Table Of ContentPROC. ENTOMOL. SOC. WASH.
96(2). 1994, pp. 350-356
NESTS AND ENEMIES OF EXOMALOPSIS {PHANAMALOPSIS) SOLANI
COCKERELL (HYMENOPTERA: APOIDEA, MUTILLIDAE;
DIPTERA: ASILIDAE)
Beth B. Norden, Karl V. Krombein, and Suzanne W. T. Batra
(BBN, KVK) Department ofEntomology, Smithsonian Institution, Washington, D.C.
20560; (SWTB) Bee Research Laboratory, Bldg. 476, United States Department ofAg-
ricuhure, Behsville, Maryland 20705.
Abstract.—T^ic bee, Exomalopsis (Phanomalopsis) solani Cockerell was studied in
Apache, Arizona, 1988 and in Rodeo, New Mexico, 1991. Bees nested communally in
hard packed, horizontal ground surrounded by low xeric vegetation. Nest structure, pro-
visions, and larvae are discussed. Evidence ofcooperative nesting without differentiation
into castes is examined. Cleptoparasites ofimmatures, Pseudomethoca bethae Krombein
(Mutillidae) and Nomada giitierreziae Cockerell (Apoidea), and a predator ofadult bees,
Mallophorina pulchra Pritchard (Asilidae), are identified.
Key Words: Communal, cleptoparasite, ground-nesting, Exomalopsis, Apoidea, Asili-
dae, Mutillidae
The genus Exomalopsis includes primar- Eriogonum, Euphorbia. Giitierrezia. Het-
ily small, neotropical bees. Exomalopsis erotheca. Lepidium. Mentzelia. Solanum,
(Phanomalopsis) solani Cockerell ranges and Sphaeralcea. The soil was hard packed,
from Colorado into southern Mexico (Hurd and consisted of coarse pebbles in a fine,
1979), and is common in southern New grayish clay/sand matrix.
Mexico and Arizona (Timberlake 1980). Nest architecture.—The three nests were
Although it is an abundant species in the completelyexcavated from the surrounding
American southwest, few nests have been substrate after blowing fine dry plaster of
examined (Rozen 1984), and some aspects Paris powder into the opening and tunnels
of the communal nesting behavior of this to outline their paths. Soil particles were
species require clarification. carefully removed with a small paintbrush,
penknife, tablespoon, and shovel. Addi-
Mater—ials and Methods tional soil was removed in a 10 cm radius
Studysites. Nestdatawereobtainedby surroundingthe traced burrows, in an effort
the excavation of three active nests. One tolocatepluggedlateralsandadditionalcells.
nest was examined 30-31 August 1988 by Provisions and immatures.—Females
BBN at Apache, Cochise Co., Arizona (Fig. were observed while collectingpollen in the
1). Two nests were excavated 5 and 10 Sep- field. Scopal pollen on hind legs and pollen
tember 1991 by Bryan N. Danforth (pers. in cells were freeze-dried, then mounted on
comm.)at 2.5 km N ofRodeo, HidalgoCo., stubs for scanning electron microscope ob-
New Mexico. All nests were located in hor- servation and photographing. Immatures,
izontal ground and were surrounded by a ranging from first instar to post-defecating
diversity oflow xeric vegetation, including larvae, were collected and preserved in
1
VOLUME 96. NUMBER 2 351
Kahle's solution for microscopic examina-
tion.
Communal behavior.—While excavating
the 1988 nest at Apache, Arizona, all E.
solanifound within this nest or returningto
it with pollen were captured. Only female
adults were found, and 19 of the total 2
females were placed in Kahle's solution for
later dissection and laboratory examina-
tion. Behavior and numbers offemales as-
sociated with all three nests were observed
and recorded. Laboratory analysis, follow-
ing Batra 1966, included measuringrelative
body sizes estimated by maximum head
width in micrometer units (1 mm = 6.4
units), mandibular wear (estimated by
bluntness ofmandible tips), wing wear (in-
dicated by the numberofnicks in both fore-
wings), ovarian and Dufour's gland devel-
opment(micrometerunits),andgutcontents
(empty, nectar, pollen).
Enemies.—All insects found within the
bee nests or in the area near them were col-
lected and identified. Immature stages, re-
moved from bee cells, were placed in shal- Fig. L Excavationof£xowa/op5/55o/a«;Coclcerell
low wells in a covered plastic culture dish nest, Apache, Anzona. 31 August 1988.
and returned to the laboratory for rearing.
