Bees As Floral Designers

PUBLISHED BY THE AMERICAN MUSEUM OF NATURAL HISTORY
CENTRAL PARK WEST AT 79TH STREET, NEW YORK, NY 10024
Number 3680, 22 pp., 44 figures, 1 table March 4, 2010
Nests, Petal Usage, Floral Preferences, and
Immatures of Osmia (Ozbekosmia) avosetta
(Megachilidae: Megachilinae: Osmiini), Including
Biological Comparisons with Other Osmiine Bees
JEROME G. ROZEN, JR,1 HIKMET O¨ ZBEK,2 JOHN S. ASCHER,3 CLAUDIO
SEDIVY,4 CHRISTOPHE PRAZ,5 ALIREZA MONFARED,6
AND ANDREAS MU¨ LLER7
ABSTRACT
Herein we describe the nests (including construction, closure, orientation, and depth of cells) of
the bee Osmia (Ozbekosmia) avosetta Warncke found nesting near Antalya, Turkey, and Sepidan,
Iran. Cells are unusual in that they are lined by two layers of colorful flower petals that sandwich a
thin middle layer of mud. Analyses of pollen taken from scopal hairs of specimens from the
Turkish site were identified as solely from Onobrychis viciifolia Scop. (Fabaceae) whereas those
from the Iranian site were from a related plant, Hedysarum elymaiticum Boiss. and Hausskn. These
facts coupled with analyses of scopal pollen from 11 other sites in Turkey, Jordan, and Syria
strongly suggest that this bee is oligolectic with respect to the plant tribe Hedysareae.
Copyright E American Museum of Natural History 2010 ISSN 0003-0082
1 Division of Invertebrate Zoology, American Museum of Natural History, Central Park West at 79th Street, New York,
NY 10024 (rozen@amnh.org).
2 Atatu¨rk University, Faculty of Agriculture, Department of Plant Protection, 25240 Erzurum, Turkey (hozbek@
atauni.edu.tr).
3 Division of Invertebrate Zoology, American Museum of Natural History, Central Park West at 79th Street, New York,
NY 10024 (ascher@amnh.org).
4 ETH Zurich, Applied Entomology, Schmelzbergstrasse 9/LFO, CH-8092 Zu¨ rich, Switzerland (claudio.sedivy@
ipw.agrl.ethz.ch).
5 Cornell University, Department of Entomology, 3119 Comstock Hall, Ithaca NY 14853 (christophe.praz@gmx.ch).
6 Yasouj University, Department of Plant Protection, Faculty of Agriculture, Yasouj, Iran (alirezamonfared1@yahoo.
com).
7 ETH Zurich, Applied Entomology, Schmelzbergstrasse 9/LFO, CH-8092 Zu¨ rich, Switzerland (andreas.mueller@
ipw.agrl.ethz.ch).
The egg and last larval instar of Osmia avosetta are described. The presence of an egg taken from
a cell and provisionally identified as belonging to Sapyga pulcherrima Morawitz suggests that this
cleptoparasite may have this bee as one of its hosts.
In addition, we report new information on and review published accounts concerning the use of
whole petals or large petal pieces in the construction of cell walls of osmiine bees. Only Osmia
(Ozbekosmia) avosetta and species of Osmia (Tergosmia) have three-layered cell walls with the
middle layer made of mud. Recorded also are the similarities and differences exhibited in pollen
and petal preferences and nest characteristics of species in these two related subgenera.
INTRODUCTION
We present for the first time information
about the nesting biology, floral preferences,
and immature stages of Osmia (Ozbekosmia)
avosetta Warncke, 1988. Although an uncommonly
encountered species, two nesting aggregations
of it were discovered almost simultaneously,
one in Turkey and the other in Iran,
and provided information for the current study.
Additionally, we review the use of petals as a
building material in osmiine bees and compare
the biology of O. avosetta with that of species
belonging to Osmia (Tergosmia). These two
subjects are dealt with in the Discussion section.
The Turkish research party consisted of the
first three authors (Rozen,O¨ zbek, and Ascher),
and the Iranian party of the next three (Sedivy,
Praz, and Monfared). Mu¨ ller was responsible
for the study of floral preferences, the review of
petal usage among osmiine bees, and the
section Comparative Biology of Ozbekosmia
and Tergosmia, as Rozen was for descriptions
of immature stages.
DESCRIPTION OF NESTING SITES
In Antalya Province, Turkey, the Turkish
party discovered two nests of Osmia avosetta at
Seklik Mevkii (N 35u529520 E 30u229300), a
small village about 6 km east of Saklıkent, the
first nest on May 31, 2009, and the second on
June 1, 2009. The elevation was approximately
1500 m on the east-facing slope of the
mountain. The two nests were about 100 m
apart, each on a small, partly to mostly barren
mound of earth fully exposed to the sun. In
each case, the nesting surface sloped 20u–40u
from horizontal and the soil was moderately
fine, loosely compacted, and friable. On June 3,
2009, we returned and found an aggregation of
nesting females about 100 m from the closest
nest site found earlier. It was at a slightly higher
elevation, but still on the eastern slope of the
mountain and fully exposed to the sun. The
ground was moderately covered with stands of
the food plant Onobrychis viciifolia Scop.
(Fabaceae) between which were more thinly
vegetated areas where we found nest entrances
(fig. 1). The slope of the surface varied here
from 0u–20u. The surface soil was crusty with
pebbles and numerous fractures; beneath, the
soil was dry and generally easily excavated,
though with some rocks.
The Iranian party discovered five nests of
Osmia avosetta, which is a new species record
for Iran, on May 31, 2009, along Yasouj-Shiraz
new road, 6 km after Tange Tizab, at 10 km
northeast of Sepidan, Fars Province, Iran (N
30u20960 E 51u509220, elev. 2270 m) (fig. 6). The
nesting site was a large, very steep scree slope
exposed to the north, with only scarce vegetation.
The food source, Hedysarum elymaiticum
Boiss. and Hausskn. (Fabaceae) (fig. 7), grew
abundantly at the site and was visited by
numerous females of Osmia avosetta, though
no males were found. Although the ground at
this site was mainly composed of stones and
gravel, all nests were located in soil that was so
loose and friable that we were able to dig out
the nests by hand. Where soil was more
compact on less sloping surfaces, no nests were
found. The five nests were scattered, and each
contained only one cell.
The first nest was found because we saw a
female enter a hole in the ground. This nest
was still open, and the bee was inside the
brood cell. We found four more nests (each
containing a completely closed brood cell) by
simply digging around other holes in the
ground, possibly an indication that the females
do not fill the burrows with pebbles
after finishing the brood cell.
