AMERICAN MUSEUM Novitates PUBLISHED BY THE AMERICAN MUSEUM OF NATURAL HISTORY CENTRAL PARK WEST AT 79TH STREET, NEW YORK, N.Y. 10024 Number 2962, 27 pp., 16 figs., 3 tables November 30, 1989

Life History Studies of the "Prinmitive" Panurgine Bees (Hymenoptera: Andrenidae: Panurginae)

JEROME G. ROZEN, JR.'

ABSTRACT

As a result of field investigations in North and in light ofinformation offered in the current paper, South America, comparative life history infor- derived from previous literature, and/or incor- mation is presented on the following genera of porated in the author's unpublished fieldnotes. panurgine bees which comprise the basal three Compansons are made with biological features of clades in the Panurginae according to Luisa Ruz: Andrena, the only genus of the Andreninae for Liphanthus, Protandrena, Pseudopanurgus, Het- which there are published accounts. Although of erosarus, Cephalurgus, Metapsaenythia, and obvious phylogenetic value, biological data con- Psaenythia. Subjects include ecology of nesting cerning the Panurginae are still too limited and sites, nest architecture and dimensions, provision- poorly understood to permit an analysis at this ing, development, larval behavior, mating behav- time. Furthermore, too few taxa have been ob- ior, voltinism, diapausing, food sources, diurnal served and outgroup comparisons are limited to and seasonal phenology, and nest cleptoparasites. Andrena. The diverse biological attributes of the Panur- A formal synoptic overview of the biological ginae that are potentially useful for phylogenetic features of the Andrenidae is presented. analysis are summarized, discussed, and evaluated INTRODUCTION I have been compiling life history infor- many of the genera for which I have notes mation on the large andrenid subfamily Pan- belong to the basal three clades in the urginae for many years. The recent study by subfamily, it seems convenient to present this Ruz (1987) presented a classification of the information here. Integrated with these new genera of these bees based on a careful anal- data are previous literature accounts on the ysis of the anatomy of the adults. Because life histories of the assemblage. Immature ' Curator, Department of Entomology, American Museum of Natural History. Copyright © American Museum of Natural History 1989 ISSN 0003-0082 / Price $3.30 2 AMERICAN MUSEUM NOVITATES NO. 2962

Liphanthus as the sister group of all other Panurginae, Protandrena as the sister group ofthe remaining Panurginae, and the assem- 4-.1 blage Pseudopanurgus to Psaenythia (as listed in table 1) the sister group for all Panurginae except forLiphanthus and Protandrena. These genera occur only in the New World. Be- longing to the basal clades of the subfamily does not, of course, necessarily mean that these genera are plesiomorphic. However, Ruz's study demonstrated that these genera, in fact, exhibit fewer adult apomorphies than the remaining genera, as also seems to be true with respect to the biological features dis- cussed here. For convenience I refer to these genera as the "primitive" panurgines. I follow the generic nomenclature used by Ruz (1987) with two exceptions: She com- bined Calliopsis (and its four subgenera), No- Fig. 1. Simplified cladogram of the bee family madopsis (and its three subgenera), Hypo- Andrenidae, from Ruz (1987). The clade Pseu- macrotera, and Liopoeum into one genus, dopanurgus-Psaenythia includes the genera Pseu- Calliopsis. I continue to follow the more tra- dopanurgus, Pterosarus, Heterosarus, Xenopan- ditional usage ofconsidering these genera dis- urgus, * Pseudosarus, * Rhophitulus, Chaeturginus, * tinct until the interrelationships oftheir taxo- Cephalurgus, Metapsaenythia, Anthemurgus, * nomic elements (i.e., the subgenera, genera, Parapsaenythia, * Anthrenoides, * and Psaenythia. and certain troublesome subgenerically un- Asterisks indicate that no nesting biologies within assigned species) are better understood (which the genus are known. is not to say that I believe the traditional usage is more meritorious). Also, I continue stages from the field studies will be examined to recognize Poecilomelitta as distinct from systematically and treated elsewhere, as will Meliturgula because I refer to my unpub- the biologies and immatures of the more lished notes on the nesting and mating bi- highly derived panurgine genera. ology of the type species, P. flavida Friese. Data presented below were gathered not However, biological information in these only to expand our understanding of the life notes seems to support Warncke's (1985) syn- histories of the Panurginae but also to aid in onymizing ofthe two genera and Ruz's (1987) determining the phylogenetic relationships acceptance of the synonymy. within the subfamily. A phylogenetic analysis Table 2 presents the dimensions of nest of the Panurginae is not attempted here be- components, provision masses, and eggs of cause available information is still too in- the panurgines treated here. complete (too few panurgine taxa, insufficient outgroup studies, and poorly understood bi- ACKNOWLEDGMENTS ological features). Nonetheless, a discussion I gratefully acknowledge the field assis- ofcharacteristics that lend themselves to such tance of the following persons, named in as- a study is presented to direct attention to data sociation with the bee genus studied: Li- of potential value. phanthus: L. E. Pefia; Protandrena: M. Because I had to assemble biological in- Favreau; Pseudopanurgus: E. Quinter; Het- formation about the Andreninae in order to erosarus: M. Favreau, K. C. Rozen; Cephal- evaluate features ofthe Panurginae, I drafted urgus: J. S. Moure and F. C. Thompson; Me- a summary statement encompassing the bi- tapsaenythia: B. L. Rozen; Psaenythia: S. ological traits of the entire family. This pro- Laroca, J. S. Moure, and F. C. Thompson. file, obviously preliminary in nature, is of- The investigations in Brazil on Cephalur- fered at the end. gus and Psaenythia were carried out while I The genera covered in this paper are listed worked in the laboratory ofPadre J. S. Moure, in table 1. Ruz's analysis (fig. 1) recognized Departamento de Zoologia, Universidade 1989 ROZEN: "PRIMITIVE" PANURGINE BEES 3

Federal do Parana, Curitiba. Dr. P. No- TABLE 1 guiera-Neto, Sao Paulo, Brazil, provided liv- The "Primitive" Panurgine Genera Treated in This ing accommodations for my party at his plan- Paper, as Identified by Ruz's (1987) Study tation near Cosmopolis where we discovered Bibliographic references are to biologies (other than pollen preference) of the species. Rozen and excavated the nests of Cephalurgus. Se- (1967), Hurd and Linsley (1972), and Ruz and fior Luis E. Pefia G., Santiago, Chile, guided Toro (1983) provided summary accounts of some me on two expeditions to northern Chile aspects of the natural histories of these bees. where I was able to pursue the biology of many Chilean bees including Liphanthus. Taxon Biology Research on Heterosarus and Pseudopanur- Liphanthus gus was conducted while I was in residence alicahue Ehrenfeld and Rozen, at the Southwestern Research Station, near 1977; present paper Portal, Cochise Co., Arizona, administered parvulus Rozen, 1970b; present pa- by Vincent D. Roth and later by Wade C. per Sherbrooke. The studies recorded here would sabulosus Friese, 1916; Claude-Jo- have been without the seph, 1926; present pa- impossible hospitality per and assistance of these persons. Protandrena I would also like to acknowledge the co- bancrofti Chandler, 1962; present operation of Dr. Luisa Ruz and Professor paper Haroldo Toro, of the Laboratorio de Zoolo- bicolor Rozen, 1967 gia, Universidad Cat6lica de Valparaiso, verbesinae Rozen, 1970a (as Psaeny- Chile. Their keen interest in and knowledge thia bicolor) about panurgine bees aided the investiga- Pseudopanurgus tions. They identified specimens and named aethiops (Cresson) Hicks, 1931; Rozen, 1967 new involved in the their fraterculus timberlakei Rozen, 1965a, 1967, pres- species study; pub- ent paper; Hurd and lications on panurgines of Chile were a sig- Linsley, 1972 nificant source of background information verticalis Timberlake Rozen, 1967 (as sp. B) concerning the subfamily; and Dr. Ruz's the- Pterosarus sis provided a meaningful framework for the boylei (Cockerell) Rozen, 1967 report of these studies. occidus (Timberlake) Rozen, 1965a (as un- Field investigations were partly supported named Pseudopanur- by the National Science Foundation GB5407 gus), 1967 (as Pseudo- and GB32193. panurgus sp. A); Hurd This manuscript was critically reviewed by and Linsley, 1972 the following specialists: Bryan N. Danforth, perlaevis (Cockerell) Rozen, 1965a; Hurd and Linsley, 1972 Wallace E. LaBerge, Charles D. Michener, p. piercei (Crawford) Pierce, 1904; Hicks, 1936 and Luisa Ruz, to whom I extend my sincere Heterosarus thanks. nanulus present paper LIPHANTHUS Xenopanurgus Pseudosarus Claude-Joseph (1926) briefly described the Rhophitulus nest of Liphanthus sabulosus, the only pre- niger (Spinola) Janvier, 1933 (as Campto- vious account of the nesting biology of this peum nigris) genus. Friese (1916), Rozen (1970b), and Eh- Chaeturginus renfeld and Rozen (1977) identified several Cephalurgus species as hosts of the nomadine cuckoo bee anomalus present paper Kelita. Ruz and Toro (1983) summarized Metapsaenythia abdominalis present paper previous information on the life histories of Anthemurgus Liphanthus and listed the known flower pref- Parapsaenythia erences of the species. Anthrenoides Psaenythia Liphanthus (Leptophanthus) alicahue interrupta Claude-Joseph, 1926; Jan- Ruz and Toro vier, 1933 HABITAT: Approximately ten nests of Li- annulata Rozen, 1977b; present pa- phanthus alicahue were excavated along a per 4 AMERICAN MUSEUM NOVITATES NO. 2962

nearly horizontal earthen path (fig. 2) near Paipote, Atacama Province, Chile, between October 15 and 18, 1969. On October 20, IL 1971, another nesting site (fig. 3) (discovered on October 12) approximately 100 m away was excavated. The cuckoo bee Kelita tuber- - culata Ehrenfeld and Rozen (Nomadini) flew 6 IC) 1-1 abundantly over the second site and seemed to be attacking the Liphanthus nests. Kelita 04 1-1 _ larvae, however, were recovered only from one nest of an undescribed genus and species ei of intermixed with those of L E _4 eCI-- panurgine Liph- anthus. In 1971 Liphanthus was not flying at lCN its former area which had 'D I.-I Cl nesting apparently become inactive. The following discussion Cl -1 00 refers to the IN C; m00'IT ICf 1969 study unless otherwise in- O-E= dicated. CA The path in which the bees nested bordered

'Uq 11-1 00 a en plowed, irrigated field, sparsely vegetated I.-I = v- 00 with low herbs, including Melilotus. The sub- IP. surface soil was moist, even-grained, mod- erately compact, without with little I , ' . , - stones, tr) organic material, and easily excavated. The 'U pollen plant was not discovered; many males

