linnaeus, 1758 (monobasic). the male genitalia. Chrysantheda Perty, 1833: 147. Type species: Chrysantheda Description: Middle sized (9 mm long) to very nitida Perty, 1833 (=Apis dentata Linnaeus, 1758) mm robust, bees. Claws of (monobasic). large (22 long), hairy female cleft; arolia small but hind tibial Caliendra Gistel 1848: viii. Type species: Chrysantheda present; with nitida Perty, 1833 {=Apis dentata Linnaeus, 1758) (auto- spurs present. Strigilis prong or strong basic) (unnecessary replacement for Chrysantheda Pertv). elevation on inner margin. Hind tibia and basi- tarsus of female as in Apinae except in social This is a genus of large, brilliant green, clep- parasites (Psithyrus). Forewing with complete toparasites of and Eulaema. The six Eufriesea spe- strong venation; marginal cell somewhat longer cies were revised Its closest than distance its by Kimsey (1979a). from apex to wing tip; stigma 146 The University of Kansas Science Bulletin

Figures 184-185. Hind tibiae and basitarsi of meliponine workers, inner surface (without marginal hairs) at left. 184, Plebeia (Plebeia) frontalis (Friese). 185, Trigona (Trigona) amalthea (OHvier). = = R rastellum, P penicillum.

Figures 186-189. Hind tibiae and basitarsi of female Apidae (workers of social species), outer surfaces. 186, Trigonisca longitarsis (Ducke). 187, Partamona near cupira (Smith). 188, Euglossa imperialn Cockerell. 189, Bombus pennsylvanicus (Degeer). Figures 190, 191. Dorsal views of scutellum of meliponine workers. 190, Scaptotrigona mexicana (Guerin). 191, Partamona near cupira (Smith). Classiucation of the Apidae 147

small, little if any longer than prestigma. vein r times hexagonal) pots separate from the pollen arising near or beyond middle, margin within pots (Haas, 1976). cell or concave. Hind marginal straight usually Social behavior: Except for the social parasites, wing without jugal lobe (Fig. 181). Clypeus slightly the Bombinae are all eusocial. Their colonies are conve.x, to moderately protuberant. Ma.x- weakly usually annual. Each is started by a single queen; illary palpus two segmented. Male S8 well devel- in temperate and arctic climates this is in the oped, sclerotized. with median apical, truncate or spring. Her early progeny are all workers, usually emarginate, hairy process, body of sternum not much smaller than the but thickened and excavated as in most Euglossinae, queen morphologically similar. Males and are apodemes distinct, directed laterally or post- young queens produced the fades and the erolaterally. S7 with disc rather broad, like pre- later; they mate, colony away, ceding sterna but smaller, apical margin rounded young queens hibernate until the following associated struc- or slightly bilobed (for this and spring. In the tropics this sort of cycle is some- see series of illustrations Ito, 1983, tures, by times modified, but it never attains the major Male well sclerotized with dis- 1985). genitalia features of highly social bees whose queens never tinct gonobase broadly interrupted midventrally; live alone and are morphologically very different short and broad, often variously large gonoco.xite; from workers. Other features oi Bombus behavior angulate, gonostylus (squama); and broad, hairy are described by Michener (1974), Free and volsella attaining the apex of the gonostylus or Buder Morse and others. exceeding it and also extending far toward the (1959), (1982) A few of are social base of the gonocoxite on the lower surface. species Bombinae workerless The homologies and terminologies for the male parasites in nests of species oi Bombus. Most of the are in the females of this genitalic parts have been confusing in Bombinae parasites genus Psithyrus; lack the and are the subject of a separate section below. genus pollen gathering and manipulating Larva: With small pointed dorsolateral tuber- structures characteristic oi Bombus and the apex of cles on thoracic segments. Mandible heavily scle- the metasoma is more pointed than in Bombus and rotized, apex bluntly rounded or minutely curled downward, housing a powerful sting. The social denticulate, acute in Psithyrus, with small pre- female parasite dominates or kills the host apical tooth on upper margin, with large apical queen and may become, in essence, the queen of a concavity on inner surface. colony consisting of herself and workers of the Larsae have been described and illustrated in host species. Fisher (1987) gives a recent study of detail by Ritcher (1933), Cumber (1949), Mich- one species with references to older works. ener (1953), Stephen and Koontz (1973), and Distribution: Bumble bees are for the most part others. There is significant variability among adapted to cool climates and thus are uncommon them that may clarify relationships among groups in places where Euglossinae are common. They of Bombus. are most abundant in the cool temperate parts of Nest: A summary of nest architecture is given the holarctic region, with many more species and by Michener (1974). Nests are commonly in subgenera in Eurasia than in North America. rodent nests, nests, cavities under bunch Williams (1985) indicates that there are 199 grass or other vegetation, etc. There may or may species in Asia, 58 in Europe, 41 in North not be a thin wax (and pollen) covering over the America, and 43 in Mexico, Central and South nest. The cells are totally different from those of America. Northward, they range in small num- all other bees, for they are closed (sometimes bers as far as there is land. Southward they occur incompletely) but grow with the growing larvae, in North Africa but not in subsaharan Africa. commonly contain several eggs and later larvae, There is one specimen of what appears to be a develop a separate bulge for each larva, and may South American species reported from Cameroon even become divided into several cells as the (Tkalcu, 1966); it was no doubt mislabeled or lar\ae mature. Katayama (1989) has discussed introduced. To the east they are numerous in the such cells and their possible evolutionary origin in Himalayas but absent below 1000 m altitude in detail. Larvae are fed progressively, either by India (Williams, 1985); to the southeast a few food introduced through the tops of the cells or by species occur in the mountains of Southeast Asia, food pressed in through pockets at the bases of the as far as Java and the Philippines, but they are cells and forming the cell floors. Both methods absent from the lowlands. In the Western Hemi- may occur in the same species, usually at different sphere there is a rather small Bombus fauna all the seasons. Both honey and pollen are stored in pots way to Tierra del Fuego, mostly in montane areas separate from brood cells; they are often made of or temperate latitudes, but unlike the situation in old cocoons but may be wholly constructed by the Africa and Asia, a few species occur in the bees. In B. mendax Gerstacker, unlike most spe- lowland moist tropics. cies, the cocoons are wholly destroyed and honey It is curious that close to the center of diversity storage is in a series of crowded (therefore some- [and the area where the most plesiomorphic 148 The University of Kansas Science Bulletin

