UDC 595.799:591.521 Entomological Review, 75 (2), 1996

"Protobee" and Its Nests: A New Hypothesis Concerningthe Early Evolution of Apoidea (Hymenoptera)*

V. G. RADCHENKO and VU". A. PESENKO

Institute of Zoology, National Academy of Sciences, Ukraine;Institute of Zoology, Russian Academy of Sciences, St. Petersburg

Abstract. Published opinions concerning the origin and early evolution of bees arecritically reviewed. A new hypothesis on the "protobee" (the nearest common ances­tor of Apoidea) is advanced and substantiated. It includes the following statements:(1) the protobee transferred pollen on the surface of its body (instead of transportingit in its crop as considered in the current version), (2) it stored doughlike (instead ofliquid) provisions for its larvae, (3) it did not line cells by secreted or other sub­stances, (4) it dug nests in soil (instead of building them in natural cavities), (5) inbuilding nests it loosened soil by mandibles and soil out of the burrow with the helpof the metasoma (it did not dig and throw soil out by the legs as many wasps do), (6)it mechanically processed (smoothed and tamped) the inner walls of cells with thehelp of the pygidial and metabasitibial plates, (7) it built branched (instead of linear)nests with cell horizontally oriented (instead of vertically as is necessary to storeliquid provisions), (8) its larva spun a cocoon (which is denied by adherents of thecurrent version).

Key words: Hymenoptera; A.poidea; evolution.

1. COMNION AND NEW VERSIONS

Wasplike ancestor of bees. According to the conventional view (Muller, 1872, 1873, 1883:Malyshev, 1911, 1913, 1959, 1966; Michener, 1944, 1964, 1965, 1979; Brothers, 1975; Rasnitsyn,1980; Lomholdt, 1982, etc.) bees originated from sphecoid wasps in the Upper Cretaceous. Accordingto Michener (1964), whose view coincides with ours, this wasplike ancestor in order to rear offspringexcavated nests in the soil consisting of a tunnel leading to small rearing chambers--cells withoutsecretory lining; its larvae spun tough cocoons. Michener associated the absence of a lining inside thecells with the fact that the wasp-ancestor of bees stored insects for food, which were well protectedfrom rapid desiccation by a tough epicuticle.

Malyshev (1913, 1950, 1951, 1959, 1966), on the contrary, supposed that in the wasplike ances­tor of bees the cocoon was absent, and cells were coated from the inside with a secretory substance thatprevented desiccation of larval food, which consisted of a mixture of chewed insects. This is exactlywhat contemporary wasps of the subfamily Pemphredoninae do. Their females line the cells with silkyfilm. Based on the external similarity of the cell linings and consistency of their content in these waspswith bees from the genus Hylaeus of the family Colletidae, which Malyshev considered to be the mostprimitive bees, he and many other authors who followed him (Bohart and Menke, 1976; Hennann,1979; Batra, 1980, 1984; McGinley, 1980; Budris, 1990; etc.) consider Pemphredoninae as the group

*Originally published in Entomologicheskoye Obozreniye, Vol. 73, No. 4, 1994, pp. 913-933.

140 ISSNOO 13-8738/96/0002-0 140© 1996 Scripta Technica, Inc.

of bees closest to the ancestor. Moreover, in his last book Malyshev (1966, pp. 300-301) insists thatPemphredoninae of the tribe Psenini are particularly close to the ancestor of bees. They build nests inready cavities, rather than excavating them in the soil as do bees of the genus Hylaeus. After revisionof views on the generality of Colletidae (see below for details) of the question of the group of wasps,the ancestor of which was common with bees, remains open. The origin of bees from the depths ofSphecoidea still remains beyond doubt, according to the great majority of researchers (among recentpublications, see Alexander, 1992).

We will mention other points of view of the origin of bees, although, in the light of contempo­rary data, they do not appear sufficiently grounded. Thus, Bernard (1951) continues to support thehypothesis of the polyphyletic origin of bees from two different groups of Sphecidae proposed longago by Friese (1926). Iuga (1989) rejects the possibility of the origin of bees from Sphecoidea becausein the labiomaxillary complex (the tongue) of Sphecoidea, which she considers to be rudimentary,many structures that are supposed to be present in the ancestor of bees with a complex proboscis arereduced. Finally Lanham (1979, 1980, 1988, etc.) in a series of publications developed the idea thatbees, as well as ants, most likely originated from Scolioidea (from Multillidae or Tiphiidae), to whichbees are similar in the presence of branching setae and absence of strigils on the hindlegs. The lattercharacter provided the rationale for Borner (1919) to unite Formicoidea, Apoidea, and Scolioidea intoone group (Haplocnemata) of sting bearers, and Sphecoidea, Pompiloidea, and Vespoidea, havingstrigils on forelegs and hindlegs, in another group of Diplocnemata. However, such a division was laterrejected because of serious contradictions with morphologic data on many other structures.

Protobee: the conventional version. According to the opinion published first by Muller (1883)and later supported by other researchers (Verhoeff, 1892; Reuter, 1913; Malyshev, 1913, 1959, 1966;Gutbir, 1916; Michener, 1953, 1964, 1979; Batra, 1980; etc.) the ancestor of bees during transitionfrom animal to plant food began to store, for its offspring, highly liquid food consisting of nectar witha small amount of pollen. This protobee did not have special adaptations on its body for collectingpollen; it simply swallowed nectar with pollen, which then was regurgitated into cells. According toMalyshev (1966) primitive bees retained the secretory cell lining from the ancestral bee, and, accord­ing to Michener (1964), they obtained such a lining simultaneously with loss of the ability to spincocoons.

The authors cited above considerably substantiate these conclusions concerning the storage ofliquid food and subsequently presence of a non-water-permeable lining by the fact that most modemrepresentatives of Colletidae, previously considered as the most generalized bees, store liquid food fortheir offspring in cells lined with a secretory film. Colletidae of the subfamilies Euryglossinae andHylaeinae carry pollen in the crop because they do not possess a collecting apparatus on the surface ofthe body (scopae; see part 2 for details). Precisely the latter fact is cited by many authors as majorevidence in favor of carrying the food in the crop by the ancestor of bees.

What kind of bee is the most primitive? The widely held understanding of the generality ofColletidae was substantiated in the well known monograph by Michener (1944) and supported by allapidologists. Only 36 years later was it doubted indirectly because of the revision of the status andphylogenetic position of groups of bees united in the family Melittidae (Michener and Greenberg,1980; see also Michener, 1981). Then Michener (1981) and Michener and Brooks (1984) conducted aspecific investigation of the structure of the glossa in bees and found the arguments of Perkins (1912)and McGinley (1980) convincing and~rejected the primitive nature of Colletidae. A major characterdistinguishing Colletidae from other bees, the broad and doubled glossa formerly considered as acharacter ancestral for all bees and directly inherited by them from a wasplike ancestor, is nowinterpreted as an apomorphic character, in other words, acquired by an ancestor of Colletidae after theyhad branched from a major stem leading to remaining families of bees.