P N V) and some females flew over the nesting Cl I =ZScd area, and males hovered around the flowers of H. o e o Csm o'e Melilotus. The 1971 population was in a bar- ren Cl C horizontal area, dry on the surface and ^ to the sun. exposed ),, o^^ NESTS: Most nest entrances were scattered = _ 00eI along the path on the sides of small depres- -} _ _ ~ o-t OCl sions or elevations on the ground surface. 0) 4Xtn I-s s sU o m o Ioo IT Nest entrances usually had inconspicuous tu- muli on the downhill sides. In 1971 most of *o'v UrA 'Uq t. or-- the scattered entrances were in an area of a square meter. Main burrows descended di- '0. I- E -E agonally in a meandering fashion. Those of mo oo oof0 nests being provisioned were open through- cli and reN _ out, those of completed nests were filled with soil just below the surface or were filled above but open below where the laterals con- nected. Laterals (3-6 mm long), of the same ~~~~~~~~~~c diameter as main burrows, branched from the main tunnel at irregular intervals and in cn random directions. Those leading to closed . c) cells were filled with soil. i~|_4 ah One completed nest (fig. 4) contained seven C) 0 cells. Cells were arranged singly or in linear series of two, but in 1971 all cells seemed to be arranged singly. Completed cells in series were separated by short, soil-filled tunnels 1.25-1.5 mm long (N = 2). Cells were sym- metrical around their long axes and lined with 1989 ROZEN: "PRIMITIVE" PANURGINE BEES 5

A I . AFr

2 Figs. 2, 3. Nesting areas ofLiphanthus alicahue near Paipote, Atacama Province, Chile. 2. Nests in path in foreground. 3. Nest restricted to small, bare area by camera bag, left foreground.

a waterproof, clear, shiny coating. They tilted placed on the special inner coatings at the from 10 to 450 from horizontal, the rear lower rear of the cells. Some cells emitted a fer- than the front. Those containing food masses mented odor, suggesting that the provisions possessed a clear, silklike partial lining cov- of this species may normally ferment. ering the rear and rear floor, in addition to The white, shiny, curved eggs were placed the normal lining. The pollen sphere was af- on top ofthe food masses with their long axes fixed to it, apparently with nectar. This par- parallel to those of the cells. At least in two tial lining was thick, not unlike that ofa Col- cases the posterior end ofthe egg was attached letes, although less extensive, and could be to the food mass while the anterior end rose peeled from the other lining. The coating and above the mass. Eggs had a smooth chorion lining were appressed to each other, there and were blunt at both ends. being no fine, silk threads between them as As with most other panurgines, young lar- in Colletes. Both linings were waterproofwhen vae fed on top of the provisions and were tested with water droplets. This unusual, par- unable to crawl. After eating the front one- tial separate lining was overlooked in 1971, half of the provisions, the larva reached the perhaps because most cells contained older last instar. It then reoriented and, while fac- larvae. ing the cell rear on its back, consumed the The cell closure was a concave spiral of provisions still attached to its venter. After three to four coils on the inside, was smooth ingesting all food it again reoriented and faced and concave on the outside, so that the clo- the cell closure on its back; it defecated, ap- sure was 1.25 mm thick at the rim and 0.63 pressing the meconial mass against the upper mm thick at the center, in one case. Cells rear of the cell. Because a single nest con- arranged in linear series were separated from tained both eggs and pupae, the species ap- one another by a tunnel approximately 1.5 parently has a number of generations an- mm long. nually. All postdefecating larvae were active, Older offspring in nests were found in the exhibiting no diapause. As indicated else- upper cells, the younger ones in the lower where, no parasitic bees were associated with cells. these nests in that no immatures of Kelita PROVISIONING AND DEVELOPMENT: Fe- were recovered from a nest. males transported moist pollen on their hind ADuLT AcTivITy: I discovered the 1971 legs, and shaped the provisions into flattened site when I noticed males flying at 11:30 a.m. homogeneously moist spheres in the nest. The They ceased their activity at about 2:00 p.m. orange spheres, uncoated and shiny, were I had seen no males the day before when I 6 AMERICAN MUSEUM NOVITATES NO. 2962

5cm

6

8

5

....

9

93...

$ I L SEPTUM?

Figs. 4-10. Nests of some "primitive" panurgines, side views. 4. Liphanthus alicahue. 5-8. Metap- saenythia abdominalis. 9. Psaenythia annulata. 10. Cell of same, showing egg and provisions. Three scales refer respectively to fig. 4, figs. 5-9, and fig. 10.

visited the site at 2:30 p.m. Males flew over when they alighted. A single pair mated, for the ground in a zigzag fashion and thrust their approximately 5 seconds while they tumbled antennae forward and somewhat upward on the ground. 1989 ROZEN: "PRIMITIVE" PANURGINE BEES 7

Figs. 1 1, 12. Nesting sites of Liphanthus. 11. L. parvulus at Penuelas, Valparaiso Province, Chile, L. E. Penia excavating nest in path. 12. L. sabulosus at Tilama, Coquimbo Province, Chile; nest entrances in barren surface, left foreground.

Liphanthus (Xenoliphanthus) parvulus the front.) Its lining consisted ofa thick trans- (Friese) parent shiny waterproof coating over the en- tire surface and bore faint polar-directed HABITAT: Numerous males of this species ridges toward the rear. The cell was empty patrolled unvegetated, essentially horizontal except for the egg of Kelita chilensis, dis- areas such as paths at Peniuelas, Valparaiso cussed below. Province, Chile (fig. 1 1). I observed them both ADULT ACTIVITY: Adults, especially males, on October 6, 1969, and again on October were abundant at 11 a.m. on October 28, a 28, 1969, when they seemed equally abun- warm, sunny day. By 2 p.m. their activity dant. Females, less numerous than males, was much reduced, though some bees were were occasionally seen on the flowers of two flying even at 2:45 p.m. Males flew swiftly, species of Adesmia. (One Adesmia was no close to the ground, and landed often on bare longer in bloom on October 28.) The region areas. Females both with was dominated by herbaceous plants and a and without pollen trees. A also landed in the same areas at which time few scattered single nest was discov- several brief attempted (or actual) copula- ered on a gently sloping barren ground ex- tions were seen. posed to the sun. The soil, containing no Although many females were rocks, was hard packed above and moist and on the flowers ofAdesmia on October 6, only soft below a depth of 3 to 4 cm. a few were seen there on October 28. Males NESTS: The nest, containing an open, un- did not attempt copulation with females on provisioned cell, was in the early stages of the flowers. construction. Its main tunnel entered the CLEPTOPARASITISM: Many individuals of raised side ofa crack in the soil at an oblique Kelita chilensis (Friese) patrolled the same angle and then bent nearly vertically. A loose barren areas as the Liphanthus males, and tumulus occurred on the lower side of the the egg of this nomadine was discovered in crack. The main tunnel was open to a depth the open cell (Rozen, 1970b). of about 5 cm where it was blocked by loose soil for a short distance. Just below this ma- Liphanthus (Liphanthus) sabulosus terial it opened, became nearly horizontal, Reed and connected to the cell. Although the cell HABITAT: Several burrows within a few was essentially horizontal, exact orientation centimeters of each other were in a barren was uncertain. (Another cell from a nest of a area adjacent to an irrigated wheat field (fig. previous generation was tilted about 150 from 12) at El Naranjo, Tilama, Coquimbo Prov- the horizontal with the rear part lower than ince, Chile, on October 24, 1969. Nests of 8 AMERICAN MUSEUM NOVITATES NO. 2962 the panurgines Liopoeum trifasciatum (Spi- NESTS: The cell, with a maximum diameter nola) and Spinoliella herbsti (Friese) were in of 7-8 mm, possessed a wall that was indis- the same area although the nests ofthese three tinguishable from the substrate and lined with species seemed segregated. The combined a moderately smooth, shiny, waterproof nesting area, bordered by short trees on one coating. The closure was a concave spiral of side and low vegetation elsewhere, was un- three coils on the inside. shaded during the main part ofthe day. Dry, PROVISIONING and DEVELOPMENT: A pollen loose, and without stones on the surface, the mass shaped as a flattened sphere was orange, soil was moist just below. The surface sloped mealy moist throughout, and was not coated about 100 from the horizontal. with either a sticky surface (nectar) or a NESTS: Hasty excavations revealed two waterproofcovering. The curved, translucent nearly horizontal cells exhibiting a conspic- white egg possessed a shiny smooth chorion. uous over the entire inner waterproofcoating PSEUDOPANURGUS surface and a rounded rear end. Claude-Jo- seph (1926) depicted the cells of this species Many ofthe species formerly placed in this in a linear series of four at the end of a short genus were recently assigned to other genera, open main tunnel. so that in fact we have biological information PROVISIONING AND DEVELOPMENT: One about only three of the currently included pollen mass, uncoated and homogeneously species (table 2). Fragmentary information moist, was recovered from the rear of a cell. suggests that a thorough examination of at A small larva on top was feeding on the front least one species might reveal why some lar- end of the mass. vae seem to overwinter as predefecating forms ADULT AcrVry: A number of males flew (Rozen, 1967) whereas others overwinter as over the surface ofthe nesting area and along postdefecating forms (present study). the earthen path leading to it. When they alighted they characteristically clung to the Pseudopanurgusfraterculus sides of small rocks so that they faced up- timberlakei (Cockerell) ward, exposing their large yellow faces to the HABITAT: Females of this species nested at sky. This behavior pattern was apparently 2 mi east of Apache, Cochise County, Ari- associated with territorial behavior or with zona, in late August 1988, and we excavated mating activity, although matings were not a number of burrows on August 24 and 30. seen. All nests were situated on nearly horizontal CLEPToPARASmSM: We saw no cuckoo bees, but Friese (1916) suggested that Kelita chi- surfaces on grazing land that contained a lensis might attack the nests of this species. mixture of low-growing xerophilous herba- ceous plants including the main food source, Haplopappus gracilis Nuttall,2 as well as scat- PROTANDRENA tered shrubs (fig. 13). This North American genus until recently NESTS: Entrances were widely scattered over was considered a subgenus of the South an area ofmore than 100 m in diameter, and American genus Psaenythia. Chandler (1962) we found three as close as 3 cm apart. Adults briefly described the nest ofProtandrena ban- of its cleptoparasite, Holcopasites insoletus crofti as did Rozen (1967) for P. bicolor (Tim- (Linsley), throughout this same area helped berlake). Rozen (1970a) later reported on the draw our attention to some of the burrows. larva and pupa as well as the nest of P. ver- Although open when the females foraged, en- besinae (Timberlake) (misidentified as P. bi- trances were usually filled with several mil- color). limeters of soil in the evening and during inclement weather when the females were in Protandrena bancrofti (Dunning) the nest. The clogged entrances appeared nar- rower than the open, nearly vertical burrows HABITAT: Marjorie Favreau discovered a beneath. All single nest ofthis species at the Southwestern cells, arranged singly, were shal- Research Station, 5 mi west of Portal, Co- 2Kindly identified by A. Cronquist, New York Bo- chise Co., Arizona, on August 26, 1973. tanical Garden. 1989 ROZEN: "PRIMITIVE" PANURGINE BEES 9