or the of species occur, according to Williams (1985)], i.e., species groups). Moreover, species the Palearctic region, the lowland tropics seem to Bombus S.I., as noted above, are very much an absolute barrier to Bombinae. have been alike, not superficially separable into genera Moreover, in of mesic Pleisto- spite widespread or subgenera, and have many distinctive cene conditions in what is now the Sahara, they behavioral attributes. Richards (1968) de- did not reach the mountains and highlands of scribed the 35 subgenera that he recognized, East Africa, as have other mesic northern groups keys, and thus for the first time pro- like . On the other hand, in the Western gave vided a worldwide classification for subgen- Hemisphere, with poorer northern bombine di- era of Bombus. versity, they range almost as far south as there is have on the land, and occur in the lowland tropics, e.g., the Many authors speculated Amazon Valley. relation oi Psithyrus to Bombus. Because of the superficial similarity of some Palearctic Psi- Relationships among Bombine Genera and thyrus to their hosts, the suggestion that Subgenera Psithyrus species arose polyphyletically from History: Traditionally two genera of Bom- different groups of Bombus was made, for binae have been recognized, Bombus and example by Richards (1927). The similari- Psithyrus, the latter consisting of social para- ties of Psithyrus species would thus have to be sites of the former. Indeed, because of their a result of convergence. Recent studies by divergent habits and the structures relating Ito (1983, 1985), Ito and Sakagami (1985), to pollen collecting, or lack of them in and Williams (1985) placing emphasis on Psithyrus, some older authors (Ashmead, male genitalia and hidden sterna, which are 1899; Friese, 1923) placed Psithyrus in a unlikely to evolve convergently, show de- different subfamily or family from Bombus. cisively that Psithyrus is a monophyletic unit As to Bombus, although various subgeneric related to certain groups of Bo7nbus. Elec- names had been proposed earlier (starting trophoretic studies of genetic relationships with Dalla Torre, 1880), and Robertson support the cohesiveness among Psithyrus (1903) had proposed Bombias as a genus, it species (Pamilo, Pekkarinen and Varvio, was Skorikov (1922) who divided Bombus 1987; Obrecht and Scholl, 1981). into numerous genera. Most authors did not Recent studies by Ito (1983, 1985) and follow him, for the genera were hard to tell Williams (1985) provide a wealth of infor- apart. Milliron (1961) divided Bombus into mation as well as interpretations. Ito gives three genera and Tkalcu (1972) recognized excellent illustrations of male sterna and eight genera. These genera, likewise, are genitalia of nearly all groups. His analyses hard to distinguish, intergrade, and have (based on genital character states of males) little usefulness. The smaller supraspecific are phenetic; they show six groups of Psithy- units, subgenera or species groups, however, rus together but in the midst of Bombus based primarily on male genitalic character groups, and closest to groups called Mucido- states, are more stable and for a Bombus bombus, Eversmannibombus, and Orientalibom- specialist are useful. There are about 35 such bus. A cladistic study of the problem by Ito units in the genus Bombus, all with sub- and Sakagami (1985) indicates a relationship generic names. Some of them such as Fervid- of Psithyrus to Orientalibombus and some spe- obombus are still quite diversified and may cies of Fervidobombus, especially Bombus not represent unified recognizable groups. dahlbomii Guerin. Ito (1983, 1985) gives a detailed and useful Williams (1985) developed a cladogram historical account, while a briefer one is for all groups of Bombinae, based on male provided by Richards (1968). Given the genitalic character states. He utilized 14 morphological homogeneity of Bombus, most characters, with 2 to 33 states per character. authors have continued to use it in the Polarities were judged by comparison with traditional broad sense. Efforts to find a few Euglossinae, although the characters with recognizable units have failed because of 24, 27, and 33 states were not ordered; they intergradation and discordance in character are branching characters. state distributions, a problem that plagues Although a different inethod of coding, even some of the finer divisions (subgenera with more characters and fewer states per Classification of the Apidae 149 character, would seem desirable and would character set on the basis that the genitalic probably permit better polarization. character states selected are those likely to be Williams' study is interesting and valuable more conservative than those involving and his major phylogenetic conclusions are other structures that do not fit the female probably correct. Mendacibombus appears in securely to prevent interruption of copula- his study as the sister group of all other tion. In short, he argues that his characters Bombinae; Psithyrus is the ne.xt branch, the are unlikely to exhibit convergence; he is sister group of all but Mendacibombus. On this probably right. basis, following the practice of those who Fourth, lack of characters is illustrated by branches that base classifications on cladograms only, (Mucidobombus , Rhodobombus) Williams recognized three genera, Men- lack synapomorphies. From the viewpoint of dacibombus. Psithyrus. and Bombus. Ito (1983, Williams' cladogram, these groups should 1985) also recognized Mendacibombus as a be regarded as paraphyletic. It should be distinctive group, but in all but one of his noted, however, that Williams' cladogram phenograms it was closely associated with was based on certain species, and that the other groups oi Bombus. Richards (1968) did traditional subgeneric names were then not consider Mendacibombus unusual. added; he is not responsible for these "sub- I regard Williams' cladogram as impor- genera." tant but, as his title and introduction indi- Fifth, the genitalic characters themselves cated, preliminary. His classificatory response