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At present intensive investigations on the comparative morphology of bees for the purpose ofreconstruction of their phylogeny, positions, and relationships (primarily Hcladogenetic," see Pesenko,1989) among many large groups of bees are still not sufficient. Thus, so far any reliable synapomorphyamong major families of lower ("with short proboscis") bees-Colletidae (+Stenotritidae),Andrenidae, Oxaeidae, and Halictidae--have never been found. They also have never been foundamong subfamilies of Melittidae (Meganomiinae, Melittinae, and Dasypodinae), which occupy anintermediate position between bees with short and long proboscis and whose divergence is probablyassociated with the earliest steps of phylogenetic development of bees. Possible candidates by maximalaffinity based on an anagenetic component of their phylogeny by morphologic characters to the closestcommon ancestor of bees, which further we will call the Hprotobee," the following taxa are equallysuitable: Paracolletini (Colletidae), Rophitinae (Halictidae), Andreninae (Andrenidae), and Melittinae(Melittidae).

Protobee: A new version. Rejection of the plesiomorphy of the glossa of Colletidae and thegeherality of this family inevitably leads to revision of the Happearance" of the protobee, which isbased on the conventional version supported in pure fonn by Michener (1979, p. 299) until 1979. Wepropose a new hypothesis concerning the protobee, according to which the closest ancestor of beesalready had the scopae and carried pollen on the surface of the body (not in the crop), stored food forlarvae in fonn of "bread" made of a pastrylike (not liquid) mass, did not line cells from inside withsecretory (or other kind of) substances, and its larvae pupated in the cocoon.

All these biologic characteristics of the protobee are supported by convincing morphologicevidence, which is summarized in the table and considered in detail below (parts 2-7). They alsomutually support each other (see 2nd and 3rd columns in the table) and are in good agreement with thegeneral picture of the most likely mode of transition to feeding larvae of primitive bees with pollen(see end of part 6). Besides, data on the morphology confirming that the major method of nestconstruction of the protobee was Heating out" soil by using mandibles, and that the protobee treatedmechanically (smoothed out and compacted) the walls of cells; these elements of behavior of theprotobee have never been discussed in the literature in detail.

It is possible to propose better grounded evidence in favor of nesting of the protobee in the soiland also to offer a better substantiated and detailed characteristic of this nest including the followingparameters: the multicellular nest consisting of a major vertical tunnel and several horizontal lateraltunnels of the same width as the major tunnel· and originating from it at different levels; each lateraltunnel leading to one cell; cells are positioned horizontally and were closed by a special lid. The tablealso includes such an obvious characteristic of the protobee as its solitary way of life; naturally, it isunderstood that it also was not a cleptoparasite.

Before moving on to the substantiation of the proposed hypothesis concerning the protobee andits nest we will note the following. The wasp which gave start to the line leading fmally to the protobeemust have undergone on this route essential evolutionary changes in morphology (emergence ofpubescence and scopae, widening of metabasitarsus and appearance of brush on it for combing offpollen from the body and fonnation of the ball of packed pollen, loss of spurs on legs, appearance ofmetabasitibial plates, etc.) and also numerous changes in bionomics, ethology, and physiology associ­ated with the transition from predation to feeding larvae with vegetable food. All these changesindicate the intensity of evolutionary transfonnations on the way from the wasp-ancestor to the prinli­tive bee, although this way need not necessarily be very long in time.

As to how all this happened, including the sequence of the appearance of certain evolutionaryand adaptive innovations, nothing can be said with certainty (except possibly some purely logical

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conclusions), because in the paleontologic record traces of this process are completely absent. Allknown fossil bees (see reviews of Zeuner and Manning, 1976; Michener, 1979, pp. 288-290, etc.)belong not only to contemporary families and subfamilies but also in great majority to modem tribesand genera of bees. Paleontologic remains of nests supposedly belonging to bees (see, e.g., Retallack,1984; Houston, 1987, etc.) also do not add anything. Therefore at this level of knowledge well­grounded hypotheses can be proposed only concerning the closest common ancestor of bees, in otherwords species differentiation of which tens of millions of years ago produced two (or more) majorphylogenetic lines of contemporary families of bees. Such an immediate ancestor of bees, which wecall the protobee, may be reconstructed as a hypothetic species characterized exclusively by a set ofplesiolnorphic states of different characters of bees, both morphologic and biologic.

Our sununary of all major data on the biology of bees (over 5000 publications were analyzed)fonus the basis of the discussion of the new hypothesis concerning the protobee offered below. Fordistinction and analysis of adaptive morphologic character of bees associated with peculiarities of theirnesting, besides references to appropriate literature data, representatives of 282 genera were examined.They were selected out of 394 genera of the world fauna from all suprageneric taxa of nonparasiticbees, 26 tribes, 14 subfamilies not divided into tribes, and 4 families not divided into subfamilies andtribes, except the tribe Manuelini, which are preserved in collections of the Zoological Institute of theRussian Academy of Sciences, 51. Petersburg.

2. COLLECTION OF POLLEN ON THE BODY SURFACE

Major evidence. Even without disputing the generalist nature of Colletidae as a family ingeneral, serious arguments are raised by the statement that the protobee was a nonpubescent insectsimilar to a wasp, transferring liquid food for larvae in its crop, in other words or insect similar tocontemporary Hylaeinae and Euryglossinae, and not capable of transferring pollen in form of packedpollen on the surface of the body as is done by representatives of the three remaining subfamilies ofColletidae and all other nonparasitic bees. The following arguments can be proposed to support thelatter proposition (and against the base protobee): 1) widened 1st segment of hindtarsi; 2) unlikelihoodof 4-5 times of independent appearance of pubescence and scopae in different branches of bees (andalso their relatively easy loss); 3) apparently specialized method of transporting of food in the crop,feeding larvae with liquid food and peculiarities of construction of cells for its storage; 4) impossibilityof combination of the concept of the feeding larva of the protobee predominately with nectar with themost probable logical model of transition of their feeding from animal to plant food. The latter twoarguments are considered in part 7.

The flattened metabasitarsus. A major synapomorphy of bees and actually the only characterby which imagines of all bees differ from sphecoid wasps is the flattened 1st hindtarsal segment(according to modern terminology, the metabasitarsus). In females of nonparasitic bees transportingpollen on the body (as a packed ball) with a scopae of any kind, the widened metabasitarsus on theinner surface of the body always bears a special brush of short, straight, stiff, and obliquely directedsetae, which is used to comb off pollen from the body and form the packed pollen ball. It is impossibleto imagine any other functional purpose of the flattened metabasitarus except adaptation to the efficienttransportation of pollen by the bee on the surface of its body.

The flattened metabasitarsus is present in all bees, without exception, including cleptoparasiticspecies and Colletidae without scopae of subfamilies Hylaeinae and Euryglossinae, and also in malesof all these species. This certainly indicates that the protobee had a flattened metabasitarsus. Therefore,it transported pollen on the surface of its body (not in the crop), supposedly even in weakly differenti­ated and not yet specialized scopae, which most likely occupied the entire outer surface of the

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Character

1. Pollen carried on surfaceof body (in scopae).

n. Mechanical treatment ofwalls of cells.

Ill. Nesting in soil, breakingsoil with mandibles.

IV. Spinning cocoon.

V. Absence of secretory lininginside cells.

VI. Preparation of larval foodin fonn of bread ofpastrylike substance.

Biologic characteristic of the protobee

Morphologic evidence

Metabasitarsus flattened(bearing brush for combingoff pollen) - synapomorphy inbees. Pubescent and unspecial­ized scopae - synapomorphyand plesiomorphy in bees.

