The corbiculae of bees Charles D. Michener

To cite this version:

Charles D. Michener. The corbiculae of bees. Apidologie, Springer Verlag, 1999, 30 (1), pp.67-74. ￿hal-00891567￿

HAL Id: hal-00891567 https://hal.archives-ouvertes.fr/hal-00891567 Submitted on 1 Jan 1999

HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Original article

The corbiculae of bees

Charles D. Michener

Snow Entomological Division, Natural History Museum, and Department of Entomology, The University of Kansas, Lawrence, KS 66045, USA

(Received 6 July 1998; accepted 23 August 1998)

Abstract - The word corbicula is ordinarily used for the ’pollen basket’ on the outer side of the hind tibia of worker honey bees and related forms. Unrelated bees have comparable but nonhomol- ogous structures, often on other parts of the body. Such structures are described on the hind femora and on the propodeum, as well as on the hind tibiae of two diverse groups of bees. © Inra/ DIB/AGIB/Elsevier, Paris bees / Apoidea / corbicula / pollen transport / anatomy

1. INTRODUCTION of pollen; it is probably easier to remove pollen from a corbicula than to remove an equal amount of pollen carried within a Most female bees have areas of fre- long, brush of hairs. The carried in the tib- dense hairs, the for pollen quently scopae, carrying ial corbiculae of the corbiculate Apidae, pollen from its floral sources to nests. A such as Apis, is moistened with nectar to scopa can be on the hind legs, on the under- form a firm mass or pellet on each hind tibia. side of the or even on the sides of metasoma, In all other corbiculae the pollen is carried the There are various and propodeum. types dry. densities of scopal hairs, presumably related to the characteristics of the pollen to be car- The case can be made for limiting the ried [10]. A common development is a space word corbicula to structures on the hind tibia surrounded by fringes of long scopal hairs. that carry moistened pollen, because this is Such a space has been called a corbicula the familiar usage of the word. So limited, it [10] and serves for transport of a large bulk is applicable only to the tribes Apini,