often involve minor changes whose polarity seems to me premature. First, Mendacibombus is subject to judgement. Bombus (Mendacibom- is recognized on his cladogram by a single bus) mendax Gerstaecker not only looks like a synapomorphy plus three plesiomorphies that Bombus but its genitalia are similar to those distinguish it from the rest of the subfamily. of other Bombus. Polarization of characters Furthermore, about two thirds of all the by outgroup comparison using Euglossinae other segments of the tree are also defined by is not only diflrtcult, but may be deceptive single synapomorphies. Thus while the tree since most similarities of Euglossinae and is in general convincing because some of the Bombinae are due to plesiomorphies, and major groups of subgenera recognized by the Euglossinae have many more au- to out it is other authors tend come together, tapomorphies (at the subfamily level) than no doubt subject to change when other do the Bombinae. Thus comparison of the to characters and taxa are added the study. states of a character is likely to be between a One objective of classification is stability; to plesiomorphic state in Bombinae and a de- base a classification on such fragile evidence rived homologue in the Euglossinae. is a mistake. Williams indicates (in litt., Finally, I do not believe that the unified 1989), however, that the male genitalia of and homogeneous group Bombus, which has numerous species not available to him in an enormous number of common character 1985 have modified his cladogram in detail states and for which predictions concerning but the general form of the tree remains characteristics of little-studied species can be about the same. made, is any less useful because it can be Second, Williams (in litt.) reports that shown to have given rise to another genus. with other species now available, he finds In short, paraphyletic taxa are sometimes Mendacibombus to represent more than one useful. One needs to know that they are clade; it is therefore paraphyletic. If it were paraphyletic, but the classification should to be subdivided, one would have genera often reflect other things than the cladistic scarcely distinguishable from one another. pattern. Third, Williams' cladogram is based ex- Given the problems described above, and clusively on character states of male geni- noting that very intensive studies of Bombi- talia. A cladogram to be used as a basis for nae have been made and that additional classification should be based on all available useful characters are hard to find, I believe synapomorphies, or at least not on one single that those who rigidly wish classifications to set of characters that in theory might exhibit be redundant, i.e., to duplicate information convergences. Williams defends his limited in cladograms, have no choice but to incor- 150 The University of Kansas Science Bulletin porate Psithyrus into Bombus. This would example, in Tapinotaspis (Exomalopsini), mean that many statements about Bombus Epicharis (Centrini), () in must contain alternatives — either with a cor- the Anthophorinae; in and other with- bicula or without, with a rastellum or ; and \n Manuelia postica {?i\i'\no\di) out, etc. but not other Manuelia, in the Xylocopinae. The alternative which I follow is to recog- As indicated by Sakagami and Michener nize a paraphyletic genus Bombus. I think (1987), Manuelia is close to the ancestor of this solution is correct not only currently, the Apidae. It therefore would not be sur- until a cladogram with more characters is prising to find the same structures in the in a devised, but also the long term, because apids that have most plesiomorphies, i.e., classification that simply duphcates the clad- the Bombinae and Euglossinae. istic pattern is redundant. The classification Euglossinae (e.g., Eufriesea pulchra Smith, should be as useful as possible, and thus Fig. 192) clearly have the two gonostyli. In reflect information beyond that in the clado- addition, however, they have a minutely gram, in this case the phenetic distinctness of hairy sclerite more basad along the lower Bombus s.l. from Psithyrus. inner margin of the gonocoxite; it appears to represent the volsella. In Epicharis Genitalia of the Bombinae elegans Smith (Anthophoridae) the two gonostyli are Partly because the Bombinae were among also clearly present, and in addition the a the first bees whose male genitalia were volsella, as separate small sclerite with a investigated, and partly because of problems long, minutely hairy, apical process. The in recognizing the homologies of certain volsellae of Eufriesea and Epicharis cannot parts, special terminologies often have been represent the lower gonostyli, which are used in describing bombine genitalia. The easily recognizable; these volsellae are greatest problems concern the identity of the clearly homologous to the volsella of Bombi- volsella. nae (Fig. 193) as recognized by Williams. At one stage I believed that the structure There are not two distinct gonostyli in Bom- called the volsella by Williams (1985) was in binae, but the gonostylus often appears fact the lower branch or lamina of the gono- bilobed, with a mesal and an apical projec- stylus. In Bombinae it extends apicad and is tion, which may represent the two gonostyli hairy like a gonostylus, and its base is not of some other bees. The volsella was cor- very different from the base of the lower rectly identified by some earlier authors, gonostylus of halictids like Nomia melanderi e.g., Boulange (1924, as voselle) and Smith Cockerell. The presence of two gonostyli (1970) who considers the structure in Bom- binae to the (really upper and lower and largely separate be cuspis of the primitive chelate gonostylar structures) is widespread and pre- volsella. sumably plesiomorphic in anthophorid bees, I here accept the terminology of Williams and seemed to explain the two apical proc- (1985); its relation to certain other termi- esses from the bombine gonocoxite. Two nologies of bombine genitalia is indicated in gonostyli are well developed and distinct, for Table 5.