Pygidial and metabasitibialplates (for compacting andpolishing walls of cells) ­plesiomorphy in bees.

Flattened mandibles (adaptedfor digging in soil) - plesio­morphy in bees.

Developed spinning apparatus ­plesiomorphy in bees.

Narrow, pointed glossa - plesio­morphy in bees (indicates onlyimpossibility of creation of lin­ing in fonn of cellophane film).

Protobee had scopae (see I).

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Biological and logicalevidence

Specialization and secondary adaptation for collect­ing and storing liquid food(see VII in Table).

Protobee did notcoat insides ofcells (see V) forprotection of foodagainst contamination.

Mechanical treatment ofwall of cells (see Il).

Improbability of multipleand independent emergenceof cocoon.

Negative correlation ofcocoon and lining (see IV).

Diversity of sourcesand methods ofpreparation of lining.

Absence of lining in cellsof protobee (see V).

Pattern of distribution ofcharacter "bread as food ofdifferent physical condi­tion." Specialization andsecondary adaptation ofpreparation of liquid food or"piled" pollen. Agreementbetween knowledge con­cerning transition of larvalfeeding from animal tovegetarian food.

Character

VII. Nest of branching type.

VIII. Solitary \vay of life

Table (continued)

Morphologic evidenceBiological and logical

evidence

Pattern of distribution of~th HefieQAtal ~81~icharacters: 4'branching nestsvs. nest of different type";horizontal cells vs. tilted orvertical cells"; "cells withoutlid." Storage of dry food (seeVI) not requiring verticallysituated cells.

Origin of bees from solitarysphecoid wasps. Pattern ofdistribution of character"solitary life - social life."

hindfemora and tibia, and also partly the lower metasoma. Moreover, it is possible that the flattening ofthe metabasitarsus took place at early steps of the evolution of the wasplike ancestor to the protobee,because this character has been fixed genetically in both sexes, although in males it does not haveimportant adaptive value.

Scopae did not appear many times. Besides cleptoparasitic bees (110 genera of 4 families,including genera Lestrimelitta and Cleptotrigona, obligatory stealing of food for larvae from nests ofother Meliponinae), which beyond any doubt lost the collecting apparatus secondarily and indepen­dently, cases of this absence in. known fossil and contemporary bees were found only amongColletidae. Scopae are absent in all representatives of the family Euryglossinae distributed in theAustralian Province and the Hylaeinae distributed nearly worldwide (with a small exception, whichwill be considered below), and also in Leioproctus (Euryglossidia) cyanescens (subfam. Colletinae;Houston, 1981). Michener's (1944, p. 237, 240) comment about the absence of the scopae also inColletidae of the subfamily Xeromelissinae (=Chilicolinae) has not been confmned: These bees trans­port pollen in the scopae, although their pubescence usually is sparse and short (Michener, 1974, p.26).

Houston (1981) convincingly linked the loss of the scopae by the female of L. cyanescens withtransition to collection of particularly large pollen grains, which cannot be held between setae; verysparse scopae is present in other species of the Australian subgenus Euryglossidia, which collect pollenfrom Hakea and Grevi//ea. It is possible that just this caused the collection of pollen in the crop also inall other cases. An important factor facilitating transition to transportation of pollen in the crop andsubsequently loss of the scopae by many representatives of Colletidae is the liquid state of the food,which almost all species of this family collect and store for their larvae. Bees probably can swallowand regurgitate pollen out of the crop only when it constitutes a small part of the nectar volume of thecrop. Besides, in the loss of the scopae by at least Hylaeinae, in our view, the transition of this group tobuilding nests in the plant substrate was very important. It took place in Xylocopinae, in which,

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according to Sakagami and Michener (1987), partial reduction of the scopae is compensated by thetransportation of a considerable part of the pollen in the crop.

Authors of published phylogenetic models agree that Hylaeinae and Euryglossinae together withXeromelissinae fonn a holophyletic group, but they disagree on the position of this group in thephylogenetic model of the entire family Colletidae and our relationships within this group of the threeconsidered subfamilies. Michener (1944, Fig. 13), based on data on the morphology of the imago,placed Hylaeinae and Euryglossinae more closely, and McGinley (1981, p. 168, Fig. 144) by themorphology of larvae is leaning toward relating Hylaeinae to Xeromelissinae. In the first case the lossof the scopae in Colletidae should take place twice, and the second case 3 times. It is clear that evenmultiple reduction (complete or partial) of the specific pubescence on legs and/or on the metasoma isconsiderably more likely (and explainable) than independent multiple appearance of the scopae in beesof different groups (2 or 3 times in Colletidae and 2 or 3 times in major branches of bees other thanColletidae), which inevitably follows from the idea of the protobee as a bare wasplike insect.

However, at least once scopae probably appeared repeatedly, because so far nothing can explainthe presence of the scopae on hindtibia in females of Hylaeinae from the recently described NewGuinean subgenus Cercorhiza of the genus Palaeorhiza (Hirashima, 1982). All the other severalhundreds of species of 15 genera of the subfamily Hylaeinae, as mentioned above, lack scopae.Because the genus Palaeorhiza cannot be recognized as a generalized genus (see Michener, 1965, p.144), the version concerning the loss of the scopae by Hylaeinae after the branching of the subgenusCercorhiza is also eliminated. The hypothesis concerning the secondary appearance of the scopae inthe immediate ancestor of this subgenus does not appear unrealistic because, unlike in the completelybare Palearctic species of Hylaeus, the only genus of Hylaeinae and Euryglossinae represented alsooutside the tropics, most tropical Hylaeinae, as well as Euryglossinae, retained pubescence on thebody. Therefore its development (increase of length and specialization) on individual parts of the body,particularly on hindtibia as in Cercorhiza, may relatively easily lead to the appearance of reducedscopae.

3. MECHANICAL TREATMENT OF WALLS OF CELLS

Model of argumentation. Compacting and polishing of walls of cells protects food for larvaestored in them from soil particles. Similar mechanical treatment of walls is known in some sphecoidwasps (for example, in Astata, see Bohart and Menke, 1976, p. 212), but it became particularlyimportant and widely distributed in bees because, first of all, it is difficult for the female to clean foodit prepares in a fonn of mixture of pollen and nectar from foreign particles and, second, larvae of beeswith their soft mouth organs cannot chew and swallow particles of soil, which causes their death(Radchenko, 1990). An alternative method of protection of food from contamination by soil (oftencompatible with the compacting of \valls) is the secretory lining of cells prepared by Colletidae, andalso lining of cells by different materials, which is done by Megachilidae. All remaining bees, and alsomany Colletidae which build nests in soil and rotting wood, with little exception, always tread thewalls of cells in a special way and often, besides compacting and polishing, cover walls with a fixingsubstance and even build them.

As will be substantiated below, the protobee, contrary to the opinion of Malyshev (1913, 1959,1966) and Michener (1964), for protection of food from contamination by soil should compact andpolish walls of cells. This biologic peculiarity of the protobee besides the predominately logicalsubstantiation offered here has also a clear morphologic evidence in the following chain: 1) presence ofthe pygidial and metabasitibial plates in females building nests directly indicate that these bees treatwalls of their cells; 2) the presence of these plates is a plesiomorphic character in the subfam. Apoidca;

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3) therefore, the protobee as the closest common ancestor of the superfamily treated walls of cells. Letus consider in greater detail fonnulated parts of evidence.