Figs. 13, 14. 13. Nesting site of Pseudopanurgus fraterculus timberlakei at 2 mi east of Apache, Cochise Co., Arizona; nests widely scattered in lower halfofpicture, E. Quinter pointing to one entrance. 14. Nesting area of Cephalurgus anomalus at Cosmopolis, Sao Paulo, Brazil; F. C. Thompson sitting on ground digging nest, J. S. Moure looking for nest entrances. low and tilted slightly to the rear (ca. 200). defecating forms, contrary to preliminary Their dimensions (table 2) were consistent conclusions (Rozen, 1967) suggesting that all with those given in Rozen (1967). Cell walls Pseudopanurgus overwinter as predefecating were notably thick (ca. 5 mm) and substan- larvae. As is the case with most panurgines, tially harder than, but otherwise indistin- feces were applied as single masses to the guishable from, the substrate. They possessed upper rear wall of the cells, the first such ob- a conspicuous waterproof coating of trans- servation for the genus. parent material over their entire surface. Cell CLEPTOPARASITISM: Although Holcopasites closures were concave spirals on the inner insoletus had been tentatively associated with surface and consisted of 3 to 4 coils of mod- both Pseudopanurgus and Pterosarus (Hurd erately loose, coarse soil. Laterals were vari- and Linsley, 1972), the recovery of its first- able in length (2-5 cm; N = 3) and filled after and last-stage larvae from the brood cells of cell closure. Each nest was occupied by a sin- Pseudopanurgusf timberlakei now confirms gle female. the association with Pseudopanurgus. The last PROVISIONING AND DEVELOPMENT: Fe- instars of this cuckoo bee were completely males shaped provisions into uncoated, flat- quiescent in contrast to the postdefecating tened spheres and deposited eggs on the tops. host larvae. A larva, perhaps early last stage, sat on the top of one pollen mass that had its front half HETEROSARUS eaten away, an indication that larvae do not This is the only genus of "primitive" pan- crawl over their food masses as they feed. We urgines to occur in both North and South recovered several postdefecating larvae still America. In spite of its wide distribution, its able to slowly curl and uncurl their bodies, nesting biology has not been described be- as has been reported for postdefecating Pro- fore. tandrena verbesinae (Rozen, 1 970a) and Me- tapsaenythia abdominalis (present paper). We also found predefecating larvae, one ofwhich Heterosarus nanulus (Timberlake) was still alive and responsive to touch (far HABITAT: We studied the nesting of this more so than the postdefecating larvae) more species and its parasite, Holcopasites tegu- than four months later; it defecated and be- laris Hurd and Linsley, August 20 to Septem- came more active during the first 10 days of ber 1, 1971, at 13 mi southwest of Apache, April 1989. Hence, larvae ofthis species seem Cochise County, Arizona, the type locality to overwinter as both predefecating and post- for both species. Burrows of Heterosarus 10 AMERICAN MUSEUM NOVITATES NO. 2962

nanulus occurred on barren and semibarren other panurgines. Ofthree mature larvae un- stretches of unpaved roads that bordered covered, one was defecating, applying the Route 80 (Rozen, 1984b: fig. 25). Although feces as elongate, parallel strips to the upper predominantly grassland, the region offered rear of the cell; another began defecating numerous herbaceous plants, particularly within several days of being discovered; the along the disturbed roadsides, and the area third had not started defecating by August adjacent to the nesting area consisted of sev- 29, 1971, when observations ceased. The two eral species ofEuphorbia (the food source for larvae pupated after defecating, suggesting this species) as well as other low-growing that the species undergoes more than one herbs. None ofthe nests were shaded by vege- generation a year. tation in spite ofscattered mesquite trees and CLEPTOPARASITISM: Female Holcopasites other shrubs. The soil, volcanic in origin, was tegularis examined or entered the burrows of moist because ofrecent rains and moderately the species on at least ten occasions during pebbly, both on the surface and at the cell our observations. Holcopasites entered sev- level. It was difficult to dig because the soil eral nests twice before we excavated them. fractured unevenly. The surface sloped only Because of the difficulty of excavating nests, barely at most ofthe nest entrances although we uncovered few cells of H. nanulus intact. one nest was found on the side of a sloping One, however, contained a first instar ofHol- embankment about 3 m high. copasites biting an egg of Heterosarus, and NESTS: Of the approximately 15 nests of another, a first instar Holcopasites ambulat- Heterosarus nanulus discovered, none was ing by pushing itself with the tip of its ab- surrounded by a tumulus. The open main domen over the cell wall. Not infrequently, tunnels, circular in cross section, descended it stopped and raised the anterior part of its nearly vertically although in a few cases they body in the air. One first instar was approx- meandered slightly, presumably because of imately 0.6 mm long, and both were semi- hard soil inclusions. Because ofthe nature of transparent, white, possessing distinct but the soil and the small diameter of the main unpigmented head capsules with sharp- tunnel, the nest structure was difficult to ex- pointed but not very long mandibles. Egg in- amine. Cells, arranged singly, were found from sertion holes were discovered in the walls of 8 to 9 cm deep though presumably some oc- both cells. Similar to the insertion holes de- curred at lower depths. scribed by Rozen (1965a), each consisted of Several laterals were 1.3-1.5 mm in di- a hinged flap beneath which was a cavity ap- ameter; their walls were rough and emboss- proximately 0.3 mm long. The vacated cho- ings from the females' pygidial plates were rions were visible but had collapsed after evident. Laterals were filled with soil after eclosion. cell closure. One nest contained four cells, with the oldest larva highest in the series. The CEPHALURGUS cells were nearly horizontal but tipped some- what to the rear. Their smooth walls pos- Cephalurgus anomalus sessed conspicuous, shiny, waterprooflinings Moure and Oliveira over their entire surface. The closure ofcoarse HABITAT: This species nested at Cosmo- particles was a concave spiral on the inside. polis, Sao Paulo, Brazil, on January 26, 1974, PROVISIONING AND DEVELOPMENT: Fe- and was studied over a three-day period. The males transported pollen as moist masses on region was originally forested but tropical ag- their hind tibiae. They deposited the food in riculture, primarily sugar cane plantations, the rear ofthe cells as amorphous masses and had long dominated so that none ofthe orig- shaped it into flattened spheres only when all inal forest survived. The nesting site was in supplies had been accumulated. Fully formed a large field (fig. 14) that had been recently masses were visibly moist on the outside and bulldozed. As a consequence, plants generally seemed to be uniformly moist on the inside. less than one meter tall, including the food An egg had been deposited on the top of one plant, Sida (Malvaceae), covered much of it. mass, and an intermediate-stage larva sat on Bare areas, some resulting from recent scrap- top of another, both in positions typical of ings, appeared randomly over the field. Al- 1989 ROZEN: "PRIMITIVE" PANURGINE BEES I1I though we searched for nests in many ofthese coloration. Such macrocephalic forms have bare patches, we found them only in two. been found in the nests of some Perdita. Both sites sloped gently and consisted of During the height of foraging (9:00 to soil which when dry was hard but when wet 10:30 a.m.) 40 pollen-laden females entered was easily excavated. The soil lacked a pow- another nest during a half hour period and 9 dery surface layer because of the heavy rains females entered a smaller nest nearby. We that occurred every afternoon during the field did not monitor exiting females in either case, investigations which took place in the rainy so that the colony size could not be estimated. season. We were impressed by seeing so much Nest entrances occurred on horizontal ground rain during the nesting period ofa panurgine, and along the sloping side of a low earthen and the moist condition of the food masses embankment, 20 to 40 cm high. Most were of these bees and unusually plump predefe- not surrounded by tumuli because of after- cating larvae (discussed below) may have been noon rains and sloping surfaces, but one, on connected to the high relative humidity and the flat, was surrounded on all sides by a abundant water. Homogeneous, the earth tumulus 3 cm in diameter and 0.7 to 0.8 cm contained no stones or pebbles, only fine high. Entrances were open during morning roots, and was dry on the surface early in the foraging but were closed around noon after morning before the rains but moist below the the females had returned. There was only a surface at all times. single entrance for each nest. The pollen plant was abundant throughout Circular in cross section and open, burrows the field but was especially prevalent near the descended with little meandering. Burrow larger of the two bare areas. The appearance walls were rough. The main burrow of one of the flowers and their time of opening and nest, containing 13 females and 1 male, did closing suggested that several species of Sida not branch, but in the other three nests each may have been represented. Flowers opened branched a number oftimes, with each branch between 8:00 and 9:00 a.m. and closed short- tending to descend more or less vertically so ly after noontime. that branches never diverged widely. In one NESTS: The smaller nesting site contained nest a short tunnel 12 mm long branched at a single nest whereas the larger one, approx- a depth of 13 cm and ended abruptly. This imately 30 m away, was composed of 10 to vestibule may have permitted females to pass 20 nests. We excavated the nest from the one another. Main tunnels and branches were small site and three from the larger one, and open for their entire lengths. Even though each contained a number offoraging females burrows of separate nests approached one as well as callow males and females. Most, if another, they did not anastomose. Females not all, other nests were also composite. The always filled laterals after cell provisioning first nest excavated contained 12 females and and closure. We were unable to trace open undoubtedly a number of others escaped de- laterals, so that their configuration is un- tection. Of these 12, 5 were teneral, lacked known. However, many cells were as far as large o6cytes and had no pollen in their ali- 7 cm from the main tunnels, indicating that mentary tracts; 5 contained large oocytes and laterals were of considerable length, perhaps pollen in their alimentary tracts; 1 (not dis- averaging 5 to 6 cm. sected) was carrying pollen; and 1 though not Cells were arranged singly rather than in obviously teneral lacked pollen and had no linear series. Tipped slightly to the rear, they large o6cytes. These facts suggest that there were essentially horizontal and appeared is no caste system and that there is probably similar to the diagrammed cell of Protan- no division of labor (but see comments on drena verbesinae (Rozen, 1967: fig. 6; mis- teneral females, below). This same nest yield- identified as P. bicolor). The closure was a ed 4 males, all fresh and apparently teneral. coarse, indistinct spiral, concave on the inner Although males of this species have large surface with about three coils. The cell wall heads, there is little variation in head width was extremely smooth, without pygidial plate and these 4 males gave no indication ofbeing markings, and indistinguishable from the subterranean, i.e., they did not have extra substrate. Cell linings were thick, waterproof, large heads, reduced compound eyes, or pale conspicuous, covered all cell surfaces except 12 AMERICAN MUSEUM NOVITATES NO. 2962