TABLE 5. Terminology of bombine male genitalia.

Snodgrass Classification of the Ai'iuae 151

Fossil Bombinae Taxonomic Account of Bombinae

None of the fossils that liave been at- As indicated above, I recognize two bom- tributed to Bombinae can be rehably placed bine genera, with the clear understanding there except probably the Oligocene and that one of them, Bomhus, is paraphyletic. Miocene species placed in Bomhus (Zcuner and Manning, 1976).

Key to the Genera of Bombinae

1. Female hind tibia with corbicula and rastellum; hind basitarsus with strong auricle; apex of metasoma of female not curved downward, S6 without carinae; hind tibia of male often bare and shiny; gonostylus and volsella usually hardened, volsella often not greatly exceeding gonostylus, usually variously angulate Bombus — Female hind tibia convex, hairy on outer surface, so that corbicula is absent; rastellum absent; hind basitarsus without auricle; apex of metasoma of female curved downward, S6 with lateral carina; hind tibia of male with abundant short dark hair; gonostylus and volsella more membranous, volsella extending well beyond gonostylus, simple, flat, without angles or teeth Psithyrus

Genus Bombus Latreille ards, 1968; Ito, 1983, 1985; Williams, 1985). It seems to here these (Figs. 173. 177, 181, 189) unnecessary repeat lists, type species, etc. The following are names proposed Bumbus Latreille, 1902b: 385. Type species: Apts terreslns since Richards' paper: Linnaeus, 1 758 (monobasic). (Festwobombus) Tkalcu, 1972: 27. Type spe- list or sub- The enormous of synonymous cies: Bombus festivus Smith, 1861, by original designa- generic names has been given elsewhere (Rich- tion.

Figures 192, 193. Ventral views of male genitalia. 192, Eufriesea pulchra (Smith), lower gonostylus = = omitted on right side. 193, Psithyrus variabilis (Crcsson). S gonostylus, V volsella. 152 The University of Kansas Science Bulletin