* Correspondence and reprints E-mail: [email protected] Bombini, Euglossini and Meliponini. How- space between these two zones of long hairs. ever, the term corbicula is used in the present The femoral surface of the corbicula is typ- broad sense by some authors [3, 10] and in ically flattened, hairless, impunctate, often fact a synonymous generic name for smooth and shining, but sometimes gives Canephorula, which carries dry pollen in a rise to a few long hairs or some short hairs. tibial corbicula, is Corbicula. Clearly vari- Because the lower surface of the femur is ous corbiculae are not homologous, any often formed into a strong longitudinal ridge more than a sternal scopa is homologous to from which the inner corbicular fringe arises, a tibial scopa. the femoral corbicula is often on the lower outer surface of the femur, rather than on One system for describing parts of legs the lower surface in a strict sense. The assumes that the legs are pulled out later- femoral corbicula is closed basal ally at right angles to the long axis of the basally by femoral hairs and the hairs body. I here follow the more traditional sys- principally by of the which are and curved tem in which are considered to be in trochanter, long legs in their normal the hind distad. They are especially well developed resting positions, in femur directed back beside the body of the the genus Andrena (Andrenidae), Dipha- and in Oxaeinae bee. Thus the corbicula of Bombus is on the glossinae (Colletidae), where have been a outer, not the anterior, surface of the hind (Andrenidae), they given the flocculus or floccus tibia and the two tibial spurs would be outer special name, (fig- ures 3 and and inner, not anterior and posterior. 4). Museum specimens that do not have large pollen loads often have pollen entan- 2. FEMORAL CORBICULAE gled in the corbicular fringes, but not occu- pying the corbiculae themselves. It is pos- The most widespread corbicular site is sible that the smooth, hairless or sparsely on the underside of the hind femur of many haired lower femoral surface evolved in members of the short-tongued bee families some other connection, and not as a pollen- Stenotritidae, Colletidae, Andrenidae and carrying area. Halictidae. While in these fam- widespread Sometimes the outer and inner corbicular ilies, the femoral corbicula is absent or little curl until their meet and hide or in the colletid subfamilies fringes tips developed close the corbicula. Such well-developed Hylaeinae and Euryglossinae, in the fringes are found, for example, in the Dipha- andrenid Panurginae and some subfamily glossinae and Oxaeinae. On the other hand small genera of Andreninae, and in the hal- in some groups, perhaps especially in those ictid subfamily Rophitinae as well as in par- Leioproctus (Colletinae) with a well-devel- asitic Halictinae. (The higher classification oped sternal scopa, the corbicular fringes used herein is based on [1] and [8], sum- are reduced, not different from marized in [5].) This femoral corbicula is being very those of long-tongued bees, which are not formed a) a zone of by long, frequently considered to have a femoral corbicula. plumose hairs that arise on the upper part are Leioproctus subgenera Hex- of the outer surface or even on the Examples upper antheda and surface of the femur and curl downward, Cephalocolletes. over the outer femoral surface (figures 1 In the halictid genus Lasioglossum, sub- and 3), and b) a band or row of long, some- genus Sphecodogastra, the fringes consist times straight hairs that arise on the inner of simple hairs and are largely reduced and surface, frequently on the lower inner sur- rather weak. However, the lowermost row of face, of the femur (figures 2 and 4). These hairs of the outer fringe is isolated by a bare are the outer and inner corbicular fringes, area and consists of long curved bristles. respectively. The femoral corbicula is the This appears to be an adaptation for the use of pollen of Onagraceae which is webbed described above. Bees having such femora together by viscin threads. include the Melittidae (a name here used in the sense to The short hairs found on hind femora of broad include the three related families in and most non- spheciform wasps (Sphecidae, Crabronidae) segregated [1]) bees are widely distributed and frequently parasitic long-tongued (Megachilidae, as well as the appressed. In some wasps (e.g. Crahro), Apidae), short-tongued groups however, the under surface of the hind femur Panurginae (Andrenidae) and Rophitinae (Halictidae). These forms do not much is flattened and shining, with or without carry short hairs, and the short simple hairs of the pollen on the femora, the tibial scopa being the structure. Such outer and inner surfaces are directed down- major pollen-carrying femoral structure, however, with ward. The same is true of parasitic bees that intergrades that of most Colletidae, Andrenidae and do not collect pollen (Nomadinae and Eri- crocidini in the Apidae, Sphecodes and its Halictidae, which (except for the forms men- relatives in the Halictidae), and of nonpara- tioned above) have well-developed femoral fringes and corbiculae and appear to carry sitic bees that carry pollen in the crop instead more on the femora than on the tibiae. of externally (Euryglossinae and Hylaeinae pollen The Stenotritidae carry more on the in the Colletidae). In such forms there is no pollen tibiae than the have indication of the outer and inner corbicular femora, yet moderately short femoral fringes. developed although fringes. Perhaps only because they are generally The long-tongued bees, however, are not more hairy insects, many bees have hind as uniform as the above comments suggest. femora that differ from those described in For example, in the Megachilidae, Lithurgus the paragraph above by having longer and has long, curved hairs on the outer femoral often more abundant hairs. The largely bare surface, some of them arising on the upper under surface of the hind femur is therefore surface, and many hairs on the inner sur- better set off from the hairy outer and inner face as well. Thus there is an approach to surfaces, the downward-directed hairs of fringes although they do not carry much which suggest the corbicular fringes pollen. The same statements apply to Cer- atina and Allodape in the apid subfamily only sparsely haired and serves as a corbic- Xylocopinae, but Xylocopa in the same sub- ula. In many species of Andrena there is in family has only short femoral hairs. In these addition a vertical fringe along the anterior forms, the more or less smooth and largely margin of the side of the propodeum. Thus hairless lower surface of the femur is as in a propodeal corbicula is formed, demarked bees with a femoral corbicula. The apid by dorsal, posterior and anterior fringes (fig- tribes Bombini and Euglossini, however, ure 13). completely lack femoral fringes and the lower femoral surface or much of it is punc- tate with short hairs, much like the other 4. TIBIAL CORBICULAE: surfaces. The tribes Apini and Meliponini THE CORBICULATE APIDAE have scattered short hairs and no sugges- tions of fringes or of a femoral corbicula. Thus the corbiculate Apidae differ distinctly By far the best known corbicula, and the from other Apinae. one widely known as the corbicula, is on the outer side of the hind tibia of the Apini, The absence of a femoral corbicula in Bombini, Euglossini and Meliponini (Api- Melittidae and bees supports long-tongued dae). These are the bees in what was called the conclusion [1] that the short- previous the apine clade in recent phylogenetic stud- Melittidae is ancestral to or tongued family ies [8]; this is not the line of Silveira the sister of the bees. apine group long-tongued [9]. The has been made, Dr The femoral corbicula of suggestion by well-developed Rudolf Jander and simultaneously by oth- most Colletidae, Andrenidae and Halicti- ers, that instead of being called representa- dae be a of these may synapomorphy tives of the apine clade, the tribes listed lost in and those that trans- groups, parasites above should be called the corbiculate in the and reduced in Api- port pollen only crop, dae. I believe that this is a useful term even the (Andrenidae) and Panurginae Rophiti- as described below, at least one Thus these three families though, nae(Halictidae). species of Eucerini (also in the Apidae) also may constitute a clade derived from or sis- has tibial corbiculae. The family name Api- ter to the melittid-long-tongued bee clade. dae has been applied to the group of four For a fuller discussion of relationships corbiculate tribes alone [4], but this usage is among these groups, see [5]. inappropriate as shown by the phylogenetic studies cited above.