Functions of the pygidial and metabasitibial plates. In a typical case the pygidial plate of thefemale is a flat. triangularly or trapezoidally elevated part in the middle of the posterior part of tergiteVI; it often occupies almost its entire postglandular area, for example, in Andrena and Anthrophora, oronly its posterior 1/3 as in Halictini. Often it is restricted laterally and extended posteriorly. Thesurface of the pygidial plate usually is effaced. but usually with shagreened, granulose, or striated, etc.,sculpruration. The metabasitibial plate is a flat elevated oval or renifonn area on the posterior surfaceof the proximal end of the hindtibia. The bee compacts walls of the cell with its pygidial plate, pushingthem with its forelegs bent at the articulations, using its metabasitibial plates, and thus preserving setaeof the scopae on hindtibia from damage. Such functions of the plates are confinned by numerous directobservations (see, e.g., Batra, 1964, 1968, 1970, 1984; Stockhammer, 1966; Roberts, 1969; Rozen,1986) and also very distinct correlation between the presence of the pygidial and metabasitibial platesin females of bees with mechanical treatment (compacting and polishing) of walls of cell for theoffspring.

Bees possessing plates. These plates are present in all species of the following biologic groups.

1. Soil-nesting bees that compact and smooth walls of cells. This group includes most species ofbees, many Colletidae (except Xeromelissinae, species of Colletes, and several Hylaeinae), allAndrenidae, Halictidae, Oxaeidae, Stenotritidae, Melittidae (except Hesperapis trochanterata; Rozen,1987; Snelling, 1987), Ctenoplectrini, Anthrophorini. and some Xylocopinae (particularly species ofProxylocopa).

2. Soil-nesting bees that build additional walls of cells made of particles of the same soil and,naturally, compact and polish the inner swface of cells. Additional walls of cells in the soil are madeby some bees of various families, almost all augochlorine Halicitidae; Proxylocopa, Centridini andsome other anthophorids of the tribes Anthophorini and Exomalopsini; probably also several species ofother taxa, in which cells have cemented walls, particularly Stenotridiidae and Melitta.

3. Bees building nests in soft rotting wood. Such species include some Halictini and part ofAugochlorini. They all build additional walls of cells using the same substrate.

4. Bees of the genus Ctenoplectra (Ctenoplectrini) and at least some species of Tetrapedia(Tetrapedini, Anthophoridae), which in tunnels of xylophagous species build cells using soil, whichthey bring packed on their legs.

5. Bees building in cells made of sawdust in \vood that is rotting, but still retains its grain. Theseinclude all species of the genus Clisodon of the tribe Anthophorini and SOIne representatives of thetribe Tapinotaspini, particularly Paratetrapedia gigantea (Rozen, 1984b). In members of this groupand also in Proxylocopa and some Ancylocelis of the 2nd group, the pygidial plate of females is narrowand extends posteriorly in the fonn of a spine. This is in good agreement with data on Sphecidae, inwhich species excavating their nests in the soil usually have a broad pygidial plate, and species nestingin branches or in Scirpus sp. have a narrow one (Bohart and Menke, 1976, p. 388).

The pygidial plate transfonned into a spine is present also in cleptoparasitic bees of the familiesHalictidae and Anthophoridae, in other words only in those families whose members possess this plate.In fctnales of some cleptoparasites, for example, Echthraclictus and Paralictus of the subfamilyHalictinae (see Michener, 1978) metabasitibial plates only partly reduced are also retained. Females ofcleptoparasitic anthophorines use the pygidial plate for breaking walls of cells of the host for the

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purpose laying their own eggs in them, and in the cleptoparasitic halictids it obviously serves for thepreparation of lids for the cells they occupy. It is interesting that cleptoparasitic Megachilidae (as wellas nest-building species of this family without the pygidial plate; see below) puncture walls of cells oftheir hosts in a similar way using the acute process on stemite VI and often on tergite VI.

Taxa of five biologic groups listed above completely exhaust the checklist of bees the females ofwhich treat (compact and polish) walls of cells mechanically or build them by using the same materialas the surrounding substrate (except Ctenoplecta and Tetrapedia).

Bees which do not have plates. The pygidial and metabasitibial plates are absent in females ofall nest-building bees not included in the 5 groups cited above. These bees, including Megachilinaeand Apidae, which switched to the mandibulary method of building cells, may also be divided into 6biologic groups.

1. Bees building cells out of materials brought from elsewhere and used in preexisting cavities orin the soil (most Megachilinae and some Euglossini) or building their nests in the open (mostMegachilinae of the genus Cha/icodoma, Anthidiellum, some Anthocopa, Osmia, etc., and also manyEuglossini).

2. Bees building cells of wax (Apidae, except Euglossini and Meliponini).

3. Bees constructing nests in preexisting cavities or in soft stems of plants and making cells oftough cellophane-like film (Xeromelissinae, many Hylaeinae and some Colletes; also see number 6below).

4. Bees building nests in hollow stems, stems with soft core or other tubular and in cracklikecavities in various substrates where walls of the cavity serve directly as walls of their cells. This groupalso includes Megachilinae of various genera that do not build walls of cells and are satisfied with sizeof the preexisting cavity and its protecting properties. They (Allopidini and some other Xylocopinae)build only walls separating adjacent cells.

5. Bees eating out nests in dead, but still hard wood. Such behavior is characteristic of both"carpenter bees" (most Xylocopini) and Megachilidae of the subfamily Lithurginae. Females ofXylocopini in the process of eating out tunnels and cells support themselves by pushing walls withtheir hindtibia, on outer sides of which robust spurs are present and found only in these bees. Femalesof Lithurginae push walls with articulations of hindlegs, where at the site of the metabasitibial platesshell-like processes are present.

6. Bees excavating their nests in the soil, but not polishing walls of cells [most Colletini,Hesperapis trochanterata (Melittidae) and all Fideliinae and Pararhophitini]. This group is especiallyinteresting for the following reasons. First, it emphasizes the strict correlation between the presence ofthe pygidial and metabasitibial plates with the mechanical treatment of walls of cells, not simply withmaking nests in the soil or in rotten wood. Second, it proves that these plates can be relatively easilyreduced during transition to the new method of making nests in preexisting cavities, free cells madeout of material transported from outside or made out of secreted material or making nests in the newsubstrate such as hard wood, and they also can be reduced during nesting in the soil when the obviousneed for them is eliminated. Third, the absence of compacting and polishing of walls of cells built inthe soil, as should be expected, appears possible only with the presence of any alternative methods ofprotection of food from contanlination by soil particles, fixation of walls in the sand by nectar(Pararhophitini), placing the egg inside the bread (Fideliinae) or making tough ccllophanelike liningfrom secreted substances (Colletini).

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Therefore. all bees mechanically treating walls of cells do it by using the pygidial and themetabasitibial plates. The mandibular method of building of Megachilinae and Apidae appeared as aresult of the transition to building nests out of materials transported from elsewhere or secreted inpreexisting cavities and is apparently a specialized method. Quite the opposite, in all species that fordifferent reasons do not compact walls of cells these plates are absent.