At the Turkish site, the entire nesting area
was extensive, about 30 m long and 25 m wide.
Some nest entrances were circular holes, 5–
7 mm in diameter, and others were irregular in
shape, often associated with the surface cracks
2 AMERICAN MUSEUM NOVITATES NO. 3680
(fig. 10). They were not uncommon (about
1/m2), but irregularly distributed. Both males
and females were seen at the nesting area
visiting flowers of Onobrychis or landing
briefly on the ground in barren areas.
Several tumbling pairs observed from a
distance were probably mating, thus explaining
the appearance of both sexes in the area.
NEST ARCHITECTURE
Since it was our last day in the field at the
Turkish site, we hurriedly excavated approximately
10 nests, which we recognized by
entering or departing bees. Only two or three
consisted of two cells. All others contained a
single closed cell, an open cell being provisioned,
a cell being constructed, or no cell. At
first we interpreted the paucity of cells to
indicate that the foraging season was only
starting. However, in hindsight we realize that,
if completed nests normally contain only
single cells or two cells, we may well have
overlooked numerous completed nests because
all but one nest studied were initially identified
by adults entering or leaving. Had we had one
more day to identify and excavate nests
lacking evidence of adult activity, conclusions
might have been different. Indeed, we now
tentatively conclude that they normally consist
of one or two cells because most of the females
collected at the time of our fieldwork bear
lightly to moderately worn wings rather than
unworn wings. Nests at both sites were
shallow, with cells ranging in depth from 1.5
to at most 5.0 cm. In addition to the nest
entrance, each had an open main burrow, 6–
7 mm in diameter that in most cases descended
vertically, but in one case slanted substantially
to one side, presumably because the female
had encountered a rock. There was no special
burrow lining nor did the burrow wall seem
consolidated in any way, such as by tamping.
CELL ORIENTATION AND STRUCTURE
Cells at both the Iranian and Turkish sites
were mostly vertical or nearly so, although a
number tilted as much as 10u–20u from
vertical. Although only single cells were found
in Iran, where two cells were found in a single
nest in Turkey, they were normally positioned
side by side and contiguous, with one cell
several millimeters higher than the other.
However, in one nest the lower cell met the
side of the other at an angle.
Cell structure, also identical at the two sites,
is complicated, as must be the stereotypic
procedure used by the female bee to construct
it. In describing cells of most bees, the inner
dimensions (length and maximum width) of
the cavity are generally presented with some
idea of the shape of the lumen, but the cell of
this species is delineated by the external shape
of the lining and characterized by the color
and materials that make up the lining. All
materials used are collected and transported
by the female from outside the nest. After the
female digs the main tunnel and cavity for one
or two cells, she brings in large pieces of petals
to line what will become the outer envelope of
the cell lining, probably first applying them to
the lower surfaces of the cavity, and with
successive importations advancing the lining
upward on all sides, as evidenced by the
shingling of petals on the cell neck (fig. 12).
The outer envelope is extended into the neck of
the cell, well beyond (about 3 mm) what will
become the top of the closed cell. Later, as the
last act of cell construction, the female will fold
these petals mesad to the long axis of the cell to
form the exterior cell closure of the completed
cell (fig. 14). Apparently because petals of a
wide range of available flowers are used, the
colors on some cells include purple, blue, tan,
yellow, and red (fig. 11–13), but on other cells
there is a more limited array of colors (figs. 8,
9), probably indicating a narrower selection of
appropriate plants in flower.
After the female completes the outer envelope,
she then brings in fine moist soil and
plasters it against the inner surface of this
lining, forming a layer 0.5–0.8 mm thick. This
layer covers the entire inner surface of the
outer envelope to where the closure will be
placed, so that the upper 3 mm of the petal
lining remains uncovered. The source and
nature of the moisture in the soil is unknown
but may be water, a secretion, or possibly
nectar. When the moist soil sets, it becomes
dull, pale, and hard (cause of the setting
unknown, but perhaps simple drying). As the
next step, the female imports petals to
completely line the cell cavity and thus forms
2010 ROZEN ET AL.: OSMIA (OZBEKOSMIA) AVOSETTA 3
the inner envelope, which extends upward
beyond the soil lining. At the entrance the
inner and outer envelopes adhere, forming a
central passageway through which the female
imports provisions and deposits her egg on the
top surface of the provisions (fig. 21). Thus,
the cell wall of the brood chamber before
closure, except for the upper 3 mm, consists of
three closely appressed layers: an outer envelope
of petals and an inner envelope of petals
that together sandwich a layer of soil.
At the Turkish site, we assumed that the
petals were harvested from the numerous
adjacent flowering plants, including
Onobrychis (fig. 1), as reflected in the multicolored
outer envelopes of the cells. However,
at the Iranian site the deep hue of the outer
envelope (figs. 8, 9) did not appear at first to
match any of the close-by flowering plants
including the pale-flowered Hedysarum elymaiticum
(fig. 7), the larval food source for
Osmia avosetta at this site. Subsequently C.S.
concluded on reexamining the cells that all
petals seemed to originate from the banner
petals of this plant and that their darker, more
purple hue resulted from withering after the
petals are cut. He noted that the petals were all
shaped like the upper part of a heart and were
arranged in the same manner: their tips
pointed downward and the cut side pointed
upward and they overlap like scales in both
the inner and the outer petal linings.
After egg laying comes the task of closing the
cell, a process that the female carries out in
three steps. She first closes the inner envelop by
folding mesad the apical petals of the inner
envelope, thus closing the cell lumen and
forming a truncated top for the inner envelope.
This top measured about 4.5 mm in diameter
(figs. 18, 19) in one case. She imports no
additional petals from the outside. The closure
petals are somewhat moist and can be teased
apart and unfolded with forceps to expose the
cell lumen below (fig. 20). The ease by which we
were able to unfold the inner closure without
tearing the petal tissue suggested the ease the
female bee had in folding the soft and compliant
petal tissue when constructing the closure.
As the next step she brings in a small
quantity of dry soil to place into the slight
concavity formed on the top of the inner
envelope closure, followed either by importing
moist soil or by adding some liquid to the dry
soil to manufacture a smoothly concave outer
(upper) surface to the soil closure (figs. 15–17).
This closure, similar in texture and thickness to
the soil lining of the cell wall, bonds at its
periphery to the soil lining. How she manufactures
the smooth surface to the concavity
remains unknown.