3. PROPODEAL CORBICULAE Michener [4] illustrated the tibial cor- biculae of the four tribes of corbiculate Api- A common propodeal hair pattern among dae. Modified versions of some of those females of short-tongued bees includes long, illustrations are shown in figures 5-9. These dense, erect hairs projecting laterally from tibial corbiculae serve not only to transport the upper margin of the lateral surface of masses of moistened pollen, but also of the propodeum. Below these long hairs the resin, wax, mud, feces, etc. The fringes propodeal surface usually bears shorter hairs. (anterior and posterior or if the tibia is All these hairs often carry some pollen. In extended horizontally, then upper and lower) some Colletinae and Diphaglossinae (Col- and the distinctive flat or concave and usu- letidae) and most Andrena [3] (Andrenidae), ally smooth corbicular surface are lost in the dorsal zone of long hairs extends pos- parasitic genera or subgenera and in robber teriorly and downward along the lateral genera (Lestrimelitta, Cleptotrigona) and angle, demarking the posterior propodeal are weakened in the necrophagous species of surface. Thus there are dorsal and posterior Trigona that do not visit flowers or collect fringes around an area that is usually bare or pollen. The tibial corbicular fringes of Apini and has no corbicular function, although when Bombini are made up of hairs that project the bee is carrying a large pollen load this more or less laterally and thus delimit the area is probably filled. An Argentine species, corbicula. In Euglossini and many Canephorula apiformis (Friese), has dis- Meliponini, however, the hairs of the pos- tinct tibial corbiculae, however. It was terior fringe project posteriorly, thus expand- placed in its own tribe, the Canephorulini, in ing but not enclosing the corbicular area. 1955 [6], but in a recent phylogenetic study As shown in figures 6 and 7, the hairs of [8], it came out among the Eucerini, or more the fringes can be remarkably sparse. In particularly, in the subtribe Eucerina. It has Partamona (figure 9) the tibia is greatly certain characters, such as the simple rather broadened so that the corbicula is large in than doubly arched gradulus of S2 of the spite of the sparse fringes. In Trigonisca female, that are probably plesiomorphic rel- (figure 8), however, the tibia is slender and ative to other Eucerina. A more detailed the hairs so sparse that no corbicula would study of the Eucerina may show Canepho- be recognized except for the presence of a rula to be the sister group of the other Euce- firm pollen mass on each hind tibia. rina, possibly to be called a subtribe of its own, the Canephorulina. Its most remark- able feature, the hind tibia with a corbicula 5. TIBIAL CORBICULAE: margined posteriorly by a single row of THE EUCERINI coarse bristles and a tuft of long plumose hairs, is shown in figure 12 (see also illus- tration by Friese [2]). The anterior fringe The other bees with tibial corbiculae, only consists of long hairs that curve over and in this case for carrying dry pollen, are in partly hide the corbicula. the tribe Eucerini (family Apidae). In this tribe, the outer surface of the hind tibia of the A second Argentine eucerine with a sug- female normally ends in a small impunctate gestion of a corbicula is the recently hairless area (figure 10). So far as I know, it described Hamatothrix silvae Urban. It lacks the unusual, possibly plesiomorphic char- 6. CONCLUSIONS acters of Cauephorula, and is thus a more ordinary eucerine, close to the genus Gae- Large spaces surrounded by scopal hairs sischia. The possible corbicula (figure 11) is of bees have arisen at least once in the short- small, scarcely larger than th7 bare space tongued families (femoral corbiculae, fig- found in most Eucerini (figure 10). The ures 1-4), once in the Andrenidae (propodeal clump of strong bristles on its posterior mar- corbiculae, figure 13), once in the corbicu- gin basally suggests the plumose hairs of late Apidae (tibial corbiculae, figures 5-9), Canephorula. If the comblike row of bristles and once in the Eucerini (tibial corbiculae of and long hairs of Canephorula comb pollen Canephorula, figure 12). Studies of how into the corbicula, the similarly positioned the corbiculae are loaded and emptied would long hairs or bristles of Hamatothrix prob- be of much interest; such studies have been ably