The presence of plates is a plesiomorphic character. The presence of both the pygidial andmetabasitibial plates was directly recorded by Michener (1944, p. 229) as a plesiomorphic character inbees. Since that time no one has doubted this interpretation. Distribution of the character Hpresence­absence of plates" among taxa of bees described above supports it. Their reduction is explained bysuccessful transition to one of the advanced types of nesting each time. The opposite understanding ofthe presence of the plates as an apomorphic character should inevitably make unrealistic the hypothesisconcerning their multiple and independent origin in different taxa of bees. The pygidial plate mostlikely was already present in the wasplike ancestor of bees. It appeared in the major branch ofSphecidae after the separation of generalized Ampulicinae and Sphecinae (Bohart and Menke, 1976, p.30, Fig. 7) and remains in the great majority of species of all remaining subfamilies. A similar viewwas published by Lomholdt (1982). The metabasitibial plates are absent in wasps. Their function,pushing to walls of tunnels and cells during excavating and compacting, is performed by processes onthe distal end of the hindfemora, which are present in Bonthynostethini, Scaphentini, Cercerini,Odontosphecini, Entomosericinae. Alyssonini, and Tachytes (Bohart and Menke, 1976), andlor byspines on hindtibia known in many other Sphecidae. The metabasitibial plate appeared in the processof formation of the protobee in association with the need to provide support for the hindlegs and avoiddamaging the scopae of setae, that had developed on them. '

Therefore, the protobee as the closest common ancestor of bees by definition represent ahypothetic species characterized by the set of all plesiomorphic characters among bees. It had pygidialand metabasitibial plates. The presence of these plates in bees is rigidly correlated with the mechanicaltreatment of walls of cells. Therefore, the protobee, contrary to the opinion of Michener (1964) andsome other authors, compacted and polished walls of cells. It is necessary to note that pygidial andmetabasitibial plates relatively easily become lost in bees that for various reasons ceased to compactand polish walls of cells. This is true of some large taxa of bees. for example, Nlegachilidae andApidae discussed above, and individual species of groups in which the typical method of constructionof cells includes mechanical treatment of their walls (see Hesperapis trochanterata in Melittidae;Rozen, 1987; Snelling, 1987).

4. NESTING IN SOIL AND ROLE OF MANDIBLES

Rejection of the idea that the protobee was similar to modem Hylaeinae-bees without scopaeand making their nests chiefly in preexisting cavities (usually in hollow stems of plants or stems withsoft pulp)-eliminates the corresponding argumentation about the substrate of nesting of the protobeeas it was formulated by Malyshev (1966, pp. 300-301; see above). The protobee made its nests in thesoil, which directly or indirectly was noted by most authors (including the discussion of the structureof the primordial nest; see the special paragraph below). Almost all bees with Hshort proboscis" nowexcavate their nests in the soil. Most Hylaeinae and individual species of some other groups areexceptions.

Another iInportant argument in favor of soil as a substrate for nesting of the protobee emergesfrom the establishment in the preceding section that the protobee possessed pygidial and metabasitibialplates, and that therefore it compacted and polished walls of cclls. The great majority of species ofmodern bees equipped with these plates live either in soil or in rotting wood. The rottcn wood cannot

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be recognized as an original substrate for making nests by bees because, fust, it is considerably lesscommon, and of course was also rarer during the Cretaceous than soil; second, very few groups couldswitch to nesting in rotten wood (Augochlorini and Clidoson) and few individual species of bees of thetribes Halictini and Tapinotaspini; third, all nests constructed by bees in rotten wood belong to suchadvanced types as the linear, linear-branching, and chamber; and fourth, finally, almost all species ofbees constructing nests in rotten wood, except species of Agapostemon, make specialized cells withbuilt-in walls made out of sawdust, which are coated above with secretory material.

There is every reason to suppose that soil was the substrate also for nesting <;>f the wasplikeancestor of bees. Probably even before the emergence of the protobee this ancestor already usedmandibles for excavating. All bees that construct their nests in the soil move it with their mandibles.which is confinned by direct observations (Batra, 1964, 1966; etc.) and by the flattened mandibles ofbees (Michener and Fraser, 1978). In any case, with the appearance of the scopae on hindlegs theprotobee already could use them for excavating, as is done by most sphecoid wasps.

5. COCOON SPINNING

Mature larvae of both the protobee and the wasplike ancestor spun cocoons, in which theypupated. This statement is supported by the following arguments discussed below: I) larva of theprotobee possessed a developed spinning apparatus, 2) unlikely multiple independent appearance ofthe cocoon in different taxa of bees.

The developed spinning apparatus. The strongest argument is the morphologic one (see sec­tion 1 above). Michener (1953, p. 1000) noted that larvae of those bee larvae that spin cocoons havelarger antennal papillae and large transversely situated of salivaria. McGinley (1981, p. 21, 127) addedprotruding labiomaxillary area, well developed lips of the salivaria, and carinae on the head(hypostomal and pleurostomal carinae) to the checklist of larval characters closely associated with thespinning of cocoons.

Known cases of violations of this correlation are rather rare, except the presence of developedstructures in some cleptoparasitic Anthophorinae which do not spin cocoons and are more likelyexceptions. Thus, among taxa of bees the larvae of which do not spin cocoons, the labiomaxillary areais prominent in larvae of Colletidae of subfamilies Hylaeinae and Xeromelissinae and Anthophoridaeof tribes Ceratinini and Xylocopini. In the last tribe, the developed antennal papilla is retained as well.The opening of the salivarium is large and transverse in larvae of Colletini, Stenotritidae, Melittidae ofthe subfam. Dasypodinae, and Halictidae of the tribe Augochlorini. And, vice versa, in individual taxawhose larvae spin cocoons some structures functionally associated with such activity became reduced;the antennal papilla is poorly developed in larvae of Megachilidae of the subfam. Lithurginae and ofthe genus Hoplitis (in this genus as well, the labiomaxillary area is depressed). Anthophoridae of tribesEucerini and Centridinini and bumblebees; labia of the salivarium are strongly reduced and thelabiomaxillary area is depressed in larvae of Colletidae of the tribe Paracolletini; finally, in larvae ofColletidae of the tribe Vaupolicanini the opening of the salivarium is round.

McGinley (1981, pp. 132-136, see characters 20, 24, 30, 61, 77 and 79) simply identified allcharacters functionally associated with cocoon spinning by the larval bee as plesiomorphic in bees.Therefore, larva of the protobee as the closest common ancestor of bees possessed strongly developedspinning apparatus.

Pattern of distribution of character "cocoon present vs. cocoon absent." Frequent occurrenceof cocoons in various taxa of bees is also an important argument supporting the idea that the protobeespun a cocoon.

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Besides Andrenidae and the small families Stenotritidae and Oxaeidae, larvae of all species orsome groups of all remaining families of bees, including generalized families, spin cocoons:Colletidae, Diphaglossinae and Paracolletini;Halictidae, Rophitinae; Melittidae, all exceptDasypodinae, if we do not consider the covering of all walls of cells with secretory substance ofunknown origin by larvae of some Heseprapis, for example, H. larreae, as a cocoon (Rozen andMcGinley, 1991); Megachilidae, all; Anthophoridae, Prarhophitini, Ctenoplectrini, Euderini,Emphorini, Centridinini, Exomalopsini, and Tapinotaspini; and Apidae, all families spin cocoons,

If we accept the opposite point of view that the larva of the protobee did not spin a cocoon, aswas considered by Michener (1964), then for the explanation of the pattern of distribution of the"cocoon present vs. cocoon absent" character among taxa of bees it is necessary to propose theabsolutely unrealistic hypothesis that such a complex structure as a cocoon appeared in bees indepen­dently no fewer than 10 times and each time the same morphologic peculiarities of larva appeared andeach time secretion of salivary glands was used as material for making a cocoon.