and Boinbus (Digressobombus) Laverty, Plowright and Citrinopsithyrus Thorp, in Thorp, Horning Dun- Williams, 1984: 1051. Type species: Megabombus di- ning, 1983: 50. Type species: Apathus citrinus Smith, for La- gressus Milliron, 1962, by original designation. 1854, by original designation. (Replacement of which turns out to be Bombus (Brachycephalibombus) 'WiUiams, 1985: 247. Type boriopsithyrus, the type species bee of the species: Bombus brachycephalm Handlirsch, 1888, by an anthophorid genus .) original designation. As shown both Ito and Williams, the sub- Bombus (Dasybombus) Labougle and Ayala, 1985: 49. by in are even more similar than Type species: Bombus macgregori Labougle and Ayala, genera Psithyrus 1985, by original designation. those of Bombus; I consider them synonyms of were treated in detail Popov The scope of this genus is indicated above in Psithyrus. They by the section on relationships among bombine gen- (1931). As indicated earlier, consists of social era and subgenera. Its distribution is that of the Psithyrus in the nests of Bombus, and lacks a subfamily. It contains all the nonparasitic species parasites worker caste. of the subfamily, and in addition a very few Psithyrus is a holarctic genus found in the areas parasitic species (Richards, 1973; Yarrow, 1970). where Bombus is most abundant, but not The named subgenera are less diflerent from ranging into the arctic or into the mountains of one another than are subgenera in most groups of high southeast Asia and islands, and in the bees. In fact, the homogeneity of the species in nearby New World, not south of Gua- the genus is outstanding. These bees have been probably ranging temala. carefully studied to find group character states by treatments of Psithyrus species are diverse specialists (Richards, 1968; Sakagami Regional included in the accounts oi Bom- 1981 I usually regional and Ito, ; Ito, 1983, 1985; Williams, 1985). bus cited above; see also do not consider recognition of the subgenera Popov (1931). essential. The only key (except regional ones) is that of Richards (1968). ACKNOWLEDGMENTS Further studies of behavioral characters like For the loan of type material important for this those of Hobbs (1964), Sakagami (1976) and study, I am indebted to Frank Koch, Museum fiir in the delineation of Katayama (1989) may help Naturkunde der Humboldt Universitat, Berlin. more useful units. Such studies are needed for David W. Roubik of the Smithsonian Tropical many more groups. Katayama (1989) recorded in Research Institute sent preparations of melipo- admirable detail the often subgenus-specific be- nine mouthparts as well as males of various not otherwise haviors in cell construction and egg laying, but species available to me. Michael Prentice and Howell V. of the the sampling of species was necessarily limited. Daly University of California sent me copies of their as Particularly, more data are needed on the earliest yet incomplete manuscript (and illustrations) on stages of colony development, when some of the the relationships of the subfamilies of Apidae. most important characters are manifest. This work was of great value in modifying my As biochemical methods of determining genetic ideas on this subject. relatedness have various authors have evolved, S. F. Sakagami of the University of Hokkaido, used such methods to indicate relationships J. M. F. Camargo of the Faculdade de Filosofia, among species of Bombus. Such studies usually Ciencias e Letras, Universidade de Sao Paulo, reinforce the groups or subgenera based on mor- and Ricardo Ayala of the Estacion Chamela, Universidad Nacional Autonoina de re- phological differences, showing that most of these Mexico, viewed the section on made groups are useful monophyletic or paraphyletic Meliponinae, many useful suggestions, and called my attention to units (Pamilo, Pekkarinen and Varvio, 1987). characters than I had not previously recognized. Important regional treatments of species are by Byron Alexander of the University of Kansas Franklin Burks (1912, 1913), Krueger (1917), reviewed the section on Apinae and made useful Moure and (1951), Sakagami (1962), Thorp, suggestions. Horning and Dunning (1983), Labougle (1990) Robert L. Dressier of the University of Florida and many others. provided helpful information for my treatment of Paul Williams of the Natural His- Genus Euglossinae; Psithyrus Lepeletier tory Museum London reviewed the section on (Figs. 173, 193) Bombinae and has been most helpful in providing materials on this in Psithyrus Lepeletier, 1832: 373. Type species: Apis unpublished subfamily, pa- of homol- rupestris Fabricius, 1793, by designation of Curtis, tiently correcting my misinterpretation 1833: pi. 468. ogies of bombine male genitalia, and in explaining his classification of this group. As for Bombus, the subgeneric (really syn- Analyses using Hennig 86 were by James naines seem not worth as onymous) listing they Pakaluk; those using PAUP were in collaboration have been listed Ito and Williams by (1983, 1985) with Stephen Reyes and Arturo Roig-Alsina; the is a recent addition to the (1985). The following use of PAUP 3.0 was through J. S. Ashe. list: Joetta Weaver and Virginia Ashlock have done Classification of thk Apiuae 153 excellent secretarial and cclitint>; work, which I separated by about a puncture width