As the final step to protect her offspring, the
female folds mesad the petals at the open end of
the outer envelope against the soil closure
(fig. 14). On at least three closures, the females
brought in and added several petals that were
not part of the lining, presumably to augment
the thickness to the top of the closure.
In Turkey a single closed cell was accidentally
encountered when we were excavating
another nest. It contained an intermediatestage
larva actively feeding on provisions. The
colorful display of petals persisted on the
outer envelope (fig. 5), but the soil lining to
the cell had hardened considerably compared
with this lining in fresher cells. Soon after
being collected the larva molted to the last
larval instar, described below. This accidental
discovery added to our suspicion the nests
contain only one or two cells, because this was
the only larva that we found in the 10 or so
nests we excavated at the Turkish site.
Cells still open from both sites were
elongate (figs. 4, 11), because the visible lining
included both the cell itself and the petal-lined
neck. They measured 18.0–19.5 mm in length
(N 5 5). Closed cells were shorter since the
linings of the neck regions are folded over and
incorporated into the cell closure, as described
above. Closed cells measured 15.0–17.5 mm
(N 5 9) in length. All cells (open and closed)
were 7.0–9.0 mm in maximum outside diameter
(N 5 7). The widest part of closed cells
was between one-quarter and one-third of the
distance from the bottom of the cell. Cells
were not symmetrical around their long axes;
all had one side that was convex while the
opposite side was slightly concave (figs. 2, 3).
Provisions were a sticky mixture of yelloworange
pollen, homogeneously combined with
nectar. They occupied roughly the lower half
of the inner envelope of petals and conformed
to the shape of the bottom of the cell. On their
surface, the female deposited her elongate,
shiny egg (fig. 21), described below.
4 AMERICAN MUSEUM NOVITATES NO. 3680
FLORAL PREFERENCES
At the nesting site near Saklıkent, Turkey,
females of Osmia avosetta were seen visiting
only the flowers of Onobrychis viciifolia Scop.
(Fabaceae) for larval provisions, although
many other flowers were available as potential
pollen and nectar sources, e.g., Anchusa,
Salvia, Centaurea, Astragalus, and Melilotus.
The microscopic analysis of pollen contained
in the abdominal scopa of nine females
collected at the nesting site on June 3, 2009,
revealed that all females had indeed harvested
pollen exclusively from Onobrychis viciifolia.
At the nesting site near Sepidan, Iran, the
females of Osmia avosetta were observed to
exclusively visit the flowers of Hedysarum
elymaiticum, although many other plants were
flowering in the proximity of the nesting site,
including several Fabaceae species of the
genera Astragalus, Lotus, and Trifolium.
Microscopic pollen analysis corroborated the
narrow host-plant preference of Osmia avosetta
at the Iranian site: pollen masses
removed from the abdominal scopa of 15
females collected at the nesting site on May 31,
2009, were entirely composed of Hedysarum
pollen as were the pollen provisions of five
brood cells dug out the same day.
The exclusive utilization of pollen of
Onobrychis and Hedysarum, which form a wellsupported
clade within the tribe Hedysareae
(Wojciechowski et al., 2004; McMahon and
Sanderson, 2006; Ahangarian et al., 2007),
indicates that Osmia avosetta is most probably
a specialist on this plant tribe. This conclusion is
supported by microscopic analysis of scopal
pollen contents of 13 additional females collected
at 11 different localities in Turkey, Syria, and
Jordan, which were all exclusively composed of
tricolpate Fabaceae pollen typical for
Onobrychis and several Hedysarum species as
well as for two other genera of the Hedysareae
(Choi and Ohashi, 1996).
PARASITISM
Figure 31
No cleptoparasites were seen entering any
of the nests at either site, but we retrieved
from a cell a single egg unlike that of Osmia
avosetta at the Turkish site. It differed by
being slightly shorter (2.5 mm long), much
thinner (maximum diameter 0.54 mm), faintly
curved, and broadly rounded at the anterior
end but tapering posteriorly and very narrowly
rounded apically (fig. 31) with the widest
part in the anterior one-quarter. We were
unsuccessful in viewing its micropyle with an
SEM. White in color like the host egg, it was
suggestive of the egg of Sapyga luteomaculata
Pic (Rozen and Kamel, 2009), which is faintly
tan, shorter (length 1.96–2.1 mm), and slimmer
(maximum diameter 0.44–0.46 mm). The
egg of S. louisi Krombein is similar though
shorter (1.5 mm long) and narrower (0.25 mm
at middiameter) (Mathews, 1965: fig. 16). The
described egg of S. pumila Cresson (Torchio,
1972: figs. 2, 4) is even shorter (1.3 mm long)
and, proportional to its length considerably
slimmer (diameter at anterior end: 0.18 mm).
The slender, distinctive torpedolike shape of
all previously described eggs strongly suggests
that the parasitic egg found in the cell of
O. avosetta is a Sapyga or some related
Sapygidae. Because two individuals of
Sapyga pulcherrima Morawitz, 1894, were
collected (but not entering nests) at the nest
site during our study, it likely is that species.
IMMATURE STAGES
Immatures of Osmia avosetta and the egg of
Sapyga pulcherrima described were collected
at Seklik Mevkii, 6 km east of Saklıkent,
Antalya Province, Turkey, June 3, 2009 (J.G.
Rozen).
DESCRIPTION OF EGG
Figures 21, 30
DIAGNOSIS: The egg of Osmia avosetta
appears unremarkable, although we were
unable to examine it with an SEM and
therefore cannot describe its micropyle.
DESCRIPTION: Length 2.93 mm (N 5 2);
approximate maximum width 0.93 mm (N 5
3). Egg index 0.81 (see Remarks). Upper
surface slightly curved in lateral view
(fig. 30); ventral surface nearly straight; anterior
end (identified by developing embryo)
slightly more narrowly rounded than posterior
end in lateral view (fig. 30); sides subparallel
2010 ROZEN ET AL.: OSMIA (OZBEKOSMIA) AVOSETTA 5
when viewed from above; micropyle not
visible with stereomicroscope. Egg color
white; chorion under stereoscope clear, shiny,
glassy, thin throughout.
MATERIAL STUDIED: Three eggs.
REMARKS: The egg index of 0.81 was
calculated by dividing the average lengths of
two eggs by the distance between the outer
rims of the tegulae of a female from which one
of the eggs was collected (Iwata and
Sakagami, 1966). This value falls well within
the medium category of Iwata and Sakagami’s
(1966: table 2) classification of bee egg size
relative to female body size. This is the second
species of osmiine bee with an egg index
reported in this category; Hoplitis (Hoplitis)
monstrabilis Tkalcu° has an egg index of 0.77
(Rozen et al., 2009).