6. THE PROBLEM OF SECRETORY LINING INSIDE CELLS

Structure of the glossae As was mentioned above (Section 1), contemporary investigations ofthe glossa of bees (McGinley, 1980; Michener, 1981; Michener and Brooks, 1984) led to the conclu­sion concerning its advanced structure in the family Colletidae and, therefore, to the rejection of thefonnerly dominant idea of the generalized nature of this family. Major arguments in favor of secondaryorigin of the short and doubled glossa of Colletidae are as follows:

1) Presence of long, acute glossa in males of genera Palaeorhiza and A1eroglossa of the subfam.Hylaeinae (Perkins, 1912; Popov, 1939; McGinley, 1980; Michener and Brooks, 1984), which issimply interpreted as preservation in them of the ancestral state' of the character, the apomorphic stateof which has adaptive functional meaning only in females (see paragraph 3 below).

2) The superficial character of similarity of the glossa of Colletidae and those sphecoid wasps inwhich it is short and broad; according to Iuga (1989), the glossa of contemporary wasps is so simpli­fied by reductions that it cannot be considered as original for the development of the glossa in bees.

3) Highly specialized and complex structure of the glossa in Colletidae with many accessorystructures (Michener and Brooks, 1984) and its obvious adaptation for placing secretory substances(products of the Dufour's gland and/or salivary glands) on inner walls for obtaining cellophanelikelining.

Recognition of the advanced character of the glossa in Colletidae combined with the reliableinterpretation of the functional meaning of peculiarities of its strucrure inevitably leads to the conclu­sion recently made by Torchio et a1. (1988) that the secretory lining of Colletidae is not aplesiomorphic character of bees. Therefore, flfSt, the protobee could not make cellophanelike secretorylining in cells because it had a generalized, narrow and pointed glossa, and, second, the similarity ofthe biology of Colletidae and wasps of the subfamily Pemphredonidae, which also make similarsecretory lining, is a secondary trait.

Negative correlation of the lining and the cocoon. In the preceding subdivision it \vas shownthat cells of the protobee did not have a cellophanelike lining similar to that made by contemporaryColletidae. At the same time among other bees linings of different kinds are known: silklike, as ifpolished, waxlike, etc. Their creation does not require use of glossa of the colletid type. In our view theprotobee not only did not make a cellophanelike lining, but it also did not make a lining of any otherkind of secreted substances or substances brought from elsewhere, for example, vegetable oils. Lining

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of cells appeared independently in different taxa of bees. The major arguments in favor of this view,although indirect, are convincing: 1) the negative correlation of the lining and cocoon, 2) differentcomposition. sources, and methods of making the lining. The second argument is considered in thefollowing subsection.

Among all bee taxa cited in subsection 5, the larvae of which spin cocoons, the secretory liningof cells was recorded only in Diphaglossinae, Paracolletini, .Melitta (lining of unclear origin was alsodescribed in Melittidae of the subfam. Meganomiinae), Eucerini, many Exomalopsini andTapinotaspini, and some species of Emphorini. Cases in which both cocoon and lining are absent areeven rarer; this is observed in Dasypodinae and also in some Panurginae (in which secondary loss ofthe lining most likely took place; see Rozen, 1967) and in most Xylocopinae, except those that buildnests in the soil. In the great majority of bees a strict alternative is observed: larvae either spin acocoon or their mother makes a secretory lining in the cells.

To explain the recorded negative correlation between the presence of the cocoon and presence ofthe lining, it is possible to propose two causes which are not mutually exclusive. First, the lining andthe cocoon perfonn in many respects similar protective functions and therefore the spinning of thecocoon with available lining of cells would be excessive. Second, salivary glands, secretion of whichserves as a major material for the spinning of the cocoon by larvae and is usually also used in thecomposition of the lining inside cells prepared by females, probably can function only at one of thephases of ontogenesis of bees, in mature larva or in imago. The latter explanation in vague fonn wasproposed by Michener (1964, p. 230) at a time when the composition of the secretion of various glandsand their participation in the substance of the cocoon and lining was little understood. However, it alsodoes not lose its importance now. Recognition of the negative correlation between spinning of thecocoon and making lining inside cells combined with the statement, substantiated in subsection 5, thatlarva of the protobee certainly spun a cocoon provides an important argument against the idea that theprotobee coated cells.

Composition, sources, and methods of making of lining. Many' bees produce secretory liningof cell walls. It is believed that in most investigated groups the secretory lining is created from asubstance produced by the Dufour's gland. It seems that this would be a good argwnent supporting thepresence of the secretory lining in cells of the protobee. Moreover, the transition from the wasplikeancestor of bees to the collection and storage of pollen food with, on one hand. high hygroscopicproperties and, on the other hand, easily desiccating and thus not suitable for feeding larvae, should befavored for the ability to make waterproof lining of cell walls.

Abundant data on differences in the chemical composition, sources, and methods of making thelining speak against the hypothesis that the protobee lined walls of cells. Most of these data wereobtained during the last 10 years. These data give reason to suppose that the lining of cells appearedmany times and independently in many different taxa of bees. Such an opinion has already beenexpressed by some authors (e.g., Hefetz, 1987).

First, great diversity of the chemical compounds of which the secretory lining of cell walls ofbees is made was recorded. Thus, short-tongued bees are divided into two groups by the chemicalcomposition of the secretion produced by the Dufour's gland (Crane, 1983a): "lactone bees"(Colletidae, Oxaeidae, Nomiinae, and Halictinae) and "ketone-carbon bees" (Andrenidae, Melittidac,and Rophitinae). Among long-proboscis bees in Anthophorini Dufour's glands produce triglycerids(Norden et aI., 1980), which are absent in most other bees. They were found only in Megachilinac,particularly in species of Megachile (see Cane and Carlson, 1984), including in Eucerini andCentridinini (Herfetz, 1987) related to them. A certain importance in the argumentation of the second-

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ary origin of the secretory lining of cells in bees may also be given to daiJ en dissimilarity of thecomposition of secretions of Dufour's gland in different bees and sphecoid wasps. Thus, according toCrane (1983b), substances secreted by the Dufour's gland of bees are absent in sphecoid wasps, whichmeans they were synthesized by bees de novo.

Second. in different taxa of bees secretions of different glands or their mixtures and also veg­etable oils are used for lining of cell walls.

It is essential that the origin of the lining of cells in most species is established only by thesimilarity of its chemical composition to the substances produced by the Dufour's gland. At the sametime in some species it can be considered already proven that the lining actually is completely madeout of secretion of labial glands (in Hylaeus: Torchio, 1984) or their secretion is added to the composi­tion of the lining but is not identified separately (in Colletes; Torchio et aI., 1988). In Panurginuspotenrillae lining of cells does not contain -substances directly discharged by Dufour's gland, althoughthey were found as additives in the composition of the food for larvae (Duffield et al., 1983). Theauthors of the study suppose that in this species either the secretion of Dufour's gland is transfonnedafter it is placed on walls of cells, or the substance of the lining is produced by another gland. Otherinteresting cases were also recorded. Thus, in Chalicodoma sicula, which as in many otherMegachilidae, does not coat cells with secretion, labial glands discharge substances (hydrocarbons)similar to the Dufour's gland secretion in the andrenid species Calliopsis andrenlformis, which it usesfor lin tng walls of cells (Kronenberg and Hefetz, 1984).