in most much appreciate. areas, clypeus and lower paraocular area not This study is a product of National Science more coarsely punctured than rest of face. Integu- Foundation Grant RSR 87-16817. ment largely testaceous, yellow marks absent. b) Head as broad as thorax. Interocular dis- APPENDIX: TRIGONA GENALIS tance greater than eye length; inner orbits con- FRIESE, A HITHERTO UNPLACED verging upward in upper thirds, gently NEW GUINEA SPECIES con\erging downward in lower third so that upper and lower interorbital distances are about by Charles C. Michener and Shoichi F. Sakagami equal (Table 6). Upper alveolar tangent well below middle of face; interalveolar distance In his seminal work on the classification of Old scarcely greater than half alveolorbital distance. World stingless bees (Meliponinae), Moure Frontal line a fine groove; frons gently convex. not include certain from (1961) did species New c) Clypeus gently convex, slightly more than Guinea. Two of these {T. genalis Friese and twice as broad as long; lateral parts of epistomal suture incurved below. atricornis Smith) are the principal subject of this Mandible with two small denticles in Appendix. Although these two species are decep- d) upper fourth of apical margin, the lower one smaller tively similar, the first is so unusual that each of than upper and almost evanescent. Labrum sim- us independently described it in manuscript as a ple. Malar area as long as about 1.5 flagellar new subgenus of Trigona, here named Papuatrigona diameters; clypeocular distance two flagellar di- Michener and T. atricornis also is Sakagami. ameters. Gena rounded, almost as wide as eye in unusual within its In the of the text it group. body side view. Labial palpus with about five large, is included by CDM in the subgenus Heterotrigona, sinuous setae on first segment, six on second; but as indicated there, SFS places it as an unusual second segment more than half length of first, less than three times as as species of Platytrigona. It does not agree with long wide, extending base of third Moure's characterization of Platytrigona, the defi- slightly beyond segment; segments three four about as as two. Galea with nition of which must be broadened to include T. plus long numerous straight or hooked setae. atricornis. weakly e) Vertex weakly procurved behind ocelli, not Most of the descriptive material on the sub- produced or ridged; ocelloccipital distance about is the work of the genus Papuatrigona CDM; equal to ocellar diameter and half of ocellocular discussion and material is both of comparative by distance, orbitoccipital distance and interocellar us, and the specific descriptions and illustrations distance, which are about equal to one another. is shorter alveolocellar not (Figs. 194 to 219) are by SFS. The subgenus f) Scape than distance, median ocellus. incorporated into the body of this work; the reaching Flagellar segments than broad, second Appendix provides added details including de- mostly slightly longer slightly longer than first which is about as long as wide. scriptive material comparable to that of Moure g) Notaulus and median line visible but not (1961). impressed; parapsidal line small. Scutellum A third species, T. keyensis Friese, described short, rounded, slightly overhanging steeply slop- from the Kai but also found in New- Kepulavan ing metanotum. is a member of the of Guinea, group Platytrigona h) Forewing extending well beyond ape.x of defined by Moure (1961), i.e., a relative of T. metasoma; stigma moderate sized, prestigma of cell over plamfrons Smith and jlaviventris Friese with the shorter than width stigma. Marginal four times as as acute at basal area of the propodeum hairy throughout. It long broad, base, only at where Rs bends differs from the species known to Moure by narrowly open apex apicad almost parallel to wing margin. M-Cu bifurcation certain characters listed in the body of the text, coincident with or rarely slightly basal or apical to under Heterotrigona. Although T. keyensis also has m-cu; Cu strong; transverse cubitals almost unre- the reddish yellow body coloration like T. genalis cognizable so that submarginal cells are almost and it is not discussed further here atricornis, confluent; submarginal angle (between Rs and M to the New Guinea collec- except give following at base of first submarginal cell) very slightly tion data: Northeast New Guinea: Wagu/Black obtuse; M bent at first recurrent vein and con- River, Western Highlands, Oct. 3, 1972 (Hoh- tinuing almost to wing margin. Hamuli seven per mann). wing; jugal lobe one-third as long as vannal lobe, half as long as cubital cell. Hind tibia more than 2.5 times as as Papuatrigona Michener and Sakagami, i) long con\ex in new subgenus wide, posterior margin (almost straight basal half), posterior distal angle obtuse and Type species: Trigona genalis Friese, 1908. somewhat rounded; hair on posterior margin To facilitate comparison with other taxa, the mostly simple and of moderate length but is fifth or si.xth of lettering system of Moure (1961) utilized. plumose hairs intermixed in distal tho- corbicula distal half. Inner a) Integument rather shiny but head and margin; occupying rax minutely punctured throughout, punctures surface with keirotrichiate zone at widest point 154 The University of Kansas Science Bulletin