DESCRIPTION OF LAST LARVAL INSTAR
Figures 32–40
The single larva recovered was an intermediate
instar that molted to the last instar soon
afterward. Last instars of larvae of probably
all Megachilinae (except for the Lithurgini)
can be recognized because of extensive body
setae, which are absent on earlier instars
(Baker et al., 1985; Rozen and Kamel, 2009).
The larva was preserved after it had started
defecating and spinning silk. Although a
considerable amount of uneaten provisions
remained in the cell, most fecal material had
been voided by the time of preservation. Head
capsule pigmentation was evident although
whether it was at its maximum development is
unknown. After being cleared by boiling in an
aqueous solution of sodium hydroxide, pigmentation
was greatly reduced.
DIAGNOSIS: As was pointed out earlier,
larvae of the Megachilidae are ‘‘very homogeneous’’
(Michener, 1953: 1040). Since then
mature larvae of other megachilid taxa have
been described (see McGinley, 1989, and
references therein; Baker et al., 1985; Rozen
and O¨ zbek, 2004; Rozen and Kamel, 2007,
2009; and Rozen et al., 2009). From these
works, we see that the Osmiini, Anthidiini,
Dioxyini, and Megachilini as mature larvae
can be easily distinguished from those of the
more basal Pararhophitini, Fideliini, and
Lithurgini because the former have conspicuous
body setae and the latter do not. However,
we still do not know how to recognize the
tribes of the more advanced megachilids on
the basis of their mature larvae, much less to
distinguish larval Osmia from other Osmiini.
Because the osmiine Hoplitis monstrabilis has
approximately five setae on the pleural swelling
of abdominal segment 8 (Rozen, et al.
2009), in contrast to approximately 80 in O.
avosetta has and perhaps also the same
number in O. (O.) ribifloris Cockerell, we at
first thought that setal abundance might prove
valuable. However, the larva of O. (Pyrosmia)
submicans Morawitz from Egypt has only 12
setae on this swelling, suggesting that setal
abundance may prove unreliable for generic
recognition after more species are surveyed.
Details of mandibular and atrial morphology
seem to vary among the Megachilinae and
may prove helpful in recognizing tribes and/or
genera despite the high degree of larval
homogeneity.
The peculiar absence of a sclerotized cardo
in the presence of a well-sclerotized stipital rod
is a feature unknown in several other mature
larval Osmia that we have examined.
DESCRIPTION: Head (figs. 33, 34, 37): Setae
long and abundant; those of frons shorter and
those of labrum very short; those of maxillary
and labial apices straight, forward projecting.
Following areas moderately to faintly pigmented:
labrum including labral sclerite (exclusive
of middle part), darkest part of which
is along subapical row of sensilla; area apicad
of darkest part also sclerotized and pigmented,
but extreme apical labral margin unpigmented,
nonsclerotized; mandibles especially at
apices and points of articulation; internal head
ridges at articulation with mandibles; dorsal
surface of premental sclerite between attachment
of articulating arms of stipites; antennal
papilla and all palpi only faintly pigmented.
Fine spiculation restricted to dorsal surface of
maxilla and lateral lobes of hypopharynx.
Area immediately above hypostomal ridge
and just behind posterior mandibular articulation
not produced as downward-directed
tubercle as present in many Coelioxys
(Rozen and Kamel, 2007: fig. 47). Coronal
ridge nearly absent; postoccipital ridge well
developed; hypostomal ridge well developed,
6 AMERICAN MUSEUM NOVITATES NO. 3680
giving rise to pronounced dorsal ramus that
extends posteriorly from middle of ridge
nearly to postoccipital ridge (fig. 33) where it
abruptly stops; anterior tentorial pit approximately
equally distant from anterior mandibular
articulation and basal ring of antenna;
epistomal ridge present only laterad of anterior
tentorial pits; tentorium robust including
dorsal arms. Parietal bands faintly evident.
Diameter of basal ring of antenna somewhat
less than twice distance from ring to center of
anterior tentorial pit; antennal papilla (fig. 39)
small, slender, gradually, evenly tapering
apically, about three times as long as basal
diameter, bearing two to three sensilla
(fig. 39). Lower margin of clypeus strongly
angled upward at midline (fig. 34), so that at
midpoint margin nearly at level of anterior
tentorial pits. Labral sclerite transverse, pigmented
(except at midline), with lower margin
extending beyond apical band of sensilla;
labrum lacking darkly pigmented median spot
extending from labral sclerite to apical labral
margin as in fully pigmented Coelioxys larvae
(Rozen and Kamel: 2007: figs. 44, 45); apical
labral margin moderately broad, distinctly
concave (figs. 34, 37).
Mandible (figs. 35, 36) moderately robust;
apex bidentate with ventral tooth longer than
dorsal tooth; both teeth acutely pointed; dorsal
apical edge of dorsal tooth finely, regularly
crenulated; ventral apical edge of upper tooth
and both edges of ventral tooth unmodified;
apical concavity pronounced, sharply defined
basally; cuspal area not developed; outer
surface without setae or tubercles. Cardo as a
sclerite absent; stipes a slender sclerotized rod
posteriorly ending abruptly at point where it
would have articulated with cardo; articulating
arm of stipes evident; maxillary palpus moderately
small, about same size as antennal
papilla and labial palpus. Labium clearly
divided into prementum and postmentum;
apex normally wide (figs. 34, 37); premental
sclerite weakly sclerotized, most evident dorsally;
postmentum nonsclerotized. Salivary lips
projecting, transverse, width about equal to
distance between bases of labial palpi; inner
surface of at least upper lip, visible only after
specimen subjected to critical-point drying
process, with numerous parallel, raised ridges
extending outward (fig. 40). Hypopharynx
consisting of two widely separated lateral lobes
that are spiculate.