for the closure, and could be easily peeled of the cell as is the case with all panurgines with forceps. except most Perdita. Feces were unusual in PROVISIONING: Females transported yel- that they were deposited as approximately 15 low-orange pollen ofSida as large moist sticky elongate pellets, each about 2 mm long, masses on the anterior surfaces of their hind roughly in the sagittal plane ofthe cell. These tibiae and to some extent on their hind fem- pellets were not flattened so that the surface ora. The finished loaf formed a flattened of the deposited meconial mass was uneven. sphere, homogeneously sticky-moist through- With aging, pellets lost their identity, perhaps out. Its surface appeared coarse because of because of the moisture in the cell or mold. the large size of the pollen grains and lacked Older fecal masses therefore appeared as sin- a waterproof coating. gle unconsolidated bodies of loose pollen DEVELOPMENT: The female placed a white, grains. elongate, curved egg with a shiny transparent We encountered very active postdefecating chorion on the top ofthe loafas diagrammed forms, six pupae, but no inactive postdefe- for Protandrena verbesinae (Rozen, 1967: fig. cating larvae; hence diapausing did not occur 6). Eggs were attached only at their anterior during the season of these observations. As and posterior ends. The anterior end was with all panurgines, no cocoon was spun. Af- blunter than the posterior end and faced the ter emerging, adults apparently spend time cell closure, as is characteristic of all panur- in the nest while their integument hardens gines. and colors. It is unknown if teneral adults Young larvae and even last instars sat sta- function in the nest while they harden, but tionary on top ofthe pollen masses while they several were encountered at the ends of bur- fed on the loaf beneath. Very small larvae rows suggesting they may assist in digging ingested considerable quantities ofliquid be- tunnels. fore eating pollen, revealed by viewing the PHENOLOGY: Adult activity outside the nest liquid-to-pollen ratio in the stomach contents during the day was synchronized with the ofrecently preserved specimens. With almost diurnal blooming period of the pollen plant. all panurgines (Panurginus is the exception), On one day, nests were opened between 8:45 larvae consume approximately halftheir pro- and 9:30 a.m. and females started foraging. vision by eating away the front half of the The first flowers opened at about 8:00 a.m. food mass while sitting on top of it. Then, and all flowers were in full bloom by 9:45. after reaching the last instar, they reorient Bee activity on the flowers diminished sub- and, resting on their dorsa, finish the food stantially by 11:30 a.m. with only scattered hemispheres cradled on their venters. Larvae females to be seen. The flowers closed be- of Cephalurgus were always encountered tween 12:30 and 2:00 p.m. perched on the loaf even when two-thirds of Because we encountered no diapausing lar- the food had been eaten and only a small vae and found all ontogenetic stages, this crescentic part (seen in side view) remained. species must have a number of generations We found no larvae resting on their dorsa per year or have continuous generations while they completed the provisions. Failure throughout the year. Numerous old vacated to observe larvae on their dorsa was, there- cells excavated from at least three ofthe nests fore, probably not the result of too small a indicate that nests are used by members of sample. The feeding activities of this species successive generations. need further research, but the species appears ADULT AcTIvITY: Mating was not ob- atypical for the subfamily. served, but the absence of males over the The fully fed larva (to be illustrated and nesting area indicated that mating does not described in a subsequent paper) was unusual take place in association with the nests. Males because of its very large abdominal region, a were numerous on the Sida flowers and flying feature not seen before in panurgines. The from one blossom to another, a possible in- postdefecating larva, in contrast, was much dication that copulation is initiated on the smaller than the predefecating form and had food plant. Padre Moure (personal commun.) proportions typical of other panurgines. stated that mating is initiated on the flowers Feces were always voided on the upper rear and that the pairs then drop to the ground. I 1989 ROZEN: "PRIMITIVE" PANURGINE BEES 13

Figs. 15, 16. 15. Nesting site of Metapsaenythia abdominalis at 2 mi WSW of Osceola, Hill Co., Texas; nests widely scattered throughout lower half of picture, taken on August 10, 1988, when adult bees no longer active. 16. Psaenythia annulata at Furnas, Vila Velha, Parana, Brazil; nests to the left of J. S. Moure, middle foreground. would have noticed pairs flying in copula if days. Because the nesting season had just be- such were the mating mode. gun, I returned to the site on August 10, 1988, CLEPTOPARASITISM: No cuckoo bees have to recover mature larvae from a nest previ- been associated with this species either at the ously marked but left to be excavated later. nesting site or at numerous other localities The site was now quiescent; no adults ofeither where the bees flew. Metapsaenythia or its cleptoparasitic bee were evident although a few scattered blossoms METAPSAENYTHIA persisted on the pollen plant. This genus contains two described species. The nesting area occupied the east side of Metapsaenythia abdominalis, biology de- a fenced pasture bordered by shrubs and trees. scribed below, occurs from Kansas and Texas Pasture plants of low-growing herbs and to the east coast of the United States. Me- grasses were generally no more than 15 cm tapsaenythia sonorana Timberlake is known tall, but the pollen plant, Monarda punctata only from the type specimen from Sonora, L., affinity towards var. stanfieldii (Small) Mexico (Timberlake, 1969). Nothing has been Cory,3 was widely distributed throughout the recorded about the life histories of either pasture and tended to be taller, with some species except that Timberlake (1969) re- plants being nearly a half meter high. Live ported that females of M. abdominalis ab- ground cover was greater than 80 percent, dominalis collect pollen from Monarda (al- and dead plant material, cattle feces, and oak though they have been taken at flowers of a leaves obscured the surface further. Only ro- number of other plants) and the type of M. dent mounds offered barren surfaces which, sonorana was captured on Tidestromia lanu- however, were unused by nesting Metap- ginosa. Mitchell (1960) recorded that Metap- saenythia. The low-growing vegetation at the saenythia a. tricolor (Cockerell), an eastern nesting area was similar to the mixture de- dark form, has been collected only from scribed above, except Monarda was scarcer Monarda punctata. and part ofthe area near an oak tree was more uniformly covered with grasses. Whereas the Metapsaenythia abdominalis (Cresson) ground surface gently sloped in most areas of HABITAT: I discovered the nesting site (fig. the pasture, the nesting site was on the high 15) of Metapsaenythia abdominalis 2 mi part ofthe pasture near two large oaks. These WSW ofOsceola, Hill County, Texas, on June 3Kindly identified by Thomas J. Starbuck, New York 26, 1988, and studied it during the next four Botanical Garden. 14 AMERICAN MUSEUM NOVITATES NO. 2962 trees cast an open, sun-flecked shade over all both cases. The enlargement of the burrow but one of the nest entrances until about 11 may have resulted from the female taking soil a.m. Afterwards all entrances except one at from the burrow wall to construct the sep- the boundary ofthe open shade were exposed tum. Septa may assist in excluding Holco- to full sun. The soil at nest excavations was pasites females from finding open cells; nei- uniformly moist, moderately fine, even- ther cell so walled offcontained Holcopasites grained, moderately compact sand that tend- eggs. The single completed nest (fig. 5) stud- ed to remain in clumps after drying. The soil ied in August had an open burrow to the contained few pebbles but was penetrated by depth of25 cm but was filled with loose, fine- fine roots. grained soil from there to about the 30 cm NESTS: I first discovered the nest area be- level, below which it was lost. Burrow walls cause of adults of the cleptoparasite, Holco- were dull, moderately rough, nonwaterproof pasites eamia (Cockerell), searching it. Five when tested with a water droplet, and pre- nests were eventually identified scattered over sumably unlined. an area about 4 m long and 2 m wide, with All laterals leading to open cells were cir- a sixth nest occurring 30 m away. Although cular in cross section, open, and invariably nests probably occurred elsewhere as evi- curved upward before widening at the cell denced by Holcopasites searching more entrance (figs. 6-8). Their walls were unlined, widely, Holcopasites activity and therefore dull, and smoother than those of the main nest occurrence was restricted to only a small burrows. Laterals leading to the closed cells part of the pasture. Two nests were a third were soil-filled and undetectable. Laterals of a meter apart but others were more widely measured by the horizontal distance between distributed. the cell entrance and main tunnel terminus Only a single Metapsaenythia female was ranged from 1.5 to 4.5 cm, but the seven cells associated with each nest, and the nest en- seemingly (but not certainly) belonging to the trances were hidden among the growing vege- closed nest (fig. 5) were distributed over a tation, dry grass, and dead leaves, so that they horizontal area 20 cm in diameter. could not be detected unless these plant ma- All cells were arranged singly (that is, not terials were removed or parted. Each was dis- in linear series) and were nearly horizontal, covered because I observed a returning fe- sloping toward the rear by 10 to 200. They male trying to enter her burrow. In spite of were elongate ovals with their rear ends being hidden, these entrances were open and rounded. They appeared symmetrical around not clearly surrounded by tumuli. Excavated their long axis so that the ceiling was not more soil, apparently intermixed with surface de- highly vaulted than the floor. The cell wall, bris, was rained upon and therefore lost its at least in one case, was slightly harder than identity quickly. the surrounding substrate, but no other fea- Except in one nest (fig. 7) that had a nearly tures distinguish the wall from the substrate. horizontal upper segment 4 cm long, all main The wall was coated with a distinct shiny burrows descended more or less vertically lining, darker than the substrate on freshly with slight bending. The deepest burrow (fig. excavated cells (but when exposed soon dried 8), 47 cm long, angled from the vertical so to be concolorous with the substrate). The that its terminus was 10 cm from a vertical lining covered all surfaces of the cell, but at line passing through its entrance. Main bur- least in one cell it ended 1 mm from the rows excavated in June were approximately narrowest point of the cell mouth. Whether 4.0 mm in diameter although one was slightly this uncoated area would have been covered smaller (3.75 mm) near its entrance. Main by the closure is uncertain. burrows were not filled with soil but two nests The cell closures of loose soil were un- (figs. 6, 8) (and possibly all) contained a thin coated and consisted ofa deeply concave spi- septum of fine dry soil immediately above ral of 3-4 coils on the inner surface. the junction with the lateral which led to the An unusual feature of the nests studied in open cell. The upper surface of the septum June was the variability in cell depth, some was concave and the area immediately above open cells being only 11 cm deep and the it was 6.0 mm and 5.5 mm in diameter in deepest, 47 cm. In the nest with two cells, the 1 989 ROZEN: "PRIMITIVE" PANURGINE BEES 15 completed cell was above the open one. The saenythia and Holcopasites populations, I completed nest excavated in August presum- studied the wing wear along the outer edge ably had seven cells, ranging in depth from of the forewing of all individuals (41 Metap- 28 to 40 cm. saenythia and 17 Holcopasites) collected in PROVISIONING: Females transported pollen June. The individuals were assigned to one as a moist solid on the hind tibiae. Each of of four categories, each reflecting the per- the five nests excavated in June contained a centage of the wing edge worn away. The fig- partly provisioned open cell. In all these cases, ures are presented in table 3, on the basis of stores were sufficiently liquid so that their combining the sexes ofeach species and then upper surfaces were horizontal and some clear ofseparating the sexes ofeach. Ifone assumes fluid (presumably nectar) was discernible in- that the rate ofwear ofthe wing ofthe species termixed with pollen grains. Such fluid pro- and of the sexes is not altered by the obvious visions are unknown among other panur- differences (discussed below) in their flight gines, whose provisions are either removed behaviors, then the relative ages of the in- from hind legs as irregular semisolid masses dividuals are reflected by the degree of wing or shaped into small spheres to which addi- wear: i.e., the more wing wear, the older the tional loads are subsequently added. The liq- individual. Table 3 suggests that the Metap- uid early loads in Metapsaenythia may have saenythia population had emerged later than resulted from females depositing moist pol- that of Holcopasites in that 73% of the Me- len and then adding nectar. On the other hand, tapsaenythia had 0-25% wing wear whereas each ofthe five nests excavated had remained only 29% of the Holcopasites fell into this open overnight (females had been either col- category and 41% exhibited excessive wing lected the day before or excluded from the wear (75-100%). The disparity between the nest) so that the nectar in the provisions may two populations may actually have been have acquired water from the visibly moist greater since many ofthe Metapsaenythia (but substrate. The single completed food loaf, on few of the Holcopasites) showed almost no the floor of the cell, was a formed semisolid wing wear (that is 0%) and some of the Hol- with a sticky surface to which sand had ad- copasites (but none of the Metapsaenythia) hered as a result ofexcavation. Its exact shape exhibited wing wear in which much of the could not be detected but it was unquestion- wing distad ofthe veins had disappeared [that ably more solid than the preliminary provi- is to say, a more precise classification might sions in the open cells. have included yet two more categories to rec- DEVELOPMENT: Cells from the nest exca- ognize: (1) 0% wing wear only and (2) wear vated in August yielded five postdefecating beyond the total destruction of the original larvae of Metapsaenythia and two of Hol- wing edge]. Eighty-four percent ofthe female copasites. Whereas the Holcopasites larvae Metapsaenythia had 0-25% wing wear, and were totally quiescent, all Metapsaenythia the remaining 16% had 25-50% wing wear, were able to slowly curl and uncurl their bod- whereas males of the same species had 64% ies, an unusual feature for postdefecating, in the 0-25% bracket and the remaining males overwintering larvae ofthe Panurginae. They fell into all ofthe three other categories. These continued these movements for months, al- figures probably reflect the fact that the species though by the end ofJanuary 1989 they could is protandrous. Although the figures for males no longer be induced to move. All Metap- of Holcopasites are too few for analysis, the saenythia postdefecating larvae were discov- fact that only three Holcopasites males were ered resting on their prominent dorsal tu- captured may be an indication that the species bercles, with their heads near the cell entrances is also protandrous and many of the males and their fecal material plastered at the upper had already died. Comparison ofthe females rear wall of the cell. Their integument was of the two species reveals that the Holcopa- coated with an oily material that caused sand sites population was substantially further ad- to adhere to it, in contrast to the dry integ- vanced with only 36% of individuals in the ument of Holcopasites overwintering larvae. 0-25% category and 64% in the other three PHENOLOGY: In an attempt to analyze the categories, whereas 84% of the Metapsaeny- relative ages ofthe individuals in the Metap- thia females were in the 0-25% category and 16 AMERICAN MUSEUM NOVITATES NO. 2962