203 204

of T. atricorms. Figures 194-205. Trigona atncornis Smith and T. gmalis Friese. 194, Face worker, 195, of T. atncornis and 196, Faces of worker and queen, T. genalis. 197-199, Lateral views of heads genalis, and base of T. atricorms workers, and T. genalis, queen. 200-202, Apex of scape, pedicel, flagellum, of of worker of T. worker and T. genalis worker and queen. 203, Posterolateral view propodeum genalis. F. Scale line = 0.5 204, 205, Mandibles of worker and queen, T. genalis. (Drawings by S. Sakagami.) third to the mm; one applies to all heads, another to antennae and mandibles, and the propodeum.

(about two-thirds of length of tibia from base) Trigona (Papuatrigona) genalis Friese nearly twice as wide as shiny posterior marginal Because neither T. genalis nor 7' atncornis has zone, not reaching apex of tibia, on distal part oi been described, we a tibia sloping gradually to marginal zone, the fully present description, metric information for both latter more depressed in middle of tibia so that including species is for with there is slope at edge of keirotrichiate zone, this (Table 6). The description T genalis, slope extending onto basal fourth of tibia. Pen- comparative information for T atricorms added in rastellum icillum and rastellum strong; bristles of parentheses; subgeneric characters listed above blunt robust, mostly tipped. are mostly not repeated. about two times as as j) Hind basitarsus long WORKER: Color. Pale honey brown, apical inner wide, about two thirds as wide as tibia, terga and apex of mandible darker. Pedicel except surface uniformly setose. base, first flagellomere (often except apex), and basal area k) Propodeum rather short, steeply rest of flagellum dusky, paler beneath. Middle and inclined, medially smooth, shiny, glabrous and hind basitarsi and posterior margin of hind but with small, isolated of hairs sub- tibia often or blackish atricornis patch dusky ( T pale narrower than tho- laterally, above. Metasoma form nearly identical, dark form chestnut brown, first four rax, not particularly elongate, terga mesoscutum dark brown, epistomal suture black; smooth, shiny. malar space, hind tibia and basitarsus, and apical is based on The name of this subgenus Papua, terga sometimes blackish). a of part New Guinea, plus Trigona. Pilosity. Occiput and \'ertex with moderatcK' Classification of thf: Apidae 155

Figures 206-211. Trigona atricornis Smith and T. genalis Friese. 206, 207, Outer views and inner views of basitarsus and apex of tibia and cross-section of inner tibial surface of workers of T. atricornis and genalis. 208, Same, queen of T. genalis. 209-211, Outer views of tibia and basitarsus, T. genalis queen and worker, T. atricornis worker. (Drawings by S. F. Sakagami.)