Body (figs. 32, 41): Body setae short, rising
from swollen bases, abundant dorsally and
laterally; pleural area of abdominal segment 8
with approximately 80 setae (fig. 41); integument
in areas without setae with patches of
very fine spicules. Body form robust; intersegmental
lines weakly incised on predefecating
larva; intrasegmental lines not evident but
possibly visible on postdefecating form; paired
body tubercles absent; middorsal body tubercles
very evident on midbody segments,
decreasing in size posteriorly (fig. 32); pleural
swellings moderately developed; abdominal
segment 10 attached to approximate middle
of segment 9; anus positioned toward top of
segment 10. Spiracles well sclerotized, unpigmented,
subequal in diameter; atrium globular
with width considerably greater than depth,
projecting above body wall, with rim; peritreme
narrow, so that diameter of atrial
opening as much as four times peritreme
width; atrial inner surface with rows of
wrinkles (figs. 42–44) concentric with primary
tracheal opening; atrial wall also with fine,
sharply pointed, concentrically directed spicules;
primary tracheal opening with collar;
subatrium variable in length, with from four
to 10 chambers; externally, subatrium tapering
in side view. Male with small crescentic
(almost circular) median integumental scar
on venter of posterior edge of abdominal
segment 9; female sex characters unknown.
MATERIAL EXAMINED: One fifth instar.
DISCUSSION
BIOLOGY OF OSMIA AVOSETTA
In light of the hazards that confront a nest
shallowly situated in loose soil on a slopping
surface, we can speculate as to how a cell with
this construction might be beneficial. With
little or no rain during the summer months,
rainfall leading to soil erosion is not a
significant threat until after the immature
reaches hibernation in its cocoon. However,
if the cell should be flooded by an unexpected
early storm, the double petal lining would
seemingly deflect much water, and the air
trapped by two layers of petals would help
float a cell that was eroded from the ground.
2010 ROZEN ET AL.: OSMIA (OZBEKOSMIA) AVOSETTA 7
Probably a more significant hazard is
desiccation especially in very shallow nests;
the double layer of petals, which are a source
of moisture in themselves, should help retain
moisture during larval development. Because
megachilid larvae in general seem little bothered
by water loss, we wonder whether
maintaining the water content of the provisions
might be the selective force for the
evolution of this elaborately structured cell
wall. The rigidity added by the soil lining, of
course, protects the cell contents from being
crushed or invaded by predators and parasites.
Although the patchwork of colors on the
outer surface of a cell (figs. 2–5, 11) or even the
strong colors (figs. 8, 9) is a striking phenomenon
to the human eye, color of the cell surface
is obviously not important to the female bee or
her nest. We think the survival value of
constructing this elaborate cell lining of petals
and soil is the texture, water content, and water
repellent– and humidity-retaining nature of
petals. High water content provides moisture,
the soft tissue of petals makes them easy for the
females to harvest, the compliant nature of the
tissue is easily folded, and the lack of plant
hairs allows petals to adhere to one another.
We here have interpreted the closure of the
brood cell of Osmia avosetta as an integral
component of the lining of the cell. Still to be
explored is the construction of the cell closures
of other osmiine taxa that use whole petals or
Changes in the body’s acid-alkaline tadalafil online uk balance to the central nervous function correctly. It can cause reduction in the flow of blood to increase in the cialis shipping penile area, thus causing an erection. Subjects of brainwave entrainment program experiments were reported to exhibit the trained mental states long after the experiments had ended, six months to be exact. order cheap levitra http://www.glacialridgebyway.com/photos.html The organic nature of Yes lubricants reassures both professionals and patients/clients, of safe and side-effect free application in cases where generico cialis on line frequent and liberal use of a lubricant is required. large petal pieces to form cell walls. In Hoplitis
(Anthocopa) dalmatica (Morawitz), whose
cells consist of an outer layer of roughly
chewed leaves and an inner layer of large petal
pieces, the females immediately close the cell
after egg deposition by folding mesad the
apical petals (Mu¨ ller, Krebs, and Amiet,
1997), corresponding to the first step of cell
closure in Osmia avosetta. With newly collected
leaf material that is applied onto the petal
layer, H. dalmatica then finally closes the
brood cell.
PETALS AS NEST BUILDING MATERIAL IN
OSMIINE BEES
Among the osmiine bees, the use of petals
for brood cell construction is not confined to
Osmia avosetta. Roughly chewed petals of
Dalea (Fabaceae) are used by Ashmeadiella
(Isosmia) rubrella Michener to build entire
brood cells (Yanega, 1994), and some osmiine
bee species, which usually utilize chewed green
leaves as nest-building material, occasionally
also use chewed petals, e.g., Hoplitis
(Dasyosmia) biscutellae (Cockerell) (Rust,
1980), Osmia (Allosmia) rufohirta Latreille
(Grandi, 1961), or O. (Helicosmia) caerulescens
(Linnaeus) (Westrich, 1990). However,
the use of whole petals or large pieces of petals
for brood cell construction is restricted among
the Osmiini to O. (Ozbekosmia) avosetta, two
species of Wainia (Caposmia), most Hoplitis
species of the subgenus Anthocopa as well as
all Osmia species of the subgenus Tergosmia
whose nesting biology has been recorded so
far (Mu¨ ller et al., unpubl.). In the two Wainia
species, which both nest in empty snail shells,
the partitions between the brood cells are
constructed from large petal pieces glued
together, whereas the nest plug is built from
petals followed by a thick layer of cemented
sand (Gess and Gess, 2008). The brood cells of
Hoplitis (Anthocopa), which are generally built
in excavated or preexisting burrows in the
ground or, more rarely, in fissures and holes in
rocks and bark, under stones or in empty
snail shells, are entirely constructed from
foreign material (Mu¨ ller et al., unpubl.).
Petals are used by most of these species as
the exclusive cell building material. However,
the two closely related H. (Anthocopa) graeca
(Tkalcu°) and H. (Anthocopa) villosa (Schenck)
apply mud in varying quantities to cement
the petals together (Ducke, 1900; Friese,
1923; Petit, 1970; Westrich, 1990; A. Mu¨ ller,
personal obs.). In contrast to O. avosetta,
however, the cells of these two species are not
three-layered; instead petals and mud are
more thoroughly mixed. A three-layered cell
structure consisting of a mud layer sandwiched
between two layers of petals, which is
very characteristic of O. avosetta, is also found
in O. lunata Benoist (A. Mu¨ ller, personal
obs.), O. rhodoensis (Zanden) (C. Praz and C.
Sedivy, personal obs.) and O. tergestensis
Ducke (Ferton, 1897; Mu¨ ller et al., 1997),
which all belong to the subgenus Tergosmia.
This unique cell structure shared by both
Ozbekosmia and Tergosmia indicates that
these two subgenera most probably form a
monophyletic group within the genus Osmia.