have the same function. made for the Apini and at least started for other corbiculate Apidae [7]. For other types nen Haaren umrandet sind. Allgemein of corbiculae, no such information exists bekannt sind die Körbchen an den Tibien and indeed their importance in pollen trans- der Hinterbeine. Diese kommen bei den port is not verified. Euglossini (Prachtbienen) und Bombini (Hummeln), sowie bei den Arbeiterinnen der Apini (Honigbienen) und Meliponini (stachellosen Bienen) vor, also bei den cor- Résumé - Les corbicules des abeilles. Les biculaten Apidae. Weniger bekannt ist dage- corbicules, qui servent à transporter le pol- gen, daß sich Körbchen bei Weibchen der len et d’autres matériaux au nid, désignent meisten kurzrüsseligen Bienen auch an der l’espace qu’entourent les franges des longs Unterseite des hinteren Femur, bei vielen poils de la brosse à pollen. Elles sont bien Andrenaarten (Sandbienen) an den Seiten connues sur les tarses des pattes postérieures des Propodeum am Thorax und bei minde- chez les Euglossini et les Bombini (bour- stens einer Art der Gattung Eucerini (Lang- dons), ainsi que chez les ouvrières des Apini hornbienen) an der hinteren Tibia befinden. (abeilles mellifères) et des Meliponini Die punktierten Bereiche auf den Bildern (abeilles sans dard), c’est-à-dire chez les zeigen jeweils die Oberfläche innerhalb der Apidae à corbicules. Par contre il n’est géné- Körbchen. Das Körbchen am Femur ist der ralement pas reconnu qu’elles existent aussi häufigste Typ und ist möglicherweise eine sur la partie inférieure des fémurs des pattes Synapomorphie von Andrenidae (Sandbie- postérieures des femelles de la plupart des nen), Colletidae (Seidenbienen) und Halic- abeilles à langue courte, sur les côtés du tidae (Schmalbienen), die diese Familien zu propodeum (premier segment abdominal en einem Zweig mit gemeinsamer Abstam- avant du pétiole) de nombreuses espèces mung von einer Urbiene zusammenfaßt. d’andrènes (Andrena sp.) et sur les tibias Entsprechend ist das Körbchen an den des pattes postérieures d’au moins une Tibien eine Synapomorphie, die die vier espèce de la tribu des Eucerini. Sur les Stämme der corbiculaten Apidae zu einem figures les parties en pointillés représentent anderen Zweig vereint. © Inra/DIB/AGIB/ la surface de l’intérieur des corbicules. La Elsevier, Paris corbicule fémorale représente le type le plus courant et peut être une synapomorphie des Bienen / Apoidea / Körbchen / Andrenidae, des Colletidae et des Halicti- Pollentransport / Anatomie dae, qui unit ces familles en un clade pro- venant d’une abeille ancestrale; de même la corbicule du tibia est une synapomorphie REFERENCES unissant en un clade les quatre tribus des à corbicules. © Inra/DIB/AGIB/ [1] Alexander B.A., Michener, C.D., Phylogenetic Apidae studies of of Paris the families short-tongued bees. Elsevier, Univ. Kansas Sci. Bull. 55 (1995) 377-424. [2] Friese H., Canephorula apiformis Friese (Hym.). Apoidea / abeille / corbicule / transport eine Bienen-Art mit dem Beginne der Körbchen- de pollen / anatomie Bildung aus Argentinien. Zool. Jahrb., Abt. Syst., Geogr. Biol. Ticre 43 ( 1920) 461-470. [3] Lanham U.N.. A suhgenerie classification of the New World bees of the genus Andrena, Univ. California Publ. Entomol. 8 (1949) i-iv + Zusammenfassung - Die Körbchen bei 183-237. Michener Classification of the Bienen. Die Körbchen der Bienen zum [4] C.D., Apidae, Univ. Kansas Sci. Bull. 54 (1990) 75-153. Transport von Pollen und anderem Mate- [5] Michener C.D., The Bees of the World: A Com- rial zum Nest sind Bereiche am letzten Bein- prehensive Guide, Johns Hopkins University paar, die von langen, mit Fransen versehe- Press, Baltimore. 1999. [6] Michener C.D., LaBerge W.E., Moure J.S., bees, Univ. Kansas Sci. Bull. 55 (1993) Canephorulini, a tribe of South American bees, 124-162. Dusenia 6 (1955) 207-212. [9] Silveira F.A., Phylogenetic relationships of the [7] Michener C.D., Winston M.L., Jander R., Pollen Exomalopsini and Ancylini, Univ. Kansas Sci. manipulation and related activities and struc- Bull. 55 (1993) 163-173. tures in bees of the Univ. Kansas family Apidae, and Sci. Bull. 51 (1978) 575-601. [10] Thorp R.W., Structural, behavioral, physi- ological adaptations of bees (Apoidea) for col- [8] Roig-Alsina A., Michener C.D., Studies of the lecting pollen, Ann. Missouri Bot. Garden 66 phylogeny and classification of long-tongued (1979) 788-812.