dense, pale brown bristles, up to about 200 ^ and laterally with sparse pale brown bristles to 50 to 150 5 long. (In. T. atricornis brown, up about fi H; T4 and similar but hairs on discs slightly similar but shorter denser. with bristles to long.) Ocellocular area with T6 pale brown 150 /i. and sparser hairs. Short appressed pale brown Sterna with simple hairs, some slightly curved hairs on upper face; more conspicuous on lower apically, to 175 ^. face, some plumose, silvery in some positions; on Structure. See measurements. Table 6, and sub- apex of clypeus some erect hairs. Mesoscutum Lateral ocellus less atricornis generic description. pro- with sparse, erect hairs, 50-75 /x long (in tuberant than in T. atricornis (Figs. 194, 195). denser and 125-150 fi) and denser fine semiap- Sculpture coarser and less shining than in atricor- pressed hairs ± 25 ^ long (in atricornis ± 50 ^). nis Basal vein usu- atricornis to (see subgeneric description). Scutellar bristles up to 175 /x long (in ally meeting cu-v of forewing, rarely basal or 250 n), rather sparse. Pleura with fine, dense distal to cu-v (in atricornis, usually basal). Hind hairs 25-30 fi and sparser, semierect, plumose tibial and basitarsal character states illustrated for to below. white hairs over 50 fi long above 300 fi genalis and atricornis. Propodeum above broadly glabrous medially, lat- erally with small patch of sparse hairs (Fig. 203) QUEEN: Entirely honey brown, with caste well as in differences to if not (this patch also present in T. atricornis as from worker common many T. moorei Schwarz). Tl and T2 discs virtually all known stingless bees: longer head, smaller glabrous with few fine pale brown hairs up to 20 ^ ocelli, longer malar space, smaller eye, longer long; T3 similar but apical fimbria more distinct supraorbital part of head, longer scape, wider 156 The University of Kansas Science Bulletin

Guinea: 50 from nest River near Ker- mesosoma, larger metasoma (cf. Figs. 195, 196), 9, Marua less reduced sting (Figs. 218, 219), more reduced ema, 6 May 1959 (CD. Michener). Northeast New and hind tibia and mouthparts (Figs. 214-217), Guinea: One, Dreikikir, Sepik District, 350 m basitarsus (Figs. 207-210). altitude, June, 1969 (J.L. and M. Gressitt). EXAMINED: CDM examined SPECIMENS Indonesian New Guinea: 22, Bodem, 10-17 July lent Dr. F. Koch of the three specimens kindly by 1959 (TC. Maa); 22, Bodem, 11 km SE of Museum fiir Naturkunde, Berlin. Two bear Oefberfaren, 100 m altitude, 7-17 July 1959 Friese's labels. The other has orange "Typus" (TO. Maa); one, Bodem, Sarmi area, 10 July and we it as the the red label, "Type," designate 1959 (TC. Maa); two, Waris, south of Hollan- It well as the other two is lectotype. (as specimens) dia, 450-500 m altitude, 1-2 August 1959 (TC. labeled "Manikion 16.28.11.03" [Feb. 16-28, Maa); Klamono Oil Fields, 14-18 August 1948 1904 Friese det. m" 1903] "'Tngona genalis [mihi]. (M.A. Lieftinck). The last specimens are in the Manikion was on the north coast of evidently Leiden Museum. All others are in the Bishop Indonesian New Guinea; one of the in specimens, Museum, Honolulu; duplicates are in the Snow addition to the labels listed above, is labeled "N. Entomological Museum, Lawrence, Kansas; the Holland. with refer- Guinea, 03", presumably Universidade Federal do Parana, Curitiba; and ence to Hollandia = Kotabaru = = ( Sukarnapura the S. F. Sakagami Collection, Hokkaido Univer- Djajapura). sity, Sapporo. Other are as follows workers specimens (all Fragmentary information on the nest on the one from Marua Papua New except queen River): Marua River is given by Michener (1961).

TABLE 6. Measurements of Trigona genalis (G) and T. atricornis (A) workers (n= 10 for each species).

Feature Classification of the Apiuak 157

212

Figures 212-219. Trigona genalis Friese. 212, 213, S6 of queen and worker. 214, 215, Maxilla, worker and queen. 216, 217, Labium, worker and queen. 218, 219, Sting and associated structures, worker and queen. (Drawings by S. F. Sakagami.) Scale line for S6, 0.5 mm; for other structures, 0.25 mm.

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