8 AMERICAN MUSEUM NOVITATES NO. 3680
This hypothesis is supported by the close
morphological similarity of O. avosetta to
Tergosmia, e.g., in the form of the female
clypeus and of the male sterna (Michener,
2007). Indeed, Warncke (1988) placed O.
avosetta in the subgenus Tergosmia before
Zanden (1994) moved it to the new subgenus
Ozbekosmia due to several deviating charac-
Fig. 1. Nesting site of Osmia avosetta in Seklik Mevkii, Turkey, to the left of observers in fore- and
midground; note pinkish-red flowers of pollen plant, Onobrychis viciifolia. Figures 2, 3. Closed brood cells of
O. avosetta, side views, showing shape and variation in coloration of outer envelopes. Figure 4. Open cell of
same, side view. Figure 5. Closed cell of same containing intermediate stage larva. (Photos J.G. Rozen.)
2010 ROZEN ET AL.: OSMIA (OZBEKOSMIA) AVOSETTA 9
Figs. 6–9. Nesting of Osmia avosetta at 10 km northeast of Sepidan, Yasouj region, Iran. 6. The site. 7.
Pollen plant, Hedysarum elymaiticum. 8, 9. Two brood cells. (Photos C. Sedivy).
10 AMERICAN MUSEUM NOVITATES NO. 3680
Fig. 10. Female of Osmia avosetta with a petal in its mandibles approaching nest entrance (photo J.S.
Ascher). Figures 11–15. Cells of Osmia avosetta. 11. Open cell, side view. 12. Close-up of neck of same,
showing sequence of plating of petals. 13. Closed cell, side view. 14. Top of same showing inward folded
petals of outer envelope. 15. Same cell, now with top of outer envelope removed revealing soil closure and
soil lining, and some inner petal lining where soil lining removed (arrow). (Photos J.G. Rozen).
2010 ROZEN ET AL.: OSMIA (OZBEKOSMIA) AVOSETTA 11
Figs. 16–21. More closed cells of Osmia avosetta. 16. Upper part of cell, side view, with petals of outer
envelope partly removed to reveal inner soil lining capped with closure of soil with concave upper surface.
17. Close-up of same showing concave soil closure, top view. 18. Same cell, now with most of soil closure
removed revealing some of petals of inner closure (arrow), top view. 19. Same, except now all of soil of inner
closure removed revealing folded petal of inner envelope, top view. 20. Another cell with outer envelope
teased open, soil closure removed, and inner envelope closure also teased open, top view. 21. Same cell with
opening widened to reveal egg floating on provisions. (Photos J.G. Rozen).
12 AMERICAN MUSEUM NOVITATES NO. 3680
Fig. 22. Two brood cells of Osmia (Tergosmia) rhodoensis in rock cavity; overlying stone removed to
make cells visible (Jordan, Jerash, 23.4.2007; photo C. Sedivy). Figures 23, 24. Brood cells of O. (T.)
tergestensis in cavities between stones; in both cases, overlying stone removed to make the cell visible. Petals
used for brood cell construction were from Geranium and Helianthemum (fig. 23) and Geranium only (fig. 24)
(Switzerland, Zeneggen, 10.7.1990; Photos A. Mu¨ ller).
2010 ROZEN ET AL.: OSMIA (OZBEKOSMIA) AVOSETTA 13
Fig. 25. Four closed brood cells and one cell still being provisioned of Osmia (Tergosmia) tergestensis
between blades of dense grass tussock; grass blades removed to make cells visible (Italy, Gimillan (Aosta),
15.7.1996; photo A. Mu¨ ller). Figure 26. Female of O. (T.) tergestensis biting off petal from flower of
Geranium pyrenaicum Burm. fil. Petal is tightly folded before being transported to nest. On each visit, female
removed one petal (Italy, Gimillan (Aosta), 15.7.1996; photo A. Krebs).
14 AMERICAN MUSEUM NOVITATES NO. 3680
Fig. 27. Open brood cell of Osmia lunata in a short cavity excavated in rather hard ground; twig concealing
nest entrance removed to make cell opening visible. Figure 28. Flower of Helianthemum sp. with one petal
bitten off by female of O. (T.) lunata (Morocco, Tafraoute, 20.4.2009; photo A. Mu¨ ller). Figure 29. Nest of O.
(T.) lunata consisting of 10 brood cells at base of small shrub. Uppermost part of cell still under construction
(top right) was the only visible sign of nest before excavation; the nine already closed cells were all hidden
under thin layer of soil (Morocco, Tafraoute, 20.4.2009; photos A. Mu¨ ller).
2010 ROZEN ET AL.: OSMIA (OZBEKOSMIA) AVOSETTA 15
ters not found in Tergosmia. A recent molecular
phylogenetic analysis of the Osmiini,
which did not include O. avosetta, placed the
three petal-using osmiine bee taxa Wainia
(Caposmia), Hoplitis (Anthocopa), and Osmia
(Tergosmia) in three distantly related clades
(Praz et al., 2008). Thus, assuming that
Ozbekosmia + Tergosmia together are indeed
monophyletic, the use of whole petals or large
petal pieces for brood cell construction has
independently evolved at least three times
within the osmiine bees.
The advantage of using large petals for
brood cell construction instead of chewed
green leaves (‘‘leaf pulp’’), which is a considerably
more widespread nest-building material
among the osmiine bees (Mu¨ ller et al.,
Figs. 30, 31. Diagrams of eggs of Osmia
avosetta and of parasite thought to be Sapyga
pulcherrima, lateral views, respectively, to same
scale; anterior ends at right.
Figs. 32–36. Diagram of fifth larval instar of Osmia avosetta. 32. Entire larva, lateral view; rectangle
identifies approximate area on abdominal segment 8 pictured in fig. 41. 33, 34. Head, frontal and lateral
views, respectively; ptp 5 position of posterior tentorial pit. 35, 36. Right mandible, dorsal and outer
views, respectively.
16 AMERICAN MUSEUM NOVITATES NO. 3680
unpubl.), remains unclear. The potential
benefits of leaf pulp, e.g., chemical protection
of the provisions by antimicrobial substances
contained in the leaves, humidity control
within the cell, or prevention of the absorption
of nectar by the substrate, are expected to be
properties of petals as well. One advantage of
the use of large petal pieces over that of leaf
pulp might be more efficient collection and
processing, as the latter can be collected only
in small quantities on a single flight. All petalusing
osmiine bee species, for which petal
collection has been recorded to date
(Westrich, 1990; A. Mu¨ ller, personal obs. for
several Hoplitis (Anthocopa) and Osmia
(Tergosmia) species), tightly fold the petal
already on the flower (fig. 26) before it is
transported to the nest in the mandibles and
eventually unfolded inside the brood cell.