All these facts show that on one hand the secretion of Dufour's gland by its chemical composi­tion may often be similar to secretions produced by other glands, and on the other hand secretionproduced by other glands for the lining of cells by bees of various taxa may be used considerably moreoften than is supposed at present. The multifunctionality of Dufour's glands and absence of rigidcorrelation benveen its development and the presence of the lining concern the same matter.

For example, it is reduced in Hylaeus (Crane, '1983a) which make a lining, and well developed infemales of Rophitinae, which do not coat their cells with anything, and the Dufour's gland secretion isadded in the food for larvae, for example, in Dufourea novaeangliae (Eickworth et al., 1986). Use ofthis secretion as an additive to the food of larvae was also recorded in many other groups of bees.Probably the major purpose of such additives is not only increase of the nutritional value of the foodbut also the protection of the pollen from fungi and also possibly prevention of its germination.

Finally, some bees, particularly Macropis nuda (Cane et al., 1983), coat cells with vegetable oil,which in appearance and chemical composition is similar to the Dufour's gland secretion of some bees.It is very likely that using oil for lining is also characteristic of several other groups, primarily ofCtenoplectrinida; the composition of the lining in these bees has not been investigated, but it is knownthat they collect vegetable oil.

Third, bees of various taxa use different parts and structures of the body to place the secretionlining on cell walls, for example, Colletidae use the glossa, which in them for this reason is broad anddoubled, Halictidae use a brush on the apex of the metabasitarsus, and Anthophora uses the flabellum.Such a diversity of nleans also directly indicates that the lining of cells as a biologic character appearedmany times and independently in different taxa of bees in the process of their evolution after thedifferentiation of immediate offspring of the protobee, which did not possess this character.

7. FOOD FOR LARVAE IN FORM OF BREAD

Basic arguments. In the light of recent data and statements proven above on the morphology

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and biology of the protobee there is every reason to suppose that the protobee collected and stored notliquid (or semiliqufd) food as was believed until now, but a pastrylike bread of various physicalcondition. The following arguments support this statement: 1) the presence of scopae in the protobee,2) the absence of tough lining in cells made by the protobee, including the cellophanelike lining, 3)preparation of larval food in fonn of bread by the great majority of bees belonging to somewhatgeneralized taxa, 4) correlat~on of the preparation of larval food in another fonn, liquid, semiliquid, orpiled-up pollen with various bionomics and ethologic specialization, 5) agreement with understandingof the transition of the larvai feeding of the wasplike ancestor of bees from animal to plant food.

Such morphologic evidence as the correlation of apomorphic states among bees of some larvalcharacters precise.ly with feeding on a liquid fonn of food would be essential. Michener (1953, p.1001) noted that in such larvae mandibles are usually reduced and weakened apically and void of cuspson the inner surface. McGinley (1980, pp. 133-134) simply indicated the direction of evolution of theselarval characters in bees: the apex of the mandible changed from acute to obliquely truncated, and themandibular cusp changed from well or moderately developed to weakly developed. Nevertheless, thepanern of distribution of these characters among taxa of bees offered by McGinley (1980, pp. 185,195, 205, and 212, characters 47 and 52) does not give reason for the sufficiently clear correlation or atleast correlation of their apomorphic states with the feeding of larvae on relatively liquid food, evenincluding semiliquid food.

This problem is probably created by the fact that possible morphologic changes associated withtransition to feeding on liquid food should be displayed mainly in young larvae. Larvae of beescollecting and storing liquid food always start eating it from the top and the pollen sinks to the bottom.Besides, despite the lining of the cell walls, with time the food may desiccate. Therefore, during lateinstars these larvae get only the hard remains of the food lin1e different from the food of larvae, thatfrom the start received pastrylike bread food or pollen stored in a pile. Unfortunately, availabledescriptions of larval structure and comparative analysis of their morphology refer usually to larvae ofthe last instar (prepupa).

Let us consider the arguments cited in sections numbered I through 5 in greater detail. Thestatements proven above constitute the fITst two arguments. According to them and contrary to theopinion of most authors who have expressed a view on the origin of bees (listed in section 1), theprotobee, first, possessed scopae and therefore could collect dry food for its larvae, and, second, it didnot make a secretory lining of cells and therefore could not store liquid larval food.

Collecting and storage of liquid food or pollen piles. The hard state of larval food of theprotobee is simply indicated by the common occurrence of it among contemporary bees and especiallyamong generalized taxa in which it is prepared in fonn of bread. Storage of somewhat liquid(honeylike or semiliquid) food, in other words food in which not pollen but nectar is predominant,most likely is an exception. Such food is eaten by larvae of most Colletidae (except someParacolletini), investigated representatives of the small family Oxaeidae, and some groups from otherfamilies: Me/ilta (semiliquid food), many Anthidiini (semi liquid food), most Centridinini,Anthophorini, and all Eucerini, as well as most Apidae (except many species of Bombus). ManyApidae store nectar (honey) and pollen separately.

Storage of liquid food requires special adaptations and suitable construction of the nest and cell.First, a waterproof lining of cells, which is made by most bees cited above, is required. Such a lining ismade out of substances secreted by Dufour's gland and/or labial glands, rarely out of resin (Euglossini)or out of wax fonned by intersegmental, tergal, and/or sternal glands (remaining Apidac; Meliponiniadd resin to their wax). In many Anthophorini and Centridini the larval food has a son1cwhat more

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liquid state rather than semiliquid or honeylike. To store such food, bees are forced to coat not only the:walls and bottom of cells but also the lid. Second, to prevent spilling of the liquid food cells should besituated vertically or at least tilted; such cells are built by most bees that store liquid and semiliquidfood. Third, the liquid food requires special means to prevent its contamination by soil and litter. Thisis achieved by different methods.

Thus, all species (except Colletidae) that build nests in the soil and store relatively liquid foodfor the offspring polish and compact not only the walls of the cells but also walls of tunnels of the nest.Many of them also construct tunnels leading directly to cells arcuately elevated (for example, moststudied representatives of the tribe Eucerini; Radchenko, 1984) or, vice versa, curved upwardly so thatcells appear to be higher than the basal part of the lateral tunnels leading to them (foi example, inMetapsaenithia abdominalis: Rozen, 1989), or at least have a part of the major tunnel horizontal (e.g.,in Anthophora caucasica: Radchenko, 1986).

Representatives of Colletidae collecting and storing semiliquid food build their nests in the soiland usually do not compact the tunnel walls. However, some of them, for example, Colletesciliatoides, C. cunicularis, C. fodiens, and Hylaeus variegatus, build "doors" of cells serving as anobstacle for penetrating of litter into the cell (Radchenko, 1988). Among other Colletidae, the SouthAmerican species Caupolicana albiventris, C. gaullei (Janvier, 1933, 1955), Ptiloglossa guinnae (Rob­erts, 1971) and P. arizonensis (Rozen, 1984a) make arcutely elevated tunnels similar to those ofEucerini.