Voucher specimens of all insects collected always separated by a distance of 1 cm or
during this study were deposited in the Na- more. Because of the difficulty in tracing
tional Museum ofNatural History, Smith- these soil-filled laterals, and their close
sonian Institution. proximity to one another, it was not pos-
sible to determine the exact numberofcells
perlateral. Cell baseswerealwayslowerthan
Results and Discussion
cell caps, but cell orientation relative to the
Nest architecture.—The inconspicuous lateralwashighlyvariable. Table 1 provides
nest entrances were smooth, circular open- data from the three nests. The presence of
ings into the horizontal soil surface. They many old, previously used cells in two of
mm
were 4.5 in diameter, and devoid ofa the nests suggests that natal nests are reused
surrounding turret or tumulus. Each nest by subsequent generations. Perhaps this ex-
consisted ofa main tunnel that descended plains the earlier observation (Linsley et al.
perpendicularly from the ground surface 1954) that E. solani appropriates aban-
withtwistsandminordetoursaroundrocks. doned burrows. Previously used cells were
The cells were encountered at depths rang- easily identified by a thin layer of fungal
ing from about 30-50 cm. Cells appeared hyphae covering the cell walls (Fig. 2F).
to be arranged in horizontal linear series Cellwalls were harderthan the surround-
that radiated from the main vertical shaft. ingsoil,andcellscouldbeextractedwithout
The lateral tunnels containing these cells breaking. Walls ofempty new cells did not
were filled with loose soil, and cells were test positive for glucose, so it is assumed
352 PROCEEDINGS OFTHE ENTOMOLOGICALSOCIETY OFWASHINGTON
Table Comparison ofthree Exomalopsis solam
1.
nests.
VOLUME 96, NUMBER 2 353
'spst'
Fig. 2. Scanningelectron micrographso(E.xomalopsissolani nest structures. A. interiorview ofcell closure
showing the concentriccoils. B, magnified cap showinguncoated soil pelletscomposing the coils. C. view into
cell base showingsmooth intenorand rough textureofsurroundingsoil that has fallen in. D, cell liningcoating
soil particles ofthe cell interior surface. E, closeup oftunnel walls revealing no lining material. F, portion of
interiorwall ofa used cell showing several uneaten pollen grainsand fungal mycelium coveringthecell lining.
354 PROCEEDINGS OFTHE ENTOMOLOGICALSOCIETY OF WASHINGTON
Fig.3. ScanningelectronmicrographsofE.xomalopsissolaniprovisions.A,pollenmassrevealingdistribution
ofdifferent pollensthroughout. B. one mass with at least fourdifferent pollenspresent. C, surfaceofcompleted
pollen mass showing coating thai may have an anti-fungal effect. D, scopa offoraging female E. solam with
pollen collected from only one host plant. E, fungal hyphae invading a pollen mass that had been cut in half
with a sterile scalpel. F, incomplete pollen mass with fungal hyphae filling the cell and pullingthe lining from
thecell'searthen wall.
VOLUME 96, NUMBER 2 355
'Jinh/I
i^^^K^5
'i?-.-S5.-'
Fig. 4. Frontal viewofheadsofcleptoparasiticwasp. Pscudomelhocabelhae. A. pristinefemalecollectedon
groundnearE. solan:nest. B, femaleshowmgconsiderable mandibularwearthatwascollectedwithinE. solani
nest.
12.47 units). Eleven ofthe 13 females that solani nests cooperatively, without the de-
hadenlarged ovaries with an egglargerthan velopment ofcastes.
themean, hadrecentlyeatennectarandpol- Enemies.—Two adult female mutillids,
len; fourofthe sixfemaleswithsmallerova- Pseudomethoca bethae Krombein (1992),
ries had not eaten recently. The size ofthe were found within the Apache nest during
Dufour'sgland was not well correlated with the 988excavation.Thesewaspsareknown
1
the size of the ovaries. However, the Du- cleptoparasites ofbee larvae. One individ-
four's gland of a bee can shrink suddenly ual with somewhat eroded mandibles was
whenever its secretion has been applied to on a cell provision, presumably feeding; the
a cell. other, with badly eroded mandibles (Fig.
The two known foragers, captured re- 4B), was within the main tunnel 39 cm be-
turning to the nest with pollen, were ofav- low ground. We assume that mandibular
erage size (16 and 17 units) and had average wearoccurred as the wasps chewed into the
mandibular wear. One had a large oocyte hardened brood cells in orderto gain access
(16 units), but the other had small oocytes to bee larvae. Nine additional adult females
(6 units). The wings ofboth bees were very ofP. bethae (Fig. 4A) were collected crawl-
worn (20 and 21 nicks). The three bees that ing on the ground near the Apache and Ro-
hadthelargestoocytes(21, 16,and 16units) deo nest sites. Also found within one ofthe
were ofaverage size (16, 16, and 17 units). Rodeonestsweretwocellscontainingapost-
They had 20, 11, and 10 wing nicks re- defecating larva and a cocoon ofunidenti-
spectively, somewhat above average wing fied mutillids (Bryan N. Danforth, pers.