TABLE 3 Analysis of Wear of Outer Edge of Forewing of All Metapsaenythia and Holcopasites Collected 2 Miles WSW Osceola, Hill County, Texas, in June 1988 The four categories represent percentages of wear (removal) of normal outer edge. For explanation, see text. 0-25% category 25-50% category 50-75% category 75-100% category Sexes combined: Metapsaenythia Individuals (N = 41) 30 5 2 4 Percentage of sample 73% 12% 5% 10% Holcopasites Individuals (N = 17) 5 4 1 7 Percentage of sample 29% 24% 6% 41% Sexes separated: Metapsaenythia Males Individuals (N = 22) 14 2 2 4 Percentage of sample 64% 9% 9% 18% Females Individuals (N = 19) 16 3 0 0 Percentage of sample 84% 16% - - Holcopasites Males Individuals (N = 3) 0 1 0 2 Percentage of sample - 33% - 67% Females Individuals (N = 14) 5 3 1 5 Percentage of sample 36% 21% 7% 36%

the remaining 16% fell only into the 25-50% which later became partly cloudy to cloudy. category. During the afternoons of these two days, fe- The earliness of the Metapsaenythia nest- males became so abundant on the flowers ing season in June was also reflected in the after 1:30 p.m. that I thought that their ac- fact that, of the five nests excavated at that tivity might normally be restricted to the time, only one contained a completely pro- afternoon; however, on June 29 and 30, days visioned and closed cell. All four females as- that remained clear, females were observed sociated with the nests fell into the 0-25% in the late morning, and no surge of females wing wear category. occurred in midafternoon as had been per- Metapsaenythia abdominalis and Holco- ceived on the two previous days. Future pasites eamia have a single generation per monitoring of flight activity will perhaps ex- year, as revealed by the presence ofpostdefe- plain the observations. cating larvae in the nest excavated in August Male flight activity primarily involved mate and by the pollen source being essentially ex- searching. Males flew moderately swiftly from hausted at the same time. one pollen plant clump to another, and they ADULT AcTIviTy: I saw male Metapsaeny- also scouted the nesting area where they thia around the flowers throughout the field probably were looking for females leaving and from when I arrived at 10:20 a.m. until I returning to nests. Males occasionally ap- departed at about 4:30 p.m., although the proached females at the flowers and at the activity was reduced at 4:15 p.m. on June 27. site, but all observed meetings ended nearly In general, males were more abundant than instantaneously as the female quickly avoid- females, and females were uncommonly seen ed the male. Several times a male would again on the mornings of June 27 and 28, days approach the same female but was again 1 989 ROZEN: "PRIMITIVE" PANURGINE BEES 17 avoided. Unless the nearly momentary en- stinging sensation resulted, but within several counters were matings, no copulations were minutes hard welts appeared in the two areas detected. where the female had been positioned, in- The female foraging flight was moderately dicating that venom had penetrated my skin slow and deliberate. A female often circled a and that the bee can use its sting as a defense flower stalk ofMonarda and alighted on one mechanism. or more blossoms to forage before departing Females almost certainly spend the night to another stalk. Not infrequently a female in their nests. Males presumably sleep in departed from one stalk to forage on another crevices and unoccupied burrows, for I ob- only to return to the first stalk, suggesting that served a male digging into a loose rodent females could not recognize flower stalks they mound one afternoon and another male had recently visited. searched the same mound. Some females landed only to take nectar CLEPrOPARASITISM: During the three days from flowers, others only to collect pollen, of observations in June, Holcopasites eamia but, if a female visited a flower for nectar and females were abundant. They flew slowly close pollen, she invariably gathered nectar first to the ground in a meandering flight. Several and pollen second. A nectaring female was males had a similar slow flight so that I was immediately identifiable because she inserted uncertain ofgender offlying Holcopasites. Not her head and mesosoma into the corolla while infrequently, a female flew back and forth her metasoma extended from the corolla and over a limited area, perhaps 10 cm in di- her hind legs held down the lower lip of the ameter, and alighted occasionally, suggesting corolla, while her wings, longitudinally plait- that she was assessing whether a hidden bur- ed and darkly infuscated, conspicuously di- row was present or occupied. No matings were verged from each side of the flower. In this observed and males seemed uncommon or posture her head and part of the mesosoma absent toward the end of the study period in were hidden within the corolla. A pollen- June. gathering female, on the other hand, clung to Of the five nests excavated in June, only the lower surface ofthe upper lip ofthe flower the one consisting oftwo cells contained Hol- and faced away from the corollar base so that copasites immatures. The closed cell yielded her head appeared face up at the apex of the five first instars (two alive and three dead, upper lip where the anthers extruded. Fe- apparently killed by the live ones) and the males presumably raked pollen from the an- dead white egg of Metapsaenythia. The va- thers with their foretarsi, although the brief cated chorions of some of these larvae were motion of their heads seemed to suggest that visible in the cell wall. The open cell con- they were chewing the pollen from the an- tained a single live egg inserted into the un- thers. Nectaring on a flower took approxi- lined part ofthe wall at the cell entrance. One mately five seconds; pollen gathering only end, protruding 0.2 mm into the lumen, ap- several seconds. peared narrow and therefore may have been An unusual feature ofthe females (and per- the egg's posterior end, but this orientation haps of males) of this species is their ability needs to be checked because anterior ends of to fold their wings longitudinally. Whereas nomadine eggs normally are at the cell sur- such wing folding is characteristic ofthe Ves- face. This egg was not inserted under a flap pidae, it has been recorded in bees only for as reported by Rozen (1965a) and Hurd and the paracolletine genus Eulonchopria where Linsley (1972) for several other species of it may be a mimetic trait (Danforth and Holcopasites, but, like that of other Holco- Michener, 1988). pasites and of Nomada, it was not cemented Live females held between the fingers emit- into the hole as is characteristic ofsome other ted an oil-of-lemon odor, characteristic of genera of Nomadinae. many panurgines. Removed from the fragment of cell wall Because females have a well-developed ex- by being placed in water, the translucent white ternal stinging apparatus, I investigated their egg was 0.5 mm long, 0.2 mm in maximum ability to sting by holding a live female against diameter. Its anterior end (as identified by the inner surface of my forearm. No certain the head capsule of the embryo) was broadly 18 AMERICAN MUSEUM NOVITATES NO. 2962