Unrelated taxa in which species collect and store liquid food and also the diversity of methods ofits storage and preservation from contamination indicate the independent transition to liquid food bylarvae in different groups of bees. There are no doubts that storage of pollen in piles also developed indifferent groups of bees secondarily and independently. Such a method not associated with the prepa­ration of bread (usually of strictly definite shape) is used by almost all Megachilinae (probably exceptOsmia arequipenis: Janvier, 1955; and O. jlavicornis: Marikovskaya, 1968), Lithurginae and followingtribes of Anthophoridae, Parahophitini, Ctenoplectrini also make their nests, some Exomalopsini andTapinotaspini also make their nests of materials brought from elsewhere.

Another type of food different from bread is the shapeless or poorly shaped pollen mass (some­times with considerable admixture of nectar) prepared to feed several larvae simultaneously. SomeMegachilidae, Fideliinae, Lithurge, and Metallinella brevicornis shifted independently to this type offood.

On transition to feeding on plant food. This is the final argument. In our view, penetration ofthe pollen into cells of the wasplike ancestor was caused by collecting small insects from flowerssmeared with pollen. Further adaptation of larvae, including development of new enzymes, to processthe pollen instead of the animal food, on one hand, and development of pubescence on the body ofimagines of the ancestor of bees, on the other hand, allowed it to switch to the collection of pollen, thatfrom the very beginning was performed by using the scopae. This hypothetical means of transition offeeding of larvae of the wasp ancestor of bees from animal food to plant food therefore rejects not onlythe primary transportation of pollen in the crop but also the storage of liquid food associated with this.In any case, the ancestor of bees during transition from animal to plant food should somehow compen­sate the demand of its larvae for fat and particularly for protein, the only source of essentialaminoacids, which are absent or present in too small amount in the nectar. Therefore, pollen containingall these substances should constitute a considerable part of the larval food of primitive bees.

We will also note that larvae of the protobee evidently possessed high mobility and high speed of

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food consumption, which also saved the food from spoilage. This is exactly what larvae of modembees do, storing somewhat dry pollen and not having secretory lining on cell walls.

8. STRUCTURE OF THE NEST

General plan of structure. There are two views on the architecture plan of the primary bee nest.On one hand, according to Michener and colleagues (Michener and Lange, 1957; Sakagami andMichener, 1962; Michener, 1964) such a nest consisted of a major entrance leading into the soil and,originating from its lower end, branches having one cell each. Primary nature of such a nest wasassociated with the fact that it is widely distributed in sphecoid wasps and among bees it occurs inrepresentatives of those that were considered as morphologically primitive. Such an opinion, however,seems insufficiently substantiated, because nests of the type described above are very rare and, in anycase, among bees have been found only in Pasiphae tristis (Colletidae), some species of Andrena, andoccasional Anthophoridae.

Several researchers (Verhoeff, 1892; Gutbir, 1916; Molchanov and Kuz'min, 1985) consider theprimary nest as unicellular. In our view it is unlikely that the protobee built nests with one cell becauseit would be the most laborious to construct. In this case construction of the cell is preceded by steps ofsearch for a place to construct the nest. After the completion of all work on its construction, filling withfood, ovipositing, and sealing the lid, the bee must fill the branch and the major tunnel of the nest withsoil in order to protect its offspring from possible intrusion by enemies into the cell. In the process ofconstruction of a multicellular nest, building of each following cell at most is associated only withpreparation of the lateral tunnel. Among excavating bees, unicellular nests usually occur only whenthey settle in loose sandy soil, where usually the probability of destruction of cells mechanically isvery high. All species in which unicellular nests are known construct multicellular nests in compactedsoils.

In our view construction by the protobee of a branching nest with lateral tunnels at differentlevels originating from the major tunnel was most probable. This type of nest actually occurs mostfrequently among wasps and lower bees with a shon tongue: in most Colletidae, Stenotritidae.Oxaeidae, Melinidae, Rophitinae, many Andrenidae, some Halictinae and Nomiinae. It is also typicalof many higher bees that build their nests in soil. Different types of nests--linear, linear-branching,with sessile cells, chambered, and with free cells--are more specialized, which is not disputed also byother authors. However, it contradicts their ideas that the ancestor of bees is a Hylaeus-like insect (partI), because most Hylaeinae usually build only linear nests.

Situation of nests and presence of lids on them. '\s it may be understood from works ofMichener and his colleagues (Michener and Lange, 1957; Sakagami and Michener, 1962; Michener,1964), they suppose that the primary orientation of cells in nests of bees was horizontal. In any caseSakagami and Michener (1962) considered the horizontal orientation of bilateral symmetrical cells as aprimary one and further (Michener (1964) proposed that the radial-symmetric cells, including venicalcells of representatives of Colletidae, originated from bilateral-symmetric cells.

This view of Michener again contradicts his understanding of primary collection and storage ofliquid food, which as was noted by Gutbir (1916) should be inevitably associated with the verticalorientation of cells. We should also note that the major argument of Michener (1964) in favor of theprimary horizontal orientation of cells, the flattened bottom of cells in Andrenidae and Halictidae, isalso insufficient. Actually among these bees there are species building cells with a flatter upper side.

Generally we also consider that cells in the nest of the protobee were situated horizontally. The

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more specialized character of vertical or strongly tilted cells associated with storage of liquid larvalfood support such a proposition. Besides, storage of pollen in horizontally situated cells does notrequire the structural or behavioral adaptations associated with obligatory maintenance of purity offood.

In our view the protobee sealed cells with a lid made out of soil particles. Lids of cells are madeby almosr all species of bees excavating nests in the soil, except several specialized cases mainlyassociated with development of social life, particularly in Halictinae (see review of Radchenko, 1993).

LITERATURE CITED

ALEXANDER, V. A. 1992. An exploratory analysis of cladistic relationships within the superfamilyApoidea, with special reference to sphecid wasps (Hymenoptera). 1. Hymenoptera Res. I ( I): 25­61.

BATRA, S. W. T. 1964. Behavior of the social bee, Lasioglossum zephynJm, within the nest (Hy­menoptera, Halictidae). Insectes Soc. 11(2): 159-186.

BATRA, S. W. T. 1966. The life cycle and behavior of the primitively social bee, Lasioglossumzephyrom (Halictinae). Univ. Kansas Sci. Bull. 46(10): 359-423.

BATRA, S. W. T. 1968. Behavior of some social and solitary halictine bees within their nests: acomparative study (Hymenoptera: Halictidae). 1. Kansas. Entomol. Soc. 41(1): 120-133.

BATRA, S. W. T. 1970. Behavior of the alkali bee, Nomia melanderi, within their nests: a comparativestudy (Hymenoptera: Halictidae). Ann. EntomoI. Soc. Amer. 63(2): 400-406.

BATRA, S. W. T. 1980. Ecology, behavior, pheromones, parasites and management of the sympatricvernal bees Cofletes inaequalis, C. thoracicus, and C. validus. J. Kansas Entomol. Soc. 53(3):509-538.

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Corrections to English translation of the paper by Radchenko and Pesenko (1996)

Page Line Written Correct

142 7th from spurs on legs spines on legsbottom

144 11th from coat insides of cells line insides of cellstop

147 5th from postglandular area [of tergum] postgradular areatop

rnany times the closest common ancestor the nearest common ancestor" setae hairs" doubled glossa [of Colletidae] bilobed glossa" [cell] lid cap, plug" [larval] food provisions" [pollen, food] bread ball" vegetable oil plant oil