COMPARATIVE BIOLOGY OF OZBEKOSMIA
AND TERGOSMIA
Apart from the three-layered structure of
the brood cells common to both Ozbekosmia
and Tergosmia, Osmia avosetta and the three
species of Tergosmia differ in several aspects
of their nesting biology (table 1). Osmia
(Tergosmia) rhodoensis and O. (Tergosmia)
tergestensis place their brood cells singly or in
small groups of up to five cells in holes and
fissures of rocks (fig. 22), between stones (figs.
23, 24), or in dense grass tussocks (fig. 25)
(Ferton, 1897; Mu¨ ller et al., 1997; C. Praz and
C. Sedivy, personal obs.). The cells of both
species, whose orientation varies from horizontal
to nearly vertical, lie freely in these
cavities and are neither glued to the substrate
nor to each other. In contrast, O. (Tergosmia)
Figs. 37–40. SEM micrographs of fifth larval instar of Osmia avosetta. 37. Head, approximate frontal
view. 38. Seta from area laterad of parietal band as identified by rectangle in figure 37 (but more lateral in
view). 39. Right antenna showing three apical sensilla. 40. Close-up of left side of salivary opening, showing
parallel ridges on upper inner surface.
2010 ROZEN ET AL.: OSMIA (OZBEKOSMIA) AVOSETTA 17
lunata excavates a short (ca. 1.5 cm), more or
less vertical burrow for each cell in rather hard
soil (A. Mu¨ ller, personal obs.; fig. 27). Unlike
O. avosetta, whose cells are built a few cm
below ground, cells of O. lunata reach the soil
surface (fig. 27). Up to 10 cells are built
immediately beside each other, separated by
few mm only (fig. 29), and each cell is hidden
under a thin and loose layer of small pebbles
and earth fragments after its closure. Earth
fragments are occasionally also used by O.
tergestensis in narrow cavities to barricade the
empty space in front of the cells (Ferton,
1897). Unfortunately, we do not know whether
the excavated burrows of O. avosetta are
actively filled or blocked with soil or other
particles after completion of the brood cell(s).
Neither Turkish Osmia avosetta nor the
Tergosmia species appear specialized with
respect to the flowers exploited as petal
sources. Known petal sources are Geranium
and Linum for O. rhodoensis (Warncke, 1988;
C. Praz and C. Sedivy, personal obs.) and
Geranium, Helianthemum, Hieracium, and
Figs. 41–44. Microphotographs of fifth larval instar of Osmia avosetta. 41. Setae of pleural swelling, left
side of abdominal segment 8, as identified by rectangle in figure 32. 42. Spiracle showing narrow peritreme
relative to large atrial opening and wrinkled atrial wall. 43, 44. Short and long subatria, respectively. (Photos
J.G. Rozen).
18 AMERICAN MUSEUM NOVITATES NO. 3680
Ononis for O. tergestensis (Ferton, 1897;
Benoist, 1931; Mu¨ ller et al., 1997; figs. 23,
24, 26). Although the only petal sources
recorded so far are Helianthemum for O.
lunata (A. Mu¨ ller, personal obs.; figs. 28, 29)
and Onobrychis and Hedysarum for O. avosetta
(this study), the colorful brood cells
testify that both species use additional plant
taxa as petal sources. However, the fact that
all five brood cells of O. avosetta detected at
the Iranian site were exclusively built with
petals of Hedysarum indicates that the Iranian
population might be specialized on a local
scale.
Unfortunately, the phylogenetic relationships
among species of the putative clade
TABLE 1
Biological Characters of Osmia (Ozbekosmia) avosetta and Three O. (Tergosmia) Species (For references
see text.)
Subgenus
Osmia avosetta
Warncke, 1988
Osmia lunata
Benoist, 1928
Osmia rhodoensis
(Zanden, 1983)
Osmia tergestensis
Ducke, 1897
Ozbekosmia Tergosmia Tergosmia Tergosmia
Nesting
site
Excavated burrows
in loose soil,
3–7 cm deep
Excavated burrows in
rather hard soil,
1.5 cm deep
Preexisting cavities:
holes and fissures
in rocks
Preexisting cavities: under
or between stones, holes
and fissures in rocks,
dense grass tussocks
Location
of cells
1.5–5 cm below soil
surface
Reach soil surface Completely hidden
within cavity
Completely hidden within
cavity
Number
of cells
per
burrow
One (rarely two) 1–10 immediately
beside each other
1–2 immediately
beside each other
1–5 immediately beside
each other
Structure
of cell
wall
Distinctly threelayered:
mud
sandwiched
between two
layers of large
petal pieces
Three-layered, but less
distinct than in other
species: outer layer,
small to large petal
pieces glued with
mud; central layer,
mud (sometimes only
weakly developed);
inner layer, large petal
pieces
Distinctly three-layered:
mud sandwiched
between two layers
of large petal pieces
Distinctly three-layered:
mud sandwiched
between two layers of
large petal pieces
Nest
barricade
? Cells hidden below thin,
loose layer of small
pebbles, earth
fragments
? In narrow cavities space in
front of horizontal cell(s)
sometimes filled to a
length of 0.5 cm with
earth fragments
Petal
sources
Hedysarum,
Onobrychis,
and others
Helianthemum and
others
Geranium, Linum Geranium, Helianthemum,
Hieracium, Ononis
Pollen
sources
Oligolectic on
Hedysareae
(Fabaceae)1
Broadly oligolectic
on Fabaceae, e.g.,
Lotus2
Polylectic with
preference for
Fabaceae; additional
pollen sources include
Campanulaceae,
Brassicaceae and
Asteraceae3
Broadly oligolectic on
Fabaceae, e.g.,
Hippocrepis, Lotus,
Onobrychis4
1Based on 37 scopal loads and 5 brood cells from 13 localities as well as on field observations.
2Based on 16 scopal loads and 11 brood cells from 8 localities as well as on field observations.
3Based on 13 scopal loads and 1 brood cell from 10 localities.
4Based on 25 scopal loads from 19 localities as well as on field observations.
2010 ROZEN ET AL.: OSMIA (OZBEKOSMIA) AVOSETTA 19
(Ozbekosmia, Tergosmia) are not yet resolved.