rounded and the posterior end tapering. Its The second burrow (fig. 9), with a concen- chorion was unsculptured, shiny, and trans- tric tumulus 2.0 cm in diameter, also de- parent. A noteworthy feature was its small scended vertically and was unfilled its entire size, also reflected in the small size ofthe first length. Laterals, filled after cell closure, var- instars. One first instar that had consumed ied in length from 1 to 4 cm, and the one no pollen was 0.8 mm long. leading to an open cell descended slightly be- The two postdefecating larvae from the fore reaching the cell. completed nest were totally quiescent, and at Nearly horizontal cells (fig. 10), arranged least one rested on its dorsum with its head singly and randomly around the burrow, had pointed toward the cell closure. The feces were walls indistinguishable from the substrate. centered at the upper rear ofthe cell, but they The inner wall surface was smooth and com- covered more of the rear wall than did those pletely coated with a shiny, presumably of Metapsaenythia. waterproof lining. The closure was a spiral, First instars possessed sclerotized, only concave on the inside. The uppermost cell faintly pigmented head capsules, sharp- was filled with soil. pointed mandibles, and elongate labral tu- PROVISIONING: Females transported pollen bercles, and they used the tip ofthe abdomen in a moist condition on their hind legs. Pol- as a pygopod to push themselves along. len-laden females visited a variety of plants, both at this locality and at others, suggesting PSAENYTHIA the species may be polylectic. The open cell contained four irregular-shaped but nearly Claude-Joseph (1926) diagrammed and identical, compact, pollen-nectar masses de- described the nest of Psaenythia interrupta posited from the female's tibiae; thus the fe- Friese, and Janvier (1933) briefly mentioned male had already made two foraging trips. its nest in conjunction with describing the Because I her mature larva. captured returning with yet another load, she would have made at least three trips to provision the cell. Of the two Psaenythia annulata (Gerstaecker) completed pollen masses, one was a perfect sphere, 3.5 mm in diameter; the other was a HABITAT: We found two nests of Psaeny- flattened sphere, 3.75 mm high and with a thia annulata at Furnas, Vila Velha, Paranfi, horizontal diameter of 4.25 mm. Both were Brazil (fig. 16), on February 9, 1974. They homogeneously mealy-moist, somewhat were a meter apart in a seldom-used earthen shiny, but without either a waterproofcoating roadway that bordered a large grass area with or a special layer of liquid on the outside. numerous low-growing herbaceous plants. On When they were removed, the cell floors were the other side of the road were low trees far moist where they had rested toward the rear enough removed so as not to shade the site. of the cells (fig. 10). Sparse plants grew on the roadway providing DEVELOPMENT: Two curved eggs were po- less than 50 percent coverage. The surface of sitioned slightly anterior of the top of the the nesting site was sandy and sloped slightly; pollen masses in the plane ofthe long axis of dry on the surface, the soil was moist im- the cell. More rounded on the anterior end mediately below. It was easily excavated, than the posterior end, they were white and containing no rocks and only small roots. had a smooth shiny chorion. No larvae were NESTS: A single female and no males were recovered. associated with each nest. Neither nest was ADuLT AcTrIVTyr: Because we observed started near objects on the surface. The en- males flying around flowers and not around trance ofthe first burrow was surrounded by nest entrances, we presumed that mating takes a small loose tumulus, and its tunnel de- place on the flower. scended vertically to a depth of 6 cm where CLEPTOPARASITISM: Rozen (1 977b) has re- it ended. Filled with loose soil, the burrow ported on the association of a species of presumably was in the early stage ofconstruc- Brachynomada near argentina Holmberg with tion. the nesting site of this species. 1989 ROZEN: "PRIMITIVE" PANURGINE BEES 19