wear.Theirmandibularwearwasnearlyav- comm.).
erage. Thesedata indicate that, although this Another aculeate cleptoparasite found
species nestscommunally, and shares a sin- within the Apache nest and in the imme-
gle nest entrance, there is no evident differ- diate vicinity was the cuckoo bee, Nomada
entiation into workers and egglayers. Un- gutierreziaeCoc)<iQK\\. Two Nomada larvae
fortunately, there was not time to mark were removed from cells containing post-
individual bees and watch them to deter- defecating E. solani larvae and were pre-
mine which individuals were foragers, and served. Five female and one male Nomada
during what time in their lives. Our data removed from six otherwise empty E. so-
support Michener's (1966) finding that E. lani cells were reared in the laboratory. Co-
PROCEEDINGS OFTHE ENTOMOLOGICALSOCIETY OF WASHINGTON
356
coonswere not spunby theNomadalarvae. graphic Services for furnishing prints, and
Parker(1984) reported this same nomadine to George L. Venable, Department of En-
We
[as Hypochrotaenia (Micronomada) gutier- tomology, for preparation ofthe plates.
reziae] to be a cleptoparasite ofthe gregar- also thank Jim Cane, Auburn University,
iously nesting Exomalopsis (Anthophonila) and an anonymous reviewer for their com-
crenulata Timberlake in southern Utah. ments on the manuscript.
Several specimensofanothernomadinebee,
Literature Cited
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by KVK near the Apache nest. While not Batra, S. W. T. 1966. The lifecycleand behaviorof
directly associated with E. solani, P. nitida theprimitivelysocialbee,Lasioglossumzephynim
ishighlysuspectsinceParanomada veliitina (BHuallliecttiinda6e6)(.10T):he35U9n^i2ve3r.sity of Kansas Science
Linsley was recorded in the nests by Rozen Cole, F. R. and A. E. Pntchard. 1964. The genus
(1984). Triopasitespenniger(CockeTeW), also Mallophora and related asilid genera in North
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chraPritchard. Fliesperchedonflowerstems tution Press.
throughout the Apache and Rodeo nesting Krombein. K. V. 1992. Host relationships, ethology
areasandgrabbedbeesastheyforaged. Oth- andsystematicsoiPseudomelhocaAshmead(Hy-
menoptera:Mutillidae,Andrenidae,Halictidaeand
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were also taken as prey by the asilid, al- cal Society ofWashington 94: 91-106.
though flies of this genus are reported to Linsley,E.G.,J.W.MacSwain,andR.F.Smith. 1954.
specialize in the collection ofHymenoptera AnoteonthenestinghabitsoiExomalopsissolani
(Cole and Pritchard 1964). Cockerell (Hymenoptera, Anthophoridae). Pan-
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Acknowledgments Michener. C. D. 1966. Evidenceofcooperative pro-
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Danforth, Cornell University, for gener- logical Society 39(2): 315-317.
ously sharing the data from the two nests Norden,B.,S.Batra.H.Fales.A. Hefetz,andG.Shaw.
of£. solanithat he found near Rodeo, New m1a9t8e0.rnaAlniDhuofopuhro'rsagbleaensd:sUsneursvueaalsgllayrcvealrifdoeosdfaronmd
Mexico. We thank Jerome G. Rozen, Jr., cell lining. Science 207: 1095-1097.
American Museum ofNatural History, for Parker, F. D. 1984. Biological notes on the bee £.v-
identifying the larvae of Exomalopsis and omalopsis {Anthophonila) crenulata Timberlake
Nomada. adults ofParanomada and Trio- (Hymenoptera: Anthophondae). Pan-Pacific En-
tomologist 60: 188-192.
pasites. and for photographing the nest dig- Rozen. J. G.. Jr. 1957. External morphological de-
ging and terrain at Apache. Arizona. Bryon scription of the larva of Exomalopsis chionura
Alexander, University of Kansas, and F. Cockerell. includingacomparison with otheran-
Christian Thompson, Systematic Entomol- thophonds(Hymenoptera:.Apoidea).Annalsofthe
ogy Laboratory, USDA, ARS, PSI kindly Entomological Society ofAmerica 50: 469^75.
identified the adult specimens of Nomada tri.be19E8x4o.maCloomppsairnaiti(vAepnoeisdteian,gbAinotlhoogpyhoofrtihdeaeb)e.e
and Mallophora respectively. Within the Amencan Museum Novitates 2798: 1-37.
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Laboratory', for skillful preparation of the I-IV. UniversityofCalifornia Publicationsin En-
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micrographs, to Victor G. Krantz, Photo-