Therefore, any hypothesis on the evolution of
nesting biology within this clade appears to be
premature. However, based on morphology
(Warncke, 1988), there is little doubt that
Osmia rhodoensis and O. tergestensis are close
relatives. Further, O. lunata might be sister to
a clade composed of O. avosetta and the other
Tergosmia species due to (1) some possibly
plesiomorphic characters compared to the
other species (e.g., form of hind leg spur and
of female clypeus) or (2) the structure of its
cells being less distinctly three-layered in that
the outermost layer is composed of petals
cemented together with mud instead of consisting
solely of petals. If in future phylogenetic
analyses O. lunata should indeed turn
out to be the sister species of the clade
(avosetta (rhodoensis, tergestensis)), the evolution
of nesting behavior within the clade
(Ozbekosmia, Tergosmia) might have led from
excavation of burrows in soil (O. lunata, O.
avosetta) to the utilization of preexisting
cavities (O. rhodoensis, O. tergestensis). This
hypothesis is supported by the fact that
species of the subgenus Hemiosmia, which
is the possible sister taxon of the clade
(Ozbekosmia, Tergosmia) (Praz et al., 2008),
place their brood cells consisting of finely
masticated leaves in excavated burrows in
loose soil (Haeseler, 2008; C. Praz and C.
Sedivy, personal obs. for Osmia difficilis
Morawitz [Iran, Yasouj region, Road to
Ghalat, June 1, 2009, new species record for
Iran]). Under this evolutionary scenario, the
central mud layer, which makes the brood
cells firm and rigid, might possibly be interpreted
as a preadaptation that later enabled
the utilization of larger cavities as nesting
sites, in which the cells have no contiguous
support from the surrounding substrate.
Interestingly, Hoplitis (Anthocopa) graeca
and H. (Anthocopa) villosa, which are exceptions
within Anthocopa in that both species use
mud to cement together the petals, often use
rather large cavities to place their brood cells
as well (Friese, 1923; Petit, 1970; Westrich,
1990; A. Mu¨ ller, personal obs.). In contrast,
the other Anthocopa species accommodate
their brood cells preferentially in narrow
burrows in the ground (Mu¨ lleret al., unpubl.).
The quantity of mud used by H. villosa to
cement together petals is known to vary much,
the extremes being pure petal cells on the one
hand and mud cells with petals only on the
outside on the other hand (Petit, 1970;
Westrich, 1990). Unfortunately, it is not
known whether the use of low mud quantities
correlates with narrow cavities that give the
brood cells all-embracing support.
One of the anonymous outside reviewers
(C.D. Michener) kindly pointed out in his
review the following: ‘‘Another group of bees
that make cells somewhat similar to those of
Osmia (Ozbekozmia) and its relatives is
Megachile Group 1 of Michener (2007).
Although these are in another tribe, the
Megachilini, they appear to have evolved
some similar behaviors. Although very well
known as cutters of large leaf pieces for cell
construction, some species use petals. Of
particular interest in the present context are
those of the subgenus Chrysosarus that construct
cells of two layers of leaves or of petals
with an intervening layer of clay, much as in
O. avosetta. A brief summary with references
to the original sources is by Michener (2007).’’
Zillikens and Steiner (2004) point out that
Megachile (Chrysosarus) pseudanthidioides
Moure from Brazil constructs an inner cell
lining of petals and an outer one of leaves with
a mud layer between. They state ‘‘The petals
were not cut to the same size as the leaves, but
were much larger and folded in the apical part
of the chamber to form the cell closure.’’
Hence, they diagram a cell with the leaves of
the outer layer cut to fit the diameter of the
upper end of the cell, but the inner petal layer
is folded inward from the sides. Thus,
exemplars of two tribes have independently
invented not only the use of petals in cell
constructions but also a similar method of use.
All of the following species of Ozbekosmia
and Tergosmia show close affinities to
Fabaceae as pollen hosts (table 1). Osmia
avosetta appears to be strictly specialized to
the tribe Hedysareae (this study), Osmia lunata
and O. tergestensis are more broadly oligolectic
on Fabaceae (Benoist, 1931; A. Mu¨ ller,
unpubl.), and O. rhodoensis is polylectic with a
preference for Fabaceae (A. Mu¨ ller, unpubl.).
Assuming the phylogenetic relationships within
the clade (Ozbekosmia, Tergosmia) as
hypothesized above, the polylectic habit of
20 AMERICAN MUSEUM NOVITATES NO. 3680
O. rhodoensis appears to be derived, supporting
the growing evidence that polylectic
species have often evolved from oligolectic
ancestors while retaining the original pollen
host, (Mu¨ ller, 1996; Larkin et al., 2008; Sedivy
et al., 2008), i.e., O. rhodoensis continues to
collect pollen of Fabaceae but has added new
pollen hosts. That pollen specialization on
Fabaceae might be ancestral in this clade is
further corroborated by the pollen preferences
of species of the subgenus Hemiosmia, the
possible sister taxon of the clade (Ozbekosmia,
Tergosmia) (Praz et al., 2008). All Hemiosmia
species investigated to date appear to be
oligolectic on Fabaceae (Haeseler, 2008; A.
Mu¨ ller, unpubl.).
ACKNOWLEDGMENTS
J.G.R. and J.S.A. extend their thanks to
Robert G. Goelet, Chairman Emeritus, Board
of Trustees, American Museum of Natural
History (AMNH), for the support that permitted
them to undertake this investigation.
They also express their appreciation for the
hospitality and guidance afforded by H.O¨ .
while undertaking fieldwork in Turkey.
Margaret A. Rozen took the SEM micrographs
of the fifth instar with the assistance of
Rebecca Rudolph and Mathew Frenkel,
Microscopy and Imaging Facility, AMNH.
Steve Thurston, Division of Invertebrate
Zoology, AMNH, expertly organized and
labeled all illustrative material.
C.S. thanks Silvia Dorn and the Walter
Hochstrasser-Stiftung, ETH Zurich, for
financing his trip to Iran. A.M. expresses
his gratitude to Fritz Gusenleitner
(Obero¨ sterreichisches Landesmuseum Linz)
for loaning pollen-loaded females of Osmia
avosetta for the pollen-analytical studies,
Albert Krebs for providing a picture of O.
tergestensis, and Michael Widmer for support
in the fieldwork on the nesting behavior of O.
lunata. A.M. extends his appreciation to
Azizollah Jaafari for his help in identifying
the host plant species, to Shahrzad Azhari for
her hospitality during the Iranian team’s stay
at Yasouj, and to Mostafa Salahi and Hadi
Adelzadeh for their field assistance.
Josef Gusenleitner kindly identified specimens
of Sapyga pulcherrima. Max Schwarz
contributed valuable literature used in this
study.
All authors extend thanks to the two
anonymous outside reviewers for their helpful
comments on improving the manuscript.
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