POTENTIAL OF BIOLOGICAL the same species as the females) in composite FEATURES IN nests of two species of Perdita, P. portalis PHYLOGENETIC ANALYSIS Timberlake and P. mellea Timberlake (not OF THE PANURGINAE formerly reported in entomological litera- ture); normal males (though exhibiting vari- Unless otherwise noted, biological data ability in head size) flew around flowers in concerning the Panurginae referenced below the vicinity of the nests. Such striking male come from the current study, Rozen (1958, dimorphism is unknown elsewhere in the 1965b, 1967 [summarizing all previous lit- family and is an apomorphy of considerable erature], 1968, 1970a, 1971 a, 1988), my un- interest both systematically and behavioral- published fieldnotes (mostly regarding South ly. Males of other species of Perdita and of American and African genera), Eickwort Panurgus show variability in head size sug- (1977), Hirashima (1962), Rust (1976, 1988), gesting that this phenomenon should be Shinn (1967), and Torchio (1975). looked for in other species that nest com- The Andreninae, the other subfamily in the munally. Andrenidae, is the obvious choice for out- DEPTH OF NESTS: This character is of lim- group comparisons. It comprises only six dis- ited use, partly because most of the nests parate genera (in contrast to the approxi- studied are still incomplete so that the deep- mately 35 genera [sensu Ruz, 1987] of the est cells are not yet constructed. Furthermore, Panurginae): the huge, primarily Holarctic very small bees tend to have shallower nests, Andrena, the two small Nearctic Megandrena and composite nests (containing numerous and Ancylandrena, and the three small Neo- females) ofAndrena and Perdita are generally tropical Euherbstia, Orphana, and Alocan- deeper than nests of related bees containing drena (Rozen, 1971b; Michener, 1986). only single females. Also, we can assume that Whereas Andrena contains approximately bees that nest in very compact soil have a 2000 species, the other genera together ac- difficult time in constructing deep nests, so count for a mere 10 species. Andrena is the that depth of nests may depend to some ex- only genus about which there is available bi- tent on the nature of the substrate. Most An- ological information. Nesting biologies of drena bees have the lowest cells well below Andrena come from selected references, es- 15 cm. The "primitive" panurgines exhibit pecially Packard (1889), Parker and Boving considerable variation in depth ofnests (depth (1925), Malyshev (1926, 1935), Michener and of lowest cell). However, the very shallow Rettenmeyer (1956), Linsley and MacSwain nests of Liphanthus are almost certainly de- (1956, 1959), Hirashima (1962), Stephen rived, and the shallow nests of such bees as (1966), Youssef and Bohart (1968), Thorp Nomadopsis, Calliopsis, and Hypomacrotera and Stage (1968), Thorp (1969), Linsley, are therefore a separately derived synapo- MacSwain, Raven, and Thorp (1973), Rozen morphy. (1973), Davis and LaBerge (1975), and TUMULI: Nest entrances of most Andrena Schrader and LaBerge (1978). There is also species and all of the "primitive" panurgine extensive literature dealing with flower re- genera treated here either lack tumuli or, if lationships. excavated soil is present, it surrounds but NUMBER OF FEMALES OCCUPYING A NEST: does not hide the entrance. The hidden en- Nest occupancy by a single female is un- trances of Andrena erythronii Robertson questionably plesiomorphic in the Apoidea. (Michener and Rettenmeyer, 1956) and A. The apomorphic condition of nest sharing vaga Panzer (as ovina Klug) appear to be an (i.e., composite nests) has developed a num- evolutionary development separate from that ber of times among a few species ofAndrena, in the Panurginae. In contrast to the plesio- Cephalurgus anomalus, Psaenythia interrup- morphic condition, entrances that are hidden ta, Melitturga, Meliturgula, Poecilomelitta, by tumuli (or by loose surface sand or soil) Panurginus, and certain groups of Perdita. are derived (Nomadopsis, Calliopsis, some MALE NEST INHABITANTS: I have found Hypomacrotera, and related South American megacephalic, small-eyed, flightless males (of genera). Nests with such hidden entrances 20 AMERICAN MUSEUM NOVITATES NO. 2962 have the main burrows clogged with loose often carried out at night, I confused nests soil (see below). Nests of some species seem closed for the night with the apomorphic con- to be devoid of any tumulus or, if soil is dition of totally filled burrows; so far as I present, the nests are thought to be in early know, none of the "primitive" panurgines stages of construction. Entrances of most have filled burrows.) composite nests are without tumuli of any BURROW SEPTA: Septa (thin partitions of sort. soil blocking main tunnels) have been noted TURRETS: Panurgine nests are not known deep in the nests of some of the "primitive" to have turrets, and such features are uncom- panurgines (Metapsaenythia, Protandrena bi- mon in Andrena species. However, conical, color, and perhaps Psaenythia interrupta). hardened turrets have been reported within This is presumably an apomorphic condition tumuli of several species of Andrena (sum- but needs further investigation. marized by Youssefand Bohart, 1968). These FILLED LATERALS: Tunnels leading to closed structures may be the result of the female cells are filled in almost all andrenid nests, impregnating the tumulus with some liquid certainly a plesiomorphic condition for the so that tumulus soil does not collapse into family. Hence open laterals (except for septa) the entrance, possibly an indication of how of Psaenythia interrupta as reported by the hardened cell walls are formed in Andrena Claude-Joseph (1926), if true, are apomor- and the "primitive" panurgines (see below). phic. Turrets ofthis sort are clearly not behavioral NUMBER OF CELLS IN A NEST: Completed homologs of those of Anthophora and the nests of almost all andrenids consist of a Emphorini (Anthophoridae). In the Andren- number of cells. Single-celled nests, known idae, these turrets at first appear as derived or suspected in several Nomadopsis species because of their uncommon occurrence. and one of Perdita, must be considered apo- However, they raise the question as to morphic. Because second and third nests of whether Andrena and the "primitive" pan- females ofsome Andrena (Michener and Ret- urgines normally apply heretofore undetect- tenmeyer, 1956) are known to have reduced ed stabilizing liquid (perhaps secretions or numbers of cells compared with first nests, nectar) to burrow walls. an investigator must sample a number ofnests SPECIAL MAN BuRRow WALLs AND DIA- before drawing conclusions about numbers METERS: Special water-absorbent walls in of cells per nest for any andrenid. main burrows of Old World Panurginus and ORDER OF CELL CONSTRUCTION: So far as Melitturga have been discussed by Rozen is known, all panurgines have progressive (1 971a) and may be related to situations where nests; that is, the youngest cells are always the burrow diameters are not constant in a deepest where there is only one female to a single nest, as in the narrowed entrances to nest and cells are arranged singly. Literature the nests of Pseudopanurgus f timberlakei. accounts suggest the same is true for Andrena These are presumably apomorphic condi- with the exception ofA. perplexa Smith (Ste- tions and need further study. phen, 1966). Nests of this species are regres- MAN BuRRow FILL: Most Andrena species sive; the entire main burrow is constructed, (but not erythronii, Michener and Retten- and the lowest cell is the first built while sub- meyer, 1956) and the "primitive" panurgines sequent cells are closer to the surface. Al- do not have the main nest tunnels filled with though progressive nests seem plesiomorphic soil during nest construction and provision- for the family, more observations are re- ing. Sometimes soil is encountered at the low- quired. er end ofotherwise open tunnels and presum- CELL ARRANGEMENT: Cells arranged singly ably is a result of cell construction. The rather than in linear series are generally found plesiomorphic open condition is distinct from in Andrena (the "linear-branched" arrange- totally filled burrows, the apomorphic state ment in nests ofA. bimaculata [Kirby] is an seen in Nomadopsis, Calliopsis, Hypomacro- interesting exception [Malyshev, 1926, 1935]) tera and relatives. (Because my early studies and in most ofthe Panurginae, and therefore on the "primitive" panurgines at the South- are thought to be primitive. Linear series have western Research Station [Rozen, 1967] were been reported for four Japanese Andrena 1989 ROZEN: "PRIMITIVE" PANURGINE BEES 21 species (Hirashima, 1962), but this reporting character depends on the hardness ofthe sub- may be suspect because the author thought strate, size of cells, and subjective judgment that such an arrangement was characteristic of the observer. ofthe genus. End-to-end linear series of cells CELL LININGS: Conspicuous shiny water- have been noted for several species of Li- proof cell linings that uniformly cover all in- phanthus, one species ofMelitturga, and No- ner surfaces of the cell except for the closure madopsis helianthi (Swenk and Cockerell), an are characteristic ofAndrena and the "prim- indication that the apomorphic condition has itive" panurgines dealt with here and there- arisen independently a number of times in fore are primitive in the family. A reduction the Panurginae. in the lining so that it is relatively incon- CELL ORIENTATION: Most andrenids build spicuous or so that only the cell floor upon cells that are nearly horizontal but tipped which the food mass rests is waterproof oc- slightly toward the rear, the presumed prim- curs in Nomadopsis, Calliopsis, Hypomacro- itive condition. Within some species (e.g., tera, related South American genera and also Pseudopanurgus verticalis Timberlake, Ptero- Perdita and is a synapomorphy. So incon- sarus boylei (Cockerell), and some Andrena) spicuous is the lining in some species in these tilting may vary from 0 to 45°. Other species genera that it can be easily overlooked al- ofAndrena have cells that uniformly tilt ap- though the cell wall has a smooth inner sur- proximately 45°. In Andrenaperplexa (Parker face. Intermediate reduction ofthe cell lining and Boving, 1925; Stephen, 1966) and Psae- has been documented for Meliturgula (Ro- nythia interrupta (Claude-Joseph, 1926) cells zen, 1968). Reduction in cell lining in New are vertical, almost certainly a condition de- World genera seems correlated with presence rived independently in each of these taxa. of a clear waterproof coating over the food CELL WALLS: Beneath the shiny cell linings mass (see below). The peculiar extra partial ofAndrena, the "primitive" panurgines, and lining under the food mass ofLiphanthus ali- some Old World genera, the immediate sub- cahue in addition to the conspicuous cell lin- strate tends to be harder than the surrounding ing seems to be a unique apomorphy, al- substrate as a result of the female applying though this feature should be analyzed in light some substance to the soil. The literature is of the "inner lining to the basal two fifths of ambiguous as to whether this wall results from the cell" ofA. perplexa (Stephen, 1966). the female permitting a hardening liquid to TRANSPORTED PROVISIONS: Among the An- soak into the soil, the soil and liquid being drenidae, there is considerable variation as worked into a mixture that is cemented into to how and in what condition pollen is carried a rough cavity, or some intermediate process to the nests. For example, females of at least taking place. Because I have been unable to some Andrena carry pollen unmoistened on detect a sharp line separating the cell wall the trochanters, femora, and tibiae ofthe hind from the substrate, I suspect that a female legs, in corbiculae on the propodeum, and moistens the substrate with the hardening attached to the ventral base ofthe metasoma. liquid and then tamps and rubs the softened In the "primitive" panurgines, pollen is often soil with her pygidial plate to form a smooth carried in a moistened condition on the an- surface. The source of the liquid needs to be terior surface ofthe hind tibiae, but, in some determined (whether a secretion or nectar, taxa, females on the foraging trip first apply and, ifa secretion, from what gland or glands). dry pollen to their hind legs and then, before The liquid is presumably different from the returning, cover the dry pollen with moist shiny material that coats and waterproofs the pollen. In some of the more specialized pan- cell wall. Because the hard, thick cell walls of urgines like Nomadopsis and Calliopsis, fe- at least some Protandrena, Pseudopanurgus, males transport very moist pollen in masses and Pterosarus species resemble those ofAn- that surround the tibiae. This mode oftrans- drena, conspicuous cell walls are thought to port is almost certainly an apomorphy, for it be plesiomorphic. The thinner, less conspic- is not encountered in other bees and seems uous walls of Perdita and other more spe- to be correlated with absence of keirotrichia cialized panurgines are judged to be apo- on the posterior surfaces of the hind tibiae morphic. Unfortunately, detection of this (Ruz, 1987). However, the mode of pollen 22 AMERICAN MUSEUM NOVITATES NO. 2962 transport including body parts involved, plu- PRoVISIONS: Provisions of most panurgines mosity of scopal hairs, and wetness or dry- are homogeneously moist and firm, but in ness of the food seems so variable from one some Protandrena, Pseudopanurgus, and group of andrenids to the next that it is cur- Pterosarus species provisions are very moist rently possible only to highlight this matter on the outside and dry inside. Those of Ce- for further study. phalurgus are sticky and very moist through- FoRMs OF EARLY DEPOSITS OF PROVISIONS: out. Although of potential phylogenetic val- Females of the "primitive" panurgines, for ue, such data are still too incompletely which there are data, store the food from each understood for use. On the other hand, clear, foraging trip on the cell floor as irregular plasticlike, waterproofcoatings on provisions masses that are unshaped until the last load ofmost Perdita, Nomadopsis, Calliopsis, Hy- is brought into the cell. At least some species pomacrotera, and South American allies are of the Old World genus Meliturgula (includ- certainly a unique synapomorphy, in contrast ing Poecilomelitta) form the first loads into to uncoated provisions of the "primitive" small spheres, as do all Nomadopsis, Cal- panurgines, the Old World panurgine genera, liopsis, Hypomacrotera species in North and Andrena. America and their South American relatives. POSITION OF PROVISIONS IN CELL: Some Surprisingly, most reports on Andrena indi- variation exists as to where females place ful- cate that early loads ofprovisions are shaped ly formed food masses in their cells, but pre- into small spheres (with the possible excep- cise placements are difficult to observe and tion of A. regularis Malloch [Schrader and therefore data are incomplete. Positioning LaBerge, 1978]). No Old World genera except food masses toward the rear end ofcells seems for Meliturgula and Poecilomelitta are known to be characteristic of most panurgines and to shape early food loads. This matter re- Andrena and is presumably the plesiomor- mains an unresolved conundrum. phic condition. Food masses applied to the FoRMs OF COMPLETED PROVISIONS: Among very rear of the cell, as in some Panurginus, the New World Panurginae, food masses are is almost certainly a derived feature. either spheres or flattened spheres (with their POSITIONS OF EGGS: Panurgine eggs (in- height less than their horizontal diameter). cluding those of the "primitive" panurgines) (In the Old World genus Melitturga, food are usually found on the top of food masses, masses of at least some species are longer as also has been reported for Andrena and than wide. Other Old World genera have for many other bees with shaped food masses. either spheres or flattened spheres, so far as Hence, other placements such as the rear known.) In all of the "primitive" panurgines (Perdita) or front (some Panurginus) of the (which are New World), the masses are flat- food mass are believed to be apomorphies. tened spheres (except for the smaller of the LARvAL AMBULATIONS: Of all the panur- two food masses ofPsaenythia annulata). In gines whose nests have been studied, only many species ofAndrena food masses are flat- larval Panurginus apparently is capable of tened spheres, but in some species the top of crawling over its food mass during feeding. the food mass is hollowed (cratered) and in All others sit on top ofprovisions and (except still others the upper and lower halves of the perhaps for Cephalurgus) reorient when they food masses are strongly asymmetrical. Be- have attained the last larval stage, presum- cause neither of these situations is found in ably by crawling with their projecting dorsal the Panurginae, the simple flattened sphere, body tubercles. Repositioned on their dorsa, found in both subfamilies, is believed plesio- the larvae then consume the remaining food. morphic in the "primitive" panurgines; com- Some Panurgus apparently move the front plete spheres, found in Perdita, Nomadopsis, part of their bodies back and forth as they Calliopsis, Hypomacrotera, and their South feed, a condition perhaps intermediate be- American relatives, apparently represent the tween the typical panurgine feeding behavior derived condition. However, it should be and that of Panurginus (Rozen, 197 la). Un- noted that Hirashima (1962) found provi- fortunately outgroup comparisons have yet sions ofAndrena knuthi Alfken to be "quite to be made to determine the polarity of this spherical." character. CONSISTENCY AND COATING OF STORED PLACEMENT OF FECES: Scanty reports in- 1 989 ROZEN: "PRIMITIVE" PANURGINE BEES 23 dicate that Andrena either places its feces at terns. As one example: Species ofHolcopasi- the upper rear or lower rear of the cell. All tes are nest parasites of species of the panurgines except for most Perdita apply their "primitive" panurgine genera Heterosarus, feces to the upper rear of the cell, the plesio- Pseudopanurgus, Metapsaenythia, and al- morphic condition for the subfamily. All most certainly Pterosarus. However, all but known Perdita except for P. portalis cradle one other Holcopasites attack the Calliopsis the feces on their venter, a unique apomor- subgenera Calliopsis, Calliopsima, Verbena- phy among bees. pis, but none of the subgenera assigned to VOLTINISM: Some of the "primitive" pan- Nomadopsis even though Ruz's (1987) anal- urgines studied have one generation per year ysis suggests that Nomadopsis, Calliopsis, and (Protandrena, Pseudopanurgus, Heterosarus) Hypomacrotera should be combined into a whereas others are suspected or known to single genus. A single species, Holcopasites have more than one (Liphanthus, Cephal- illinoiensis minimus (Linsley), is associated urgus). Elsewhere in the Panurginae both uni- with Hypomacrotera callops Cockerell and voltine and multivoltine taxa are known. The Porter. On the other hand, all subgenera of value of this character for phylogenetic in- Nomadopsis host Oreopasites, as does Hy- terpretation is questionable because we do pomacrotera subalpinus (Cockerell) and sev- not know whether internal factors, external eral species of Perdita. No Oreopasites has factors, or both control voltinism. Further- been associated with Calliopsis as formerly more, although most Andrena are single identified or any of the "primitive" panur- brooded, double broods have been reported gines even though they are sympatric. More for a number of species (see Linsley, 1937). data may help. DIAPAUSING LARVAE: All panurgines spend the winter as larvae, and most overwintering larvae are totally quiescent. However, larvae BIOLOGICAL PROFILE OF ofMetapsaenythia and at least some Protan- THE ANDRENIDAE drena, Pseudopanurgus, and Meliturgula curl The format of this summary follows pre- and uncurl slowly in a semidiapause. Fur- vious accounts of the biologies of higher bee thermore some Pseudopanurgus overwinter taxa: Fideliinae (Rozen, 1977a), Diphaglos- as predefecating, nondiapausing larvae. Out- sinae (Rozen, 1 984a), and Exomalopsini group comparisons with Andrena are prob- (Rozen, 1984b). Preliminary in nature, it is ably invalid because Andrena species over- based on literature cited above, data pre- winter as adults (with the possible exception sented above, and unpublished fieldnotes. ofA. accepta Viereck [Rozen, 1973]) that are NESTING: Family distributed worldwide not in a physiological diapause. Perhaps stud- (except for Australia); ground nesting species, ies of other genera of Andreninae will estab- abundant in temperate and in warm-arid re- lish the polarity of these features. gions. Body size minute to moderately large, MATING BEHAVIOR: Patterns in panurgine but mostly small. All species nonsocial, non- bees have been studied only in a few cases cleptoparasitic; most species noncommunal but, if better documented, appear to be po- but some in composite nests and many others tentially useful for phylogenetic analysis. nesting in irregular aggregations. Nesting sur- Certainly the ability of some Perdita females faces usually horizontal or nearly so, but to forage while in copula is apomorphic as is sometimes sloping, rarely vertical; usually in the ability of paired couples of some Perdita sunny areas. Substrate generally moderately and of the species of the subgenus Noma- firm, with or without stones and roots, but dopsis to fly from flower to flower and to their extremely variable from soft sand to sand- nesting sites. However, there are undoubt- stone. Nests shallow to moderately deep (ca. edly many different aspects ofmating behav- 1 m), apparently mostly progressive but at iors that need to be factored before they can least one regressive. Nest pattern (of non- be studied. communal species) consisting ofmain tunnel CUCKOO BEE ASSOCIATES: The associations and radiating short and long laterals leading between taxa ofnomadine cleptoparasitic bees to cells, usually at various depths. Entrances and their andrenid host taxa reveal interest- ofnoncomposite nests usually with tumuli of ing, complex, and presently inexplicable pat- loose soil, rarely with conical turrets embed- 24 AMERICAN MUSEUM NOVITATES NO. 2962 ded in tumuli; entrances of composite nests concave smooth surface in a few cases; inner normally without tumuli; entrances either surface not lined with waterproofing secre- open during foraging or, in some taxa, hidden tion. by tumuli (or completely obscured by loose PROVISIONING: Foraging females either de- surface soil). Main burrow almost always cir- positing early pollen or pollen/nectar loads cular in cross section, with walls nonwater- from hind legs as unshaped masses on floor proof, generally rougher than cell walls, rarely ofcell until entire provisions ofcell are gath- with special wall; main burrow nearly straight ered, or shaping early loads into small moist to strongly meandering, shallow or deep; bur- spheres, depending on taxon. Completed pro- row mostly open or soil-filled during provi- visions shaped into flattened sphere, flat- sioning depending on taxon; burrows ofsome tened sphere with depression on top, com- taxa with thin septa of soil at various depths. plete sphere, flattened radially symmetrical Laterals leading to closed cells soil-filled ex- mass with the top half not symmetrical with cept for those ofPsaenythia interrupta. Nests bottom half, or somewhat elongate spheroid; usually but not invariably with a number of provisions often mealy, firm, and homoge- cells, in most species arranged singly, but in neous, sometimes very moist on outside and some arranged in short linear series; cells of nearly dry and fluffy on inside, other times most species nearly horizontal but inclined very moist (almost semiliquid), depending on slightly, usually toward rear; some species taxon; provisions of some taxa (always those with cells variable in inclination (but rear end that have spherical food masses) coated with always lower than front) from nearly hori- shiny transparent waterproof substance per- zontal to inclined 450; others with cells more haps of same material as cell lining. Food or less consistently inclined 450; still others mass normally placed on cell floor toward with cells vertical. Cells elongate-oval with rear, sometimes near middle of floor, and maximum diameter greater than diameter of rarely at very rear of cell; mass resting un- lateral, rounded at the rear, apparently usu- attached to cell floor, sometimes attached to ally nearly symmetrical around longitudinal floor by small amount of liquid (nectar?), axis, but in some large species cell ceiling sometimes droplets ofliquid (nectar?) visible more vaulted than cell floor. Cell walls (i.e., on cell wall, and rarely (in some Andrena) ceiling, sides, floor, and rear, but not closure; mass surrounded by liquid reported to be the cell lining, a secreted film that the female nectar. Food masses of most species not applies to the walls, is considered a separate undergoing extensive liquefaction before structure, described below) usually smooth, being consumed, but liquefaction reported in though pygidial embossings visible in some some Andrena. species; walls of some taxa thick and harder DEVELOPMENT: Slender, curved, white, than substrate, of other taxa thin and only shiny egg without reticulated chorion, one to slightly harder than substrate, of still others a cell, often placed on top ofprovisions, either smooth on the inside but otherwise undiffer- attached by posterior end or by both ends, in entiated from substrate; except for hardness, sagittal plane ofcell; in some taxa eggs placed cell walls indistinguishable and not sharply somewhat behind food masses, in others defined from substrate. Cell linings of some somewhat toward or on front. Young larvae taxa shiny, waterproof, transparent, covering ofall panurgines except some Panurginus re- all of cell surfaces except closures; linings of maining stationary on top of food masses other taxa less conspicuous, often reduced, while they feed until reaching last instar; on and on some species detectable only as a reaching last stadium, larvae (with possible waterproof area restricted to cell floor where exception of Cephalurgus) reorienting and food mass rests (contrary to earlier accounts then, while resting on dorsal tubercles, feed- [Rozen, 1967], at least the lower rear ofPer- ing on remaining food held on their venters; dita cells are waterproof even though a lining young Panurginus larvae capable ofcrawling is not visible); lining material presumably around food mass as they feed. Feeding ac- glandular. Cell closures invariably concave tivities of andrenines unknown. Defecation spiral on the inner surface with three to seven taking place only after all food consumed. coils; outer surface usually not detectable, but Feces applied to upper rear wall of cell (all 1989 ROZEN: "PRIMITIVE" PANURGINE BEES 25 panurgines except Perdita and one Andrena), scriptions ofimmature stages ofPerdita to lower rear of cell (reported for a few An- octomaculata and P. halictoides (Hy- or held on venter Co- menoptera: Andrenidae). J. Kansas drena), (most Perdita). Entomol. Soc. 50: 577-599. coons not constructed in any species. Species Friese, H. overwintering as mature diapausing, totally 1916. Neue Bienen-Arten aus Chile und Siid- quiescent, postdefecating larvae (most pan- amerika. Stettiner Entomol. Ztg. 77: urgines), as mature semidiapausing postdefe- 163-174. cating larvae (in Protandrena, Metapsaeny- Hicks, C. H. thia, Pseudopanurgus, and Meliturgula), as 1931. Notes on certain bees, with a consid- predefecating mature larvae (in Pseudopan- eration ofthe use ofthe abdomen in nest urgus), or as adults (most ifnot all Andrena). construction. Canadian Entomol. 63: ADULT AcTIvITY: Bees primarily diurnal, 173-178. mostly active in late morning and early after- 1936. Nesting habits of certain western bees. Canadian Entomol. 68: 47-52. noon; few species (some larger forms) early Hirashima, Y. matinal, active in late afternoon, or vesper- 1962. Systematic and biological studies of the tine (crepuscular). Bees usually univoltine, but family Andrenidae ofJapan (Hymenop- some species with more than one brood per tera, Apoidea). Part I. Biology. J. Fac. year; adult activity very early spring to mid- Agric., Kyushu Univ. 12: 22 pp. fall, depending on taxon. Species monolectic, Hurd, P. D., Jr., and E. G. Linsley oligolectic, or narrowly polylectic. Mating be- 1972. Parasitic bees of the genus Holcopasites haviors extremely variable. Ashmead (Hymenoptera: Apoidea). CLEPTroPARAsITIc BEES: Nests ofmany taxa Smithsonian Contrib. Zool. 114: 41 pp. attacked by many groups of species-specific Janvier, H. or Nomadinae 1933. Etude biologique de quelques hyme- genus-specific (Neolarrini, nopteres du Chili. Ann. Sci. Nat., Zool., Holcopasitini, Ammobatini, Ammobatoidi- ser. 10, 16: 209-356. ni, and Nomadini) and infrequently by Sphe- Linsley, E. G. codes (Halictidae), but not by other clepto- 1937. The occurrence of double broods in parasitic bees, so far as is known. North American andrenid bees (Hy- menoptera). Bull. Brooklyn Entomol. Soc. 32: 125-127. Linsley, E. G., and J. W. MacSwain REFERENCES 1956. Further notes on the taxonomy and bi- Chandler, L. ology of the andrenine bees associated 1962. Notes on the species ofPsaenythia (Hy- with Oenothera (Hymenoptera: An- menoptera: Andrenidae) in the eastern drenidae). Pan-Pac. Entomol. 32: 111- United States. J. Kansas Entomol. Soc. 121. 35: 313-314. 1959. 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Shinn, A. F. genus (Hymenoptera, Andrenidae). 1967. A revision of the bee genus Calliopsis Entomol. News 80: 89-92. and the biology and ecology of C. an- Torchio, P. F. dreniformis (Hymenoptera, Andreni- 1975. The biology of Perdita nuda and de- dae). Univ. Kansas Sci. Bull. 46: 753- scriptions of its immature forms and 936. those of its Sphecodes parasite (Hyme- Stephen, W. P. noptera: Apoidea). J. Kansas Entomol. 1966. Andrena (Cryptandrena) viburnella. I. Soc. 48: 257-279. Bionomics. J. Kansas Entomol. Soc. 39: Warncke, K. 42-51. 1985. Beitriige zur Bienenfauna des Iran 19.- Thorp, R. W. 20. Die Gattungen Panurgus Pz. und 1969. Systematics and ecology of bees of the Meliturgula Fr. (Hymenoptera, Api- subgenus Diandrena (Hymenoptera: dae). Boll. Mus. Civ. Stor. Nat. Venezia Andrenidae). Univ. Calif. Publ. Ento- 34(1983): 221-235. mol. 52: 146 pp. Youssef, N. N., and G. E. Bohart Thorp, R. W., and G. I. Stage 1968. The nesting habits and immature stages 1968. Ecology of Andrena placida with de- of Andrena (Thysandrena) candida scriptions of the larva and pupa. Ann. Smith (Hymenoptera, Apoidea). J. Entomol. Soc. Am. 61: 1580-1586. Kansas Entomol. Soc. 41: 442-455. Timberlake, P. H. 1969. Metapsaenythia, a new panurgine bee Recent issues of the Novitates may be purchased from the Museum. Lists of back issues of the Novitates, Bulletin, and Anthropological Papers published during the last five years are available free of charge. Address orders to: American Museum ofNatural History Library, Department D, Central Park West at 79th St., New York, N.Y. 10024. L

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